Nutr Clín Diet Hosp.

2025; 45(1):128-136
Artículo Original DOI: 10.12873/451marola

Risk of hospital malnutrition, inflammatory markers,

and medical nutrition therapy in digestive surgery patient:
a retrospective cohort study from eastern indonesia
Kartika MAROLA1, Agussalim BUKHARI2, Nurpudji A. DAUD2, WARSINGGIH3, AMINUDDIN2, MARNIAR2
1 Clinical Nutrition Medical Speciality Education Program, Faculty of Medicine, Hasanuddin University, Makassar, South Sulawesi, Indonesia.
2 Department of Nutrition, Faculty of Medicine, Hasanuddin University, Makassar, South Sulawesi, Indonesia.
3 Department of Digestive Surgery, Faculty of Medicine, Hasanuddin University, Makassar, South Sulawesi, Indonesia.

Recibido: 24/octubre/2024. Aceptado: 18/diciembre/2024.

ABSTRACT Result: The most common diagnosis is rectal cancer.

Moderate MUST score in 144 patients (40.7%), low MUST
Introduction: The prevalence of hospital malnutrition in
score in 140 patients (39.6%) and high MUST scores in
Indonesian 23.9% - 60.5%. It is important to evaluate nutri-
69 patients (19.5%). 96 patients (27%) received medical
tional status of patients at admission to prevent malnutrition
nutrition therapy, 71% with severe protein energy malnu-
and to identify the need for nutritional therapy. Nutrition, im-
trition diagnosis, 29% with moderate protein energy mal-
munity, and the gastrointestinal tract are closely interrelated.
nutrition diagnosis.
Malnutrition is widely reported in surgical patients, especially
those who have undergone major surgery, and is a particular Conclusion: Malnutrition is common among digestive
risk in patients undergoing surgery for upper gastrointestinal surgery patients and is associated with impaired immune
cancer or colorectal cancer. Studies show a high prevalence of function, as evidenced by hypoalbuminemia and higher NLR
malnutrition or high nutritional risk during hospital admission, in malnourished patients. MUST modified score directly corre-
but this is rarely assessed in the clinical setting, especially for lated with hypoalbuminemia, increased of NLR, and patient
patients undergoing elective surgery. There has been no mortality in RSUP. Dr. Wahidin Sudirohusodo Makassar, South
study on digestive surgery patients receiving medical nutri- Sulawesi.
tional therapy (MNT).
Method: A retrospective cohort study was conducted, in- KEYWORDS
cluding 353 digestive surgery patients who were admitted be-
Inflammatory status, nutritional assessment, retrospec-
tween January 2022 and January 2024. This study used med-
tive studies, immune function, surgical complications, clini-
ical record data with a total sample of digestive surgery patients.
cal recovery.
Nutritional status was assessed using the Malnutrition Universal
Screening Tool (MUST). This study identified the MUST modified
scores of digestive surgery patients, with albumin, Neutrophil- INTRODUCTION
to-Lymphocyte Ratio (NLR), and Total Lymphocyte Count (TLC) Hospital Malnutrition often under-recognized condition
values. Statistical analyses were performed using chi-square among hospitalized patients in Asia. Poor nutritional status is
tests for categorical variables and t-tests or Mann-Whitney U associated with an increased risk of adverse clinical out-
tests for continuous variables, with a p-value of <0.05 consid- comes, including infectious and non-infectious complications,
ered statistically significant. increased length of stay and increased mortality1.

The prevalence of malnutrition in Indonesian hospitals

varies between 23.9% and 60.5%. This may be due to vari-
Correspondencia: ability in the patient population as well as the parameters
Agussalim Bukhari used. Malnutrition in hospitals can be caused by individual
[email protected] and/or institutional factors2.

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The prevalence of malnutrition in hospitals varies according instance, Enteral Nutrition (EN) is preferred for patients who
to the patient population, screening and assessment methods, can tolerate it, as it maintains gut integrity and function. For
and hospital setting; however, it is generally estimated that 20 patients unable to use their gastrointestinal tract, Parenteral
to 50% of hospitalized patients are malnourished on admis- Nutrition (PN) provides essential nutrients intravenously. MNT
sion, and approximately one-third of patients who are not mal- is tailored to each patient’s needs, ensuring they receive the
nourished on admission may become malnourished during right balance of macronutrients and micronutrients9.
hospitalization. Certain patient populations, including surgical
There has been no study on hospital malnutrition, especially
patients, critically ill patients, geriatrics and cancer patients are
digestive surgery patients at RSUP. Dr. Wahidin Sudirohusodo,
known to be particularly susceptible to malnutrition3.
so the novel of this study is to identify problems related to hos-
Disease-related malnutrition is a common condition but is pital malnutrition in digestive surgery patients at RSUP. Dr.
often underestimated or even unrecognized in chronic dis- Wahidin Sudirohusodo Makassar for the period January 2022 -
eases. Malnutrition negatively impacts clinical outcomes and January 2024.
increases mortality through impaired wound healing, in-
creased rates of infection and other complications, increased MATERIAL AND METHODS
duration and intensity of treatment, and increased length of
Study Design and Participants
hospital stay4.
This study utilized a retrospective cohort design to assess
Malnutrition is widely reported in surgical patients, espe- the prevalence of malnutrition and its association with clinical
cially those who have undergone major surgery, and is par- outcomes in digestive surgery patients.
ticularly at risk in patients undergoing surgery for upper gas-
trointestinal cancer or colorectal cancer. Pre-operative This study used medical record data with a total sample of
malnutrition has been shown to increase length of hospital digestive surgery patients. The population of this study were
stay, higher rates of infection and mortality at the surgical inpatients at the RSUP. Dr. Wahidin Sudirohusodo Makassar
site, and is associated with higher post-operative complica- period January 2022 - January 2024 according to the inclu-
tions, increased costs, poorer quality of life and lower survival sion criteria. The sample size in this study was determined us-
rates. Studies show a high prevalence of malnutrition or high ing the total sampling method.
nutritional risk during hospital admission, but this is rarely as- Inclusion criteria were patients diagnosed with digestive
sessed in the clinical setting, especially for patients who will surgery disease, aged > 18 years, hospitalized ³ 7 days.
undergo elective surgery5. Patients were excluded if they had incomplete medical records
Malnutrition is common in surgical patients and between or were above the age of 59, and hospitalized < 7 days.
16 - 67% of surgical patients are malnourished before sur-
gery. Estimates vary depending on the population examined Nutritional Assessment
and the diagnostic instruments used6. Malnutrition risk was evaluated using the Malnutrition
Approximately 44% of all patients hospitalized for elective Universal Screening Tool (MUST). MUST applied at Wahidin
surgical procedures are at risk of malnutrition. However, this Sudirohusodo Hospital:
prevalence varies depending on the criteria for malnutrition 1. Adult patients with BMI score with standard:
and the screening tools used. In surgical patients, preopera- a. BMI 20 (>30 Obese) :0
tive malnutrition is associated with an increased risk of post- b. BMI 18, - 20 :1
operative complications, increased mortality and medical c. BMI < 18,5 :2
costs, and longer hospital stays7.
2. Nutritional status classification for children with graphic
Patients undergoing gastrointestinal surgery have de- standard CDC, weight for height:
creased oral intake, tumor cachexia, impaired absorption due a. >90 – 110% :0
to intestinal obstruction, or reduced intestinal length which af- b. 70–90% :1
fects their nutritional status. Other surgical parameters such
c. <70% :2
as preoperative sepsis, American Society of Anesthesiology
(ASA) score of more than 3, emergency surgery, open sur- 3. Score of unplanned weight loss in the last 3-6 months:
gery, long duration of surgery, and massive intraoperative a. Weight loss <5% :0
blood loss contribute to poor postoperative outcomes. In ad- b. Weight loss 5-10% :1
dition, low socioeconomic status, Indian customs, restrictions c. Weight loss>10% :2
on intake of certain foods pose additional risks8.
4. Nutritional intake score for acute patients:
Medical Nutritional Therapy (MNT) involves the use of spe- a. Nutritional intake>5 days :0
cific nutritional interventions to manage medical conditions. For b. No nutritional intake>5 days :2

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RISK OF HOSPITAL MALNUTRITION, INFLAMMATORY MARKERS, AND MEDICAL NUTRITION THERAPY IN DIGESTIVE SURGERY PATIENT: A RETROSPECTIVE COHORT STUDY...

5. If the patient cannot be weighed, then do upper arm cir- Statistical Analysis
cumference measurement, upper arm circumference
Descriptive statistics were used to summarize patient
classification for adults:
characteristics. Categorical variables were analysed using
a. >85% :0 chi-square tests, while continuous variables were analysed
b. 70.1 – 84.9% :1 using t-tests or Mann-Whitney U tests, depending on the
c. <70% :2 distribution of the data. A p-value of <0.05 was considered
statistically significant.
TOTAL SCORES =
Interpretation of scores:
RESULT
• Low risk (0) = Monitoring after 7 days.
This study involved 353 patients. The study obtaining ethi-
• Medium risk (1 – 2) = Monitoring intake for 3 days,
cal approval from the Health Research Ethics Committee of
continued every 7 days if no change. Treatment plan
the Faculty of Medicine, Hasanuddin University with number:
can be changed as needed.
313/UN4.6.4.5.31/PP36/2024.
• High risk (³3) = Collaborate with Nutrition Support
Team. This study involved 353 samples with mean age 43.4
± 11 years old. Gender was dominated by 212 males (60%)
and 141 females (40%). The highest MST score was a mod-
Data Collection
erate MST score of 144 patients (40.7%), a low MST score
Data on patient demographics, nutritional status, inflam- of 140 patients (39.6%) and a high MST score of 69 pa-
matory markers, length of stay, and mortality were collected tients (19.5%). There were 50 patients who died during
from the hospital’s medical records. The primary outcomes hospitalization (14%) and 303 patients survived (86%).
measured were LOS, inflammatory response (Albumin, NLR, 27% patients with clinical nutrition collaboration, the most
TLC), and mortality. Data were analysed to determine the cor- diagnoses 71% with severe protein energy malnutrition,
relation between malnutrition risk and these outcomes. and 29% with moderate protein energy malnutrition.

Figure 1. Flow chart of trail

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Table 1. Basic characteristics of patients Tabla 2. Most common diagnoses in subjects

Basic Characteristics n % Digestive surgery patients n %

Men 212 60 Rectal cancer 38 24

Sex
Woman 141 40 Colon cancer 34 21

Age 18 – 59 y.o 43.4 ±11 Intra-abdominal tumor 15 9.3

No education 37 10,5 Choledocholithiasis 13 8

Elementary 41 11,6 Cholelithiasis 12 7.4

Education
Secondary 55 15,5 Hepatoma 12 7.4
status
High School 150 42,4 Rectal tumor 12 7.4

Bachelor 70 19,8 Colon tumor 11 7.4

Married 301 85,2 Colorectal cancer 8 5

Marital
Unmarried 42 11,8 GIST 6 3.7
Status
Widowed 10 2,8

Employee 213 60,5

Occupation DISCUSSION
Status
Unemployed 140 39,5 The aim of this study was to determine the association of
the hospital malnutrition risk score, Malnutrition Universal
Low risk 140 39,6
Screening Tools (MUST) modified score, with inflammatory
MUST
modified Moderate risk 144 40,7 biomarkers, length of hospitalization, mortality, MNT and
Score non MNT.
High risk 69 19,5
This study found that 60.4% of digestive surgery patients
Yes 50 14 were at moderate and high risk of malnutrition.
Mortality
Surgical trauma elicits a series of events that generate an
No 303 86
immune response with activation of the cytokine cascade in
Medical Yes 96 27 the postoperative period. Cytokines play an important role in
Nutrition regulating the inflammatory response at the site of injury,
Therapy No 257 73 thereby facilitating the wound healing process. However, ex-
cessive cytokine production can have systemic consequences
Medical Moderate PEM 28 29
Nutrition
leading to postoperative complications and death10.
Diagnosis Severe PEM 68 71 Malnutrition is a major problem in the gastrointestinal peri-
operative setting, as only 40% of malnourished patients are
ultimately treated. Malnutrition can be defined as a condition
The table 3 shows a significant MST modified score and al- that occurs when the body does not receive enough essential
bumin level (p = 0.000), MST scores and NLR (P = 0.027). nutrients to maintain healthy growth and function. This can
result from insufficient nutrient intake and/or the inability to
The table 5 shows a significant MST modified score and
absorb nutrients properly, or an unbalanced diet. Malnutrition
mortality rates (P= 0.006).
has been associated with poor clinical outcomes, as it has
The table 7 shows a significant MST modified score, MNT been shown that malnourished patients have a relative mor-
and non MNT, p = 0.000. tality risk of 1.6-1.9 and remain hospitalized for 1.5-1.7 times
longer. Thus, up to 80% of patients who present with com-
The table 8 shows a higher mortality rate in patients who
promised nutritional status on admission will further deterio-
received medical nutrition therapy. This may be influenced
rate if no nutritional regimen is provided11.
by the diagnosis, severity of the disease, complications,
and the length of time the patient was consulted to clinical It has been observed that patients who are malnourished
nutrition. at the time of admission also appear to be at a higher risk of

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RISK OF HOSPITAL MALNUTRITION, INFLAMMATORY MARKERS, AND MEDICAL NUTRITION THERAPY IN DIGESTIVE SURGERY PATIENT: A RETROSPECTIVE COHORT STUDY...

Table 3. Correlation of MUST modified score and inflammatory biomarkers

MUST Modification Score

Inflammation biomarkers Total p value
Low Moderate High

n 51 34 9 94
Normal
% 54.3% 36.2% 9.6% 100%

n 44 39 21 104
Mild hypoalbuminemia
% 42.3% 37.5% 20.2% 100%
Albumin 0.004*
Moderate n 22 39 22 83
hypoalbuminemia % 26.5% 47% 26.5% 100%

Severe n 23 32 17 72
hypoalbuminemia % 31.9% 44.4% 23.6% 100%

n 73 66 27 166
Normal
% 44% 39.8% 16.3% 100%

Mild depletion n 20 22 16 58
of immunity % 34.5% 37.9% 27.6% 100%
TLC 0.464
Moderate depletion n 22 24 14 60
of immunity % 36.7% 40% 23.3% 100%

Severe depletion n 25 32 12 69
of immunity % 36.2% 46.4% 17.4% 100%

n 48 44 11 103
Normal
% 46.6% 42.7% 10.7% 100%

n 34 31 28 93
Mild increase of NLR
% 36.6% 33.3% 30.1% 100%
NLR 0.028*
n 24 28 9 61
Moderate increase of
% 39.3% 45.9% 14.8% 100%

n 34 41 21 96
Severe increase of
% 35.4% 42.7% 21.9% 100%

Values are n (%). Significant if p<0.05.

Comparison was performed using Chi square test.

poor nutritional intake during hospitalization. Surgery can ex- response is characterized by a period of negative nitrogen
acerbate malnutrition through a systemic inflammatory re- balance leading to increased muscle and fat breakdown,
sponse, which in turn increases metabolic activity, increases sympathetic nervous system stimulation and insulin resist-
energy consumption, impairs organ function, and compro- ance. Increased metabolic activity leads to an increase in
mises immunity. In addition, undernourished patients may de- body temperature and respiratory rate: in patients undergo-
velop infections at the surgical site; therefore, they have a
ing elective surgery, there can be a 10-15% increase in basal
greater chance of morbidity11.
energy expenditure and in the absence of complications, it
The metabolic response to surgery triggers various meta- can take 3-8 days to transition from catabolism to anabolism.
bolic and endocrine changes and the perioperative catabolic Therefore, it is common for patients to experience weight

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Table 4. Correlation of MUST modified score and length of stay (LOS) in hospital

MUST Modification Score

LOS Total P value
Low Moderate High

n 39 36 19 94
7-14 days
% 41.5% 38.3% 20.2% 100%
LOS 0.847
n 101 108 50 259
> 14 days
% 39% 41.7% 19.3% 100%

Table 5. Correlation of MUST modified score and mortality

MUST Modification Score

Mortality Total P value
Low Moderate High

n 10 27 14 51
Yes
% 19.6% 52.9% 27.5% 100%
Mortality 0.006*
n 130 117 55 302
No
% 43% 38.7% 18.2% 100%

Table 6. Length of stay (LOS) and length of consulted to clinical nutrition

Mean SD Median Minimum Maximum

LOS 20.2 8.9 18 7 53

Length of consulted 7.5 7.8 5 0 30

Table 7. Assosiation of MUST modified score and Medical Nutrition Therapy (MNT), Non Medical Nutrition Therapy (Non - MNT)

Nutrion therapy
MUST Modified Score Total p value
MNT Non MNT

n 20 120 140
Low
% 21.1% 46.5% 39.7%

n 46 98 144
MUST Moderate 0.000*
% 48.4% 38% 40.8%

n 29 40 69
High
% 30.5% 15.5% 19.5%

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Table 8. Analysis of MUST modified score, mortality rates, and MNT

MNT
Jumlah Nilai p
With MNT Non MNT

n 27 23 50
Death
% 28.4% 8.9% 14.2%
Outcome 0.000*
n 68 235 303
Survive
% 71.6% 91.1% 85.8%

loss after gastrointestinal surgery. It has been found that new data suggest that increased catabolism is the more fre-
50% of patients lose more than 10% of their body weight a quent reason, hypoalbuminemia in chronic diseases, is asso-
year after upper gastrointestinal surgery and half of patients ciated with decreased albumin synthesis due to wasting and
undergoing colorectal surgery fail to reach their calorie in- cachexia. The mechanism that causes hypoalbuminemia in
take targets, and almost no patients reach their protein in- acute conditions differs from that in chronic diseases because
take targets after hospital discharge12. capillary leakage into the interstitial space due to inflamma-
tory processes is the main source of hypoalbuminemia in
This study found that 73.4% of digestive surgery patients acute conditions. In addition, reduced synthesis, dilution of
were admitted with hypoalbuminemia. 44.4% of patients with blood due to fluid administration, renal and intestinal losses
moderate MUST modified score had severe hypoalbuminemia. due to congestion, and increased catabolism also play a role6.
Hypoalbuminemia is prevalent in hospitalized and critically Historically, serum albumin concentration was considered a
ill patients. Critical illness is associated with hypoalbuminemia marker of nutritional status and clinicians monitored albumin
through various mechanisms. It can alter the distribution of concentration in patients during hospital stays. It was based
albumin between the intravascular and extravascular com- on the pathophysiological rationale that albumin concentra-
partments resulting in decreased albumin synthesis and in- tions reflect circulating proteins in plasma, with lower con-
creased albumin degradation and clearance. The reduction in centrations indicating nutritional deficiencies13.
albumin synthesis results from increased transcription of
genes for positive acute phase proteins (such as C-reactive In this study, 71% of digestive surgery patients were ad-
protein) and decreased transcription rate of albumin messen- mitted to the hospital with increased NLR. 46% of patients
ger RNA. However, the increased degradation and clearance with a moderate MUST modified score had a moderate in-
of albumin is due to an increase in capillary leakage, which is crease in NLR.
influenced by several cytokines in the inflammatory process
such as TNF-alpha, interleukin-6, and prostaglandins8. Neutrophils are one of the first responders at sites of in-
fection and injury and as such are powerful mediators of
Plasma albumin has three main functions: osmotic, trans- acute inflammation14.
port, and nutritional, and accounts for more than 75-80% of
the total plasma osmotic pressure (25 mmHg). During physi- The neutrophil to lymphocyte ratio, calculated as a simple
ological stress, a decrease in serum albumin levels to hypoal- ratio between neutrophil and lymphocyte counts measured in
buminemia levels leads to a decrease in oncotic pressure, peripheral blood, is a biomarker that reflects the balance be-
which in turn causes interstitial oedema6. tween two aspects of the immune system: acute and chronic
inflammation (as indicated by neutrophil counts) and adaptive
Albumin, a very important protein, transports hormones, immunity (lymphocyte counts). In cancer patients, higher NLR
fatty acids and exogenous drugs and regulates plasma on- has been associated with poor prognosis. Nutrition, immunity,
cotic pressure. As albumin levels decrease during injury and inflammation, and cancer are closely linked, which in turn can
infection, albumin is referred to as a negative active phase affect the survival prognosis of cancer patients. Gastric cancer
protein. The maintenance protein called serum albumin is patients often experience symptoms such as weight loss, hy-
rapidly upregulated by inflammatory signals. Low serum al- poproteinemia, anemia and malabsorption, which are associ-
bumin levels are mostly caused by inflammatory conditions, ated with inhibition of humoral and cellular immune function,
by high levels of the cytokine’s interleukin-6 (IL-6) and tumor altered inflammatory response and wound healing. In radical
necrosis factor-alpha (TNF-alpha). A common finding in both distal gastrectomy, a large part of the stomach, including tu-
acute and chronic diseases is hypoalbuminemia. Although mor and normal tissue, is removed, resulting in malnutrition,

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 NUTRICIÓN CLÍNICA Y DIETÉTICA HOSPITALARIA

which greatly increases the risk of tumor recurrence. Surgical sess the risk of malnutrition and was applied at the RSUP. Dr.
trauma can inhibit the body’s fluid and cellular immune func- Wahidin Sudirohusodo Makassar.
tion and stimulate the body to produce inflammation and trau-
This study has limitations that need to be considered. This
matic changes, resulting in poor nutrition6.
study used an observational design, which means that the
The neutrophil to lymphocyte ratio (NLR) has been exten- findings are correlational and cannot be used to determine di-
sively evaluated and shown to be associated with outcomes rect correlation. Other factors may influence the results so in-
and predict disease course among patients with various med- terventional studies are needed for further confirmation.
ical conditions including ischemic stroke, cerebral hemor-
rhage, major cardiac events, as well as sepsis and infectious CONCLUSSION
diseases. Moreover, in cancer patients, higher NLR has been
In conclusion, this study underscores the high prevalence
associated with poor prognosis. This adverse association may
of hospital malnutrition among digestive surgery patients and
reflect the contribution of severe inflammation and poor im-
its association with weakened immune function. MUST modi-
mune function to the development of these diseases15.
fied score directly correlated with hypoalbuminemia, in-
Recent studies have demonstrated the usefulness of NLR in creased of NLR, and patient mortality in RSUP. Dr. Wahidin
assessing the extent of the systemic inflammatory response. Sudirohusodo Makassar, South Sulawesi. The findings high-
Lee et al. reported that elevated NLR can predict length of light the importance of early nutritional screening and inter-
hospital stay in patients undergoing surgery for severe chole- vention in this population. Addressing malnutrition through
cystitis, while Xie et al. applied NLR to predict gastrointestinal timely and targeted nutritional therapy may improve immune
resection in inguinal hernia caused by ischemia16. function and reduce the risk of complications, ultimately con-
tributing to better outcomes for digestive surgery patients.
This study revealed that 53% of digestive surgery patients
were admitted with immune depletion. At moderate MUST
ACKNOWLEDGEMENTS
modified scores, 46.4% of patients had severe immune de-
pletion. Indicating that nutrition affects immunity. The author would like to express gratitude to all teachers
at the Nutrition Department, Faculty of Medicine, Hasanuddin
Both of nutritional status and systemic inflammatory re- University
sponse have been shown to play an important role in the de-
velopment and progression of various diseases and the sur-
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