Gastric cancer is the fifth most common malignant disease and the fourth leading cause of cancer-related death worldwide [1]. Higher incidences of gastric cancer are observed in Asian countries: in Korea, gastric cancer remains the most prevalent malignant disease in male [2]. Despite progress in multidisciplinary treatment, radical gastric resection remains the mainstay of treatment for gastric cancer. After gastrectomy, patients suffer from poor appetite, eating restriction, gastrointestinal symptoms, and malabsorption, which can result in weight loss and nutritional deficits. With improvements in survival of gastric cancer, there is increasing emphasis on patient-centered outcomes, with appropriate management of postoperative nutrition recognized as essential to maintain better quality of life in patients undergoing gastrectomy [3].

Body composition measurement is useful for assessing nutritional status after surgery. Bioelectrical impedance analysis (BIA) is a non-invasive, safe, rapid, and accurate method for evaluating body composition and is increasingly used for nutritional assessment in patients undergoing gastrectomy. Many studies have investigated the impacts of body composition on postoperative outcomes after gastrectomy [4]. After surgery, patients show immediate changes in body composition, including loss of lean body mass (LBM) and fat mass [5,6]. Body composition remains stable or partly improves 6 to 12 months after surgery [7]. Some studies have investigated risk factors for postoperative body composition change, with sex, gastric resection, operative approach, and postoperative complications found to significantly affect body composition after gastrectomy [8,9].

Due to increases in life expectancy, it is becoming more common to operate on elderly patients. According to a nationwide survey in South Korea in 2019, approximately 30% of gastric cancer patients who underwent surgery were older than 70 years, a near threefold increase from 1995 [10]. Elderly patients often have comorbidities and reduced physiologic reserve, resulting in increased operative risk [11]. Furthermore, nutrition status and body composition undergo significant changes with age, represented by decreased muscle mass, increased adiposity, and decreased total body water [11]. We hypothesized that elderly patients experience different body composition changes after gastrectomy compared to non-elderly patients. Identifying such differences would help clinicians to establish appropriate management plans for postoperative care and nutritional support in this patient group. Therefore, the aim of this study was to investigate body composition changes in elderly gastric cancer patients undergoing gastrectomy.

1. Study design

We performed a prospective study of patients who underwent gastrectomy for gastric carcinoma in the Division of Gastroenterologic Surgery at Chonnam National University Hwasun Hospital from June 2019 to June 2021. Exclusion criteria were emergency surgery for bleeding or perforation, chemotherapy or chemoradiation therapy within six months, non-resectional surgery (bypass surgery or exploratory laparotomy), and combined resection of other organs. We screened 251 patients who underwent distal or total gastrectomy for primary gastric cancer. The operative approaches included both laparoscopic and open surgery, and 18 were excluded. Finally, 233 patients were included in the analysis. We divided patients into an elderly group (>70 years) and a non-elderly group (≤70 years) and compared body composition changes between the two groups. This study was approved by the Institutional Review Board at Chonnam National University Hwasun Hospital (CNUHH2019-061). A written informed consent was obtained from all participating patients.

2. Operative technique and postoperative care

Patients underwent distal or total gastrectomy with regional lymph node dissection following South Korean gastric cancer treatment guidelines [12]. Laparoscopic surgery was indicated in most patients except those with very advanced disease, such as extensive lymph node metastasis or large tumor. After distal gastrectomy, Billroth-II or Roux-en Y gastrojejunostomy was performed at the surgeons' discretion. After total gastrectomy, Roux-en esophagojejunostomy was performed in all patients.

Perioperative management followed our institution's enhanced recovery after surgery (ERAS) protocols [13]. In brief, preoperative fasting was avoided, and a carbohydrate-rich drink was administered 2 hours before surgery. No mechanical bowel preparation was performed. Routine insertion of a nasogastric tube or abdominal drainage was not performed. After the operation, patients commenced an oral diet from postoperative day 1. Limited amounts of intravenous fluid were administered only for three postoperative days. Patients were discharged from the hospital starting on postoperative day 6 when they satisfied the predefined discharge criteria.

3. Assessment of body composition

Body composition was measured using segmental multifrequency BIA (InBody S10; InBody, Co. Ltd, Seoul, Korea). We measured body composition preoperatively and at postoperative 1 month, 3 months, 6 months, and 12 months. According to the manufacturer’s protocol, patients were examined before breakfast in the morning. The patients were asked to lie comfortably on a bed while the examiner attached clamp electrodes to both arms and legs.

Using the InBody, we obtained the following data regarding body composition: intracellular water, extracellular water, body weight, skeletal muscle mass (SMM), body fat mass (BFM), percent body fat (PBF), LBM, and body mass index (BMI). Other nutritional information estimated using the InBody was body cell mass (BCM), bone mineral content (BMC), visceral fat area (VFA), and basal metabolic rate (BMR).

4. Statistical analyses

Data are expressed as mean±standard deviation or n (%). Categorical variables were compared using the chi-square or Fisher’s exact test as appropriate and continuous variables using Student’s t-test. A linear mixed model and paired t-test were used to assess differences in body composition changes between the two groups. P-values <0.05 were considered statistically significant. All statistical analyses were performed using SPSS, version 25.0 (IBM Corp., Armonk, NY, USA).

1. Characteristics of patients

Table 1 shows the baseline characteristics of elderly and non-elderly patients. The mean ages of the elderly and non-elderly groups were 75.1±3.9 and 56.5±8.4 years, respectively. The elderly group had higher American Society of Anesthesiologists scores than the non-elderly group. Operative outcomes, such as surgical approach and gastric resection, did not significantly differ between the two groups. However, D2 lymphadenectomy and Billroth II reconstruction were performed more frequently in the elderly group. The two groups showed no significant difference in final pathologic stage. All but 1 patient completed outpatient follow-up for 12 months. There were no deaths during the follow-up period. We obtained Inbody measurements for 216 patients at 1 month, 211 patients at 3 months, 204 patients at 6 months, and 183 patients at 12 months (92.7%, 90.6%, 87.6%, and 78.5% of the entire patient sample, respectively).

Table 1

Patient characteristics

Variable		Non-elderly (n=164)	Elderly (n=69)	P-value
Age (yr)		56.5±8.4	75.1±3.9	<0.001
Sex	Female	52 (31.7)	25 (36.2)	0.503
	Male	112 (68.3)	44 (63.8)
BMI (kg/m2)		24.4±3.2	24.1±3.3	0.489
ASA status	1	62 (37.8)	5 (7.2)	<0.001
	2	101 (61.6)	52 (75.4)
	3	1 (0.6)	12 (17.4)
Abdominal operation history		18 (11.0)	8 (11.6)	0.891
Smoking	None	83 (50.6)	45 (65.2)	0.009
	Current	43 (26.2)	6 (8.7)
	Former	35 (21.3)	18 (26.1)
Operative approach	Open	6 (3.7)	6 (8.7)	0.112
	Laparoscopy	158 (96.3)	63 (91.3)
Gastric resection	Distal	139 (84.8)	58 (84.1)	0.893
	Total	25 (15.2)	11 (15.9)
Lymphadenectomy	D1+	134 (81.7)	48 (69.6)	0.041
	D2	30 (18.3)	21 (30.4)
Reconstruction	Billroth II	69 (42.1)	44 (63.8)	0.002
	Roux-en-Y	95 (57.9)	25 (36.2)
Omentectomy	Partial	149 (90.9)	57 (82.6)	0.073
	Complete	15 (9.1)	12 (17.4)
Tumor size (cm)		2.8±1.6	3.4±1.9	0.599
pTa	T1	127 (77.4)	44 (63.8)	0.098
	T2	18 (11.0)	9 (13.0)
	T3	11 (6.7)	11 (15.9)
	T4	8 (4.9)	5 (7.2)
pNa	N0	138 (84.1)	51 (73.9)	0.250
	N1	12 (7.3)	10 (14.5)
	N2	7 (4.3)	5 (7.2)
	N3	7 (4.3)	3 (4.3)
TNM stagea	Stage I	135 (82.3)	50 (72.5)	0.236
	Stage II	20 (12.2)	13 (18.8)
	Stage III	9 (5.5)	6 (8.7)

Values are presented as mean±standard deviation or number (%).

BMI = body mass index; ASA classification = American Society of Anesthesiologists physical status classification.

^apTNM stages are based on the American Joint Committee on Cancer TNM classification, seventh edition.

Short-term surgical outcomes are presented in Table 2. There was no significant difference in operating time or operative blood loss. The overall morbidities in the elderly and non-elderly groups were 17.4% and 11.6%, respectively, but this difference was not statistically significant. There were also no significant differences between the two groups in length of hospital stay, gas passage day, or diet resumption.

Table 2

Short-term surgical outcomes

Variable	Non-elderly (n=164)	Elderly (n=69)	P-value
Operating time (min)	180.6±63.6	163.5±56.8	0.055
Operative blood loss (mL)	35.5±62.0	30.7±25.8	0.531
Morbidity	19 (11.6)	12 (17.4)	0.234
Local	19 (11.6)	11 (15.9)	0.365
Systemic	2 (1.2)	1 (1.4)	0.887
Mortality	0	0
Harvested lymph nodes	50.6±18.5	55.1±21.1	0.105
Blood transfusion	3 (1.8)	1 (1.5)	0.844
Fever	5 (3.0)	5 (7.2)	0.149
Gas passage (day)	2.7±1.0	2.6±0.8	0.148
Diet resumption (day)	1.8±2.1	1.7±1.6	0.701
Hospital stay (day)	7.5±2.0	7.5±1.5	0.914

Values are presented as mean±standard deviation or number (%).

2. Body composition changes

Fig. 1 shows body composition changes up to postoperative 12 months between the two groups. Overall, body weight, protein, muscle mass, and fat mass decreased immediately after surgery and gradually improved until postoperative 12 months. Interestingly, the decrease in BFM was remarkable until postoperative 12 months compared to body weight, SMM, and LBM changes. When body composition changes were compared between the two groups, a linear mixed model showed no significant time×group interactions for any body composition factors, including body water, protein, SMM, BFM, or LBM.

Fig. 1. Body composition changes in non-elderly and elderly groups. (A) Intracellular water, (B) extracellular water, (C) protein, (D) body weight, (E) body mass index, (F) skeletal muscle mass, (G) body fat mass, (H) percent body fat, (I) lean body mass, (J) body cell mass, and (K) visceral fat area.

Table 3 shows detailed body composition data for the two groups. BFM showed the greatest decrease in both groups (−23.4% in the non-elderly and −26.5% in the elderly). The LBM loss in both groups was around −2.2% at postoperative six months. There were no significant differences in changes of any body composition factors at postoperative 6 and 12 months between the two groups (Fig. 1).

Table 3

Rates of change in body composition in elderly and non-elderly patients

Variable	Baseline			6 months				12 months
	Non-elderly (n=164)	Elderly (n=69)		Non-elderly (n=143)	Elderly (n=61)	P-value		Non-elderly (n=135)	Elderly (n=48)	P-value
ICW (L)	23.7±17.1	19.8±3.7		–3.3±9.2	–3.5±9.9	0.879		–2.5±10.1	–1.9±7.6	0.712
ECW (L)	14.7±10.1	12.7±2.4		–1.7±8.4	–0.9±8.0	0.543		–0.6±10.5	0.1±7.0	0.654
Protein (kg)	10.3±7.4	8.5±1.6		–3.4±8.8	–2.7±8.7	0.593		–2.8±9.5	–3.4±14.2	0.756
Mineral (kg)	3.3±0.7	2.9±0.5		–0.9±8.6	–0.2 ±10.5	0.629		0.7±9.4	1.1±10.5	0.846
BW (kg)	66.9±11.2	61.9±12.4		–9.27±11.3	–8.3±11.7	0.579		–9.0±6.5	–8.0±10.5	0.449
BMI (kg/m2)	24.5±3.2	24.0±3.6		–8.4±7.1	–7.0±12.1	0.285		–9.0±6.6	–6.8±11.4	0.106
SMM (kg)	28.9±22.3	23.7±4.9		–3.7±9.4	–3.1±9.3	0.697		–2.8±9.8	–2.0±8.3	0.614
BFM (kg)	18.3±13.4	18.1±7.6		–23.4±21.8	–26.5±20.6	0.362		–28.1±27.5	–26.8±28.2	0.776
PBF (%)	26.0±8.7	29.0±8.0		–16.8±21.6	–17.1±23.5	0.928		–20.9±25.5	–21.6±27.1	0.874
LBM (kg)	49.5±10.0	43.8±8.2		–2.3±5.4	–2.1±8.4	0.826		–1.5±6.1	–1.1±7.4	0.718
BCM (kg)	32.1±6.6	28.2±5.4		–2.9 ±5.6	–2.9 ±8.6	0.962		–2.0±6.2	–1.8±7.7	0.854
BMC (kg)	2.7±0.6	2.4±0.4		–0.7±9.3	0.4 ±10.9	0.489		1.2±9.9	1.8±10.7	0.744
VFA (cm2)	77.6±37.3	87.0±42.3		–19.7±30.7	–20.0±32.2	0.943		–29.7±30.3	–24.3±36.5	0.323
BMR (kcal)	1,448.6±177.9	1,316.0±177.9		–1.7±7.5	–1.5±6.1	0.823		–1.8±11.5	–0.8±5.3	0.534

Values are presented as mean±standard deviation.

ICW = intracellular water; ECW = extracellular water; BW = body weight; BMI = body mass index; SMM = skeletal muscle mass; BFM = body fat mass; PBF = percent body fat; LBM = lean body mass; BCM = body cell mass; BMC = bone mineral content; VFA = visceral fat area; BMR = basal metabolic rate.

In the present study, we investigated chronologic changes of body composition after gastrectomy and compared such changes between elderly and non-elderly patients. The strength of this study is its prospective design and inclusion of patients receiving standardized perioperative care. We found that changes of body composition, including BMI, LBM, SMM, and fat mass, did not significantly differ between the two groups. This suggests that age does not significantly affect body composition after gastrectomy.

Elderly patients are more vulnerable to surgical stress due to physiological changes in diverse functions associated with aging. Impaired cardiovascular systems and respiratory function and disorders of fluid and electrolyte balance are common in the elderly [11]. Body composition also changes with aging. The proportion of body fat increases and is accompanied by decreases in total body water and SMM [14]. Therefore, sarcopenia is a common age-related clinical problem that increases risk in elderly patients undergoing surgery [15]. Furthermore, LBM loss after surgery is aggravated in the elderly due to several factors. Previous research showed that skeletal muscle protein synthesis tended to be lower in old individuals [16,17]. Immunologic and inflammatory responses to surgical stress, which accelerate muscle catabolism, are more profound in the elderly after surgery [18]. Postoperative oral intake tends to be inadequate in the elderly because of disability, frailty, poor appetite, frequent gastrointestinal symptoms, and socioeconomic conditions. Therefore, elderly patients may require more aggressive and tailored postoperative nutrition support, such as provision of oral nutrition supplementation or a high-protein diet.

Aoyama et al. [8] investigated risk factors for loss of LBM measured using bioelectrical impedance in patients undergoing gastrectomy and showed that infectious surgical complications, total gastrectomy, and male sex were significantly associated with severe LBM loss, but age was not. However, their study examined short-term outcomes and used an arbitrary cut-off value to define severe LBM loss. Therefore, LBM loss could not be compared adequately between the elderly and non-elderly in the study. Meanwhile, in another study comparing weight loss and body composition change in elderly (>70 years) and non-elderly patients, LBM loss was significantly more severe at 1 and 3 months after gastrectomy in elderly patients, while total body weight loss was similar between the two groups [19]. Our study showed that elderly patients had body composition changes similar to those of non-elderly patients. However, the number of elderly patients in our sample was relatively small, and elderly patients were defined as those >70 years of age. Therefore, the impact of age on body composition changes requires further investigation. Identifying differences in body composition changes in the elderly will help clinicians to develop more practical nutritional support plans.

Recently, there has been growing interest in body composition assessment in patients with gastric cancer for nutritional evaluation and prognostication. Body composition can be measured using CT, dual-energy X-ray absorptiometry, and BIA. Among these, BIA is increasingly used because it is a simple, quick, non-invasive method that can assess body composition at the bedside. Previous studies showed that body composition could be used to predict postoperative complications in patients undergoing gastrectomy. In a systematic review including 39 studies of body composition assessment in patients with gastric cancer, preoperative sarcopenia was associated with significantly higher rates of overall postoperative complications and mortality [4]. In a recent prospective study, preoperative lower skeletal mass and high visceral and subcutaneous adipose tissue radiation attenuation were associated with higher risk of major complications after gastrectomy [20]. The type and extent of surgery may impact long-term body mass and composition. Park et al. [7] showed that total gastrectomy resulted in significantly decreased protein mass, BFM, SMM, and VFA compared to distal gastrectomy at postoperative three years. The impact of operative approach (open or laparoscopy) on body composition change is controversial. In a previous study comparing open and laparoscopic distal gastrectomy, patients undergoing laparoscopic surgery showed significantly lower visceral fat loss [9]. However, another study showed no significant difference in loss of body weight and LBM between open and laparoscopic distal gastrectomy [21].

There are some limitations in this study. First, we examined patients treated at a single institution, and most of our patients had early gastric cancer. Due to nationwide screening for gastric cancer in South Korea, more than half of gastric cancer patients are diagnosed at an early stage. Therefore, the results of our study should be validated in another cohort. Second, body composition assessment using the BIA method has limited accuracy in patients with abnormal hydration states due to conditions such as malnutrition, edema, or old age [22]. Last, although we applied a prospective design, some patients failed to return for all visits to undergo body composition measurement. These missing data could influence the results.

In summary, the present study investigated body composition changes in elderly patients undergoing gastrectomy. We found that body composition in the elderly did not significantly differ from that in non-elderly patients. However, our results should be validated in future research. Information about body composition changes will help clinicians to develop practical nutritional support plans for elderly patients.

Conceptualization: OJ. Data curation: JHK, SEK. Formal analysis: OJ, JHK. Funding acquisition: OJ. Investigation: OJ, JHK, MRJ, SEK. Methodology: OJ. Project administration: OJ. Resources: OJ. Supervision: MRJ. Validation: OJ, MRJ. Writing – original draft: JHK. Writing – review & editing: OJ, MRJ.

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

This study was supported by the research fund of the Korean Society of Surgical Metabolism and Nutrition (KSSMN) and a grant (HCRI 19016) from Chonnam National University Hospital Biomedical Research Institute.