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Laparoscopic versus open surgery for rectal neuroendocrine tumors: a multicenter real-world study

BMC Cancer volume 24, Article number: 956 (2024) Cite this article

Abstract

Background

Owing to the lack of evidence-based medical studies with large sample sizes, the surgical approach for the radical resection of rectal neuroendocrine tumors remains controversial.

Methods

We retrospectively collected the medical records of patients with rectal neuroendocrine tumors who underwent radical resection at 17 large tertiary care hospitals in China between January 1, 2010, and April 30, 2022. All patients were divided into laparoscopic and open surgery groups. After propensity score matching to reduce confounders, the postoperative and oncologic outcomes were compared between the groups.

Results

We enrolled 174 patients with rectal neuroendocrine tumors who underwent radical surgery. After random matching, 124 patients were included in the comparison (62, laparoscopic surgery group; 62, open surgery group). The laparoscopic surgery group had fewer complications (14.5% vs. 35.5%, P = 0.007) and superior relapse-free survival (P = 0.048). Subgroup analysis revealed that the laparoscopic surgery group had fewer complications (10.9% vs. 34.7%, P = 0.004), shorter postoperative hospital stays (9.56 ± 5.21 days vs. 12.31 ± 8.61 days, P = 0.049) and superior relapse-free survival (P = 0.025) in the rectal neuroendocrine tumors ≤ 4 cm subgroup.

Conclusions

Laparoscopic surgery was associated with improved postoperative outcomes and oncologic prognosis for patients with rectal neuroendocrine tumors ≤ 4 cm; it can serve as a safe and feasible option for radical surgery of rectal neuroendocrine tumors.

Peer Review reports

Background

Neuroendocrine neoplasms (NENs) are rare neoplasms that arise from embryonic neuroendocrine cells and are characterized by the presence of neuroendocrine markers. These neoplasms can occur in various organs throughout the body, with the rectum being a common site of incidence (1.04 per 100,000 people) [1, 2]. Based on the Ki-67 index and mitotic count, rectal NENs (RNENs) can be stratified into rectal neuroendocrine tumors (RNETs), rectal neuroendocrine carcinoma (RNEC), and rectal mixed neuroendocrine and non-neuroendocrine neoplasms (RMiNENs), which exhibit substantial heterogeneity. Tumor grade is a major predictor of metastasis and prognosis in RNENs [3, 4].

Currently, the National Comprehensive Cancer Network (NCCN), European Neuroendocrine Tumor Society (ENETS), and Chinese Society of Clinical Oncology (CSCO) guidelines recommend radical resection for RNETs with risk factors (e.g., tumor size > 2 cm, T stage > T1, and lymph node metastasis), RNEC, and RMiNEN [5,6,7]. Laparoscopic techniques have been widely used in the treatment of RNETs [8, 9]. However, the outcomes of laparoscopic surgery for RNETs have been scarcely described owing to their rarity and the even rarer indications for radical surgery. Additionally, laparoscopic surgery lacks tactile sensation and poses the risk of tumor rupture and iatrogenic dissemination. However, comparisons with open surgery are lacking; thus, the surgical options for RNETs remain to be determined.

In this study, we collected diagnostic and treatment data from 17 large tertiary care hospitals in China over a 13-year period to evaluate the efficacy of laparoscopic and open surgery through a subgroup analysis of tumor size.

Materials and methods

Patients and data collection

This study retrospectively reviewed the data of patients diagnosed with RNETs at 17 large-scale medical centers in China between January 1, 2010, and April 30, 2022. Demographic, clinicopathological, treatment, and outcome data were extracted from the electronic medical records of each hospital by surveyors with expertise in NENs using standardized data collection templates. The inclusion criteria were as follows: (1) confirmation of neuroendocrine tumors by pathology; (2) primary rectal neuroendocrine tumors; (3) surgical treatment. The exclusion criteria were as follows: (1) comorbidities with other malignancies; (2) incomplete clinical data or follow-up information; (3) distant metastasis; (4) local resection. In total, 174 of 1,459 patients were enrolled in the study. The procedure used to identify eligible study participants is shown in Fig. 1.

Fig. 1
figure 1

Patient selection flowchart

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Criteria

Tumor size was determined based on the longest tumor diameter, as recorded in the pathological reports. Tumor site was divided into low (≤ 7 cm), median (7–12 cm), and high RNETs (12–15 cm), according to the distance from the lower edge of the tumor to the anal verge. Tumor stage was classified according to the American Joint Committee on Cancer (AJCC) cancer staging manual, whereas tumor grade was classified based on the WHO 2019 classification. The mitotic count was expressed as the number of mitotic cells in ten high-power fields from hematoxylin and eosin-stained slides examined under a microscope. The Ki-67 index was calculated as the percentage of cells labeled using immunohistochemistry. Complications within 30 days after surgery were recorded and graded according to the Clavien-Dindo classification. Patients with tumor size > 2 cm, T stage > T1, tumor grade G3, lymph node metastasis, or neurovascular invasion were recommended to undergo radical resection. Patients with T stage ≥ T2, lymph node metastasis, neurovascular invasion, or tumor size > 2 cm were considered to have a high risk for recurrence; a multidisciplinary team was involved in formulating adjuvant therapy plans for these patients. Somatostatin analog therapy was recommended for somatostatin receptor-positive patients.

Follow-up

Relapse-free survival (RFS) was calculated from the date of intervention to that of recurrence. Follow-up was conducted via telephone and out- or inpatient means. Patients who underwent complete resection were followed up every 6 months for the first 5 years and annually thereafter. The final follow-up was conducted in July 2022. Follow-up examinations included routine blood tests, chromogranin A tests, chest computed tomography (CT), and whole-abdominal and pelvic contrast-enhanced CT or magnetic resonance imaging (MRI). Positron-emission tomography (PET)-CT was performed if recurrence or metastasis was suspected. Loss to follow-up was defined as failure to contact patients or their family members.

Statistical analysis

Normally distributed quantitative data were presented as means ± standard deviations and were compared using the independent-sample t test; non-normally distributed quantitative data were presented as medians with interquartile ranges and were compared using the Mann‒Whitney U test. Categorical data were expressed as numbers and percentages, and were analyzed using either the chi-square test or Fisher’s exact test. RFS was analyzed using the Kaplan-Meier method, wherein variables were compared using the log-rank test in univariate analysis and Cox proportional hazard regression in multivariable analysis. Propensity score matching was employed to minimize the influence of confounding factors; propensity score matching (PSM) was employed [10]. The propensity score was calculated according to the preoperative data available regarding sex, age, tumor size, tumor site, and neoadjuvant therapy. The nearest neighbor matching algorithm was used to match patients based on the logic of the propensity score. A standard deviation < 10% was considered acceptable for assessing the matching covariate balance [11]; the distribution of propensity scores in both matched and unmatched groups was assessed using dot plots (Supplemental Fig. 1).

Statistical analyses were performed using R software (version 4.0.0). The optimal cut-off value for continuous variables was determined using the X-tile software. Variables with P < 0.10 in the univariate analysis were included in the multivariate analysis. P < 0.05 was considered statistically significant.

Results

Demographic data and clinicopathological characteristics

This study included 174 patients who underwent radical surgery for localized RNETs. Among them, 112 (64.4%) were males and 62 (35.6%) were females. The median patient age was 56 years (range: 26–83 years). The median tumor size was 2.0 cm, ranging from 0.1 to 7.5 cm. The tumor grade was categorized as G1 in 95 (54.6%) patients, G2 in 52 (29.9%), and G3 in 27 (15.5%). According to the TNM staging, 52 (29.9%) patients were classified as T1, 50 (28.7%) as T2, 56 (32.2%) as T3, and 16 (9.2%) as T4. Lymph node metastasis was clinically positive in 88 (50.6%) patients based on histopathology results. Sixty (34.5%) patients received adjuvant therapy. The demographic and clinicopathological characteristics of the patients are summarized in Table 1.

Table 1 Comparison of demographic and clinicopathological characteristics before and after propensity score matching
Full size table

Before PSM, 112 (64.4%) patients underwent laparoscopic surgery, while 62 (35.6%) underwent open surgery. No significant differences were observed between the groups in terms of sex (P = 0.976), age (P = 0.976), tumor site (P = 0.144), neoadjuvant therapy (P = 0.139), or adjuvant therapy (P = 0.383); however, the tumor size in the laparoscopic surgery (LAP) group was significantly lower than that in the open surgery (OPEN) group (P = 0.041). No significant differences were observed after matching. The clinicopathological characteristics of the two groups before and after matching are shown in Table 1.

Surgical outcomes

The operation time and postoperative hospital stay were comparable between the LAP and OPEN groups (Before PSM: 176.63 ± 56.56 min vs. 172.08 ± 86.52 min, P = 0.676; 10.41 ± 5.56 days vs. 12.32 ± 7.78 days, P = 0.062. After PSM: 174.45 ± 60.82 min vs. 172.08 ± 86.52 min, P = 0.860; 10.11 ± 5.55 days vs. 12.32 ± 7.78 days, P = 0.071). Moreover, the proportion of patients in the LAP group who underwent stoma creation and total mesorectal excision (TME) was similar to that in the OPEN group (Before PSM: 44.6% vs. 40.3%, P = 0.582; 64.3% vs. 74.2%, P = 0.180; After PSM: 38.7% vs. 40.3%, P = 0.854; 69.4% vs. 74.2%, P = 0.549). Before PSM, the R0 resection rate was higher in the LAP group than in the OPEN group (99.1% vs. 95.2%; P = 0.049). Moreover, the LAP group had a lower incidence of postoperative complications as compared to the OPEN group (13.4% vs. 35.5%, P = 0.001). After PSM, there was no significant difference in the R0 resection rate between the two groups (98.4% vs. 95.2%, P = 0.133). However, the LAP group had a significantly lower postoperative complication rate than the OPEN group (14.5% vs. 35.5%, P = 0.007). The surgical outcomes of the two groups before and after matching are shown in Table 1.

Oncologic outcomes

The study had a median follow-up period of 34 months (range: 1-123). The 1-, 3-, and 5-year RFS for RNETs patients who underwent radical surgery were 90.3%, 78.1%, and 76.0%, respectively (Fig. 2). The optimal cutoff value for tumor size to predict RFS was determined to be 4.0 cm for the two subgroups, and 2.0 and 4.0 cm for the three subgroups. Multivariate analysis revealed that tumor grade (G2: hazard ratio [HR], 3.263; 95% CI: 1.369–7.652, P = 0.012; G3: HR, 4.036. 95% CI: 1.102–9.632, P = 0.009), lymph node metastasis (Positive: HR, 2.896; 95% CI: 1.135–6.320, P = 0.030), and surgery type (OPEN: HR, 2.362; 95% CI: 1.069–5.324, P = 0.040) were independent risk factors for RFS. The log-rank test and Cox proportional hazards regression analysis of RFS are shown in Table 2.

Fig. 2
figure 2

Relapse-free survival curve of the entire cohort of 174 rectal neuroendocrine tumors patients

Full size image
Table 2 Univariate and multivariate relapse-free survival analysis
Full size table

Before PSM, the 1-, 3-, and 5-year RFS were 93.6%, 83.2%, and 81.4% in the LAP group, and 84.3%, 69.8%, and 67.4% in the OPEN group, respectively. The difference was statistically significant (P = 0.045). After PSM, the 1-, 3-, and 5-year RFS were 95.2%, 85.3%, and 85.3% in the LAP group, and 84.3%, 69.8%, and 67.4% in the OPEN group, respectively. The difference was also statistically significant (P = 0.048). Survival curves according to surgical type before and after PSM are shown in Fig. 3A and B.

Fig. 3
figure 3

Comparison of relapse-free survival between the laparoscopic surgery group and open surgery group: (A) Before propensity score matching; (B) After propensity score matching; (C) ≤ 4 cm subgroup after propensity score matching; (D) > 4 cm subgroup after propensity score matching

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Subgroup analysis

Tumor size was strongly correlated with surgical resection difficulty; thus, we performed a subgroup analysis based on this factor. In the aforementioned prognostic analysis, we found that the optimal cut-off value of the tumor size for predicting RFS was 4.0 cm. In the RNETs ≤ 4 cm subgroup, there were 49 patients in the LAP group and 55 in the OPEN group; in the RNETs > 4 cm subgroup, there were 13 patients in the LAP group and seven in the OPEN group. No significant differences were observed in their baseline characteristics.

There were no significant differences in the R0 resection rate or operation time in either the RNETs ≤ 4 cm (100.0% vs. 95.9%, P = 0.220; 175.29 ± 63.16 min vs. 170.63 ± 92.01 min, P = 0.762) or the RNETs > 4 cm subgroups (85.7% vs. 92.3%, P = 0.299; 167.86 ± 40.50 min vs. 177.54 ± 64.41 min, P = 0.724). Meanwhile, the proportion of patients in the LAP group who underwent stoma creation and TME was similar to those in the OPEN group, in either the RNETs ≤ 4 cm (38.2% vs. 36.7%, P = 0.879; 67.3% vs. 73.5%, P = 0.490) or the RNETs > 4 cm subgroups (42.9% vs. 53.8%, P = 1.000; 71.4% vs. 84.6%, P = 0.587). The LAP group had a lower incidence of postoperative complications than the OPEN group in the RNETs ≤ 4 cm subgroup (10.9% vs. 34.7%, P = 0.004), while no significant difference was observed in the RNETs > 4 cm subgroup (42.9% vs. 38.5%, P = 1.000). Similarly, the postoperative hospital stay in the LAP group was significantly shorter than that in the OPEN group in the RNETs ≤ 4 cm subgroup (9.56 ± 5.21 days vs. 12.31 ± 8.61 days, P = 0.049), while no significant difference was observed in the RNETs > 4 cm subgroup (14.43 ± 6.60 days vs. 12.38 ± 3.33 days, P = 0.465). The clinicopathological characteristics and surgical outcomes of the subgroups are shown in Table 3.

Table 3 Comparison of demographic and clinicopathological characteristics in subgroup analysis of tumor size after propensity score matching
Full size table

The RFS of the LAP group was superior to that of the OPEN group in the RNETs ≤ 4 cm subgroup (P = 0.025), whereas no significant difference was found in the RNETs > 4 cm subgroup (P = 0.724). Survival curves according to the surgical type are shown in Fig. 3C and D.

Discussion

Radical resection, including low anterior and abdominoperineal resection, is the primary treatment for localized RNETs. However, while radical resection achieves more complete tumor dissection and improves patient survival, it may also result in poor functional outcomes as compared to local excision [12,13,14,15,16]. Therefore, the choice between local excision and radical resection is crucial in managing patients with RNETs.

In this study, the preoperative imaging results served as important references for selecting surgical methods for patients with RNETs. By effectively communicating with the patients and their families, we determined the optimal surgical approach after carefully assessing the tumor size, tumor grade, T stage, and lymph node metastasis status. For RNETs, we recommend radical resection for patients with tumor size > 2 cm, T stage > T1, tumor grade G3, lymph node metastasis, or neurovascular invasion. Radical resection has been suggested in patients with RNEC and RMANEC. These indications for radical resection are similar to those outlined in the CSCO guidelines for RNENs [5].

Laparoscopic surgery has become the standard treatment for digestive tract tumors. Several retrospective case-control studies and randomized controlled trials have demonstrated that laparoscopic surgery has a long-term prognosis not inferior to that of open surgery, as well as having the advantages of less trauma and rapid postoperative recovery [17,18,19,20]. However, evidence comparing laparoscopic and open surgery for RNETs remains scarce, owing to their rarity and even rarer indications for radical surgery. Therefore, we designed and implemented a multicenter study to compare the postoperative and oncological outcomes between laparoscopic and open surgery for RNETs. To the best of our knowledge, this is the largest study of RNETs in patients who underwent radical resection.

RNETs are located in the pelvic cavity, with complex adjacent organs and a narrow surgical space, thus making precise localization and safe resection difficult. Laparoscopic surgery can effectively reduce traction injury to the surrounding organs by directly reaching the lesion site with extended surgical instruments. Image reproduction is achieved through the endoscope and monitor, which makes it possible for surgeons to observe the surgical field more intuitively, thus assisting in safe tumor resection. Studies have shown that laparoscopic surgery for NENs in the stomach and small bowel yields short-term outcomes comparable to those of open surgery [21, 22]. In this study, we found that laparoscopic surgery for RNETs resulted in a lower incidence of complications and a higher rate of R0 resection than open surgery. To improve the credibility of our retrospective data analysis, we performed PSM between the groups to balance the covariates and confounders. After PSM, we found a lower incidence of postoperative complications in the LAP group, with no significant differences in the R0 resection rate, operation time, or postoperative hospital stay. These results demonstrate that laparoscopic surgery may offer better surgical outcomes for RNETs owing to its minimally invasive nature.

Although laparoscopic surgery lacks tactile sensation, which poses a risk for tumor rupture and iatrogenic dissemination, studies have shown satisfactory long-term prognosis in laparoscopic resection of RNETs, with a 3-year overall survival rate of 97.8% [8, 9]. However, comparisons between laparoscopic and open surgeries, in terms of oncological outcomes for RNETs, remain lacking. In our study, we used PSM to minimize the influence of confounding factors. The results suggested that laparoscopic surgery was associated with a better RFS than open surgery before and after PSM. In conclusion, laparoscopic surgery is a safe and feasible option for radical surgery in patients with RNETs.

Tumor size is associated with difficulty in surgical resection during the treatment of digestive tract tumors; a larger tumor size often indicates a more complicated surgical procedure, thus increasing the risk for intraoperative complications. To assess the impact of tumor size on short- and long-term outcomes, we performed a subgroup analysis of patients with RNETs after PSM using a cutoff value of 4 cm. Among patients with RNETs ≤ 4 cm, those in the laparoscopic group had fewer complications, shorter postoperative hospital stays, and superior RFS as compared with those in the open group. Among patients with RNETs > 4 cm, the short- and long-term outcomes did not significantly differ between the laparoscopic and open groups. Similarly, previous studies at our medical center have shown that in rectal gastrointestinal stromal tumors, laparoscopic surgery was associated with superior RFS and fewer complications only in patients with ≤ 5-cm tumors, whereas these advantages were lost in those with > 5 cm [23]. These results suggest that laparoscopic surgery has advantages related to tumor size in the management of rectal neoplasms.

This study had several limitations. First, although we used PSM to reduce potential bias and performed a subgroup analysis to investigate the impact of the surgical approach on patient outcomes, the retrospective nature of the study affected its statistical power and clinical value. In addition, RNETs are slow-growing tumors [24]; a longer follow-up period is required for a comprehensive clinical evaluation of patient status. Furthermore, the number of cases in the RNETs > 4 cm subgroup was too low to draw definitive conclusions. However, to the best of our knowledge, this is currently the largest study to compare laparoscopic with open surgery for RNETs, and thus may provide valuable guidance for their treatment. We look forward to a subsequent large prospective multicenter study to provide more reliable medical evidence for choosing a radical surgical approach for RNETs.

Conclusion

In summary, laparoscopic surgery is a safe and feasible option for radical resection of localized RNETs. For patients with RNETs ≤ 4 cm, laparoscopic surgery was associated with a superior RFS, a reduced rate of complications, and shorter postoperative hospital stays. For patients with RNETs > 4 cm, laparoscopic surgery has oncological and surgical outcomes similar to those of open surgery.

Data availability

The datasets used and analyzed during the current study are available from the corresponding author upon reasonable request.

Abbreviations

AJCC:

American Joint Committee on Cancer

CSCO:

Chinese Society of Clinical Oncology

CT:

Computed tomography

ENETS:

European Neuroendocrine Tumor Society

MRI:

Magnetic resonance imaging

NCCN:

National Comprehensive Cancer Network

NENs:

Neuroendocrine neoplasms

PET:

Positron-emission tomography

PSM:

Propensity score matching

RFS:

Relapse-free survival

RMANEC:

Rectal mixed adenoneuroendocrine carcinoma

RNEC:

Rectal neuroendocrine carcinoma

RNENs:

Rectal neuroendocrine neoplasms

RNETs:

Rectal neuroendocrine tumors

TME:

Total mesorectal excision

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Acknowledgements

Not applicable.

Funding

This study was funded by the National Natural Science Foundation of China (Grant Nos. 81702386 and 81874184) and the Key Project of the Hubei Health Commission (Grant No. WJ2019Q030).

Author information

Authors and Affiliations

  1. Department of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, no. 1277 Jiefang Avenue, Wuhan, 430022, Hubei Province, China

    Xinyu Zeng, Chengguo Li & Kaixiong Tao

  2. Department of Gastrointestinal Surgery, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China

    Minhao Yu

  3. Department of Colorectal Cancer, Liaoning Cancer Hospital & Institute, Shenyang, China

    Rui Zhang

  4. Department of General Surgery, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Beijing, China

    Guole Lin

  5. Department of Gastrointestinal Surgery, Taihe Hospital, Hubei University of Medicine, Shiyan, China

    Maojun Di

  6. Department of Gastrointestinal Surgery I Section, Renmin Hospital of Wuhan University, Wuhan, China

    Hongxue Wu

  7. Department of Colorectal Surgery, Jiangsu Province Hospital, Nanjing Medical University, Nanjing, China

    Yueming Sun

  8. Department of Gastrointestinal Surgery, Tongji Medical College, Hubei Cancer Hospital, Huazhong University of Science and Technology, Wuhan, China

    Zhiguo Xiong

  9. Department of Colorectal and Anal Surgery, Zhongnan Hospital of Wuhan University, Wuhan, China

    Congqing Jiang

  10. Department of General Surgery, Hebei Medical University Fourth Affiliated Hospital, Hebei Provincial Tumor Hospital, Shijiazhuang, China

    Bin Yu

  11. Department of Gastrointestinal Surgery, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, Guangzhou, China

    Shengning Zhou

  12. Department of Gastrointestinal Surgery, Department of General Surgery, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, China

    Yong Li

  13. Department of General Surgery, Xiangyang Central Hospital, Affiliated Hospital of Hubei University of Arts and Science, Xiangyang, China

    Xiaofeng Liao

  14. Department of Colorectal and Anal Surgery, The First Affiliated Hospital of Shandong First Medical University, Jinan, China

    Lijian Xia

  15. Department of Colorectal Surgery, Shanghai Changhai Hospital, Naval Medical University, Shanghai, China

    Wei Zhang

  16. Department of Colorectal Surgery, Fujian Medical University Union Hospital, Fuzhou, 350001, Fujian Province, China

    Weizhong Jiang

Authors
  1. Xinyu Zeng
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  2. Chengguo Li
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  3. Minhao Yu
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  4. Rui Zhang
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  5. Guole Lin
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  6. Maojun Di
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  7. Hongxue Wu
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  8. Yueming Sun
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  9. Zhiguo Xiong
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  10. Congqing Jiang
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  11. Bin Yu
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  12. Shengning Zhou
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  13. Yong Li
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  14. Xiaofeng Liao
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  15. Lijian Xia
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  16. Wei Zhang
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  17. Weizhong Jiang
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  18. Kaixiong Tao
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Contributions

Weizhong Jiang and Kaixiong Tao had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.Concept and design: Chengguo Li, Weizhong Jiang, Kaixiong Tao.Acquisition, analysis, or interpretation of data: Xinyu Zeng, Chengguo Li, Minhao Yu, Rui Zhang, Guole Lin, Maojun Di, Hongxue Wu, Yueming Sun, Zhiguo Xiong, Congqing Jiang, Bin Yu, Shengning Zhou, Yong Li, Xiaofeng Liao, Lijian Xia, Wei Zhang.Drafting of the manuscript: Xinyu Zeng, Chengguo Li.Critical revision of the manuscript for important intellectual content: Minhao Yu, Rui Zhang, Guole Lin, Maojun Di, Hongxue Wu, Yueming Sun, Zhiguo Xiong, Congqing Jiang, Bin Yu, Shengning Zhou, Yong Li, Xiaofeng Liao, Lijian Xia, Wei Zhang, Weizhong Jiang, Kaixiong Tao.Statistical analysis: Minhao Yu, Rui Zhang, Guole Lin, Maojun Di, Hongxue Wu, Yueming Sun.Administrative, technical, or material support: Zhiguo Xiong, Congqing Jiang, Bin Yu, Shengning Zhou, Yong Li, Xiaofeng Liao, Lijian Xia, Wei Zhang, Weizhong Jiang, Kaixiong Tao.Supervision: Weizhong Jiang, Kaixiong Tao.

Corresponding authors

Correspondence to Weizhong Jiang or Kaixiong Tao.

Ethics declarations

Ethics approval and consent to participate

This study conformed to the Declaration of Helsinki. This study was approved by the Medical Ethics Committee of the Union Hospital, Tongji Medical College, Huazhong University of Science and Technology (Approval Number: [2022]0433). At the last follow-up, we informed the patients about the study in detail and obtained signed informed consent. For patients who died at the time of the study, we contacted their immediate family members, explained the study in detail, and obtained signed informed consent forms.

Consent for publication

Not Applicable.

Competing interests

The authors declare no competing interests.

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Zeng, X., Li, C., Yu, M. et al. Laparoscopic versus open surgery for rectal neuroendocrine tumors: a multicenter real-world study. BMC Cancer 24, 956 (2024). https://doi.org/10.1186/s12885-024-12711-x

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  • DOI: https://doi.org/10.1186/s12885-024-12711-x

Keywords

BMC Cancer

ISSN: 1471-2407

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