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Endoscopic and surgical treatment of T1N0M0 colorectal neuroendocrine tumors: a population-based comparative study

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Abstract

Background

With the rapid advances in endoscopic technology, endoscopic therapy (ET) is increasingly applied to the treatment of small (≤ 20 mm) colorectal neuroendocrine tumors (NETs). However, long-term data comparing ET and surgery for management of T1N0M0 colorectal NETs are lacking. The purpose of this work was to compare overall survival (OS) and cancer-specific survival (CSS) of such patients with ET or surgery.

Methods

Patients with T1N0M0 colorectal NETs were identified within the Surveillance Epidemiology and End Results (SEER) database (2004–2016). Demographics, tumor characteristics, therapeutic methods, and survival were compared. Propensity score matching (PSM) was used 1:3 and among this cohort, Cox proportional hazards regression models were performed to evaluate correlation between treatment and outcomes.

Results

Of 4487 patients with T1N0M0 colorectal NETs, 1125 were identified in the matched cohort, among whom 819 (72.8%) underwent ET and 306 (27.2%) underwent surgery. There was no difference in the 5-year and 10-year OS and CSS rates between the 2 treatment modalities. Likewise, analyses stratified by tumor size and site showed that patients did not benefit more from surgery compared with ET. Moreover, multivariate analyses found no significant differences in OS [Hazard Ratio (HR) = 0.857, 95% Confidence Interval (CI): 0.513–1.431, P = 0.555] and CSS (HR = 0.925, 95% CI: 0.282–3.040, P = 0.898) between the 2 groups. Similar results were observed when comparisons were limited to patients with different tumor size and site.

Conclusions

In this population-based study, patients with lesions < 10 mm treated endoscopically had comparable long-term survival compared with those treated surgically, which demonstrates ET as an alternative to surgery in T1N0M0 colorectal NETs of < 10 mm. Further high-quality prospective studies are warranted to comprehensively evaluate the role of ET in patients with tumors 10 to 20 mm.

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Data availability

The data were abstracted from the Surveillance, Epidemiology, and End Results (SEER) database. This is an open database. (https://seer.cancer.gov).

Abbreviations

ET:

Endoscopic therapy

NETs:

Neuroendocrine tumors

OS:

Overall survival

CSS:

Cancer-specific survival

SEER database:

Surveillance Epidemiology and End Results database

PSM:

Propensity score matching

HR:

Hazard Ratio

95% CI:

95% Confidence Interval

NCCN:

National Comprehensive Cancer Network

NCI:

National Cancer Institute, AJCC: American Joint Committee on Cancer

References

  1. Cives M, Strosberg JR (2018) Gastroenteropancreatic neuroendocrine tumors. CA Cancer J Clin 68:471–487

    Article  Google Scholar 

  2. Ford MM (2017) Neuroendocrine tumors of the colon and rectum. Dis Colon Rectum 60:1018–1020

    Article  Google Scholar 

  3. Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, Abdalla EK, Fleming JB, Vauthey JN, Rashid A, Evans DB (2008) One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol 26:3063–3072

    Article  Google Scholar 

  4. Leoncini E, Boffetta P, Shafir M, Aleksovska K, Boccia S, Rindi G (2017) Increased incidence trend of low-grade and high-grade neuroendocrine neoplasms. Endocrine 58:368–379

    Article  CAS  Google Scholar 

  5. Shafqat H, Ali S, Salhab M, Olszewski AJ (2015) Survival of patients with neuroendocrine carcinoma of the colon and rectum: a population-based analysis. Dis Colon Rectum 58:294–303

    Article  Google Scholar 

  6. Modlin IM, Oberg K, Chung DC, Jensen RT, de Herder WW, Thakker RV, Caplin M, Delle Fave G, Kaltsas GA, Krenning EP, Moss SF, Nilsson O, Rindi G, Salazar R, Ruszniewski P, Sundin A (2008) Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol 9:61–72

    Article  CAS  Google Scholar 

  7. Dasari A, Shen C, Halperin D, Zhao B, Zhou S, Xu Y, Shih T, Yao JC (2017) Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the united states. JAMA Oncol 3:1335–1342

    Article  Google Scholar 

  8. Landry CS, Brock G, Scoggins CR, McMasters KM, Martin RC 2nd (2008) A proposed staging system for rectal carcinoid tumors based on an analysis of 4701 patients. Surgery 144:460–466

    Article  Google Scholar 

  9. Landry CS, Brock G, Scoggins CR, McMasters KM, Martin RC 2nd (2008) Proposed staging system for colon carcinoid tumors based on an analysis of 2,459 patients. J Am Coll Surg 207:874–881

    Article  Google Scholar 

  10. Chen T, Yao LQ, Xu MD, Zhang YQ, Chen WF, Shi Q, Cai SL, Chen YY, Xie YH, Ji Y, Chen SY, Zhou PH, Zhong YS (2016) Efficacy and safety of endoscopic submucosal dissection for coloresctal carcinoids. Clin Gastroenterol Hepatol 14:575–581

    Article  Google Scholar 

  11. Son HJ, Sohn DK, Hong CW, Han KS, Kim BC, Park JW, Choi HS, Chang HJ, Oh JH (2013) Factors associated with complete local excision of small rectal carcinoid tumor. Int J Colorectal Dis 28:57–61

    Article  Google Scholar 

  12. Kim J, Kim JH, Lee JY, Chun J, Im JP, Kim JS (2018) Clinical outcomes of endoscopic mucosal resection for rectal neuroendocrine tumor. BMC Gastroenterol 18:77

    Article  Google Scholar 

  13. Modlin IM, Kidd M, Latich I, Zikusoka MN, Shapiro MD (2005) Current status of gastrointestinal carcinoids. Gastroenterology 128:1717–1751

    Article  Google Scholar 

  14. Kloppel G, Anlauf M (2005) Epidemiology, tumour biology and histopathological classification of neuroendocrine tumours of the gastrointestinal tract. Best Pract Res Clin Gastroenterol 19:507–517

    Article  Google Scholar 

  15. National Comprehensive Cancer Network. (NCCN) Clinical Practice Guidelines in Oncology. Neuroendocrine and Adrenal Tumors, Version 1. 2019. http://www.nccn.org/professionals/physician_gls/f_guidelines.asp. Accessed March 5, 2019

  16. Scherubl H (2009) Rectal carcinoids are on the rise: early detection by screening endoscopy. Endoscopy 41:162–165

    Article  CAS  Google Scholar 

  17. Konishi T, Watanabe T, Kishimoto J, Kotake K, Muto T, Nagawa H, Japanese Society for Cancer of the C, Rectum (2007) Prognosis and risk factors of metastasis in colorectal carcinoids: results of a nationwide registry over 15 years. Gut 56:863–868

    Article  Google Scholar 

  18. Gleeson FC, Levy MJ, Dozois EJ, Larson DW, Wong Kee Song LM, Boardman LA (2014) Endoscopically identified well-differentiated rectal carcinoid tumors: impact of tumor size on the natural history and outcomes. Gastrointest Endosc 80:144–151

    Article  Google Scholar 

  19. Chen H, Chen Y (2017) Consensus and controversy of endoscopic diagnosis and treatment of gastroenteropancreatic neuroendocrine tumors. Zhonghua Wei Chang Wai Ke Za Zhi 20:982–986

    PubMed  Google Scholar 

  20. Al Natour RH, Saund MS, Sanchez VM, Whang EE, Sharma AM, Huang Q, Boosalis VA, Gold JS (2012) Tumor size and depth predict rate of lymph node metastasis in colon carcinoids and can be used to select patients for endoscopic resection. J Gastrointest Surg 16:595–602

    Article  Google Scholar 

  21. Ngamruengphong S, Kamal A, Akshintala V, Hajiyeva G, Hanada Y, Chen YI, Sanaei O, Fluxa D, Haito Chavez Y, Kumbhari V, Singh VK, Lennon AM, Canto MI, Khashab MA (2019) Prevalence of metastasis and survival of 788 patients with T1 rectal carcinoid tumors. Gastrointest Endosc 89:602–606

    Article  Google Scholar 

  22. Surveillance, Epidemiology, and End Results Program Overview. https://seer.cancer.gov/about/factsheets/SEER_Overview.pdf. Accessed 28 Feb 2019

  23. American Joint Committee on Cancer. Cancer staging manual, 8th ed. Available at: https://cancerstaging.org/references-tools/deskreferences/Documents/AJCC%20Cancer%20Staging%20Form%20Supplement.pdf. Accessed Oct 28, 2018

  24. SEER Site-Specific: Surgery of Primary Site Codes (SEER program code manual, 3rd ed: two-digit site-specific surgery codes. 2003)

  25. Modlin IM, Lye KD, Kidd M (2003) A 5-decade analysis of 13,715 carcinoid tumors. Cancer 97:934–959

    Article  Google Scholar 

  26. Fields AC, Saadat LV, Scully RE, Davids JS, Goldberg JE, Bleday R, Melnitchouk N (2019) Local Excision Versus Radical Resection for 1- to 2-cm Neuroendocrine Tumors of the Rectum: A National Cancer Database Analysis. Dis Colon Rectum 62:417–421

    Article  Google Scholar 

  27. de Mestier L, Lorenzo D, Fine C, Cros J, Hentic O, Walter T, Panis Y, Couvelard A, Cadiot G, Ruszniewski P (2019) Endoscopic, transanal, laparoscopic, and transabdominal management of rectal neuroendocrine tumors. Best Pract Res Clin Endocrinol Metab 33:e101293

    Article  Google Scholar 

  28. Leoncini E, Carioli G, La Vecchia C, Boccia S, Rindi G (2016) Risk factors for neuroendocrine neoplasms: a systematic review and meta-analysis. Ann Oncol 27:68–81

    Article  CAS  Google Scholar 

  29. Li J, Wang Y, Han F, Wang Z, Xu L, Tong J (2016) Disadvantage of survival outcomes in widowed patients with colorectal neuroendocrine neoplasm: an analysis of surveillance, epidemiology and end results database. Oncotarget 7:83200–83207

    Article  Google Scholar 

  30. Ni SJ, Sheng WQ, Du X (2010) Pathologic research update of colorectal neuroendocrine tumors. World J Gastroenterol 16:1713–1719

    Article  CAS  Google Scholar 

  31. Maryanski J, Cyran-Chlebicka A, Szczepankiewicz B, Cebulski W, Slodkowski M, Wronski M (2018) Surgical treatment of extra-appendiceal colorectal neuroendocrine tumors. Pol Przegl Chir 90:7–12

    Article  Google Scholar 

  32. Meier B, Albrecht H, Wiedbrauck T, Schmidt A, Caca K (2020) Full-thickness resection of neuroendocrine tumors in the rectum. Endoscopy 52:68–72

    Article  Google Scholar 

  33. Xu M, Wang XY, Zhou PH, Li QL, Zhang Y, Zhong Y, Chen W, Ma L, Ishaq S, Qin W, Hu J, Yao L (2013) Endoscopic full-thickness resection of colonic submucosal tumors originating from the muscularis propria: an evolving therapeutic strategy. Endoscopy 45:770–773

    Article  Google Scholar 

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Acknowledgements

We would like to thank the researchers and study participants for their contributions.

Funding

This research work was supported by the Key Medical Talents of Jiangsu Province (Grant No. ZDRCA2016034) (to LM).

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Authors and Affiliations

Authors

Contributions

HLZ, SZ and KJ designed the study. HLZ and WW performed data mining. JZ and CMZ analyzed the data. HLZ, SZ and RYT drafted the initial manuscript. KJ, LLY, HHY and LM contributed to the revision of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Lin Miao.

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Disclosures

Hanlong Zhu, Si Zhao, Chunmei Zhang, Kun Ji, Wei Wu, Linlin Yin, Haihao Yan, Jian Zhou, Ruiyi Tang and Lin Miao have declared that they have no conflicts of interest or financial ties to disclose.

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Institutional review board approval was not needed for this study as it utilized publically available data.

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Supplementary Information

Below is the link to the electronic supplementary material.

464_2021_8535_MOESM1_ESM.png

Supplementary file1 Kaplan-Meier survival curves comparing endoscopic therapy and surgery for entire cohort before propensity matching. (A) Overall survival; (B) Cancer-specific survival. (PNG 48 KB)

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Zhu, H., Zhao, S., Zhang, C. et al. Endoscopic and surgical treatment of T1N0M0 colorectal neuroendocrine tumors: a population-based comparative study. Surg Endosc 36, 2488–2498 (2022). https://doi.org/10.1007/s00464-021-08535-6

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  • DOI: https://doi.org/10.1007/s00464-021-08535-6

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