Association of preoperative body mass index with postoperative complications and survival for patients with gastric cancer: A systematic review and meta-analysis

Zhenzhen Li; Lili Cui; Jing Sun; Wanlu Liu

doi:10.1371/journal.pone.0317985

. 2025 Jan 28;20(1):e0317985. doi: 10.1371/journal.pone.0317985

Association of preoperative body mass index with postoperative complications and survival for patients with gastric cancer: A systematic review and meta-analysis

Zhenzhen Li ^1,^*, Lili Cui ¹, Jing Sun ¹, Wanlu Liu ¹

Editor: Valeria Guglielmi²

PMCID: PMC11774357 PMID: 39874306

Abstract

Objective

The relationship among body mass index (BMI), postoperative complications, and clinical outcomes in patients undergoing gastrectomy for gastric cancer remains unclear. This study aimed to evaluate this association using a meta-analysis.

Method

We conducted a systematic search of the PubMed, Embase, and Cochrane Library databases up to February 25, 2024. Patients were classified into underweight (<18.5 kg/m²), normal weight (18.5–25.0 kg/m²), and overweight (≥25.0 kg/m²) groups based on BMI categories. Meta-analysis was performed using a random-effects model. Additionally, exploratory sensitivity and subgroup analyses were performed.

Results

Twenty-two studies involving 41,144 patients with gastric cancer were included for quantitative analysis. Preoperative underweight (odds ratio [OR]: 1.26; 95% confidence interval [CI]: 1.03–1.55; P = 0.024) and overweight (OR: 1.19; 95%CI: 1.09–1.30; P <0.001) were associated with an increased risk of postoperative complications. Furthermore, preoperative underweight was associated with poorer overall survival (hazard ratio [HR]: 1.40; 95%CI: 1.28–1.53; P <0.001), whereas preoperative overweight was associated with better over-survival (HR: 0.82; 95%CI: 0.73–0.91; P <0.001). Furthermore, preoperative underweight was not associated with disease-free survival (HR: 1.48; 95%CI: 0.97–2.26; P = 0.069), whereas preoperative overweight was associated with longer disease-free survival (HR: 0.80; 95%CI: 0.70–0.91; P = 0.001). In terms of specific postoperative complications, preoperative underweight was associated with an increased risk of septic shock (OR: 3.40; 95%CI: 1.26–9.17; P = 0.015) and a reduced risk of fever (OR: 0.39; 95%CI: 0.18–0.83; P = 0.014). Preoperative overweight was associated with an increased risk of wound infections (OR: 1.78; 95%CI: 1.08–2.93; P = 0.023), intestinal fistula (OR: 5.23; 95%CI: 1.93–14.21; P = 0.001), arrhythmia (OR: 6.38; 95%CI: 1.70–24.01; P = 0.006), and pancreatic fistula (OR: 3.37; 95%CI: 1.14–9.96; P = 0.028).

Conclusion

This study revealed that both preoperative underweight and overweight status were associated with an increased risk of postoperative complications. Moreover, the postoperative survival outcomes were significantly better in overweight compared to that of underweight patients.

Trial registration

Registration: INPLASY202480004.

Background

Gastric cancer (GC) is the fifth most common malignancy and the third leading cause of cancer-related mortality globally [1]. Anatomically, GC is categorized into two types: cardia and non-cardia cancers, with China contributing to 70% of new cardia cases and 50% of new non-cardia cases worldwide [1,2]. Over recent decades, the global incidence of GC has declined, largely due to successful management of modifiable risk factors such as eradication of Helicobacter pylori infection, dietary improvements, regulation of body mass index (BMI), and reduction in smoking and alcohol consumption [3,4]. Currently, surgery is the primary treatment for GC [5,6]. Moreover, factors influencing the prognosis of GC have garnered considerable attention, contributing to a more precise preoperative risk assessment. Four primary risk factors for GC include preoperative carcinoembryonic antigen levels and cancer antigen 19–9 levels, systemic inflammation, and perioperative blood transfusion. These factors have been proven to be significantly correlated with the prognosis of patients with GC [7,8]. In addition to these established risk factors, the health condition of patients with GC is also an important factor affecting their prognosis [9].

Accumulating evidence suggests that nutritional status is associated with the prognosis of various types of cancer [10–12]. Additionally, BMI is a commonly used measure in population-level studies, which provides a general indication of body mass relative to height. Numerous studies have identified a low BMI as an important predictive factor for poor prognosis in patients [13–15]; however, some studies have reported no association between BMI and oncological outcomes [16,17]. Notably, patients with excessive obesity tend to have lower survival rates. However, several studies have revealed that obese patients with cancer have longer survival periods [18–20]. Fat and muscle secrete various hormones and cytokines that may influence the survival of patients with cancer based on body composition [21,22]. These inconsistent results are not solely attributable to variations in patient inclusion and BMI classification. Thus, the relationship between BMI and GC prognosis necessitates further investigation. In this study, we conducted a systematic review and meta-analysis to elucidate the potential association between preoperative BMI and the risk of postoperative complications, and survival outcomes in patients with GC.

Methods

Search strategy and selection criteria

The Meta-analysis of Observational Studies in Epidemiology protocol checklist [23] and Preferred Reporting Items for Systematic Reviews and Meta-analyses guidelines [24] were used to conduct and report the meta-analysis. This study was conducted according to the Preferred Reporting of Systematic Reviews and Meta-analyses (PRISMA) guidelines and was registered on the INPLASY platform (No. INPLASY202480004). Studies published in English and Chinese on the association between preoperative BMI, postoperative complications, and survival outcomes in patients with GC met the inclusion criteria without restrictions on publication status. We searched the PubMed, EmBase, and Cochrane Library databases, selecting studies meeting the criteria published up to February 25, 2024, using the following search terms: “gastric cancer,” “underweight,” “overweight,” “obesity,” and “body mass index.” The reference lists of the retrieved studies were manually reviewed to identify new potentially relevant studies.

The study selection process was conducted independently by two reviewers, and any disagreements between them were resolved by discussion until a consensus was reached. Studies were selected on the basis of their titles, designs, exposures, and outcomes. Studies were included based on the following criteria. (1) Patient demographics: all participants were diagnosed with GC and underwent surgery. (2) Exposure: this included patients who were preoperatively underweight, with a BMI less than 18.5 kg/m², and those preoperatively overweight, with a BMI of 25.0 kg/m² or more. (3) Control group: the control group comprised individuals with normal weight, defined as those with a BMI of 18.5–25.0 kg/m². (4) Outcomes assessed: we focused on postoperative complications, overall survival (OS), and disease-free survival (DFS). (5) Study design: there were no limitations in the type of study design, encompassing both prospective and retrospective cohorts.

Data collection and quality assessment

The information and data were extracted by one reviewer and verified by the other. The details of the abstracted information included the first author’s name, publication year, region, study design, inclusion period, sample size, age, proportion of men, BMI categories, type of gastrectomy, tumor node metastasis stage, reported effect estimates, and outcomes. The quality of the included studies was evaluated using the Newcastle-Ottawa Scale (NOS), with a maximum score of 9 for each individual study. Studies scoring 0–3, 4–6, and 7–9 were categorized as low, moderate, and high quality, respectively [25]. Any discrepancies in in data collection and quality assessment between reviewers were resolved by a third reviewer who consulted the original article.

Statistical analysis

The association between preoperative BMI and the risk of postoperative and specific complications was assigned as a categorical variable, and odds ratios (OR) with 95% confidence intervals (CI) were calculated based on the crude data before data pooling. The relationship between preoperative BMI and OS or disease-free survival (DFS) was calculated based on the effect estimates in each study, and hazard ratios (HR) with 95% CIs were calculated. Subsequently, a random-effects model was used to pool effect estimates regarding the association between preoperative BMI, postoperative complications, and survival outcomes, considering the underlying variations among the included studies [26,27]. Statistical heterogeneity was assessed using I² and Cochran’s Q statistics, and significant heterogeneity was defined as I² >50.0% or P <0.10 [28,29]. Sensitivity analyses were performed for postoperative complications, OS, and DFS to assess the robustness of the pooled conclusions by sequentially removing each study [30]. Furthermore, subgroup analyses were performed for postoperative complications, OS, and DFS according to country, age, proportion of male, study quality, and interaction, and the P test with a ratio of effect estimates was used to compare differences between subgroups [31]. Publication bias was assessed using both qualitative and quantitative methods, including funnel plots and the Egger-Begg test results [32,33]. All P values reported in this study were two-sided, with a significance level of 0.05. Statistical analyses were performed using the Stata software (version 10.0; StataCorp, College Station, Texas, USA).

Results

Search results

An electronic search yielded 1,724 articles, of which 1,246 were included after eliminating duplicates. In total, 1,188 studies were excluded because they reported irrelevant topics. 58 studies were downloaded for full-text evaluation, and 36 were discarded because they reported GC risk (n = 16), other BMI categories (n = 13), or the same population (n = 7). Ultimately, 22 retrospective cohort studies were included in the meta-analysis [13–15,17,19,34–50], and no additional eligible studies were identified after manually reviewing the reference lists of the retrieved studies (Fig 1).

Study characteristics

Table 1 summarizes the baseline characteristics of the included studies and patients. All studies were retrospective cohorts involving 41,144 patients with GC. Nineteen studies were conducted in Eastern countries (China, Japan, and Korea), whereas the remaining three were conducted in Western countries (USA and Italy). The mean age of the patients included in the studies ranged from 55.4–78.5 years, and the proportion of male in each study varied from 52.0–78.9%. The quality of the studies was assessed using the NOS, with 3, 13, and 6 studies receiving scores of 8, 7, and 6, respectively (S1 Table).

Table 1. The baseline characteristics of included studies and involved patients.

Study	Region	Study design	Inclusion period	Sample size	Age (years)	Male (%)	BMI categories (kg/m²)	Type of gastrectomy	TNM stage	Study quality
Pacelli 2008 [34]	Italy	Retrospective	2000–2006	196	65.5	61.2	< 18.5; 18.5–24.9; 25.0–29.9; ≥30.0	Exploratory laparotomy (27); gastroenteric by-pass (9); total gastrectomy (55); distal subtotal gastrectomy (90); other (15)	I-IV	6
Nozoe 2012 [35]	Japan	Retrospective	1998–2010	308	67.5	70.5	< 18.5; 18.5–24.9; ≥25.0	Total gastrectomy (100); distal subtotal gastrectomy (208)	I-IV	7
Yasunaga 2013 [36]	Japan	Retrospective	2010	15582	69.1	68.6	< 18.5; 18.5–24.9; 25.0–29.9; ≥30.0	NA	I-III	6
Kim 2014 [37]	Korea	Retrospective	2005–2008	304	60.0	68.1	< 18.5; 18.5–24.9; 25.0–29.9; ≥30.0	Total gastrectomy (74); distal subtotal gastrectomy (230)	I-III	7
Wong 2014 [38]	USA	Retrospective	1997–2012	186	67.0	52.0	< 18.5; 18.5–24.9; 25.0–29.9; ≥30.0	Distal gastrectomy (68); total gastrectomy (64); proximal gastrectomy (2); wedge resection (1)	I-III	7
Chen 2015 [19]	China	Retrospective	2000–2010	1248	58.0	72.8	< 18.5; 18.5–24.9; ≥25.0	Distal gastrectomy (681); total gastrectomy (329); proximal gastrectomy (238)	I-IV	7
Ejaz 2015 [39]	USA	Retrospective	2000–2012	775	65.9	57.5	< 18.5; 18.5–24.9; 25.0–29.9; ≥30.0	Total gastrectomy (462); distal subtotal gastrectomy (313)	I-III	7
Wada 2015 [40]	Japan	Retrospective	2001–2005	427	66.0	70.3	< 18.5; 18.5–24.9; ≥25.0	Total gastrectomy (126); distal subtotal gastrectomy (301)	I-IV	7
Migita 2016 [41]	Japan	Retrospective	2003–2011	638	67.1	72.6	< 18.5; 18.5–24.9; ≥25.0	NA	I-III	7
Lee 2016 [42]	Korea	Retrospective	2000–2008	1909	58.3	67.9	< 18.5; 18.5–24.9; ≥25.0	Distal gastrectomy (1354); total gastrectomy (550); proximal gastrectomy (1)	I-IV	6
Feng 2018 [43]	China	Retrospective	2008–2015	1210	59.0	78.4	< 18.5; 18.5–24.9; ≥25.0	Distal gastrectomy (32); total gastrectomy (114); proximal gastrectomy (7)	I-III	8
Lee 2018 [13]	Korea	Retrospective	2000–2016	7765	58.6	66.4	< 18.5; 18.5–24.9; 25.0–29.9; ≥30.0	Total gastrectomy (1865); subtotal gastrectomy (5534); functional gastrctomy (366)	I-III	6
Park 2018 [44]	Korea	Retrospective	2009–2013	2063	60.1	68.3	< 18.5; 18.5–24.9; ≥25.0	Distal gastrectomy (1603); total gastrectomy (334); proximal gastrectomy (105); pylorus-preserving gastrectomy (21)	I-III	8
Kim 2018 [45]	Korea	Retrospective	2004–2010	510	60.9	66.5	< 18.5; 18.5–24.9; ≥25.0	Total gastrectomy (111); subtotal gastrectomy (399)	I-IV	7
Wang 2018 [46]	China	Retrospective	2011–2016	827	61.4	72.1	< 18.5; 18.5–24.9; ≥25.0	NA	I-IV	7
Han 2018 [47]	China	Retrospective	2007–2010	788	59.0	77.5	< 18.5; 18.5–24.9; ≥25.0	NA	I-IV	6
Zhang 2019 [48]	China	Retrospective	2015–2017	426	55.4	66.9	< 18.5; 18.5–24.9; ≥25.0	Distal gastrectomy (365); total gastrectomy (45); proximal gastrectomy (16)	I-IV	6
Park 2020 [14]	Korea	Retrospective	2006–2010	1868	57.8	67.1	< 18.5; 18.5–24.9; 25.0–29.9; ≥30.0	Total gastrectomy (708); subtotal gastrectomy (1160)	II-III	7
Miyasaka 2020 [49]	Japan	Retrospective	2004–2018	440	66.3	69.3	< 18.5; 18.5–24.9; ≥25.0	Total gastrectomy (440)	I-III	7
Zhao 2021 [17]	China	Retrospective	2003–2011	871	NA	74.7	< 18.5; 18.5–24.9; ≥25.0	Distal gastrectomy (469); total gastrectomy (258); proximal gastrectomy (144)	I-III	7
Ma 2021 [15]	China	Retrospective	2013–2018	2526	NA	78.9	< 18.5; 18.5–24.9; 25.0–29.9; ≥30.0	Radical gastrectomy (2526)	I-III	8
Jeong 2023 [50]	Korea	Retrospective	2007–2015	277	78.5	66.7	< 18.5; 18.5–24.9; ≥25.0	Distal gastrectomy (173); total gastrectomy (64)	II-III	7

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Postoperative complications

Fourteen studies reported an association between preoperative BMI and the risk of postoperative complications. Preoperative underweight (OR: 1.26; 95%CI: 1.03–1.55; P = 0.024) and overweight (OR: 1.19; 95%CI: 1.09–1.30; P <0.001) were associated with an elevated risk of postoperative complications (Fig 2). There was significant heterogeneity in preoperative underweight status (I² = 48.6%; P = 0.021), whereas there was not in preoperative overweight status (I² = 12.1%; P = 0.320). Sensitivity analysis revealed that the association between preoperative underweight status and risk of postoperative complications varied, whereas the relationship between preoperative overweight status and postoperative complications remained robust (S1 and S2 Figs).

For specific postoperative complications, preoperative underweight was associated with an increased risk of septic shock (OR: 3.40; 95%CI: 1.26–9.17; P = 0.015) and a reduced risk of fever (OR: 0.39; 95%CI: 0.18–0.83; P = 0.014). Moreover, preoperative overweight was associated with an increased risk of wound infections (OR: 1.78; 95%CI: 1.08–2.93; P = 0.023), intestinal fistula (OR: 5.23; 95%CI: 1.93–14.21; P = 0.001), arrhythmia (OR: 6.38; 95%CI: 1.70–24.01; P = 0.006), and pancreatic fistula (OR: 3.37; 95%CI: 1.14–9.96; P = 0.028). No other significant associations were observed between preoperative BMI and the risk of specific postoperative complications (Table 2).

Table 2. The summary results for specific postoperative complications.

Outcomes	BMI categories	Number of studies	OR and 95%CI	P value	I² (%)	P value for heterogeneity
Pneumonia	Underweight	5	1.00 (0.41–2.44)	0.998	67.2	0.016
Pneumonia	Overweight	5	1.25 (0.91–1.72)	0.166	0.0	0.968
Abdominal abscess	Underweight	3	1.38 (0.60–3.20)	0.451	0.0	0.611
Abdominal abscess	Overweight	3	1.02 (0.55–1.90)	0.951	0.0	0.873
Septic shock	Underweight	2	3.40 (1.26–9.17)	0.015	0.0	0.388
Septic shock	Overweight	2	1.24 (0.39–3.93)	0.718	0.0	0.344
Anastomotic leak	Underweight	6	1.18 (0.55–2.51)	0.672	0.0	0.657
	Overweight	6	1.41 (0.73–2.72)	0.312	18.0	0.297
Wound dehiscence	Underweight	1	0.44 (0.02–8.21)	0.581	-	-
Wound dehiscence	Overweight	2	2.16 (0.48–9.79)	0.317	0.0	0.868
Gastrointestinal perforation, obstruction, and ischemia	Underweight	1	1.61 (0.06–41.17)	0.774	-	-
Gastrointestinal perforation, obstruction, and ischemia	Overweight	1	0.90 (0.06–14.67)	0.943	-	-
Hemoperitineum	Underweight	3	2.23 (0.71–7.03)	0.172	0.0	0.375
Hemoperitineum	Overweight	3	1.92 (0.51–7.18)	0.331	38.7	0.196
Wound infections	Underweight	3	0.77 (0.35–1.69)	0.521	0.0	0.942
Wound infections	Overweight	3	1.78 (1.08–2.93)	0.023	0.0	0.503
Urinary tract infections	Underweight	3	2.35 (0.56–9.92)	0.246	0.0	0.394
Urinary tract infections	Overweight	3	0.81 (0.22–2.93)	0.749	0.0	0.890
Nausea	Underweight	1	1.67 (0.66–4.20)	0.278	-	-
Nausea	Overweight	1	1.94 (0.85–4.46)	0.117	-	-
Gastroparesis	Underweight	2	0.74 (0.26–2.11)	0.576	0.0	0.643
Gastroparesis	Overweight	2	1.11 (0.59–2.11)	0.740	0.0	0.837
Mechanical obstruction	Underweight	2	2.71 (0.23–32.34)	0.431	68.2	0.076
Mechanical obstruction	Overweight	2	1.02 (0.41–2.50)	0.969	0.0	0.756
Ileus	Underweight	2	1.29 (0.31–5.36)	0.729	30.8	0.229
Ileus	Overweight	2	1.44 (0.52–3.99)	0.480	0.0	0.544
Intestinal fistula	Underweight	2	2.46 (0.30–20.02)	0.399	37.9	0.205
Intestinal fistula	Overweight	2	5.23 (1.93–14.21)	0.001	0.0	0.570
Gastrointestinal hemorrhage	Underweight	1	5.78 (0.36–92.84)	0.216	-	-
Gastrointestinal hemorrhage	Overweight	1	10.08 (0.91–111.73)	0.060	-	-
Diarrhea	Underweight	1	1.14 (0.05–23.94)	0.931	-	-
Diarrhea	Overweight	1	0.99 (0.05–20.78)	0.997	-	-
Arrhythmia	Underweight	1	1.44 (0.16–12.96)	0.745	-	-
Arrhythmia	Overweight	1	6.38 (1.70–24.01)	0.006	-	-
Pleural effusion	Underweight	3	1.28 (0.16–10.33)	0.815	79.0	0.009
Pleural effusion	Overweight	3	0.82 (0.35–1.90)	0.637	0.0	0.571
ARDS	Underweight	1	3.87 (0.64–23.33)	0.140	-	-
ARDS	Overweight	1	0.71 (0.04–13.78)	0.820	-	-
Heart failure	Underweight	1	1.14 (0.05–23.94)	0.931	-	-
Heart failure	Overweight	1	2.50 (0.23–27.75)	0.455	-	-
Renal failure	Underweight	1	3.87 (0.64–23.33)	0.140	-	-
Renal failure	Overweight	1	1.67 (0.17–16.11)	0.659	-	-
Liver failure	Underweight	1	5.78 (0.36–92.84)	0.216	-	-
Liver failure	Overweight	1	1.66 (0.07–40.85)	0.757	-	-
CNS complications	Underweight	1	1.92 (0.20–18.59)	0.573	-	-
CNS complications	Overweight	1	1.67 (0.17–16.11)	0.659	-	-
Pancreatic fistula	Underweight	2	1.08 (0.13–9.26)	0.945	0.0	0.463
Pancreatic fistula	Overweight	2	3.37 (1.14–9.96)	0.028	0.0	0.727
Fever	Underweight	1	0.39 (0.18–0.83)	0.014	-	-
Fever	Overweight	1	1.17 (0.68–2.01)	0.571	-	-
Chyle leakage	Underweight	1	1.61 (0.31–8.43)	0.572	-	-
Chyle leakage	Overweight	1	0.36 (0.02–6.53)	0.488	-	-
Incisional hernia	Underweight	1	0.28 (0.04–2.07)	0.211	-	-
Incisional hernia	Overweight	1	1.37 (0.70–2.69)	0.361	-	-
Hemorrhage	Underweight	1	0.87 (0.36–2.11)	0.754	-	-
Hemorrhage	Overweight	1	0.94 (0.54–1.64)	0.821	-	-
Thrombus	Underweight	1	0.78 (0.10–6.18)	0.818	-	-
Thrombus	Overweight	1	0.84 (0.23–3.05)	0.793	-	-

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Subgroup analyses of the association between preoperative BMI and risk of postoperative complications were also performed, as shown in Table 3. We noted that preoperative underweight status was associated with an elevated risk of postoperative complications when pooled studies were conducted in Eastern countries; the mean age of the patients was <65.0 years, and the proportion of male patients was <70.0%. Moreover, preoperative overweight was associated with an increased risk of postoperative complications in studies conducted in Eastern countries, particularly when the mean age of the patients was <65 years, irrespective of the proportion of male and study quality. Finally, it was observed that the association between preoperative underweight and the risk of postoperative complications could be influenced by the mean age of patients (OR: 0.67; 95%CI: 0.47–0.97; P = 0.032).

Table 3. Subgroup analyses for postoperative complications, overall survival, and disease-free survival.

Outcomes	Factors	Subgroups	BMI categories	Number of studies	OR and 95%CI	P value	I² (%)	P value for heterogeneity	Ratio between subgroups for underweight	Ratio between subgroups for overweight
Postoperative complications	Country	Eastern	Underweight	12	1.28 (1.02–1.60)	0.033	55.2	0.011	1.07 (0.61–1.88); P = 0.823	1.23 (0.93–1.64); P = 0.143
		Eastern	Overweight	12	1.21 (1.11–1.33)	< 0.001	12.8	0.320
		Western	Underweight	2	1.20 (0.71–2.01)	0.497	0.0	0.389
		Western	Overweight	2	0.98 (0.75–1.28)	0.892	0.0	0.643
	Age (years)	≥ 65.0	Underweight	7	1.12 (0.99–1.26)	0.081	0.0	0.720	0.67 (0.47–0.97); P = 0.032	0.88 (0.69–1.12); P = 0.283
		≥ 65.0	Overweight	7	1.13 (0.95–1.36)	0.164	28.5	0.211
		< 65.0	Underweight	5	1.66 (1.19–2.34)	0.003	49.1	0.097
		< 65.0	Overweight	5	1.29 (1.10–1.52)	0.002	12.4	0.335
	Male (%)	≥ 70.0	Underweight	6	1.12 (0.82–1.52)	0.493	29.7	0.212	0.81 (0.53–1.23); P = 0.320	1.19 (0.96–1.48); P = 0.114
		≥ 70.0	Overweight	6	1.37 (1.12–1.68)	0.002	31.4	0.200
		< 70.0	Underweight	8	1.39 (1.03–1.85)	0.029	61.1	0.012
		< 70.0	Overweight	8	1.15 (1.06–1.24)	< 0.001	0.0	0.638
	Study quality	High	Underweight	10	1.27 (0.93–1.74)	0.138	49.5	0.037	1.00 (0.65–1.53); P = 1.000	1.05 (0.87–1.27); P = 0.608
		High	Overweight	10	1.23 (1.04–1.47)	0.019	34.0	0.136
		Moderate	Underweight	4	1.27 (0.95–1.70)	0.103	59.1	0.062
		Moderate	Overweight	4	1.17 (1.08–1.27)	< 0.001	0.0	0.786
Overall survival	Country	Eastern	Underweight	11	1.40 (1.27–1.53)	< 0.001	0.0	0.702	0.97 (0.61–1.54); P = 0.883	0.99 (0.60–1.63); P = 0.962
		Eastern	Overweight	11	0.81 (0.72–0.90)	< 0.001	41.0	0.075
		Western	Underweight	2	1.45 (0.92–2.29)	0.112	0.0	0.604
		Western	Overweight	2	0.82 (0.50–1.35)	0.435	64.8	0.092
	Age (years)	≥ 65.0	Underweight	4	1.57 (1.16–2.12)	0.003	0.0	0.866	1.14 (0.83–1.57); P = 0.428	1.15 (0.78–1.69); P = 0.488
		≥ 65.0	Overweight	4	0.86 (0.59–1.25)	0.420	68.9	0.022
		< 65.0	Underweight	7	1.38 (1.24–1.53)	< 0.001	0.0	0.495
		< 65.0	Overweight	7	0.75 (0.68–0.82)	< 0.001	0.0	0.663
	Male (%)	≥ 70.0	Underweight	5	1.44 (1.28–1.62)	< 0.001	0.0	0.767	1.07 (0.89–1.28); P = 0.490	1.19 (0.98–1.44); P = 0.085
		≥ 70.0	Overweight	5	0.89 (0.78–1.01)	0.079	26.6	0.244
		< 70.0	Underweight	8	1.35 (1.17–1.55)	< 0.001	0.0	0.633
		< 70.0	Overweight	8	0.75 (0.65–0.87)	< 0.001	36.4	0.138
	Study quality	High	Underweight	10	1.37 (1.20–1.56)	< 0.001	0.0	0.622	0.96 (0.80–1.15); P = 0.644	1.09 (0.91–1.31); P = 0.344
		High	Overweight	10	0.84 (0.73–0.96)	0.011	48.2	0.043
		Moderate	Underweight	3	1.43 (1.26–1.62)	< 0.001	0.0	0.919
		Moderate	Overweight	3	0.77 (0.68–0.86)	< 0.001	0.0	0.451
Disease free survival	Country	Eastern	Underweight	5	1.47 (0.93–2.32)	0.098	79.2	0.001	0.92 (0.22–3.86); P = 0.914	1.17 (0.67–2.06); P = 0.575
		Eastern	Overweight	5	0.81 (0.71–0.92)	0.002	0.0	0.871
		Western	Underweight	1	1.59 (0.41–6.14)	0.501	-	-
		Western	Overweight	1	0.69 (0.40–1.19)	0.179	-	-
	Age (years)	≥ 65.0	Underweight	3	1.98 (0.65–6.00)	0.227	70.1	0.035	1.57 (0.49–5.08); P = 0.450	0.91 (0.62–1.35); P = 0.652
		≥ 65.0	Overweight	3	0.74 (0.51–1.06)	0.104	0.0	0.932
		< 65.0	Underweight	3	1.26 (0.87–1.84)	0.217	70.4	0.034
		< 65.0	Overweight	3	0.81 (0.70–0.93)	0.003	0.0	0.551
	Male (%)	≥ 70.0	Underweight	1	4.44 (2.34–8.43)	< 0.001	-	-	3.50 (1.72–7.13); P = 0.001	0.90 (0.31–2.60); P = 0.846
		≥ 70.0	Overweight	1	0.72 (0.25–2.06)	0.541	-	-
		< 70.0	Underweight	5	1.27 (0.93–1.73)	0.127	47.3	0.108
		< 70.0	Overweight	5	0.80 (0.70–0.91)	0.001	0.0	0.825
	Study quality	High	Underweight	5	1.44 (0.73–2.84)	0.297	79.1	0.001	0.97 (0.47–2.01); P = 0.941	1.08 (0.83–1.40); P = 0.585
		High	Overweight	5	0.84 (0.68–1.03)	0.095	0.0	0.861
		Moderate	Underweight	1	1.48 (1.14–1.92)	0.003	-	-
		Moderate	Overweight	1	0.78 (0.66–0.92)	0.003	-	-

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Furthermore, we assessed publication bias regarding the association between preoperative BMI and risk of postoperative complications, as shown in S3 and S4 Figs. We noted no significant association between preoperative underweight (P value for Egger: 0.537; P value for Begg: 0.827) and overweight (P value for Egger: 0.323; P value for Begg: 0.381) and the risk of postoperative complications.

OS

Thirteen studies reported an association between preoperative BMI and OS. Preoperative underweight was associated with decreased OS (HR: 1.40; 95%CI: 1.28–1.53; P <0.001), whereas overweight was associated with increased OS (HR: 0.82; 95%CI: 0.73–0.91; P <0.001) (Fig 3). There was no significant heterogeneity in preoperative underweight status (I² = 0.0%; P = 0.820), but there was significant heterogeneity in preoperative overweight status (I² = 42.9%; P = 0.050). The pooled conclusions regarding the association between preoperative underweight or overweight status and OS remained stable (S5 and S6 Figs).

Subgroup analyses of the association between preoperative BMI and OS are shown in Table 3. We noted that a preoperative underweight status was associated with poor OS in most subgroups, whereas no significant association was observed in pooled studies conducted in Western countries. Furthermore, preoperative overweight was associated with enhanced OS in most subgroups. However, this association was not observed in pooled studies conducted in Western countries involving patients with a mean age of ≥65.0 years and where the proportion of male patients was ≥70.0%.

Furthermore, we assessed the publication bias in the association between preoperative BMI and OS (S7 and S8 Figs). There was no significant publication bias in the association between preoperative underweight (P value for Egger: 0.800; P value for Begg: 0.951) and overweight (P value for Egger: 0.759; P value for Begg: 0.855) and OS.

DFS

Six studies reported an association between the preoperative BMI and DFS. Preoperative underweight was not associated with DFS (HR: 1.48; 95%CI: 0.97–2.26; P = 0.069), whereas preoperative overweight was associated with increased DFS (HR: 0.80; 95%CI: 0.70–0.91; P = 0.001) (Fig 4). There was significant heterogeneity in preoperative underweight status (I² = 73.9%; P = 0.002), whereas there was no evidence of heterogeneity in preoperative overweight status (I² = 0.0%; P = 0.907). Sensitivity analysis revealed that preoperative underweight status was associated with poor DFS after excluding the study by Park et al. [44]. In contrast, preoperative overweight status did not affect DFS after excluding the study by Lee et al. [13] (S9 and S10 Figs).

Subgroup analyses on the association between preoperative BMI and DFS are shown in Table 3. Preoperative underweight was correlated with diminished DFS when the proportion of male was ≥70.0%, and the studies assessed were of moderate quality. Furthermore, an association was found between preoperative overweight and extended DFS in scenarios where studies were conducted in Eastern countries, the average age of patients was <65.0 years, the proportion of male was <70.0%, and the quality of the studies was moderate. Notably, the relationship between preoperative underweight and DFS appeared to be influenced by the proportion of male (OR: 3.50; 95%CI: 1.72–7.13; P = 0.001).

Furthermore, we assessed the publication bias regarding the association between preoperative BMI and DFS, as shown in S11 and S12 Figs. There was no significant publication bias in the association between preoperative underweight (P value for Egger: 0.869; P value for Begg: 0.707) and overweight (P value for Egger: 0.864; P value for Begg: 1.000) with DFS.

Discussion

This comprehensive quantitative study included 41,144 patients with GC from 22 retrospective cohort studies and analyzed a diverse range of characteristics. We found that preoperative underweight status was associated with an increased risk of postoperative complications and poor OS, but it did not affect DFS. Regarding specific postoperative complications, preoperative underweight status was linked to a higher risk of septic shock and a lower risk of fever. Additionally, preoperative overweight status was associated with an increased risk of postoperative complications and longer OS and DFS. Regarding specific postoperative complications, preoperative overweight status was associated with a high risk of wound infections, intestinal fistulas, arrhythmias, and pancreatic fistulas. Finally, the association among preoperative BMI, postoperative complications, and survival outcomes may have been influenced by factors such as mean age and proportion of male patients.

Several systematic reviews and meta-analyses have addressed the association between preoperative underweight or overweight status and GC prognosis [51,52]. Zhao et al. identified 12 studies and found that underweight was associated with an increased risk of postoperative complications and poor short- and long-term survival outcomes [51]. Another meta-analysis of 36 studies, that applied a BMI cutoff of 25 kg/m², conducted by the same team, suggested that a high BMI was associated with an increased risk of postoperative complications, particularly infectious complications. However, it did not affect the postoperative mortality or long-term survival of patients with GC [52]. Nonetheless, this study has the following limitations: (1) the association between preoperative underweight status and postoperative outcomes in GC has not been thoroughly explored; (2) the reference group for the prognosis of overweight patients with GC preoperatively had a BMI <25 kg/m², which may have included underweight patients, potentially introducing bias into the association between preoperative overweight status and postoperative outcomes; and (3) new studies meeting the inclusion criteria have been published in recent years, necessitating an update to the meta-analysis outcomes. Thus, the current study aimed to assess the potential association among preoperative BMI, risk of postoperative complications, and survival outcomes.

The results indicated that preoperative underweight status was associated with an increased risk of postoperative complications. Tumor growth may result in significant nutrient depletion and malnutrition-related symptoms, primarily due to systemic inflammatory response induced by the tumor growth, leading to insulin resistance and accelerated catabolism of proteins and adipose tissues. Moreover, studies have demonstrated that preoperative serum albumin levels in underweight patients are lower than those in normal-weight patients, which may contribute to the higher incidence postoperative complications [53,54]. Moreover, preoperative underweight status was associated with poor OS, which may be explained by the fact that underweight patients tend to have later tumor staging and more aggressive tumor invasion than other patients [55]. A preoperative underweight status can result from inadequate nutritional intake, which the aggressive nature of the tumor may exacerbate. However, low body weight may not be an independent prognostic factor in patients with GC [41]. Furthermore, tumor progression can lead to preoperative weight loss and tumor-related malnutrition, increasing the risk of postoperative complications and nutritional deficiencies, which can negatively affect the survival outcomes of patients with GC. Poor nutritional status and increased postoperative complications may delay the initiation of adjuvant chemotherapy and increase the potential toxicity of the chemotherapy drugs [56,57]. These unfavorable conditions are important factors that lead to postoperative recurrence and poor prognosis these patients [58].

Furthermore, this study found that preoperative overweight status was associated with an increased risk of postoperative complications. Being overweight can significantly complicate GC surgery [59]. Excess intra-abdominal fat may interfere with intraoperative lymph node dissection and hinder the retrieval of lymph nodes from resected specimens. Additionally, it may cover major blood vessels, increasing the technical complexity of the surgery and elevating the risk of intraoperative bleeding. Notably, substantial intraoperative bleeding can further obscure the surgical field, making lymph node dissection challenging. These unfavorable conditions inevitably prolong surgical and anesthesia times, leading to an increased risk of postoperative complications. Excess subcutaneous fat tissue at the incision site, high intra-abdominal pressure, and high surface tension may be the reasons for incision-related issues [60]. Additionally, a preoperative overweight status was associated with longer OS and DFS in patients with GC. A preoperative overweight status may be associated with improved OS and DFS, a phenomenon known as the “obesity paradox.” The underlying mechanism could involve overweight individuals having greater nutritional reserves and metabolic support, which aid in resisting physiological stress during treatment, as well as anti-inflammatory factors potentially produced by fat tissue, influencing the tumor microenvironment, and indirectly affecting tumor progression [61]. Nonetheless, overweight and obesity remain recognized as risk factors for GC, suggesting that they play distinct roles in the early stages of disease initiation and development [62].

Regarding specific postoperative complications, we found that a preoperative underweight status was associated with an increased risk of septic shock and a reduced risk of fever. Importantly, the association between low preoperative body weight and postoperative fever was based on a single study [43]; this result may coincide and requires further validation. Additionally, preoperative overweight status was associated with an increased risk of wound infections, intestinal fistulas, arrhythmias, and pancreatic fistulas, likely due to excess intra-abdominal fat. Lastly, age and sex might affect the association between preoperative BMI, postoperative complications, and survival outcomes, This could be explained as follows. (1) Older individuals are more prone to complications and face higher surgical risks compared to younger patients. Additionally, younger patients typically respond better to treatment and have a greater capacity for physical recovery than older ones do; (2) male patients are more prone to develop GC than female patients, and their prognosis tends to be less favorable, primarily due to differences in hormone levels, biochemical mechanisms, and healthcare-seeking behaviors between men and women [63].

This study has certain limitations. First, all the included studies were retrospective in nature, which may have been influenced by recall and uncontrollable confounding biases. Second, the analysis of postoperative complications was based on crude data, and other factors that may affect postoperative complications were not adjusted for. This could have affected the risk of postoperative complications in relation to preoperative BMI. Third, the association between preoperative BMI and survival outcomes in patients was based on adjusted HR and 95%CIs; however, the factors adjusted for in the included studies were not consistent, which may have introduced an uncontrollable confounding bias. Fourth, we adopted the universal BMI classification criteria; however, the impact of overweight and underweight populations on the prognosis of cancer patients differs between Eastern and Western countries. This variation influences the effect of the preoperative BMI on the prognosis of patients with GC. Fifth, tumor staging and postoperative chemotherapy regimens significantly influenced the prognosis of patients with GC; however, detailed stratified data to further investigate the association between preoperative BMI and the prognosis of patients with GC were not available. Sixth, the association of preoperative BMI with the prognosis of patients with GC might be affected by fat mass, muscle mass, and waist circumference; however, this information was not available in the included studies. Seventh, weight-related metabolic or cardiovascular complications in overweight or obese patients with GC may affect surgical procedures, postoperative complications, and survival outcomes. Nonetheless, the included studies did not provide stratified data on weight-related metabolic or cardiovascular complications. Finally, this study was based on a meta-analysis of published literature, and because the analysis was based on pooled data, there was inevitable publication bias and limitations in the exploratory analysis.

Conclusions

The study identified a significant association between preoperative underweight status, higher risk of postoperative complications, and poorer survival outcomes. Additionally, preoperative overweight status was significantly associated with a higher risk of postoperative complications but improved survival outcomes in patients with GC. Therefore, a large-scale prospective study is needed to validate our findings.

Supporting information

S1 Checklist. PRISMA 2020 checklist.

(DOCX)

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S1 Fig. Sensitivity for the association of preoperative underweight with the risk of postoperative complications.

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S2 Fig. Sensitivity for the association of preoperative overweight with the risk of postoperative complications.

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S3 Fig. Funnel plot for the association of preoperative underweight with the risk of postoperative complications.

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S4 Fig. Funnel plot for the association of preoperative overweight with the risk of postoperative complications.

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S5 Fig. Sensitivity for the association of preoperative underweight with overall survival.

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S6 Fig. Sensitivity for the association of preoperative overweight with overall survival.

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S7 Fig. Funnel plot for the association of preoperative underweight with overall survival.

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S8 Fig. Funnel plot for the association of preoperative overweight with overall survival.

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S9 Fig. Sensitivity for the association of preoperative underweight with disease free survival.

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S10 Fig. Sensitivity for the association of preoperative overweight with disease free survival.

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S11 Fig. Funnel plot for the association of preoperative underweight with disease free survival.

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S12 Fig. Funnel plot for the association of preoperative overweight with disease free survival.

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S1 Table. Quality scores of prospective cohort studies using Newcastle-Ottawa Scale.

(DOC)

pone.0317985.s014.doc^{(69.5KB, doc)}

S1 Data

(XLSX)

pone.0317985.s015.xlsx^{(24.5KB, xlsx)}

S2 Data

(XLSX)

pone.0317985.s016.xlsx^{(16.9KB, xlsx)}

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

The author(s) received no specific funding for this work.

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PLoS One. 2025 Jan 28;20(1):e0317985. doi: 10.1371/journal.pone.0317985.r001

Author response to previous submission

14 Nov 2024

Attachment

Submitted filename: Response to reviewer.docx

pone.0317985.s017.docx^{(16.8KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0317985.r002

Decision Letter 0

Valeria Guglielmi

20 Dec 2024

PONE-D-24-52307Association of preoperative body mass index with postoperative complications and survival for patients with gastric cancer: A systematic review and meta-analysisPLOS ONE

Dear Dr. Li,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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We look forward to receiving your revised manuscript.

Kind regards,

Valeria Guglielmi

Academic Editor

PLOS ONE

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A numbered table of all studies identified in the literature search, including those that were excluded from the analyses.

For every excluded study, the table should list the reason(s) for exclusion.

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Additional Editor Comments:

Dear Authors,

after careful review, we are pleased to inform you that your manuscript has been positively evaluated. However, there are a few minor revisions that we kindly request before proceeding to the final stages of the publication process.

Please address the points mentioned by the first Reviewer and submit the revised manuscript within one week.

We look forward to receiving your updated manuscript and thank you for your valuable contribution.

Best regards,

Valeria Guglielmi

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

Reviewer #2: I Don't Know

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Zhenzhen Li and colleagues submitted their research article in september (PONE-D-24-35040) and in the first peer review process I suggested minor revisions. The following is the point-by-point response provided by the authors to the previous submission.

Response to reviewer 1

General comments: In this article, Zhenzhen and colleagues conducted a systematic review and meta-analysis to evaluate postoperative outcomes (complications, disease-free survival, and overall survival) in individuals undergoing surgery for gastric cancer (GC) based on preoperative BMI categories (controls: BMI 18.5–25; underweight: BMI <18.5; overweight: BMI >25 kg/m²). The results show that both underweight and overweight individuals have a higher risk of postoperative complications compared to controls. Overweight individuals exhibited improved overall and disease-free survival, while underweight individuals had worse outcomes in both.

The study’s methodology is robust, and the results are straightforward. Moreover, the authors acknowledge some unavoidable limitations. However, several points merit further consideration:

Response: As behalf of all co-authors, I would like to appreciate this referee due to thoughtful comments proposed by the peer review. We have made revisions to the manuscript in accordance with the reviewer's comments.

Question 1: A revision of the manuscript’s English language by a native speaker would improve clarity, as some phrases may be misleading (e.g., "increasing evidence suggests that nutritional status is related to the postoperative incidence of different types of cancer," or "preoperative underweight may be due to excessive nutritional intake caused by tumor aggressiveness," and "male patients are more likely to develop GC than female patients, leading to poorer prognosis").

Response: Thanks for this suggestion, and these sentences have already changed in the revised manuscript, as follows: “Accumulating evidence suggests that nutritional status is associated with the prognosis of various types of cancer”; “A preoperative underweight status can result from inadequate nutritional intake, which the aggressive nature of the tumor may exacerbate”; and “male patients are more prone to develop GC than female patients, and their prognosis tends to be less favorable, primarily due to differences in hormone levels, biochemical mechanisms, and healthcare-seeking behaviors between men and women”. Moreover, The entire text has been revised by native English-speaking experts at Editage company.

Question 2: The authors observed differences in subgroup analyses between studies conducted in Eastern vs. Western countries. The European Association for the Study of Obesity (EASO) advocates for ethnicity-specific BMI cut-offs, as evidence indicates that Asian populations have distinct relationships between BMI, body fat percentage, and health risks compared to Caucasian populations. Could the observed differences be attributed to the use of a universal BMI cut-off, which overlooks these physiological differences? Commenting on this would enrich the discussion.

Response: Thanks for this suggestion. In subgroup analyses, we did not find a significant difference between Eastern and Western countries regarding the association between preoperative BMI and the prognosis of GC patients (see Table 3). Consequently, we have stated this observation in the limitations section. Please refer to Para 6, section Discussion, as follows: “Fourth, we adopted the universal BMI classification criteria; however, the impact of overweight and underweight populations on the prognosis of cancer patients differs between Eastern and Western countries. This variation influences the effect of the preoperative BMI on the prognosis of patients with GC”

Question 3: Two significant factors not considered in the study, which may have impacted the results, are tumor staging and the potential administration of chemotherapy. This is a critical limitation that should be emphasized.

Response: Thanks for this suggestion. We are aware that tumor staging and postoperative chemotherapy regimens can significantly affect patient outcomes. Nevertheless, our inability to access specific stratified data has hindered our efforts to further explore the relationship between preoperative BMI and the prognosis of GC patients, limiting our capacity for additional exploratory analyses. We have included this limitation in the respective section of our discussion. Please refer to Para 6, section Discussion, as follows: “Fifth, tumor staging and postoperative chemotherapy regimens significantly influenced the prognosis of patients with GC; however, detailed stratified data to further investigate the association between preoperative BMI and the prognosis of patients with GC were not available.”

Question 4: An intriguing finding is the association between preoperative overweight status and improved overall and disease-free survival. While the authors suggest that this may be due to early-stage cancer, it is essential to note that obesity is a known risk factor for GC. This observation should be highlighted, otherwise the results of this study could be misinterpreted.

Response: Thanks for this suggestion, and these results have already re-explanation in the revised manuscript. Please refer to Para 4, section Discussion, as follows: “A preoperative overweight status may be associated with improved OS and DFS, a phenomenon known as the “obesity paradox.” The underlying mechanism could involve overweight individuals having greater nutritional reserves and metabolic support, which aid in resisting physiological stress during treatment, as well as anti-inflammatory factors potentially produced by fat tissue, influencing the tumor microenvironment, and indirectly affecting tumor progression [61]. Nonetheless, overweight and obesity remain recognized as risk factors for GC, suggesting that they play distinct roles in the early stages of disease initiation and development [62]”

In this revised submission, the authors have effectively addressed all the points I previously highlighted. I commend them for their diligent efforts and for the transparency with which they have acknowledged the limitations of their research.

I would not say that "BMI serves as an indicator of a person's nutritional status and body fat levels", as it is a simple measure that serves primarily as a tool for population-level studies rather than for assessing the nutritional status or body composition of an individual.

I finally suggest checking for typos (in Introduction: "contributingto... ofnew... to be significantly correlate...").

Reviewer #2: This meta-analysis aims to elucidate potential associations between preoperative BMI and the risk of postoperative complications, as well as survival outcomes in GC patients.

The authors have made revisions to the manuscript in accordance with my comments.

**********

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Reviewer #1: No

Reviewer #2: No

**********

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PLoS One. 2025 Jan 28;20(1):e0317985. doi: 10.1371/journal.pone.0317985.r003

Author response to Decision Letter 0

7 Jan 2025

Journal requirements:

Question 1: Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf.

Response: We sincerely appreciate your pointing out that our manuscript needs to ensure compliance with the style requirements of PLOS ONE, especially regarding file naming. We have carefully read the style templates provided in the links and conducted a comprehensive and meticulous review and revision of our manuscript to ensure full compliance with the PLOS ONE publication standards.

We would like to express our gratitude again for your attention and guidance on the manuscript format. We have made every effort to ensure that the manuscript complies with the style requirements of PLOS ONE in all aspects. If the reviewer finds any format issues or has other questions during further review, we will be happy to make modifications and improvements at any time.

Question 2: As required by our policy on Data Availability, please ensure your manuscript or supplementary information includes the following:

A numbered table of all studies identified in the literature search, including those that were excluded from the analyses.

For every excluded study, the table should list the reason(s) for exclusion.

If any of the included studies are unpublished, include a link (URL) to the primary source or detailed information about how the content can be accessed.

A table of all data extracted from the primary research sources for the systematic review and/or meta-analysis. The table must include the following information for each study:

Name of data extractors and date of data extraction

Confirmation that the study was eligible to be included in the review.

All data extracted from each study for the reported systematic review and/or meta-analysis that would be needed to replicate your analyses.

An explanation of how missing data were handled.

Response: Thank you for bringing our attention to the requirements regarding data availability. We have thoroughly addressed these points and have included the necessary information in both the main text and supplementary information as follows: (1) We have created a numbered table in the manuscript titled “The baseline characteristics of included studies and involved patients” (Table 1). This table lists all the studies identified during the literature search. For each study, it includes columns for the study ID, author names, year of publication, and a brief description of the study; (2) For the excluded studies, we have clearly indicated the reasons for exclusion in an additional column. The reasons are categorized and detailed: reported GC risk (n = 16), other BMI categories (n = 13), or the same population (n = 7). This provides transparency and allows other researchers to understand the selection process; (3) Another table, “Data Extraction Table”, has been prepared in the supplementary information. This table contains all the data extracted from the primary research sources for our systematic review and/or meta - analysis; (4) In the supplementary information, we have included a table titled “quality of the included studies” (S1 Table). This table shows the completed assessments for each study and outcome, as applicable to our analysis.

We understand the importance of providing these underlying data for the integrity and reproducibility of our research. We have made every effort to ensure that all the required information is presented in a clear and organized manner. If you require any further clarification or have additional questions regarding the data availability, please do not hesitate to contact us.

Question 3: Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Response: We are grateful for your feedback regarding the reference list in our manuscript. We have meticulously examined each reference in the list to confirm that all necessary information is included and accurately presented. This includes verifying the authors' names, article titles, journal names, publication years, volume numbers, page numbers, and DOIs (if applicable). We have cross-checked the references with the in - text citations to ensure that they are consistent and that every citation in the text corresponds to a correct entry in the reference list.

Additional Editor Comments:

General comments: Dear Authors,

Please address the points mentioned by the first Reviewer and submit the revised manuscript within one week.

Response: We are extremely grateful for the positive evaluation of our manuscript and would like to express our sincere appreciation for the time and effort you have dedicated to reviewing our work. We have carefully addressed all the points raised by the first reviewer and have made the necessary revisions to improve the quality of our manuscript. The following is a detailed response to each of the reviewer's comments:

Reviewer #1:

General comments: Zhenzhen Li and colleagues submitted their research article in september (PONE-D-24-35040) and in the first peer review process I suggested minor revisions. The following is the point-by-point response provided by the authors to the previous submission.

“Response to reviewer 1

General comments: In this article, Zhenzhen and colleagues conducted a systematic review and meta-analysis to evaluate postoperative outcomes (complications, disease-free survival, and overall survival) in individuals undergoing surgery for gastric cancer (GC) based on preoperative BMI categories (controls: BMI 18.5-25; underweight: BMI <18.5; overweight: BMI >25 kg/m2). The results show that both underweight and overweight individuals have a higher risk of postoperative complications compared to controls. Overweight individuals exhibited improved overall and disease-free survival, while underweight individuals had worse outcomes in both.

The study’s methodology is robust, and the results are straightforward. Moreover, the authors acknowledge some unavoidable limitations. However, several points merit further consideration:

Response: We would like to express our sincere gratitude for your kind words regarding our revised submission. Your feedback has been invaluable in improving the quality of our manuscript. Regarding your comment about the description of BMI, we fully understand your perspective and appreciate the opportunity to clarify and correct this in our manuscript. We acknowledge that our previous description of BMI was inaccurate and could have been misleading. We understand that BMI is indeed a simple measure that has its limitations, especially when it comes to individual - level assessment of nutritional status and body composition. In the revised manuscript, we have adjusted the text to more accurately reflect the nature of BMI. We have rephrased the relevant sentence to state that "BMI is a commonly used measure in population-level studies, which provides a general indication of body mass relative to height." This new wording emphasizes the appropriate context in which BMI is used and acknowledges its shortcomings more explicitly.

Question 1: I finally suggest checking for typos (in Introduction: "contributingto... ofnew... to be significantly correlate...").

Response: We sincerely appreciate your meticulous review and the valuable feedback regarding the typos in our manuscript. We take your suggestions very seriously and have made the necessary corrections to ensure the accuracy and professionalism of our work.

Upon carefully reviewing the Introduction section, we have identified and rectified the following typos: (1) In the phrase “contributingto...”, a space was missing. We have corrected it to “contributing to”; (2) Regarding “ofnew...”, an extra space was inadvertently left out. It has been amended to “of new”; (3) As for “to be significantly correlate...”, this was a grammar error. We have revised it to “to be significantly correlated...”, as “correlated” is the appropriate form to convey the intended meaning in this context. We have also conducted a comprehensive proofreading of the entire manuscript to identify and correct any other potential typos or grammar errors. We understand the importance of presenting a polished and error - free manuscript, and we are committed to upholding the highest standards of academic writing.

Reviewer #2:

General comments: This meta-analysis aims to elucidate potential associations between preoperative BMI and the risk of postoperative complications, as well as survival outcomes in GC patients.

The authors have made revisions to the manuscript in accordance with my comments.

Response: We are extremely grateful for your recognition of the revisions we made to the manuscript in accordance with your comments. Your guidance has been instrumental in shaping our work and bringing it to a higher standard.

We are delighted that our efforts to address your concerns have been

Attachment

Submitted filename: Response to reviewer.docx

pone.0317985.s018.docx^{(21.7KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0317985.r004

Decision Letter 1

Valeria Guglielmi

9 Jan 2025

Association of preoperative body mass index with postoperative complications and survival for patients with gastric cancer: A systematic review and meta-analysis

PONE-D-24-52307R1

Dear Dr. Zhenzhen Li,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Valeria Guglielmi

Academic Editor

PLOS ONE

PLoS One. doi: 10.1371/journal.pone.0317985.r005

Acceptance letter

Valeria Guglielmi

17 Jan 2025

PONE-D-24-52307R1

PLOS ONE

Dear Dr. Li,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

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Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

If we can help with anything else, please email us at customercare@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Prof. Valeria Guglielmi

Academic Editor

PLOS ONE

Attachment

Submitted filename: pone.0317985.docx

pone.0317985.s019.docx^{(89.6KB, docx)}

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Checklist. PRISMA 2020 checklist.

(DOCX)

pone.0317985.s001.docx^{(29.6KB, docx)}

S1 Fig. Sensitivity for the association of preoperative underweight with the risk of postoperative complications.

(TIF)

pone.0317985.s002.tif^{(2.6MB, tif)}

S2 Fig. Sensitivity for the association of preoperative overweight with the risk of postoperative complications.

(TIF)

pone.0317985.s003.tif^{(2.6MB, tif)}

S3 Fig. Funnel plot for the association of preoperative underweight with the risk of postoperative complications.

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S4 Fig. Funnel plot for the association of preoperative overweight with the risk of postoperative complications.

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S5 Fig. Sensitivity for the association of preoperative underweight with overall survival.

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S6 Fig. Sensitivity for the association of preoperative overweight with overall survival.

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S7 Fig. Funnel plot for the association of preoperative underweight with overall survival.

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S8 Fig. Funnel plot for the association of preoperative overweight with overall survival.

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S9 Fig. Sensitivity for the association of preoperative underweight with disease free survival.

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S10 Fig. Sensitivity for the association of preoperative overweight with disease free survival.

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S11 Fig. Funnel plot for the association of preoperative underweight with disease free survival.

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S12 Fig. Funnel plot for the association of preoperative overweight with disease free survival.

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S1 Table. Quality scores of prospective cohort studies using Newcastle-Ottawa Scale.

(DOC)

pone.0317985.s014.doc^{(69.5KB, doc)}

S1 Data

(XLSX)

pone.0317985.s015.xlsx^{(24.5KB, xlsx)}

S2 Data

(XLSX)

pone.0317985.s016.xlsx^{(16.9KB, xlsx)}

Attachment

Submitted filename: Response to reviewer.docx

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Data Availability Statement

All relevant data are within the paper and its Supporting Information files.

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PERMALINK

Association of preoperative body mass index with postoperative complications and survival for patients with gastric cancer: A systematic review and meta-analysis

Zhenzhen Li

Lili Cui

Jing Sun

Wanlu Liu

Roles

Abstract

Objective

Method

Results

Conclusion

Trial registration

Background

Methods

Search strategy and selection criteria

Data collection and quality assessment

Statistical analysis

Results

Search results

Fig 1. Literature search and study selection details.

Study characteristics

Table 1. The baseline characteristics of included studies and involved patients.

Postoperative complications

Fig 2. Association of preoperative BMI with the risk of postoperative complications.

Table 2. The summary results for specific postoperative complications.

Table 3. Subgroup analyses for postoperative complications, overall survival, and disease-free survival.

OS

Fig 3. Association of preoperative BMI with OS.

DFS

Fig 4. Association of preoperative BMI with DFS.

Discussion

Conclusions

Supporting information

Data Availability

Funding Statement

References

Author response to previous submission

Decision Letter 0

Valeria Guglielmi

Roles

Author response to Decision Letter 0

Decision Letter 1

Valeria Guglielmi

Roles

Acceptance letter

Valeria Guglielmi

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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