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Impact of preoperative nutritional status on surgical outcomes in patients with pediatric gastrointestinal surgery

Background Malnutrition has a high incidence among pediatric surgical patients and contributes to increased risks of postoperative complications and extended hospital stays. Purpose The present study aimed to determine the influence of preoperative nutritional status on the postoperative outcomes of pediatric patients who underwent elective gastrointestinal (GI) surgery. Methods This prospective observational study was conducted at Cairo University Specialized Pediatric Hospital. According to the designated inclusion criteria, 75 surgical cases of both sexes were included. A structured questionnaire was developed and administered. This questionnaire included 3 main sections: demographic data and nutritional status parameters at admission and discharge. Pre- and postoperative nutritional statuses were compared. Results According to both the subjective global nutritional assessment and STRONGKIDS score Questioner, more than 60% of patients in the upper GI patient group were at risk of malnutrition. Wasting status was most common in the upper GI patient group (67%; vs. 39.1% in the lower GI group). Underweight status was more common in the hepatobiliary and upper GI patient groups (nearly 50% for each group) than in the lower GI group (30.4%). On the other hand, stunted patients had a higher incidence of complications and a prolonged hospital stay (P=0.003 and P=0.037, respectively), while underweight lower GI patients experienced a prolonged hospital stay (P=0.02). A higher proportion of patients with preoperative anemia than those without preoperative anemia required a blood transfusion (P=0.003). Conclusion Nutritional assessment is a crucial component of pediatric surgical patient management. Both underweight and wasting statuses were more common among hepatobiliary and upper GI patients. Postoperative complications and a long hospital stay were more common among stunted patients.


Introduction
Nutrition is crucial to maintain normal growth, physiologic ho meostasis, and substantial resistance to infection. 1) Malnutrition is a highlyoccurring incident among pediatric surgical patients particularly; patients undergoing gastrointestinal (GI) surgery as a result of anorexia, dietary restriction, malabsorption, increased intestinal losses, or altered nutrient requirements. 2) Moreover, the hypermetabolic state induced by surgical stress and postope rative restriction of oral intake can exaggerate malnutrition 3) ; this results in debilitating immunity and stress resistance. Therefore, hypermetabolic states are regarded as a commutative risk factor for complications such as infection, poor wound healing, GI tract bacterial overgrowth, prolonged hospital stay, and mortality. 46) Parameters for the assessment of body energy and protein re serves have been developed over the years providing a reliable assessment of nutritional status with various methods that could be objective or subjective. 7) There are 2 main classes of objective MAC was taken at a midpoint between the acromion and the olecranon with the arm flexed at 90° angle and with the tape mea sure perpendicular to the long axis of the arm. TSF was measured using a skin fold caliper at the point previously marked for the MAC, while MAMC was calculated through the following formula (MAC- [3.14×TSF]). Z scores for arm circumference forage and triceps skin foldforage of infants from 3 to 60 months of age were reported using 2007 WHO Child Growth Standards. 11) SGNA included: weight change, dietary intake, oral motor skill development, feeding tolerance, functional capacity, muscle wasting, and ankle edema. In assigning overall score, all items were considered in the context of each other. The patients were categorized as either wellnourished if normal ratings in all or most items were achieved or as malnourished in case of moderate to severe ratings in most or all items. 8) STRONGKIDS included the following. Firstly, we considered the presence of an underlying illness, the prospect of a major sur gery, and clinical nutritional assessment. Secondly, we considered the presence of one of the following items: (1) excessive diarrhea; (2) reduction of food intake during the last few days; (3) pre existing nutritional intervention; and (4) inability to consume adequate nutritional intake due to pain, weight loss or stationary weight. Assessment score ranged from 0 to 5. Patients with a score of 0 were classified as being at low risk for malnutrition; those with a score between 1 and 3 were at moderate risk of malnutrition; those with a score more than 4 were at high risk of malnutrition. 9) 3) Section 3: Postoperative clinical outcomes In the third section, the postoperative outcome assessment in cluded the existence of complications and length of hospital stay.
Complications were described according to the presence of postoperative infections that could be local, systemic, or both. Noninfectious complications involved the need of postoperative blood transfusion and intensive care unit admission. A standar dized complication classification system of ClavienDindo was used to monitor postoperative complications. 12) Patients were categorized according to the length of hospital stay into 2 groups: short stay (less than 7 days) and long stay (more than 7 days).
Throughout the study, we did not interfere with nutritional support provided by the clinical nutrition team which relies on encouraging breast feeding or providing artificial formula or complementary diet with proper calculation of caloric and protein requirements according to age nutritional support provided orally except for gastrostomy patients. Micronutrients supplied if indicated.

Questionnaire administration
Both patients' nutritional assessment and reporting postopera tive outcomes were carried out by a single investigator who re ceived an adequate training in the Pediatric Department at CUSPH. The training included the different methods of assessment of the nutritional parameters (Supplementary material). assessment: anthropometric measures and serum proteins levels. Subjective assessments included questionnaires which depend on patient history and recall. 8,9) The present study aims to figure out the preoperative nutritional status, and its influence on postope rative outcome of pediatric patients who underwent elective GI surgery.

Methods
This prospective observational study took place at Cairo Uni versity Specialized Pediatric Hospital (CUSPH) during the period from July 2017 to January 2018. To achieve the aim of the study, we adopted the following methodology: forming study popula tion, and developing and administering a questionnaire.

Study population
The candidates for our study were recruited from the Pediatric Surgery Department at CUSPH during the study period. We included patients whose age ranged from 1 to 60 months (this age group was vulnerable for malnutrition). The neonate had another neonatal surgical department. Based on the designated inclusion criteria, 75 surgical cases were included in our study from both genders. We excluded from the study the following patients: (I) emergency surgical cases

Questionnaire development
A structured questionnaire was developed after reviewing the literature to determine the parameters of nutritional assessment and clinical outcomes (included Supplementary material).
The questionnaire was composed of 3 main sections: demo graphic data of the cases, nutritional status parameters (upon admission and upon discharge), and postoperative clinical out comes.

1) Section 1: Demographic data
The demographic data identified the enrolled patients' age, sex, and associated comorbid conditions. Nutritional history involved presence of breast feeding, problems with weaning, and previous nutritional support.
2) Section 2: nutritional assessment The nutritional assessment tools were divided into objective and subjective. The objective parameters included: measurements of weight, length, mid arm circumference (MAC), triceps skin fold thickness (TSF), mid arm muscle circumference (MAMC) as well as 2 biochemical markers; albumin and hemoglobin levels. The subjective methods were based on history and clinical judg ment, and they included subjective global nutritional assessment (SGNA) and STRONGKIDS score.
The mechanical scale and stadiometer were used to measure weight and length, respectively. Z scores for weightforage, length forage, and weight for lengthforage of infants from 1 to 60 months of age were reported using 2000 CDC growth charts. 10) www.e-cep.org https://doi.org/10.3345/cep.2020.00458 475

Ethical consideration
We obtained an informed consent from caregivers before conducting the questionnaire. Moreover, we also obtained an ethical approval from the Ethical Committee of Cairo University (approval number and date: I151015/2017).

Data analysis
Statistical analysis was performed using SPSS ver. 16.0 (SPSS Inc., Chicago, IL, USA) and Microsoft Excel 2013 (15.0.4420. 1017) 32bit software. Normally distributed continuous variables were expressed as mean and standard deviations. Nonnormally distributed data were expressed by median and range. Compari son of numerical variables was done using Student t test and Fisher exact test for independent samples in comparing 2 groups of normally distributed data, and Mann Whitney U test was used for nonnormal data. Comparison of numerical variables mea sured before and after surgical intervention was done using paired t test for normally distributed data. To examine the rela tionship among the 3 groups or more, an analysis of variance was performed. Correlation between continuous data was analyzed by Spearman correlation. P value less than 0.05 was considered statistically significant.
Each preoperative subjective and objective parameter was cor related discretely to the postoperative complications and length of hospital stay to determine the impact of the nutritional status on the postoperative outcomes. The postoperative nutritional status was also considered.

Patients' demography
Seventyfive patients were enrolled in the study. Including 47 males (63%) and 28 females (37%) with a median age of 10 months (range, 1-60 months). Diagnoses of the patients are displayed in Table 1. Eight patients (11%) had associated comor bid conditions, 2 cases are obese, 2 cases had atrial septal defect, 1 case is asthmatic, 1 had cerebral palsy, 1 is Down syndrome, and 1 had meromilia.

Patients' base line nutritional (preoperative) assessment
Preoperative weightforage z score was less than 2 (under weight) in 28 patients while 17 patients had lengthforage z score less than 2 were (stunted), By using the subjective global nutritional assessment (SGNA) score, it showed that 61 patients (81%) were wellnourished and 14 patients (19%) were malno urished. On the other hand, the STRONGKIDS score found that 13 patients (18%) were at moderate risk of malnutrition, while 25 patients (33%) were at high risk for malnutrition. TSF and MAC were applicable to be interpreted in 62 patients. TSF z score less than 2 was found in 40 patients, while MAC z score less than 2 was found in 19 patients. Interpreting the MAMC with percentiles, we found that 15 patients were ≤5th percentile. The preoperative laboratory assessment revealed the mean of the serum albumin was 3.8 (standard deviation [SD], ±0.5), mean of serum hemoglobin level was 10.5 (SD, ±1.3), the anemic patients were 48 (64% of the included patients).
We evaluated included patients on day 7 postoperative because this is the standard duration for hospital stay of most of uncom plicated surgical cases. We compared the different nutritional as sessment parameters preoperatively and postoperatively in each group. Accordingly, upper GI patients' group showed a signifi cant lower difference in postoperative as regard MAC (P=0.01) while STRONGKIDS score showed lower risk in postoperative with statistically significant difference (P=0.0007). Furthermore, a significant lower difference between pre and postoperative values TSF and MAC (P=0.01, P=0.04, respectively) in the hepatobiliary patients' group (Table 2).

Postoperative clinical outcomes
Depicting the postoperative complications using Clavien Dindo classification is featured in (Table 3). Grade I represented surgical site infection (SSI) with no systemic illness; this was obvious among upper and lower GI patients as we found 2 and The overall incidence of postoperative infectious complications was 33.3% among the 3 different anatomical patients' group. The detected cases among the lower GI patients' group were 16 cases, while among the upper GI and the hepatobiliary patients' groups were 5 and 4, respectively.
We noticed that 17.3% (n=13) of included patients required postoperative blood transfusion. All of them had moderate anemia except only 3 cases had mild degree of anemia preopera tively. Two cases among the upper GI, 8 cases among the lower GI, and 3 cases among hepatobiliary patients' groups received postoperative blood transfusion.
We classified the patients into 2 groups according to the post Underweight z score less than -2. b) Stunted z score less than -2. c) Wasted z score less than -2. d) z score less than -2. e) Anemia hemoglobin less than normal for age (n=27). f) Hypoalbuminemia albumin less than 3.5 gm/dL. g) STRONGKIDS moderate risk score 1-3. h) SGNA reference (n=8). Boldface indicates a statistically significant difference with P<0.05.

Impact of nutritional status on postoperative outcomes
When we compared preoperative anthropometric measures for all patients to postoperative complications, we found a signifi cantly lower difference with the preoperative lengthforage z score and weightforage z score in complicated cases (P=0.001, P=0.046 respectively) ( Table 4; Fig. 1A, B). We also realized that the preoperative lengthforage z score was significantly lower in cases with prolonged hospital stay (P=0.022) ( Table 5, Fig. 2). When comparing anemic and nonanemic patients as regard the postoperative blood transfusion revealed that preoperative anemic patients had higher incidence of blood transfusion than nonanemic group with statistically significant difference (P= 0.003). Neither presence of postoperative complications and duration of hospital stay were related to history of blood transfu sion.
Furthermore, STRONGKIDS and SGNA scores were not correlated for both postoperative complications and length of hospital stay. Neither weight for length, TSF, MAC, nor MAMC  Values are presented as mean±standard deviation or number (%). Boldface indicates a statistically significant difference with P<0.05. were correlated to postoperative complications and length of hospital stay. A remarkable prolonged length of hospital stay was noticed with increasing the ClavienDindo classification grade of compli cation (P=0.001).

Discussion
SGNA is a method of nutritional assessment based on clinical judgment, and it can be adapted to identify presurgical malnutri tion, while STRONGKIDS is a nutritional screening tool that has been developed according to the newest ESPEN (European Society for Clinical Nutrition and Metabolism) guidelines. 8,9) The upper GI group of patients showed the highest prevalence of preoperative malnourishment by both SGNA and STRONGKIDS scoring system.
In this study, the incidence of wasting in included patients preoperatively was 46.6%. The highest percentage was found in upper GI group and hepatobiliary group. Furthermore, we found that the rate of underweight was higher among upper GI and hepatobiliary patients' groups nearly 50% of each group. Upper GI group had the highest percentage of wasting as well as underweight. This could be attributed to periods of decreased intake, interrupted feeding, defective intake, malabsorption, and intestinal losses imposed by the variety of surgical interventions that contributed to the development of undernutrition despite efforts to provide adequate energy and other nutrients. 2,13) The nutritional assessment is the cornerstone in management of surgical patients, should not rely on weight evaluation only, other anthropometric measurements should be used such as TSF, MAC, and MAMC. Because of these are not affected by fluid accumulation. Some patients experienced substantial third space fluid accumulation, 11) particularly if they had decreased serum albumin levels in certain surgical procedure such as the correction of pure esophageal atresia, endoanal pull through for Hirschsprung disease, Kasai procedure, and excision of choledo chal cyst with hepatoduodenostomy. 1) Weight is not the best parameter in patients with chronic liver diseases since visceromegaly and ascites may mask malnutrition. Almost 50% of our hepatobiliary patients had abnormal MAMC and TSF measurements. It could be attributed to the increased energy expenditure in this category of patients and to fat malab sorption. 14) The highest incidence of hypoalbuminemia was among hepato biliary patients' group. This could be explained by increasing the utilization of protein as source of energy and the reduction in liver capacity for protein synthesis. 14) Serum albumin is considered a negative acute phase reactant with longer halflife. This does not reflect the nutritional status, and it is worthy to be assessed with prealbumin that has shorter halflife. 2,15,16) Therefore, albumin is considered a predictor of morbidity except in hepatic patients. 8,17) Nearly 64% of our patients were anemic. Onethird of anemic patients required blood transfusion so the preoperative assess ment of hemoglobin is mandatory. The highest prevalence of anemia was among hepatobiliary and lower GI patient' groups (76% and 66%, respectively). This could be multifactorial due to the underlying surgical procedures, associated morbidity, micro nutrient deficiencies, and recurrent infections. 18) Stunting is indicator of chronic malnutrition which is major risk for morbidity hence postoperative complication. 5) It was recorded in 2014 by Egypt Demographic and Health Survey that the prevalence of stunting among children under 5% was 21%. 19) This could be explained by the fact of low diet quality due to low socioeconomic status of the population. Furthermore, mothers start lactation with relatively poor energy stores, which is insuffi cient to produce a sufficient amount of milk for an optimal infant growth.
When pre and postoperative anthropometric data were com pared to each other, no momentous difference was detected. However, there was a significant reduction in postoperative TSF, MAC, and MAMC among both upper GI and hepatobiliary patients' groups reflecting the changes in muscles and fat stores. This could denote the hypercatabolic state due to surgical stress. 3) On the other hand, there were no notable changes in TSF, MAC, and MAMC among lower GI patients' group. It is worth men tioning that this category started feeding within the first 24 hours after surgery. Patients in the lower GI group experienced few hours of minimal nutritional intake which preserved their nutri tional state postoperatively. Indeed, good caloric and protein intake postoperatively help to maintain these parameters in the normal range. 2022) SSI is considered the most common complication following major GI surgery, affecting between 25%-40% of patients. The rate of SSI doubles from lowincome to highincome settings, persisting after risk adjustment for patients and hospital con founders. 23) We found that onethird 24) of our patients experi enced infectious complications postoperatively. The effects of SSI can be lifethreatening. They are related to onethird of postoperative deaths. Furthermore, SSI can cause pain and discomfort, increase length of hospital stay, and further amplify the risk of potential nosocomial infection. Blood transfusion is accounted a noninfectious complication, its incidence with similar surgeries in middleincome countries is about 31.1%. 23) Onethird of our patients who had infectious complications are wasted. Preoperative malnutrition has shown to increase complications following surgery and the length of hospital stay. Therefore, identifying patients who are at risk of malnutrition prior to surgery is important to optimize their nutritional status prior to the procedure and to minimize suboptimal outcomes. The lack of a universally accepted definition for malnutrition is considered a restriction in evaluating preoperative patients for malnutrition. Furthermore, because the aims of the tools differ, judging the inferiority or superiority of one tool over the other is out of question. Therefore, much of the literature evaluates a variety of nutritional markers using numerous scoring methods. 21,24) We followed the same principle and used different markers www.e-cep.org https://doi.org/10.3345/cep.2020.00458 479 to correlate with the postoperative outcome.
The preoperative lengthforage was significantly related to both postoperative complications either infectious or noninfec tious as well as postoperative length of hospital stay. This goes with the finding of Secker and Jeejeebhoy 8) as the lengthforage of patients who underwent abdominal and thoracic surgeries was correlated significantly with length of hospital stay. Length forage is generally considered an indicator of the patient's long term or previous nutritional status; thus, these results suggest that patients with chronic malnutrition had increased length of hospital stay. 8,25) Nevertheless, we found a relation between pre operative weightforage and postoperative complications with statistical significance (P=0.046). Incidence of complications was substantially related to the length of hospital stay. 25,26,27) It is worth mentioning that one of limitations we faced in this study was that the patients' assessment was performed by a single investigator. This resulted in limited study duration and a small size of patients' population.
In pediatric surgical patients, nutritional assessment is an in dispensable aspect of an initial evaluation. Postoperative compli cations have a higher incidence among stunted patients, while long hospital stay occurs with both stunted and underweight pa tients. Anemic patients should be corrected before the procedure as it significantly indicator for postoperative complication.