Efficacy of high-protein diet protocol and education after distal gastrectomy for gastric cancer patients to prevent loss of lean body mass in Korea: a non-randomized controlled study
Hee Kyung Yoon1, Sun Ae Kim2, Ji Yoon Han3, Dong Jin Kim1
1Department of Surgery, Eunpyeong St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea;
2Department of Nursing, Eunpyeong St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea;
3Department of Clinical Nutrition, Eunpyeong St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea
2Department of Nursing, Eunpyeong St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea;
3Department of Clinical Nutrition, Eunpyeong St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea
Correspondence to: Dong Jin Kim, email: djdjcap@catholic.ac.kr
Received November 13, 2023; Revised March 5, 2024; Accepted March 11, 2024.
© 2024 The Korean Society of Surgical Metabolism and Nutrition and The Korean Society for Parenteral and Enteral Nutrition.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
- Abstract
- Purpose: We studied whether active education of patients about the importance of a high-protein diet can prevent lean body mass loss after gastrectomy for gastric cancer.
Methods: In the study group, intensive high protein diet education and monitoring was performed immediate post operative, 1, 3, and 6 months after surgery. Study group patients were compared with data from the control group formed using propensity matching with the study group for age, sex, resection extent, and TNM stage. Clinicopathologic factors were compared between the groups, and changes in quality of life (QOL) and lean body mass between preoperative levels and 6 months after surgery were assessed.
Results: Among the 100 patients, 31 patients from each group were matched with propensity matching. The groups had no significant clinicopathologic differences. Although the changes in QOL scale and body composition did not differ statistically between the groups, a favorable trend was observed in the study group. Six months after surgery, the mean change in the QOL scale, which measured physical, role, emotional, cognitive, and social functioning, decreased less than the control group or even increased in the study group. In the body composition analysis, the study group showed greater reductions in weight, body mass index, fat mass, and body fat percentage than the control group, and their lean body mass and skeletal muscle mass decreased less.
Conclusion: A high-protein diet protocol and education might increase patient QOL and prevent a decrease in lean body weight 6 months after distal gastric resection. - Keywords : Body mass index; Gastrectomy; Diet, high-protein; Quality of life; Republic of Korea
- Introduction
Background
Gastric cancer is the most common cancer and the fourth most common cause of cancer-related death in the Korea. Globally, it ranks 5th in incidence and was the 4th leading cause of death among all solid cancers, excluding non-melanoma skin cancer, in 2020 [1]. In Korea, new cases of gastric cancer (26,662) ranked 4th (10.8%), followed by thyroid cancer (11.8%), lung cancer (11.7%), and colon cancer (11.2%) in 2020, according to the report of the Korean Central Cancer Registry [2-4]. Thanks to early detection through national and public screening programs and advances in treatment, the proportion of surgically treated early gastric cancer increased from 28.6% in 1995 to 63.6% in 2019, and the 5-year survival rate increased from 43.9% (1993–1995) to 77.5% (2015–2019) [4,5].
As long-term survival has increased, nutritional status and quality of life (QOL) after gastrectomy have become more critical. Because removing or partially removing the stomach, and also vagotomy, can significantly affect the ability to process food and nutrients, gastrectomy makes the digestion of food and absorption of nutrients more challenging and can lead to weight loss and nutrient deficiencies. Therefore, after gastric cancer surgery, appropriate nutritional management and support are crucial for maintaining proper nutritional status.
Specifically, the 2019 Update of the Guidelines published by American Association of Clinical Endocrinologists/The Obesity Society/American Society for Metabolic and Bariatric Surgery (AACE/TOS/ASMBS) recommend that protein intake be individualized, assessed, and guided by a registered dietitian according to sex, age, and weight. A minimal protein intake of 60 g/day and up to 1.2–1.5 g/kg ideal body weight per day should be adequate; higher amounts of protein intake (up to 2.1 g/kg ideal body weight per day) need to be assessed on an individual basis [6].
Despite the importance of protein supplementation, few studies have addressed the role of an education program for post-gastrectomy patients.
Objectives
We analyzed whether a high-protein diet education protocol could prevent the loss of lean body mass during a 6-month follow-up period after gastrectomy. Our goal was to establish and implement a program that can appropriately supply the necessary amount of protein after surgery.
- Methods
Ethics statement
All the participants provided written informed consent before participating in the study. This study was approved by the Institutional Review Board of Eunpyeong St. Mary’s Hospital (IRB No.: PC23RAS10187)
Study design
It is a non-randomized controlled study. It was described according to TREND statement (https://www.cdc.gov/trendstatement/index.html).
Setting/participants
Beginning in May 2021, we planned a high-protein nutrition education program to prevent patients from losing lean body mass after gastric cancer surgery, and this research is an interim analysis conducted to determine whether the program is effective. The original study is a prospective single-arm study requiring 33 patients. The primary endpoint is a decrease in the loss of lean body mass 12 months after surgery, and the research is testing the hypothesis that nutrition education emphasizing protein intake can prevent the loss of lean body mass and improve patient QOL.
We calculated the study population for the single-arm study using the following considerations.
Interventions
Our high-protein diet education protocol involves recording a patient’s protein intake, tracking and monitoring their body mass index (BMI) (including lean body mass), and controlling their protein mass. Our diet education recommends that patients ingest a minimum of 60 g/day of protein for a month after surgery. After that, protein supplements of 1.2 g/kg of ideal body weight/day were recommended. As a practical change, protein powder was added to the post-gastrectomy in-hospital diet immediately after surgery. Nutritional education sessions were performed immediately post-op and 1, 3, and 6 months after surgery. During each diet education session, patients were interviewed about their compliance with the protein intake recommendation, including an examination of meal plans or photographs provided by the patients. The nutritional protocol and examples of patients’ diet reports are available in the Supplement Table 1 and Supplement Fig. 1-3.
Assignment method
Among all 252 patients who underwent gastrectomy for gastric cancer, 100 patients were available with both pre-operative and postoperative 6-month body composition and quality of life data including 32 patients who maintained high-protein education program more than 6 months. Propensity matching was performed between high-protein education group and the others.
Finally, 31 patients were assigned to each group (Fig. 1).
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Fig. 1. Scheme of the study population.
Blinding (masking)
No blinding was done.
Outcome variables
Demographic findings, clinicopathological characteristics, and QOL scale are outcome variables.
Data sources/measurements
Baseline clinicopathological characteristics (age, sex, surgical procedures, extent of resection, and type of anastomosis) were investigated. Age, sex, extent of resection, and TNM stage were used in the propensity matching analysis. Surgical resection was categorized as proximal, distal, and total gastrectomy. The reconstruction method after gastrectomy was classified as Roux-en-Y, Billroth-I, and Billroth-II.
To assess the patients’ nutritional status, a mini-nutritional assessment was conducted preoperatively and 6 months after surgery. When patients organized their diets and brought them to the nutritional sessions, we calculated their protein intake and determined their compliance by comparing how much they consumed with the recommended amount.
To measure QOL, we administered the European Organization for Research and Treatment Center Quality of Life Questionnaire (EORTC QLQ)-C30 (3rd edition) and the Korean version of the EORTC QLQ-STO22. The EORTC QLQ-C30 comprises 30 items about the respondent’s physical, role, emotional, cognitive, and social functioning. The EORTC QLQ-STO22 is specific to gastric cancer, and asks about dysphagia, pain, reflux, dietary restriction, anxiety, dry mouth, body image, and taste alterations [7].
Measurements of body composition, especially lean body weight, were performed using a bioelectrical impedance analysis (BIA) (InBody 770; Biospace Co., Ltd.). Weight, BMI, body fat mass, body fat percentage, and lean body mass (weight excluding fat) were emphasized.
The clinicopathological characteristics, surgical results, QOL before and 6 months after surgery, and body composition profiles were compared between the two propensity-matched groups. As a subgroup analysis, we conducted a within-group analysis of patients from the experimental group who had nutritional assessment compliance of 90% or more.
Bias
To minimize the selection bias, we conducted propensity matching between high-protein intensive nutritional education group and conventional group.
Study size
One-year post-gastrectomy fat-free weight loss was previously reported to be 3.05 kg, with a standard deviation of 2.8 kg [8]. We predicted that, with active high-protein diet education and tracking, the mean difference in fat-free weight loss could be reduced by 1 kg. With a type 1 error of 5% and a dropout rate of 10% taken into consideration, a sample size of 33 individuals was required.
The nutrition education was fully conducted with 32 patients among 33 enrolled patients. One patient was lost to follow-up.
Unit of analysis
The unit of analysis was the same as the unit of assignment.
Statistical methods
The clinicopathologic comparisons were performed using the unpaired student’s test or Wilcoxon’s rank-sum test for continuous variables and Fishers exact test or the chi-square test for categorical variables. To assemble the control group, the propensity score matching used age, sex, extent of resection, and TNM stage. All analyses were performed using SAS (version 9.4; SAS Institute). Statistical significance was set at P<0.05.
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- Results
Participants
Among 252 patients who underwent gastrectomy during the study period, 100 patients, 68 control and 32 study patients, had available QOL and body composition data both preoperatively and 6 months after surgery. After propensity score matching was performed, we compared 31 patients from the control group with 31 patients from the study group. One member of the study group who received a proximal gastrectomy was excluded. The median ages of patients in the control and study groups were 64.10±8.73 and 62.48±9.07 years, respectively. In the control group, 20 patients (64.52%) were male, and 11 (35.48%) were female. In the study group, 21 patients (67.74%) were male, and 10 (32.26%) were female. In the both the control and study groups, all patients received distal gastrectomy (100.0%). The control group and study group did not differ preoperatively in any variables. In the control group, 21 patients (67.74%) were stage 1, 9 patients (29.03%) were stage 2, and 1 patient (3.23%) was stage 3. In the study group, 21 patients (67.74%) were stage 1, 3 patients (9.68%) were stage 2, and 7 patients (22.58%) were stage 3. Stage 2 and stage 3 were grouped together in the analyses and compared with stage 1, so the numerical difference between stage 2 and stage 3 is irrelevant because the sum is the same. These baseline clinicopathological characteristics are summarized in Table 1.
Main results
In the QOL questionnaire completed 6 months after surgery, the study group reported higher global QOL (1.61±29.06), whereas the control group reported a decrease of 1.11±22.18 (P=0.7926). Scores on the physical functioning scale decreased by 4.09±14.47 in the control group and 0.43±13.21 in the study group (P=0.1813). The role functioning scale decreased by 6.99±14.77 in the control group and 3.76±25.35 in the study group (P=0.1861). The emotional functioning scale decreased by 0.54±17.07 in the control group and increased by 8.06±17.01 in the study group (P=0.2148). The cognitive functioning scale decreased by 5.38±16.32 in the control group and increased by 2.15±14.75 in the study group (P=0.0905). The social functioning scale decreased by 5.38±25.96 in the control group and increased by 2.15±26.44 in the study group (P=0.1338). These results are summarized in Table 2 and Fig. 2.
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Fig. 2. Average difference in the quality of life 6 months after surgery between the control group and the study group. QOL = quality of life.
Although none of these findings were statistically significant, the study group showed greater reductions in weight, BMI, fat mass, and body fat percentage than the control group. However, lean body mass and skeletal muscle mass decreased less in the study group than the control group. The control group lost 4.75±4.85 kg in weight, and the study group lost 5.56±3.71 kg (P=0.4596). BMI decreased by 1.45±2.07 in the control group and 2.17±1.36 in the study group (P=0.1764). Body fat mass decreased by 3.40±3.69 kg in the control group and 4.53±3.37 kg in the study group (P=0.2110), and lean body mass decreased by 1.35±2.48 kg in the control group and 1.03±2.95 kg in the study group (P=0.9775). Skeletal muscle mass decreased by 1.30±2.37 kg in the control group and 1.02±2.79 kg in the study group (P=0.9719). Body fat percentage decreased by 3.15%±4.16% in the control group and 4.18%±4.47% in the study group (P=0.1286). These findings are summarized in Table 3 and Fig. 3.
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Fig. 3. Average difference in the Inbody composition analysis 6 months after surgery between the control group and the study group. BMI = body mass index.
When we collected and analyzed only those in the study group with compliance of 90% or more (n=22), the within-group differences from preoperative levels to 6 months post-surgery became more pronounced. The study group with compliance of 90% or more (n=22) lost 4.72±3.01 kg in weight, and their BMI decreased by 1.90±1.11, body fat mass decreased by 3.99±3.00 kg, muscle mass decreased by 0.74±3.10 kg, and body fat percentage decreased by 4.41%±4.52%. Whereas the control group (n=31) lost 1.35±2.48 kg of lean body mass, the study group with compliance of 90% or more (n=22) lost only 0.73±3.28 kg, less than both the control group and the overall study group (n=31, 1.4±2.1 kg). These findings are summarized in Table 3 and Fig. 4.
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Fig. 4. Mean difference in the body composition loss analysis 6 months after surgery in the study population with good compliance. BMI = body mass index.
- Discussion
Key results
This study reports an interim analysis of a prospective study of the potential of education about a high-protein diet to minimize lean body loss after gastrectomy. Whereas the original single-arm study had an endpoint of 1 year postoperatively, this study compared the study group with a control group 6 months after surgery.
This study does not show statistical significance in preventing lean body loss and QOL deterioration. However, the study group showed a definitive tendency, especially among those whose diet education compliance was more than 90%, toward better QOL and a smaller decrease in lean body and muscle mass.
Interpretation/comparison with previous researches
The QOL comparison revealed higher QOL in the group that received dietary education. More research is needed to understand why cognitive function declined more in the control group than the study group, but studies have indicated that protein intake is generally associated with cognitive function in elderly patients. One study showed that dietary protein intake and protein intake from total animal, total meat, eggs, and legumes was positively associated with cognitive function in adults aged 60 years and older, and higher milk and milk product consumption was negatively associated with cognitive function [9].
In the examination of body composition, both fat-free weight and skeletal muscle mass decreased less in the study group than the control group. Weight, fat mass, body fat percentage, and BMI all decreased more in the control group, and that difference was more pronounced in study patients whose compliance was above 90%. Weight loss and BMI loss were arithmetically larger than in the control group, but it is meaningful that much of that weight loss was caused by body fat loss rather than lean body loss. In fact, a protein diet is emphasized after variational surges specifically to induce weight loss while minimizing muscle mass loss. Therefore, our goal was to prevent lean body loss rather than weight loss.
Extensive research has been conducted on post-gastric-cancer-surgery malnutrition, weight loss, and variations based on surgical techniques [10]. However, there has been a deficiency in proactive planning and education about nutritional supplementation, which was the focus of this study. Weight loss after gastric cancer surgery is particularly attributed to protein deficiency, rather than carbohydrate or fat deficiency. Additionally, deficiencies in nutrients such as iron; vitamin B-12; thiamine; folic acid; zinc; calcium; fat-soluble vitamins A, D, E, and K; and other micronutrients can contribute to lean body loss. Protein deficiency leads to muscle wasting, which also reduces QOL and increases the mortality rate. In this study, we found that education about a high-protein diet can improve QOL and reduce the loss of lean body weight and skeletal muscle mass.
The Inbody BIA test is the method most widely used in the actual clinical field and is easily measured with simple equipment. In recent years, the frequency of the current has been varied, and it is now possible to measure extracellular fluid and intracellular fluid separately. Restraints are calculated at a standardized rate according to race, sex, and age [11]. Because BIA focuses on total body water measurement, the results can differ according to water intake or excretion. However, the reproducibility of body composition analyses measured through BIA seems to be very high, and it shows good agreement with other test methods. Studies comparing the measurement results from the Inbody test and Dual Energy X-ray Absorptiometry (DEXA, the current clinical gold standard) in obese adults indicate that the Inbody test has high correlation or no significant difference from DEXA [12,13]. However, another study shows that the results differ somewhat depending on age, sex, and obesity, so more research is needed [14].
In this study, QOL was measured using the EORTC QOL-C30 questionnaire, which is an appropriate framework for a large, international patient sample with different cancer sites and stages. Although QOL was not the main issue addressed by our educational program, we wanted to compare the changing patterns of QOL in the intensively educated patients with control patients because we hypothesized that the feeling of comprehensive management might improve the patients’ QOL. Although we found no statistical significance, there was a definite tendency toward a smaller decrease in QOL in the study group. Because the number of subjects in this study was determined using the estimated lean body loss change 1 year after surgery, our sample size might be insufficient to show significance after 6 months.
The strengths of this study include our attempt to implement nutritional education, which is not often conducted, and the specific establishment of a diet emphasizing protein. Second, our results actually demonstrate a favorable tendency toward reducing lean body mass loss, which makes our program applicable in actual clinical practice. Third, compliance was monitored. From those strengths, we expect to find favorable results in our 1-year follow-up result.
Limitations
It is a retrospective analysis and a pilot study, which might have led to an inability to observe significant differences. Second, this study was conducted with an insufficient number of patients from a single center. Although the number of subjects was set according to the Lipids in Health and Disease (2018) report that the loss of lean body weight in the first year after gastric cancer surgery was 3.05 kg with a standard deviation of 2.8 kg, it might be insufficient to show significance in a comparative analysis with an observed mean lean body loss 1.35 kg and a standard deviation of 2.48 kg. Third, it was difficult to accurately calculate the protein intake of the historical control group. Therefore, it is difficult to determine the direct correlation and causal relationship between nutritional education and protein intake. Continuing study is required.
Conclusion
This study has demonstrated that emphasizing a high-protein diet and implementing an education protocol tended to prevent a decrease in lean body weight. However, longer follow-up and a large-scale multicenter study are needed to demonstrate the role of intensive high-protein diet education.
- Authors’ contribution
Conceptualization: DJK. Data curation: DJK, JYH. Formal analysis: DJK. Funding acquisition: DJK. Investigation: DJK. Methodology: SAK. Project administration: JYH, SAK. Resources: DJK. Software: DJK. Supervision: DJK. Validation: DJK, JYH. Visualization: HKY. Writing – original draft: HKY, DJK. Writing – review & editing: all authors.
- Conflict of interest
- The authors of this manuscript have no conflicts of interest to disclose.
- Funding
- This study was conducted with funds from the Korean Society of Surgical Metabolism and Nutrition (No.: KSSMN 2020-005).
- Data availability
- Raw data is not available due to institutional principle.
- Acknowledgments
- All authors thank So Ra Kim, who supported us with data management and administrative work.
- Supplementary materials
Supplementary materials can be found via https://doi.org/10.15747/ACNM.2024.16.1.10
Supplement Table 1. Nutritional protocol after gastrectomy in Eunpyeong St. Maryʼs Hospital.
Supplement Fig. 1. Nutrition counseling service named smart nutrition learning-mate.
Supplement Fig. 2. Example of patient reported diet schedule #1.
Supplement Fig. 3. Example of patient reported diet schedule #2.
acnm-16-1-10-supple.zip
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Author ORCID Information-
- Hee Kyung Yoon
https://orcid.org/0009-0009-1590-003X - Sun Ae Kim
https://orcid.org/0009-0006-2947-7832 - Ji Yoon Han
https://orcid.org/0009-0008-4901-9905 - Dong Jin Kim
https://orcid.org/0000-0001-5103-5607
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