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Effect of different surgical approaches on the survival and safety of Siewert type II esophagogastric junction adenocarcinoma: a systematic review and meta-analysis

BMC Cancer volume 23, Article number: 1130 (2023) Cite this article

Abstract

Background

Whether a transthoracic (TT) procedure by a thoracic surgeon or a transabdominal (TA) by a gastrointestinal surgeon is best for Siewert type II esophagogastric junction adenocarcinoma (EGJA) remains unknown. Survival and perioperative outcomes were compared between the two groups in this meta-analysis to clarify this argument.

Methods

We searched 7 databases for eligible studies comparing TT and TA procedures for Siewert type II EGJA. The final analyzed endpoints included intraoperative and hospitalization outcomes, recurrence, complication, and survival.

Results

Seventeen studies involving 10,756 patients met the inclusion criteria. The TA group had higher rates of overall survival (OS) (HR: 1.31 [1.20 ~ 1.44], p < 0.00001) and disease-free survival (DFS) (HR: 1.49 [1.24 ~ 1.79], p < 0.0001). The survival advantage of OSR and DFSR increased with time. Subgroup analysis of OS and DFS suggested that TA remained the preferred approach among all subgroups. More total/positive lymph nodes were retrieved, and fewer lymph node recurrences were found in the TA group. The analysis of perioperative outcomes revealed that the TA procedure was longer, had more intraoperative blood loss, and prolonged hospital stay. Similar R0 resection rates, as well as total recurrence, local recurrence, liver recurrence, peritoneal recurrence, lung recurrence, anastomosis recurrence and multiple recurrence rates, were found between the two groups. The safety analysis showed that the TT procedure led to more total complications, anastomotic leakages, cases of pneumonia, and cases of pleural effusion.

Conclusions

The TA procedure appeared to be a suitable choice for patients with Siewert type II EGJA because of its association with longer survival, fewer recurrences, and better safety.

Peer Review reports

Introduction

In Western countries, the incidence of esophagogastric junction adenocarcinoma (EGJA) has increased significantly each year [1, 2]. Compared with esophageal and gastric cancer, its therapeutic effect is unsatisfactory, and one of the important reasons is that the treatment methods are not uniform or standardized, especially the surgical methods [3]. The classification system reported by Siewert et al. has been widely accepted in clinical practice in the past 20 years [4]. Esophagectomy + proximal gastrectomy (transthoracic [TT] or thoracoabdominal) is suitable for Siewert type I EGJA, and extended gastrectomy + distal esophagus resection (transabdominal [TA]) is suitable for type III EGJA [5]. However, for Siewert type II EGJA, whether esophagectomy + proximal gastrectomy performed in the TT procedure is better than extended gastrectomy + distal esophagus resection performed in the TA procedure has been debated by thoracic surgeons and gastrointestinal surgeons for decades.

In clinical studies, there were also notable differences regarding this argument. Chen et al. reported that the TA approach was associated with a longer overall survival (OS) time than the TT approach [6]. Voron et al. reported longer disease-free survival (DFS) in the TA group [7]. The survival advantages of the TA group were also found in some other studies [8, 9]. Longer survival may be associated with better lymph node dissection and fewer complications (anastomotic leakage, pneumonia, etc.) [9,10,11]. However, Blank et al. reported an opposite survival result [12]. In some other studies, no survival differences were found between the two groups [13, 14].

To clarify this clinical debate, the survival rate, recurrence rate, and perioperative outcomes were compared between the two groups in this meta-analysis.

Materials and methods

Throughout the implementation of this study, the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) statement was used as a checklist. (Table S1). (This study has been registered in PROSPERO, ID: CRD42023401527).

Search strategy

PubMed, ScienceDirect, The Cochrane Library, Scopus, Ovid MEDLINE, EMBASE, Web of Science, and Google Scholar were searched to find relevant literature published from their inception to January 2023. We used text and medical subject headings (MeSH) terms as follows: “Transthoracic”, “Transabdominal”, and “esophagogastric junction adenocarcinoma” (details are listed in Table S2). We also hand-searched the references of the included studies for further relevant articles.

Selection criteria

Inclusion criteria:

  1. (1)

    Population: Patients with Siewert type II EGJA.

  2. (2)

    Intervention and comparison: TT (Surgery procedure of digestive tract: esophagectomy, proximal gastrectomy and esophagogastrostomy; Range of lymph node dissection [LND]: two-fields lymphadenectomy. Different transthoracic approaches [Left single incision or thoracoabdominal two incisions], managements of residual stomach [gastric tube or not] and surgical forms [traditional open surgery or minimally invasive surgery] are all acceptable) vs. TA (Surgery procedure of digestive tract: extended gastrectomy with distal esophagus resection, and esophagojejunostomy; Range of LND: D1+ or D2 lymphadenectomy. Different surgical forms [traditional open surgery or minimally invasive surgery] are all acceptable).

  3. (3)

    Outcomes: Intraoperative and hospitalization outcomes, recurrence, complication, and survival.

  4. (4)

    Study design: Cohort study (CT) or RCT.

Exclusion criteria: basic/animal-based study, review, meta-analysis, abstract only, and study lacking the data of the above outcomes.

Data extraction

The following data were extracted by two independent investigators (HYZ and YMY): participant characteristics, intraoperative and hospitalization outcomes (operating time, intraoperative blood loss, etc.), recurrence (total, local, lymph node recurrence, etc.), complications (total complication, complication [Clavien-Dindo classification III–IV], postoperative mortality, etc.) [15], and survival (OS, DFS, etc.). Disagreements were resolved by the above two investigators through recheck and discussion.

Outcome assessments

As a supplement to survival data (OS, PFS), we also analyzed the survival rate at 1, 2, 3, and 5 years. Subgroup analysis of OS and DFS was performed according to published year, region, TT group, surgical volume, and study design.

Quality assessment of the included studies

The Jadad Scale (5 points) was used to assess the RCTs. The assessment tool focused on three main items: accountability of patients, randomization, and masking. Studies of high quality scored three or more [16].

The Newcastle–Ottawa Scale (NOS, 9 points) was used to assess the CTs. The assessment tool focused on the following criteria: selection (four points), comparability (two points), and exposure (three points). Studies of high quality scored eight or nine points, and studies of medium quality scored six or seven points [17].

The evidence level of the results was assessed by the Grades of Recommendations Assessment, Development and Evaluation (GRADE) system based on publication bias, inconsistency, indirectness, risk of bias, and imprecision [18].

Statistical analysis

All statistical analyses were performed using STATA 12.0 software and Review Manager 5.3. The pooled risk ratio (RR) was used to analyze dichotomous variables (recurrences, complications, etc.). The mean difference (MD) was used to analyze continuous variables (intraoperative blood loss, operating time, etc.). The hazard ratio (HR) was used to analyze survival data (OS and DFS). In the analysis of advantageous outcomes (OS, number of lymph nodes retrieved, etc.), RR > 1, MD > 0, or HR < 1 suggested that it was beneficial to the TT group. In the analysis of disadvantageous outcomes (recurrences, intraoperative blood loss, etc.), RR > 1 or MD > 0 suggested that it was beneficial to the TA group. I2 and Cochran’s Q test were used to assess interstudy heterogeneity. When the p value was > 0.1 and the I2 value was ≤ 50%, a fixed-effects model was used; otherwise, a random-effects model was applied. Funnel plots were conducted to assess publication bias. A p value < 0.05 indicated that the results were significantly different.

Results

Study identification and characteristics

After screening 2459 relevant publications, we included 17 studies for the meta-analysis, of which 15 studies were CTs and the other 2 studies were RCTs (Fig. 1) [6,7,8,9,10,11,12,13,14, 19,20,21,22,23,24,25,26]. These 17 studies included 10,756 patients in total, including 8026 in the TA group and 2730 in the TT group. Table 1 summarizes the characteristics of the 17 studies. Table S3 summarizes the quality assessments of the included studies, in which 9 studies were of high quality and 8 studies were of medium quality. Table 2 summarizes the evidence level assessments of the results, in which all evidence levels were very low or low.

Fig. 1
figure 1

Flow chart of the study selection process

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Table 1 Summary of the baseline characteristics of the included studies
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Table 2 GRADE quality assessment by therapeutic strategy and study design for the outcomes
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Survival

Longer OS was achieved in the TA group (HR: 1.31 [1.20 ~ 1.44], p < 0.00001, Fig. 2). In the analysis of OSR, the survival rate of the TA group was higher than that of the TT group in all years (1, 2, 3, and 5 years) (Fig. 3). The survival advantage of OSR increased with time (RR increased from 0.96 to 0.79) (Fig. 4A).

Fig. 2
figure 2

Forest plots of overall survival and disease-free survival associated with transthoracic surgery and transabdominal surgery

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Fig. 3
figure 3

Forest plots of overall survival rate at 1, 2, 3, 5 years associated with transthoracic surgery and transabdominal surgery

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Fig. 4
figure 4

Line charts of overall survival rate (1, 2, 3, 5 years, A) and disease-free survival rate (1, 2, 3, 5 years, B) associated with transthoracic surgery and transabdominal surgery

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Longer DFS was achieved in the TA group (HR: 1.49 [1.24 ~ 1.79], p < 0.0001, Fig. 2). In the analysis of DFSR, the survival rate of the TA group was higher than that of the TT group in all years (1, 2, 3, and 5 years) (Fig. 5). The survival advantage of DFSR increased with time (RR increased from 0.87 to 0.71) (Fig. 4B).

Fig. 5
figure 5

Forest plots of disease-free survival rate at 1, 2, 3, 5 years associated with transthoracic surgery and transabdominal surgery

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Subgroup analysis of survival

A subgroup analysis of OS and DFS was performed according to publication year (earlier than 2017 or 2017–2023), region (East Asia or Europe), TT group (thoracoabdominal or left transthoracic), surgical volume (> 20 per year or < 20 per year), and study design (RCT or CT). In the analysis of OS and DFS, there was no change in the preferred procedure among all subgroups. However, in the subgroups of region (Europe), TT group (left transthoracic), surgical volume (< 20 per year), and study design (RCT), there was no significant difference in OS associated with TA procedures. In subgroups of surgical volume (> 20 per year) and study design (RCT), there was no significant difference in the DFS advantage of the TA group (Table 3).

Table 3 Subgroup analysis of overall survival and disease-free survival
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Intraoperative and hospitalization indicators

Operating time (MD: 35.75 [3.08 ~ 68.42] minutes, p = 0.03, Fig. 6A), intraoperative blood loss (MD: 32.16 [4.83 ~ 59.49] mL, p = 0.02, Fig. 6B), number of lymph nodes retrieved (MD: -4.17 [4.83 ~ 59.49], p = 0.02, Fig. 6C), number of positive lymph nodes retrieved (MD: -3.07 [-0.74~-0.01], p = 0.04, Fig. 6D), and length of hospital stay (MD: 2.47 [0.60 ~ 4.35] days, p = 0.01, Fig. 6F) were better in the TA group. The R0 resection rate (RR: 0.99 [0.95 ~ 1.03], p = 0.64, Fig. 6E) was similar between the two groups.

Fig. 6
figure 6

Forest plots of intraoperative and hospitalization indicators associated with transthoracic surgery and transabdominal surgery: (A) operating time; (B) intraoperative blood loss; (C) number of lymph node retrieved; (D) number of positive lymph node retrieved; (E) R0 resection; (F) hospital stay

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Recurrence

Fewer lymph node recurrences (RR: 2.90 [1.12 ~ 7.52], p = 0.03) were found in the TA group. The total recurrence, local recurrence, liver recurrence, peritoneal recurrence, lung recurrence, anastomosis recurrence and multiple recurrence rates were similar between the two groups (Figure S1).

Complications

In summary, more total complications (RR: 1.39 [1.10 ~ 1.74], p = 0.005) were found in the TA group. Complications (Clavien‒Dindo classification III–-IV) and postoperative mortality were similar between the two groups (Fig. 7).

Fig. 7
figure 7

Forest plots of complication summary (total complication, complication [Claviene Dindo classification III-IV] and postoperative mortality) associated with transthoracic surgery and transabdominal surgery

Full size image

Fewer anastomotic leakages (RR: 1.58 [1.10 ~ 2.27], p = 0.01), pneumonia (RR: 1.71 [1.30 ~ 2.25], p = 0.0001) and pleural effusion (RR: 1.92 [1.04 ~ 3.52], p = 0.04) were found in the TA group. Similar incidences of postoperative hemorrhage, anastomotic bleeding, intraperitoneal bleeding, anastomotic leakage, reoperation, wound infection, peritonitis, pneumothorax, jejunal stump leakage, duodenum stump leakage, wound rupture, esophago-bronchial fistula, gastric tube perforation, necrosis of gastric tube, pancreatic fistula, gastroparesis, anastomotic stricture, pyothorax, bowel obstruction and dumping syndrome were found between the two groups (Table 4, Figure S2).

Table 4 Complications in TT group and TA group
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Sensitivity analysis

In the analysis of intraoperative blood loss, operating time, number of lymph nodes retrieved, number of positive lymph nodes retrieved, and length of hospital stay, significant heterogeneity was found. After removal of each study, the tendency of the results did not change, which confirmed the stability and reliability of these results (Figure S3).

Publication bias

Funnel plots based on the data regarding survival (OS, PFS) (Figure S4A), OSR (Figure S4B), and DFSR (Figure S4C) suggested that there was no significant publication bias.

Discussion

EGJA is one of the major cancers with high morbidity and mortality rates worldwide; however, its treatment is not standardized, and the therapeutic effect is unsatisfactory [27]. Whether a transthoracic (TT) procedure by a thoracic surgeon or a transabdominal (TA) by a gastrointestinal surgeon is best for Siewert type II esophagogastric junction adenocarcinoma (EGJA) remains unknown [8, 12, 13]. We first conducted this meta-analysis to answer this question. In this study, the TA procedure achieved longer OS and DFS than the TT procedure. The OSR and the DFSR increased with time. More total/positive lymph nodes were retrieved, and fewer lymph node recurrences were found in the TA group. In the analysis of perioperative outcomes, a longer operating time, more intraoperative blood loss, and a longer hospital stay were found in the TA group. In the analysis of complications, more total complications, anastomotic leakage, pneumonia, and pleural effusion were found in the TT group.

In this analysis, longer OS and DFS were the strongest supporting evidence for the TA group. Better survival results were also reported by Voron et al.’s and Xing et al.’s studies [7, 8]. Two results in our study might explain this advantage: (1) More total lymph nodes and positive lymph nodes were retrieved in the TA group, which directly led to a lower rate of lymph node recurrence after surgery. We believed that the insufficient dissection of lymph nodes is mainly related to the increased difficulty of abdominal lymph node dissection in TT procedures and thoracic surgeons’ lack of understanding of abdominal lymph node dissection [9, 10, 28]. (2) Another explanation for this advantage is the safety of the surgery. In our analysis, a longer operating time, more intraoperative blood loss, a longer hospital stay, and more complications were found in the TT group, which directly led to the higher perioperative mortality rate and indirectly affected the long-term survival of patients [11]. In subgroup analysis of survival, TA procedures remained the preferred choice among all subgroups. The OSR (RR increased from 0.96 to 0.79) and DFSR (RR increased from 0.87 to 0.71) increased with time. In summary, we believe that TA procedures had survival advantages over TT procedures.

Fewer postoperative complication was another advantage of the TA approach. The addition of thoracotomy and thoracic lymph node dissection will increase the incidence of complications, which is also in line with the actual clinical situation. In our study, more total complications, anastomotic leakages, pneumonia cases, and pleural effusion cases were found in the TT group. Anastomotic leakage is the most troublesome complication after the resection of esophageal and cardiac tumors and one of the main causes for perioperative death. In our study, the probability of anastomotic leakage was 5.41% in the TT group and 5.08% in the TA group; the tendency of favoring TA was confirmed in the 8/11 relevant studies [8, 12, 13, 19, 20, 22, 23, 25]. Xing et al. reported a similar result and suggested that a prolonged operation and difficult reinforcement of the anastomosis might be the cause of this difference [8]. We believe that better blood supply and higher probability of incarceration of the cardiac hole may also explain the higher probability of anastomotic leakage in the TT group. Pneumonia is highly prevalent in patients who undergo the TT approach and may endanger the patient’s life during the perioperative period. The tendency to favor TA was confirmed in all 8 relevant studies [9, 11, 12, 19, 20, 22, 23, 26]. The higher rate of pneumonia in the TT group was mainly due to a chest wall injury caused by thoracotomy and the collapse and expansion of the lung during operation [29]. Based on the above reasons, for the EGJA patients in poor physical condition who cannot tolerate thoracotomy, the TA surgery is a good choice.

Although this study systematically analyzed all relevant studies with large size samples and all the involved outcomes, there were still some deficiencies that need to be considered. First, not all the included studies (2/17) were RCTs, which might decrease the evidence level of the results. Second, there were differences in the surgical volume, surgical methods, and criteria for determining the outcomes in different research centers, especially in the TT group. Although subgroup analysis and sensitivity analysis were conducted, there was still heterogeneity in the combined analysis of the outcomes. Third, some meta-analyses involved relatively few or even only one study, which may have affected the reliability of the results. Fourth, the patients were enrolled at different time points in these 17 studies, possibly leading to major changes in surgical methods and surgical requirements that might affect the consistency of outcomes. Fifth, due to insufficient data provided, there might be differences between the two groups regarding tumor size, staging, and lymph node metastasis, which might affect the comparability of the data between the groups.

Conclusion

For patients with Siewert type II EGJA, the TA procedure was a better choice because of its ability to prolong OS and DFS when compared with the TT procedure. The OSR and DFSR increased with time. More complete lymph node dissection and fewer lymph node recurrences were the main reasons for the survival advantage seen in the TA group. In terms of safety, more total complications, anastomotic leakages, pneumonia cases, and pleural effusion cases were found in the TT group. However, due to the above deficiencies, the conclusions of this study still need to be verified in large sample RCTs in the future.

Availability of data and materials

The data sets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

CT:

Cohort study

CI:

Confidence interval

DFS:

Disease-free survival

DFSR:

Disease-free survival rate

EGJA:

Esophagogastric junction adenocarcinoma

GRADE:

Grading of Recommendations Assessment, Development and Evaluation

HR:

Hazard ratio

MeSH:

Medical subject headings

MD:

Mean difference

NOS:

Newcastle-Ottawa Scale

OS:

Overall survival

OSR:

Overall survival rate

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

RCT:

Randomized clinical trial

RR:

Risk ratio

TA:

Transabdominal

TNM:

Tumor Node Metastasis

TT:

Transthoracic

References

  1. Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023;73(1):17–48.

    Article  PubMed  Google Scholar 

  2. Giaquinto AN, Miller KD, Tossas KY, Winn RA, Jemal A, Siegel RL. Cancer statistics for African American/Black people 2022. CA Cancer J Clin. 2022;72(3):202–29.

    Article  PubMed  Google Scholar 

  3. Ajani JA, D’Amico TA, Bentrem DJ, Chao J, Corvera C, Das P, et al. Esophageal and Esophagogastric Junction Cancers, Version 2.2019, NCCN Clinical Practice guidelines in Oncology. J Natl Compr Canc Netw. 2019;17(7):855–83.

    Article  PubMed  CAS  Google Scholar 

  4. Siewert JR, Stein HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg. 1998;85(11):1457–9.

    Article  PubMed  CAS  Google Scholar 

  5. Greally M, Agarwal R, Ilson DH. Optimal management of gastroesophageal junction cancer. Cancer. 2019;125(12):1990–2001.

    Article  PubMed  Google Scholar 

  6. Chen Y, Zhao XK, Xu RH, Song X, Yang MM, Zhou FY, et al. Transthoracic, thoracoabdominal, and transabdominal surgical approaches for gastric cardia adenocarcinomas: a survival evaluation based on a cohort of 7103 patients. World J Surg Oncol. 2022;20(1):217.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Voron T, Gronnier C, Pasquer A, Thereaux J, Gagniere J, Lebreton G, et al. Adenocarcinoma of the oesophagogastric junction Siewert II: an oesophageal cancer better cured with total gastrectomy. Eur J Surg Oncol. 2019;45(12):2473–81.

    Article  PubMed  Google Scholar 

  8. Xing J, Liu M, Xu K, Gao P, Tan F, Yao Z, et al. Short-term and long-term outcomes following transhiatal versus right Thoracoabdominal Resection of Siewert Type II adenocarcinoma of the Esophagogastric Junction. Cancer Manag Res. 2020;12:11813–21.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Zhang W, Chen X, Liu K, Yang K, Chen X, Zhao Y, et al. Comparison of survival outcomes between transthoracic and transabdominal surgical approaches in patients with Siewert-II/III esophagogastric junction adenocarcinoma: a single-institution retrospective cohort study. Chin J Cancer Res. 2016;28(4):413–22.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Oh SE, Lee GH, An JY, Lee JH, Sohn TS, Bae JM, et al. Comparison of transabdominal and transthoracic surgical approaches in the treatment of Siewert type II esophagogastric junction cancers: a propensity score-matching analysis. Eur J Surg Oncol. 2022;48(2):370–6.

    Article  PubMed  Google Scholar 

  11. Yang ZF, Wu DQ, Wang JJ, Feng XY, Zheng JB, Hu WX, et al. Surgical approach for Siewert type II adenocarcinoma of the esophagogastric junction: transthoracic or transabdominal? -a single-center retrospective study. Ann Transl Med. 2018;6(23):450.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Blank S, Schmidt T, Heger P, Strowitzki MJ, Sisic L, Heger U, et al. Surgical strategies in true adenocarcinoma of the esophagogastric junction (AEG II): thoracoabdominal or abdominal approach? Gastric Cancer. 2018;21(2):303–14.

    Article  PubMed  Google Scholar 

  13. Tosolini C, Reim D, Schirren R, Feith M, Friess H, Novotny AR. Influence of the surgical technique on survival in the treatment of carcinomas of the true cardia (Siewert type II) - right thoracoabdominal vs. transhiatal-abdominal approach. Eur J Surg Oncol. 2019;45(3):416–24.

    Article  PubMed  CAS  Google Scholar 

  14. Reddavid R, Strignano P, Sofia S, Evangelista A, Deiro G, Cannata G, et al. Transhiatal distal esophagectomy for Siewert type II cardia cancer can be a treatment option in selected patients. Eur J Surg Oncol. 2019;45(10):1943–9.

    Article  PubMed  Google Scholar 

  15. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien-Dindo classification of Surgical Complications: five-year experience. Ann Surg. 2009;250(2):187–96.

    Article  PubMed  Google Scholar 

  16. Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17(1):1–12.

    Article  PubMed  CAS  Google Scholar 

  17. Wells GA, Shea BJ, O’Connell D, Peterson J, Welch V, Losos M et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of non-randomised studies in meta-analyses. Available at http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm. Accessed 2012.

  18. Guyatt GH, Oxman AD, Schünemann HJ, Tugwell P, Knottnerus A. GRADE guidelines: a new series of articles in the Journal of Clinical Epidemiology. J Clin Epidemiol. 2011;64(4):380–2.

    Article  PubMed  Google Scholar 

  19. Zhou J, Wang H, Niu Z, Chen D, Wang D, Lv L, et al. Comparisons of clinical outcomes and prognoses in patients with Gastroesophageal Junction Adenocarcinoma, by Transthoracic and Transabdominal Hiatal approaches: a Teaching Hospital Retrospective Cohort Study. Med (Baltim). 2015;94(50):e2277.

    Article  Google Scholar 

  20. Kurokawa Y, Sasako M, Sano T, Yoshikawa T, Iwasaki Y, Nashimoto A, et al. Ten-year follow-up results of a randomized clinical trial comparing left thoracoabdominal and abdominal transhiatal approaches to total gastrectomy for adenocarcinoma of the oesophagogastric junction or gastric cardia. Br J Surg. 2015;102(4):341–8.

    Article  PubMed  CAS  Google Scholar 

  21. Reeh M, Mina S, Bockhorn M, Kutup A, Nentwich MF, Marx A, et al. Staging and outcome depending on surgical treatment in adenocarcinomas of the oesophagogastric junction. Br J Surg. 2012;99(10):1406–14.

    Article  PubMed  CAS  Google Scholar 

  22. Ovrebo KK, Lie SA, Laerum OD, Svanes K, Viste A. Long-term survival from adenocarcinoma of the esophagus after transthoracic and transhiatal esophagectomy. World J Surg Oncol. 2012;10:130.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Zheng B, Chen YB, Hu Y, Wang JY, Zhou ZW, Fu JH. Comparison of transthoracic and transabdominal surgical approaches for the treatment of adenocarcinoma of the cardia. Chin J Cancer. 2010;29(8):747–51.

    Article  PubMed  Google Scholar 

  24. Omloo JM, Lagarde SM, Hulscher JB, Reitsma JB, Fockens P, van Dekken H, et al. Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the mid/distal esophagus: five-year survival of a randomized clinical trial. Ann Surg. 2007;246(6):992–1001.

    Article  PubMed  Google Scholar 

  25. Wayman J, Dresner SM, Raimes SA, Griffin SM. Transhiatal approach to total gastrectomy for adenocarcinoma of the gastric cardia. Br J Surg. 1999;86(4):536–40.

    Article  PubMed  CAS  Google Scholar 

  26. Graham AJ, Finley RJ, Clifton JC, Evans KG, Fradet G. Surgical management of adenocarcinoma of the cardia. Am J Surg. 1998;175(5):418–21.

    Article  PubMed  CAS  Google Scholar 

  27. Cao F, Hu C, Xu ZY, Zhang YQ, Huang L, Chen JH, et al. Current treatments and outlook in adenocarcinoma of the esophagogastric junction: a narrative review. Ann Transl Med. 2022;10(6):377.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Miyawaki Y, Sato H, Fujiwara N, Aoyama J, Oya S, Sugita H, et al. Verification of oncological local control for hand-assisted laparoscopic abdominal lymph node dissection in Esophageal cancer Surgery: a propensity score-matched analysis. Esophagus. 2021;18(2):187–94.

    Article  PubMed  Google Scholar 

  29. Murakami K, Yoshida M, Uesato M, Toyozumi T, Isozaki T, Urahama R, et al. Does thoracoscopic esophagectomy really reduce post-operative Pneumonia in all cases? Esophagus. 2021;18(4):724–33.

    Article  PubMed  Google Scholar 

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Funding

This study was supported by National Natural Science Foundation of China (NSFC), number of grants (81560349). Role of the Funding: The funding had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

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Author notes

  1. Hongyang Zheng and Xingmei Yin contributed to the work equally and should be regarded as co-first authors.

Authors and Affiliations

  1. Department of Thoracic Surgery, Third Affiliated Hospital of Naval Medical University, Shanghai, 201805, China

    Hongyang Zheng, Tiewen Pan, Xiandong Tao & Xiaolin Xu

  2. Department of Blood Transfusion, Third Affiliated Hospital of Naval Medical University, Shanghai, 201805, China

    Xingmei Yin

  3. Department of Digestive Surgery, Shanghai Songjiang District Central Hospital, No. 746 Zhongshan Middle Road, Songjiang District Shanghai, Shanghai, 201600, China

    Zhenjia Li

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  1. Hongyang Zheng
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Contributions

Authors’ contributions: Zhenjia Li had full access to all of the data in the manuscript and takes responsibility for the integrity of the data and the accuracy of the data analysis. All authors read and approved the final manuscript.Concept and design: All authors. Acquisition, analysis, or interpretation of data: All authors. Drafting of the manuscript: Hongyang Zheng and Zhenjia Li. Statistical analysis: Hongyang Zheng, Xingmei Yin, Zhenjia Li, Tiewen Pan, Xiandong Tao and Xiaolin Xu.Critical revision of the manuscript for important intellectual content: Hongyang Zheng, Xingmei Yin and Zhenjia Li.Supervision: Hongyang Zheng, Xingmei Yin and Zhenjia Li.

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Correspondence to Zhenjia Li.

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Supplementary Information

Additional file 1: Figure S1

Forest plots of recurrences associated with transthoracic surgery and transabdominal surgery. Figure S2 Forest plots of complications associated with transthoracic surgery and transabdominal surgery. Figure S3Sensitivity analysis ofintraoperative blood loss(A), operating time(B), number of lymph node retrieved(C), number of positive lymph node retrieved (D) and hospital stay(E). Figure S4 Funnel plots of survival (overallsurvivalanddisease-free survival, A), overallsurvivalrate (1, 2, 3, 5 years, B) and disease-free survival rate (1, 2, 3, 5 years, C). Table S1PRISMA 2009 Checklist. Table S2 Search strategy. Table S3 Methodological quality assessments of the included studies.

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Zheng, H., Yin, X., Pan, T. et al. Effect of different surgical approaches on the survival and safety of Siewert type II esophagogastric junction adenocarcinoma: a systematic review and meta-analysis. BMC Cancer 23, 1130 (2023). https://doi.org/10.1186/s12885-023-11640-5

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BMC Cancer

ISSN: 1471-2407

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