Trunk Fat Volume Can Be a Predictor of Short-Term Surgical Outcomes After Gastrectomy: A Retrospective Cohort Study

Obesity can affect postoperative outcomes of gastrectomy. Visceral fat area is superior to body mass index in predicting postoperative complications. However, visceral fat area measurement is time-consuming and is not optimum for clinical use. Meanwhile, trunk fat volume (TFV) can be easily measured via bioelectrical impedance analysis. Hence, this current study aimed to determine the association of trunk fat volume in predicting the occurrence of complications after gastrectomy. We retrospectively reviewed patients who underwent curative gastrectomy for gastric cancer between November 2016 and November 2019. The trunk fat volume-to-the ideal amount (%TFV) ratio was obtained using InBody 770 before surgery. The patients were classied into the obese and nonobese groups according to %TFV (TFV-H group, ≥ 150 %; TFV-L group, < 150 %) and body mass index (BMI-H group, ≥ 25 kg/m 2 ; BMI-L group, < 25 kg/m 2 ). We compared the short-term postoperative outcomes (e.g., operative time, blood loss volume, number of resected lymph nodes, and duration of hospital stay) between the obese and nonobese patients. Risk factors for complications were assessed using logistic regression analysis.

Gastric cancer is the fourth most common cancer worldwide [1], and gastrectomy has been considered essential for its curative treatment. Postoperative complications adversely affect the long-term survival of patients with gastric cancer. Therefore, the risk factors of postoperative complications should be identi ed and postoperative complication rates reduced [2].
Excessive intra-abdominal fat tissue poses di culties during surgery. Obesity is associated with shortterm surgical outcomes, including complications after gastrectomy [3,4], and is evaluated using several methods. Body mass index (BMI) is the most widely used tool for obesity assessment because it is easy to use, and usually, individuals with BMI > 25 kg/m 2 are considered obese in Japan [5]. Visceral fat area (VFA), which refers to intra-abdominal fat, is another index used to evaluate obesity. It is measured at the level of the umbilicus on single-slice computed tomography (CT) scan. Recently, several studies have reported that BMI cannot accurately re ect perioperative outcomes, and VFA is more accurate in predicting short-term postoperative outcomes [3,4,[6][7][8]. However, measuring VFA is time-consuming, and evaluating each patient for VFA is burdensome for mostly busy clinicians.
Trunk fat volume (TFV), which re ects the fat mass of the body trunk, is another parameter that can be used to evaluate obesity. TFV can be easily measured using bioelectrical impedance analysis (BIA). BIA is a simple method to measure body compositions, including fat mass; this method is increasingly used worldwide because it is non-invasive, cost-effective, and simple to use [9]. Recent studies have shown that body composition measurements can help in evaluating nutrition status after surgery and in predicting surgical outcomes [10]. However, to the best of our knowledge, the relationship between TFV and postoperative outcomes has not been reported in previous studies. Hence, this study aimed to identify the e cacy of TFV in predicting outcomes after gastrectomy.

Patients
This was a single institutional retrospective cohort study conducted at the University of Tokyo Hospital. In total, 278 patients underwent gastrectomy for gastric cancer from November 2016 to November 2019. In our institution, preoperative examinations consist of upper gastrointestinal endoscopy with biopsies, CT scans, and laboratory tests. Besides, we routinely measure body composition using BIA preoperatively with written consent. Clinical cancer stage was determined according to the Japanese Classi cation of Gastric Carcinoma (15th edition) [11]. Treatment strategies were mainly based on Japanese Gastric Cancer treatment guidelines (4th and 5th edition) [12,13]. Patients who could not undergo curative resection and those who received neoadjuvant chemotherapy were excluded. Study procedures were carried out in accordance with the Declaration of Helsinki. The ethics committee of the faculty of medicine at the University of Tokyo approved this study and waived the requirement for informed consent to this study as anonymized data were used (approval number: 3962).
De nition of obesity assessed using BMI and TFV The patients were divided into obese and nonobese groups according to both BMI and TFV. Patients with BMI ≥ 25 kg/m 2 were classi ed under the BMI high (BMI-H) group and patients with BMI < 25 kg/m 2 under the BMI low (BMI-L) group. We obtained the TFV and body fat mass (BFM) using BIA with InBody 770® (InBody Co., Ltd., Seoul, Korea) one or two days before surgery. This tool uses direct segmental multifrequency BIA. It introduces alternating currents into the body and measures impedance, which comprises resistance and reactance. Moreover, it uses eight electrodes and individually measures the impedance of each body part (e.g., the trunk, right and left arms, and right and left legs) at six different frequencies to evaluate body compositions [14,15]. The accuracy of BIA has been evaluated in several studies, and it is correlated with standard body composition parameters obtained using different modalities, such as dual-energy X-ray absorptiometry, CT scan, and air displacement plethysmography [9,14,16,17]. We classi ed patients according to TFV in the following manner. First, we calculated the TFVto-BFM ratios. The median in each sex was de ned as an ideal distribution of trunk body fat (% in men and % in women, respectively). Second, we calculated the ideal BFM multiplying the ideal body weight (height×height×22 for men and height×height×21 for women [18]) by the ideal percentage of body fat (15% for men and 23% for women [19]). Third, we de ned the product by multiplying these two components as the ideal TFV. Finally, we calculated the TFV-to-the ideal TFV (%TFV) ratio of each patient.
The median TFV-to-BFM ratio of men and women were 0.50 and 0.47, respectively. Following these calculations, we derived the following equations according to sex.

Surgical procedures
We performed distal gastrectomy, total gastrectomy, proximal gastrectomy, or pylorus-preserving gastrectomy with radical lymphadenectomy as per the treatment guidelines of the Japanese Gastric Cancer Association [12,13]. Laparoscopic gastrectomy was used in the preoperative diagnosis of T1-2N0 tumors. Patients who underwent distal or total gastrectomy had Roux-en-Y reconstruction. Esophagogastric anastomosis, jejunal interposition anastomosis, or side overlap esophagogastrostomy that is based on the study of Yamashita [20] was conducted for the reconstruction of proximal gastrectomy. A gastro-gastro anastomosis was established for the reconstruction of pylorus-preserving gastrectomy.
Evaluation of short-term postoperative outcomes We have compared the short-term postoperative outcomes, including operative time, volume of blood loss, number of resected lymph nodes, and duration of hospital stay between the obese and nonobese patients. Moreover, the risk factors for complications were assessed. The Clavien-Dindo classi cation system [21] was used to assess postoperative morbidity. Complications greater than grade 2 were considered as clinically signi cant and those greater than grade 3a as severe.

Statistical analysis
The Pearson's chi-square test or Fisher's exact test was used in the univariate analysis. Meanwhile, logistic regression was utilized in the multivariate analysis, which was performed using factors with p values < 0.1 in the univariate analysis. The student's t-test or Wilcoxon signed-rank test was utilized for continuous value. P values < 0.05 were considered statistically signi cant. JMP® 15 (SAS Institute Inc., Cavy, NC, the USA) was utilized for all statistical analyses.

Characteristics of the patients
Of 278 patients, 14 who underwent R1 or R2 resection, and 32 who received neoadjuvant chemotherapy were excluded. Finally, 232 patients were included in our study. The characteristics of the patients are shown in Table 1. In both criteria, obese patients underwent signi cantly more open gastrectomy and had severer comorbidities. Besides, the TFV-H group had a higher proportion of male patients, early-stage disease, and D1 + dissection, which were not evident in the BMI group. Other properties were comparable between the two groups. A signi cant correlation was observed between %TFV and BMI (r = 0.784, p < 0.001) (Fig. 1). Correlation between obesity and short-term outcomes .75], p < 0.001) than the TFV-L group. Although the BMI-H group had a signi cantly longer operative time than the BMI-L group (321.9 ± 78.5min vs 288.1 ± 62.2 min, p = 0.006), the number of resected lymph nodes did not differ signi cantly between the two groups. The volume of blood loss and duration of hospital stay were comparable between the two groups in both criteria.   The details of postoperative complications are presented in Table 4. Severe complications were also more common in the TFV-H group than in the TFV-L group although the difference was not signi cant (10.8 % vs 4.5 %, p = 0.070). In terms of complications, anastomotic leakage, pancreatic stula, and pneumonia were more common in the TFV-H group than in the TFV-L group. However, only the occurrence of pancreatic stula was statistically signi cant (5.8 % vs 0.9 %, p = 0.039). Meanwhile, the rate of each complication in the BMI-H group was comparable with that in the BMI-L group.

Discussion
This study revealed that obesity evaluated using %TFV and total or proximal gastrectomy was independently associated with postoperative complications. The %TFV may be a better parameter than BMI for the evaluation of the di culty of gastrectomy and prediction of postoperative complications such as pancreatic stula. These ndings indicate that TFV may help to determine the necessity of drain management or frequent following up of blood tests and X-ray examination in the postoperative period and enable the early detection of each complication.
Excessive visceral fat poses di culties during surgery, and obesity is associated with unfavorable surgical outcomes, including longer operative time, higher postoperative complication rates, lower number of resected lymph nodes, and prolonged hospital stay [4,8,[22][23][24]. BMI is the most commonly used parameter for the evaluation of obesity. Several studies have shown that a higher BMI is associated with worse surgical outcomes [24,25]. However, other studies revealed that BMI may not be a predictive factor of postoperative outcomes [3,[6][7][8]. This nding might be attributed to the fact that BMI is easy to assess. That is, it is calculated using height and weight. However, it does not directly re ect intraabdominal fat volume [8,26]. Whether obesity evaluated using BMI can be used to accurately predict operative risks remains controversial. Hence, VFA is used for the evaluation of obesity. It is measured on a cross-sectional CT scan and may directly re ect intra-abdominal fat. Several studies have shown that VFA is more accurate than BMI in predicting postoperative complications [3,8,27,28]. Notably, VFA measurement is time-consuming and might not be suitable for clinical use. Thus, a simpler parameter is preferred in daily use. Besides, VFA is not always ideal as it is measured only on a one-slice CT scan.
In this study, we used %TFV obtained using BIA, which is increasingly used in recent studies [14,15]. As expected, %TFV was found to be strongly correlated with BMI. However, theoretically, %TFV can only evaluate trunk fat mass, and BMI can assess whole body elements, including muscles and extremities. Therefore, the use of %TFV may be more suitable in predicting any di culties encountered during surgery. Our results were consistent with this theory. Compared with VFA, %TFV cannot be utilized to distinguish subcutaneous fat from visceral fat, which is considered a disadvantage. However, its simplicity counteracts this detriment in daily clinical practice given that it can predict postoperative outcomes.
Preoperative exercise intervention has been reported to be bene cial, especially in obese patients [29].
When we conduct preoperative interventions, there is a concern about tumor progression, particularly in patients with advanced cancer. However, preoperative wait time up to 90 days has been reported not to affect survival even in cStage / gastric cancer patients [30]. Hence, obese patients might have the bene ts of fewer complications by preoperative exercise. In this study, %TFV ≥ 150 was an independent risk factor for postoperative complications, and this population might be a good candidate for preoperative intervention, although further study is required for a rm conclusion.
In this study, pancreatic stula and anastomotic leakage were more common in the TFV-H group than in the TFV-L group and this result was in accordance with that of a previous study [31]. Previous studies have reported the possible causes of poor outcomes among obese patients. High visceral fat may be associated with the misrecognition of anatomy and technical di culty in achieving a good view of the surgical eld. Occasionally, this causes excessive counter traction and over-compression in the pancreas during lymph node dissection [8,[25][26][27][28]31]. These factors result in tissue trauma, a higher volume of blood loss, prolonged operative time, and pancreatic stula. Excessive tension on the anastomosis site due to thick and heavy mesenteric fat may be a risk factor for anastomotic leakage [22,27,32]. In this study, pneumonia was more frequently observed in the TFV-H group, which was consistent with the result of a previous study [33]. Obesity is associated with decreased total lung capacity attributed to high intraabdominal pressure or excessive subcutaneous fat around the thorax [34]. Di culty in clearing airway secretions and delayed ambulation may be contributory factors for pulmonary complications, such as atelectasis and pneumonia. However, the number of patients who had each complication was extremely low in this study, and only the occurrence of pancreatic stula showed a signi cant difference. Thus, further investigations should be conducted to accurately identify the occurrence of complications after surgery.
The current study had several limitations. First, this was a retrospective, single-center study. Hence, it was susceptible to selection and cognitive bias. Hence, a larger multicenter study should be performed to obtain a rm conclusion. Second, different surgeons performed gastrectomy during the study period.
Hence, the differences in the ability of the surgeons might have affected the results. Although skilled surgeons supervised trainee surgeons who performed gastrectomy, the effect might still be signi cant. Third, the ideal TFV was derived from the median TFV-to-BFM ratio, which was obtained from data in this study because no previous studies have discussed the ideal distribution of body fat. However, this value should be determined based on the general population. Finally, TFV obtained using BIA represents both subcutaneous and visceral fat. Fat mass is more likely to accumulate in the visceral area in men than in women [6]. The surgical procedure is mainly affected by visceral fat [26], and whether the use of a similar %TFV threshold in both men and women is acceptable has not been con rmed. Thus, further studies should be conducted to identify the ideal threshold for each sex.

Conclusions
%TFV is superior to BMI as a predictive factor for short-term outcomes after gastrectomy. Obesity evaluated using %TFV is an independent risk factor of postoperative complications. Moreover, %TFV may be a useful parameter in the evaluation of obesity and a predictor of postoperative short-term outcomes.

Declarations
Ethics approval and consent to participate: This study was conducted in accordance with the Declaration of Helsinki. The ethics committee of the faculty of medicine at the University of Tokyo approved this study and waived the requirement for informed consent to this study as anonymized data were used. All methods were carried out appropriately based on Japanese guidelines of gastric cancer.