REVIEW

CURRENT
OPINION Febrile urinary tract infections: pyelonephritis
and urosepsis
Caroline Schneeberger a, Frits Holleman b, and Suzanne E. Geerlings c

Purpose of review
Complicated infections of the urinary tract (UTI) including pyelonephritis and urosepsis are also called
febrile UTI. This review describes insights from the literature on this topic since July 2014.
Recent findings
Recent studies regarding risk factors and consequences of febrile UTI confirmed existing knowledge. It
remains difficult to obtain insight into the epidemiology of febrile UTI because urine and blood cultures are
frequently missing. The relationship between host and virulence factors of Escherichia coli was further
explored showing that less virulent strains can cause infection in immunocompromised patients. In contrast
to obstructive uropathy, diabetes, and being older, neutropenia was not a risk factor for lower UTI or
urosepsis. A randomized controlled trial revealed that ceftolozane–tazobactam was marginally superior to
levofloxacin as treatment for complicated UTI. Case series supported the notion that xanthogranulomatous
and emphysematous pyelonephritis are more common in diabetic patients and that drainage or surgery is
often required.
Summary
Neutropenia was not a risk factor for lower UTI or urosepsis. When local resistance percentages to the
frequently prescribed fluoroquinolones are high, the combination of ceftolozane–tazobactam may be an
alternative as treatment for complicated UTI. Xanthogranulomatous and emphysematous pyelonephritis
need to be considered in diabetic patients presenting with UTI symptoms.
Keywords
emphysematous pyelonephritis, febrile urinary tract infection, obstructive pyelonephritis, pyelonephritis,
urosepsis, xanthogranulomatous pyelonephritis

INTRODUCTION microorganism and the host. Organisms causing

Infections of the urinary tract are common in var- febrile UTI have different genes encoding for
ious patient groups and are one of the most import- virulence factors, that is, characteristics that help
ant causes of sepsis (urosepsis). In clinical practice it the microorganism to infect the host. An example
can be difficult to differentiate between pyeloneph- is the pyelonephritis-associated pili (pap) gene
ritis (limited to the urinary tract including renal cluster encoding for P-fimbriae adhesions that
parenchym and pyelum) and urosepsis (infection enhance colonization by adhering to renal
of the urinary tract with bacteraemia). Therefore, parenchyma.
these diseases are often designated ‘febrile urinary
tract infection (UTI)’ [1].
The review provides an overview of the most
a
recent clinical studies of interest (published from Department of Medical Microbiology, University of Amsterdam,
b
Department of Internal Medicine and cDepartment of Infectious Dis-
July 2014 till now) concerning the pathophysiology,
eases, Centre for Infection and Immunity Amsterdam, Academic Medical
epidemiology, risk factors, consequences, and treat- Centre, Amsterdam, the Netherlands
ment of febrile UTI. Correspondence to Caroline Schneeberger, Department of Medical
Microbiology, Academic Medical Centre, University of Amsterdam, Mei-
bergdreef 9, Amsterdam 1105 AZ, the Netherlands. Tel: +31612388308;
PATHOPHYSIOLOGY e-mail: [email protected]
The pathophysiology of febrile UTI is dependent Curr Opin Infect Dis 2016, 29:80–85
on the interaction between the causative DOI:10.1097/QCO.0000000000000227

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 Febrile urinary tract infections Schneeberger et al.

control of a reversible epigenetic switch that defines

KEY POINTS if the cell is fimbriated (switch on) or afimbriated
 The interaction between the host and the virulence (switch off). Based on fluorescence intensity vari-
factors of E. coli isolates from patients with febrile UTI ation mainly present in the F1651 system the
was further explored underscoring that less virulent authors conclude that ‘that F1651 is an exquisite
strains can cause infection in hosts with a decreased example of regulatory expression that arms bacteria
immune system whereas more virulence factors are with strategies for surviving in more than one
needed to affect the immunocompetent host. particular environment’ [7 ].
&

 Obstructive uropathy, diabetes mellitus, and being The molecular characterization and subsequent
older are important known risk factors of febrile UTI, testing in animal models of virulence factors of 67 E.
though being neutropenic is not a risk factor. coli bloodstream isolates of adults with urosepsis
showed that there is an interdependence between
 The diagnosis of febrile UTI may be delayed in the
elderly and patients with diabetes mellitus since they bacterial and host characteristics. On the one hand,
less often present with typical symptoms of a febrile UTI less virulent strains tended to be isolated from older
possibly resulting in more severe disease manifestation. men with urinary tract abnormalities. On the other
hand, more virulent strains tended to be isolated
 Emphysematous and xanthogranulomatous
from younger women without urinary tract abnor-
pyelonephritis are more common in patients with &&

diabetes mellitus. Percutaneous drainage is often malities [8 ].

needed to treat both special forms of pyelonephritis. An accumulation of in the gyrA gene is one of
the mechanisms for quinolone resistance. However,
E. coli strains become less virulent after acquisition
&
of a gyrA mutation. Sanchez-Cespedes et al. [9 ]
showed that strains with a mutation in the gyrA
Escherichia coli gene had decreased capacity to cause cystitis and
E. coli remains the most common organism causing pyelonephritis partly because the strain had less
pyelonephritis and urosepsis in recent studies expression of virulence factor genes such as papA
&
[2,3,4 ]. and papB.
The following studies underscore that different
infections or host factors require expression or acti-
vation of different virulence factors. EPIDEMIOLOGY
A ‘higher gene diversity’ is present in uropatho- A clear insight into the epidemiology of febrile UTI
genic E. coli isolates from hospitalized patients with remains difficult to obtain. Firstly, not all causes of
pyelonephritis than from outpatients with cystitis. underlying sepsis, including UTI, can always be
This indicates that E. coli isolates need more viru- found. This is also caused by the fact that no proper
lence factors to cause pyelonephritis than cystitis. microbiological cultures are collected before the
Especially the pap genes (encoding for P-fimbriae start of antibiotics. In 813 (67.7%) of the 1251
adhesions), traT genes (outer membrane protein patients with a clinical diagnosis of pyelonephritis,
that increases serum resistance ability), aer genes who collected urine cultures, a positive result was
(siderophore), hly (toxins acting as secretory viru- found, whereas only 366 (34%) of the 1032 patients,
lence factors), and pathogenicity islands operons from whom blood cultures were collected, had bac-
(mobile genetic elements or ‘island’ needed for &
teraemia [10 ]. Secondly, it can be difficult to dis-
horizontal transfer of virulence determinants) were tinguish between pyelonephritis and urosepsis,
more prevalent among strains from patients with because different studies used different definitions.
&
pyelonephritis than patients with cystitis [5 ]. Some definitions are only based on the presence of
Flagellar motility is another virulence factor of positive urine or blood cultures; others on a com-
E. coli to escape host immune responses and to move bination of UTI symptoms with the presence of
to other infection sites such as the upper urinary & &&
pyuria [10 ,11 ,12 ].
&&

tract. Higher motility strains (motility diameter

6.6 mm) were more common in spontaneous bac- Extended-spectrum b-lactamase
terial peritonitis (59%) compared with UTI (16%), Infections of the urinary tract are increasingly
urosepsis (34%), biliary tract infection (29%), and caused by extended-spectrum b-lactamase (ESBL)
&
colonization (32%) [6 ]. producing E. coli even in patients without health-
F1651 and Pap, two adhesive factors, play a key &
care-associated risk factors [13 ]. A prevalence ESBL
role in establishing extraintestinal disease (as for producing E. coli of 71.4% in patients hospitalized
example in the urinary tract) caused by E. coli. with a complicated UTI has recently been described
The presence of both F1651 and Pap is under the in Mexico [2].

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Urinary tract infections

DIAGNOSTICS In another retrospective study analyzing 173

An important question is whether blood and urine patients Cornejo-Dávila et al. [2] found that recent
cultures are always both needed to find the causa- use of antibiotics (95.3%) and obstructive uropathy
tive microorganism. In a study by Ledochowski et al. (73.4%) were associated with development of a
83 (31%) of the 264 patients with both urine and complicated UTI.
blood cultures collected at the same time had bac- It would have great advantages to be able to
teraemia. In only 11 patients (4.2%) the blood predict who needs broad-spectrum antibiotics. Park
&

culture had an additional value. We think that et al. [18 ] concluded that older age (>55 years),
because blood cultures, in contrast to urine, can antibiotic use within the previous year, and diabetic
be collected immediately at admission before anti- patients with recurrent pyelonephritis are risk fac-
microbials are given, they may be more useful than tors for community-acquired pyelonephritis with an
shown in this study [14 ].
&
ESBL producing E. coli.
In patients with an obstruction of the urinary Elderly may be more susceptible to infections,
tract it can be more difficult to identify the causative including infections of the urinary tract, because
microorganism in a voided urine portion. Of the 65 they often have many comorbidities, urinary tract
patients that underwent a ureteroscopic interven- abnormalities, and a decreased immune response
tion for ureteral stones 35 patients had a positive (e.g. as a result of steroid use). The incidence of
urine culture. In more than 25% of the cases a bacteraemia (39.1 vs. 27.8%) and ESBL producing
difference was found between the voided urine Enterobacteriaceae (9.0 vs. 5.5%) were higher in
samples and the urine samples captured at the time elderly women (>65 years) with community-onset,
of decompression of the urinary tract. These results nonobstructive pyelonephritis compared with non-
highlight that both samples are needed to assure elderly women. In addition, the elderly less often
adequate antibiotic coverage [15 ].
&
showed the typical symptoms of an upper or lower
Radiological techniques like ultrasound and UTI. No differences in clinical cure rates were found
computed tomography are used to find signs of between elderly and nonelderly women. The most
obstruction (e.g. hydronephrosis and urethral common comorbidity in both elderly and noneld-
stones) or other forms of renal involvement. Per- erly women was diabetes mellitus (respectively 40.9
&&

forming ultrasound identified common causes of and 25.9%) [19 ].

obstruction such as urolithiasis and tumours in The importance of diabetes mellitus is further
93% of cases [16 ].
&
supported by investigators of another study who
found that women with diabetes mellitus and com-
munity-acquired pyelonephritis more often had
RISK FACTORS bacteraemia and needed longer hospitalization
There are several known risk factors for febrile UTI. compared with women without diabetes mellitus
&&
An important group is the anatomical risk factors of (median 9.0 vs. 7.0 days) [20 ]. Also patients with
the urinary tract including stones, tumours, diabetes mellitus and pyelonephritis less often suf-
anomalies, and stenosis. Interventions involving fered from the ‘typical’ pyelonephritis symptoms
the urogenital tract such as an indwelling catheter such as flank pain or symptoms of a lower UTI
&& &&
or transrectal prostate biopsy are risk factors, [19 ,20 ]. This could result in a delayed diagnosis
because bacteria are often introduced in the nor- of pyelonephritis in these patients, and therefore
mally sterile urinary tract [17]. In case of obstructive lead to more severe complications such as
pyelonephritis, antibiotics alone are not sufficient emphysematous pyelonephritis.
and treatment of the cause of obstruction is import- In contrast to diabetes, being neutropenic is
&
ant to guarantee drainage [16 ]. not a risk factor for infection of the urinary
It had been found that more than two-thirds tract. The incidence of both lower UTI (3/109;
(70.9%) of the patients who presented with pyelo- 2.8%) and urosepsis (1/109; 0.9%) was rare in
nephritis (n ¼ 1325) suffered from a functional or 109 febrile neutropenic adults admitted to the
&&
structural abnormality in the urinary tract. This total emergency department [11 ]. Based on this 3-year
number of patients included 16.2% who were immu- review of 109 patients admitted with febrile neu-
nocompromised and 14.8% who had a long-term tropenia on chemotherapy for different types of
bladder catheter, nephrostomy tube, or ureteral malignancies, the authors conclude that empiric
catheter. The attributable mortality of pyelonephritis antibiotic therapy for febrile neutropenia do not
was 4.1% compared with a crude mortality of 6.5%. need to cover the most common uropathogens.
The attributable mortality was independently associ- The hypothesis is that neutropenia as result of
ated with age more than 75 years, immunosuppres- chemotherapy does not affect IgA-mediated geni-
&
sion, and the presence of a septic shock [10 ]. tourinary mucosal immunity.

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 Febrile urinary tract infections Schneeberger et al.

TREATMENT Long-term follow-up of patients who were

Empirical treatment should be adjusted to local treated for obstructive pyelonephritis showed that
resistance patterns of the most common causative 11% developed a recurrent obstructive pyeloneph-
&

organisms. Defining adequate empiric therapy ritis and one-third a recurrent UTI (33%) [16 ]. Close
becomes increasingly complicated as a result of surveillance and low-dose antibiotic prophylaxis
increasing multidrug-resistant bacteria worldwide. may be desirable for these patients especially when
Besides increasing prevalence of ESBL producing the underlying cause of obstructive pyelonephritis
Enterobacteriaceae, fluoroquinolone resistance is such as a tumour is not treated.
increasingly common with resistance rates of up to The overall mortality was 2.3% (n ¼ 32) in 1363
50%. Wagenlehner et al. performed a randomized, hospitalized patients; an obstruction as a result
double-blind, double-dummy, noninferiority trial of urolithiasis and age over 80 years, systemic
[Assessment of the Safety Profile and Efficacy of cef- inflammatory response syndrome, disseminated
tozolane/tazobactam in Complicated UTI (ASPECT- intravascular coagulation status, disturbance of con-
cUTI)] to compare ceftolozane–tazobactam, a new sciousness, and solitary kidney were associated with
&

cephalosporin combined with a b-lactamase inhibi- mortality [4 ].

tor, with the fluoroquinolon levofloxacin for the In a propensity-matched analysis of 322
treatment of complicated UTIs including pyeloneph- women with a community-onset complicated non-
ritis. They used a composite primary endpoint of obstructive pyelonephritis because of Enterobacter-
microbiological eradication and clinical cure 5–9 iaceae, parameters reflecting more severe infection
days after treatment in a microbiologically modified indicative of early clinical failure (n ¼ 61) com-
intention to treat population, analyzing patients pared with early clinical success (n ¼ 261) were:
with at least one positive urine culture (at least the presence of bacteraemia, increased C-reactive
105 cfu). More than 80% of the study population protein at least 15 mg/dl, ESBL producing Enter-
suffered from pyelonephritis. Ceftolozane–tazobac- obacteriaceae, and increased white blood cell counts
at least 15,000/m3 [22 ].
&

tam was superior to levofloxacin [306 (76.9%) of 398

vs. 275 (68.4%) of 402, 95% confidence interval (CI) Knowing these factors could help clinicians to
&&
2.3–14.6] [12 ]. The found superiority could be earlier recognize treatment failure and adjust treat-
explained by the difference baseline susceptibility, ment strategy where necessary.
which was higher for levofloxacin (26.7%) than for
ceftolozane–tazobactam (2.7%). It is difficult to
Special forms of pyelonephritis
extrapolate these results to an individual country
since fluoroquinolone resistance percentages differ Xanthogranulomatous pyelonephritis is an uncom-
between countries. mon type of pyelonephritis with typical granuloma-
In a retrospective study similar microbiological tous lesions with lipid-filled macrophages.
failure rate (16/83, 19.3% vs. 4/67, 4.0%; weighted Xanthogranulomatous pyelonephritis is known to
hazard ratio 0.99; 95% CI 0.31–3.19) and clinical be more common in women and patients with a
cure rate (hazard ratio 1.05; 95% CI 0.24–4.62) were metabolic syndrome such as obesity or diabetes mel-
found in patients with community-acquired pyelo- litus. In a retrospective study of 35 patients, most
nephritis because of ESBL producing E. coli treated were women (91%) and almost one-third of the cases
with carbapenem and noncarbapenem antibiotics. suffered from diabetes mellitus. In more than two-
The authors of this study indicate that noncarbape- thirds of the patients, urolithiasis was the underlying
nem antibiotics including aminoglycosides and flu- cause. Almost all patients needed surgery, underscor-
oroquinolones are equitable replacements for ing that antibiotic therapy alone may not be enough
&&

carbapenems for treating community-acquired pye- to treat xanthogranulomatous pyelonephritis [23 ].

&
lonephritis [21 ]. However, this may not be the case Emphysematous pyelonephritis is another
in a region with currently high fluoroquinolone special form of pyelonephritis, which is more com-
resistance. In addition, a difference of 15% can be mon in patients with diabetes mellitus. It is caused
considered clinically relevant, whereas the small by gas-producing bacteria and results in a severe
number of patients may explain why the difference necrotizing infection of the renal parenchyma. A
is not statistically significant. study by Kumar found that patients with diabetes
mellitus and emphysematous pyelonephritis
(n ¼ 26) more often needed a nephrectomy and
OUTCOME had poorly controlled blood sugar with an haemo-
Febrile UTI may have far-reaching consequences, globin A1C more than 7.5% compared with patients
including recurrent infections, loss of kidney func- with nonemphysematous pyelonephritis (n ¼ 79).
tion, and death. No difference in mortality was found between

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Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.

Urinary tract infections

diabetic patients with emphysematous and with mellitus. Percutaneous drainage is often needed to
&
‘normal’ pyelonephritis [24 ]. treat both special forms of pyelonephritis.
In a study with 12 patients most patients suf-
fered from diabetes mellitus and only in 50% of the Acknowledgements
cases were positive urine cultures found. Most None.
patients (n ¼ 10) needed percutaneous drainage
&
and subsequent nephrectomy [25 ]. Financial support and sponsorship
Besides diabetes mellitus (68.2%), obstructive None.
uropathy was an important risk factor, which was
present in more than half of the patients (n ¼ 23) in a Conflicts of interest
&&
study by Lu et al. [26 ]. The identified predictors of
S.G. received funding from Nordic Pharma to advise
failure of conservative therapy in patients with
about intravenous fosfomycin.
emphysematous pyelonephritis were need for emer-
gency haemodialysis, the presence of severe hypo-
albuminemia or polymicrobial infections.
REFERENCES AND RECOMMENDED
READING
Papers of particular interest, published within the annual period of review, have
CONCLUSION been highlighted as:
& of special interest
Febrile UTI often remains a clinical diagnosis since && of outstanding interest

positive urine cultures that confirm diagnosis are

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84 www.co-infectiousdiseases.com Volume 29  Number 1  February 2016

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structive acute pyelonephritis. Korean J Intern Med 2015; 30:372–383. Dis 2014; 14:418.
Higher C-reactive protein levels, bacteraemia, presence of ESBLs producing Both diabetes mellitus and obstructive uropathy were important risk factors for
uropathogens, and longer hospitalization were more common in elderly women emphysematous pyelonephritis. Emergency haemodialysis, severe hypoalbumine-
compared with nonelderly women. Besides elderly with nonobstructive pyelone- mia, and polymicrobial infections were associated with failure of conservative
phritis more often present without typical UTI symptoms. therapy in patients with emphysematous pyelonephritis.

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