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Infection Control in Healthcare

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Infection Control in Healthcare

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Muhta Syam
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© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd

57793_CH02_ARIAS.

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References 67

132. Simonds DN, Horan TC, Kelley R, Jarvis WR. Detecting pediatric nosocomial infections: how
do infection control and quality assurance personnel compare? Am J Infect Control. 1997;25:
202–208.
133. Larson E, Horan T, Cooper B, et al. Study of the definition of nosocomial infections (SDNI).
Am J Infect Control. 1991;19:259–267.
134. Haley RW, Schaberg DR, McClish DK, et al. The accuracy of retrospective chart review in
measuring nosocomial infection rates. Am J Epidemiol. 1980;111:516–533.
135. Scheckler WE, Brimhall D, Buck AS, et al. Requirements for infrastructure and essential
activities of infection control and epidemiology in hospitals: a consensus panel report. Am J
Infect Control. 1998;26:47–60. http://www.apic.org/AM/Template.cfm?Section=Guidelines&
CONTENTID=1090&TEMPLATE=/CM/ContentDisplay.cfm. Accessed February 21, 2008.
136. Friedman C, Barnette M, Buck AS, et al. Requirements for infrastructure and essential activ-
ities of infection control and epidemiology in out-of-hospital settings: a consensus panel
report. Am J Infect Control. 1999;27:418–430. http://www.apic.org/AM/Template.cfm?Section
=Guidelines&CONTENTID=1082&TEMPLATE=/CM/ContentDisplay.cfm. Accessed Febru-
ary 21, 2008.
137. National Nosocomial Infection Surveillance System. Nosocomial infection rates for interhos-
pital comparison: limitations and possible solutions. Infect Control Hosp Epidemiol.
1991;12:609–621.
138. The Quality Indicator Study Group. An approach to the evaluation of quality indicators of
outcome of care in hospitalized patients, with a focus on nosocomial infection indicators.
Infect Control Hosp Epidemiol. 1995;16:308–316.
139. Keita-Perse O, Gaynes RP. Severity of illness scoring systems to adjust nosocomial infection
rates: a review and commentary. Am J Infect Control. 1996;24:429–434.
140. Stevenson KB. Regional data set of infection rates for long-term care facilities: description of
a valuable benchmarking tool. Am J Infect Control. 1999;27:20–26.
141. Cleves MA, Weiner JP, Cohen W, et al. Assessing HCFA’s Health Care Quality Improvement
Program. Joint Comm J Qual Improv. 1997;23:550–560.
142. Hofer TP, Bernstein SJ, Hayward RA, DeMonner S. Validating quality indicators for hospital
care. Joint Comm J Qual Improv. 1997;23:455–467.
143. Phillips CD, Zimmerman D, Bernabei R, Jonsson PV. Using the resident assessment instru-
ment for quality enhancement in nursing homes. Age Ageing. 1997;26(Suppl 2):77–81.
144. Morris JN, Hawes C, Fries BE, et al. Designing the national resident assessment instrument
for nursing homes. Gerontologist. 1990;30:293–307.
145. Steinbrook R. Public report cards—cardiac surgery and beyond. N Engl J Med. 2006;355:
1847–1849.
146. Leape LL. Reporting of adverse events. N Engl J Med. 2002;347:1633–1638.
147. Lovett LL, Massanari MM. Role of surveillance in emerging health systems: measurement is
essential but not sufficient. Am J Infect Control. 1999;27:135–140.
148. Bobinski MA. Legal issues in hospital epidemiology and infection control. In: Mayhall CG, ed.
Hospital Epidemiology and Infection Control. Baltimore, MD: Williams & Wilkins; 1996:
1138–1145.
149. Bartley J. Accrediting and regulatory agencies. In: APIC Text of Infection Control and Epi-
demiology. 2nd ed. Washington, DC: Association for Professionals in Infection Control and
Epidemiology; 2005;10-1-10-12.
150. Occupational Safety and Health Administration. Directive - CPL 02-00-106 - CPL 2.106—
enforcement procedures and scheduling for occupational exposure to tuberculosis. Occupa-
tional Safety and Health Administration; 1996. http://www.osha.gov/pls/oshaweb/owadisp
.show_document?p_table=DIRECTIVES&p_id=1586. Accessed February 21, 2008.
151. Occupational Safety and Health Administration. Occupational exposure to bloodborne
pathogens: final rule. Federal Register. December 6, 1991;56(235):64004–64182. http://
www.osha.gov/pls/oshaweb/owadisp.show_document?p_table=FEDERAL_REGISTER&p_id
=13197. Accessed February 21, 2008.
57793_CH02_ARIAS.qxd 1/19/09 2:27 PM Page 68

68 SURVEILLANCE PROGRAMS, PUBLIC HEALTH, AND EMERGENCY PREPAREDNESS

152. Centers for Medicare and Medicaid Services, U.S. Department of Health and Human Ser-
vices. Part 482—Conditions of Participation for Hospitals: 42CFR 482.42. October 1, 2002.
153. The Joint Commission. Surveillance, prevention, and control of infection. In: 2008 Compre-
hensive Accreditation Manual for Hospitals. Chicago, IL: The Joint Commission; 2008.
154. Committee on Accreditation of Rehabilitation Facilities. Medical Rehabilitation Standards
Manual. Tucson, AZ: CARF International; 2008.
155. Roush S, Birkhead G, Koo D, Cobb A, Fleming D. Mandatory reporting of diseases and condi-
tions by health care professionals and laboratories. JAMA. 1999;282:164–170.
156. World Health Organization. World Health Report 2007: A Safer Future: Global Public Health
Security in the 21st Century. Geneva: World Health Organization; 2007. http://www.who
.int/whr/2007/whr07_en.pdf. Accessed February 18, 2008.
157. Lemon SM, Hamburg MA, Sparling PF, Choffnes ER, Mack A, and the Forum on Microbial
Threats. Global Infectious Disease Surveillance and Detection: Assessing the Challenges-
Finding Solutions, Workshop Summary. Washington, DC: National Academies Press; 2007.
http://www.nap.edu/catalog.php?record_id=11996. Accessed February 17, 2008.
158. International health regulations (2005). Geneva, Switzerland: World Health Organization;
2006. http://www.who.int/csr/ihr. Accessed February 21, 2008.
159. Petrosillo N, Puro V, DiCarlo A, Ippolito G. The initial hospital response to an epidemic. Arch
Med Res. 2005;36(6):706–712.

SUGGESTED READINGS AND RESOURCES

Readings
APIC Text of Infection Control and Epidemiology. 2nd ed. Washington, DC: Association for Profes-
sionals in Infection Control and Epidemiology; 2005.
CDC. Public health focus: surveillance, prevention, and control of nosocomial infections. MMWR.
1992;41:783–787.
Dato V, Wagner MM, Fapohunda A. How outbreaks are detected: a review of surveillance systems
and outbreaks. Pub Health Report. 2004;119:464–471. http://www.publichealthreports.org/
userfiles/119_5/119464.pdf. Accessed May 10, 2008.
Davis JR, Lederberg J, eds. Forum on emerging infections, board on global health. Emerging Infec-
tious Diseases from the Global to the Local Perspective: Workshop Summary. Washington, DC:
National Academies Press; 2001. http://books.nap.edu/catalog.php?record_id=10084. Accessed
February 17, 2008.
Haley RW, Culver DH, White JW, et al. The efficacy of infection surveillance and control programs
in preventing nosocomial infections in U.S. hospitals. Am J Epidemiol. 1985;121:182–205.
Jarvis WR, ed. Bennett and Brachman’s Hospital Infections. 5th ed. Philadelphia, PA: Lippincott
Williams & Wilkins; 2007.
Lee TB, Montgomery OG, Marx J, Olmsted RN, Scheckler WE. Recommended practices for surveil-
lance: Association for Professionals in Infection Control and Epidemiology (APIC), Inc. Am J
Infect Control. 2007;35:427–440. http://www.apic.org/Content/NavigationMenu/PracticeGuidance/
SurveillanceDefinitionsReportsandRecommendations/AJIC_Surveillance_2007.pdf. Accessed
February 21, 2008.
Massanari RM, Wilkerson K, Swartzendruber S. Designing surveillance for noninfectious out-
comes of medical care. Infect Control Hosp Epidemiol. 1995;16:419–426.
Mayhall CG. Hospital Epidemiology and Infection Control. 3rd ed. Baltimore, MD: Lippincott,
Williams & Wilkins; 2004.
Roy MC, Perl TM. Basics of surgical-site infection surveillance. Infect Control Hosp Epidemiol.
1997;18:659–668.
Smith PW, ed. Infection Control in Long-Term Care Facilities. 2nd ed. Albany, NY: Delmar
Publishers; 1994.
57793_CH02_ARIAS.qxd 1/19/09 2:27 PM Page 69

Suggested Readings and Resources 69

Smith P, Rusnack P. Infection prevention and control in the long-term-care facility. Am J Infect
Control. 1997;25:488–512.
Wenzel RP, ed. Prevention and Control of Nosocomial Infections. 4th ed. Baltimore: Lippincott
Williams & Wilkins; 2002.

Resources
World Health Organization. International health regulations (2005). Geneva, Switzerland: World
Health Organization; 2005. http://www.who.int/csr/ihr. Accessed May 10, 2008.
Surgical Care Improvement Project. http://www.medqic.org/dcs /ContentServer?cid=1122904930422
&pagename=Medqic%2FContent%2FParentShellTemplate&parentName=Topic&c=MQParents.
Accessed February 19, 2008.
CDC National Healthcare Safety Network (NHSN). http://www.cdc.gov/ncidod/dhqp/nhsn.html.
Accessed February 15, 2008.
Resources for information on emerging infections and emergency planning include the CDC’s
Emergency Preparedness and Response Web site (http://www.bt.cdc.gov/planning/), the
online journal Emerging Infectious Diseases (http://www.cdc.gov/nciod/EID), the World
Health Organization (http://www.who.int/en/), and the Agency for Healthcare Research and
Quality, Public Health Emergency Preparedness (http://www.ahrq.gov/prep/). Accessed
March 26, 2008.
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CHAPTER 3

Outbreaks Reported in
Acute Care Settings
Kathleen Meehan Arias

An ounce of prevention is worth a pound of cure.


—Benjamin Franklin

INTRODUCTION

Outbreaks of infectious diseases in hospitals have long been recognized. A


study of the nosocomial transmission of epidemic louse-borne typhus fever
was published in England in 18641 and “hospital fever” is one of the many
names given to this disease. In the mid-1800s, Ignaz Semmelweis recom-
mended hand washing to prevent the spread of puerperal fever, and Florence
Nightingale promoted isolation of infected patients, a clean environment, and
hygienic handling of food and water to prevent the spread of disease. Despite
the advances of modern medicine, outbreaks continue to occur as a result of
health care provided in a variety of settings.2–9 The hospital outbreaks of
typhus and puerperal fevers that occurred in the 1800s were replaced in the
late 1900s by outbreaks of methicillin-resistant Staphylococcus aureus
(MRSA) and vancomycin-resistant Enterococcus (VRE). However, the primary
control measures used to prevent the spread of infectious agents remain the
same: hand hygiene, isolation of infected persons, environmental cleanliness,
and safe handling of food and water.
Personnel responsible for managing infection prevention and control and
performance improvement programs in healthcare settings should study
reports of outbreak investigations to expand their knowledge of the epidemiol-
ogy of healthcare-associated infections (HAIs) and other iatrogenic events. By
reviewing the findings of these investigations, it is possible to identify the fol-
lowing:
• Factors contributing to outbreaks, such as etiologic agents, common sources
and reservoirs, and modes of transmission; devices, products, and other
vehicles; and procedures, practices, and technical errors
• Measures for controlling or preventing a similar outbreak
If an outbreak is suspected in a healthcare setting, a literature search
should be conducted to identify relevant articles, as discussed in Chapter 9.
The purpose of this chapter is to discuss outbreaks that have been reported
in acute care facilities. It is not intended to be an exhaustive review of out-
breaks that have occurred in hospitals. Rather, its purpose is to provide an
overview of the wide variety of organisms, diseases, and conditions that have

71
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72 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

been responsible for epidemics in the acute care setting. Information on the
agents, reservoirs, and modes of transmission is included, along with the con-
trol measures that were used to interrupt the outbreak. The outbreak reports
discussed in this chapter were identified by conducting electronic literature
searches of the PubMed databases from 1985 through March 2008, by review-
ing the table of contents of selected journals and the references in relevant
articles, and by performing targeted searches of the Internet. The reports of
these outbreak investigations highlight the importance of maintaining an
active surveillance program in all healthcare settings in order to identify an
outbreak or a cluster of events so that control measures can be implemented
as soon as possible.
Most of the outbreaks discussed in this text have been grouped into the set-
tings in which they occurred. However, infection control professionals (ICPs)
should be familiar with outbreaks that have been reported in all types of
healthcare settings because procedures, practices, products, and devices may
be used in more than one setting. The outbreaks discussed in this chapter
occurred primarily in hospitals, although similar outbreaks may occur in other
healthcare settings. Outbreaks caused by MRSA, VRE, Mycobacterium tubercu-
losis, Sarcoptes scabiei, Clostridium difficile, noroviruses, and the influenza
virus occur in both acute care and long-term care settings and are discussed in
Chapter 7 along with gastrointestinal and food-borne outbreaks. Although the
terms outbreak and epidemic are most commonly used in reference to infec-
tious diseases, they are also used to describe the sudden occurrence or increase
of noninfectious diseases and conditions; therefore, examples of outbreaks
caused by noninfectious agents are also included.

ENDEMIC VS. EPIDEMIC INFECTIONS

Most hospital-associated infections occur endemically; only a small propor-


tion occur as part of an outbreak.2 Results of one study showed that patients
involved in epidemics accounted for 3.7% of all nosocomial infections detected
over a 5-year period.10 In another study it was estimated that true outbreaks
involved approximately 2% of all patients who contracted a HAI.3 Among
infections reported to the Centers for Disease Control and Prevention (CDC)
National Nosocomial Infections Surveillance system, approximately 5%
occurred in epidemics.5 Although these numbers are small, they are important
because these infections (1) result in significant morbidity and mortality,
(2) may cause disruption of services, (3) may be difficult to investigate and con-
trol, and (4) are potentially preventable.

ORGANISMS RESPONSIBLE FOR HOSPITAL-ASSOCIATED


OUTBREAKS

The organisms responsible for the majority of endemic and epidemic infections
in hospitals change over time. In the 1950s and 1960s, a pandemic of S. aureus
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Organisms Responsible for Hospital-Associated Outbreaks 73

caused major outbreaks in communities and hospitals. In the 1970s, gram-


negative organisms, such as the Enterobacteriaceae and Pseudomonas aeruginosa,
emerged as major nosocomial pathogens. Throughout the 1980s, MRSA
became established in many hospitals, and in the late 1980s and early 1990s
multidrug-resistant Mycobacterium tuberculosis (MDR-TB) caused multiple
outbreaks in healthcare facilities, affecting both patients and personnel. A
major concern in the 1990s was the evolution and nosocomial spread of antibi-
otic-resistant organisms such as the Enterobacteriaceae, MDR-TB, and VRE,
and the anticipated emergence of vancomycin-resistant S. aureus.11–13 In the
early 2000s, novel virulent strains of Clostridium difficile, a well-known
pathogen, caused hospital outbreaks that resulted in significant morbidity and
mortality in several countries.14 Antimicrobial-resistant organisms have continued
to evolve and spread globally, and multidrug-resistant strains of Pseudomonas,
Acinetobacter, Klebsiella, and Enterobacter have caused hospital-associated out-
breaks worldwide.15–17
Infection prevention and control personnel and healthcare providers must
be aware of both newly recognized infectious agents and reemerging patho-
gens that have the potential for causing endemic and epidemic HAI.18–20 Since
the 1970s over 35 new human pathogens have been identified, and many
known pathogens have emerged or reemerged. New and reemerging pathogens
that have caused outbreaks in hospitals include bacteria such as Clostridium
difficile, Legionella pneumophila, Mycobacterium tuberculosis (especially mul-
tidrug- and extensively multidrug-resistant strains), MRSA, VRE, and Strep-
tococcus pyogenes (group A streptococcus), and viruses such as adenovirus,
Ebola, hepatitis B and C, norovirus, rotavirus, and the severe acute respiratory
syndrome coronavirus.14,18,20–23
When the site of infection and the organism causing a suspected outbreak is
known, it is possible to use the knowledge gained from published reports of
outbreaks to develop hypotheses on the likely modes of transmission and
potential sources and reservoirs. Four major modes of transmission are com-
monly involved in healthcare-associated outbreaks: contact, vehicle (common
source), droplet spread, and airborne. Outbreaks caused by S. aureus are asso-
ciated with human reservoirs, and this organism is transmitted directly by
person-to-person contact, indirectly from patient to patient on the hands of
personnel, or by a human disseminator, such as a nasal carrier. Organisms
such as Pseudomonas, Flavobacterium, Mycobacterium gordonae and M. chelonae,
and gram-negative bacteria such as Klebsiella, Enterobacter, and Serratia
readily grow in fluids and are frequently associated with common-source out-
breaks involving contaminated solutions. Aspergillus and Legionella are
spread by airborne transmission. Epidemics caused by these two organisms
usually involve environmental sources, such as cooling towers or contami-
nated potable water for Legionella, and construction or some disruption in the
physical plant for Aspergillus. Many organisms have more than one mode of
transmission and may have several potential sources or reservoirs in the
healthcare setting, as shown in Table 3–1.24–27
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74 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Table 3–1 Organisms Associated with Outbreaks in the Healthcare Setting, Their Likely
Modes of Transmission, and Potential Sources

Likely Mode(s) of Potential Sources/


Organism Site of Infection Transmission Reservoirs
Clostridium difficile Gastrointestinal Contact/cross- Infected patients
infection via hands
Vehicle/common Contaminated
source equipment
Enterococcus Genitourinary, Contact/cross- Infected or colonized
species Surgical wound infection via hands patients
Vehicle/common Contaminated
source equipment
Group A Surgical wound Contact Infected personnel
streptococcus
Pharyngitis Vehicle/common Food contaminated by
source infected person
Hepatitis A Hepatitis Vehicle/common Food contaminated by
source infected person
Contact/cross- Infected patients
infection via hands and personnel
Influenza Respiratory Droplet Infected patients,
personnel, and visitors
Legionella Respiratory Airborne Contaminated water
Vehicle/common Contaminated water
source/contact of
mucosal surfaces
with water
Mycobacterium Respiratory Vehicle/common Contaminated
species, not source bronchoscope
tuberculosis
Mycobacterium Respiratory Airborne Infected patients
tuberculosis or personnel
Vehicle/common Contaminated
source bronchoscope
Pseudomonas, Blood, Vehicle/common Contaminated fluids;
Burkholderia, and Respiratory source devices and equipment
Ralstonia species with aqueous reservoirs
Contact/cross- Infected and
infection via hands colonized patients
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Outbreaks Associated with Products, Devices, and Procedures 75

Table 3–1 (Continued )

Likely Mode(s) of Potential Sources/


Organism Site of Infection Transmission Reservoirs
Salmonella species Gastrointestinal Vehicle/common Food contaminated by
source improper handling or
by personnel carrier
Contact/cross- Infected patients
infection via hands
Staphylococcus Surgical wound Contact Personnel carrier
aureus
Skin, respiratory, Contact/cross- Infected and
blood infection via hands colonized patients
Gastrointestinal Vehicle/common Food contaminated by
source infected person

OUTBREAKS ASSOCIATED WITH PRODUCTS, DEVICES, AND


PROCEDURES (COMMON SOURCE OUTBREAKS)

Because some products, devices, and procedures are repeatedly associated


with hospital epidemics, it is useful to study published reports of these out-
breaks so that preventive measures can be identified and implemented. The
Hospital Infections Program of the CDC conducted investigations of 125
healthcare-associated outbreaks occurring from January 1980 to July 1990
and reported the following.4
1. Products, procedures, or devices were involved in 46% of the outbreaks:
22% were product related, 13% were procedure related, and 11% were
device related.
2. Bacterial pathogens caused 62% of the outbreaks, fungi caused 9%,
viruses caused 8%, mycobacteria caused 4%, and toxins or other organ-
isms caused 18%.
3. The proportion of outbreaks caused by products, devices, and procedures
increased from 47% in the first half of the decade to 67% between 1986
and July 1990.

Outbreaks Associated with Products

Multiple outbreaks of infection and colonization, illnesses, or adverse reactions


associated with the use of products have been reported.28–65 Many of these out-
breaks involved products that were intrinsically or extrinsically contaminated
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76 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

by microbial agents or their toxins; however, several outbreaks did not have an
infectious etiology. ICPs in all healthcare settings should be familiar with the
types of products associated with outbreaks because these products may be
used not only in acute care facilities, but also in the long-term care and ambu-
latory care settings.38,40,41,64,66

Intrinsic Contamination of Products


As used here, the term intrinsic refers to contamination that occurs before a
product’s arrival at a healthcare facility, such as a product contaminated dur-
ing manufacture. These products may cause widespread outbreaks in multiple
facilities before they are recognized.39,67–69 A variety of intrinsically contami-
nated products have caused outbreaks in hospitals: intravenous fluids, povidone-
iodine solution, packed red blood cells, fresh-frozen plasma, intravenous
immunoglobulin, gauze, skin lotion, polygeline plasma extender, powdered
infant formula, saline solutions including prefilled saline syringes, alcohol-free
mouthwash, fruit salads, a pediatric oxygen-delivery device, heparin solution,
nebulized sulbutamol, ultrasound gel, lyophilized enteral nutrition, injectable
steroids, and peritoneal dialysis fluid.28-30,33,34,38,39,49,52,55,56,59–65,67–82 Examples
of outbreaks caused by intrinsically contaminated products are shown in
Table 3–2.
The use of pharmaceutical compounding has increased substantially in the
past decade, and several outbreaks have been caused by contaminated prod-
ucts that were prepared at off-site compounding pharmacies.74–76,83 Some of
these contaminated medications resulted in meningitis and bloodstream infec-
tions and substantial morbidity and mortality.83 Deficiencies that led to the
contamination of the products included inadequate training of personnel,
improper aseptic technique, incorrect autoclaving practices, and lack of end-
product sterility testing.
If a product that is associated with a cluster of infections is believed to be
intrinsically contaminated, hospital personnel should notify the manufac-
turer, the local health department, and the appropriate government agency. In
the United States, if antiseptics, medications, or medical devices are believed
to be intrinsically contaminated, the Food and Drug Administration (FDA)
should be notified through the FDA MedWatch Adverse Event Reporting Sys-
tem (http://www.fda.gov/medwatch). In addition, healthcare providers using
the item should immediately be notified of the suspected contamination and
should be instructed to remove all of the implicated product from stock and
save it for further study. Although healthcare facilities may not be able to pre-
vent all infections associated with an intrinsically contaminated product, ICPs
should be alert to clusters or increasing numbers of isolates of unusual organ-
isms, because these may possibly be associated with contaminated products or
medications. Active surveillance programs are necessary to recognize promptly
any product-associated outbreaks so that measures can be taken to identify
the implicated product and to prevent its continued use.30

Extrinsic Contamination of Products


Extrinsic contamination occurs during the use of a product. Extrinsically
contaminated products associated with outbreaks include antimicrobial soap,
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Outbreaks Associated with Products, Devices, and Procedures 77

Table 3–2 Outbreaks Involving Intrinsically Contaminated Products

Year(s)
Reported/
Outbreak Reference No. Product Comments
Enterobacter cloacae 1976 (28, 29) Intravenous fluid 1971—Nationwide
and Enterobacter 1978 (30) outbreak of septicemia
agglomerans (reference 29 is reprint
septicemia of original report with a
discussion of the outbreak)
Pseudomonas 1981 (33) Povidone iodine 1981—First report of
(currently 1992 (34) nosocomial infections
Burkholderia) cepacia caused by intrinsically
peritonitis and contaminated povidone
pseudobacteremia iodine
Pseudomonas 1982 (38) Poloxamer-iodine Occurred in outpatients on
aeruginosa peritonitis solution chronic peritoneal dialysis
and wound infection
Hepatitis C infection 1994 (49) Intravenous Worldwide outbreak; first
immunoglobulin recognized outbreak of
blood-borne pathogens
associated with immune
globulin product licensed
in the United States
Fever and hypotension 1995 (52) Polygeline Product intrinsically
after cardiac surgery plasma extender contaminated by cell wall
products of Bacillus
stearothermophilus
Primary cutaneous 1996 (55) Contaminated Gauze showed evidence
Aspergillosis gauze (one case of water exposure;
prompted an contamination probably
investigation) occurred prior to
arrival at hospital
Cutaneous lesions 1996 (56) Skin lotion Lesions occurred in
caused by immunocompromised
Paecilomyces lilacinus patients; two patients
died; product recalled
Burkholderia (currently 1997 (59) Saline solution Saline used to flush
Ralstonia) pickettii indwelling intravascular
bacteremia devices
Sterile peritonitis 1997 (60) Peritoneal dialysis Nationwide outbreak
following continuous fluid resulted in recall of product;
cycling peritoneal contaminated by endotoxin
dialysis

Continued
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78 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Table 3–2 (Continued )

Year(s)
Reported/
Outbreak Reference No. Product Comments
Ralstonia pickettii 1998 (62) 0.9% saline R. pickettii has been
respiratory tract solution used isolated from several
colonization for respiratory products marketed as
therapy sterile
Pyrogenic reactions 1998 (63) Intravenous Associated with once-daily
2000 (70) gentamicin dosing of gentamicin
received from one
manufacturer; led to
nationwide recall of product
Enterobacter cloacae 1998 (64) Prefilled saline Occurred in outpatient
bloodstream infections syringes hematology/oncology
service at a hospital
Burkholderia cepacia 1998 (65) Alcohol-free Product used for routine
respiratory tract 2000 (67) mouthwash oral care of ventilated
infection and patients
colonization in
intensive care units
Pseudomonas 2005 (71) Heparin/saline Infections in four states
fluorescens and flush solution in led to nationwide recall
Pseudomonas sp. preloaded of product from one
bloodstream infections syringe manufacturer
Invasive Enterobacter 2006 (72) Powdered infant Multiple cases reported
sakazakii disease in formula from North America,
infants Europe, and the
Middle East
Infection and 2007 (73) Pediatric oxygen- Ralstonia spp. isolated from
colonization with delivery device patients in 12 states led
Ralstonia species to national recall of device
Salmonella 2007 (68) Fruit salads Infections diagnosed in
oranienburg infections served at persons in 10 northeastern
healthcare US states and one Canadian
facilities province; fruit salads were
produced by one processing
plant; source of contamina-
tion was not determined
Pseudomonas putida 2008 (74) Heparin catheter- Solution purchased by
and Stenotrophomonas lock solution hospital from a
maltophilia infections compounding pharmacy
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Outbreaks Associated with Products, Devices, and Procedures 79

benzalkonium chloride antiseptic, disinfectant solutions, saline solution,


gauze dressings, gentian violet dye, albuterol, trypan blue solution, ultra-
sonography coupling gel, total parenteral nutrition (TPN) solution, radiopaque
contrast medium, propofol, and dextrose solution.31,35–37,40,41,45–48,50–53,58,61,84–88
Table 3–3 contains examples of outbreaks caused by in-use, or extrinsic, con-
tamination of a product.
Some products, such as benzalkonium chloride solution, have been associ-
ated with multiple outbreaks and are no longer recommended for use in the
healthcare setting because of the ease with which they can become contami-
nated.66,89–91 In 1976 the CDC recommended the elimination of benzalkonium
chloride solution as an antiseptic; however, a study reported in 1991 that
many healthcare facilities were still using this product.91 Personnel who are
using benzalkonium chloride for skin antisepsis should be instructed to use an
alternative product. Other products, such as the anesthetic agent propofol,
have been associated with multiple outbreaks but are still widely used.45–47
Healthcare personnel who use propofol should be made aware of the hazards
associated with it and should be instructed to adhere to the manufacturer’s
instructions for preventing contamination.
Since many types of solutions have the potential to become contaminated
during use, healthcare personnel should be educated on the proper handling of
fluids and the use of aseptic technique. Even hand care products, such as
lotions92–94 and plain and antimicrobial soap,58,95 can become contaminated
during use and can serve as reservoirs for infectious agents.
Measures to prevent in-use contamination of products include the following:
• Education and competency testing of personnel on aseptic technique
when preparing, handling, and administering fluids such as intravenous
solutions and nutritional products
• Use of proper hand hygiene practices
• Protocols for proper use of multidose and single-dose vials and enforce-
ment of these protocols
• Storage of medications and supplies in clean areas where they are pro-
tected against dust and water
• Adherence to proper protocols and quality assurance measures when
compounding pharmaceuticals83

Noninfectious Adverse Events Related to Products


Clinicians also need to maintain surveillance for noninfectious adverse
reactions due to procedures and therapeutic agents. Products that have
resulted in clusters of illness, deaths, and injury in hospitals include disinfec-
tants, intravenous additives, fiberboard infectious waste containers, transfu-
sions with leukoreduced red blood cells, and contaminated heparin products
as shown in Table 3–4.32,39,54,57,77,82,96 If a therapeutic agent is associated with a
cluster of adverse reactions, healthcare providers should notify the facility’s
pharmacy, the manufacturer, and the FDA (if the occurrence is in the United
States).
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80 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Table 3–3 Outbreaks Involving Extrinsically Contaminated Products

Year(s) Comments; Reason for


Reported/ Extrinsic Contamination,
Outbreak Reference No. Product When Applicable
Pseudobacteremia 1976 (31) Contaminated Antiseptic used to prepare
due to Pseudomonas benzalkonium skin prior to venipuncture;
(currently Burkholderia) chloride several patients may have
cepacia and/or antiseptic become bacteremic
Enterobacter species
Endotoxemia following 1980 (35) Possible Source not determined but
computerized axial contamination of contaminated hot water
tomography radiopaque bath had been used to
contrast medium warm contrast medium
and glucagon prior to infusion
Serratia marcescens 1981 (36) Heparinized Saline may have become
bacteremia saline irrigation contaminated when first
fluid likely mixed
Cutaneous 1996 (37) Outside Outside of packages
Aspergillosis packaging of contaminated by spores
dressing supplies and dust during
construction in central
inventory supply area
Mycobacterium 1987 (40) Gentian violet Gentian violet used to
chelonae surgical skin-marking mark incision site prior to
wound infections solution plastic surgery was
contaminated with
M. chelonae; occurred in a
surgeon’s office
Serratia marcescens 1987 (41) Benzalkonium Occurred in orthopedic
septic arthritis chloride antiseptic surgeons’ office among
solution patients who had received
injections of methylpred-
nisolone; likely reservoir
was canister of cotton balls
soaking in benzalkonium
chloride solution;
S. marcescens was isolated
from canister and office
used multidose vials instead
Postoperative febrile 1990 (45) Propofol Multiple outbreaks have
episodes and 1995 (46) resulted from lack of
bloodstream and 1997 (47) aseptic technique; this
surgical site infections lipid-based medication is
easily contaminated
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Outbreaks Associated with Products, Devices, and Procedures 81

Table 3–3 (Continued )

Year(s) Comments; Reason for


Reported/ Extrinsic Contamination,
Outbreak Reference No. Product When Applicable
Pseudomonas 1991 (48) Fentanyl citrate Narcotic theft by employee
(currently Ralstonia) who replaced fentanyl with
pickettii bacteremia contaminated distilled water
Burkholderia cepacia 1995 (50) Albuterol Lack of aseptic technique
respiratory tract infection 1996 (51) multidose vial by respiratory therapy and
and colonization in intensive care unit person-
mechanically ventilated nel; respiratory therapy
patients personnel carried multi-
dose vials in their pockets
Pseudomonas 1995 (53) Food coloring P. aeruginosa isolated from
aeruginosa ventilator- dye added to 32 oz bottles of food
associated respiratory nasogastric coloring dye; multiple-use
tract infections and tube feedings bottles were replaced by
colonization single-use vials
Neonatal infection and 1997 (58) 1% chlorxylenol Nursing staff used
colonization with antiseptic hand personal bottles of soap
Serratia marcescens soap that became contaminated
during use
Burkholderia cepacia 1998 (61) 5% dextrose One-liter bag of solution
septicemia in cardiac solution used to used to dilute heparin for
patients dilute heparin multiple patients on
cardiology ward
Pyoderma in neonates 2000 (84) Ultrasound Common container of
coupling gel sonography gel was used
and applied with a wooden
spatula that was reused for
multiple infants
Serratia marcescens 2006 (85) Total parenteral Investigators observed
bloodstream infections nutrition (TPN) incorrect use of single-
on a surgical ward solution dose and multidose vials
and very low adherence to
hand hygiene; single-dose
vials used for multiple
doses; TPN solution likely
contaminated when nurses
on unit added medications
to the TPN bags
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82 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Table 3–4 Products Associated with Noninfectious Adverse Events

Year(s)
Reported/
Outbreak Reference Product Comments
Neonatal 1978 (32) Phenolic Hyperbilirubinemia
hyperbilirubinemia disinfectant developed in infants
detergent exposed to a phenol
solution used for dis-
infecting nursery surfaces
Cluster of unusual 1986 (39) Commercially Product was newly
illness and deaths available marketed; precise consti-
in neonates intravenous tuents in E-ferol that caused
vitamin E illness and death were not
preparation able to be determined
Needlestick injuries 1995 (54) Fiberboard Hospital changed product;
in hospital employees infectious waste injuries occurred when
containers needles pierced walls of
new container
Illness and sudden 1997 (57) Commercially Additive caused precipitate
deaths in adult patients available amino in the PPN
acid additive used
for peripheral
parenteral
nutrition (PPN)
Adverse ocular 1998 (82) Leucocyte- Nationwide outbreak of red
reactions (“red eye”) 2006 (96) reduced red eye syndrome associated
blood cell product with transfusion of specific
lots of leukoreduced red
blood cell units led to recall
of product
Acute allergic-type 2008 (77) Intravenous Solution contaminated
reactions among heparin solution during manufacture with
patients undergoing heparin-like product; led to
hemodialysis nationwide recall

For additional information on outbreaks of hospital-associated infections


related to contaminated substances, the reader is referred to the excellent
review by Vonberg and Gastmeier.97

Outbreaks Associated with Devices

Devices used for therapeutic and diagnostic procedures have long been asso-
ciated with outbreaks in the acute care and ambulatory care settings.98–135
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Outbreaks Associated with Products, Devices, and Procedures 83

When invasive devices are used, the risk of infection and of outbreaks
increases. Outbreaks have been traced to contaminated endoscopes used for
endoscopic retrograde cholangiopancreatography 98–101 and upper gastroin-
testinal procedures,98,100,102–105 bronchoscopes,98,106–112 automated endoscope
washers,100,105,108,109 respiratory therapy devices and equipment,73,113,114 hemo-
dynamic monitoring systems,115–118 jet gun injectors,119 reusable fingerstick
blood-sampling devices,120–121 urologic apparatus,122–125 electronic thermome-
ters,126,127 hemodialysis equipment,128 needleless valves used for intravascular
access,129,130 biopsy devices,124,131 balloons used in manual ventilation,132 and
external ventricular catheters.133 In addition, adverse reactions in patients
have resulted from residual gluteraldehyde on devices that were not thor-
oughly rinsed after soaking in a gluteraldehyde solution.134,135
Table 3-5 lists examples of device-related outbreaks and the infection con-
trol and technical errors associated with their occurrence. The major reasons for
these epidemics were (1) improper cleaning and disinfection procedures, (2) con-
tamination of endoscopes by automatic washers/disinfectors, (3) improper
handling of sterile fluids and equipment, and (4) lack of adherence to aseptic
technique.
Measures used to prevent these types of outbreaks include the following:
• Careful attention to cleaning and disinfection protocols for endoscopes
and bronchoscopes
• Careful maintenance and quality control of automated endoscope wash-
ing and disinfection machines
• Careful attention to cleaning and disinfection protocols for respiratory
therapy equipment
• Proper use and dilution of disinfectant solutions
• Consistent use of disposable single-patient use equipment for hemody-
namic monitoring and urodynamic testing
• Strict adherence to sterile technique when handling sterile supplies
• Correct use and cleaning of devices in accordance with manufacturers’
instructions

Outbreaks Associated with Procedures

Many diagnostic and therapeutic procedures place a patient at risk for


developing a HAI or other iatrogenic event, such as injury or allergic reaction.
Most procedure-related infections are not associated with outbreaks and are
usually thought to be a result of host factors such as impaired or disrupted host
defenses, immunosuppression, colonization with healthcare-associated organ-
isms, and underlying diseases. However, outbreaks have been associated with
procedures such as gastrointestinal endoscopy, 98,100,102–105 bronchoscopy,98,106–112
hemodialysis,128,136–139 peritoneal dialysis,140,141 hemodynamic pressure moni-
toring,117–118 cystoscopy and transurethral resection of the prostate,142,143 organ
transplants,144,145 pulsatile lavage for debridement,146 ultrasonography,147 and
various surgical procedures.148,149
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84 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Table 3–5 Examples of Device-Related Outbreaks and Associated Infection Control or


Technical Errors

Year
Reported/ Infection Control or
Outbreak Reference No. Device Technical Error
Hepatitis B infection 1986 (119) Jet gun injector Nozzle tip contaminated
with blood; was not
properly disinfected
Mycobacterium 1989 (107) Bronchoscope Suction valve of
tuberculosis bronchoscope not
disinfected despite
rigorous cleaning and
disinfection
Pseudomonas 1991 (100) UGI endoscope Flawed automatic
aeruginosa infection disinfector
and colonization
post-UGI endoscopy
Bloody diarrhea 1992 (134) Endoscope Residual gluteraldehyde in
associated with improperly rinsed
endoscopy endoscope
Proctitis following 1993 (135) Endoscope Residual gluteraldehyde in
endorectal ultrasound improperly rinsed
examination endoscope
Pseudomonas 1993 (99) Endoscope Flawed automatic
aeruginosa and disinfector
Enterobacteriaceae
bacteremia post-ERCP
Pseudomonas cepacia 1993 (113) Reusable Improper disinfection
respiratory tract electronic solution used
colonization/ infection ventilator
and bacteremia probes
Gram-negative 1996 (115) Hemodynamic Pressure monitoring
bacteremia in cardiac pressure equipment left uncovered
surgery patients monitoring overnight in the operating
equipment room
Hepatitis C infection 1997 (104) Colonoscope Improper cleaning and
disinfection of colonoscope
Multidrug-resistant 1997 (110) Bronchoscope Inadequate cleaning and
Mycobacterium disinfection of
tuberculosis bronchoscope
Multidrug-resistant 1997 (123) Urodynamic Improperly processed
Pseudomonas transducer transducer used for
aeruginosa urinary urodynamic testing
tract infection and
urosepsis
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Outbreaks Associated with Products, Devices, and Procedures 85

Table 3–5 (Continued )

Year
Reported/ Infection Control or
Outbreak Reference No. Device Technical Error
Hepatitis B infection in 1997 (121) Fingerstick blood Disposable component of
a hospital and a sampling devices device became
nursing home contaminated with blood
and was not routinely
changed between patients
Bloodstream infections 1998 (128) Hemodialysis Newly installed attachment
(BSIs) caused by equipment used to drain spent
multiple pathogens priming saline became
contaminated
Bacillus cereus 2000 (132) Balloons used The exteriors of the
systemic infections in manual balloons were cleaned
and colonization in a ventilation with detergent that did
neonatal intensive not reach the interior of
care unit balloon and was not
sufficient to kill B. cereus
spores; outbreak ended
when balloons were
sterilized by autoclaving
Pseudomonas 2001 (125) Pressure The cover was labeled as
aeruginosa urinary transducer cover a single-use device,
tract infections following for urodynamic but it was used on
urodynamic studies system for multiple patients
measuring
bladder pressure
Burkholderia cepacia 2003 (114) Mechanical Ventilator disinfection
colonization and ventilator procedures not followed;
infection in two poor separation of clean
pediatric units and dirty items
Increased incidence 2006 (129) Positive pressure Increased bloodstream
of catheter-related 2007 (130) needleless valve infections noted after
bloodstream infections used for introduction of a new
intravascular needleless valve intravenous
access access port reported
by several investigators
Pseudomonas 2007 (124) Steel biopsy Inadequate reprocessing
aeruginosa infections needle guide procedures; device was
after transurethral disinfected with high-level
resection of the disinfectant and then rinsed
prostate (TURP) with tap water rather than
sterilized as recommended
by manufacturer

UGI = upper gastrointestinal; ERCP = endoscopic retrograde cholangiopancreatography


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86 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Gastrointestinal Endoscopy and Bronchoscopy


Numerous outbreaks and pseudo-outbreaks related to gastrointestinal
endoscopy and bronchoscopy procedures have been reported in both the inpa-
tient and outpatient settings.9,98,150 Despite the fact that the risk of infection
associated with these devices is well known, some personnel in endoscopy
suites do not follow appropriate protocols for reprocessing scopes.151–154
Because endoscopes are complex instruments that are difficult to clean and
disinfect, staff responsible for processing them must be instructed to follow
meticulously the proper protocols for cleaning, disinfecting, and sterilization of
the endoscopes and their related parts. If automatic endoscope reprocessors
are used, personnel must be instructed in their use.
A multisociety guideline for reprocessing gastrointestinal endoscopes was
published in 2003 by the American Society for Gastrointestinal Endoscopy
(ASGE) and the Society for Healthcare Epidemiology of America (SHEA).153
The ASGE has published a variety of guidelines, including one on infection
control during gastrointestinal endoscopy.155 Culver et al. provide recommen-
dations for bronchoscope reprocessing based on their review of outbreaks
related to bronchoscopy.156
Measures to prevent infections and outbreaks related to endoscopy proce-
dures include the following153,155,156:
• Implementation of an infection surveillance, prevention, and control pro-
gram based on recognized standards and guidelines
• Establishment of an initial and ongoing training program for personnel
who process endoscopes
• A mechanism to ensure that personnel adhere to protocols for cleaning
and disinfection or sterilization of endoscopes and related accessories
• Following disinfection, use of either a sterile water rinse followed by
forced-air drying or a tap water rinse followed by forced air drying and a
70% alcohol rinse
• Adherence to protocols for proper handling and storage of endoscopes
after processing to prevent recontamination
• Rigorous adherence to established protocols and the manufacturer’s
instructions for the use of automatic endoscope reprocessors
• A quality assurance program to monitor the effectiveness of the disinfec-
tion and sterilization processes and the competency of the personnel who
reprocess endoscopes and related accessories.
In 2001 and 2002, several hospitals in the United States and Europe re-
ported HAIs related to bronchoscopy that were traced to a loose port on the
bronchoscope.111,112 The outbreaks resulted in a recall of several bronchoscope
models.
Several outbreaks related to gastrointestinal endoscopy and bronchoscopy
procedures are noted in Table 3-5. For additional information on outbreaks
and pseudo-outbreaks associated with bronchoscopy, the reader is referred to
the editorial by Weber and Rutala150 and the review by Culver et al.156
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Outbreaks Associated with Products, Devices, and Procedures 87

Hemodialysis and Peritoneal Dialysis


HAIs are well-recognized complications of hemodialysis. Outbreaks in hemo-
dialysis centers have occurred as a result of improper handling or inadequate
cleaning and disinfection of reusable dialysers136–138; cross-contamination of
blood tubing by ultrafiltrate waste128; sharing of staff, equipment, supplies,
and medications between patients139; failure to isolate patients with chronic
hepatitis B virus (HBV)139; and failure to vaccinate susceptible hemodialysis
patients against HBV.139
Care must be taken to ensure that hemodialysis personnel are familiar with
the proper use and disinfection of the equipment they are using. One outbreak
of bloodstream infections occurred in two outpatient hemodialysis centers
affiliated with a hospital; it was associated with a change in the setup of the
hemodialysis system. The reservoir was a newly installed, commercially mar-
keted attachment used to drain spent saline. The attachment became heavily
contaminated with multiple gram-positive, gram-negative, and fungal
pathogens and served as a portal of entry into the blood tubing.128
Outbreaks related to peritoneal dialysis have been associated with contami-
nated peritoneal dialysis machines140,141 and the use of intrinsically contaminated
povidone iodine solution.28 Personnel responsible for cleaning, disinfecting,
and handling equipment used for peritoneal dialysis must practice strict asep-
tic technique and carefully follow manufacturers’ directions for the specific
equipment they are using.
Outbreaks related to hemodialysis and peritoneal dialysis and measures to
prevent transmission of infectious agents in the dialysis setting are further
discussed in Chapter 5.

Outbreaks Associated with Surgery


Most surgical site infections are caused by endogenous or exogenous organ-
isms that are introduced into the wound at the time of surgery. However, out-
breaks associated with surgical procedures may be caused either by
contaminated antiseptics,157 dressings,158–160 equipment,115,148 medications or
solutions,40,88,161 or by organisms disseminated by a personnel carrier. These
outbreaks are generally recognized when a cluster of surgical site infections
caused by the same organism is detected. The type of organism causing the
infections will often provide a clue to a source or reservoir. Outbreaks of post-
operative infections caused by S. aureus or group A streptococci are invariably
associated with a human carrier. Outbreaks caused by gram-negative organ-
isms and fungi are frequently associated with an environmental source.115
In addition to surgery-related outbreaks caused by infectious agents, clus-
ters of adverse events associated with exposure to chemicals have also been
reported in surgical patients. In one report, six patients who had cardiac
surgery developed postoperative bleeding, which was caused by residual
detergent in reprocessed laparotomy sponges.162 In another, an outbreak of
corneal edema following cataract surgery was thought to be caused by inade-
quate rinsing of small-lumen surgical instruments that had been disinfected
by soaking in gluteraldehyde.163
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88 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Although postoperative infections and complications following cataract


surgery are uncommon, they can be devastating.164–166 Outbreaks associated
with cataract surgery are discussed in Chapter 5.

OUTBREAKS ASSOCIATED WITH PSEUDOMONAS, RALSTONIA,


AND BURKHOLDERIA SPECIES

Outbreaks associated with Ralstonia pickettii, Pseudomonas aeruginosa,


and Burkholderia cepacia are frequently related to therapeutic and diagnostic
procedures and contaminated devices and solutions, as demonstrated in
Tables 3–2, 3–3 and 3–5.167–169 Whenever a cluster of colonizations or infections
with one of these organisms is identified, a contaminated solution or aqueous
reservoir should be suspected.

OUTBREAKS ASSOCIATED WITH HUMAN CARRIERS OR


DISSEMINATORS

Human carriers and disseminators have been responsible for hospital out-
breaks of S. aureus, Streptococcus pyogenes (group A beta-hemolytic streptococci
[GAS]), Candida species, Serratia marcescens, Pseudomonas aeruginosa,
hepatitis A, hepatitis B, hepatitis C, and Salmonella. Many organisms have
more than one mode of transmission. Although hospital outbreaks caused by
S. aureus, group A streptococcus, and hepatitis A are often associated with a
human carrier, each of these organisms can be spread either by direct person-
to-person contact or by food that is contaminated by a carrier. HBV may be
directly transmitted from person to person by a carrier or indirectly via conta-
minated medications or equipment. Salmonella may be directly transmitted
from person to person or via contaminated food.

Staphylococcus aureus
Although cross-infection on the hands of personnel is thought to be the pri-
mary mode of transmission of S. aureus in healthcare settings, some outbreaks
have been associated with colonized or infected healthcare workers.170,171
Healthcare workers commonly carry S. aureus in their nares and on their
hands.172 Outbreaks of surgical site infections caused by S. aureus have been
associated with personnel carrying the organism on their skin and hair 173 and
in their nares.174,175 One outbreak of MRSA surgical site infections was associ-
ated with a healthcare worker with chronic sinusitis who was a carrier for pro-
longed periods.175 One of his family members was also found to be a carrier of
the epidemic strain. Staphylococcal outbreaks in nurseries171,176,177 and inten-
sive care units (ICU)171,178 have also been associated with personnel carriers.
In a review of 165 MRSA outbreaks, Vonberg et al. determined that there was
strong evidence that healthcare workers were the source in 11 (6.6%) of the
outbreaks.171 In 8 of these outbreaks, the healthcare worker had a respiratory
tract infection or skin infection; in only 3 (1.6%) was the healthcare worker
source an asymptomatic carrier.
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Outbreaks Associated with Human Carriers or Disseminators 89

There is a phenomenon of airborne dispersal of Staphylococcus aureus that


is called the “cloud” phenomenon; several outbreaks have been associated with
healthcare workers who were considered to be airborne dispersers.170,178 These
outbreaks can occur despite personnel adherence to standard precautions and
good hand hygiene and are difficult to control until the carrier is identified
and effectively treated or removed from the setting.
Outbreaks caused by MRSA are discussed in Chapter 7. Since the control
measures for preventing the transmission of MRSA are essentially the same
as those for methicillin-sensitive S. aureus, the reader is referred to Chapter 7
for a review of control measures used to interrupt staphylococcal outbreaks.
S. aureus was the fourth most frequently identified bacterial agent causing
food-borne outbreaks in the United States, as reported to the CDC between
1998 and 2002.179 Dietary personnel who have a staphylococcal infection may
contaminate food and be the source of a food-borne outbreak. Hospital person-
nel who have boils or skin lesions known or suspected to be infected with
S. aureus—especially on the hands—should be restricted from patient care
activities and from handling food until they have been treated and their infec-
tion has resolved. If investigators suspect a common source outbreak (i.e., a
personnel carrier), they should examine personnel for evidence of skin break-
down or infection.

Group A Beta-Hemolytic Streptococcus

GAS can spread rapidly from person to person and can cause serious disease
in a variety of healthcare settings.180 Numerous outbreaks of healthcare-asso-
ciated group A streptococci have been reported.180–196 A review of the literature
revealed more than 50 nosocomial outbreaks of GAS reported worldwide
between 1966 and 1995.180 A Canadian study group identified 20 outbreaks
that occurred from 1992 through 2000 in hospitals in Ontario, Canada.193 His-
torically, healthcare-associated outbreaks of GAS have involved newborns,188
postpartum women,180–185 patients in burn units180,187 and geriatric units, post-
operative surgical patients, and residents of long-term care facilities.180,191,193
Outbreaks have also been reported in medical units189 and in critical care
units.190,193 In addition to person-to-person spread, GAS may be transmitted
by contaminated food. An outbreak of streptococcal pharyngitis in a hospital
pediatric clinic was traced to food that had been contaminated by a healthcare
worker who was a GAS carrier.192
Nosocomial outbreaks are often associated with colonized or infected
healthcare personnel. Although nasopharyngeal carriers are thought to be
particularly likely to transmit GAS, personnel implicated in group A strepto-
coccal surgical wound infection outbreaks have been found to carry the organ-
ism in their scalp,181 vagina,182,183 or anus.184,185 In one report, an outbreak of
group A streptococcal surgical site infections was associated with an asympto-
matic anesthesiologist who was a pharyngeal carrier.186 The outbreak resulted
from the exposure of the anesthesiologist to his infected daughter. In several
reported outbreaks, the source of infection or colonization in hospital person-
nel was a household contact.180,181,183,186
It should be noted that healthcare workers either may serve as the index
case or may become infected through contact with infected patients or other
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90 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

healthcare workers during the course of their work. In several reports, an out-
break of GAS infections occurred in healthcare workers following exposure to
an infected patient.195,196 In one report, three healthcare workers developed
GAS pharyngitis after exposure in the operating room to a patient with GAS
pharyngitis and necrotizing fasciitis.195 The three healthcare workers reported
their infections shortly after becoming symptomatic. An important measure
for preventing and interrupting GAS outbreaks is the recognition by person-
nel of signs and symptoms, such as pharyngitis, that are consistent with GAS
infection so that treatment may promptly be provided.
Because nosocomial infections caused by group A beta-hemolytic streptococ-
cus are relatively uncommon and can cause significant morbidity and mortal-
ity, the occurrence of one healthcare-associated GAS infection at any site
should prompt a search for other cases to detect a potential outbreak. This
search can be done by reviewing laboratory reports and by asking hospital
surgeons and other healthcare providers if they are aware of any GAS infec-
tions, especially surgical site infections. In its guidelines for preventing GAS
infections in postpartum and postsurgical patients, the CDC recommends that
“One nosocomial postpartum or postsurgical invasive GAS infection should
prompt enhanced surveillance and isolate storage, whereas two cases caused
by the same strain should prompt an epidemiological investigation that
includes the culture of specimens from epidemiologically linked healthcare
workers.”197(p950)
The reader is referred to Chapter 4 for a discussion of the epidemiology and
mode of transmission of GAS and measures that can be used to recognize, pre-
vent, and control an outbreak of GAS. Recommendations for preventing and
controlling GAS outbreaks can also be found in the CDC guideline for infec-
tion control in healthcare personnel,25 and the reviews by Weber et al180 and
Daneman et al.193

Candida and Nocardia Species

Several outbreaks of postoperative surgical site infections caused by Can-


dida species have been associated with personnel carriers. One outbreak of
Candida albicans sternal wound infections following cardiac surgery was
associated with a scrub nurse who had recurrent vaginal infections,198 and an
outbreak of Candida tropicalis sternal wound infections was also associated
with a scrub nurse.199 An outbreak of Candida osteomyelitis and diskitis after
spinal surgery was associated with a nurse who had artificial fingernails.200
A few clusters of surgical site infections caused by Nocardia farcinica have
been reported.201,202 In one, the source was not determined,202 and in the other
the source was determined to be a colonized anesthesiologist.201

Gram-Negative Organisms

Outbreaks caused by gram-negative organisms such as Pseudomonas and


Serratia are frequently associated with contaminated environmental reser-
voirs such as equipment, lotions, and solutions89; however, they can also be
associated with onychomycosis, artificial nails, transient carriage on the
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Outbreaks Associated with Human Carriers or Disseminators 91

hands of personnel, or by personnel who become colonized carriers.203–205 An


outbreak of Serratia marcescens infection and colonization in a neurosurgical
ICU was associated with a healthcare worker who had psoriasis and whose
hands were repeatedly colonized with Serratia marcescens over a prolonged
period.204 An outbreak of P. aeruginosa pneumonia and bloodstream infections
in a neonatal intensive care unit (NICU) was associated with a healthcare
worker who had otitis externa and ear cultures that grew the epidemic strain
of P. aeruginosa.206
Some studies have shown that overcrowding and staff shortages can con-
tribute to transient carriage on the hands of personnel and epidemic spread of
organisms.207 However, in many outbreaks, it is not possible to identify the
source or reservoir or mode of transmission of the causative agent.203,206,207

Hepatitis B Virus

Transmission of HBV in the healthcare setting has long been recognized


and has been associated with unsafe injection practices, contaminated equip-
ment and medications (especially in hemodialysis settings), and direct trans-
mission from an infected healthcare worker to a patient. Clusters of HBV
infection have been traced to transmission from infected obstetricians, gyne-
cologists, dentists, and surgeons to their patients during surgery.208–214 Of the
three most commonly recognized blood-borne pathogens—HBV, hepatitis C
virus (HCV), and human immunodeficiency virus (HIV)—HBV is the most
easily transmitted from person to person because an infected person can carry
more than a billion HBV particles per milliliter of blood.139 Risk factors associ-
ated with transmission of HBV from healthcare worker to patient include the
presence of hepatitis B e antigen in the healthcare worker’s blood, the type of
surgical procedure (such as vaginal hysterectomy and cardiac, orthopedic, and
major pelvic surgery), and the potential for injury of the healthcare worker
(such as a needlestick during suturing) during the invasive procedure.208,214
Twelve HBV-infected healthcare workers infected 38 patients from 1991 to
2005 in the United Kingdom and the Netherlands alone.214 It is likely that
many cases of HBV infection transmitted in healthcare settings are not recog-
nized owing to the long incubation period, the occurrence of asymptomatic
infection, and the lack of healthcare-associated HBV infection surveillance
systems.214,215
Recommendations for preventing transmission of hepatitis B from infected
healthcare providers to patients have been published by the CDC (currently
being revised),211 the SHEA,208 United States and European consensus pan-
els,216,217 public health agencies, hospital associations, and others.218,219 Each of
these published guidelines provides slightly different recommendations
regarding the management of HBV-infected healthcare workers who directly
perform invasive procedures. In the United States there is “no uniform
national policy for definitive guidance concerning whether and under what
conditions infected physicians can practice.”217(1165) However, ICPs and hospi-
tal leaders must ensure that their facility has adequate protocols in place to
prevent healthcare worker-to-patient transmission of HBV, HCV, and HIV.
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92 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Because HBV in human plasma can survive for at least 1 week in the envi-
ronment,220 inanimate objects contaminated with blood can serve as vehicles
for the transmission of the virus. When a cluster of healthcare-associated HBV
infections is detected, and appears to be unrelated to surgery, the mode of
transmission is most likely via exposure to a contaminated inanimate object
rather than contact with an infected healthcare worker. When investigating
an outbreak of HBV, investigators must review and observe infection control
practices involving the use of needles, syringes, and multidose vials because
the improper use of these items can result in the transmission of blood-borne
pathogens from patient to patient.221,222
Outbreaks of HBV and other bloodborne pathogens related to unsafe injec-
tion practices and lack of adherence to infection prevention protocols are dis-
cussed in Chapter 5. Recommendations for safe injection practices and
medication handling are also discussed in that chapter.

Hepatitis C Virus

There are several reports of clusters of HCV transmitted directly from a


healthcare worker to patients.214,223,224 In all of these cases, transmission was
associated with a surgical procedure. In a review of healthcare-associated
HCV infections, Perry et al. discussed 11 reports in which healthcare workers
transmitted their HCV infection to 38 patients.214
Guidelines for preventing transmission of HCV from infected healthcare
workers to patients have been published by the CDC,225 SHEA, 208 and oth-
ers.218,219 All of these guidelines emphasize the need for infected healthcare
workers to strictly follow routine infection prevention and control measures,
such as standard precautions, to prevent the transmission of blood-borne
pathogens. However, in the United States there is no uniform policy for the
management or restriction of HCV-infected workers who perform invasive
procedures.
HCV can also be transmitted from patient to patient via contaminated
equipment and medications, unsafe injection practices, and medical proce-
dures. Outbreaks of healthcare-associated HCV infection via unsafe injection
practices and hemodialysis are discussed in Chapter 5 along with measures to
prevent the transmission of HCV in the healthcare setting.

Human Immunodeficiency Virus

As of early 2008, worldwide, HIV transmission from an infected healthcare


worker to a patient has been reported in four instances:
1. From a dentist in the United States to a patient who had an invasive
dental procedure226,227
2. From an orthopedic surgeon in France to a patient who had a hip
replacement 228
3. From a nurse to a patient in France, with no evidence of blood exposure 229,230
4. From an obstetrician/gynecologist in Spain to a patient who had a
cesarean section231,232
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Outbreaks Associated with Human Carriers or Disseminators 93

Guidelines for preventing transmission of HIV from surgeon to patient have


been published by the CDC,211 SHEA,208 the UK Department of Health,233 and
others.217 Although there is no uniform national standard in the United
States, all published guidelines to date have promoted the use of standard pre-
cautions, including hand hygiene and protective barriers, to minimize the
exposure of patients to blood and blood-borne pathogens. They differ on the
restrictions recommended for HIV-infected healthcare workers who perform
invasive procedures.

Salmonella Species

Most reported hospital Salmonella outbreaks have been caused by improper


handling of contaminated foods234; however, several epidemics have been
traced to symptomatic dietary235 and nursing personnel236 and to infected
patients.237 In one outbreak, Salmonella poona was most likely introduced
into an NICU by an asymptomatic infant whose mother was infected with S.
poona.237 The organism was then transmitted to two other infants via cross-
infection by personnel. To prevent transmission of Salmonella in the health-
care setting, dietary and patient care personnel with acute gastrointestinal
illness should be restricted from caring for patients and handling patient care
items or food until symptoms subside.25 Some health departments have regu-
lations governing the restriction and culturing of healthcare workers and food
handlers who have Salmonella infection.
Food-borne outbreaks and control measures for preventing the spread of
agents such as Salmonella that cause gastrointestinal infections are discussed
in Chapter 7.

Hepatitis A Virus

Hepatitis A virus (HAV) is most commonly transmitted in the hospital set-


ting via the fecal-oral route by contact with feces or fecally contaminated
items.25 Transmission by ingestion of contaminated food or beverages is
known to occur in hospitals but is rarely reported in the literature.238,239
Transmission has also occurred by blood transfusion25,240–243 and by cross-
infection from a patient with asymptomatic or unrecognized HAV infec-
tion.244,245 There is no chronic carrier state for HAV as there is for HBV and
HCV. HAV is excreted in the stool, and transient viremia can occur.24 Persons
with HAV infection are most infectious during the prodromal stage, before the
onset of jaundice.24
Several outbreaks in nurseries were traced to neonates who received blood
transfusions from a donor with HAV infection.240–242 Once introduced into the
unit, HAV was transmitted by cross-infection to other infants and personnel
and to parents and relatives of the infected infants. Activities that have been
associated with nosocomial spread of HAV include eating and drinking in
patient care areas240,241,246,247 and failure to wash hands after caring for an
infected infant.246,247 In another outbreak, the source for nosocomial HAV was
an adult patient with symptomatic HAV infection who was hospitalized for an
unrelated reason, and HAV was transmitted to six healthcare workers and
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94 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

one patient.244 For more information on nosocomial HAV outbreaks the reader
is referred to the article by Chodick et al., who reviewed reports of outbreaks
in healthcare settings that were published between 1975 and 2003.243
Recommendations for preventing transmission of HAV include good hand
hygiene and use of standard precautions.26 Contact precautions should be
used for infants and children less than 3 years of age for the duration of hospi-
talization; for children 3–14 years of age for 2 weeks after onset of symptoms;
and for persons over 14 years of age for 1 week after onset of symptoms.26
The CDC Advisory Committee on Immunization Practices (ACIP) recom-
mends that hepatitis A vaccine, in preference to immune globulin, be adminis-
tered for postexposure prophylaxis to close contacts of index patients only if
an epidemiologic investigation indicates that nosocomial spread between
patients or between patients and staff in a hospital has occurred.248

OUTBREAKS SPREAD FROM PERSON TO PERSON BY AIRBORNE


AND DROPLET TRANSMISSION

Diseases Spread by Airborne Transmission

Outbreaks of nosocomial infections spread by the airborne route have long


been recognized in hospitals,249,250 although they are relatively uncommon
compared to outbreaks spread by contact. Only a few diseases have been docu-
mented to be spread from person to person via a true airborne route (i.e., by
airborne droplet nuclei, which are small particle residues of evaporated respi-
ratory secretions that can remain suspended in the air and can be dispersed
widely by air currents).26,249 Three diseases caused by pathogens that can be
truly airborne and have caused numerous epidemics in the healthcare setting
are tuberculosis, measles, and varicella (chickenpox). Because tuberculosis
outbreaks have been reported in a variety of healthcare settings, this disease
is discussed in detail in Chapter 7.

Measles
Measles is one of the most contagious diseases in humans. Transmission of
measles has occurred in hospitals, physicians’ offices, and emergency
rooms.250–254 Measles may be introduced into the healthcare setting by infected
patients or healthcare workers and is easily transmitted either via contact
with respiratory secretions of infected persons or via the airborne route.26
Infected healthcare workers can transmit the disease to patients, to other
healthcare workers, and to family members. Measles is readily spread because
the virus may remain airborne for prolonged periods and because infected per-
sons with measles may shed the virus in respiratory secretions during the pro-
dromal period before the disease is recognized.26 Transmission from patient to
patient has occurred in physicians’ offices even when direct contact did not
occur.255 Fifteen of the 75 measles outbreaks reported in the United States
during 1993–1996 involved transmission in a healthcare setting.254 During
1989–1991, a major resurgence of measles occurred in the United States; how-
ever, in 1996 only 508 cases were reported, of which 65 were classified as inter-
national importations.254
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Outbreaks Via Airborne and Droplet Transmission 95

Measles is rarely now seen in the United States owing to a highly immu-
nized population; however, measles is still endemic in many other countries.
Many physicians and healthcare providers have not seen a case of measles,
and therefore it sometimes may be difficult to obtain a prompt diagnosis when
a patient presents with a rash and a fever. Measles transmission in the United
States is usually associated with an imported case. In 2005, 66 confirmed
cases of measles were reported to the CDC, and 34 of these were from a single
outbreak in Indiana associated with an unvaccinated 17 year old who
returned home to the United States from Romania.256,257 In May 2008, the
CDC announced that a total of 64 confirmed measles cases had been prelimi-
narily reported to the CDC by April 25, the most reported by this date for any
year since 2001.258 This increased incidence of measles in the United States
was related to importation of measles by travelers, many of whom were
returning from Europe where several outbreaks were occurring.258 Of the 64
cases, 63 were unvaccinated or had unknown or undocumented vaccine status,
one was an unvaccinated healthcare worker who was infected in a hospital, 17
(39%) were infected while visiting a healthcare facility, and one was born
before 1957.
Recommendations for preventing transmission of measles have been pub-
lished by the CDC25,26,254,259 and the American Academy of Pediatrics260 and
include the following:
• Prompt recognition of persons with measles; measles should be suspected
in persons with a fever and rash, regardless of age
• Prompt isolation of persons with suspected or known measles; airborne
precautions should be implemented in a private room with negative air-
flow and nonrecirculating air26
• Protocols to ensure measles immunity in all healthcare workers; measles
vaccine should be provided to all healthcare workers who cannot show
proof of immunity, as follows:25,254,259
1. Healthcare workers born before 1957 are generally considered to be
immune to measles.
2. Healthcare workers born during or after 1957 are considered
immune if they have one of the following:
– Documentation of physician-diagnosed measles
– Documentation of two doses of live measles vaccine on or after
their first birthday
– Serologic evidence of measles immunity
Because some outbreaks have involved persons born before 1957, some
experts advocate requiring proof of immunity by vaccination or serology even
for those adults born before 1957.261
Transmission of measles can be prevented if recommendations for im-
munization of children, adolescents, and adults are followed. The ACIP
recommendations regarding immunization of healthcare workers259 and
immunization for measles, mumps, and rubella254 should be used when devel-
oping healthcare facility policies. In addition, some state and local health
departments require measles immunity for healthcare workers, and these
requirements must be incorporated into a facility’s policies.
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96 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Because measles is highly communicable, one case (even a community-


acquired case) should be considered a potential outbreak and should be
accorded immediate action to prevent further transmission. The suspected
case should promptly be reported by telephone to the local health department
so that measures to prevent further spread can be implemented as soon as
possible. Actions that should quickly be taken to interrupt measles transmis-
sion include the following:
• Identification and prompt isolation of persons with suspected or con-
firmed measles.26 Suspected cases should promptly be reported to the
health department; however, a diagnosis of measles should be verified
before exposure follow-up is conducted. Serologic testing is recommended
to confirm the diagnosis; however, if measles is clinically diagnosed, expo-
sure follow-up should begin before laboratory confirmation is received.
Information on the clinical and laboratory diagnosis of measles is pro-
vided in Appendix C.10
• Compilation of a list of all potentially exposed personnel, patients, and
visitors as soon as possible, especially if the suspected case is seen in the
emergency room.
• Identification of all exposed personnel, patients, and visitors. It is impor-
tant to define exposed person before conducting contact tracing. Exposure
may be defined as being in the same room (or area supplied by the same
air-handling system) at the same time as a patient with measles or for up
to 1 hour after the patient with measles left the room or area.
• Evaluation of immunity in all exposed personnel and patients: Guidelines
for evaluating immunity can be found above and in Appendix C.
• Restriction of susceptible exposed personnel from duty, from 5 days after
the first exposure to 21 days after the last exposure to measles, regardless
of postexposure vaccination.25,254
• Isolation of exposed susceptible patients, if they are still hospitalized,
using airborne precautions in a private room with negative airflow and
nonrecirculating air, from 5 days after the first exposure to 21 days after
the last exposure to measles.26
• Prompt provision of measles vaccine to susceptible persons to halt disease
transmission. Note: During an outbreak, serologic testing to identify sus-
ceptible persons is not necessary.25,254 The vaccine should be provided to
those born during or after 1957 who have no documentation of complete
measles vaccination or physician-documented diagnosis of measles and
should be considered for those born before 1957 if they do not have sero-
logic documentation of immunity or receipt of two doses of measles vac-
cine. Guidelines for providing the measles vaccine and immune globulin
can be found in the ACIP recommendations for measles, mumps, and
rubella immunization.254
Community outbreaks can result in transmission into a healthcare facil-
ity,262,263 and nosocomial transmission can spread into the community. Out-
breaks of measles in healthcare settings can be associated with significant
morbidity and disruption of services. They are disruptive and costly to control
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Outbreaks Via Airborne and Droplet Transmission 97

due to (1) the time needed to conduct a contact investigation, (2) the lost work-
days for restricted personnel who either acquire measles or who are exposed
and are not immune, and (3) the cost of the measles vaccine for exposed per-
sonnel, patients, and visitors.
One of the most important measures to prevent measles transmission is to
ensure that all persons who work in a healthcare setting have acceptable evi-
dence of measles immunity.254,263

Varicella (Chickenpox)
Varicella-zoster virus (VZV) causes varicella (chickenpox) and zoster (shin-
gles). Varicella is one of the most communicable diseases of humans and is
readily spread from person to person via direct contact with infected lesions,
droplet spread, or airborne transmission.26,264,265 Healthcare-associated out-
breaks of varicella in hospitals and physicians’ offices have been well docu-
mented.264–270 True airborne transmission has been documented in the
hospital setting when susceptible patients have developed varicella even
though they did not have face-to-face contact with the infected source
patient.266,268 Community outbreaks can result in healthcare-associated expo-
sures and transmission.267 VZV can easily be introduced into the healthcare
setting by infected patients, personnel, and visitors (including the children of
personnel) since infected persons may be contagious up to 2 days prior to the
development of symptoms.24,26
Guidelines for prevention and control of VZV infections in healthcare set-
tings have been published by the CDC,25,26,271 the American Academy of Pedi-
atrics,272 and others.264,273,274 These guidelines should be reviewed when
developing hospital policies.
Measures that should be implemented in healthcare settings to prevent
varicella transmission include the following:
• Implementation of protocols to ensure varicella immunity in personnel271
• Prompt recognition of infected patients, personnel, and visitors. Note: The
diagnosis of chickenpox should be verified by infection control and/or
employee health personnel before exposure follow-up and contact tracing
is conducted.
• Prompt and appropriate isolation of infected patients (airborne precau-
tions in a private room with negative airflow and nonrecirculating air)26
• Compilation of a list of all potentially exposed personnel, patients, and
visitors as soon as possible, especially if the suspected case is seen in the
emergency room
• Prompt identification of exposed persons. It is important to define exposed
person before conducting contact tracing. Weber et al. define exposure as
“being in an enclosed airspace with the source case (i.e., same room) or in
intimate contact with the source in an open area during a potentially con-
tagious stage of illness. Varicella is considered contagious beginning 48
hours prior to the onset of rash and until all lesions are dried and
crusted.”264(p699)
• Evaluation of immunity in all exposed personnel, patients, and visitors271
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98 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

• Restriction of susceptible exposed personnel from duty beginning on the


8th day after the first exposure through the 21st day after the last expo-
sure to chickenpox, or until all lesions are dried and crusted if varicella
occurs25,271
• Isolation of exposed susceptible patients, if they are still hospitalized,
during the period of potential infectiousness (airborne precautions in a
private room with negative airflow from 8 days after the first exposure
through 21 days after the last exposure)26
• Provision of the varicella vaccine to exposed personnel who are not
immune; however, the vaccine’s efficacy in preventing postexposure devel-
opment of varicella is unknown, and the vaccinated personnel should be
managed as if they were not immunized.271
Varicella exposure management, follow-up, and contact tracing can result in
considerable time expenditure by infection control and employee health staff,
and the exclusion of exposed susceptible personnel from duty can lead to sig-
nificant cost and disruption of services for a healthcare facility.267 Much of this
disruption can be prevented if persons with varicella are promptly identified
and appropriately isolated and if healthcare facilities ensure that all of their
personnel are immune to varicella.271

Diseases Spread by Droplet Transmission

Diseases that are spread from person to person via droplet transmission are
caused by pathogens that are expelled in large particle droplets of respiratory
secretions by a person who is coughing, talking, or sneezing or by droplets that
are produced during a procedure such as tracheal suctioning or bron-
choscopy.26 These droplets are not widely dispersed into the air and are gener-
ally said to travel several feet before settling to the ground. Diseases that have
caused outbreaks in healthcare settings and that can be spread via droplet
transmission include adenovirus infections,250,275–277 mumps,278,279 influenza,280
parvovirus B19 infection,281–283 rubella,284–286 Mycoplasma pneumoniae infec-
tion,287 respiratory syncytial virus (RSV) infections,288–300 and pertussis.301–303
Although the influenza virus has been transmitted in the acute care setting,
the majority of healthcare-associated outbreaks are reported in long-term care
settings, and influenza is therefore discussed in Chapter 4.

Respiratory Syncytial Virus Infection


RSV infection is most common in infants and children and, although it can
cause a severe pneumonia or bronchiolitis, it usually causes a mild disease.
Community outbreaks of RSV disease are seasonal, generally occurring
between December and March in North America. RSV can be introduced into
the hospital by infected patients, personnel, or visitors and can be easily
transmitted directly from person to person via large particle aerosols during
close contact with an infected person or indirectly via RSV-contaminated
hands or articles.27,288,289 The portal of entry for RSV is the conjunctiva or nasal
mucosa, and transmission frequently occurs when contaminated hands touch
the eyes or nose.27 Hand hygiene is the most important measure for prevent-
ing the transmission of RSV. Outbreaks of RSV infection have most commonly
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Outbreaks Via Airborne and Droplet Transmission 99

been reported in pediatric units,290 nurseries,291,292,300 and long-term care facil-


ities,293,294 and in immunocompromised adults in hematology/oncology and
bone marrow transplant units295,299 and ICUs.296 RSV infection may occur con-
currently with other respiratory tract infections, making outbreaks difficult to
recognize.297,299
Measures used to control RSV outbreaks have been published by the
CDC26,27 and include the following:
• Appropriate hand hygiene
• Adherence to contact isolation precautions, especially gloves and gowns
• Use of private rooms for infected patients; when a private room is not
available, an RSV-infected patient may be cohorted in a room with another
patient who has an active RSV infection but who has no other infection
• Work restrictions for personnel who have symptoms of acute upper respi-
ratory tract infection
• Restriction of visitors who have symptoms of upper respiratory tract
infection from visiting patients, especially pediatric, cardiac, and im-
munosuppressed patients

Pertussis
Pertussis, or whooping cough, is generally considered to be a childhood dis-
ease; however, approximately 29% of cases reported in 2004 occurred in adults
19 years of age or older and 34% in individuals between 11 and 18 years of
age.301 Disease in adults may be subclinical,302 mild, or atypical,303 and
although pertussis has been shown to be a common cause of prolonged cough
in adults, it is frequently not recognized as the etiology.304–307 Pertussis is eas-
ily spread from person to person by direct contact with the respiratory
droplets of infected persons. Multiple outbreaks of pertussis have been
reported in acute care facilities,304,308–317 and many have involved both patients
and staff.306–308,311,312,316 Outbreaks in the community may involve hospital per-
sonnel who then introduce pertussis into the hospital.306,307,318 Bordetella per-
tussis may also be introduced into the hospital by an infected patient, parent,
or visitor.310 There has been a resurgence of pertussis in many countries,
including the United States, since the 1990s,319–321 and outbreaks in hospitals
can readily occur when B. pertussis is circulating in the community.307,321
Unfortunately, pertussis can be difficult to diagnose, which makes early recog-
nition and implementation of preventive measures problematic.322
Guidelines for preventing the transmission of Bordetella pertussis and for
managing pertussis exposures have been published by the CDC25,26,323,324 and
others325,326 and include the following:
• Droplet precautions for infected patients: private room and use of masks
until 5 days after patient is started on effective therapy
• Droplet precautions for suspected cases until pertussis is ruled out
• Evaluation and appropriate therapy for exposed individuals who are
symptomatic, including personnel and household contacts
• Work restrictions for symptomatic personnel until 5 days of therapy are
completed
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100 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

• Postexposure prophylaxis for exposed individuals who are asymptomatic,


including personnel and household contacts
• Implementation of a program for routine provision of pertussis vaccine to
personnel to prevent infection and avoid outbreaks.26,324
The article by Haiduven et al. contains a pertussis workup checklist and
pertussis exposure forms that can be used for managing exposures in patients
and personnel.326
Outbreaks of pertussis occur regularly in healthcare facilities worldwide. In
addition to causing significant morbidity and disruption of services, they are
labor intensive and costly to control.315–317 The number and size of pertussis
outbreaks in hospitals can be reduced through routine immunization of
healthcare workers, timely recognition of cases, and implementation of appro-
priate infection prevention and control measures.

More on Diseases Spread by the Airborne and Droplet Routes

Appendix G contains Guidelines for the Prevention and Control of Upper


and Lower Acute Respiratory Illnesses (including Influenza and Pneumonia)
in Long-Term Care Facilities developed by the Maryland Department of
Health Mental Hygiene.
Exhibit 3–1 provides examples of diseases that have been responsible for
outbreaks in hospitals and are caused by organisms transmitted via the airborne
and droplet routes.26 Because a detailed description of each of these diseases is
beyond the scope of this chapter, for information on signs and symptoms, diag-
nosis, epidemiology, and infection prevention and control measures the reader
is referred to the Control of Communicable Diseases Manual by Heymann24
and the CDC guidelines for isolation precautions,26 prevention of healthcare-
associated pneumonia,27 and infection control in healthcare personnel.25

Exhibit 3–1 Airborne and Droplet-Spread Diseases Responsible for Outbreaks in


Healthcare Facilities

Airborne Droplet
Measles Adenovirus
Tuberculosis Group A streptococcus
Varicella Influenza
Mumps
Mycoplasma pneumoniae infection
Erythema infectiosum (parvovirus B-19)
Pertussis
Rubella
Respiratory syncytial virus infection
Severe acute respiratory syndrome
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Outbreaks of Diseases that Have Environmental Reservoirs 101

OUTBREAKS OF GASTROENTERITIS

Outbreaks of gastroenteritis are caused by infectious and noninfectious


agents and occur frequently in hospitals and long-term care settings. These
agents may be spread directly from person to person or indirectly via contami-
nated food, water, and environmental surfaces. Gastroenteritis outbreaks are
discussed in Chapter 7.

OUTBREAKS OF DISEASES THAT HAVE ENVIRONMENTAL


RESERVOIRS

Legionnaires’ disease (LD) and aspergillosis are two major nosocomial dis-
eases that have airborne and droplet modes of transmission but have environ-
mental, rather than human, reservoirs.

Legionnaires’ Disease

Epidemiology
Legionella species are gram-negative bacilli that are ubiquitous in nature
and live in aqueous habitats. They can be isolated from hot and cold tap water,
ponds, streams, and the surrounding soil. Nosocomial cases of LD were
reported shortly after the etiologic agent of LD was identified in 1977,327,328
and multiple healthcare-associated outbreaks and clusters have since been
reported.327,329–336 Healthcare-associated LD has generally been associated
with contamination of the water in cooling systems27,334,335 or the potable hot
water systems in hospitals,27,329–333,336 and these systems may remain colo-
nized for prolonged periods.333 In one hospital, persistent colonization of the
water supply was associated with contaminated shock absorbers installed
within the pipes to decrease noise.331
In 2005 and 2006, 11,980 cases of LD were reported by 35 countries in
Europe, and 629 of these were reported as nosocomial.336 Sixty-six of the
nosocomial cases were involved in 19 outbreaks in hospitals or healthcare
facilities. Fifteen of these outbreaks were “attributed to contaminated hot or
cold water systems, two to wet cooling systems, and two to an unknown
source.” 336
A 1994 community outbreak of Legionella pneumophila pneumonia in
Wilmington, Delaware, was associated with the cooling towers of a hospital.337
Although no hospitalized patients were affected, hospital staff and persons liv-
ing in the area surrounding the hospital developed LD.
Hospitals play an important role in the detection of outbreaks. Recognition
of a cluster of community-acquired cases of LD by the staff of a community
hospital led to the detection of an outbreak of LD among passengers of a cruise
ship.338 Because tests for Legionella species are not routinely performed, it is
likely that many cases, both community and healthcare associated, are not
recognized.
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102 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Mode of Transmission
The mode of transmission for Legionella pneumophila is via inhalation of
the organism in aerosolized water droplets that can be produced by cooling
towers, showers, room air humidifiers, and respiratory therapy nebulization
devices.27,335

Control Measures
To avoid transmission of Legionella in the hospital, sterile water (not tap or
distilled water) should be used to rinse and fill respiratory therapy equipment.
Recommendations for preventing nosocomial LD have been published by the
CDC27 and World Health Organization339 and include information on decontam-
inating potable water and cooling systems. Control measures used to interrupt
outbreaks in hospitals have included hyperchlorination and superheating of
the hot water system, use of sterile water in nebulizers, and use of biocides in
cooling towers.327–329,331
Criteria for defining healthcare-associated cases have been published by a
variety of organizations and public health agencies and differ slightly.27,336,339
The incubation period for LD is generally 2–10 days, and the CDC defines
healthcare-associated LD as follows:27(pg.27)
Definite: Laboratory-confirmed legionellosis that occurs in a patient
who has spent greater than or equal to 10 days continuously in a
healthcare facility prior to onset of illness
Possible: Laboratory-confirmed infection that occurs in a patient who
has spent 2–9 days in a healthcare facility before onset of illness
The CDC recommends initiating an investigation for the source of
Legionella spp. when healthcare-associated legionellosis is detected, as out-
lined in Exhibit 3–2.
An epidemiologic investigation of the source of Legionella spp. includes
“(1) retrospective review of microbiologic and medical records,( 2) active sur-
veillance to identify all recent or ongoing cases of legionellosis, (3) identifica-
tion of potential risk factors for infection (including environmental exposures,
such as showering or use of respiratory-therapy equipment) by line listing of
cases; analysis by time, place, and person; and comparison with appropriate
controls, (4) collection of water samples from environmental sources impli-
cated by the epidemiologic investigation and from other potential sources of
aerosolized water, and (5) subtype matching between Legionella spp. isolated
from patients and environmental samples.”27(p30)
Much information on Legionella and LD can be found at www.Legionella.org.

Aspergillosis

Epidemiology and Mode of Transmission


Aspergillus species are ubiquitous in nature and can easily be cultured from
the hospital environment.340 This fungus produces spores that are approxi-
mately 3 µm in size and that can remain suspended in air for prolonged peri-
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Outbreaks of Diseases that Have Environmental Reservoirs 103

Exhibit 3–2 Response to Identification of Laboratory-Confirmed


Healthcare-Associated Legionellosis

A. In facilities with hemopoietic stem-cell transplant (HSCT) or solid-organ transplant


recipients:
When one inpatient of an inpatient HSCT or solid-organ transplant unit develops a
case of laboratory-confirmed definite (i.e., after >10 days of continuous inpatient stay)
or possible (i.e., within 2–9 days of inpatient stay) healthcare-associated Legionnaires’
disease, or when two or more patients develop laboratory-confirmed Legionnaires’
disease within 6 months of each other and after having visited an outpatient transplant
unit during part of the 2–10 day period before illness onset:
In consultation with the facility’s infection control team, conduct a combined
epidemiologic and environmental investigation to determine the source(s) of
Legionella spp. Include but not limit the investigation to such potential sources as
showers, water faucets, cooling towers, hot-water tanks, and carpet-cleaner water
tanks.
B. In facilities that do not house severely immunocompromised patients (e.g., HSCT or
solid-organ transplant recipients):
When a single case of laboratory-confirmed definite healthcare-associated Legionnaires’
disease is identified, or when two or more cases of laboratory confirmed possible
healthcare-associated Legionnaires’ disease occur within 6 months of each other:
Conduct an epidemiologic investigation through a retrospective review of microbiologic,
serologic, and postmortem data to identify previous cases, and begin an intensive
prospective surveillance for additional cases of healthcare-associated Legionnaires’
disease.

Source: Adapted from Centers for Disease Control and Prevention. Guidelines for Preventing Health-
Care-Associated Pneumonia, 2003. Recommendations of CDC and the Healthcare Infection Control
Practices Advisory Committee. p. 71. http://www.cdc.gov/ncidod/dhqp/gl_hcpneumonia.html. Accessed
April 19, 2008.

ods.341 The usual portal of entry is via inhalation of aerosolized spores.27 How-
ever, primary cutaneous aspergillosis resulting from inoculation of spores onto
nonintact skin has been reported.37,55 Immunocompromised patients are at
greatest risk of developing invasive pulmonary infection, which can result in
significant morbidity and mortality.342
Multiple outbreaks of nosocomial aspergillosis have been reported in hospi-
tals.37,55,340,343–350 Most outbreaks have been associated with construction or
renovation in, or adjacent to, the hospital.37,340,344–346,348 In one outbreak, expo-
sure to a radiology suite that was undergoing extensive renovation was the
only common environmental factor found among six patients who developed
nosocomial aspergillosis during a 1-month period.348 Although most outbreaks
involve pulmonary aspergillosis in immunosuppressed patients,37,343–346 there
are several reports of outbreaks of primary cutaneous aspergillosis caused by
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104 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

contact with contaminated medical supplies, such as dressings37,55 and intra-


venous arm boards.347 In one report, an outbreak of cutaneous aspergillosis
was recognized when three cases of extensive wound aspergillosis occurred in
surgical and burn patients in a 3-week period. The source was traced to the
outer packaging of dressing supplies (dressing trays, gauze, bandages, and
tapes) that had become contaminated during renovation in the central inven-
tory control area of the hospital.37 An investigation of a cluster of cases of pul-
monary infections with Aspergillus fumigatus in a transplant unit found that
patient-to-patient transmission of A. fumigatus likely occurred from
aerosolization of conidiophores during surgical dressing changes and wound
debridement of a patient who had an extensive abdominal wound infected
with A. fumigatus.350 In addition to outbreaks of infection, pseudo-outbreaks
involving aspergillosis have been reported as a result of contamination of
microbiology cultures in the laboratory.351

Control Measures
Measures used to prevent transmission of fungal spores to patients include
implementation of protocols to prevent dispersal of construction-related dust
and bioaerosols,27,89,340,352 placement of high-risk patients (e.g., those with
severe and prolonged granulocytopenia) in a protected environment,26 routine
inspection and maintenance of air-handling systems in high-risk patient care
areas (such as operating rooms, nurseries, ICUs, bone marrow or solid organ
transplant units, and oncology units),27 and protection of sterile supplies from
contamination.
Guidelines and recommendations for controlling the airborne transmission
of Aspergillus in the hospital have been published by the CDC,27,89 Walsh and
Dixon,340 Carter and Barr,352 public health agencies, and others.353–355 Mea-
sures used to control transmission of Aspergillus spores during construction
and renovation projects include the following:
• Construction of impermeable barriers of plastic or drywall that extend
from the floor to the ceiling to control the dissemination of dust and dirt
and to separate the construction site from patient care areas, the phar-
macy, and areas where sterile supplies are stored
• Frequent cleaning and vacuuming of the work site and the areas adjacent
to the work site
• Restriction of pedestrian traffic through the work area to prevent the
tracking of dust and dirt through the facility
• Careful attention to traffic patterns of the construction crew, personnel,
patients, and visitors to avoid the spread of dirt and dust through the hos-
pital and to reduce the risk of patient exposure to infectious agents
• Evaluation of air patterns and air-handling systems in the work site and
the surrounding areas to ensure that dust and spores are not dissemi-
nated through the facility via air currents
• Ventilation of construction areas so they are at negative pressure to sur-
rounding critical areas such as patient care units and clean and sterile
supply rooms.
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Outbreaks and Pseudo-Outbreaks Associated with a Water Reservoir 105

OUTBREAKS AND PSEUDO-OUTBREAKS ASSOCIATED


WITH A WATER RESERVOIR

Many outbreaks and pseudo-outbreaks in inpatient and outpatient health-


care settings have been traced to a water reservoir,356–367 including potable or
drinking water, ice and ice machines, toilet water, and warm-water and sonicator
baths. Table 3–6 lists several examples. Whenever outbreaks or pseudo-
outbreaks are caused by nontuberculous mycobacteria or Legionella, Pseudo-
monas, Flavobacterium, or Acinetobacter species, an aqueous reservoir should
be suspected.
For additional information on waterborne infection risks for hospitalized
patients, the reader is referred to the review article by Emmerson.368

Potable Water
Nontuberculous mycobacteria are commonly found in municipal water sup-
plies and are frequent causes of pseudo-outbreaks. Sniadeck et al. described
an outbreak of Mycobacterium xenopi pseudo-infections that occurred in
13 patients over a 1-year period.363 Acid-fast bacilli smears were negative, and
only a few colonies of the organism were isolated from each of the specimens
(six sputa, two bronchial washings, four urines, and one stool). None of the
patients had disease that was compatible with M. xenopi infection. The source
of the organism was believed to be the hospital’s potable water system, which
contaminated the specimens at the time of collection. A review of specimen
collection and instrument disinfection procedures revealed the following:
1. Tap water was used to rinse a patient’s mouth just prior to collecting a
sputum specimen.
2. Tap water was used as a final rinse after cold sterilization of broncho-
scopes.
3. Urine for mycobacterial culture was occasionally collected in previously
used bedpans that had been rinsed with tap water.
4. Tap water was used for colonic irrigation.
This report highlights the need to instruct personnel to collect specimens for
culture carefully in order to minimize microbial contamination, and to avoid
using tap water as a final rinse when cleaning and disinfecting bronchoscopes.
Copepods and nonpathogenic freshwater microorganisms present in hospi-
tal drinking water have caused pseudo-outbreaks.364,365 Copepods are small
animals, such as Cyclops, that are the intermediate hosts of animal parasites
of humans (e.g., the guinea worm, Dracunculus medinensis, and the fish tape-
worm, Diphyllobothrium latum).

Ice
Contaminated ice machines and ice baths used to cool medical devices such
as syringes have been responsible for nosocomial outbreaks.356 An outbreak of
bacteremia caused by Flavobacterium species was traced to syringes that were
cooled in ice from the ice machine in an ICU before being used to collect arter-
ial specimens for blood gas determination.357 Guidelines for minimizing the
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106 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Table 3–6 Outbreaks and Pseudo-Outbreaks Associated with a Water Reservoir

Year Reported/
Outbreak Reservoir Source Reference No.
Flavobacterium Hospital potable Syringes cooled in ice from 1975 (357)
septicemia water ice machine in intensive
care unit
Pseudomonas Hospital potable Contaminated water bath 1981 (358)
septicemia water in the operating room used
to thaw fresh-frozen plasma
Pseudomonas Water in physical Contaminated Hubbard 1981 (359)
aeruginosa wound therapy tank; associated with
infections department discontinuation of using
bleach to disinfect tank
Mycobacterium Water supply in Hemodialyzers that were 1990 (360)
chelonae infections outpatient hemo- manually reprocessed
dialysis center using Renalin germicide
Pseudomonas Distilled water Distilled water used by 1991 (48)
pickettii bacteremia employee to replace Fen-
tanyl during narcotic theft
Gram-negative Hospital potable Pressure monitoring equip- 1996 (115)
bacteremia water ment left open and uncovered
overnight in the operating
room contaminated by house-
keeping personnel who
sprayed a water-disinfectant
mixture when cleaning
Legionellosis Hospital potable Contaminated ice machine 1997 (361)
(one case prompted water
an investigation)
Pseudo-outbreak Water in Fecal specimens for 1997 (362)
of Pseudomonas hospital toilet surveillance cultures were
aeruginosa collected from the toilet
Mycobacterium Hospital potable M. simiae was recovered 2004 (367)
simiae colonization water from hospital tap water,
and one possible patients’ home showers,
infection and well supplying the
hospital water

risk of transmission of infectious agents by ice and ice machines have been
published by the CDC89,369 and by Burnett et al.370

Water Baths
Warm-water baths have frequently served as the source of outbreaks.356
Organisms present in water baths used to thaw blood components and peri-
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Outbreaks of Nosocomial Pneumonia in Intensive Care Units 107

toneal dialysis solutions can easily contaminate the outer surfaces of these
items and can enter the container when it is opened or punctured. Items being
thawed in water baths should be placed in an impermeable plastic wrapper to
avoid contamination. Alternatively, peritoneal dialysis fluid can be warmed by
using a dry-heat source or a microwave oven.

OUTBREAKS OF NOSOCOMIAL PNEUMONIA IN


INTENSIVE CARE UNITS

Although most nosocomial pneumonias (NPs) arise from aspiration of


endogenous oropharyngeal or gastric flora, outbreaks of NP in ICUs have been
caused by exogenously acquired organisms.27,371 Outbreaks of NP can be
caused by a variety of bacteria, viruses, and fungi. Organisms causing NP can
be transmitted by person-to-person contact or by healthcare workers or other
patients through contact with contaminated respiratory therapy devices and
equipment.27,371–378 Examples of NP outbreaks in ICUs that were spread by
contact are shown in Table 3–7. Control measures used to interrupt transmis-
sion of the pathogens are also shown.
Most outbreaks of NP that are spread by cross-infection can be controlled by
implementation of routine infection prevention and control practices, such as
contact isolation precautions, appropriate use of gloves and hand hygiene, and
intensive surveillance.371 It is often difficult to recognize clusters and out-
breaks that are caused by common pathogens, such as S. aureus, because
these organisms may be causing endemic infections. However, outbreaks
caused by unusual gram-negative organisms, such as Burkholderia (formerly
Pseudomonas) cepacia and Stenotrophomonas (formerly Xanthomonas) mal-
tophilia, are more likely to be detected because these isolates are more likely
to be noticed.
Outbreaks associated with bronchoscopy and respiratory therapy solutions
and equipment, such as albuterol, mechanical ventilator circuits, and nebuliz-
ers, have been discussed previously in this chapter. Most of these outbreaks
can be prevented by routine use of aseptic technique when handling fluids and
by adherence to proper cleaning, disinfection, and sterilization protocols for
devices and equipment.
Outbreaks of Legionella and Aspergillus pneumonia associated with envi-
ronmental reservoirs have occurred in ICU patients.345,371,377–382 Control mea-
sures for these outbreaks depend on the specific reservoir and source of the
organism, as outlined in Table 3–8. Information on outbreaks caused by these
two pathogens was given in a previous section of this chapter.
For a comprehensive review of outbreaks of nosocomial pneumonia reported
in ICU patients, including a discussion of the steps used to investigate an out-
break of NP, the reader is referred to the article by Maloney and Jarvis.371 The
CDC Guidelines for Preventing Health Care-Associated Pneumonia provide
information on the etiology, epidemiology, pathogenesis, diagnosis, risk factors,
and control measures for preventing NP.27 They include guidelines for con-
ducting outbreak investigations for specific pathogens. Control measures rec-
ommended by the CDC include staff education on basic infection prevention
and control practices, infection surveillance, sterilization or disinfection and
Table 3–7 Reported Epidemics of Nosocomial Pneumonia (NP) in Intensive Care Unit Patients Spread by Contact Transmission, 1982–1993

Number
57793_CH03_ARIAS.qxd

Author of Patients
(Reference Study with NP/ Patients/ Respiratory Control
Pathogen No.) Year Population Colonization Risk Factors Personnel Equipment Measures*
1/19/09

Branhamella Patterson et al372 1988 Intermediate 8/2 Respiratory therapy x 1, 2, 5, 7


catarrhalis care unit Steroid use
Ward location
2:28 PM

Influenza A Centers for 1988 Med/Surg 3/NA* NA 5


virus Disease Control373 ICU**
Methicillin- Locksley et al.374 1982 Hospital-wide 15/1 Mechanical X 1, 3, 5, 7, 8
resistant ventilation ICU/
Page 108

Staphylococcus burn ward


aureus
Parainfluenza Singh-Naz et al.375 1990 Intermediate 6/1 NA X 1, 2, 3, 5
virus ICN**
Pseudomonas Weems113 1993 General ICU NA/120 Mechanical ventilation X 6
cepacia Respiratory therapy
Conly et al.116 1986 Medical ICU, 4/21 Mechanical ventilation
surgical ICU Antimicrobial therapy X X 3, 4, 6
297
Respiratory Valenti et al. 1982 NICU/SCN** 7/1 Endotracheal or X 1, 3
syncytial virus nasogastric intubation
and rhinovirus Mechanical ventilation
Xanthomonas Villarino et al.376 1992 CCU**, 42/0 Trauma ICU X X 1, 3, 4, 5, 6
maltophilia Trauma ICU, Mechanical ventilation
Med/Surg ICU Antimicrobial therapy

NOTE: *Control measures: 1 = isolation precautions; 2 = cohorting of infected patients; 3 = appropriate hand washing and glove use; 4 = staff education; 5 = prospective
surveillance; 6 = high-level disinfection and sterile water for respiratory equipment; 7 = appropriate antimicrobial therapy; 8 = treatment of carrier state.
**Med/Surg = medical and surgical; ICU = intensive care unit; NA = not available; ICN = intensive care nursery; NICU/SCN = neonatal intensive care and special care
nursery; CCU = critical care unit.
Source: Reprinted from Maloney SA, Jarvis WR. Epidemic nosocomial pneumonia in the intensive care unit. Chest. 1995; 16:213.
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Outbreaks of Sick Building Syndrome and Building-Related Illness 109

proper handling of medical equipment and devices, installation and mainte-


nance of special ventilation systems for patients at high risk for aspergillosis,
and isolation precautions for patients with known or suspected infection.27
For a discussion of outbreaks of pneumonia and other infections that have
been reported in neonatal intensive care units, the reader is referred to the
review by Gastmeier et al.385

OUTBREAKS OF SICK BUILDING SYNDROME AND


BUILDING-RELATED ILLNESS

Much has been published on “sick building syndrome” and indoor air pollu-
tion;386–392 however, little has been published regarding noninfectious episodes
of building-associated illnesses in healthcare facilities.388,389,393,394 In one
review of indoor air pollution, building-associated illnesses were linked to
inadequate ventilation in approximately half of the cases studied, and in
many cases no causal factor was found.387 Brandt-Rauf et al. described an out-
break of eye and respiratory tract irritation in operating room personnel.388
The outbreak was attributed to emergency generator diesel exhaust emissions
that entered the ventilation system for the operating room suite; however, per-
sonnel continued to complain of symptoms after this problem was rectified
and a definitive etiology for the ongoing symptoms was not identified.388 There
are also several reports of outbreaks of illness, including headache, nausea,
and vomiting, in hospital personnel that were traced to vapors of xylene that
had been disposed of down a drain.393,394
Hospital personnel in infection control, employee health, and safety man-
agement are frequently called upon to investigate clusters of complaints of
symptoms and illnesses by healthcare personnel, who often attribute the prob-
lems to exposure to some factor in the workplace. Infection prevention and
control personnel who are asked to investigate such incidents should follow
the epidemiologic principles used to investigate outbreaks of infection and
other conditions as outlined in Chapter 8. In many cases of building-related
complaints, it is difficult to determine if symptoms are truly a result of building-
related exposures. A review article on indoor air pollution by Gold provides
helpful information that can be used when evaluating building-related com-
plaints, and Gold suggests that the following questions be asked:389
1. Is the building tight?
2. Are there any significant levels of indoor air pollutants?
3. What is the overall prevalence of symptoms?
4. Are the symptoms clustered in any one work area?
When investigating building-related complaints, it is helpful to evaluate the
following:
1. The work exposure histories of the personnel involved, such as exposure
to chemicals, paint fumes, exhaust fumes from nearby vehicles, photo-
copying machines, volatile organic substances from new carpets, or mold
spores from wet carpets
2. The time of day that the symptoms occur(red)
Table 3–8 Outbreaks of NP Associated with Specific Environmental Reservoirs, 1978–1994

Number
57793_CH03_ARIAS.qxd

Author Study of Patients Control


Pathogen (Reference) Year Population with NP Risk Factors Reservoir Source Measures*
Legionella Fisher-Hoch 1981 General 11 Immunosuppression; Water supply Tap water; 1,3
species et al. (377) hospital Admission to new and cooling cooling tower
1/19/09

building system
Arnow et al. 1982 General 5 Immunosuppressive Water supply Respiratory 2,3
(378) hospital therapy; Jet nebulizer equipment
use
2:28 PM

Brady 1988 Pediatric 7 Immunosuppressive Water supply Showers 2,4, and


- (379) hospital therapy; chronic lung/ Respiratory appropriate
kidney disease equipment antimicrobial
therapy
Mastro et al. 1991 General 13 Chronic lung disease; Water supply Respiratory 1,2
Page 110

(380) hospital Jet nebulizer use; equipment


>3 days in ICU
Blatt et al. 1993 Military 14 Immunosuppressive Water supply Tap water 2.3
(381) hospital therapy; nasogastric
tube use; antimicrobial
therapy; bed bathing
Aspergillus Arnow et al. 1978 Renal unit 2 Immunosuppressive Construction Surface dust 7.,8
species (345) transplantation therapy; proximity to
construction
Weems et al. 1987 Pediatric 5 Hematologic malig- Construction NA 7,8
(382) hospital nancy; construction
activity
Arnow et al. 1991 General 29 Malignancy; hematology/ Ventilation Ventilator 5,6
(383) hospital oncology ward system filters
Surface dust
Buffington 1994 Pediatric 7 Hematologic malig- Construction NA 5,7,8
et al. (384) hospital nancy; construction
activity

NOTE: *Control measures: 1 = hyperchlorination and superheating of hospital water supply; 2 = sterile water for rinsing and use in respiratory equipment; 3 = prospective surveillance;
4 = staff education and shower prohibition; 5 = aggressive hospital cleaning and inspection; 6 = retrofitting of ventilation system; 7 = impermeable barriers around construction site; 8 =
relocation of immunocompromised patients.
NA = not available
Source: Reprinted from Maloney SA, Jarvis WR. Epidemic nosocomial pneumonia in the intensive care unit. Chest. 1995;16:216.
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Newly Recognized Agents and Sources for Outbreaks 111

3. The time of day that exposure(s) to possible pollutants occur(red)


4. The temporal relationship between time of exposure and onset of symptoms
5. The relationship of symptoms at and away from work; for instance, do
symptoms subside on weekends or when employees are away from the
workplace?
6. Physical factors, such as poor lighting
7. Psychological factors, such as job dissatisfaction, especially if no other
causative factors can be found.
It is important that employers listen to, and address, the concerns of person-
nel and demonstrate a genuine effort to identify the cause and implement cor-
rective measures. Such support will encourage employee productivity and
workplace satisfaction and will reduce the risk of legal or regulatory actions
taken by personnel against the employer.
The American College of Occupational and Environmental Medicine published
an evidenced-based statement on the adverse human health effects associated
with molds in the indoor environment; this is available from the Journal of
Occupational and Environmental Medicine.393

NEWLY RECOGNIZED AGENTS AND SOURCES FOR


HEALTHCARE-ASSOCIATED OUTBREAKS

Candida Species

Epidemiology
The Candida species emerged in the 1980s as an important cause of nosoco-
mial infection in severely ill and immunocompromised patients.396–400 The
most commonly reported Candida species causing infection in humans are C.
albicans, C. tropicalis, C. (Torulopsis) glabrata, C. parapsilosis, C. krusei, and
C. lusitaniae.396,397 Risk factors for nosocomial candidiasis include intravenous
therapy (especially TPN), exposure to antibiotics, and neutropenia.396,398,399
Although most Candida infections arise from a patient’s endogenous flora,
nosocomial transmission via contaminated intravenous fluids and medical
devices and the hands of personnel has been documented.198–200,396,398–404
Although many reported clusters and outbreaks of Candida species have no
identified source,402 outbreaks have been associated with TPN,405,406 intravenous
blood pressure-monitoring devices,407 and personnel carriers.198–200,402,404 Can-
dida species are important pathogens in NICUs. Studies demonstrate that
Candida can be acquired by the neonate either vertically from the mother or
horizontally (nosocomial) in an NICU401–403,405 and that a mother can carry dif-
ferent strains of Candida albicans at different body sites.403 Studies show that
TPN fluids can promote growth of Candida species and may serve as a reser-
voir for infection.405 In one NICU, an outbreak of Candida bloodstream infec-
tions caused by C. albicans, C. parapsilosis, and C. tropicalis was associated
with a contaminated retrograde medication administration system used for
TPN.405
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112 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Control Measures
Further epidemiologic studies are needed to identify and investigate com-
mon source outbreaks, nosocomial clusters, and instances of person-to-person
transmission of Candida species so that the reservoirs and the modes of trans-
mission for exogenously acquired candidiasis can be clarified.403–408 Since little
is known about the epidemiology of nosocomial Candida infections acquired
from exogenous sources, it is difficult to identify control measures that can be
used to interrupt transmission. Based on a review of the reports noted in this
section, the following measures can be recommended to prevent the nosoco-
mial spread of Candida species, to interrupt an outbreak, and to identify a
possible cause of an outbreak:

• Since several investigators have associated outbreaks with transmission


by personnel,198–200 and since hand carriage of Candida species by health-
care workers has been documented,404,409 careful hand hygiene should be
practiced before and after patient care, especially when caring for
neonates, severely ill patients, and immunocompromised patients, and
before handling intravenous solutions and related equipment. If an out-
break is suspected, personnel should be reminded of the importance of
proper hand hygiene.
• Since Candida outbreaks have been associated with TPN 405,406 and intra-
venous blood pressure-monitoring devices,407 personnel preparing and
administering intravenous solutions, especially TPN, should be taught
proper aseptic technique. If an outbreak is suspected, personnel practices
should be observed to ensure that aseptic technique is being used.
• If a cluster or suspected increase in Candida infections occurs, an epi-
demiologic investigation should be conducted to verify the existence of an
outbreak and to identify potential sources and modes of transmission as
discussed in Chapter 8. If an outbreak is suspected, the laboratory should
be requested to save isolates from patients for possible typing.
• If an epidemiologic investigation suggests an outbreak, control measures
should be implemented based on the potential sources and possible modes
of transmission identified.
• If initial control measures do not prevent transmission, culture surveys of
patients, personnel, or an implicated source may be considered, based on
the findings of the epidemiologic investigation; however, cultures should
not be done unless the laboratory is involved in planning the specimen
collection process and unless molecular typing will be done to determine
the relatedness of any strains of Candida that are isolated.
• Because of the risk of contamination of retrograde medication adminis-
tration systems, facilities using these systems need to evaluate carefully
the practices used to maintain them.405
• Because clusters of Candida infections may be caused by more than one
strain of Candida, laboratory typing methods must be chosen and inter-
preted carefully in conjunction with observational epidemiologic data.410
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Newly Recognized Agents and Sources for Outbreaks 113

Identifying New Risk Factors and Sources for Infection

Emerging infectious diseases are considered to be those in which the inci-


dence in humans increased since the 1970s or threatens to increase in the near
future.411,412 It is sobering to note that many of the diseases discussed in this
text are considered emerging, or reemerging, infectious diseases, such as LD,
candidiasis, cryptosporidiosis, acquired immune deficiency syndrome, HBV
and HCV, and infections caused by MRSA, VRE, MDR-TB, Clostridium diffi-
cile, human parvovirus B19, norovirus, rotavirus, and Pneumocystis carinii.
Two additional organisms that recently have been identified as causative
agents in nosocomial outbreaks are Escherichia coli O157:H7 and Helicobacter
pylori.413 Weber and Rutala noted that “The reasons for the emergence of new
nosocomial pathogens include enhanced survival of immunocompromised
hosts, acquisition and spread of adaptive genes (i.e., antibiotic resistance and
virulence genes), enhanced ability to survive in new ecologic niches, increasing
use of invasive procedures, unrecognized virulence, prior underidentification
due to difficulties inculturing, and increased recognition due to taxonomic
clarification.”413(p306)
In 1998 the CDC published Preventing Emerging Infectious Diseases: A
Strategy for the 21st Century, a plan to combat infectious diseases.412 One of
the objectives of this plan is to “identify the behaviors, environments, and host
factors that put people at increased risk for infectious diseases and their
sequelae.”412(p29) Table 3–9 shows examples of new risk factors and sources for
infections that were identified by CDC investigators from 1994 to 1998.414–417
Four of the five examples given involve outbreaks of infections acquired as a
result of healthcare activities in acute and home care settings. Exhibit 3–3
demonstrates an area for risk factor research that was identified by the CDC
investigators: the relationship between healthcare practices and bloodstream
infection rates in the acute and home care settings.415,418–421
Additional new and reemerging risks and organisms responsible for healthcare-
associated outbreaks and pseudo-outbreaks in the early 2000s include the
following:
• Biofilm formation on medical devices such as gastrointestinal endoscopes,
bronchoscopes, and respiratory therapy devices that can inhibit the abil-
ity of disinfectants to destroy microorganisms, make these devices diffi-
cult to clean and disinfect, and result in the growth of organisms that can
be transferred to patients73,422,423
• The use of probiotics (biotherapeutic agents) and the demonstration that
organisms such as Saccharomyces cerevisiae that are used in probiotics
can be transmitted to untreated patients in the same unit as a patient
that is treated with a biotherapeutic preparation424
• Pantoea agglomerans (formerly Erwniia herbicola then Enterobacter
agglomerans)425–428
• A large multistate outbreak of mumps in the United States in 2006 that
resulted in infections in healthcare workers429
• The role of the environment and environmental surfaces in the transmis-
sion of pathogens in outbreaks89,430,431
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114 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

Table 3–9 Examples of New Risk Factors and Sources for Infection Identified by
CDC Investigations, 1994–1998

Outbreak investigations provide some of the most important opportunities for identifying
risk factors for disease. The investigations described below were conducted in
collaboration with many partners in state and local health departments, other federal
agencies, and other organizations.

Year Location Problem Finding Implications


1994 United States Hepatitis C414 Strong association Led to requirements for
with particular lots viral inactivation steps
of intravenous (IV) and new testing proce-
immunoglobulin dures to ensure safety
from one company of IV and intramuscular
immunoglobulin products
1994 Rhode Island Bloodstream BSIs associated with First outbreak to link
infections use of inoculation these devices with
(BSIs)415 devices. Findings led adverse outcomes in
to CDC recommenda- patients
tions on the use and
management of
needleless devices.
1995 Democratic Ebola Transmission linked No evidence of airborne
Republic of infection416 to direct contact with transmission. Led to
Congo ill patients updating of policies for
managing patients with
viral hemorrhagic fever
in the United States.
1996 Indiana Vancomycin- Illness linked to prior Highlighted rapid spread
resistant use of antibiotics. of this strain in the
Enterococci417 Implementation of United States. Also
control measures showed feasibility and
reduced transmission effectiveness of control
measures to reduce the
spread of antibiotic-
resistant organisms in
hospitals.
1997 New York HIV Cluster of cases of HIV detection and
–1998 HIV infection in women prevention programs
who had sex with one need to be strengthened
HIV-positive man in rural communities.

Source: Reprinted from Centers for Disease Control and Prevention. Preventing Emerging Infectious
Diseases: A Strategy for the 21st Century. U.S. Department of Health and Human Services; 1998:30.
http://www.cdc.gov/mmwr/preview/mmwrhtml/00031393.htm.
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Summary 115

Exhibit 3–3 Bloodstream Infections in ICU and Home Healthcare Patients

Since 1993, CDC has investigated three outbreaks of bloodstream infection (BSI)417,418
among patients in intensive care units (ICUs) that were associated with decreases in
nurse-to-patient ratios. In each of these outbreaks, rates of BSI increased when the number
of healthcare workers per patient decreased or when the level of training of those workers
decreased. The epidemiologic relationship between nursing staff numbers and training
levels and the rates of BSIs remained significant even after controlling for other factors.
Since that time, CDC has also investigated three outbreaks of BSIs among patients
receiving home infusion therapy.415,420,421 Risk factors for these outbreaks include practices
related to care of the intravenous line, the use of particular types of intravenous devices,
and socioeconomic factors. Interventions that involve teaching and training home
healthcare providers and families of home care patients are being evaluated.

Source: Reprinted from Centers for Disease Control and Prevention. Preventing Emerging Infectious
Diseases: A Strategy for the 21st Century. U.S. Department of Health and Human Services; 1988:31.
http://www.cdc.gov/mmwr/preview/mmwrhtml/00031393.htm.

THE IMPORTANCE OF PERSONNEL AND EMPLOYEE HEALTH

Because healthcare workers (including employees, physicians, volunteers,


and students) play an important role in initiating and propagating outbreaks
in healthcare settings, each facility should have policies and procedures that
address personnel health and include hand hygiene and personal hygiene,
standard precautions, immunization, and work restrictions for certain infec-
tious diseases. Because many outbreaks involve vaccine-preventable diseases,
ICPs should ensure that the latest recommendations for healthcare worker
immunization are implemented in their facility and that efforts are made to
increase immunization rates in healthcare personnel.254,259,271,315,316,324,432–434
Because immunization recommendations are frequently revised, those who
are developing personnel policies should identify the latest public health rec-
ommendations on preventing diseases such as pertussis, influenza, varicella,
hepatitis B, measles, mumps and rubella, and refer to the Healthcare Infection
Control Practice Advisory Committee (HICPAC) guideline for infection control
in healthcare personnel.25 Appendix D contains a list of the immunizations
recommended for healthcare personnel and provides the MMWR issue and an
Internet address for the ACIP guidelines for each of the vaccines. The HICPAC
summary of recommended work restrictions for personnel can be found in
Appendix E.

SUMMARY

Outbreaks in acute care and other healthcare settings are caused by a variety
of infectious and noninfectious agents. New, emerging and well-known path-
ogens will continue to evolve and present a challenge to ICPs, clinicians, and
healthcare providers. Infection surveillance, prevention, and control programs
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116 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

in hospitals play an integral role in identifying the occurrence of infectious dis-


eases and their risk factors, modes of transmission, and sources so that effec-
tive prevention and control measures can be identified and implemented.

REFERENCES

1. LaForce FM. The control of infections in hospitals: 1750 to 1950. In: Wenzel RP, ed. Preven-
tion and Control of Nosocomial Infections. Baltimore, MD: Williams & Wilkins; 1987:1–12.
2. Stamm WE, Weinstein RA, Dixon RE. Comparison of endemic and epidemic nosocomial infec-
tions. Am J Med. 1981;70:393–397.
3. Haley RW, Tenney JH, Lindsey JO, Garner JS, Bennett J. How frequent are outbreaks of
nosocomial infection in community hospitals? Infect Control. 1985;6:233–236.
4. Jarvis WR, and the Epidemiology Branch, Hospital Infections Program, Centers for Disease
Control. Nosocomial outbreaks: the Centers for Disease Control’s hospital infections program
experience; 1980–1990. Am J Med. 1991:91:3B–101S–3B–106S.
5. Beck-Sague C, Jarvis W, Martone WJ. Outbreak investigations. Infect Control Hosp Epi-
demiol. 1997;18:138–145.
6. Jackson M, Fierer J. Infections and infection risk in residents of long-term care facilities: a
review of the literature; 1970–1984. Am J Infect Control. 1985;13:63–77.
7. Nicolle LE, Garibaldi RA. Infection control in long-term-care facilities. Infect Control Hosp
Epidemiol. 1995;16:348–353.
8. Smith P, Rusnak PG. Infection prevention and control in the long-term-care facility. Am J
Infect Control. 1997;25:488–512.
9. Herwaldt LA, Smith SD, Carter CD. Infection control in the outpatient setting. Infect Control
Hosp Epidemiol. 1998;19:41–74.
10. Wenzel RP, Thompson RL, Landry SM, et al. Hospital-acquired infections in intensive care
unit patients: an overview with emphasis on epidemics. Infect Control. 1983;4:371–375.
11. Beck-Sague C, Dooley SW, Hutton MD, et al. Outbreak of multidrug-resistant Mycobacterium
tuberculosis infections in a hospital: transmission to patients with HIV infection and staff.
JAMA. 1992;268:1280–1286.
12. Boyle JF, Soumakis SA, Rendo A, et al. Epidemiologic analysis and genotypic characteriza-
tion of a nosocomial outbreak of vancomycin-resistant enterococci. J Clin Microbiol.
1993;31:1280–1285.
13. Edmond MB, Wenzel RP, Pasculle W. Vancomycin-resistant Staphylococcus aureus: perspec-
tives on measures needed for control. Ann Intern Med. 1996;124:329–334.
14. McFarland LV, Beneda HW, Clarridge JE, Raugi GJ. Implications of the changing face of
Clostridium difficile disease for health care practitioners. Am J Infect Control. 2007;35:
237–253.
15. Luna CM, Aruj PK. Nosocomial Acinetobacter pneumonia. Respirology. 2007;12(6):787–791.
16. Paauw A, Verhoef J, Fluit AC, et al. Failure to control an outbreak of qnrA1-positive multidrug-
resistant Enterobacter cloacae infection despite adequate implementation of recommended
infection control measures. J Clin Microbiol. 2007;45(5):1420–1425.
17. Wenger P, Tokars J, Brennan P, et al. An outbreak of Enterobacter hormaechi infection and
colonization in an intensive care nursery. Clin Infect Dis. 1997;24:1243–1244.
18. Lederberg J, Shope R, Oaks S, eds. Emerging Infections: Microbial Threats to Health in the
United States. Washington, DC: National Academy Press; 1992:36-41. http://www.nap.edu/
catalog.php?record_id=2008. Accessed April 21, 2008.
19. Centers for Disease Control and Prevention. Addressing Emerging Infectious Disease
Threats: A Prevention Strategy for the United States. US Dept of Health and Human Services;
1994. http://www.cdc.gov/mmwr/preview/mmwrhtml/00031393.htm. Accessed April 21, 2008.
20. Ostroff SM. Emerging infectious diseases in the institutional setting: another hot zone. Infect
Control Hosp Epidemiol. 1996;17:484–489.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 117

References 117

21. Merrell DS, Falkow S. Frontal and stealth attack strategies in microbial pathogenesis.
Nature. 2004;430:250–256.
22. Smolinski MS, Hamburg MA, Lederberg J., eds. Microbial Threats to Health: Emergence,
Detection, and Response. Executive Summary. Washington, DC: National Academies Press;
2003;1. http://www.nap.edu/catalog.php?record_id=10636. Accessed April 21, 2008.
23. Peiris JSM, Guan Y. Confronting SARS: a view from Hong Kong. Philos Trans R Soc Lond B
Biol Sci. 2004;29;359:1075–1079. http://www.pubmedcentral.nih.gov/articlerender.fcgi?
artid=1693390. Accessed April 21, 2008.
24. Heymann DL. Control of Communicable Diseases Manual. 18th ed. Washington, DC: APHA
Press; 2005.
25. Bolyard EA, Tablan OC, Williams WW, et al. Guideline for infection control in health care
personnel; 1998. Am J Infect Control. 1998;26:289–354. http://www.cdc.gov/ncidod/
dhqp/gl_hcpersonnel.html. Accessed April 19, 2008.
26. Siegel JD, Rhinehart E, Jackson M, Chiarello L, and the Healthcare Infection Control Prac-
tices Advisory Committee. Guideline for Isolation Precautions: Preventing Transmission of
Infectious Agents in Healthcare Settings. Atlanta, GA: CDC; June 2007. http://www.cdc.gov/
ncidod/dhqp/gl_isolation.html. Accessed November 25, 2007.
27. Centers for Disease Control and Prevention. Guidelines for Preventing Health-Care-Associated
Pneumonia. Recommendations of CDC and the Healthcare Infection Control Practices Advi-
sory Committee. http://www.cdc.gov/ncidod/dhqp/gl_hcpneumonia.html. Accessed April 19,
2008.
28. Maki DG, Rhame FS, Mackel DC, Bennett JV. Nationwide epidemic of septicemia caused by
contaminated intravenous products, I: epidemiologic and clinical features. Am J Med.
1976;60:471–485.
29. Centers for Disease Control and Prevention. Epidemiologic notes and reports: nosocomial
bacteremias associated with intravenous fluid therapy—USA. MMWR. 1996;46:1227–1233.
30. Goldmann DA, Dixon RE, Fulkerson CC, et al. The role of nationwide infection surveillance
in detecting epidemic bacteremia due to contaminated intravenous fluids. Am J Epidemiol.
1978;108:207–213.
31. Kaslow RA, Mackel DC, Mallison GF. Nosocomial pseudo-bacteremia: positive blood cultures
due to contaminated benzalkonium chloride antiseptic. JAMA. 1976;236:2407–2409.
32. Wysowski DK, Flynt JW Jr, Goldfield M, Altman R, Davis AT. Epidemic neonatal hyperbiliru-
binemia and use of a phenolic disinfectant detergent. Pediatr. 1978;61:165–167.
33. Berkelman RL, Lewin S, Allen JR, et al. Pseudobacteremia attributed to contamination of
povidone-iodine with Pseudomonas cepacia. Ann Intern Med. 1981;95:32–36.
34. Panlilio AL, Beck-Sague CM, Siegel JD, et al. Infections and pseudoinfections due to povidone-
iodine solution contaminated with Pseudomonas cepacia. Clin Infect Dis. 1992;14:1078–1083.
35. Sharbaugh RJ. Suspected outbreak of endotoxemia associated with computerized axial
tomography. Am J Infect Control. 1980;8:26–28.
36. Cleary TJ, MacIntyre DS, Castro M. Serratia marcescens bacteremias in an intensive care
unit. Am J Infect Control. 1981;9:107–111.
37. Bryce EA, Walker M, Scharf S, et al. An outbreak of cutaneous aspergillosis in a tertiary-care
hospital. Infect Control Hosp Epidemiol. 1996;17:170–172.
38. Parrott PL, Terry PM, Whitworth EN, et al. Pseudomonas aeruginosa peritonitis associated
with contaminated poloxamer-iodine solution. Lancet. 1982;2:683–685.
39. Martone WJ, Williams WW, Mortensen ML, et al. Illness with fatalities in premature infants:
association with intravenous vitamin E preparation, E-Ferol. Pediatr. 1986;78:591–600.
40. Safranek TJ, Jarvis WR, Carson LA, et al. Mycobacterium chelonae wound infections after
plastic surgery employing contaminated gentian violet skin-marking solution. N Engl J Med.
1987;317:197–201.
41. Nakashima AK, McCarthy MA, Martone WJ, Anderson RL. Epidemic septic arthritis caused
by Serratia marcescens and associated with a benzalkonium chloride antiseptic. J Clin
Microbiol. 1987;25:1014–1018.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 118

118 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

42. Centers for Disease Control and Prevention. Yersinia enterocolitica bacteremia and endo-
toxin shock associated with red blood cell transfusion-United States; 1987–1988. MMWR.
1988;37:577–578.
43. Centers for Disease Control and Prevention. Red blood cell transfusions contaminated with
Yersinia enterocolitica—United States; 1991–1996, and initiation of a national study to
detect bacteria-associated transfusion reactions. MMWR. 1997;46:553–556.
44. Chodick G, Ashkenazi S, Lerman Y. The risk of hepatitis A infection among healthcare work-
ers: a review of reported outbreaks and sero-epidemiologic studies. J Hosp Infect.
2006;62:414–420.
45. Centers for Disease Control and Prevention Postsurgical infections associated with an
extrinsically contaminated intravenous anesthetic agent—California, Illinois, Maine, and
Michigan; 1990. MMWR. 1990;39:426–427, 433.
46. Bennett SN, McNeil MM, Bland LA, et al. Postoperative infections traced to contamination of
an intravenous anesthetic, propofol. N Engl J Med. 1995;333:147–154.
47. Kuehnert MJ, Webb RM, Jochimsen EM, et al. Staphylococcus aureus bloodstream infections
among patients undergoing electroconvulsive therapy traced to breaks in infection control
and possible extrinsic contamination by propofol. Anesth Analg. 1997;85:420–425.
48. Maki DG, Klein BS, McCormick R, et al. Nosocomial Pseudomonas pickettii bacteremias
traced to narcotic tampering. JAMA. 1991;265:981–986.
49. Centers for Disease Control and Prevention. Outbreak of hepatitis C associated with intra-
venous immunoglobulin administration—United States; October 1993–June 1994. MMWR.
1994;43:505–509.
50. Hamill RJ, Houston ED, Georghiou PR, et al. An outbreak of Burkholderia cepacia respira-
tory tract colonization and infection associated with nebulized albuterol therapy. Ann Intern
Med. 1995;122:762–766.
51. Reboli AC, Koshinski R, Arias K, et al. An outbreak of Burkholderia cepacia lower respiratory
tract infection associated with contaminated albuterol nebulization solution. Infect Control
Hosp Epidemiol. 1996;17:741–743.
52. Trilla A, Codina C, Salles M, et al. A cluster of fever and hypotension on a surgical intensive
care unit related to the contamination of plasma expanders by cell wall products of Bacillus
stearothermophilus. Infect Control Hosp Epidemiol. 1995;16:335–339.
53. File TM, Tan JS, Thomson RB, et al. An outbreak of Pseudomonas aeruginosa ventilator-
associated respiratory infections due to contaminated food coloring dye—further evidence of
the significance of gastric colonization proceeding nosocomial pneumonia. Infect Control
Hosp Epidemiol. 1995;16:417–418.
54. Anglim AM, Collmer JE, Loving J, et al. An outbreak of needlestick injuries in hospital
employees due to needles piercing infectious waste containers. Infect Control Hosp Epi-
demiol. 1995;16:570–576.
55. Larkin JA, Greene JN, Sandin RL, Houston SH. Primary cutaneous aspergillosis: case report
and review of the literature. Infect Control Hosp Epidemiol. 1996;17:365–366.
56. Orth B, Frei R, Itin PH, et al. Outbreak of invasive mycoses caused by Paecilomyces lilacinus
from a contaminated skin lotion. Ann Intern Med. 1996;125:799–806.
57. Shay DK, Fann LM, Jarvis WR. Respiratory distress and sudden death associated with
receipt of a peripheral parenteral nutrition admixture. Infect Control Hosp Epidemiol.
1997;18:814–817.
58. Archibald LK, Shah B, Schulte M, et al. Serratia marcescens outbreak associated with extrin-
sic contamination of 1% chloroxylenol soap. Infect Control Hosp Epidemiol. 1997;18:704–709.
59. Chetoui H, Melin P, Struelens MJ, et al. Comparison of biotyping, ribotyping, and pulsed-field
gel electrophoresis for investigation of a common-source outbreak of Burkholderia pickettii
bacteremia. J Clin Microbiol. 1997;35:1398–1403.
60. Mangram AJ, Archibald LK, Hupert M, et al. Outbreak of sterile peritonitis among continu-
ous cycling peritoneal dialysis patients. Kidney Int. 1998;54:1367–1371. http://www.nature
.com/ki/journal/v54/n4/full/4490374a.html. Accessed April 14, 2008.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 119

References 119

61. Van Laer F, Raes D, Vandamme P, et al. An outbreak of Burkholderia cepacia with septicemia
on a cardiology ward. Infect Control Hosp Epidemiol. 1998;19:112–113.
62. Centers for Disease Control and Prevention. Nosocomial Ralstonia pickettii colonization
associated with intrinsically contaminated saline solution—Los Angeles, California, 1998.
MMWR. 1998;47:285–286.
63. Centers for Disease Control and Prevention. Endotoxin-like reactions associated with intra-
venous gentamicin—California, 1998. MMWR. 1998;47:877–880.
64. Centers for Disease Control and Prevention. Enterobacter cloacae bloodstream infections
associated with contaminated prefilled saline syringes—California, November 1998. MMWR.
1998;47:959–960.
65. Centers for Disease Control and Prevention. Nosocomial Burkholderia cepacia infection and
colonization associated with intrinsically contaminated mouthwash—Arizona, 1996–1998.
MMWR. 1998;47:926–928.
66. Sautter RL, Mattman LH, Legaspi, RC. Serratia marcescens meningitis associated with a
contaminated benzalkonium chloride solution. Infect Control. 1984;5:223–225.
67. Matrician L, Ange G, Burns S, et al. Outbreak of nosocomial Burkholderia cepacia infection
and colonization associated with intrinsically contaminated mouthwash. Infect Control Hosp
Epidemiol. 2000;21:739–741.
68. Centers for Disease Control and Prevention. Salmonella Oranienburg Infections Associated
with Fruit Salad Served in Health-Care Facilities—Northeastern United States and Canada,
2006. MMWR. 2007;56(39);1025–1028. http://www.cdc.gov/mmwR/preview/mmwrhtml/
mm5639a3.htm. Accessed April 22, 2008.
69. Sunenshine RH, Tan ET, Terashita DM, et al. A multistate outbreak of Serratia marcescens
bloodstream infection associated with contaminated intravenous magnesium sulfate from a
compounding pharmacy. Clin Infect Dis. 2007;45(5):527–533.
70. Buchholz U, Richards C, Murthy R, et al. Pyrogenic reactions associated with single daily
dosing of intravenous gentamicin. Infect Control Hosp Epidemiol. 2000;21:771–774.
71. Centers for Disease Control and Prevention. Pseudomonas bloodstream infections associated
with a heparin/saline flush—Missouri, New York, Texas, and Michigan; 2004–2005. MMWR.
2005;54:269–72. http://www.cdc.gov/mmwR/preview/mmwrhtml/mm5411a1.htm. Accessed
April 22, 2008.
72. Bowen AB, Braden CR. Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis.
2006 Aug;12(8):1185–1189. http://www.cdc.gov/ncidod/eid/vol12no08/05–1509.htm. Accessed
April 21, 2008.
73. Jhung MA, Sunenshine RH, Noble-Wang J, et al. A national outbreak of Ralstonia mannito-
lilytica associated with use of a contaminated oxygen-delivery device among pediatric
patients. Pediatr. 2007;119(6):1207–1209.
74. Souza Dias MB, Bernardes Habert A, Borrasca V, et al. Salvage of long-term central venous
catheters during an outbreak of Pseudomonas putida and Stenotrophomonas maltophilia
infections associated with contaminated heparin catheter-lock solution. Infect Control Hosp
Epidemiol. 2008;29:125–130.
75. Centers for Disease Control and Prevention. Exophiala infection from contaminated in-
jectable steroids prepared by a compounding pharmacy. MMWR. 2002; 51:1109–12.
http://www.cdc.gov/mmwR/preview/mmwrhtml/mm5149a1.htm. Accessed April 22, 2008.
76. Civens R, Vugia DJ, Alexander R, et al. Outbreak of Serratia marcescens infection following
injections of betamethasone compounded at a community pharmacy. Clin Infect Dis. 2005;
43:831–837.
77. Centers for Disease Control and Prevention. Acute allergic-type reactions among patients
undergoing hemodialysis-multiple states; 2007–2008. MMWR. 2008;57(05);124–125. http://
www.cdc.gov/mmwR/preview/mmwrhtml/mm5705a4.htm. Accessed April 22, 2008.
78. Molina-Cabrillana J, Bolanos-Rivero M, Alvarez-Leon EE, et al. Intrinsically contaminated
alcohol-free mouthwash implicated in a nosocomial outbreak of Burkholderia cepacia colo-
nization and infection. Infect Control Hosp Epidemiol. 2006;27:1181–1182.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 120

120 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

79. Ghazal SS, Al-Mudaimeehg K, Al Fakihi EM, Asery AT. Outbreak of Burkholderia cepacia
bacteremia in immunocompetent children caused by contaminated nebulized sulbutamol in
Saudi Arabia. Am J Infect Control. 2006;34:394–398.
80. Hutchinson J, Runge W, Mulvet M, et al. Burkholderia cepacia infections associated with
intrinsically contaminated ultrasound gel: the role of microbial degradation of parabens.
Infect Control Hosp Epidemiol. 2004;25(4):291–296.
81. Matsouka DM, Costa SF, Mangini C, et al. A nosocomial outbreak of Salmonella enteritidis
associated with lyophilized enteral nutrition. J Hosp Infect. 2004;58:122–127.
82. Adverse ocular reactions following transfusions—United States; 1997–1998. MMWR.
1998;47(03):49–50. http://www.cdc.gov/mmwR/preview/mmwrhtml/00051231.htm. Accessed
April 22, 2008.
83. Pegues DA. Improving and enforcing compounding pharmacy practices to protect patients.
Clin Infect Dis. 2006;43:838–840.
84. Weist K, Wendt C, Petersen LR, Versmold H, Ruden H. An outbreak of pyoderma among
neonates caused by ultrasound gel contaminated with methicillin-susceptible Staphylococcus
aureus. Infect Control Hosp Epidemiol. 2000;21:761–764.
85. Pan A, Dolcetti L, Barosi C, et al. An outbreak of Serratia marcescens bloodstream infections
associated with misuse of drug vials in a surgical ward. Infect Control Hosp Epidemiol.
2006;27:79–82.
86. Gaillot O, Maruejouls C, Abachin E, et al. Nosocomial outbreak of Klebsiella pneumoniae pro-
ducing SHV-5 extended-spectrum beta-lactamase, originating from a contaminated ultra-
sonography coupling gel. J Clin Microbiol. 1998;36:1357–1360.
87. Kimura AC, Calvet H, Higa JI, et al. Outbreak of Ralstonia pickettii bacteremia in a neonatal
intensive care unit. Pediatr Infect Dis J. 2005;24(12):1099–1103.
88. Mateos I, Valencia R, Torres MJ, Cantos A, Conde M, Aznar J. Nosocomial outbreak of
Pseudomonas aeruginosa endophthalmitis. Infect Control Hosp Epidemiol. 2006;27:1249–
1251.
89. Sehulster L, Chinn RY, Arduino MJ, et al. Guidelines for environmental infection control in
health-care facilities; 2003. Recommendations of CDC and the Healthcare Infection Control
Practices Advisory Committee (HICPAC). MMWR. 2003;52(RR-10):1–42. http://www.cdc.gov/
ncidod/dhqp/gl_environinfection.html. Accessed April 5, 2008.
90. Dixon RE, Kaslow RA, Mackel DC, Fulkerson CC, Mallinson GF. Aqueous quaternary ammo-
nium antiseptics and disinfectants: use and misuse. JAMA. 1976;236:2415–2417.
91. Donowitz LG. Benzalkonium chloride is still in use. Infect Control Hosp Epidemiol.
1991;12:186–187.
92. France DR. Survival of Candida albicans in hand creams. N Z J Med. 1968;67:552–554.
93. Morse LJ, Williams HL, Grann FP, et al. Septicemia due to Klebsiella pneumoniae originating
from a hand cream dispenser. N Engl J Med. 1967;277:472–473.
94. Morse LJ, Schonbeck LE. Hand lotions—a potential nosocomial hazard. N Engl J Med.
1968;278:376–378.
95. Anderson K. The contamination of hexachlorophene soap with Pseudomonas pyocyanea. Med
J Aust. 1962;2:463.
96. Alonso-Echanove J, Cairns L, Richards M, et al. Nationwide outbreak of red eye syndrome
associated with transfusion of leukoreduced red blood cell units. Infect Control Hosp Epi-
demiol. 2006;27:1146–1152.
97. Vonberg RP, Gastmeier P. Hospital-acquired infections related to contaminated substances.
J Hosp Infect. 2007;65:15–23.
98. Sprach DH, Silverstein FE, Stamm WE. Transmission of infection by gastrointestinal
endoscopy and bronchoscopy. Ann Intern Med. 1993;118:117–128.
99. Struelens MJ, Rost F, Deplano A, et al. Pseudomonas aeruginosa and Enterobacteriaceae bac-
teremia after biliary endoscopy: an outbreak investigation using DNA macrorestriction
analysis. Am J Med. 1993;95:489–498.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 121

References 121

100. Alvarado CJ, Stolz SM, Maki DG. Nosocomial infections from contaminated endoscopes: a
flawed automated endoscope washer: an investigation using molecular epidemiology. Am J
Med. 1991;91:272S–280S.
101. Fraser TG, Reiner S, Malczynski M, Yarnold PR, Warren J, Noskin G. Multidrug-resistant
Pseudomonas aeruginosa cholangitis after endoscopic retrograde cholangiopancreatography:
failure of routine endoscope cultures to prevent an outbreak. Infect Control Hosp Epidemiol
2004;25:856–859.
102. Schliessler KH, Rozendaal B, Taal C, Meawissen SGM. Outbreak of Salmonella agona after
upper intestinal fiberoptic endoscopy. Lancet. 1980;2:1246.
103. Birnie GG, Quigley EM, Clements GB, Follet EAC, Watkinson G. Endoscopic transmission of
hepatitis B virus. Gut. 1983;24:171–174.
104. Bronowicki JP, Venard V, Botte C, et al. Patient-to-patient transmission of hepatitis C virus
during colonoscopy. N Engl J Med. 1997;337:237–240.
105. Allen JI, O’Connor AM, Olson MM, et al. Pseudomonas infection of the biliary system result-
ing from use of a contaminated endoscope. Gastroenterol. 1987;92:759–763.
106. Nelson KE, Larson PA, Schraufnagel DE, Jackson J. Transmission of tuberculosis by flexible
fiberbronchoscopes. Am Rev Respir Dis. 1983;127:97–100.
107. Wheeler PW, Lancaster D, Kaiser AB. Bronchopulmonary cross-contamination and infection
related to mycobacterial contamination of suction valves of bronchoscopes. J Infect
Dis.1989;159:954–958.
108. Blanc DS, Parret T, Janin B, et al. Nosocomial infections and pseudoinfections from contami-
nated bronchoscopes: two-year follow-up using molecular markers. Infect Control Hosp Epi-
demiol. 1997;18:134–136.
109. Gubler JG, Salfinger M, von Graevenitz A. Pseudoepidemic of nontuberculous mycobacteria
due to a contaminated bronchoscope cleaning machine: report of an outbreak and review of
the literature. Chest. 1992;101:1245–1249.
110. Agerton T, Valway S, Gore B, et al. Transmission of a highly drug-resistant strain (Strain W1)
of Mycobacterium tuberculosis: community outbreak and nosocomial transmission via a con-
taminated bronchoscope. JAMA. 1997;278:1073–1077.
111. Cetre JC, Nicolle MC, Salord H. Outbreaks of contaminated broncho-alveolar lavage related
to intrinsically defective bronchoscopes. J Hosp Infect. 2005;61(1):39–45.
112. Srinivasin A, Wolfenden LL, Song X, et al. An outbreak of Pseudomonas aeruginosa infections
associated with flexible bronchoscopes. N Engl J Med. 2003;348:221–227.
113. Weems JJ. Nosocomial outbreak of Pseudomonas cepacia associated with contamination of
reusable electronic ventilator temperature probes. Infect Control Hosp Epidemiol.
1993;14:583–586.
114. Loukil C, Saizou C, Doit C, et al. Epidemiologic investigation of Burkholderia cepacia acqui-
sition in two pediatric intensive care units. Infect Control Hosp Epidemiol. 2003;24:
707–710.
115. Rudnick JR, Beck-Sague CM, Anderson RL, Schable B, Miller JM, Jarvis WR. Gram-negative
bacteremia in open-heart-surgery patients traced to probable tap-water contamination of
pressure-monitoring equipment. Infect Control Hosp Epidemiol. 1996;17:281–285.
116. Conly JM, Klass L, Larson L, et al. Pseudomonas cepacia colonization and infection in inten-
sive care units. Can Med Assoc J. 1986;134:363–366.
117. Beck-Sague CM, Jarvis WR. Epidemic bloodstream infections associated with pressure trans-
ducers: a persistent problem. Infect Control Hosp Epidemiol. 1989;10:54–59.
118. Centers for Disease Control and Prevention. Guidelines for the prevention of intravascular
catheter-related infections. MMWR. 2002;51(No. RR-10):1-36. http://www.cdc.gov/mmwr/PDF/
rr/rr5110.pdf.Accessed April 28, 2008.
119. Centers for Disease Control. Hepatitis B associated with jet gun injection—California.
MMWR. 1986;35:373–376.
120. Centers for Disease Control. Nosocomial transmission of hepatitis B virus associated with a
spring-loaded finger stick device—California. MMWR. 1990;39:610–613.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 122

122 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

121. Centers for Disease Control and Prevention. Nosocomial hepatitis B virus infection associ-
ated with reusable fingerstick blood sampling devices—Ohio and New York City; 1996.
MMWR. 1997;46:217–221.
122. Hamill RJ, Wright CE, Andres N, Koza MA. Urinary tract infection following instrumenta-
tion for urodynamic testing. Infect Control Hosp Epidemiol. 1989;10:26–32.
123. Climo MW, Pastor A, Wong ES. An outbreak of Pseudomonas aeruginosa related to contami-
nated urodynamic equipment. Infect Control Hosp Epidemiol. 1997;18:509–510.
124. Gillespie K, Arnold J, Noble-Wang B, et al. Outbreak of Pseudomonas aeruginosa infections
after transrectal ultrasound-guided prostate biopsy. Urology. 2007;69:912–914.
125. Yardy GW, Cox RA. An outbreak of Pseudomonas aeruginosa infection associated with con-
taminated urodynamic equipment. J Hosp Infect. 2001;47:60–63.
126. Livornese L, Dias S, Samel C, et al. Hospital-acquired infection with vancomycin-resistant
Enterococcus faecium transmitted by electronic thermometers. Ann Intern Med. 1992;
117:112–116.
127. Karanfil LV, Murphy M, Josephson A, et al. A cluster of vancomycin-resistant Enterococcus
faecium in an intensive care unit. Infect Control Hosp Epidemiol. 1992;13:195–200.
128. Arnow PM, Garcia-Houchins S, Neagle MB, Bova JL, Dillon JJ, Chou T. An outbreak of blood-
stream infections arising from hemodialysis equipment. J Infect Dis. 1998;178:783–791.
129. Maragakis LL, Bradley KL, Song X, et al. Increased catheter-related bloodstream infection
rates after the introduction of a new mechanical valve intravenous access port. Infect Control
Hosp Epidemiol. 2006;27:67–70.
130. Rupp ME, Sholtz LA, Jourdan DR, et al. Outbreak of bloodstream infection temporally asso-
ciated with the use of an intravascular needleless valve. Clin Infect Dis. 2007;44(11):
1408–1414.
131. Corne P, Godreuil S, Jean-Pierre H, et al. Unusual implication of biopsy forceps in outbreaks
of Pseudomonas aeruginosa infections and pseudo-infections related to bronchoscopy. J Hosp
Infect. 2005;61(1):20–26.
132. Van der Zweit WC, Parlevliet GA, Savelkoul PH, et al. Outbreak of Bacillus cereus infections
in a neonatal intensive care unit traced to balloons used in manual ventilation. J Clin Micro-
biol. 2000;38:4131–4136. http://www.pubmedcentral.nih.gov/picrender.fcgi?artid=87553&
blobtype=pdf. Accessed April 25, 2008.
133. Trick WE, Kioski CM, Howard KM, et al. Outbreak of Pseudomonas aeruginosa ventriculitis
among patients in a neurosurgical intensive care unit. Infect Control Hosp Epidemiol.
2000;21:204–208.
134. Durante L, Zulty JC, Israel E, et al. Investigation of an outbreak of bloody diarrhea: associa-
tion with endoscopic cleaning solution and demonstration of lesions in an animal model. Am
J Med. 1992;92:476–480.
135. Burtin P, Ruget O, Petit R, Boyer J. Gluteraldehyde-induced proctitis after anorectal ultra-
sound examination: a higher risk of incidence than expected? Gastrointest Endosc.
1993;39:859–860.
136. Beck-Sague CM, Jarvis WR, Bland LA, Arduino MJ, Aguero SM, Verosic G. Outbreak of
gram-negative bacteremia and pyrogenic reactions in a hemodialysis center. Am J Nephrol.
1990;10:397–403.
137. Welbel SF, Schoendorf K, Bland LA, et al. An outbreak of gram-negative bloodstream infec-
tions in chronic hemodialysis patients. Am J Nephrol. 1995;15:1–4.
138. Flaherty JP, Garcia-Houchins S, Chudy R, Arnow PM. An outbreak of gram-negative bac-
teremia traced to contaminated O-rings and reprocessed dialyzers. Ann Intern Med.
1993;119:1072–1078.
139. Centers for Disease Control and Prevention. Outbreaks of hepatitis B virus infection among
hemodialysis patients—California, Nebraska, and Texas; 1994. MMWR. 1996;45:285–289.
140. Band JD, Ward JI, Fraser DW. Peritonitis due to a Mycobacterium chelonei-like organism
with intermittent chronic peritoneal dialysis. J Infect Dis. 1982;145:9–17.
141. Berkelman RL, Godley J, Weber JA, et al. Pseudomonas cepacia peritonitis associated with
contamination of automatic peritoneal dialysis machines. Ann Intern Med. 1982;96:456–458.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 123

References 123

142. Kayabas U, Bayraktar M, Otlu B, et al. An outbreak of Pseudomonas aeruginosa because of


inadequate disinfection procedures in a urology unit: A pulsed-field gel electrophoresis-based
epidemiologic study. Am J Infect Control. 2008;36:33–38.
143. Pena C, Dominguez MA, Pujol M, Verdaguer R, Gudiol F, Ariza J. An outbreak of carbapenem-
resistant Pseudomonas aeruginosa in a urology ward. Clin Microbiol Infect. 2003;9:938–943.
144. Centers for Disease Control and Prevention. Transplantation-transmitted tuberculosis—
Oklahoma and Texas; 2007. MMWR. 2008;57:333–336.
145. Singh N, Paterson DL. Mycobacterium tuberculosis infection in solid-organ transplant recipi-
ents: impact and implications for management. Clin Infect Dis. 1998;27:1266–1277.
146. Young L, Sable A, Price CS. Epidemiologic, clinical, and economic evaluation of an outbreak
of clonal multidrug-resistant Acinetobacter baumannii infection in a surgical intensive care
unit. Infect Control Hosp Epidemiol. 2007;28:1247–1254.
147. Schabrun S, Chipchase L, Rickard H. Are therapeutic ultrasound units a potential vector for
nosocomial infection? Physiother Res Int. 2006;11(2):61–71.
148. Kronman MP, Baden HP, Jeffries HE, Heath J, Cohen GA, Zerr DM. An investigation of
Aspergillus cardiac surgical site infections in 3 pediatric patients. Am J Infect Control.
2007;35:332–327.
149. Berthelot P, Carricajo A, Aubert G, Akhavan H, Gazielly D, Lucht F. Outbreak of postopera-
tive shoulder arthritis due to propionibacterium acnes infection in nondebilitated patients.
Infect Control Hosp Epidemiol. 2006;27:987–990.
150. Weber DJ, Rutala WA. Lessons from outbreaks associated with bronchoscopy. Infect Control
Hosp Epidemiol. 2001;22:403–408.
151. Kaczmarek RG, Moore RM, McCrohan J, et al. Multi-state investigation of the actual disin-
fection/sterilization of endoscopes in health care facilities. Am J Med. 1992;92:257–261.
152. Gorse GJ, Messner RL. Infection control practices in gastrointestinal endoscopy in the
United States: a national survey. Infect Control Hosp Epidemiol. 1991;12:289–296.
153. Multidisciplinary guideline for reprocessing flexible gastrointestinal gastroscopes. Endoscopy.
2003;58:1–8. http://www.asge.org/WorkArea/showcontent.aspx?id=3376. Accessed April 28, 2008.
154. Honeybourne D, Newmann CS. An audit of bronchoscopy practice in the United Kingdom: a
survey of adherence to national guidelines. Thorax. 1997;52:709–713.
155. American Society for Gastroenterology. Infection control during gastrointestinal endoscopy.
Gastrointest Endosc. 1999;49:836–841.
156. Culver DA, Gordon SM, Mehta AC. Infection control in the bronchoscopy suite: a review of
outbreaks and guidelines for prevention. Am J Respir Crit Care Med. 2003;167:1050–1056.
http://ajrccm.atsjournals.org/cgi/reprint/167/8/1050. Accessed April 28, 2008.
157. Bassett DCJ, Stokes KJ, Thomas WRG. Wound infection with Pseudomonas multivorans. A
waterborne contaminant of disinfectant solutions. Lancet. 1970;1:1188–1191.
158. Everett ED, Pearson S, Rogers W. Rhizopus surgical wound infection associated with elasti-
cized adhesive tape dressing. Arch Surg. 1979;114:738–739.
159. Keys TF, Haldorson AM, Rhodes KH, Roberts GD, Fifer EZ. Nosocomial outbreak of Rhizopus
infections associated with Elastoplast wound dressings—Minnesota. MMWR. 1978;27:33–34.
160. Pearson RD, Valenti WM, Steigbigel RT. Clostridium perfringens wound infections associated
with elastic bandages. JAMA. 1980;244:1128–1130.
161. Mitchell RG, Hayward AC. Postoperative urinary tract infections caused by contaminated
irrigating fluid. Lancet. 1966;1:793–795.
162. Geiss HK, Schmitt J, Frank SC. Bleeding after cardiovascular surgery caused by detergent
residues in laparotomy sponges. Infect Control Hosp Epidemiol. 1997;18:579–581.
163. Courtright P, Lewallen S, Holland SP, Wendt TM. Corneal decompensation after cataract
surgery: an outbreak investigation in Asia. Ophthalmol. 1995;102:1461–1465.
164. Pegues CF. Outbreak investigations: red-eyed rabbits and community service. Infect Control
Hosp Epidemiol. 2006;27:1143–1145
165. Hugonnet S, Dosso A, Dharan S, et al. Outbreak of endophthalmitis after cataract surgery:
the importance of the quality of the surgical wound. Infect Control Hosp Epidemiol. 2006;
27:1246–1248.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 124

124 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

166. Mateos I, Valencia R, Torres MJ, Cantos A, Conde M, Aznar J. Nosocomial outbreak of
Pseudomonas aeruginosa endophthalmitis. Infect Control Hosp Epidemiol. 2006; 27:1249–1251.
167. Labarca JA, Trick WE, Peterson CL, et al. A multistate nosocomial outbreak of Ralstonia
pickettii colonization associated with an intrinsically contaminated respiratory care solution.
Clin Infect Dis. 1999;29:1281–1286.
168. Maroye P, Doermann HP, Rogues AM, Gachie JP, Megraud F. Investigation of an outbreak of
Ralstonia pickettii in a paediatric hospital by RAPD. J Hosp Infect. 2000;44:276–272.
169. Moreira BM, Leobons MBGP, Pellegrino FLPC, et al. Ralstonia pickettii and Burkholderia
cepacia complex bloodstream infections related to infusion of contaminated water for injec-
tion. J Hosp Infect. 2005;60:51–55.
170. Sheretz RJ, Bassetti S, Bassetti-Wyss B. “Cloud” Health-Care Workers. Emerg Infect Dis.
2001;7:241–244.
171. Vonberg R-P, Stamm-Balderjahn S, Hansen S, et al. How often do asymptomatic healthcare
workers cause methicillin-resistant Staphylococcus aureus outbreaks? A systematic evalua-
tion. Infect Control Hosp Epidemiol. 2006;27:1123–1127.
172. Wenzel RP. Healthcare workers and the incidence of nosocomial infection: can treatment of
one influence the other? a brief review. J Chemother. 1994;4:33–40.
173. Dineen P, Drudin L. Epidemics of postoperative wound infection associated with hair carri-
ers. Lancet. 1973;2:1157–1159.
174. Kreiswirth BN, Kravitz GR, Schlievert PM, Novick RP. Nosocomial transmission of a strain
of Staphylococcus aureus causing toxic shock syndrome. Ann Intern Med. 1986;105:704–707.
175. Faibis F, Laporte C, Fiacre A, et al. An outbreak of methicillin-resistant Staphylococcus
aureus surgical-site infections initiated by a healthcare worker with chronic sinusitis. Infect
Control Hosp Epidemiol. 2005;26:213–215.
176. Belani A, Sheretz RJ, Sullivan ML, Russell BA, Reumen PD. Outbreak of staphylococcal
infection in two nurseries traced to a single carrier. Infect Control. 1986;7:487–490.
177. Mean M, Mallaret MR, Andrini P, et al. A neonatal specialist with recurrent methicillin-
resistant Staphylococcus aureus (MRSA) carriage implicated in the transmission of MRSA to
newborns. Infect Control Hosp Epidemiol. 2007;28:625–628.
178. Sheretz RJ, Reagan DR, Hampton KD, et al. A cloud adult: the Staphylococcus aureus-virus
interaction revisited. Ann Intern Med. 1996;124:539–547.
179. Centers for Disease Control and Prevention. Surveillance for food-borne disease outbreaks—
United States,; 1998–2002. Surveillance Summaries; 2006. MMWR. 2006;55(SS-10):9.
180. Weber DJ, Rutala WA, Denny FW. Management of healthcare workers with pharyngitis or
suspected streptococcal infections. Infect Control Hosp Epidemiol. 1996;17:753–761.
181. Mastro TD, Farley TA, Elliot JA, et al. An outbreak of surgical wound infections due to group
A streptococcus carried on the scalp. N Engl J Med. 1990;32:968–972.
182. Stamm WE, Feeley JC, Facklam RR. Wound infections due to group A streptococcus traced to
a vaginal carrier. J Infect Dis. 1978;138:287–292.
183. Berkelman RL, Martin D, Graham DR, et al. Streptococcal wound infections caused by a
vaginal carrier. JAMA. 1982;247:2680–2682.
184. Schaffner W, Lefkowitz LB Jr, Goodman JS, Koenig MG. Hospital outbreak of infections with
group A streptococci traced to an asymptomatic anal carrier. N Engl J Med. 1969;280:1224–1225.
185. Viglionese A, Nottebart VF, Bodman HA, Platt R. Recurrent group A streptococcal carriage in
a health care worker associated with widely separated nosocomial outbreaks. Am J Med.
1991;91(suppl 3B):329S–333S.
186. Paul SM, Genese C, Spitalny K. Postoperative group A beta-hemolytic streptococcus outbreak
with the pathogen traced to a member of a healthcare worker’s household. Infect Control
Hosp Epidemiol. 1990;11:643–646.
187. Ridgway EJ, Allen KD. Clustering of group A streptococcal infections on a burns unit: impor-
tant lessons in outbreak management. J Hosp Infect. 1993;25:173–182.
188. Isenberg HD, Tucci V, Lipsitz P, Facklam RR. Clinical laboratory and epidemiological investi-
gations of a Streptococcus pyogenes cluster epidemic in a newborn nursery. J Clin Microbiol.
1984;19:366–370.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 125

References 125

189. Ramage L, Green K, Pyskir D, Simor AE. An outbreak of fatal infections due to group A strep-
tococcus on a medical ward. Infect Control Hosp Epidemiol. 1996;17:429–431.
190. Lannigan R, Hussain Z, Austin TW. Streptococcus pyogenes as a cause of nosocomial infection
in a critical care unit. Diagn Microbiol Infect Dis. 1985;3:337–341.
191. Schwartz B, Elliott JA, Butler JC, et al. Clusters of invasive group A streptococcal infections
in family, hospital, and nursing home settings. Clin Infect Dis. 1992;15:277–284.
192. Decker MD, Lavely GB, Hutcheson RH, Schaffner W. Foodborne streptococcal pharyngitis in
a hospital pediatrics clinic. JAMA. 1985;253:679–681.
193. Daneman N, Green KA, Low DE, et al., and the Ontario Group A Streptococcal Study Group.
Surveillance for hospital outbreaks of invasive group A streptococcal infections in Ontario,
Canada; 1992 to 2000. Ann Intern Med. 2007;147(4):234–241. http://www.annals.org/cgi/
reprint/147/4/234.pdf. Accessed April 22, 2008.
194. Felkenr M, Pascoe N, Shupe-Rickecker K, Goodman E. The wound care team: a new source of
group a streptococcal nosocomial transmission. Infect Control Hosp Epidemiol. 2005;
26(5):462–465.
196. Chandler RE, Lee LL, Townes JM, Taplitz RA. Transmission of Group A Streptococcus lim-
ited to healthcare workers with exposure in the operating room. Infect Control Hosp Epi-
demiol. 2006; 27:1159–1163.
196. Kakis A, Gibbs L, Eguia J, et al. An outbreak of group A streptococcal infection among health
care workers. Clin Infect Dis. 2002;35(11):1353–1359.
197. Prevention of Invasive Group A Streptococcal Infections Workshop Participants. Prevention
of invasive group A streptococcal disease among household contacts of case patients and
among postpartum and postsurgical patients: recommendations from the Centers for Disease
Control and Prevention. Clin Infect Dis. 2002;35:950–959.
198. Pertowski CA, Baron RC, Lasker BA, Werner SB, Jarvis WR. Nosocomial outbreak of Can-
dida albicans sternal wound infections following cardiac surgery traced to a scrub nurse. J
Infect Dis. 1995;172:817–822.
199. Isenberg HD, Tucci V, Cintron F, et al. Single source outbreak of Candida tropicalis compli-
cating coronary bypass surgery. J Clin Microbiol. 1989;27:2426–2428.
200. Parry MF, Grant B, Yukena M, et al. Candida osteomyelitis and diskitis after spinal surgery:
an outbreak that implicates artificial nail use. Clin Infect Dis. 2001; 32:352–357. http://
www.journals.uchicago.edu/doi/pdf/10.1086/318487. Accessed April 25, 2008.
201. Wegener PN, Brown JM, McNeil MM, Jarvis WR. Nocardia farcinica sternotomy site infec-
tions in patients following open heart surgery. J Infect Dis. 1998;178:1539–1543.
202. Exmelin L, Malbruny B, Vergnaud M, Provost F, Boiron P, Morel C. Molecular study of noso-
comial nocardiosis outbreak involving heart transplant recipients. J Clin Microbiol.
1996;34:1014–1016.
203. Maragakis LL, Winkler A, Tucker MG, et al. Outbreak of multidrug-resistant Serratia
marcescens infection in a neonatal intensive care unit. Infect Control Hosp Epidemiol.
2008;29:418–423.
204. de Vries JJC, Baas WH, vander Ploeg K, Heesink A, Degener JE, Arends JP. Outbreak of Ser-
ratia marcescens colonization and infection traced to a healthcare worker with long-term car-
riage on the hands. Infect Control Hosp Epidemiol. 2006; 27:1153–1158.
205. Zawacki A, O’Rourke E, Potter-Boyne G, et al. An outbreak of Pseudomonas aeruginosa pneu-
monia and bloodstream infection associated with intermittent otitis externa in a healthcare
worker. Infect Control Hosp Epidemiol. 2004;25:1083–1089.
206. Friedman ND, Kotsanas D, Brett J, Billah B, Korman TM. Investigation of an outbreak of
Serratia marcescens in a neonatal unit via a case control study and molecular typing. Am J
Infect Control. 2008;36:22–28.
207. Liu S-C, Leu H-S, Yen M-Y, Lee P-I, Chou M-C. Study of an outbreak of Enterobacter cloacae
sepsis in a neonatal intensive care unit: the application of epidemiologic chromosome profil-
ing by pulsed-field gel electrophoresis. Am J Infect Control. 2002;30:381–385.
208. AIDS/TB Committee of the Society for Healthcare Epidemiology of America. Management of
healthcare workers infected with hepatitis B virus, hepatitis C virus, human immunodefi-
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 126

126 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

ciency virus, or other bloodborne pathogens. Infect Control Hosp Epidemiol. 1997;18:349–
363.
209. Bell D, Shapiro CN, Chamberland ME, Ciesielski CA. Preventing bloodborne pathogen trans-
mission from healthcare workers to patients: the CDC perspective. Surg Clin North Am.
1995;75:1189–1203.
210. Prentice MB, Flower AJE, Morgan GM, et al. Infection with hepatitis B virus after open
heart surgery. BMJ. 1992;304:761–764.
211. Centers for Disease Control. Recommendations for preventing transmission of human
immunodeficiency virus and hepatitis B virus to patients during exposure-prone invasive
procedures. MMWR. 1991;40(RR-8):1–9. http://www.cdc.gov/mmwR/preview/mmwrhtml/
00014845.htm. Accessed April 30, 2008.
212. Spijkerman IJB, van Doorn L-J, Janssen MHW, et al. Transmission of hepatitis B virus from
a surgeon to his patients during high-risk and low risk surgical procedures during 4 years.
Infect Control Hosp Epidemiol. 2002;23:306–312.
213. Redd JT, Baumbach J, Kohn W, Nainan O, Khristova M, Williams I. Patient-to-patient trans-
mission of hepatitis B virus associated with oral surgery. J Infect Dis. 2007;195:1311–1314.
214. Perry JL, Pearson RD, Jagger J. Infected health care workers and patient safety: a double
standard. Am J Infect Control. 2006;34:313–319.
215. Allos BM, Schaffner W. Transmission of hepatitis B in the health care setting: the elephant in
the room…or the mouse? J Infect Dis. 2007;195:1245–1247.
216. Mele A, Ippolito G, Craxi A, et al. Risk management of HBsAG or anti-HCV positive health-
care workers in hospital. Dig Liver Dis. 2001;33:795–802.
217. Reitsma AM, Closen ML, Cunningham M, et al. Infected physicians and invasive procedures:
safe practice management. Clin Infect Dis. 2005;40:1665–1672. http://www.journals
.uchicago.edu/doi/pdf/10.1086/429821. Accessed April 30, 2008.
218. United Kingdom Department of Health. Guidance for health care workers: protection against
infection with blood-borne viruses. Recommendations of the Expert Advisory Group on AIDS
and the Advisory Group on Hepatitis. London, UK: Her Majesty’s Stationery Office, 1993.
http://www.dh.gov.uk/assetRoot/04/01/44/74/04014474.pdf. Accessed April 30, 2008.
219. Gunson RN, Shouval D, Roggendorf M, et al. Hepatitis B virus (HBV) and hepatitis C virus
(HCV) infections in health care workers (HCW): guidelines for prevention of transmission of
HBV and HCV from HCW to patients. J Clin Virol. 2003;27:213–230.
220. Bond WW, Favero MS, Petersen NJ, Gravelle CR, Ebert JW, Maynard JE. Survival of hepati-
tis B virus after drying and storage for one week. Lancet. 1981;27:550–551.
221. Oren I, Hershow RC, Ben-Porath E, et al. A common-source outbreak of fulminant hepatitis
B in a hospital. Ann Intern Med. 1989;110:691–698.
222. Centers for Disease Control and Prevention. Improper infection-control practices during
employee vaccination programs—District of Columbia and Pennsylvania, 1993. MMWR.
1993;42:969–971.
223. Esteban JI, Gomez J, Martell M, et al. Transmission of hepatitis C virus by a cardiac surgeon.
N Engl J Med. 1996;334:555–560.
224. Lot F, Delarocque-Astagneau E, Thiers V, et al. Hepatitis C virus transmission from a health-
care worker to a patient. Infect Control Hosp Epidemiol. 2007;28:227–229.
225. Centers for Disease Control and Prevention. Recommendations for prevention and control of
hepatitis C virus (HCV) infection and HCV-related chronic disease. MMWR. 1998;47(RR-
19):1–39.
226. Centers for Disease Control. Update: transmission of human immunodeficiency virus infec-
tion during an invasive dental procedure—Florida. MMWR. 1991;40:21–33.
227. Scully C, Greenspan JS. Human immunodeficiency virus (HIV) transmission in dentistry. J
Dent Res. 2006;85:794–800.
228. Lot F, Seguier JC, Fegueux S, et al. Probable transmission of HIV from an orthopedic surgeon
to a patient in France. Ann Intern Med. 1999;130:1–6.
229. Goujon CP, Schneider VM, Grofti J, et al. Phylogenetic analyses indicate an atypical nurse-to-
patient transmission of human immunodeficiency virus type 1. J Virol. 2000;74:2525–2532.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 127

References 127

230. Astagneau P, Lot F, Fegueux S, et al. Lookback investigation of patients potentially exposed
to HIV type I after a nurse-to-patient transmission. Am J Infect Control. 2002;30:242–245.
231. Bosch X. Second case of doctor-to-patient HIV transmission. Lancet Infect Dis. 2003;3:261.
232. Mallolas J, Arnedo M, Pumarola T. Transmission of HIV-1 from an obstetrician to a patient
during a caesarean section. AIDS. 2006;20:285–287.
233. UK Department of Health. HIV Infected Health Care Workers: A Consultation Paper on Man-
agement and Patient Notification. London, UK: Department of Health; 2002. http://www
.dh.gov.uk/assetRoot/04/01/85/96/04018596.pdf. Accessed April 30, 2008..
234. Centers for Disease Control. Foodborne nosocomial outbreak of Salmonella reading—Con-
necticut. MMWR. 1991;40:804–806.
235. Opal SM, Mayer KH, Roland F, Brondum J, Heelan J, Lyhte L. Investigation of a food-borne
outbreak of salmonellosis among hospital employees. Am J Infect Control. 1989;17:141–147.
236. Perlino CA, Parrish CM, Terry PM. Salmonella infantis outbreak in neonates in an interme-
diate intensive care nursery. Presented at: Third Decennial International Conference on
Nosocomial Infections; July 31–August 3, 1990; Atlanta, GA. Abstract 62.
237. Stone A, Shaffner M, Sautter R. Salmonella poona infection and surveillance in a neonatal
nursery. Am J Infect Control. 1993;21:270–273.
238. Meyers JD, Romm FJ, Tihen WS, Bryan JA. Food-borne hepatitis A in a general hospital: epi-
demiologic study of an outbreak attributed to sandwiches. JAMA. 1975;231:1049–1053.
239. Eisenstein AB, Aach RD, Jacobsohn W, Goldman A. An epidemic of infectious hepatitis in a gen-
eral hospital: probable transmission by contaminated orange juice. JAMA. 1963;185:171–174.
240. Rosenblum LS, Villarino ME, Naina OV, et al. Hepatitis A outbreak in a neonatal intensive
care unit: risk factors for transmission and evidence of prolonged viral excretion among
preterm infants. J Infect Dis. 1991;164:476–482.
241. Azimi PH, Roberto RR, Guralnik J, et al. Transfusion-acquired hepatitis A in a premature
infant with secondary nosocomial spread in an intensive care nursery. Am J Dis Child.
1986;140:23–27.
242. Noble RC, Kane MA, Reeves SA, Roeckel I. Posttransfusion hepatitis A in a neonatal inten-
sive care unit. JAMA. 1984;252:2711–2715.
243. Chodick G, Ashkenazi S, Lerman Y. The risk of hepatitis A infection among healthcare work-
ers: a review of reported outbreaks and sero-epidemiologic studies. J Hosp Infect.
2006;62:414–420.
244. Goodman RA, Carder CC, Allen JR, Orenstein WA, Finton RJ. Nosocomial hepatitis A trans-
mission by an adult patient with diarrhea. Am J Med. 1982;73:220–226.
245. Petrosillo N, Raffaele B, Martini L, et al. A nosocomial and occupational cluster of hepatitis A
virus infection in a pediatric ward. Infect Control Hosp Epidemiol. 2002;23:343–345.
246. Doebbeling BN, Li N, Wenzel RP. An outbreak of hepatitis A among health care workers: risk
factors for transmission. Am J Public Health. 1993;83:1679–1684.
247. Drusin LM, Sohmer M, Groshen SL, Spiritos MD, Senterfit LB, Christenson WN. Nosocomial
hepatitis A infection in a pediatric intensive care unit. Arch Dis Child. 1987;62:690–695.
248. Centers for Disease Control and Prevention. Update: prevention of hepatitis A after exposure
to hepatitis A virus and in international travelers. Updated recommendations of the Advisory
Committee on Immunization Practices (ACIP). MMWR. 2007;56(41);1080–1084.
http://www.cdc.gov/mmwR/preview/mmwrhtml/mm5641a3.htm. Accessed May 2, 2008.
249. Eickhoff TC. Airborne nosocomial infection: a contemporary perspective. Infect Control Hosp
Epidemiol. 1994;15:663–672.
250. Sepkowicz KA. Occupationally acquired infections in health care workers, pt I. Ann Intern
Med. 1996;125:826–834.
251. Atkinson WL. Measles and healthcare workers. Infect Control Hosp Epidemiol. 1994;15:5–7.
252. Gurevich I, Barzarga RA, Cuhna BA. Measles: lessons from an outbreak. Am J Infect Control.
1992;20:319–325.
253. Rank EL, Brettman L, Katz-Pollack H, DeHertogh D, Neville D. Chronology of a hospital-
wide measles outbreak: lessons learned and shared from an extraordinary week in late
March 1989. Am J Infect Control. 1992;20:315–318.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 128

128 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

254. Centers for Disease Control and Prevention. Measles, mumps, and rubella—vaccine use and
strategies for elimination of measles, rubella, and congenital rubella syndrome and control of
mumps: recommendations of the Advisory Committee on Immunization Practices (ACIP).
MMWR. 1998;47(RR-8):1–57. http://www.cdc.gov/MMWR/preview/MMWRhtml/00053391.htm.
Acessed April 6, 2008.
255. Bloch AB, Orenstein WA, Ewing WM, et al. Measles outbreak in a pediatric practice: airborne
transmission in an office setting. Pediatr. 1985;75:676–683.
256. Centers for Disease Control and Prevention. Import-associated measles outbreak—Indiana,
May–June 2005. MMWR. 2005;54(42):1073–1075. http://www.cdc.gov/mmwr/preview/mmwrhtml/
mm5442a1.htm. Accessed April 5, 2008.
257. Parker AA, Staggs W, Dayan GH, et al. Implications of a 2005 measles outbreak in Indiana
for sustained elimination of measles in the United States. N Engl J Med. 2006;355(5):447–
455. http://content.nejm.org/cgi/content/abstract/355/5/447. Accessed April 5, 2008.
258. Centers for Disease Control and Prevention. Measles—United States, January 1–April 25,
2008. MMWR. 2008;57(Early Release):1–4. http://www.cdc.gov/mmwr/preview/mmwrhtml/
mm57e501a1.htm?s_cid=mm57e501a1_e. Accessed May 1, 2008.
259. Centers for Disease Control and Prevention. Immunization of health-care workers: recom-
mendations of the Advisory Committee on Immunization Practices (ACIP) and the Hospital
Infection Control Practices Advisory Committee (HICPAC). MMWR.1997;6(RR-18):1–42.
http://www.cdc.gov/mmwr/preview/mmwrhtml/00050577.htm. Accessed April 6, 2008.
260. American Academy of Pediatrics. Measles. In: Peter G, ed. 2006 Red Book: Report of the Commit-
tee on Infectious Diseases. 24th ed. Elk Grove Village, IL: American Academy of Pediatrics; 2006.
261. Uckay I, Hugonnet S, Kaiser L, Sax H, Pittet D. Age limit does not replace serologic testing
for determination of immune status for measles. Infect Control Hosp Epidemiol.
2007;28:1117–1120.
262. Rivera ME, Mason WH, Ross LA, Wright HT Jr. Nosocomial measles infection in a pediatric
hospital during a community-wide epidemic. J Pediatr. 1991;119:183–186.
263. Houck P, Scott-Johnson G, Krebs L. Measles immunity among community hospital employ-
ees. Infect Control Hosp Epidemiol. 1991;12:663–668.
264. Weber DJ, Rutala WA, Hamilton H. Prevention and control of varicella-zoster infections in
healthcare facilities. Infect Control Hosp Epidemiol. 1996;17:694–705.
265. Sawyer MH, Chamberlain CJ, Wu YN, Aintablian N, Wallace MR. Detection of varicella-
zoster virus DNA in air samples from hospital rooms. J Infect Dis. 1994;169:91–94.
266. Leclair JM, Zaia JA, Levin MJ, Congdon RG, Goldmann DA. Airborne transmission of chick-
enpox in a hospital. N Engl J Med. 1980;302:450–453.
267. Faoagali JL, Darcy D. Chickenpox outbreak among the staff of a large, urban adult hospital:
costs of monitoring and control. Am J Infect Control. 1995;23:247–250.
268. Gustafson TL, Lavely GB, Brawner ER, Hutcheson RH, Wright PF, Schaffner W. An outbreak
of airborne nosocomial varicella. Pediatr. 1982;70:550–556.
269. Apisarnthanarak A, Kitphati R, Tawatsupha P, et al. Outbreak of varicella-zoster virus infec-
tion among Thai healthcare workers. Infect Control Hosp Epidemiol. 2007;28:430–434.
270. Yehia A, Aly N, Al Obaid I, Al-Qulooshi N, Zahed Z. Occupationally related outbreak of chick-
enpox in an intensive care unit. Med Princ Pract. 2007;16:399–401.
271. Centers for Disease Control and Prevention. Prevention of varicella: recommendations of the
Advisory Committee on Immunization Practices (ACIP). MMWR. 2007;56(RR-04):1–40.
272. American Academy of Pediatrics. Varicella-zoster. In: Peter G, ed. 2006 Red Book: Report of
the Committee on Infectious Diseases. 24th ed. Elk Grove Village, IL: American Academy of
Pediatrics; 2006.
273. Brawley RL, Wenzel RP. An algorithm for chickenpox exposure. Pediatr Infect Dis J.
1984;3:502–504.
274. Stover BH, Bratcher DF. Varicella-zoster virus: infection, control and prevention. Am J Infect
Control. 1998;26:369–381.
275. Levandowski RA, Rubenis M. Nosocomial conjunctivitis caused by adenovirus Type 4. J
Infect Dis. 1981;143:28–31.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 129

References 129

276. Brummit CF, Cherrington JM, Katzenstein DA. Nosocomial adenovirus infections: molecular
epidemiology of an outbreak due to adenovirus 3a. J Infect Dis. 1988;158:423–432.
277. Birenbaum E, Linder N, Varsano N, et al. Adenovirus type 8 conjunctivitis outbreak in a
neonatal intensive care unit. Arch Dis Child. 1993;68:610–611.
278. Wharton M, Cochi SL, Hutcheson RH, Schaffner W. Mumps transmission in hospitals. Arch
Intern Med. 1990;150:47–49.
279. Fischer PR, Brunetti C, Welch V, Christenson JC. Nosocomial mumps: report of an outbreak
and its control. Am J Infect Control. 1996;24:13–18.
280. Buxton Bridges C, Kuehnert MJ, Hall CB. Transmission of influenza: implications for control
in health care setting. Clin Infect Dis. 2003;37:1094–1101.
281. Shishiba T, Matsunaga Y. An outbreak of erythema infectiosum among hospital staff mem-
bers including a patient with pleural fluid and pericardial effusion. J Am Acad Dermatol.
1993;29:265–267.
282. Seng C, Watkins P, Morse D, et al. Parvovirus B19 outbreak on an adult ward. Epidemiol
Infect. 1994;113:345–353.
283. Pillay D, Patou G, Hurt S, Kibbler CC, Griffiths PD. Parvovirus B19 outbreak in a children’s
ward. Lancet. 1992;339:107–109.
284. Poland GA, Nichol KL. Medical students as sources of rubella and measles outbreaks. Arch
Intern Med. 1990;150:44–46.
285. Fliegel PE, Weinstein WM. Rubella outbreak in a prenatal clinic: management and preven-
tion. Am J Infect Control. 1982;10:29–33.
286. Polk FB, White JA, DeGirolami PC, Modlin JF. An outbreak of rubella among hospital per-
sonnel. N Engl J Med. 1980;303:541–545.
287. Klausner JD, Passaro D, Rosenberg J, et al. Enhanced control of Mycoplasma pneumoniae
pneumonia with azithromycin prophylaxis. J Infect Dis. 1998;177:161–166.
288. Hall CB. Nosocomial viral respiratory infections: perennial weeds on pediatric wards. Am J
Med. 1981;70:670–676.
289. Hall CB, Douglas RG Jr. Possible transmission by fomites of respiratory syncytial virus. J
Infect Dis. 1980;141:98–102.
290. Hall CB. Respiratory syncytial virus: its transmission in the hospital environment. Yale J
Biol Med. 1982;55:219–223.
291. Hall CB. The nosocomial spread of respiratory syncytial viral infections. Annu Rev Med.
1983;34:311–319.
292. Snydman DR, Greer C, Meissner HC, McIntosh K. Prevention of nosocomial transmission of
respiratory syncytial virus in a newborn nursery. Infect Control Hosp Epidemiol. 1988;9:105–
108.
293. Falsey AR. Noninfluenza respiratory virus infection in long-term care facilities. Infect Control
Hosp Epidemiol. 1991;12:602–608.
294. Sorvillo FJ, Huie SF, Strassburg MA, Butsumyo A, Shandera WAX, Fannin SL. An outbreak
of respiratory syncytial virus pneumonia in a nursing home for the elderly. J Infect.
1984;9:252–256.
295. Harrington RD, Hooton TM, Hackman RC, et al. An outbreak of respiratory syncytial virus in
a bone marrow transplant center. J Infect Dis. 1992;165:987–993.
296. Guidry GG, Black-Payne CA, Payne DK, Jamison RM, George RB, Bocchini JA Jr. Respira-
tory syncytial virus infection among intubated adults in a university intensive care unit.
Chest. 1991;100:1377–1384.
297. Valenti WM, Clarke TA, Hall CB, et al. Concurrent outbreaks of rhinovirus and respiratory
syncytial virus in an intensive care nursery: epidemiology and associated risk factors. J Pedi-
atr. 1982;100:722–726.
298. Goldmann DA. Epidemiology and prevention of pediatric viral respiratory infections in
health-care institutions. Emerg Infect Dis. 2001;7:249–253.
299. Jalal H, Bibby DF, Bennett J, et al. Molecular investigations of an outbreak of parainfluenza
virus type 3 and respiratory syncytial virus infections in a hematology unit. J Clin Microbiol.
2007;45:1690–1696.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 130

130 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

300. Halasa NB, Williams JV, Wilson GJ, Walsh WF, Schaffner W, Wright PF. Medical and eco-
nomic impact of a respiratory syncytial virus outbreak in a neonatal intensive care unit.
Pediatr Infect Dis J. 2005;24(12):1040–1044.
301. Broder KR, Cortese MM, Iskander JK, et al. Preventing tetanus, diphtheria, and pertussis
among adolescents: use of tetanus toxoid, reduced diphtheria toxoid and acellular pertussis
vaccines recommendations of the Advisory Committee on Immunization Practices (ACIP).
MMWR Recomm Rep. 2006; 55:1–34.
302. Long SS, Welkon CJ, Clark JL. Widespread silent transmission of pertussis in families: anti-
body correlates of infection and symptomatology. J Infect Dis. 1990;161:480–486.
303. Black S. Epidemiology of pertussis. Pediatr Infect Dis J. 1997;16:S85–S89.
304. Weber DJ, Rutala WA. Pertussis: an underappreciated risk for nosocomial outbreaks. Infect
Control Hosp Epidemiol. 1998;19:825–828.
305. Cherry JD. Nosocomial pertussis in the nineties. Infect Control Hosp Epidemiol. 1995;16:553–
555.
306. Bryant K, Humbaugh K, Brothers K, et al. Measures to control an outbreak of pertussis in a
neonatal intermediate care nursery after exposure to a healthcare worker. Infect Control
Hosp Epidemiol. 2006;27:541–545.
307. Boulay BR, Murray CJ, Ptak J, Kirkland KB, Montero J, Talbot EA. An outbreak of pertussis
in a hematology-oncology care unit: implications for adult vaccination policy. Infect Control
Hosp Epidemiol. 2006; 27:92–95.
308. Linneman CC Jr, Ramundo N, Perlstein PH, Minton SD, Englender GS. Use of pertussis vac-
cine in an epidemic involving hospital staff. Lancet. 1975;2:540–543.
309. Valenti WM, Pincus PH, Messner MK. Nosocomial pertussis: possible spread by a hospital
visitor. Am J Dis Child. 1980;134:520–521.
310. Kurt TL, Yeager AS, Guenette S, Dunlop S. Spread of pertussis by hospital staff. JAMA.
1972;221:264–267.
311. Bassinet L, Matrat M, Njamkepo E, et al. Nosocomial pertussis outbreak among adult
patients and healthcare workers. Infect Control Hosp Epidemiol. 2004;25:995–997.
312. Pascual FB, McCall CL, McMurtray A, et al. Outbreak of pertussis among healthcare work-
ers in a hospital surgical unit. Infect Control Hosp Epidemiol. 2006;27(6):546–552.
313. Bonmarin I, Poujol I, Lévy-Bruhl D. Nosocomial infections and community clusters of per-
tussis in France, 2000–2005. Eur Surveill. 2007;12(11). http://www.eurosurveillance.org/
em/v12n11/1211–226.asp. Accessed May 1, 2008.
314. Vranken P, Pogue M, Romalewski C, Ratard R. Outbreak of pertussis in a neonatal intensive
care unit—Louisiana, 2004. Am J Infect Control. 2006;34:550–554.
315. Calugar A, Ortega-Sanchez IR, Tiwari T, et al. Nosocomial pertussis: costs of an outbreak and
benefits of vaccinating health care workers. Clin Infect Dis. 2006;42(7):981–988.
316. Daskalaki I, Hennessey P, Hubler R, Long SS. Resource consumption in the infection control
management of pertussis exposure among healthcare workers in pediatrics. Infect Control
Hosp Epidemiol. 2007;28:412–417.
317. Baggett HC, Duchin JS, Shelton W. Two nosocomial pertussis outbreaks and their associated
costs—King County, Washington, 2004. Infect Control Hosp Epidemiol. 2007;28:537–543.
318. Christie CD, Glover AM, Wilke MJ, Marx ML, Reising SF, Hutchinson NM. Containment of
pertussis in the regional pediatric hospital during the greater Cincinnati epidemic of 1993.
Infect Control Hosp Epidemiol. 1995;16:556–563.
319. Tam TWS, Bentsi-Enchill A. The return of the 100-day cough: resurgence of pertussis in the
1990s. CMAJ. 1998;159(6):695–596.
320. de Melker HE, Schellekens JFP, Neppelenbroek SE, et al. Reemergence of pertussis in the
highly vaccinated population of the Netherlands: observations on surveillance data. Emerg
Infect Dis. 2000;6:348–335.
321. Wirsing von König C, Riffelman M,. Pertussis: An old disease in new clothes [Epub ahead of
print]. Eur Surveill. 2007;12(9). http://www.eurosurveillance.org/em/v12n09/1209–221
.asp. Accessed May 2, 2008.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 131

References 131

322. Centers for Disease Control and Prevention. Outbreaks of respiratory illness mistakenly
attributed to pertussis—New Hampshire, Massachusetts, and Tennessee, 2004–2006.
MMWR. 2007;56(33);837–842.
323. Centers for Disease Control and Prevention. Guidelines for the Control of Pertussis Out-
breaks. Centers for Disease Control and Prevention: Atlanta, GA, 2000. (Amendments made
in 2005 and 2006). http://www.cdc.gov/vaccines/pubs/pertussis-guide/guide.htm. Accessed
May 1, 2008.
324. Centers for Disease Control and Prevention. CDC. Preventing tetanus, diphtheria, and per-
tussis among adults: use of tetanus toxoid, reduced diphtheria toxoid and acellular pertussis
vaccine. Recommendations of the Advisory Committee on Immunization Practices (ACIP),
supported by the Healthcare Infection Control Practices Advisory Committee (HICPAC), for
use of Tdap among health-care personnel. MMWR. 2006;55(No. RR-17).
325. Rutala WA, Weber DJ. Management of healthcare workers exposed to pertussis. Infect Con-
trol Hosp Epidemiol. 1994;15:411–415.
326. Haiduven DJ, Hench CP, Simpkins SM, Stevens DA. Standardized management of patients
and employees exposed to pertussis. Infect Control Hosp Epidemiol. 1998;19:861–864.
327. Haley CE, Cohen ML, Halter J, Meyer RD. Nosocomial Legionnaires’ disease: a continuing
common-source epidemic at Wadsworth Medical Center. Ann Intern Med. 1979;90:583–586.
328. Thacker SB, Bennett JV, Tsai TF, et al. An outbreak in 1965 of severe respiratory illness
caused by the Legionnaires’ disease bacterium. J Infect Dis. 1978;138:512–519.
329. Mermel LA, Josephson SL, Giorgio CH, Dempsey J, Parentau S. Association of Legionnaires’
disease with construction: contamination of potable water? Infect Control Hosp Epidemiol.
1995;16:76–81.
330. Doebbeling BN, Ishak MA, Wade BH, et al. Nosocomial Legionella micdadei pneumonia: 10
years experience and a case-control study. J Hosp Infect. 1989;13:289–298.
331. Memish ZA, Oxley C, Contant J, Garber GE. Plumbing system shock absorbers as a source of
Legionella pneumophila. Am J Infect Control. 1992;20:305–309.
332. Venezia RA, Agresta MD, Hanley EM, Urquhart K, Schoonmaker D. Nosocomial legionellosis
associated with aspiration of nasogastric feedings diluted in tap water. Infect Control Hosp
Epidemiol. 1994;15:529–533.
333. Centers for Disease Control and Prevention. Sustained transmission of nosocomial Legion-
naires’ disease—Arizona and Ohio. MMWR. 1997;46:416–421.
334. Dondero TJ, Rendtorff RC, Mallison GF, et al. An outbreak of Legionnaires’ disease associ-
ated with a contaminated cooling tower. N Engl J Med. 1980;302:365.
335. Arnow PM, Chou T, Weil D, et al. Nosocomial Legionnaires’ disease caused by aerosolized tap
water from respiratory devices. J Infect Dis. 1982;146:460–467.
336. Ricketts K, Joseph C, Legionnaires’ disease in Europe: 2005–2006 [Epub ahead of print].
Eur Surveill 2007;12(12). http://www.eurosurveillance.org/em/v12n12/1212–224.asp. Accessed
July 29, 2008.
337. Brown CM, Nuorti P, Breiman RF, et al. A community outbreak of Legionnaires’ disease
linked to hospital cooling towers: an epidemiological method to calculate dose of exposure. Int
J Epidemiol. 1999;28:353–359.
338. Guerrero IC, Filippone C. A cluster of Legionnaires’ disease in a community hospital—a clue
to a larger epidemic. Infect Control Hosp Epidemiol. 1996;17:177–178.
339. Bartram J, Chartier Y, Lee JV, Pond K, Surman-Lee S, eds. Legionella and the Prevention of
Legionellosis. Geneva, Switzerland: World Health Organization; 2007. http://www.who.int/
water_sanitation_health/emerging/legionella/en/index.html. Accessed May 2, 2008.
340. Walsh TJ, Dixon DM. Nosocomial aspergillosis: environmental microbiology, hospital epi-
demiology, diagnosis, and treatment. Eur J Epidemiol. 1989;5:131–142.
341. Cole EC, Cook CE. Characterization of infectious aerosols in health care facilities: an aid to
effective engineering controls and preventive strategies. Am J Infect Control. 1998;26:453–
464.
342. Pannuti CS, Gingrich RD, Pfaller MA, Wenzel RP. Nosocomial pneumonia in adult patients
undergoing bone marrow transplantation: a 9-year study. J Clin Oncol. 1991;9:77–84.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 132

132 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

343. Rotstein C, Cummings KM, Tidings J, et al. An outbreak of invasive aspergillosis among allo-
geneic bone marrow transplants: a case-control study. Infect Control. 1985;6:347–355.
344. Opal SM, Asp AA, Cannady PB Jr, Morse PL, Burton LJ, Hammer PG II. Efficacy of infection
control measures during a nosocomial outbreak of disseminated aspergillosis associated with
hospital construction. J Infect Dis. 1986;153:634–637.
345. Arnow PM, Anderson RL, Mainous D, et al. Pulmonary aspergillosis during hospital renova-
tion. Am Rev Respir Dis. 1978;118:49–53.
346. Flynn PM, Williams BG, Hetherington SV, Williams BF, Giannini MA, Pearson TA. Aspergillus
terreus during hospital renovation. Infect Control Hosp Epidemiol. 1993;14:363–365.
347. McCarty JM, Flam MJ, Pulen G, et al. Outbreak of primary cutaneous aspergillosis related to
intravenous arm boards. J Pediatr. 1986;108:721–724.
348. Hopkins CC, Weber DJ, Rubin RH. Invasive Aspergillus infection: possible non-ward common
source within the hospital environment. J Hosp Infect. 1989;13:19–25.
349. Thio CL, Smith D, Merz WG, et al. Refinements of environmental assessment during an out-
break investigation of invasive aspergillosis in a leukemia and bone marrow transplant unit.
Infect Control Hosp Epidemiol. 2000;21(1):18–23.
350. Pegues DSA, Lasker BA, McNeil MM, et al. Cluster of cases of invasive aspergillosis in a
transplant intensive care unit: evidence of person-to-person airborne transmission. Clin
Infect Dis. 2002;34:412–416. http://www.journals.uchicago.edu/doi/pdf/10.1086/338025.
Accessed May 2, 2008.
351. Hruszkewycz V, Ruben B, Hypes CM, Bostic GD, Staszkiewicz J, Band JD. A cluster of pseu-
dofungemia associated with hospital renovation adjacent to the microbiology laboratory.
Infect Control Hosp Epidemiol. 1992;13:147–150.
352. Carter CD, Barr BA. Infection control issues in construction and renovation. Infect Control
Hosp Epidemiol. 1997;18:587–596.
353. Maryland Department of Health and Mental Hygiene, Community Health Administration.
Guidelines for Prevention and Control of Nosocomial Pulmonary Aspergillosis, 1999.
http://www.cha.state.md.us/edcp/guidelines/aspers2.html. Accessed May 2, 2008.
354. Carreras E. Preventing exposure to molds. Clin Microbiol Infect. 2006;12(suppl 7):77–83.
http://www.blackwell-synergy.com/doi/abs/10.1111/j.1469–0691.2006.01608.x. Accessed May
2, 2008.
355. Gangneux J-P, Bretagne S, Cordonnier C, et al. Prevention of nosocomial fungal infection: the
French approach. Clin Infect Dis. 2002;35:343–345. http://www.journals.uchicago.edu/doi/
pdf/10.1086/341318. Accessed May 2, 2008.
356. Rutala WA, Weber DJ. Water as a reservoir of nosocomial pathogens. Infect Control Hosp Epi-
demiol. 1997;18:609–616.
357. Stamm WE, Colella JJ, Anderson RL, Dixon RE. Indwelling arterial catheters as a source of
nosocomial bacteremia: an outbreak caused by Flavobacterium species. N Engl J Med.
1975;292:1099–1102.
358. Casewell MW, Slater NGP, Cooper JE. Operating theatre water baths as a cause of
Pseudomonas septicaemia. J Hosp Infect. 1981;2:237–240.
359. McGuckin MB, Thorpe RJ, Abrutyn E. Hydrotherapy: an outbreak of Pseudomonas aerugi-
nosa wound infections related to Hubbard tank treatments. Arch Phys Med Rehabil.
1981;62:283–285.
360. Lowry PW, Beck-Sague CM, Bland LA, et al. Mycobacterium chelonae infection among
patients receiving high-flux dialysis in a hemodialysis clinic in California. J Infect Dis.
1990;161:85–90.
361. Graman PS, Quinlan GA, Rank JA. Nosocomial legionellosis traced to a contaminated ice
machine. Infect Control Hosp Epidemiol. 1997;18:637–640.
362. Verweij PE, Bilj D, Melchers W, et al. Pseudo-outbreak of multiresistant Pseudomonas aerugi-
nosa in a hematology unit. Infect Control Hosp Epidemiol. 1997;18:128–131.
363. Sniadack DH, Ostroff SM, Karlix MA, et al. A nosocomial pseudo-outbreak of Mycobacterium
xenopi due to a contaminated potable water supply: lessons in prevention. Infect Control
Hosp Epidemiol. 1993;14:636–641.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 133

References 133

364. Van Horn KG, Tatz JS, Li KI, Newman L, Wormser GP. Copepods associated with a perirectal
abscess and copepod pseudo-outbreak in stools for ova and parasite examinations. Diagn
Microbiol Infect Dis. 1992;15:561–565.
365. Klotz SA, Normand RE, Kalinsky RG. “Through a drinking glass and what was found there”:
pseudocontamination of a hospital’s drinking water. Infect Control Hosp Epidemiol.
1992;13:477–481.
366. Muyldermans G, de Smet F, Pierard D, et al. Neonatal infections with Pseudomonas aerugi-
nosa associated with a water-bath used to thaw fresh frozen plasma. J Hosp Infect. 1998;
9(4):309–314.
367. Conger NG, O’Connell RJ, Laurel VL, et al. Mycobacterium simiae outbreak associated with a
hospital water supply. Infect Control Hosp Epidemiol. 2004;25:1050–1055.
368. Emmerson AM. Emerging waterborne infections in health-care settings. Emerg Infect Dis.
2007;7:272–276. http://www.cdc.gov/ncidod/eid/vol7no2/emmerson.htm. Accessed May 2,
2008.
369. Manangan LP, Anderson RL, Arduino MJ, Bond WW. Sanitary care and maintenance of ice-
storage chests and ice-making machines in health care facilities. Am J Infect Control.
1998;26(2):111–112.
370. Burnett IA, Weeks GR, Harris DM. A hospital study of ice-making machines: their bacteriol-
ogy, design, usage, and upkeep. J Hosp Infect. 1994;28:305–313.
371. Maloney SA, Jarvis WR. Epidemic nosocomial pneumonia in the intensive care unit. Chest.
1995;16:209–223.
372. Patterson TF, Patterson JE, Masecar BL, et al. A nosocomial outbreak of Branhamella
catarrhalis confirmed by restriction endonuclease analysis. J Infect Dis. 1988;157:996–1001.
373. Centers for Disease Control. Suspected nosocomial influenza cases in an intensive care unit.
MMWR. 1988;37:3–4.
374. Locksley RM, Cohen ML, Quinn TC, et al. Multiply antibiotic-resistant Staphylococcus
aureus: introduction, transmission, and evolution of nosocomial infection. Ann Intern Med.
1982;97:317–324.
375. Singh-Naz N, Willy M, Riggs N. Outbreak of para-influenza virus type 3 in a neonatal nurs-
ery. Pediatr Infect Dis J. 1990;9:31–33.
376. Villarino ME, Stevens LE, Schable BS, et al. Risk factors for epidemic Xanthomonas infec-
tion/colonization in intensive care unit patients. Infect Control Hosp Epidemiol. 1992;13:201–
206.
377. Fisher-Hoch SP, Tobin JO, Nelson AM, et al. Investigation and control of Legionnaires’ dis-
ease in a district general hospital. Lancet. 1981;1:933–936.
378. Arnow PM, Chou T, Weil D, et al. Nosocomial Legionnaires’ disease caused by aerosolized tap
water from respiratory devices. J Infect Dis. 1982;146:460–467.
379. Brady MT. Nosocomial Legionnaires’ disease in a children’s hospital. J Pediatr. 1988;115:
46–58.
380. Mastro TD, Fields BS, Breiman RF, et al. Legionnaires’ disease and use of medication nebu-
lizers. J Infect Dis. 1991;163:667–671.
381. Blatt SP, Parkinson MD, Pace E, et al. Nosocomial Legionnaires’ disease: aspiration as a pri-
mary mode of disease acquisition. Am J Med. 1991;95:16–22.
382. Weems JJ, Davis BJ, Tablan OC, et al. Construction activity: an independent risk factor for
invasive aspergillosis and zygomycosis in patients with hematologic malignancy. Infect Con-
trol. 1987;8:71–75.
383. Arnow PM, Sadigh M, Costas C, et al. Endemic and epidemic aspergillosis associated with in-
hospital replication of Aspergillus organisms. J Infect Dis. 1991;164:998–1002.
384. Buffington J, Reporter R, Lasker B, et al. Investigation of an epidemic of invasive aspergillo-
sis: utility of molecular typing with the use of random amplified polymorphic DNS probes.
Pediatr Infect Dis J. 1994;13:386–393.
385. Gastmeier P, Loui A, Stamm-Balderjahn S, et al. Outbreaks in neonatal intensive care
units—They are not like others. Am J Infect Control. 2007;35:172–176.
57793_CH03_ARIAS.qxd 1/19/09 2:28 PM Page 134

134 OUTBREAKS REPORTED IN ACUTE CARE SETTINGS

386. Samet JM, Marbury MC, Spengler JD. Health effects and sources of indoor air pollution, pt.
1. Am Rev Respir Dis. 1987;136:1486–1508.
387. Samet JM, Marbury MC, Spengler JD. Health effects and sources of indoor air pollution, pt.
2. Am Rev Respir Dis. 1988;137:221–242.
388. Brandt-Rauf PW, Andrews LR, Schwarz-Miller J. Sick-hospital syndrome. J Occup Med.
1991;33:737–739.
389. Gold DR. Indoor air pollution. Clin Chest Med. 1992;13:215–229.
390. Hodgson M. Indoor environmental exposures and symptoms. Environ Health Perspect.
2002;110:(Suppl 4):663–667. http://www.ehponline.org/members/2002/suppl-4/663–667hodgson/
hodgson-full.html. Accessed May 3, 2008.
391. Jaakkola MS, Yang L, Ieromnimon A, Jaakkola JJK. Office work exposures and respiratory
and sick building syndrome symptoms. Occup Environ Med. 2007;64(3):178–184. [Erratum
in: Occup Environ Med. 2007 Jun;64(6):428.] http://oem.bmj.com/cgi/content/full/64/3/178.
Accessed May 3, 2008.
392. Donnell HD Jr, Bagby JR, Harmon RG, et al. Report of an illness outbreak at the Harry S
Truman State Office Building. Am J Epidemiol. 1989;129(3):550–558.
393. Klaucke DN, Johansen M, Vogt RL. An outbreak of xylene intoxication in a hospital. Am J
Ind Med. 1982;3(2):173–178.
394. Klauck D, Vogt R. A case exercise: outbreak investigation at a Vermont community hospital. J
Public Health Manag Pract. 2005;11(4):301–305.
395. Hardin BD, Kelman BJ, Saxon A. ACOEM evidence-based statement. adverse human health
effects associated with molds in the indoor environment. J Occup Environ Med.
2003;45(5):70–478. http://www.joem.org/pt/re/joem/fulltext.00043764-200305000-00006.htm;
jsessionid=LcDNJvXVnnDgJvDR7d155vzr6LtQRhMWdVdf03HSSnmK1JL6D3Wt!1379360954!
181195629!8091!-1?&fullimage=true. Accessed May 3, 2008.
396. Pfaller MA. Nosocomial candidiasis: emerging species, reservoirs, and modes of transmission.
Clin Infect Dis. 1996;22(suppl 2):S89–S94.
397. Jarvis WR. Epidemiology of nosocomial fungal infections with emphasis on Candida species.
Clin Infect Dis. 1995;20:1526–1530.
398. Pfaller MA, Diekma DJ. Epidemiology of invasive candidiasis: a persistent public health
problem. Clin Microbiol Rev. 2007;20(1):133–163. http://www.pubmedcentral.nih.gov/
articlerender.fcgi?tool=pubmed&pubmedid=17223626. Accessed May 3, 2008.
399. Perlroth J, Choi B, Spellberg B. Nosocomial fungal infections: epidemiology, diagnosis, and
treatment. Med Mycol. 2007;45(4):321–346.
400. Pappas PG. Invasive candidiasis. Infect Dis Clin North Am. 2006;20(3):485–506.
401. Waggoner-Fountain LA, Whit Walker M, Hollis RJ, et al. Vertical and horizontal transmission
of unique Candida species to premature newborns. Clin Infect Dis. 1996:22:803–808.
402. Fowler SL, Rhoten B, Springer SC, Messer SA, Hollis RJ, Pfaller MA. Evidence for person-to-
person transmission of Candida lusitaniae in a neonatal intensive care unit. Infect Control
Hosp Epidemiol. 1998;19:343–345.
403. Reef SE, Lasker BA, Butcher DS. Nonperinatal nosocomial transmission of Candida albicans
in a neonatal intensive care unit: prospective study. J Clin Microbiol. 1998;36:1255–1259.
404. van Asbeck EC, Huang YC, Markham AN, Clemons KV, Stevens DA. Candida parapsilosis
fungemia in neonates: genotyping results suggest healthcare workers hands as source, and
review of published studies. Mycopathologia. 2007;164(6):287–293.
405. Sheretz RJ, Gledhill KS, Hampton KD, et al. Outbreaks of Candida bloodstream infections
associated with retrograde medication administration in a neonatal intensive care unit. J
Pediatr. 1992;120:455–461.
406. Solomon SL, Khabbaz R, Parker RH, et al. An outbreak of Candida parapsilosis bloodstream
infections in patients receiving parenteral nutrition. J Infect Dis. 1984;149:96–102.
407. Solomon SL, Alexander H, Eley JW, et al. Nosocomial fungemia in neonates associated with
intravascular pressure monitoring devices. Pediatr Infect Dis J. 1986;5:680–685.

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