Development of a Perioperative Enteral Nutrition Program for Gastric Cancer Surgery

Abstract

Objective: This study aimed to summarize the current evidence-based approach to perioperative enteral nutritional (EN) program for gastric cancer (GC) surgery and to develop a staged and operable EN management scheme based on the evidence to provide clinical guidance for improving perioperative EN management in patients with GC.

Methods: First, we synthesized expert consensuses, systematic reviews, and guidelines related to GC patients who had undergone surgery, based on a review of the literature and expert meetings. Subsequently, after carefully evaluating and selecting relevant EN management data, we created a preliminary draft of a perioperative EN program. Following Delphi expert consultations, the final version of the perioperative EN program was constructed after revision.

Results: After two rounds of consultation, the expert opinions tended to be consistent. The expert positive coefficient was 1.00, and the expert authority coefficient was 0.90. After the second round of consultation, the coefficient of variation of the importance score ranged from 0.05 to 0.20, and the coefficient of variation of the feasibility score ranged from 0.09 to 0.23. The Kendall harmony coefficients were 0.338 and 0.392, and the difference between them was statistically significant (p < 0.001). The final practice plan includes 4 first-level, 16 s-level, and 64 third-level items.

Conclusions: The perioperative EN program constructed in this study is comprehensive in content, feasible, and evidence-based, and can provide insights for clinical improvement.

Introduction

Gastric carcinoma (GC) is one of the most frequently diagnosed cancers in China, ranking third in incidence and mortality rates (1). Patients with GC commonly experience malnutrition, which is exacerbated by surgery (2). Malnutrition has been associated with both poor prognosis and increased risk of surgical complications (3). Thus, clinical research has increasingly focused on perioperative nutrition management rather than tumor excision. From a nutritional perspective, postoperative parenteral or enteral supplementation has been suggested as a crucial aspect of patient care. Enteral nutrition (EN) is the delivery of nutrients to patients via the digestive tract and can be categorized as either tube feeding (TF) or oral nutritional supplements (ONS), depending on the specific route of EN administration (4). The application of Enhanced Recovery After Surgery (ERAS) and prehabilitation concepts, which were originally introduced in colon surgery, has been extended to gastric cancer surgery. The importance of preoperative EN and early postoperative EN management for surgical patients has recently been emphasized among scholars. The aim is to optimize the preoperative physical function status of patients and establish a foundation to expedite their postoperative recovery. The implementation of these strategies allows patients to quickly return to their preoperative state. The choice between EN and parenteral nutrition (PN) depends on the intestinal health of the patient and the patient tolerance to the nutrient-supply method. When the intestinal function of the patient allows for it, EN is generally preferred over PN in surgical wards following major gastrointestinal surgery. The reason is that EN is more physiological, involves fewer risks, and entails less cost.

Most studies on EN support in GC patients are currently limited to the preoperative or postoperative stage, and considerably few have explored the comprehensive management of the perioperative period. Complications associated with EN can influence the effectiveness of EN, particularly in patients who receive EN in the early stages after surgery because they may be prone to intolerance (5). Proper management can reduce EN-related complications and increase the chance for patient tolerate to EN. However, both domestic and foreign nutrition management guidelines (6–8) provide no systematic process for managing EN during the perioperative period of GC. Therefore, they cannot be used directly, hindering medical and nursing staff from accessing relevant information rapidly and comprehensively. Therefore, a scientific and reasonable management plan needs to be constructed to provide a comprehensive and holistic EN program for GC patients and thereby improve their nutritional status.

The Delphi method, a type of expert consultation, involves gathering expert knowledge and opinions on certain issues that require consultation, categorizing and statistically analyzing them, and then presenting anonymous feedback to the experts to refine their responses. The procedure is repeated until the expert viewpoints tend to be consistent (9–10). To provide the groundwork for the subsequent step of promoting clinical practice application, this study systematically retrieved and integrated evidence related to perioperative EN management in GC. An evidence-based approach was used. Following Delphi expert consultation, a set of clinically feasible and effective practice protocols for perioperative EN management was developed.

Establishment of the research group

The research team consisted of 10 specialists, which included the following: 4 experts with senior titles (gastrointestinal surgeons, gastrointestinal surgery nurses, nursing management and nutrition physicians); 3 experts with intermediate titles (attending physicians and nursing team leaders engaged in gastrointestinal surgery treatment); and 3 experts with junior titles (gastrointestinal surgery nurses and physicians). The research team was primarily responsible for literature research, compiling and distributing the consultation questionnaire, selecting experts, as well as analyzing and collating the results. The study complied with the provisions of the Declaration of Helsinki (as revised in 2013) and was approved by the Institutional Review Board of the Affiliated Jiangning Hospital of Nanjing Medical University.

Formation of the first draft of the perioperative EN program for GC

Literature review

Databases were scoured, including BMJ Best Practice, PubMed, Joanna Briggs Institute, Embase, National Institute for Health and Clinical Excellence, Scottish Intercollegiate Guidelines Network, National Guideline Clearinghouse, Cochrane Library, CINAHL, Chinese Biomedical Literature Database, China National Knowledge Internet, WanFang Data, VIP, MedLive. Keywords included “gastric/gastrointestinal,” “neoplasm*/cancer*/tumor*/carcinoma,*” “preoperative period/preoperative care/perioperative nursing/postoperative care,” “nutrition/malnutrition,” “enteral nutrition/oral nutritional supplements/nasogastric tube/sip feeds/nasogastric,” and “guideline/evidence summary/consensus/systematic review/meta analysis.” The inclusion criteria for this study were as follows: (I) The study population consisted of patients undergoing surgery for GC; (II) The study focused on perioperative EN for GC; and (III) The literature included consensus statements, systematic reviews, and guidelines. The exclusion criteria applied were as follows: (I) Content primarily focused on GC patients undergoing radiotherapy; (II) Literature limited to draft versions or abstracts only; (III) Insufficient literature available on the subject; and (IV) Studies with a quality assessment rating of C.

Evidence evaluation criteria

The guidelines were assessed using The Appraisal of Guidelines for Research and Evaluation instrument (11). A systematic evaluation of multiple systematic reviews was conducted (12). The JBI Center for Evidence-Based Health Care Expert Consensus Evaluation Criteria were used for expert consensus evaluation (2016).

Evidence quality evaluation

A blind strategy was used by two researchers trained in evidence-based nursing to assess, retrieve, and integrate the quality of the literature. The choice would be considered final if they were of similar opinions; if their opinions differed, the evidence-based care team of the hospital would arbitrate the dispute. In case of conflicting evidence, priority would be given to certain types of evidence, such as high-quality evidence, the most current evidence published in authoritative journals, and evidence based on previous research. The evidence levels were categorized into five levels in accordance with the 2014 version of the JBI evidence pre-grading and recommendation level system.

Content of the entry pool extraction

In this study, we initially collected 6449 articles. After performing deduplication, primary screening, and rescreening, we were left with only 28 articles for further analysis, including 10 guidelines (6–8, 13–19), 11 systematic reviews (20–30), and 7 expert consensuses (4,31–36). Ultimately, 34 pieces of evidence were summarized based on 8 aspects, including nutritional risk screening and assessment, calculation of nutritional target requirements, indications and contraindications for perioperative EN, perioperative EN modalities, perioperative nutrition preparation selection, perioperative EN timing, preoperative intestinal preparation, EN intolerance, and complication monitoring.

Study group meeting

To discuss and modify the structure and content of the entry pool, 10 experts in gastrointestinal surgeons, gastrointestinal surgery nurses, and nursing management and nutrition physicians attended the meeting. They provided suggestions and reasons for adding, deleting, or modifying the entry, and further adjusted it to improve its connotation. The first protocol contained 4 primary items, 13 secondary items, and 39 tertiary items.

Formulation of expert consultation questionnaires

The expert consultation questionnaire consisted of five parts: (I) a research introduction briefly stating the research background, purpose, significance, and filling method; (II) an expert information questionnaire including educational background, professional title, working years, working field, and so on; (III) a table summarizing the opinions of the experts consulted on perioperative EN program, The table was organized using first-, second-, and third-level indexes. Each index contained scoring columns for “importance” and “feasibility” to help sort the contents of the solution. A 5-point Likert scale was adopted, with points ranging from 1 to 5 to assign ratings from “not important or not feasible” to “very important or very feasible.” In addition, each index had a column of suggestions for modification, allowing experts to modify, supplement, or delete each index; (IV) expert familiarity and judgment basis; and (V) appendix: a summary of relevant attachments and documentary evidence.

Selection of consultants

Seventeen experts were conveniently selected from Shanghai, Qingdao, Nanjing, and so on. The selection criteria were (I) healthcare professionals working in one of the following departments—General Surgery, Gastrointestinal Cancer Surgery, or Nutrition; (II) working in a third-class A hospital; (III) holding a senior title; (IV) having >10 years of working experience; (V) holding a bachelor’s degree or higher; (VI) having a background in this research direction and a foundation in scientific research; (VII) providing informed consent and voluntarily participating in the study.

Implementation of expert consultation

From July to November 2022, the researchers distributed and collected questionnaires through field investigation. After the first round of expert consultation, the researchers modified the indexes based on the screening criteria and expert opinions to form the second-round questionnaire. The screening criteria for indicators were (i) mean importance score > 3.50 and mean operability score > 3.50 and (ii) coefficient of variation < 0.25. The interval and the filling period of each round of consultation were 2–4 wk. After the second round of consultation, the expert opinions exhibited a good centralized trend. Thus, the consultation was stopped, while the scheme was modified and improved depending on the results of the second-round consultation.

Statistical methods

IBM SPSS Statistics 22 was used to statistically analyze the data collected in this study. The weight assigned to each indicator was calculated using the Precedence Chart Method, based on the importance ratings provided by the experts. The measurement data for the general characteristics of the experts were expressed as mean ± standard deviation, and the counting data were expressed as frequency and percentage. The importance and feasibility of each index were evaluated using the mean, standard deviation, and coefficient of variation. The expert positive coefficient was expressed using the questionnaire recovery rate. The degree of expert authority was expressed by the expert authority coefficient. The degree of expert opinion coordination was expressed by the coefficient of variation, and the Kendall harmony coefficient. p < 0.05 was considered statistically significant.

Results

General information of experts

The same group of experts was consulted in the two rounds of this study. A total of 17 experts aged 38–54 (45.65 ± 4.76) years were conveniently selected from Shanghai, Nanjing, Zhenjiang, Luzhou, Hefei, Changzhou, Suzhou, Hangzhou, Qingdao, and Guiyang. Among these experts, 10 (58.82%) worked in clinical nursing and 7 (41.18%) worked in clinical healthcare; 9 (52.90%) had working experience of 10–20 years, 4 (23.52%) had working experience of 20–30 years, and 4 (23.52%) with had working experience ≥30 years. Moreover, from the same group of experts, 8 were undergraduates (47.06%), 7 had a master’s degree (41.18%), and 2 were doctors (11.76%). In addition, all experts held senior titles.

Expert positive coefficient, degree of authority, degree of coordination of opinions and weight assigned to each indicator

The expert positive coefficient was expressed by the questionnaire recovery rate and the number of comments given by the experts. In the two rounds of consultation, 17 questionnaires were distributed and 17 were recovered, with an effective recovery rate of 100% (i.e., >80%) indicating the high enthusiasm of experts. In the first round, 9 (52.94%) experts submitted 24 opinions orally or in writing, and in the second round, 6 (35.29%) experts submitted 26 opinions orally, indicating the satisfactory participation of the experts.

The degree of expert authority was expressed using the expert authority coefficient. This coefficient represented the arithmetic mean of the familiarity of the experts with the index and the basis of their judgment. An expert authority coefficient > 0.70 generally indicates that experts demonstrate good authority. The expert authority was high, as evidenced by the expert authority coefficient of 0.90, expert judgment basis of 0.94, expert familiarity of 0.87, and expert judgment basis of 0.94 for the two consultation rounds.

The Kendall harmony coefficient and coefficient of variation were used to measure the level of coordination among expert opinions. The Kendall harmony coefficient ranged from 0 to 1, with higher values indicating a higher degree of coordination. After the second round of consultation, the coefficient of variation of the importance score ranged from 0.05 to 0.20, and the coefficient of variation of the feasibility score ranged from 0.09 to 0.23. The Kendall harmony coefficients were 0.338 and 0.392, respectively, and showed statistically significant differences (p < 0.001). The importance score, feasibility score, and coefficient of variation of each index in this study are listed in Table 1.

Table 1. Results of the second round of expert consultation.

Index (evidence level)	Importance		Feasibility
	Score ($\overline{x}$ ± s)	Variable coefficient	Score ($\overline{x}$ ± s)	Variable coefficient
1 Organization and management	4.47 ± 0.51	0.115	4.29 ± 0.47	0.109
1.1 Establishment of a multidisciplinary comprehensive treatment cooperation group.	4.76 ± 0.44	0.092	4.12 ± 0.7	0.169
1.1.1 Members of the collaboration group: surgeons, endocrinologists, nutritionists, case managers, exercise rehabilitation therapists, nurses, and pharmacists (5b).	4.53 ± 0.51	0.114	4.35 ± 0.79	0.181
1.1.2 Selection criteria for the team members: with 5 years of clinical work, intermediate title or higher; with nutrition-related qualification certificates or participated in nutrition-related training; familiarity of surgeons with nutritional therapy for patients with gastrointestinal tumors; designation of the nutritionist as a national secondary nutritionist or higher; experience as gastrointestinal surgery and nutrition specialist nurses, familiarity with clinical nutrition knowledge and skills, familiarity with the treatment for common complications of enteral nutrition, ability to implement clinical nutrition assessment, in addition to diagnosis and treatment, and professional nutrition counseling and guidance. Pharmacists were required to have undergone training in enteral nutrition from clinical pharmacists (5b).	4.47 ± 0.51	0.115	4.24 ± 0.75	0.178
1.2 Management methods	4.47 ± 0.51	0.115	4.41 ± 0.51	0.115
1.2.1 Two-level management system: The gastrointestinal surgeon is responsible for managing the group in accordance with the two-level management system. The system included one team leader represented by the deputy chief physician of gastrointestinal surgery; two deputy team leaders represented by the nutrition doctor and the competent nurse; one case manager; one nurse; one pharmacist, and one exercise rehabilitation therapist (5b).	4.47 ± 0.51	0.115	4.35 ± 0.7	0.161
1.2.2 Management system: A perioperative enteral nutrition support management system was established, and paper documents were organized, including the nutrition group management system, nutrition consultation process, perioperative enteral nutrition support management process, enteral nutrition operation process, enteral nutrition standard, and nutrition evaluation and monitoring (5b).	4.65 ± 0.49	0.106	4.41 ± 0.51	0.115
1.2.3 Team training: Training programs and training manuals were developed for homogeneous training (5b).	4.76 ± 0.44	0.092	4.47 ± 0.51	0.115
1.2.4 Quality inspection: Nutrition quality management standards and regular inspection were formulated (5b).	4.47 ± 0.51	0.115	4.41 ± 0.51	0.115
2 Assess diagnosis	4.76 ± 0.44	0.092	4.35 ± 0.49	0.113
2.1 Nutritional risk screening	4.82 ± 0.39	0.081	4.71 ± 0.59	0.125
2.1.1 Screening time: Nutritional risk screening was performed at the time of diagnosis and admission; within 24 h postoperatively when the condition changed; 1 month after discharge; and 3 months after the operation (5b).	4.47 ± 0.51	0.115	4.35 ± 0.79	0.181
2.1.2 Screening tool: NRS 2002 (recommended)(1a).	4.65 ± 0.49	0.106	4.41 ± 0.71	0.161
2.2 Nutritional assessment	4.71 ± 0.47	0.1	4.53 ± 0.51	0.114
2.2.1 Evaluation indicators: When NRS2002 ≥ 3 points, further nutritional assessment was performed. Evaluation indicators include body measurement (weight loss, BMI, triceps skinfold thickness, upper arm circumference, etc.), body function measurement (muscle strength, pace), body composition measurement (muscle, fat), and laboratory examination (albumin, blood routine, blood glucose) (5b).	4.71 ± 0.47	0.100	4.35 ± 0.7	0.161
2.2.2 Evaluation scale: Patient-Generated Subjective Global Assessment or PG-SGA is recommended if possible (5b).	4.47 ± 0.72	0.160	4.41 ± 0.71	0.161
2.3 Gastrointestinal function assessment	4.65 ± 0.49	0.106	4.41 ± 0.62	0.14
2.3.1 Adopt the AGI scoring system: if AGI grade I–III, EN should be actively started; when AGI ≤ 1, ONS should be selected as far as possible; and AGI grade IV should be suspended EN (5c).	4.59 ± 0.51	0.111	4.53 ± 0.51	0.114
2.4 Malnutrition diagnosis	4.71 ± 0.47	0.100	4.53 ± 0.62	0.138
2.4.1 Clinical diagnostic criteria for malnutrition: If NRS2002 ≥ 3 points, on this basis, meeting at least one phenotypic index and one etiological index is required, in accordance with the latest standards outlined by the GLIM consensus on malnutrition assessment (diagnosis) (1a).	4.71 ± 0.47	0.100	4.35 ± 0.49	0.113
2.4.2 Emphasis on the differential diagnosis of malnutrition and sarcopenia, weakness, cachexia, and abnormal trace elements (5c).	4.41 ± 0.51	0.115	4.29 ± 0.59	0.137
3 Methods of enteral nutrition	4.94 ± 0.24	0.049	4.59 ± 0.51	0.111
3.1 Nutritional target requirements	4.76 ± 0.44	0.092	4.47 ± 0.8	0.179
3.1.1 GC perioperative recommended protein 1.2–1.5 g/(kg·d); 1.5–2.0 g/(kg·d) recommended for patients undergoing major surgery or in severe stress response; sugars 3–4 g/(kg·d); lipids were 1.5–2 g/(kg·d) (4b).	4.59 ± 0.62	0.135	4.24 ± 0.66	0.157
3.1.2 Preoperative oral high-protein or immunonutrition is recommended to ensure 3 meals of ONS daily, and the daily calorie of ONS is at least 400–600 kcal (1a).	4.59 ± 0.62	0.135	4.24 ± 0.66	0.157
3.1.3 Preoperative ideal actual supplement should reach about 80% of the target requirement(5b).	4.24 ± 0.75	0.178	4.18 ± 0.73	0.174
3.1.4 Patients with insulin resistance should increase the proportion of fat and reduce carbohydrates when choosing energy substrates (5b).	4.35 ± 0.7	0.161	4.06 ± 0.83	0.204
3.1.5 Relatively low-calorie energy supply of 15–25 kcal/(kg·d) was allowed in the early postoperative period (1b).	4.53 ± 0.51	0.114	4.06 ± 0.56	0.137
3.2 Perioperative EN indications and contraindications.	4.82 ± 0.39	0.081	4.59 ± 0.51	0.111
3.2.1 Indications: Patients with moderate-to-severe malnutrition; patients who cannot meet energy needs from normal food; patients benefiting from GC surgery (5b).	4.47 ± 0.51	0.115	4.29 ± 0.69	0.16
3.2.2 Contraindications: Indwelling gastrointestinal decompression for various reasons; active gastrointestinal bleeding; anastomotic fistula that has been diagnosed and not properly handled; severe abdominal infection, which can cause an increase in abdominal pressure; early postoperative inflammatory intestinal obstruction or other causes of complete intestinal obstruction; intestinal ischemia; shock state caused by any complication that is not fully recovered; high-output fistula (1c).	4.88 ± 0.33	0.068	4.71 ± 0.47	0.1
3.3 Perioperative EN routes	4.65 ± 0.61	0.130	4.59 ± 0.51	0.111
3.3.1 According to the five-step treatment model, when the daily diet fails to meet 60% of the target requirement for more than 3–5 d, EN should be administered. If tolerated, ONS is preferred. When the total enteral nutrition fails to meet 60% of the target demand for more than 3–5 days, EN + PN is administered (1a).	4.82 ± 0.39	0.081	4.47 ± 0.62	0.14
3.3.2 Patients who could not eat for more than 5 d or expected low oral intake, and could not maintain more than 50% of the recommended intake for more than 7 d should choose TF (1a).	4.65 ± 0.49	0.106	4.29 ± 0.59	0.137
3.3.3 If preoperative TF is required, nasogastric tube or gastrointestinal tube placement is preferred; a gastric or jejunal fistula is recommended when the nutrition time is expected to be more than 4 weeks. The jejunal approach should be selected for patients with gastroparesis, gastric feeding intolerance, or a high risk of aspiration (1b).	4.59 ± 0.51	0.111	4.29 ± 0.77	0.18
3.3.4 After the surgery, patients who are awake from anesthesia may drink a small amount of water orally. The small intestine can regain its function 6–12 h after the operation (if possible, gastrointestinal electromyography can be used to evaluate the condition, and plasma motilin levels can be detected 6-12 h after the operation). At this time, EN can be started. Patients with no oral nutritional contraindications may opt for ONS and gradually transition to a normal diet depending on their level of tolerance. An oral transparent liquid or a small amount of clear liquid food 250–500 mL is taken on the day after the operation and gradually increased each day. If the volume of the oral liquid reaches 2000–2500 mL/d, the intravenous infusion may be stopped (1a).	4.47 ± 0.72	0.16	4.29 ± 0.69	0.16
3.3.5 For GC patients with low preoperative nutritional status, at high risk for complications during surgery, and with a postoperative need for adjuvant chemoradiotherapy or long-term nutritional therapy, an indwelling jejunal nutrition tube during operation is recommended (5b).	4.59 ± 0.51	0.111	4.18 ± 0.81	0.194
3.3.6 Patients with high nutritional risk who cannot eat independently should start TF support within 24 h after surgery. When the postoperative oral and/or tube-feeding enteral intake < 50 % of the nutritional target, parenteral nutrition is recommended (1a).	4.65 ± 0.61	0.13	4.41 ± 0.62	0.14
3.3.7 Enteral nutrition delivery method: for TF, a continuous infusion with a nutrition pump is recommended, and patients without conditions could opt for an interstitial gravity infusion. For patients receiving ONS, prompt administration is recommended (1a).	4.59 ± 0.51	0.111	4.24 ± 0.56	0.133
3.4 Perioperative EN preparation	4.59 ± 0.51	0.111	4.53 ± 0.62	0.138
3.4.1 As an alternative to a balanced diet, EN preparations are the first choice when starting oral nutrition. To improve patient acceptance of oral nutrient solutions, it should be based on the eating habits and preferences of an individual. Preparations that meet their tastes should be selected, and if adding safe flavorings to ONS is necessary, appropriate methods should be adopted (5b).	4.71 ± 0.47	0.1	4.41 ± 0.62	0.14
3.4.2 For all perioperative patients benefiting from GC surgery, enteral immunonutrition should be prioritized. In addition, the combination of arginine, glutamine, ω-3 polyunsaturated fatty acids, and nucleic acids is recommended (1a).	4.24 ± 0.83	0.196	4.00 ± 0.94	0.234
3.4.3 For patients with normal gastrointestinal function, a whole protein formula for EN is recommended; for those with gastrointestinal dysfunction or absorption disorder (AGI I–III), hydrolyzed protein formulae (amino acid type and short peptide type) are recommended (5b).	4.24 ± 0.75	0.178	4.06 ± 0.75	0.184
3.4.4 Patients with diabetes should use EN preparations with diabetes-specific formulations (1c).	4.35 ± 0.7	0.161	4.18 ± 0.81	0.194
3.4.5 For patients with severe liver dysfunction or renal failure, glutamine is not recommended for EN; for patients with sepsis, arginine-containing immune-enhanced EN preparations are not recommended (1a).	4.53 ± 0.62	0.138	4.29 ± 0.99	0.229
3.4.6 Daily intake of minerals (electrolytes and trace elements), vitamins, and soluble dietary fiber (2b).	4.47 ± 0.62	0.14	4.29 ± 0.85	0.198
3.5 Perioperative EN time	4.53 ± 0.62	0.138	4.35 ± 0.7	0.161
3.5.1 For patients with moderate malnutrition and who require major surgery, PN + EN treatment for 7-14 d before surgery is recommended, and for those with severe malnutrition can be extended for four weeks as appropriate (1a).	4.47 ± 0.8	0.179	4.18 ± 0.81	0.194
3.5.2 Preoperative enteral immunonutrition should be used for at least 5 d (1a).	4.53 ± 0.51	0.114	4.24 ± 0.75	0.178
3.5.3 All malnourished patients should continue immunonutrition for 7 d even after surgery without complications or until the patient can consume at least 60% of the energy requirement by mouth (5b).	4.18 ± 0.64	0.152	3.82 ± 0.81	0.212
3.5.4 For malnourished patients, preoperative nutritional support should be maintained until four weeks or longer after surgery (5b).	4.35 ± 0.61	0.139	4.18 ± 0.73	0.174
3.5.5 Patients who choose ONS for nutritional support after surgery use it for at least 7 d (5b).	4.35 ± 0.7	0.161	4.29 ± 0.77	0.18
3.6 Preoperative bowel preparation	4.41 ± 0.62	0.14	4.47 ± 0.51	0.115
3.6.1 For patients with suspected transverse colon involvement, mechanical bowel preparation with an isotonic buffer can be selected before combined organ resection. For patients with chronic constipation, saline enema is preferred, and for those with pyloric obstruction, insertion of a nasogastric tube is recommended for warm saline gastric lavage (5b).	4.53 ± 0.62	0.138	4.24 ± 0.75	0.178
3.6.2 Early GC patients without delayed gastric emptying, gastrointestinal motility abnormalities, diabetes, or emergency surgery may drink clear fluids until 2 h before anesthesia. Solids shall be allowed until 6 h before anesthesia. Preoperative intake of an 800 mL carbohydrate drink the night before and 400 mL 2–3 h before surgery, such as a 12.5% sugar solution (1a).	4.59 ± 0.62	0.135	4.53 ± 0.72	0.158
3.6.3 In advanced GC, the effect of the tumor on gastric motility and upper gastrointestinal patency should be considered. The fasting time should be prolonged, and the number of oral carbohydrates should be reduced. GC patients with obstruction can change preoperative oral carbohydrates to a preoperative intravenous glucose solution of 200g (5b).	4.53 ± 0.51	0.114	4.41 ± 0.87	0.197
4 EN adverse reactions and effect evaluation	4.71 ± 0.47	0.1	4.35 ± 0.61	0.139
4.1 EN adverse reaction monitoring indicators	4.59 ± 0.62	0.135	4.41 ± 0.62	0.14
4.1.1 Sensory adverse reactions: taste (dry mouth, taste discomfort) (1c).	4.18 ± 0.73	0.174	4.18 ± 0.73	0.174
4.1.2 Gastrointestinal intolerance indicators: Nausea and vomiting (> 1/12 h); abdominal distension, and Intra-abdominal pressure(IAP) (IAP is measured with a pressure sensor connected to an abdominal drainage tube. Within 4–6 h, take Three precise abdomen pressure readings are taken, with a minimum value of >12 mmHg, or two readings of abdominal perfusion pressure < 60 mmHg); diarrhea (refer to Hart’s diarrhea score, with total score ≥ l2 for diarrhea); disappearance of bowel sounds (unheard/3–5 min); hyperactive bowel sounds (>10 beats/min); gastric retention (5 mL/kg or 300 mL); reflux (gastric content reflux to the throat cavity); aspiration (patients with irritating cough and/or shortness of breath or even cyanosis during eating or noneating) (3a).	4.65 ± 0.49	0.106	4.29 ± 0.92	0.214
4.1.3 Metabolic complications: hyperosmotic dehydration, abnormal blood glucose, electrolyte abnormalities, etc (2c).	4.71 ± 0.47	0.1	4.59 ± 0.51	0.111
4.1.4 Infectious complications: aspiration pneumonia (2d).	4.59 ± 0.51	0.111	4.41 ± 0.51	0.115
4.1.5 Other complications: incontinence dermatitis, device-related pressure injury (5b).	4.24 ± 0.56	0.133	4.35 ± 0.49	0.113
4.2 EN Adverse Reaction Prevention	4.76 ± 0.44	0.092	4.35 ± 0.7	0.161
4.2.1 Principle of enteral nutrition: the concentration from low to high, the temperature of 38 °C–40 °C (the use of a heater is recommended), the amount from less to more, low speed (20–30 mL/h), and a gradual increase in the feeding dose. For patients with good tolerance, the feeding amount should reach the target requirement within 72 h. For patients with poor gastrointestinal tolerance, the feeding amount should gradually and cautiously reach the target requirement within 7 d. As the thickness of the solution increases, the osmotic pressure decreases (5b).	4.76 ± 0.44	0.092	4.76 ± 0.44	0.092
4.2.2 TF monitors gastrointestinal intolerance indicators every 4–6 h, and the infusion rate is adjusted (4c).	4.71 ± 0.47	0.1	4.41 ± 0.51	0.115
4.2.3 Prevention of incontinence dermatitis: diarrhea patients should take corresponding measures to alleviate diarrhea depending n the classification of diarrhea, and perform perianal care to keep the local skin clean and dry (4c).	4.41 ± 0.51	0.115	4.35 ± 0.49	0.113
4.2.4 Metabolic complications: strengthen monitoring, and laboratory examination depending on the condition of the patient (5b).	4.41 ± 0.62	0.14	4.41 ± 0.51	0.115
4.2.5 Instrument-related pressure injury: The appropriate model or material (polyurethane or silicone) instrument is selected; multidisciplinary team management and health education are provided; Use of biologically active skin protectants, rennet smears, or alternative adhesive tapes are used for prophylactic purposes (1a).	4.35 ± 0.7	0.161	4.29 ± 0.59	0.137
4.2.6 Prevention of reflux/aspiration and aspiration pneumonia: Patients with disturbance of consciousness, particularly those with an unclear mind or GCS score < 9 and elderly patients, should be turned over. Their respiratory secretions need to be suctioned before nasal feeding. The head and chest may rise 30° or higher during nasal feeding, and the patient should remain in a semi-reclining position within 30 min after nasal feeding (turning over, patting the back, immediately sucking the sputum, and moving the patient should be avoided) (2a).	4.94 ± 0.24	0.049	4.53 ± 0.51	0.114
4.3 Treatment of EN adverse reactions	4.71 ± 0.47	0.1	4.47 ± 0.62	0.14
4.3.1 Patients with discomfort: Replacement of EN preparations depending on their dietary preferences is recommended (5b).	4.35 ± 0.7	0.161	4.00 ± 0.87	0.217
4.3.2 Patients with nausea and vomiting: The placement of the nasogastric tube should be checked, and the infusion rate should be reduced by 50%. When the patient is vomiting, EN administration should be suspended. The patient should be reevaluated after 2 h and should be given gastrointestinal motility drugs if necessary (2a).	4.65 ± 0.49	0.106	4.47 ± 0.51	0.115
4.3.3 Patients exhibiting abdominal distension with IAP: For those with mild IAP (12–15 mmHg), the speed of EN can be maintained, 6 h reassessment; for those with moderate IAP (16–25 mmHg), the speed can be reduced by 50%. An abdominal plain film is used to exclude intestinal obstruction, and after 6 h, the condition may be reassessed. For patients experiencing continuous abdominal distension, gastric motility drugs may be used, depending on the underlying condition. For those experiencing severe abdominal distension with IAP > 25 mmHg, EN should be stopped. An abdominal plain film may be used to evaluate intestinal obstruction, or an abdominal CT scan may be performed (1c).	4.59 ± 0.62	0.135	4.06 ± 0.83	0.204
4.3.4 When the bowel sounds disappear, EN should be suspended, a drug should be administered, and an evaluation for 2 h should be performed (5b).	4.29 ± 0.59	0.137	4.18 ± 0.64	0.152
4.3.5 Diarrhea: For Grade I diarrhea (stool frequency < 4 times/d, volume < 500 mL, slightly wet and soft), the infusion rate should be maintained. For Grade II diarrhea (stool frequency 4–6 times/d, volume 500–1000 mL, wet and not formed), the infusion rate should be maintained, and the condition should be reevaluated for 6 h. for Grade III diarrhea (stool frequency ≥ 7 times/ d, volume > 1000 mL, loose stool or watery), the infusion rate needs to be reduced by 50%, antidiarrheal drugs should be given via the feeding tube. Drug treatment should be initiated, and the condition of the patient should be monitored and recorded, including antibiotics and other gastrointestinal drugs. A stool routine test should be conducted. In addition, a toxin test should be performed. If it lasts for more than 48 h, switching to short-peptide formula feeding is advised. For Grade IV diarrhea (with hemodynamic changes, life-threatening), EN should be discontinued, drug treatment should be initiated, and the condition of the patient should be monitored for 24 h (5b).	4.47 ± 0.62	0.14	4.41 ± 0.62	0.14
4.3.6 Gastric retention does not exceed 500 mL: Stopping EN is not recommended (5b).	4.41 ± 0.62	0.14	4.29 ± 0.69	0.16
4.3.7 Reflux/aspiration/aspiration pneumonia: EN should be discontinued. The patient should be positioned on their right side and instructed to lower their head to help clear any inhaled material from the airway. The gastric contents should be extracted to prevent further reflux, which may lead to serious consequences (3e).	4.65 ± 0.61	0.13	4.53 ± 0.51	0.114
4.3.8 Metabolic complications: Hyperglycemia and glucose intolerance can be supplemented with insulin, or the existing preparation may be changed to low-glucose enteral nutrition preparations. In addition, the infusion rate and solution concentration may be reduced. For hypertonic dehydration, the concentration and amount of EN should be gradually increased, the changes in serum electrolyte and urea nitrogen levels should be monitored regularly, and the 24 h intake and output of patients should be strictly recorded. Patients with water and electrolyte metabolism disorders should undergo testing to detect imbalances in electrolytes, blood glucose, plasma protein, and other indicators. The results should be analyzed to determine the type and severity of the metabolic disorder and evaluate the nutritional status of the patient, The use of the nutrient solution should be adjusted, depending on the condition of the patient. Intravenous rehydration should be performed to correct water and electrolyte imbalances promptly (5b).	4.53 ± 0.8	0.177	4.53 ± 0.8	0.177
4.3.9 Other complications: Incontinence dermatitis may develop. Depending on the cause of diarrhea in patients, certain measures may be taken to address these complications, including the use of probiotics, albumin supplementation, heating enteral nutrition infusion, and optimization of the infusion of EN, among others (5b).	4.35 ± 0.61	0.139	4.47 ± 0.51	0.115
4.4 EN effect evaluation	4.47 ± 0.51	0.115	4.29 ± 0.47	0.109
4.4.1 Body measurements (weight loss, BMI, triceps skinfold thickness, upper arm circumference, etc.) and body function measurements (muscle strength and pace) were evaluated weekly (patients can get out of bed) (5b).	4.53 ± 0.51	0.114	4.35 ± 0.79	0.181
4.4.2 Laboratory nutrition indicators (including serum sodium, serum potassium, urea nitrogen, serum creatinine, blood glucose, albumin, prealbumin, total bilirubin, etc.): Depending on the condition of the patient, the blood routine and serum protein were checked weekly, and the information was promptly reported to the doctor to evaluate the effect of EN (5b).	4.71 ± 0.47	0.1	4.53 ± 0.62	0.138
4.4.3 The postoperative complications, length of hospital stay, and length of hospital stay at discharge should be determined and recorded. The quality of life 1 and 3 months after discharge should be evaluated (5b).	4.65 ± 0.49	0.106	4.53 ± 0.51	0.114

EN: Enteral nutrition; ONS: Oral nutritional supplements; TF: Tube feeding; NRS2002: Nutritional risk screening 2002; BMI: Body mass index; PG-SGA: Patient-generated subjective global assessment; GLIM: Global leadership initiative on malnutrition; AGI: Acute gastrointestinal injury; GCS: Glasgow coma scale; IAP: Intra-abdominal pressure.

The final established weighting of the perioperative EN program for gastric cancer surgery is shown in Table 2.

Table 2. Weight of each level indicator and composite weight.

Level 1 indicator	Weight	Level 2 indicator	Weight (%)	Composite weight (%)	Level 3 indicator	Weight (%)	Composite weight (%)
1	6.25	1.1	75.00	4.69	1.1.1	75.00	3.52
					1.1.2	25.00	1.17
		1.2	25.00	1.56	1.2.1	12.50	0.20
					1.2.2	31.25	0.49
					1.2.3	43.75	0.68
					1.2.4	12.50	0.20
2	31.25	2.1	25.00	7.81	2.1.1	25.00	1.95
					2.1.2	75.00	5.86
		2.2	6.25	1.95	2.2.1	55.56	1.08
					2.2.2	11.11	0.22
					2.2.3	33.33	0.65
		2.3	25.00	7.81	2.3.1	100	7.81
		2.4	43.75	13.67	2.4.1	25.00	3.42
					2.4.2	75.00	10.25
3	43.75	3.1	25.00	10.94	3.1.1	22.45	2.46
					3.1.2	18.37	2.01
					3.1.3	26.53	2.90
					3.1.4	2.04	0.22
					3.1.5	6.12	0.67
					3.1.6	12.25	1.34
					3.1.7	12.25	1.34
		3.2	30.56	13.37	3.2.1	75.00	10.03
					3.2.2	25.00	3.34
		3.3	19.44	8.51	3.3.1	20.41	1.74
					3.3.2	10.20	0.87
					3.3.3	2.04	0.17
					3.3.4	10.20	0.87
					3.3.5	20.41	1.74
					3.3.6	10.20	0.87
					3.3.7	26.53	2.26
		3.4	13.89	6.08	3.4.1	5.56	0.34
					3.4.2	5.56	0.34
					3.4.3	13.89	0.84
					3.4.4	30.56	1.86
					3.4.5	22.22	1.35
					3.4.6	22.22	1.35
		3.5	8.33	3.65	3.5.1	32.00	1.17
					3.5.2	4.00	0.15
					3.5.3	16.00	0.58
					3.5.4	16.00	0.58
					3.5.5	32.00	1.17
		3.6	2.78	1.22	3.6.1	55.56	0.68
					3.6.2	33.33	0.41
					3.6.3	11.11	0.14
4	18.75	4.1	18.75	3.52	4.1.1	4.00	0.14
					4.1.2	28.00	0.99
					4.1.3	36.00	1.27
					4.1.4	20.00	0.70
					4.1.5	12.00	0.42
		4.2	43.75	8.20	4.2.1	25.00	2.05
					4.2.2	19.44	1.59
					4.2.3	11.11	0.91
					4.2.4	11.11	0.91
					4.2.5	2.78	0.23
					4.2.6	30.56	2.51
		4.3	31.25	5.86	4.3.1	4.94	0.29
					4.3.2	19.75	1.16
					4.3.3	16.05	0.94
					4.3.4	1.24	0.07
					4.3.5	11.11	0.65
					4.3.6	8.64	0.51
					4.3.7	19.75	1.16
					4.3.8	13.58	0.80
					4.3.9	4.94	0.29
		4.4	6.25	1.17	4.4.1	11.11	0.13
					4.4.2	55.56	0.65
					4.4.3	33.33	0.39

Expert consultation results

Following two rounds of expert consultation, the indexes were modified based on the selection criteria of index items, combined with expert opinions and research group discussion: (I) One new secondary index referred to as “EN effect evaluation” was inserted. (II) Twenty-two tertiary indexes were added, such as “using the acute gastrointestinal injury (AGI) scoring system, if AGI is I–III, EN should be actively initiated, and when AGI is less than or equal to I, ONS should be selected as far as possible; if AGI is IV, EN should be withheld,” as well as “infectious complications: aspiration pneumonia” and other indicators. (III) One primary index was modified: “EN adverse reactions and effect evaluation.” (IV) Three secondary items were updated: “nutritional assessment” was changed to “nutritional evaluation” and “prevention of EN adverse reactions" was changed to "EN Adverse reaction prevention” and “EN adverse reaction management.” (V) Thirteen tertiary items were revised. For example, the phrase “Recommended immunoenteral nutrition dose 750–1000 mL/d” was changed to “Preoperative immunoenteral nutrition dose 750–1000 mL/d,” and the phrase “timing of screening: nutritional risk screening at diagnosis or at admission” was changed to “timing of screening: nutritional risk screening at diagnosis, at admission, within 24 h after surgery, at a change in condition, and at postoperative review 1 month after discharge and 3 months after surgery,” and so on. Table 1 presents the final protocol, which contains 4 primary items, 16 secondary items, and 64 tertiary items for perioperative EN management in GC.

Discussion

Constructing a perioperative EN management program for GC patients is of great significance

China has one of the highest incidence and mortality rates of GC worldwide, according to GLOBOCAN 2022 data published by the International Agency for Research on Cancer (1). Currently, surgery is considered the first-line treatment for GC, and radiotherapy and chemotherapy are used as adjuvant treatments. Although it can extend their lives, this approach causes significant harm to patients, including longer surgical incisions, higher complication rates, longer recovery times from postoperative stress and hospitalization, and susceptibility to malnutrition (37). Advances in medical technology and nursing care have shown the significance of nutritional status and intake. This recognition spans the entire course of treatment for GC, from the diagnostic stage through the perioperative period to long-term postoperative care (4). We developed an evidence-based practice protocol for the perioperative nutritional management of GC patients in the current study. Consisting of 64 entries, the protocol provides a fairly comprehensive practice guideline. The perioperative period was selected because it is the most stressful and traumatic time for patients with GC.

Perioperative EN management program for GC patients is scientific and reliable

To develop an evidence-based practice protocol, we formed a team following the theoretical approach of evidence-based care. The team jointly developed the formula and scope of the search. They also systematically searched for guidelines, consensus, and systematic evaluation related to perioperative EN management for GC patients both at home and abroad. Subsequently, a two-person independent evaluation and consistency testing of the protocol was conducted. The clinical application and viability of the findings were assessed by a group of experts via a conference. The 17 experts who participated in this study were selected from 10 cities, including Shanghai, Nanjing, Zhenjiang, Luzhou, Hefei, Changzhou, Suzhou, Hangzhou, Qingdao, and Guiyang. Among the considerations in the selection of experts were multidisciplinary teamwork and the participation of stakeholder groups, including clinical nursing staff, nursing managers, clinicians, and dieticians. All experts held senior titles, ensuring the depth and breadth of the knowledge structure. Multidisciplinary cooperation and the inclusion of stakeholder groups, including clinical nursing staff, nursing managers, clinicians, and dieticians were also considered in the selection of experts. Some experts had overlapping research expertise in various fields, indicating their high geographic coverage and disciplinary representation. This survey reveals that the expert authority coefficient was 0.90, indicating a high level of expertise, the experts demonstrated familiarity with the subject matter, and the results were credible. A 5-point Likert scale was adopted to evaluate the indexes. Both the mean scores of importance and operability of indexes were >3.50, and the coefficient of variation was <0.25, ensuring the reliability of data collection and analysis (38).

The expert response rate in both rounds was 100% each, and the percentages of the comments were 52.94% and 35.29%, demonstrating the level of engagement of the experts in the discussion. The specialists collaborated and contributed 50 ideas for modification. The protocol development process was generally meticulous and well-organized, ensuring the scientific validity of the established protocol.

Perioperative EN management program for GC patients has clinical applicability

This study employed a Delphi expert letter to examine the clinical applicability and viability of the recommendations in the preliminary draft, with consideration of the possibility that patients in China may have different baseline characteristics than those in other countries with regard to medical resources, cultural context, and baseline traits. For instance, one of the original entries for nutritional risk screening stated that it “should be performed at diagnosis or at admission,” but experts advise changing it to “should be performed at diagnosis, at admission, within 24 h after surgery, at a change in condition, and at 1 month after discharge” because EN for patients with GC should be provided throughout the diagnostic phase, perioperative period, and long-term postoperative support. For instance, the expert felt that implementing EN support treatment for patients prior to admission posed challenges. Thus, deleting one of the entries of preoperative EN support was advised, which read “Preoperative TF/ONS should preferably be given before admission to avoid unnecessary hospitalization and reduce the risk of hospital infection.” This study summarized the most relevant research about perioperative nutritional support for patients with stomach cancer by using an evidence-based methodology. The evidence-based practice plan for managing EN during surgery for patients with gastric cancer developed by Delphi expert correspondence validation is scientifically and clinically useful, serving as a foundation for further development and deployment. However, only the domestic and international literature in English and Chinese was searched during the early stages of the evidence-based search in this study, leaving out the next level of evidence for guidelines, consensus, and systematic evaluation, which could have resulted in omissions.

Clinical significance of indicator weight levels in the management of EN for GC

The study results show that the first-level indicators (methods of enteral nutrition) have the highest weight (43.75%) in the perioperative EN program for gastric cancer management. These indicators include nutritional target requirements, perioperative EN indications and contraindications, perioperative EN routes, perioperative EN preparation, perioperative EN time, and preoperative bowel preparation. Among the indicators, perioperative EN indications and contraindications (13.37%), nutritional target requirements (10.94%), and perioperative EN routes (8.57%) hold the top three positions in terms of weight. Identifying the indications and contraindications of EN for gastric cancer patients before administering EN is crucial. In previous studies, the emphasis was primarily on postoperative EN. However, increased attention has recently been paid to improving the preoperative nutritional status of gastric cancer patients. The French Society of Digestive Surgery recommends providing immune EN support for well-nourished gastric cancer patients before surgery (39). Early postoperative EN is safe for most gastric cancer surgery patients and can improve their short-term prognosis. The perioperative EN process for GC patients requires dynamic evaluation to identify any potential contraindications. In cases of absolute contraindications, such as complete intestinal obstruction, uncontrollable peritonitis, intestinal ischemia, severe shock, and others, total parenteral nutrition should be given in a timely manner. Second, the accurate calculation of target nutritional requirements during the perioperative period is critical. Indirect calorimetry is currently considered the gold standard because of its safety, non-invasiveness, and relatively high accuracy for determining nutritional requirements. It is generally used for patients with evident nutritional risks; however, it is associated with lengthy measurement times and significant workload requirements (40). Formula calculation typically uses parameters such as weight, height, age, gender, and body composition, but no prediction equation that can accurately reflect the energy expenditure of patients is currently available (41). Surgical trauma and inflammatory response can subject gastric cancer patients to physiological stress shortly after surgery. Gastric cancer patients undergoing stress often experience an uncontrolled catabolic metabolism that cannot be suppressed by food intake. Nutritional treatment alone may not be adequate to stop endogenous energy production, causing excessive muscle consumption in patients. In the early stages of post-operative stress, maintaining relatively inadequate calories and nitrogen may provide advantages. This approach allows for low-calorie intake to reduce high blood sugar and insulin consumption. However, the body increases its protein demand during periods of stress. Thus, the proportion of protein in the diet can be increased. Third, the selection of the perioperative EN administration route is also significant. To meet the nutritional target requirement of the patient, EN is preferred because of its physiological nature, lower risk, and cheaper. ONS or TF is selected based on the intestinal function of the patient. PN may be used in combination when necessary, or total parenteral nutrition (TPN) may be used.

In the Level 1 indicator, “Assess diagnosis” (31.25%) ranks second. Among the Level 2 indicators within Assess diagnosis, the proportion of malnutrition diagnosis is the largest (13.67%), followed by the same weight of nutritional risk screening and gastrointestinal function evaluation (7.81%). Although screening for malnutrition risk in gastric cancer patients is the first step, further clarifying the diagnosis of malnutrition is more important. After the diagnosis of GC is confirmed, nutritional risk screening should be conducted as soon as possible to identify those with nutritional risks. With a robust evidence base, the Nutritional Risk Screening 2002 (NRS 2002) is recommended by numerous national and international nutrition associations (42). The NRS 2002 is the preferred tool for inpatient nutritional risk screening because of its relatively straightforward operation. The Global Leadership Initiative on Malnutrition (GLIM) consensus (43) released in 2018 indicated that based on this nutritional risk screening, at least one phenotypic indicator and one etiological indicator must be met to diagnose malnutrition. Further classification can be made. into moderate to severe malnutrition, based on the phenotypic indicator. The diagnostic criteria for malnutrition are constantly evolving. To a certain extent, the GLIM consensus has unified the diagnostic criteria for malnutrition. Prospective studies need to be conducted in the future to validate the clinical effectiveness of the GLIM consensus and establish its association with clinical outcomes. Furthermore, nutritional assessment should be conducted when conditions allow. Nutritional assessment is distinct from diagnosis but encompasses a more comprehensive and detailed evaluation. Nutritional assessment can comprehensively use nutritional indicators and evaluation scales. The Patient-Generated Subjective Global Assessment (PG-SGA) is the most sensitive evaluation scale for gastric cancer patients (44–45). The use of PG-SGA in combination with other assessments, such as anthropometric measurements, body function tests, body composition measurements, and laboratory tests for comprehensive evaluation is recommended. Among the different methods for measuring body composition, the European Working Group on Sarcopenia in Older People (EWGSOP) recommends the use of dual X-ray absorptiometry (DXA) or assessing body composition. DXA and bioelectrical impedance analysis (BIA), the most commonly used instruments in Asia, provide reliable and accurate assessments of skeletal muscle index (SMI). Therefore, AWGS2019 recommends using DXA or multi-frequency BIA to measure SMI in combination with height adjustment (46). In addition, new and more appropriate tools for assessing the nutritional status of gastric cancer patients need to be developed.

In addition, the weight assigned to the first-level indicators of adverse reactions and effect evaluation of EN is relatively high (18.75%). Perioperative EN is relatively safe for gastric cancer, but adverse reactions also exist, particularly after gastrectomy. Implementing proactive measures to prevent adverse reactions and promptly identifying and treating them can reduce pain and discomfort in patients. Timely adjustments to the nutritional program and support methods can reduce the incidence of postoperative complications, improve the treatment effect, and alleviate the condition and burden on the patient. The effectiveness of EN therapy is directly related to the health status and recovery speed of the patient, promotes medical quality, and reduces the incidence of medical complications. Adverse reactions may inevitably occur during the use of EN, but selecting a safer and more effective EN formula and reducing the occurrence of adverse reactions present a challenge to medical workers in clinical practice. Thus far, no guideline or expert consensus exists on establishing a clear and perfect clinical adverse reaction monitoring plan for EN, such as the determination of EN-related diarrhea, gastric retention volume, and appropriate range of blood sugar fluctuations. The prevention and treatment of adverse reactions of EN during the perioperative period of gastric cancer included in this study can provide strong evidence for developing monitoring and management protocols for EN-related adverse reactions in the future. These findings also offer scientific basis and management recommendations for strengthening post-market supervision after the launch of specialized medical-purpose formula food. This study has practical significance for ensuring the effectiveness and safety of EN use among patients. The efficacy evaluation can provide timely feedback on the effect of EN therapy. It can help recognize problems and resolve issues that can potentially arise, thereby improving the management of EN. Consequently, the quality of medical care is enhanced, and optimal medical care is ensured. Considering that the evaluation indicators are relatively simple and easy to obtain, this program mainly recommends body measurements, organism function measurements, laboratory nutrition indexes, and so on. However, this selection may lead to incomplete evaluation indexes. A complete evaluation index system for the effect of EN in gastric cancer patients can be further constructed in the future.

Finally, the first-level indicator of organizational management has the lowest weight, indicating its relatively low importance in the entire program. Although guidelines indicate that the nutritional management of cancer patients requires a multidisciplinary team including nurses, doctors, dietitians, pharmacists, and managers—challenges may arise in clinical practice. The use of a multidisciplinary team model in nutritional management has greatly improved the nutritional status and adverse outcomes of patients in recent years. The results of this study suggest that a multidisciplinary team should include surgeons, endocrinologists, nutritionists, case managers, exercise rehabilitation therapists, nurses, and pharmacists. Nurses play a crucial role in implementing nutritional risk screening and assessment, administering EN programs, and coordinating and communicating communicators between doctors, technicians, and patients. In clinical practice, the leadership role of nurses should be fully utilized to mobilize their proactive initiative. With their specialized knowledge, endocrinologists can provide the most common guidance in the area of nutrition and metabolism. Exercise rehabilitation therapists assist in recovery and promote the effect of EN. Case managers and nurses carry the responsibility of educating patients and their families on implementing the EN program at home. Coordination and cooperation among the entire team are essential in ensuring the successful implementation of the program and attaining scientific management of patient care.

Specificity and universality of the program

The specificity of this program lies in its focus on the clinical characteristics of patients with GC, providing specific nutritional intervention to meet their nutritional needs and promote postoperative recovery. Compared with other diseases, gastric cancer itself may lead to obstruction or dysmotility of the upper digestive tract. Compared with other surgeries, gastrectomy can also directly alter the structure and function of the upper digestive tract, affecting the ability of the patient to eat. Therefore, the use of EN in gastric cancer patients and gastrectomy patients may vary from other diseases and surgeries.Gastrointestinal surgery often leads to impaired intestinal function, characterized by weakened gastrointestinal motility, reduced gastrointestinal secretion, and decreased absorption capacity. EN is a commonly used method for treating malnutrition and is an important means to promote postoperative recovery. EN plays a role in maintaining stable intestinal function, as well as ensuring the balance of energy metabolism and adequate nutritional supply for patients. For patients who require prolonged fasting or have undergone gastrointestinal disconnection, EN can help restore their nutritional status and shorten hospitalization time. Therefore, similar EN strategies may also have potential applications in other malnourished patients with gastrointestinal surgery. However, the nutritional requirements of patients with different diseases and surgeries vary, requiring adjustments and optimizations based on actual conditions. Therefore, the design and adjustments of the EN program should be tailored based on the specific conditions and nutritional needs of patients to ensure the effectiveness and safety of treatment during practical applications.

Limitations

This study acknowledges the limitation of including only experts from China in the two rounds of expert consultations. The lack of evaluations and suggestions from authoritative experts outside of China may introduce a potential bias to the research results. Therefore, if conditions allow in the future, the regional scope of expert consultation can be expanded. In addition, the Kendall harmony coefficients in this study were 0.338 and 0.392, indicating a relatively low level of agreement among the experts; however, the difference between these coefficients was statistically significant (p < 0.001). This result indicates that with a 95% confidence level, the expert opinions are consistent, but the degree of consistency is moderate; the results remain acceptable.

This study developed a complete perioperative EN management plan for gastric cancer. However, the plan has not been implemented clinically owing to limitations related to time, workload, and resources. Therefore, the specific effects of this plan remain unknown. In future research, the plan constructed in this study can be clinically verified. Moreover, the perioperative EN management plan constructed in this study includes an excessive number of evidence-based recommendations and as such may be challenging to implement clinically. Therefore, the implementation of this prevention plan in hospital clinics should consider several factors, including gastric cancer patients, working environment, and hospital conditions to effectively implement the work of improving malnutrition in gastric cancer patients.

During the process of evidence screening in this study, literature retrieval may be incomplete, resulting in the omission of relevant indicators. Consequently, the initial establishment of the indicator system may be incomplete.

This study did not distinguish the effect of different surgical procedure or surgical approach on the use of EN in gastric cancer patients. However, the necessity of EN might depend on the surgical procedure such as total gastrectomy or partial gastrectomy, surgical approach such as laparotomy, laparoscopic or robotic. In the future, the effect of adopting different EN management methods for different surgical procedure or surgical approach can be further clarified. One point for clarification is whether the time to start EN after laparoscopic or robotic surgery can be earlier than laparotomy. Another point is whether the transition from oral nutritional supplements to solid food varies between patients undergoing total gastrectomy and patients undergoing partial gastrectomy.

Conclusions

A perioperative EN management program for GC patients was proposed in this study, which fully considered the practical aspects of clinical nursing, while also demonstrating a high degree of scientific rigor and reliability. The subsequent step is the clinical application of the proposed protocol to verify its effectiveness.

Ethics statement

The authors assume full responsibility for all aspects of the work and have ensured that any questions related to the accuracy or integrity of any part of the study are appropriately investigated and resolved. All experts who participated in the study provided informed consent and volunteered to do so. The study adhered to the principles outlined in the Declaration of Helsinki (as revised in 2013) and was approved by the Institutional Review Board of The Affiliated Jiangning Hospital of Nanjing Medical University.

Authors’ contributions

All authors contributed to the study’s conception and design. Preparation of materials, data collection, and analysis were performed by J.Z., X.N., and X.Z. The initial draft of the manuscript was written by Y.J.G. and X.Z. All authors provided valuable input and feedback on previous versions of the manuscript. All authors read and approved the final manuscript.

Fundings and resource acquisition was coordinated by X.Z. The quality of the research was supervised by A.L., H.L., and D.Y. All participants provided signed informed consent regarding publishing their data.

Disclosure statement

The authors declare that they have no conflicts of interest to disclose.

Additional information

Funding

This study was funded by Nanjing Health Science and Technology Development Special Fund Project [YKK21230].