Skip to main content
Log in

Peritoneal metastases in patients with neuroendocrine neoplasms: a challenging site of metastases with clinical and prognostic implications

  • Original Article
  • Published:
Journal of Endocrinological Investigation Aims and scope Submit manuscript

Abstract

Purpose

Peritoneal metastases (PM) of neuroendocrine neoplasm (NEN) origin are identified with increasing frequency and exert a significant effect on quality of life and clinical status of the patients. The aim of this study was to identify the characteristics and the prognostic significance of PM in patients with NENs.

Methods

A retrospective analysis of the data of patients from two tertiary referral centers was performed. We defined a control group of age- and gender-matched NEN patients with comparable stage IV disease but no PM.

Results

We analysed 70 patients (41 females) with PM. Small intestine was the most common primary NEN site (87.1%). PM prevalence was 10.3%. Forty-four patients presented with synchronous PM, whereas 26 developed metachronous PM. The majority of patients had other concomitant metastases (50 hepatic, 6 lung and 12 bone metastases). Twelve patients developed intestinal obstruction. After PM diagnosis, 76% of patients received treatment with somatostatin analogues while six patients (8.6%) were treated with peptide receptor radionuclide therapy (PRRT). The median progression-free survival (PFS) in the PRRT-treated group was 15 months (95% CI 2–28). Median overall survival (OS) in the PM group was 142 months [95% CI 71–213] while it was not reached in the control group.

Conclusion

Peritoneal metastases show low prevalence among NEN patients and are most likely to develop in patients with small intestinal NENs and advanced metastatic disease. The presence of PM does seem to be associated with a negative prognostic impact on OS of NEN patients and their identification and prompt treatment is of major importance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

All data supporting the findings of this study are available upon request.

References

  1. Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, Abdalla EK, Fleming JB, Vauthey JN, Rashid A et al (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(18):3063–3072. https://doi.org/10.1200/JCO.2007.15.4377

    Article  PubMed  Google Scholar 

  2. Pavel M, O’Toole D, Costa F, Capdevila J, Gross D, Kianmanesh R, Krenning E, Knigge U, Salazar R, Pape UF et al (2016) ENETS consensus guidelines update for the management of distant metastatic disease of intestinal, pancreatic, bronchial neuroendocrine neoplasms (NEN) and NEN of unknown primary site. Neuroendocrinology 103(2):172–185. https://doi.org/10.1159/000443167

    Article  CAS  PubMed  Google Scholar 

  3. Dasari A, Shen C, Halperin D, Zhao B, Zhou S, Xu Y, Shih, T.: Yao, J.C. (2017) Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the United States. JAMA Oncol 3(10):1335–1342. https://doi.org/10.1001/jamaoncol.2017.0589

    Article  PubMed  PubMed Central  Google Scholar 

  4. Madani A, Thomassen I, van Gestel Y, van der Bilt JDW, Haak HR, de Hingh I, Lemmens V (2017) Peritoneal metastases from gastroenteropancreatic neuroendocrine tumors: incidence, risk factors and prognosis. Ann Surg Oncol 24(8):2199–2205. https://doi.org/10.1245/s10434-016-5734-x

    Article  PubMed  Google Scholar 

  5. Elias D, Sideris L, Liberale G, Ducreux M, Malka D, Lasser P, Duvillard P, Baudin E (2005) Surgical treatment of peritoneal carcinomatosis from well-differentiated digestive endocrine carcinomas. Surgery 137(4):411–416. https://doi.org/10.1016/j.surg.2004.11.007

    Article  PubMed  Google Scholar 

  6. Vasseur B, Cadiot G, Zins M, Flejou JF, Belghiti J, Marmuse JP, Vilgrain V, Bernades P, Mignon M, Ruszniewski P (1996) Peritoneal carcinomatosis in patients with digestive endocrine tumors. Cancer 78(8):1686–1692

    Article  CAS  PubMed  Google Scholar 

  7. Kianmanesh R, Ruszniewski P, Rindi G, Kwekkeboom D, Pape UF, Kulke M, Sevilla Garcia I, Scoazec JY, Nilsson O, Fazio N et al (2010) ENETS consensus guidelines for the management of peritoneal carcinomatosis from neuroendocrine tumors. Neuroendocrinology 91(4):333–340. https://doi.org/10.1159/000286700

    Article  CAS  PubMed  Google Scholar 

  8. Au JT, Levine J, Aytaman A, Weber T, Serafini F (2013) Management of peritoneal metastasis from neuroendocrine tumors. J Surg Oncol 108(6):385–386. https://doi.org/10.1002/jso.23399

    Article  PubMed  Google Scholar 

  9. Merola E, Prasad V, Pascher A, Pape UF, Arsenic R, Denecke T, Fehrenbach U, Wiedenmann B, Pavel ME (2020) Peritoneal carcinomatosis in gastro-entero-pancreatic neuroendocrine neoplasms: clinical impact and effectiveness of the available therapeutic options. Neuroendocrinology 110(6):517–524. https://doi.org/10.1159/000503144

    Article  CAS  PubMed  Google Scholar 

  10. Swellengrebel HA, Zoetmulder FA, Smeenk RM, Antonini N, Verwaal VJ (2009) Quantitative intra-operative assessment of peritoneal carcinomatosis—a comparison of three prognostic tools. Eur J Surg Oncol 35(10):1078–1084. https://doi.org/10.1016/j.ejso.2009.02.010

    Article  CAS  PubMed  Google Scholar 

  11. Gilly FN, Cotte E, Brigand C, Monneuse O, Beaujard AC, Freyer G, Glehen O (2006) Quantitative prognostic indices in peritoneal carcinomatosis. Eur J Surg Oncol 32(6):597–601. https://doi.org/10.1016/j.ejso.2006.03.002

    Article  CAS  PubMed  Google Scholar 

  12. de Mestier L, Lardiere-Deguelte S, Brixi H, O’Toole D, Ruszniewski P, Cadiot G, Kianmanesh R (2015) Updating the surgical management of peritoneal carcinomatosis in patients with neuroendocrine tumors. Neuroendocrinology 101(2):105–111. https://doi.org/10.1159/000371817

    Article  CAS  PubMed  Google Scholar 

  13. Nagtegaal ID, Odze RD, Klimstra D, Paradis V, Rugge M, Schirmacher P, Washington KM, Carneiro F, Cree IA, Board W.H.O.C.o.T.E. (2020) The 2019 WHO classification of tumours of the digestive system. Histopathology 76(2):182–188. https://doi.org/10.1111/his.13975

    Article  PubMed  Google Scholar 

  14. Schwartz LH, Litiere S, de Vries E, Ford R, Gwyther S, Mandrekar S, Shankar L, Bogaerts J, Chen A, Dancey J et al (2016) RECIST 1.1-Update and clarification: from the RECIST committee. Eur J Cancer 62:132–137. https://doi.org/10.1016/j.ejca.2016.03.081

    Article  PubMed  PubMed Central  Google Scholar 

  15. Boudreaux JP, Putty B, Frey DJ, Woltering E, Anthony L, Daly I, Ramcharan T, Lopera J, Castaneda W (2005) Surgical treatment of advanced-stage carcinoid tumors: lessons learned. Ann Surg 241(6):839–845. https://doi.org/10.1097/01.sla.0000164073.08093.5d. (discussion 845–6)

    Article  PubMed  PubMed Central  Google Scholar 

  16. Pavel M, Grossman A, Arnold R, Perren A, Kaltsas G, Steinmuller T, de Herder W, Nikou G, Plockinger U, Lopes JM et al (2010) ENETS consensus guidelines for the management of brain, cardiac and ovarian metastases from neuroendocrine tumors. Neuroendocrinology 91(4):326–332. https://doi.org/10.1159/000287277

    Article  CAS  PubMed  Google Scholar 

  17. Tan EH, Tan CH (2011) Imaging of gastroenteropancreatic neuroendocrine tumors. World J Clin Oncol 2(1):28–43. https://doi.org/10.5306/wjco.v2.i1.28

    Article  MathSciNet  PubMed  PubMed Central  Google Scholar 

  18. Sundin A, Arnold R, Baudin E, Cwikla JB, Eriksson B, Fanti S, Fazio N, Giammarile F, Hicks RJ, Kjaer A et al (2017) ENETS consensus guidelines for the standards of care in neuroendocrine tumors: radiological. Nucl Med Hybrid Imaging Neuroendocrinol 105(3):212–244. https://doi.org/10.1159/000471879

    Article  CAS  Google Scholar 

  19. Bahri H, Laurence L, Edeline J, Leghzali H, Devillers A, Raoul JL, Cuggia M, Mesbah H, Clement B, Boucher E et al (2014) High prognostic value of 18F-FDG PET for metastatic gastroenteropancreatic neuroendocrine tumors: a long-term evaluation. J Nucl Med 55(11):1786–1790. https://doi.org/10.2967/jnumed.114.144386

    Article  CAS  PubMed  Google Scholar 

  20. Binderup T, Knigge U, Loft A, Federspiel B, Kjaer A (2010) 18F-fluorodeoxyglucose positron emission tomography predicts survival of patients with neuroendocrine tumors. Clin Cancer Res 16(3):978–985. https://doi.org/10.1158/1078-0432.CCR-09-1759

    Article  CAS  PubMed  Google Scholar 

  21. Hajjar R, Mercier F, Passot G, Pasquer A, Gelli M, Levine EA, Villeneuve L, Poncet G, Walter T, Glehen O (2022) Cytoreductive surgery with or without hyperthermic intraperitoneal chemotherapy for small bowel neuroendocrine tumors with peritoneal metastasis. Eur J Surg Oncol 48(7):1626–1630. https://doi.org/10.1016/j.ejso.2022.03.019

    Article  PubMed  Google Scholar 

Download references

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Marina Tsoli, Harry Wilson, Panagiotis Armonis, Lucasz Kamieniarz and Jessica Thuringer. The first draft of the manuscript was written by Marina Tsoli and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to M. Tsoli.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Ethics approval

This study was conducted retrospectively from data obtained for clinical purposes and was performed in line with the principles of the Declaration of Helsinki.

Informed consent

Written informed consent was obtained from all the study participants.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsoli, M., Wilson, H., Armonis, P. et al. Peritoneal metastases in patients with neuroendocrine neoplasms: a challenging site of metastases with clinical and prognostic implications. J Endocrinol Invest (2024). https://doi.org/10.1007/s40618-024-02330-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s40618-024-02330-5

Keywords

Navigation