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Effect of Malnutrition Assessed by Comprehensive Nutritional Screening Tool on In-Hospital Mortality after Surgery for Gastrointestinal Perforation
Surg Metab Nutr 2021;12(1):1-6
Published online June 30, 2021
© 2021 The Korean Society of Surgical Metabolism and Nutrition.

Seung-Young Oh, M.D., Ph.D.1,2, Hannah Lee, M.D., Ph.D.1,3, Ho Geol Ryu, M.D., Ph.D.1,3, Hyuk-Joon Lee, M.D., Ph.D.2

1Critical Care Center, Seoul National University Hospital, Seoul, 2Department of Surgery, Seoul National University College of Medicine, Seoul, 3Department of Anesthesia and Pain Medicine, Seoul National University College of Medicine, Seoul, Korea
Correspondence to: Seung-Young Oh
E-mail ORCID

This study was supported by a grant from the Korean Society of Surgical Metabolism and Nutrition and JW-pharma 2018.
Received December 19, 2020; Revised January 22, 2021; Accepted February 10, 2021.
This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Purpose: This study examined the effects of malnutrition on in-hospital mortality after surgery for gastrointestinal (GI) perforation.
Materials and Methods: Patients who underwent surgery for GI perforation between 2010 and 2017 were analyzed retrospectively. The preoperative nutritional status was assessed by the Seoul National University Hospital-Nutrition Screening Index, a tool that comprehensively evaluates 11 factors that reflect the nutritional status. The risk factors for in-hospital mortality after surgery for GI perforation were evaluated by univariate and multivariate analyses.
Results: Four hundred and eighty-nine patients were divided into two groups: 439 patients in the survival group and 50 patients in the in-hospital mortality group. The risk of malnutrition was higher (93.6% vs. 65.9%, P<0.001) in the in-hospital mortality group than in the survival group. The preoperative albumin level was lower, and the blood urea nitrogen level was higher in the in-hospital mortality group than in the survival group. Emergency surgery, lymphoma as a cause of perforation, and fecal-contaminated ascites were also identified as factors associated with in-hospital mortality. Multivariate analyses demonstrated that a high risk of malnutrition (HR=5.71, 95% CI 1.38~26.02, P=0.017), lymphoma as a cause of perforation (HR=4.12, 95% CI 1.17~14.51, P=0.028), low preoperative albumin (HR=4.77, 95% CI 2.35~9.69, P<0.001), and high preoperative BUN (HR=1.03, 95% CI 1.01~1.05, P=0.001) had significant effects on the in-hospital mortality after surgery for GI perforation.
Conclusion: A high risk of malnutrition assessed by the composite index was associated with in-hospital mortality after surgery for a GI perforation.
Keywords : Gastrointestinal perforation, In-hospital mortality, Nutritional risk, Nutrition screening

Gastrointestinal (GI) perforation is a typical disease requiring urgent surgical treatment. It is a life-threatening condition, which reportedly has a mortality rate of 20% despite advances in surgical skill.[1,2] Clinical outcomes after surgery for GI perforation are known to be affected by various factors such as cause of perforation, underlying comorbidities, operative findings, and nutritional status.

Hypoalbuminemia is a known risk factor for in-hospital mortality after surgery for GI perforation.[3,4] It is a representative biochemical parameter that is considered to reflect nutritional status; however, it is reported that hypoalbuminemia is not suitable for accurate nutritional assessment because it is easily affected by an acute phase response in critically ill patients.[5,6] According to a study conducted by Putwatana et al. [7] a hypoalbuminemia level of less than 3.5 g/dL is a risk factor for complications after major abdominal surgery, but hypoalbuminemia does not properly reflect a patient’s recent nutritional status because it can fluctuate depending on changes other than nutritional status such as water distribution or accumulation and disease statuses. Therefore, to demonstrate whether nutritional status affects clinical prognosis after surgery for GI perforation, the result of a comprehensive nutritional assessment, not that of a single parameter, should be included in the analysis.

This study aimed to evaluate the effect of malnutrition on in-hospital mortality after surgery for GI perforation and emphasized the importance of nutritional support in patients at risk of GI perforation.


This was a retrospective cohort study whose protocol was approved by the institutional review board (IRB) of Seoul National University Hospital (SNUH) (IRB No. 1711-109-901). All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation and with the Helsinki Declaration of 1964 and later versions and adhered to the relevant guidelines.

This study was performed on adult patients (age ≥18 years) who underwent gastrointestinal perforation at SNUH between 2013 and 2017. Data collection was performed by a retrospective review of electronic medical records.

Nutritional status was evaluated using the Seoul National University Hospital-Nutrition Screening Index (SNUH-NSI) developed by SNUH. SNUH-NSI consists of body weight change, appetite status, digestive symptoms, most recent laboratory results including serum levels of albumin, total cholesterol, hemoglobin, C-reactive protein (CRP) and total lymphocyte count within 2 weeks prior to hospitalization, age, body mass index (BMI), and diet type on the first day of hospitalization. Each factor is divided into three stages, R1, R2, and R3 according to the degree to which the severity of malnutrition is reflected. After combining all factors, the patients were finally classified into three groups: high-risk, moderate-risk, and low-risk groups. Initial nutritional assessment using SNUH-NSI was performed within 24 hours after admission for all hospitalized patients admitted to the SNUH (Table 1). This tool was validated by comparing the results of nutritional status assessment with those obtained from the Patient Generated Subjective Global Assessment (PG-SGA) from 174 patients who underwent gastrectomy.[8]

Seoul National University Hospital-Nutrition Screening Index (SNUH-NSI)

R1 R2 R3
Appetite Bad - Normal/good
Change of weight Yes - No
Difficulty in disgesting - Yes No
Diet type Fluid diet Soft blended diet of NPO Normal regular diet
Serum-albumin (g/dL) <2.8 2.8~3.3 ≥3.3
Serum-cholesterol (mg/dL) - <130 ≥130
Total lymphocyte count (cells/mm3) <800 800~1,500 ≥1,500
Hemoglobin (g/dL) - Male <13.0 Male ≥13.0
Female <12.0 Female ≥12.0
C-reactive protein (mg/dL) - >1 ≤1
BMI (kg/m2) <18 or ≥ 25 18~25
Age (years) - >75 ≤75
Status of malnutrition ∙ P1; High-risk group of malnutrition; (more than 2 of R1) or (1 of R1 and more than 2 of R2)
∙ P2; Medium-risk group of malnutrition; (1 of R1) or (more than 2 of R2)
∙ P3; Low-risk group of malnutrition; the others

BMI = body mass index; R = risk factor; NPO = nothing by mouth.

Data were collected regarding (1) patient demographics (age, sex, BMI, and underlying comorbidities), (2) preoperative factors (nutritional status, and laboratory test results), and (3) operation-related factors (type of operation, site of perforation, cause of perforation, and character of ascites).

While comparing patient characteristics, a P-value<0.05 was considered statistically significant. Statistical analyses were performed using IBM SPSS Statistics 22 (IBM Cor. Released 2013. IBM SPSS Statistics for Windows, Version 22.0. Armonk, NY: IBM Corp.).


Among the 489 included patients, 50 patients were classified into the in-hospital mortality group and the others were classified into the survival group. There were no significant differences between the two groups in age, sex, BMI, and several comorbidities including hypertension, diabetes mellitus, coronary artery disease, and cerebrovascular disease. The in-hospital mortality group showed significantly higher rates of chronic liver disease (9 [18.0%] vs. 38 [8.7%], P=0.035) and chronic kidney disease (11 [22.4%] vs. 38 [8.7%], P=0.003) than the survival group (Table 2).

Patient demographics

Survival (n=439) In-hospital mortality (n=50) P-value
Age (years) 60.4±17.0 65.1±14.1 0.057
Sex (M:F) 261:178 26:24 0.311
BMI (kg/m2) 21.8±3.5 21.2±3.6 0.228
Hypertension 178 (40.6%) 23 (46.0%) 0.466
Diabetes 71 (16.2%) 11 (22.0%) 0.300
Chronic liver disease 38 (8.7%) 9 (18.0%) 0.035
Chronic kidney disease 38 (8.7%) 11 (22.4%) 0.003
Coronary artery disease 27 (6.2%) 6 (12.0%) 0.119
Cerebrovascular disease 18 (4.1%) 4 (8.0%) 0.266

Data are presented as mean±SD, or number (%).

BMI = body mass index.

Nutritional status was poorer and the rate of high risk of malnutrition was higher (93.6% vs. 65.9%, P<0.001) in the in-hospital mortality group than in the survival group. Regarding preoperative laboratory tests, albumin (2.5±0.6 vs. 3.2±0.7, P<0.001) and total protein (4.9±1.3 vs. 6.1±2.4, P=0.001) levels were lower, and levels of blood urea nitrogen (35.1±20.1 vs. 22.1±15.3, P<0.001) and creatinine (1.83±1.46 vs. 1.27±1.27, P=0.004) were higher in the in-hospital mortality group than in the survival group (Table 3).

Preoperative factors

Survival (n=439) In-hospital mortality (n=50) P-value
Nutritional risk < 0.001
Low risk 30 (6.9%) 0 (0.0%)
Moderate risk 119 (27.2%) 3 (6.4%)
High risk 288 (65.9%) 44 (93.6%) < 0.001
Albumin (g/dL) 3.2±0.7 2.5±0.6 < 0.001
Total protein (g/dL) 6.1±2.4 4.9±1.3 0.001
Blood urea nitrogen (mg/dL) 22.1±15.3 35.1±20.1 < 0.001
Creatinine (mg/dL) 1.27±1.27 1.83±1.46 0.004
C-reactive protein (mg/dL) 13.1±12.1 14.9±11.1 0.349

Data are presented as mean±SD, or number (%).

As for operation related factors, emergency operation (P=0.018), lymphoma as a cause of GI perforation (P<0.001), and fecal-contaminated ascites (P=0.014) were identified as associated factors with in-hospital mortality group (Table 4).

Operation related factors

Survival (n=439) In-hospital mortality (n=50) P-value
Type 0.018
Elective 104 (95.4%) 5 (4.6%)
Emergency 311 (87.4%) 45 (12.6%)
Perforation site 0.006
Stomach 37 (94.9%) 2 (5.1%)
Duodenum 53 (93.0%) 4 (7.0%)
Small intestine 99 (82.5%) 21 (17.5%)
Appendix 43 (100.0%) 0 (0.0%)
Colon and rectum 200 (90.9%) 20 (9.1%)
Perforation cause
Inflammatory bowel disease 16 (3.6%) 0 (0.0%) 0.391
Malignancy 112 (25.8%) 18 (13.8%) 0.102
Lymphoma 10 (2.3%) 6 (12.0%) <0.001
Ascites 0.021
Clear 195 (92.4%) 16 (7.6%)
Turbid 184 (90.2%) 20 (9.8%)
Fecal contaminated 60 (81.1%) 14 (18.9%) 0.014
Stoma formation 178 (40.7%) 27 (54.0%) 0.072

Data are presented as number (%).

In the multivariate analysis, a high risk of malnutrition, lymphoma as a cause of GI perforation, preoperative hypoalbuminemia less than 2.8 g/dL, and high preoperative BUN were identified as risk factors for in-hospital mortality after surgery for GI perforation. In particular, in the case of patients with a high risk of malnutrition, it was confirmed that the hazard ratio was more than 5 times higher (HR=5.714, 95% CI 1.381~26.019, P=0.017) than that in those who are not at a high risk of malnutrition (Table 5). Moreover, in the receiver-operating characteristic (ROC) curve analysis using preoperative albumin, a representative factor reflecting nutritional status, the area under the curve was 0.790 (95% CI 0.726~0.852) (Figure 1).

Risk factors for in-hospital mortality after surgery for gastrointestinal perforation

P-value HR 95% CI
High risk of malnutrition 0.017 5.714 1.381~26.019
Lymphoma 0.028 4.115 1.167~14.509
Hypoalbuminemia <2.8 g/dL <0.001 4.769 2.347~9.690
Blood urea nitrogen (mg/dL) 0.001 1.028 1.011~1.045

Fig. 1. Receiver operating characteristic curve for prediction of in-hospital mortality after surgery for gastrointestinal perforation according to preoperative albumin level.

Factors known as risk factors in the clinical course of peritonitis include age, sex, cause of peritonitis, severity of peritonitis, and characteristics of ascites. Mannheim et al. created a scoring system that predicts the prognosis of peritonitis by considering the degree of influence of each factor. However, based on the results of several studies conducted after the Mannheim Prognostic Index, unstable hemodynamic status, preoperative anemia, high CRP levels, and some of the parameters used to assess nutritional status were identified as new risk factors for mortality due to peritonitis.[3,4]

Low preoperative albumin and cholesterol levels, known to reflect nutritional status, are the representative risk factors for in-hospital mortality after surgery for GI perforation.[3,4] It is known that more energy than usual is required for recovery after surgery,[9,10] but in most cases of surgery due to GI perforation, patients should fast for a few days. Even if adequate parenteral nutrition is performed during this period, the nutritional status of the patient is inevitably deteriorated, so the baseline nutritional status is very important to withstand this period. In this study, it was demonstrated that a high risk of malnutrition assessed using a composite tool, as well as preoperative hypoalbuminemia, is a risk factor for in-hospital mortality after surgery for GI perforation, and its hazard ratio was five times higher than that of each nutritional parameter.

SNUH-NSI is a nutrition screening tool for screening patients with a high risk of malnutrition. To assess the nutritional status of a patient, a comprehensive evaluation of various parameters such as biochemical, clinical, and dietary parameters is required rather than using a single parameter.[11]Comprehensive nutritional assessment tools include the Subjective Global Assessment (SGA) and Patient Generated-SGA (PG-SGA); however, it is difficult to select patients with malnutrition by conducting an in-depth nutritional assessment for all hospitalized patients.[12] For this reason, the Nutrition Risk Screening-2002 (NRS-2002), a tool that selects patients at risk of malnutrition through nutrition screening for many patients in a short time, was developed.[13] SNUH-NSI is also a type of nutrition screening tool, and all parameters except biochemical parameters should be entered during the history taking process at the time of hospitalization, and are automatically calculated and reported using these information. Therefore, it is efficient in terms of time required.

Lymphoma as a cause of perforation is another well-known risk factor for in-hospital mortality after surgery for GI perforation. GI perforation in lymphoma is a common complication. It is caused by the involvement of the tumor itself, but can also be caused by rapid tumor necrosis and tissue impairment after chemotherapy.[14-17] In the case of GI perforation after chemotherapy for lymphoma, it has been reported that the mortality rate is quite high because of the immunocompromised condition of the patient.[18,19] For this reason, preemptive surgical resection of the involved site before initiation of chemotherapy is considered in selected cases.

This study has several limitations. First, since GI perforation requires surgical treatment as soon as possible after diagnosis, there is no time for nutritional support before surgery. For the results of this study to be of great practical significance, preoperative intervention, for example, correction of hypoalbuminemia or transfusion, to improve nutritional status for a short period preoperatively, should have a positive effect on clinical outcomes. Second, since this was a retrospective study, there were missing data in some of the preoperative laboratory tests and operation-related factors. Moreover, there are many patients whose parameters already known to affect clinical prognosis, such as preoperative lactate level, were not measured. Therefore, such variables could not be included in the analysis.

In conclusion, a high risk of malnutrition assessed by composite index is significantly associated with in-hospital mortality after surgery for GI perforation. Prospective studies on whether correction of nutritional parameters during a short interval from diagnosis to emergency surgery can improve clinical prognosis are needed.


The authors of this manuscript have no conflicts of interest to disclose.

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