Open Access, Peer-reviewed
pISSN 2093-582X
eISSN 2093-5641
    J Gastric Cancer. 2021 Dec;21(4):352-367. English.
    Published online Nov 26, 2021.
    https://doi.org/10.5230/jgc.2021.21.e34
    Copyright © 2021. Korean Gastric Cancer Association
    Original Article

    Risk Factors for the Severity of Complications in Minimally Invasive Total Gastrectomy for Gastric Cancer: a Retrospective Cohort Study

    Chul Kyu Roh,1,2,* Soomin Lee,1,2 Sang-Yong Son,1,2 Hoon Hur,1,2 and Sang-Uk Han1,2
      • 1Department of Surgery, Ajou University School of Medicine, Suwon, Korea.
      • 2Gastric Cancer Center, Ajou University Medical Center, Suwon, Korea.
    • Correspondence to Sang-Uk Han. Department of Surgery, Ajou University School of Medicine, 164 World cup-ro, Yeongtong-gu, Suwon 16499, Korea. Email: hansu@ajou.ac.kr
      *Present address: Department of Surgery, National Police Hospital, Seoul, Korea.
    Received July 30, 2021; Revised October 21, 2021; Accepted November 03, 2021.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    Purpose

    Minimally invasive gastrectomy is a promising surgical method with well-known benefits, including reduced postoperative complications. However, for total gastrectomy of gastric cancers, this approach does not significantly reduce the risk of complications. Therefore, we aimed to evaluate the incidence and risk factors for the severity of complications associated with minimally invasive total gastrectomy for gastric cancer.

    Materials and Methods

    The study included 392 consecutive patients with gastric cancer who underwent either laparoscopic or robotic total gastrectomy between 2011 and 2019. Clinicopathological and operative characteristics were assessed to determine the features related to postoperative complications after minimally invasive total gastrectomy. Binomial and multinomial logistic regression models were used to identify the risk factors for overall complications and mild and severe complications, respectively.

    Results

    Of 103 (26.3%) patients experiencing complications, 66 (16.8%) and 37 (9.4%) developed mild and severe complications, respectively. On multivariate multinomial regression analysis, independent predictors of severe complications included obesity (OR, 2.56; 95% CI, 1.02−6.43; P=0.046), advanced stage (OR, 2.90; 95% CI, 1.13−7.43; P=0.026), and more intraoperative bleeding (OR, 1.04; 95% CI, 1.02−1.06; P=0.001). Operation time was the only independent risk factor for mild complications (OR, 1.06; 95% CI, 1.001−1.13; P=0.047).

    Conclusions

    The risk factors for mild and severe complications were associated with surgery, indicating surgical difficulty. Surgeons should be aware of these potential risks that are related to the severity of complications so as to reduce surgery-related complications after minimally invasive total gastrectomy for gastric cancer.

    Keywords
    Gastric cancer; Gastrectomy; Laparoscopy; Postoperative complications; Risk factors

    INTRODUCTION

    Surgical treatment is the only curative treatment for resectable gastric cancer. Remarkable improvements in surgical techniques, devices, and perioperative management have reduced the complication rate of minimally invasive gastrectomy for gastric cancer over the past decades [1, 2]. Moreover, minimally invasive approaches are now increasingly considered as surgical treatment options for patients with gastric cancer because of their improved short-term postoperative results, without adverse effects on oncological outcomes, when compared with those of open surgery [3, 4, 5, 6, 7].

    However, despite significant advances in surgical techniques, minimally invasive total gastrectomy is still associated with considerable postoperative morbidity and mortality [8, 9]. Minimally invasive total gastrectomy for cancer is more complex and time-consuming than other gastrectomy procedures such as omentectomy, lymphadenectomy, and reconstruction [10]. Among them, reconstruction of minimally invasive total gastrectomy requires a more sophisticated technique than open total gastrectomy, and it may increase the risk of anastomosis-related complications [11, 12, 13, 14]. Therefore, previous studies that investigated potential risk factors during total gastrectomy raise particular concerns regarding anastomosis-related complications [15, 16, 17, 18, 19].

    Although several studies have reported risk factors for complications after total gastrectomy, only a few have assessed the risk factors for complications definitively for minimally invasive total gastrectomy, including both laparoscopic and robotic surgery, for gastric cancer [20, 21, 22, 23]. Moreover, the risk factors for the severity (mild or severe) of complications, such as the multinomial logistic regression model, have not been evaluated concurrently using a unified model. Complications following minimally invasive total gastrectomy for gastric cancer remain an important clinical issue on account of their negative effects on functional and oncological outcomes. Thus, in this study, we aimed to evaluate the clinical, pathological, and operative factors associated with an increased risk for the severity of complications after minimally invasive total gastrectomy for gastric cancer by using a unified model.

    MATERIALS AND METHODS

    Study design and patients

    We analyzed prospectively collected data of patients who underwent minimally invasive (robotic or laparoscopic) total gastrectomy for gastric cancer at the Department of Surgery, Ajou University School of Medicine, from January 2011 to December 2019. All cases of total gastrectomy were performed by three surgeons. While one surgeon had performed at least 50 minimally invasive total gastrectomies before the study period, the other two surgeons had no experience performing minimally invasive total gastrectomy. This study thus analyzed the experience of one surgeon after the learning curve and the initial experience of two surgeons for minimally invasive total gastrectomy. We included patients who underwent curative total gastrectomy and excluded those patients who underwent complete gastrectomy, palliative gastrectomy, or emergency gastrectomy. After a detailed explanation, the patients were given the choice to undergo robotic or laparoscopic gastrectomy. All patients provided written informed consent prior to surgery. The Institutional Review Board of Ajou University Hospital, Suwon, Korea, approved this study (approval number: AJIRB-MED-MDB-21-313).

    Surgical procedures of minimally invasive total gastrectomy

    The typical surgical procedures for minimally invasive total gastrectomy, laparoscopic and robotic, have been described previously in detail [24]. We performed lymphadenectomy according to the Korean and Japanese gastric cancer treatment guidelines [25, 26]. After total gastrectomy, esophagojejunostomy using circular staplers was performed extracorporeally or intracorporeally, whereas esophagojejunostomy using linear staplers was performed only intracorporeally. For extracorporeal esophagojejunostomy using a circular stapler, an upper midline mini-laparotomy of approximately 7 cm was performed after esophageal mobilization. For intracorporeal esophagojejunostomy using a circular stapler, a transverse mini-laparotomy was performed at the left lower port site. The circular stapler body inserted into the jejunum was placed in the peritoneal cavity. Pneumoperitoneum was maintained by covering the mini-laparotomy site with a wound protector. Esophagojejunostomy was performed using a 25- or 21-mm circular stapler, followed by jejunojejunostomy. The surgeon selected a stapler size suitable for the esophageal lumen. In the majority of patients, a 25-mm stapler was used for esophagojejunostomy. Since 2015, we have been performing esophagojejunostomy and jejunojejunostomy intracorporeally using linear staplers. A 45-mm linear stapler was used to create a side-to-side esophagojejunostomy between the esophagus and the prepared Roux limb [17]. Since January 2009, robotic total gastrectomy has been utilized at our institution using the da Vinci® S, Si, or Xi systems (Intuitive Surgical, Sunnyvale, CA, USA).

    Complication assessment

    Data related to complications were prospectively collected and discussed at a weekly conference. Postoperative complications were defined as complications that occurred in patients during the index admission or within 30 days after the initial surgery. The Clavien-Dindo classification system was used to assess postoperative morbidity and mortality [27]. Clavien-Dindo grade was further divided into two subgroups based on the severity of complications: mild (grade ≤II) and severe (grade ≥IIIa).

    Outcomes

    The incidence of overall, mild, and severe complications after minimally invasive total gastrectomy was assessed in all patients. Clinicopathological and operative characteristics were compared between patients who experienced mild or severe complications and those who did not. The following potential risk factors for complications were considered in the analysis: patient characteristics (age, sex, body mass index [BMI], American Society of Anesthesiologists [ASA] score, preoperative serum hemoglobin, and albumin), pathological characteristics (tumor histology, location, size, stage, and length of proximal margin), and operative characteristics (surgical approach, anastomosis method, operative time, estimated blood loss, extent of lymphadenectomy, and combined resection). We divided BMI into 2 subgroups (>27.5 and ≤27.5 kg/m2) according to the World Health Organization Asian-BMI classification, which defines BMI >27.5 kg/m2 as obese [28].

    Statistical analysis

    Continuous variables were analyzed using Student’s t-test and are reported as the mean and standard deviation. Student’s t-test was performed to compare two continuous variables, and the analysis of variance test was used to compare more than 2 continuous variables. Categorical variables were analyzed using the χ2 test or Fisher’s exact test and are reported as numbers with percentages. For multiple post hoc comparisons based on the severity of complications, Bonferroni correction was applied to appropriately adjust the level of significance.

    Binomial logistic regression analysis was used to identify the risk factors for overall complications after minimally invasive total gastrectomy. In addition, among patients who experienced complications, we evaluated the clinical, pathological, and operative factors associated with the severity of complications using multinomial logistic regression analysis by comparing three categories of outcomes in a unified model, including no complications, mild complications, and severe complications. Multinomial logistic regression was performed using no complications (patients who did not experience any complications) as the reference. All variables (clinical, pathological, and operative) were included in the multivariate analysis, and the relative odds ratios (ORs) and their variances were calculated for retained independent factors [29, 30]. The effect size of significant factors was reported as the relative OR and corresponding 95% confidence interval (CI). The relative OR was computed as the ratio of the ORs for mild versus no complications and severe versus no complications. Statistical significance was set at P<0.05. Data were analyzed using IBM SPSS version 25.0 (IBM Corp., Armonk, NY, USA).

    RESULTS

    Study cohort

    A total of 437 patients underwent minimally invasive total gastrectomy for gastric cancer between 2011 and 2019. We excluded 45 patients who underwent completion total gastrectomy (n=33), palliative total gastrectomy (n=11), and emergency gastrectomy due to bleeding (n=1). Data from the remaining 392 patients were included in the analysis: 289 (73.7%) patients were in the “no complication group” and 103 (26.3%) patients were in the “overall complication group” (Fig. 1). The distribution of complications according to the Clavien-Dindo classification is listed in Supplementary Table 1.

    Fig. 1
    Patient flow diagram.

    Distribution of complications

    As shown in Table 1, the incidence of overall complications after minimally invasive total gastrectomy for gastric cancer was 26.3% (n=103). According to the severity of complications, mild complications occurred in 66 (16.8%) patients, and severe complications were observed in 37 (9.4%) patients. Local complications (n=67, 17.1%) occurred more frequently than systemic complications (n=24, 6.1%). Ileus (n=18, 4.6%) and pulmonary complications (n=15, 3.8%) were the most frequent complications among local and systemic complications, respectively. The most common mild and severe complications were ileus (n=12, 3.1%) and anastomotic leakage (n=7, 1.8%).

    Table 1
    Distribution of complications

    Features related to overall complications

    Clinical, pathological, and operative characteristics were comparable between the no complications and overall complication groups, except for operation time and estimated blood loss. Operation time was significantly longer in the overall complications group than in the no complications group (204.7±53.5 vs. 189.4±49.0 minutes; P=0.008). Estimated blood loss in the overall complication group was also significantly greater than that in the no complications group (176.1±164.3 vs. 125.9±126.5 mL; P=0.005). No mortality was observed in this study (Table 2). The time to soft diet (6.6±4.4 vs. 5.0±1.0 days; P<0.001) and discharge from hospital (10.8±7.0 vs. 7.1±1.3 days; P<0.001) were significantly delayed in the overall complications group compared to the no complications group (Supplementary Fig. 1).

    Table 2
    Features of overall complications

    Characteristics of complications according to severity

    Clinical and pathological characteristics did not differ significantly among the three groups, except for BMI and ASA score. The proportion of obese patients tended to be higher in the severe complications group than in the other groups (24.3 vs. 12.8 and 9.1%, respectively; P=0.082). Patients with an ASA score of 2 or higher were marginally more common in the severe complications group than in the other groups (62.2 vs. 48.8 and 37.9%, respectively; P=0.058). Operative characteristics, operation time, and estimated blood loss were significantly different among the three groups. In multiple comparisons, operation time was longer in the mild complications group than in the no complications group (208.1±48.2 vs. 189.4±49.0 minutes; adjusted P=0.020). The estimated blood loss was greater in the severe complications group (222.7±226.0 mL) than in the no complications and mild complications groups (125.9±126.5 mL; adjusted P<0.001, and 150.0±110.1 mL; adjusted P=0.029, respectively, Table 3). The time to the soft diet of the severe complications group (8.6±6.5 days) was significantly delayed compared to those of the mild and no complications groups (5.5±1.6 and 5.0±1.0 days, respectively; P<0.001). Duration of hospital stay was longer in the severe and mild complications groups (15.1±9.9 and 8.5±2.7 days, respectively) than in the no complications group (7.1±1.3 days; P= 0.01 and P<0.001, respectively, Supplementary Fig. 2).

    Table 3
    Features of mild and severe complications

    Risk factors for overall complications

    Table 4 summarizes the outcomes of univariate and multivariate binomial logistic regression analyses for overall complications. No significant risk factors were found in the clinical and pathological characteristics. Among operative characteristics, operation time (unadjusted OR, 1.06; 95% CI, 1.01−1.11; P=0.009), and estimated blood loss (unadjusted OR, 1.02; 95% CI, 1.01−1.04; P=0.003) were risk factors for overall complications in the univariate analysis. On multivariate analysis, estimated blood loss was identified as the only independent risk factor for overall complications (adjusted OR, 1.02; 95% CI, 1.001−1.04; P=0.037).

    Table 4
    Binomial logistic regression analysis for overall complications

    Risk factors for the severity of complications

    Among the clinical characteristics, obesity (BMI >27.5 kg/m2) marginally increased the risk of severe complications relative to no complications in the univariate multinomial logistic regression analysis (unadjusted OR, 2.19; 95% CI, 0.96−5.00; P=0.063). Among the pathological characteristics, pathological stage II or III was a risk factor for severe complications (unadjusted OR, 1.82; 95% CI, 0.92−3.63; P=0.087); however, this was not statistically significant. Estimated blood loss significantly increased the risk of severe complications relative to no complications (unadjusted OR, 1.04; 95% CI, 1.02−1.06; P=0.001). The only risk factor for mild complications relative to no complications was operative time (unadjusted OR, 1.07; 95% CI, 1.05−1.13; P=0.007). The risk factors for severe complications relative to mild complications were obesity (unadjusted OR, 3.21; 95% CI, 1.04−9.91; P=0.042) and an ASA score of 2 or higher (unadjusted OR, 2.69; 95% CI, 1.18−6.18; P=0.019, Supplementary Table 2).

    Table 5 summarizes the outcomes of the multivariate multinomial logistic regression analysis according to the severity of the complications. A longer operation time increased the risk of mild complications relative to no complications (adjusted OR, 1.06; 95% CI, 1.001−1.13; P=0.047). Obesity (BMI >27.5 kg/m2), advanced stage (II or III), and increased estimated blood loss increased the risk of severe complications relative to both no complications and mild complications. The surgeon’s experience as a factor was not associated with the overall and severity of complications, although the surgeon’s experience with minimally invasive total gastrectomy was different (Supplementary Tables 3 and 4).

    Table 5
    Multivariate multinomial logistic regression analysis according to severity of complications

    DISCUSSION

    The incidence of overall complications in the study group was 26.3%, with incidences of mild and severe complications of 16.8% and 9.4%, respectively. A longer operation time was associated with a higher risk of mild complications, and obesity (BMI >27.5 kg/m2), advanced stage (II or III), and increased intraoperative bleeding increased the risk of severe complications accordingly. Additionally, more intraoperative bleeding was associated with a higher risk of overall complications.

    The incidence of severe complications after minimally invasive total gastrectomy ranges from 1.5% to 11.6% [10, 31, 32, 33, 34]. The rate of severe complications (9.4%) in the present study is consistent with previous reports. Severe complications adversely affect both short- and long-term outcomes [35, 36, 37]. Similarly, in the present study, delayed initiation of a soft diet led to prolonged hospitalization and additional interventions for treatment in some patients.

    This study is the first to evaluate the risk factors related to the severity of complications after minimally invasive total gastrectomy for gastric cancer using a unified model. Previous studies have reported patient-related factors, including age, ASA score, and comorbidities, as causes of severe complications. In the present study, obesity, higher pathological stage, and intraoperative blood loss had independent effects on the risk of severe complications; thus, severe complications were considered to be associated with surgical difficulty.

    Intraoperative blood loss is a risk factor for severe complications. This is similar to open surgery, which increases the risk of short-term complications, such as anastomotic leakage. As intraoperative blood loss increases, it adversely affects long-term survival outcomes [38, 39]. Lower oxygen saturation at the surgical site due to intraoperative bleeding is associated with a high incidence of surgical site infection in abdominal surgery [40]. This study revealed that intraoperative blood loss is an important risk factor for severe complications in minimally invasive total gastrectomy, similar to open surgery. However, determining the absolute cutoff value of intraoperative blood loss for severe complications is impractical. When intraoperative blood loss was divided by the quartile range, the risk of severe complications significantly increased in the fourth quartile (>200 mL) than in the first quartile (≤50 mL, Supplementary Table 5). This implies that intraoperative blood loss may reflect the quality and difficulty of the surgery.

    Another risk factor for severe complications is obesity, which has become one of the most prominent public health concerns worldwide. A previous study reported that, by 2030, approximately 38% of adults will be overweight and approximately 20% will be obese worldwide [41]. Difficulty in securing the surgical field, increased intraoperative blood loss, and longer operation times in obese patients, particularly in those with excessive visceral fat, make surgery technically difficult [42]. An excessive visceral fat area increases the risk of severe complications, such as anastomotic leakage, in gastric cancer surgery [43, 44]. This suggests that obesity is likely to cause increased technical challenges during gastric cancer surgery.

    The advanced stage was another risk factor for severe complications. In cases of advanced stage, manipulation of the stomach with soft tissues in minimally invasive surgery is difficult, and intraoperative bleeding tends to increase. In a large cohort study in Japan, the incidence of anastomotic leakage and reoperation was found to be higher in laparoscopic total gastrectomy than in open total gastrectomy for the treatment of advanced gastric cancer, although overall complication rates were not significantly different [10]. Advanced cancer may also be regarded as a factor affecting surgical difficulty in minimally invasive total gastrectomy.

    Consequently, estimated blood loss, obesity, and advanced stage were identified as risk factors for severe complications in this study, and they were all associated with surgical difficulties [45, 46, 47, 48, 49]. In cases with these risk factors, the risk of severe complications is speculated to increase in minimally invasive total gastrectomy, even if the surgery is performed by an established laparoscopic surgeon.

    In this study, operative time was the only risk factor for mild complications. When the operation time was divided by the quartile range, the risk of mild complications significantly increased in the fourth quartile (≥220 min) compared to the first quartile (<160 minutes, Supplementary Table 6). The operation time of minimally invasive surgery is generally longer than that of open surgery, which can explain its inability to significantly reduce complications compared to open total gastrectomy [50, 51]. The longer operation time of the minimally invasive approach could be attributed to the demanding procedures and non-standardization of procedures. In minimally invasive total gastrectomy, esophagojejunostomy or extended lymph node dissection for advanced cancer is one of the most technically challenging procedures. However, these procedures have not yet been standardized. While the use of a circular stapler has generally been the standard for open total gastrectomy for decades, the standard for esophagojejunostomy has not yet been established in minimally invasive surgery. For this reason, several methods of reconstruction using linear staplers, circular staplers, and an orally inserted anvil have been reported in the literature [15, 16, 17, 18, 19]. In addition, several methods for splenic hilar dissection have also been described accordingly [32, 52, 53, 54, 55]. Standardization of procedures and avoidance of unnecessary procedures may help reduce the operative time in minimally invasive total gastrectomy.

    This study has several limitations. First, there was a risk of bias in patient selection due to the retrospective nature of the study. Second, the total number of patients who experienced severe complications was relatively small, although the study duration was approximately one decade. Thus, a large cohort of patients from multiple centers is warranted to verify the results of this study. Third, the generalizability of the current findings to the Western population is uncertain because of the inclusion of only an Eastern cohort in this study. Eastern populations have relatively lower BMIs and more early-stage gastric cancers than Western populations. Potential risk factors for mild and severe complications in the Western population might differ from those in the Eastern population. Therefore, validation in a Western population is warranted accordingly.

    In conclusion, the risk factors for mild and severe complications after minimally invasive total gastrectomy for gastric cancer were associated with surgery, thus demonstrating the technical difficulty of the procedure. Severe complications were associated with obesity, advanced stage, and more intraoperative blood loss, and mild complications were associated with a longer operative time. Surgeons must weigh the potential risks associated with the severity of complications and continue to standardize these demanding procedures.

    SUPPLEMENTARY MATERIALS

    Supplementary Table 1

    Distribution of complications according to the Clavien-Dindo classification.

    Click here to view.(28K, xls)

    Supplementary Table 2

    Univariate multinomial logistic regression analysis according to the severity of complications.

    Click here to view.(36K, xls)

    Supplementary Table 3

    Binomial logistic regression analysis of the association of surgeon’s factor with overall complications.

    Click here to view.(27K, xls)

    Supplementary Table 4

    Multivariate multinomial logistic regression analysis of the association of surgeon’s factor with the severity of the complication.

    Click here to view.(27K, xls)

    Supplementary Table 5

    Effect of estimated blood loss on complications.

    Click here to view.(28K, xls)

    Supplementary Table 6

    Effect of operation time on complications.

    Click here to view.(28K, xls)

    Supplementary Fig. 1

    Comparison of the postoperative course according to the overall complications.

    Click here to view.(533K, ppt)

    Supplementary Fig. 2

    Comparison of the postoperative course according to the severity of complications.

    Click here to view.(585K, ppt)

    Notes

    Author Contributions::

    • Conceptualization: R.C.K.

    • Data curation: R.C.K., L.S.

    • Formal analysis: S.S.Y., H.H.

    • Writing - original draft: R.C.K.

    • Writing - review & editing: H.H., H.S.U.

    Conflict of Interest:No potential conflict of interest relevant to this article was reported.

    ACKNOWLEDGMENTS

    We would like to thank Editage (www.editage.co.kr) for English language editing.

    References

      1. Kehlet H, Wilmore DW. Evidence-based surgical care and the evolution of fast-track surgery. Ann Surg 2008;248:189–198.
      1. Wee IJ, Syn NL, Shabbir A, Kim G, So JB. Enhanced recovery versus conventional care in gastric cancer surgery: a meta-analysis of randomized and non-randomized controlled trials. Gastric Cancer 2019;22:423–434.
      1. Kim W, Kim HH, Han SU, Kim MC, Hyung WJ, Ryu SW, et al. Decreased morbidity of laparoscopic distal gastrectomy compared with open distal gastrectomy for stage I gastric cancer: short-term outcomes from a multicenter randomized controlled trial (KLASS-01). Ann Surg 2016;263:28–35.
      1. Lee HJ, Hyung WJ, Yang HK, Han SU, Park YK, An JY, et al. Short-term outcomes of a multicenter randomized controlled trial comparing laparoscopic distal gastrectomy with D2 lymphadenectomy to open distal gastrectomy for locally advanced gastric cancer (KLASS-02-RCT). Ann Surg 2019;270:983–991.
      1. Kim HH, Han SU, Kim MC, Kim W, Lee HJ, Ryu SW, et al. Effect of laparoscopic distal gastrectomy vs open distal gastrectomy on long-term survival among patients with stage i gastric cancer: the KLASS-01 randomized clinical trial. JAMA Oncol 2019;5:506–513.
      1. Shin HJ, Son SY, Wang B, Roh CK, Hur H, Han SU. Long-term comparison of robotic and laparoscopic gastrectomy for gastric cancer: a propensity score-weighted analysis of 2084 consecutive patients. Ann Surg 2021;274:128–137.
      1. Hyung WJ, Yang HK, Park YK, Lee HJ, An JY, Kim W, et al. Long-term outcomes of laparoscopic distal gastrectomy for locally advanced gastric cancer: the KLASS-02-RCT randomized clinical trial. J Clin Oncol 2020;38:3304–3313.
      1. Ahmad R, Schmidt BH, Rattner DW, Mullen JT. Factors influencing readmission after curative gastrectomy for gastric cancer. J Am Coll Surg 2014;218:1215–1222.
      1. Chen K, Pan Y, Zhai ST, Yu WH, Pan JH, Zhu YP, et al. Totally laparoscopic versus open total gastrectomy for gastric cancer: a case-matched study about short-term outcomes. Medicine (Baltimore) 2017;96:e8061
      1. Kodera Y, Yoshida K, Kumamaru H, Kakeji Y, Hiki N, Etoh T, et al. Introducing laparoscopic total gastrectomy for gastric cancer in general practice: a retrospective cohort study based on a nationwide registry database in Japan. Gastric Cancer 2019;22:202–213.
      1. Lee KG, Lee HJ, Yang JY, Oh SY, Bard S, Suh YS, et al. Risk factors associated with complication following gastrectomy for gastric cancer: retrospective analysis of prospectively collected data based on the Clavien-Dindo system. J Gastrointest Surg 2014;18:1269–1277.
      1. Kim DJ, Lee JH, Kim W. Comparison of the major postoperative complications between laparoscopic distal and total gastrectomies for gastric cancer using Clavien-Dindo classification. Surg Endosc 2015;29:3196–3204.
      1. Nomura S, Sasako M, Katai H, Sano T, Maruyama K. Decreasing complication rates with stapled esophagojejunostomy following a learning curve. Gastric Cancer 2000;3:97–101.
      1. Roh CK, Choi S, Seo WJ, Cho M, Kim HI, Lee SK, et al. Incidence and treatment outcomes of leakage after gastrectomy for gastric cancer: experience of 14,075 patients from a large volume centre. Eur J Surg Oncol 2021;47:2304–2312.
      1. Chen K, Pan Y, Cai JQ, Xu XW, Wu D, Yan JF, et al. Intracorporeal esophagojejunostomy after totally laparoscopic total gastrectomy: a single-center 7-year experience. World J Gastroenterol 2016;22:3432–3440.
      1. Duan W, Liu K, Fu X, Shen X, Chen J, Su C, et al. Semi-end-to-end esophagojejunostomy after laparoscopy-assisted total gastrectomy better reduces stricture and leakage than the conventional end-to-side procedure: a retrospective study. J Surg Oncol 2017;116:177–183.
      1. Son SY, Cui LH, Shin HJ, Byun C, Hur H, Han SU, et al. Modified overlap method using knotless barbed sutures (MOBS) for intracorporeal esophagojejunostomy after totally laparoscopic gastrectomy. Surg Endosc 2017;31:2697–2704.
      1. Zhang S, Khaliq J, Li D, Jiang X, Sun R, Li Y. Robotic total gastrectomy with π-shaped esophagojejunostomy using a linear stapler as a novel technique. World J Surg Oncol 2018;16:238.
      1. Lee SW, Kawai M, Tashiro K, Kawashima S, Tanaka R, Tanaka K, et al. The crossover technique for intracorporeal esophagojejunostomy following laparoscopic total gastrectomy: a simple and safe technique using a linear stapler and two barbed sutures. Surg Endosc 2019;33:1386–1393.
      1. Migita K, Takayama T, Matsumoto S, Wakatsuki K, Enomoto K, Tanaka T, et al. Risk factors for esophagojejunal anastomotic leakage after elective gastrectomy for gastric cancer. J Gastrointest Surg 2012;16:1659–1665.
      1. Zuiki T, Hosoya Y, Kaneda Y, Kurashina K, Saito S, Ui T, et al. Stenosis after use of the double-stapling technique for reconstruction after laparoscopy-assisted total gastrectomy. Surg Endosc 2013;27:3683–3689.
      1. Oshi M, Kunisaki C, Miyamoto H, Kosaka T, Akiyama H, Endo I. Risk factors for anastomotic leakage of esophagojejunostomy after laparoscopy-assisted total gastrectomy for gastric cancer. Dig Surg 2018;35:28–34.
      1. Rawicz-Pruszyński K, Sędłak K, Mlak R, Mielko J, Polkowski WP. Mixed type histology as a predictive factor for esophagojejunostomy leak in advanced gastric cancer. Cancers (Basel) 2020;12:E1701
      1. Kang BH, Xuan Y, Hur H, Ahn CW, Cho YK, Han SU. Comparison of surgical outcomes between robotic and laparoscopic gastrectomy for gastric cancer: the learning curve of robotic surgery. J Gastric Cancer 2012;12:156–163.
      1. Japanese Gastric Cancer AssociationJapanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer 2017;20:1–19.
      1. Guideline Committee of the Korean Gastric Cancer Association (KGCA), Development Working Group & Review PanelKorean Practice Guideline for Gastric Cancer 2018: an evidence-based, multi-disciplinary approach. J Gastric Cancer 2019;19:1–48.
      1. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205–213.
      1. WHO Expert ConsultationAppropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 2004;363:157–163.
      1. Lee K, Ahn H, Moon H, Kodell RL, Chen JJ. Multinomial logistic regression ensembles. J Biopharm Stat 2013;23:681–694.
      1. Sun B, VanderWeele T, Tchetgen Tchetgen EJ. A multinomial regression approach to model outcome heterogeneity. Am J Epidemiol 2017;186:1097–1103.
      1. Gong CS, Kim BS, Kim HS. Comparison of totally laparoscopic total gastrectomy using an endoscopic linear stapler with laparoscopic-assisted total gastrectomy using a circular stapler in patients with gastric cancer: a single-center experience. World J Gastroenterol 2017;23:8553–8561.
      1. Yang K, Cho M, Roh CK, Seo WJ, Choi S, Son T, et al. Robotic spleen-preserving splenic hilar lymph node dissection during total gastrectomy for gastric cancer. Surg Endosc 2019;33:2357–2363.
      1. Yang HK, Hyung WJ, Han SU, Lee YJ, Park JM, Cho GS, et al. Comparison of surgical outcomes among different methods of esophagojejunostomy in laparoscopic total gastrectomy for clinical stage I proximal gastric cancer: results of a single-arm multicenter phase II clinical trial in Korea, KLASS 03. Surg Endosc 2021;35:1156–1163.
      1. Sakamoto T, Fujiogi M, Matsui H, Fushimi K, Yasunaga H. Short-term outcomes of laparoscopic and open total gastrectomy for gastric cancer: a nationwide retrospective cohort analysis. Ann Surg Oncol 2020;27:518–526.
      1. Sierzega M, Kolodziejczyk P, Kulig J, Polish Gastric Cancer Study GroupImpact of anastomotic leakage on long-term survival after total gastrectomy for carcinoma of the stomach. Br J Surg 2010;97:1035–1042.
      1. Nagasako Y, Satoh S, Isogaki J, Inaba K, Taniguchi K, Uyama I. Impact of anastomotic complications on outcome after laparoscopic gastrectomy for early gastric cancer. Br J Surg 2012;99:849–854.
      1. Kamarajah SK, Navidi M, Griffin SM, Phillips AW. Impact of anastomotic leak on long-term survival in patients undergoing gastrectomy for gastric cancer. Br J Surg 2020;107:1648–1658.
      1. Ito Y, Kanda M, Ito S, Mochizuki Y, Teramoto H, Ishigure K, et al. Intraoperative blood loss is associated with shortened postoperative survival of patients with stage II/III gastric cancer: analysis of a multi-institutional dataset. World J Surg 2019;43:870–877.
      1. Mizuno A, Kanda M, Kobayashi D, Tanaka C, Iwata N, Yamada S, et al. Adverse effects of intraoperative blood loss on long-term outcomes after curative gastrectomy of patients with stage II/III gastric cancer. Dig Surg 2016;33:121–128.
      1. Ives CL, Harrison DK, Stansby GS. Tissue oxygen saturation, measured by near-infrared spectroscopy, and its relationship to surgical-site infections. Br J Surg 2007;94:87–91.
      1. Kelly T, Yang W, Chen CS, Reynolds K, He J. Global burden of obesity in 2005 and projections to 2030. Int J Obes 2008;32:1431–1437.
      1. Chen K, Pan Y, Zhai ST, Cai JQ, Chen QL, Chen DW, et al. Laparoscopic gastrectomy in obese gastric cancer patients: a comparative study with non-obese patients and evaluation of difference in laparoscopic methods. BMC Gastroenterol 2017;17:78.
      1. Tokunaga M, Hiki N, Fukunaga T, Ogura T, Miyata S, Yamaguchi T. Effect of individual fat areas on early surgical outcomes after open gastrectomy for gastric cancer. Br J Surg 2009;96:496–500.
      1. Takeuchi M, Ishii K, Seki H, Yasui N, Sakata M, Shimada A, et al. Excessive visceral fat area as a risk factor for early postoperative complications of total gastrectomy for gastric cancer: a retrospective cohort study. BMC Surg 2016;16:54.
      1. Kunisaki C, Makino H, Takagawa R, Sato K, Kawamata M, Kanazawa A, et al. Predictive factors for surgical complications of laparoscopy-assisted distal gastrectomy for gastric cancer. Surg Endosc 2009;23:2085–2093.
      1. Jeong O, Ryu SY, Zhao XF, Jung MR, Kim KY, Park YK. Short-term surgical outcomes and operative risks of laparoscopic total gastrectomy (LTG) for gastric carcinoma: experience at a large-volume center. Surg Endosc 2012;26:3418–3425.
      1. Wu XS, Wu WG, Li ML, Yang JH, Ding QC, Zhang L, et al. Impact of being overweight on the surgical outcomes of patients with gastric cancer: a meta-analysis. World J Gastroenterol 2013;19:4596–4606.
      1. Kinoshita T, Kaito A. Current status and future perspectives of laparoscopic radical surgery for advanced gastric cancer. Transl Gastroenterol Hepatol 2017;2:43.
      1. Zhao B, Zhang J, Mei D, Luo R, Lu H, Xu H, et al. Does high body mass index negatively affect the surgical outcome and long-term survival of gastric cancer patients who underwent gastrectomy: a systematic review and meta-analysis. Eur J Surg Oncol 2018;44:1971–1981.
      1. Liu F, Huang C, Xu Z, Su X, Zhao G, Ye J, et al. Morbidity and mortality of laparoscopic vs open total gastrectomy for clinical stage I gastric cancer: the CLASS02 multicenter randomized clinical trial. JAMA Oncol 2020;6:1590–1597.
      1. van der Wielen N, Straatman J, Daams F, Rosati R, Parise P, Weitz J, et al. Open versus minimally invasive total gastrectomy after neoadjuvant chemotherapy: results of a European randomized trial. Gastric Cancer 2021;24:258–271.
      1. Huang CM, Huang ZN, Zheng CH, Li P, Xie JW, Wang JB, et al. Huang’s three-step maneuver shortens the learning curve of laparoscopic spleen-preserving splenic hilar lymphadenectomy. Surg Oncol 2017;26:389–394.
      1. Ji X, Fu T, Bu ZD, Zhang J, Wu XJ, Zong XL, et al. Comparison of different methods of splenic hilar lymph node dissection for advanced upper- and/or middle-third gastric cancer. BMC Cancer 2016;16:765.
      1. Kinoshita T, Shibasaki H, Enomoto N, Sahara Y, Sunagawa H, Nishida T. Laparoscopic splenic hilar lymph node dissection for proximal gastric cancer using integrated three-dimensional anatomic simulation software. Surg Endosc 2016;30:2613–2619.
      1. Wang B, Son SY, Han SU. A simple approach for splenic hilar lymphadenectomy during laparoscopic total gastrectomy for advanced gastric cancer: the SHINY (Splenic HIlar Node dissection after total gastrectomY) maneuver. J Gastrointest Surg 2020;24:1223–1227.
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    MeSH Terms
    Cohort Studies*
    Gastrectomy*
    Hemorrhage
    Humans
    Incidence
    Laparoscopy
    Logistic Models
    Obesity
    Postoperative Complications
    Respect
    Retrospective Studies*
    Risk Factors*
    Stomach Neoplasms*
    Surgeons
    Metrics
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