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Outcomes of laparoscopic tumor ablation for neuroendocrine liver metastases: a 20-year experience

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Abstract

Background

Since neuroendocrine tumors have an indolent behavior, studies looking at oncologic outcomes should report a long-term follow-up. Over the years, we have been treating selected patients with neuroendocrine liver metastases (NELM) with laparoscopic ablation (LA) and reported favorable local tumor control. The aim of this study is to see whether this local efficacy translates into long-term oncologic outcomes.

Methods

This was an IRB-approved study of patients who underwent LA for NELM at a single center. Overall and progression-free survivals were analyzed using Kaplan–Meier and Cox proportional hazards model.

Results

Study included 58 women and 71 men with a median age of 58 (IQR 47–67) years. Tumor type included carcinoid (n = 92), pancreatic islet cell (n = 28), and medullary thyroid cancer (n = 9). There was a median of 6 (IQR 3–8) tumors, measuring 1.6 (IQR 1.1–2.4) cm. At a median follow-up of 73 (IQR 34–135) months, local liver recurrence per patient, new liver recurrence, and new extrahepatic recurrence rates were 22, 68, and 33%, respectively. Local tumor recurrence per lesion was 5% (n = 42/770). Median overall survival was 125 months, with 5-year, and 10-year overall survivals being, 76%, and 59%, respectively; and median disease-free survival was 13 months, with 5-year, and 10-year progression-free survivals being 26%, and 6%, respectively. On Cox proportional hazards model, overall survival was independently predicted by tumor size, grade, and resection status of primary.

Conclusion

To our knowledge, this is the largest single-center experience with the longest follow-up regarding the utilization of LA for NELM. Our results demonstrate that in selected patients, LA achieves a 95% local tumor control and 59% 10-year overall survival.

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References

  1. Siperstein AE, Berber E (2001) Cryoablation, percutaneous alcohol injection, and radiofrequency ablation for treatment of neuroendocrine liver metastases. World J Surg 25:693–696

    Article  CAS  Google Scholar 

  2. Thompson GB, van Heerden JA, Grant CS, Carney JA, Ilstrup DM (1988) Islet cell carcinomas of the pancreas: a 20-year experience. Surgery 104:1011–1017

    CAS  PubMed  Google Scholar 

  3. Touzios JG, Kiely JM, Pitt SC, Rilling WS, Quebbeman EJ, Wilson SD, Pitt HA (2005) Neuroendocrine hepatic metastases: does aggressive management improve survival? Ann Surg 241:776–783

    Article  Google Scholar 

  4. Ejaz A, Reames BN, Maithel S, Poultsides GA, Bauer TW, Fields RC, Weiss M, Marques HP, Aldrighetti L, Pawlik TM (2017) The impact of extrahepatic disease among patients undergoing liver-directed therapy for neuroendocrine liver metastasis. J Surg Oncol 116(7):841–847. https://doi.org/10.1002/jso.24727

    Article  PubMed  Google Scholar 

  5. Sarmiento JM, Heywood G, Rubin J, Ilstrup DM, Nagorney DM, Que FG (2003) Surgical treatment of neuroendocrine metastases to the liver: a plea for resection to increase survival. J Am Coll Surg 197:29–37. https://doi.org/10.1016/S1072-7515(03)00230-8

    Article  PubMed  Google Scholar 

  6. Berber E, Flesher N, Siperstein AE (2002) Laparoscopic radiofrequency ablation of neuroendocrine liver metastases. World J Surg 26:985–990. https://doi.org/10.1007/s00268-002-6629-5

    Article  PubMed  Google Scholar 

  7. Maire F, Hammel P, Kianmanesh R, Hentic O, Couvelard A, Rebours V, Zappa M, Raymond E, Sauvanet A, Louvet C, Lévy P, Belghiti J, Ruszniewski P (2009) Is adjuvant therapy with streptozotocin and 5-fluorouracil useful after resection of liver metastases from digestive endocrine tumors? Surgery 145:69–75. https://doi.org/10.1016/j.surg.2008.08.007

    Article  PubMed  Google Scholar 

  8. di Bartolomeo M, Bajetta E, Buzzoni R, Mariani L, Carnaghi C, Somma L, Zilembo N, di Leo A (1996) Clinical efficacy of octreotide in the treatment of metastatic neuroendocrine tumors. A study by the Italian Trials in Medical Oncology Group. Cancer 77:402–408. https://doi.org/10.1002/(SICI)1097-0142(19960115)77:2%3c402:AID-CNCR25%3e3.0.CO;2-4

    Article  PubMed  Google Scholar 

  9. Frilling A, Modlin IM, Kidd M, Russell C, Breitenstein S, Salem R, Kwekkeboom D, Lau W, Klersy C, Vilgrain V, Davidson B, Siegler M, Caplin M, Solcia E, Schilsky R (2014) Recommendations for management of patients with neuroendocrine liver metastases. Lancet Oncol 15:e8–e21. https://doi.org/10.1016/S1470-2045(13)70362-0

    Article  PubMed  Google Scholar 

  10. Glazer ES, Tseng JF, Al-Refaie W, Solorzano CC, Liu P, Willborn KA, Abdalla EK, Vauthey J-N, Curley SA (2010) Long-term survival after surgical management of neuroendocrine hepatic metastases. HPB 12:427–433. https://doi.org/10.1111/j.1477-2574.2010.00198.x

    Article  PubMed  PubMed Central  Google Scholar 

  11. Fairweather M, Swanson R, Wang J, Brais LK, Dutton T, Kulke MH, Clancy TE (2017) Management of neuroendocrine tumor liver metastases: long-term outcomes and prognostic factors from a large prospective database. Ann Surg Oncol 24:2319–2325. https://doi.org/10.1245/s10434-017-5839-x

    Article  PubMed  Google Scholar 

  12. Nave H, Mössinger E, Feist H, Lang H, Raab H (2001) Surgery as primary treatment in patients with liver metastases from carcinoid tumors: a retrospective, unicentric study over 13 years. Surgery 129:170–175

    Article  CAS  Google Scholar 

  13. Chamberlain RS, Canes D, Brown KT, Saltz L, Jarnagin W, Fong Y, Blumgart LH (2000) Hepatic neuroendocrine metastases: does intervention alter outcomes? J Am Coll Surg 190:432–445

    Article  CAS  Google Scholar 

  14. Mayo SC, de Jong MC, Pulitano C, Clary BM, Reddy SK, Gamblin TC, Celinksi SA, Kooby DA, Staley CA, Stokes JB, Chu CK, Ferrero A, Schulick RD, Choti MA, Mentha G, Strub J, Bauer TW, Adams RB, Aldrighetti L, Capussotti L, Pawlik TM (2010) Surgical management of hepatic neuroendocrine tumor metastasis: results from an international multi-institutional analysis. Ann Surg Oncol 17:3129–3136. https://doi.org/10.1245/s10434-010-1154-5

    Article  PubMed  Google Scholar 

  15. Bagante F, Spolverato G, Merath K, Postlewait LM, Poultsides GA, Mullen MG, Bauer TW, Fields RC, Lamelas J, Marques HP, Aldrighetti L, Tran T, Maithel SK, Pawlik TM (2017) Neuroendocrine liver metastasis: the chance to be cured after liver surgery. J Surg Oncol 115:687–695. https://doi.org/10.1002/jso.24563

    Article  PubMed  Google Scholar 

  16. Saxena A, Chua TC, Sarkar A, Chu F, Liauw W, Zhao J, Morris DL (2011) Progression and survival results after radical hepatic metastasectomy of indolent advanced neuroendocrine neoplasms (NENs) supports an aggressive surgical approach. Surgery 149:209–220. https://doi.org/10.1016/j.surg.2010.06.008

    Article  PubMed  Google Scholar 

  17. Takahashi H, Akyuz M, Aksoy E, Karabulut K, Berber E (2017) Local recurrence after laparoscopic radiofrequency ablation of malignant liver tumors: results of a contemporary series. J Surg Oncol 115:830–834. https://doi.org/10.1002/jso.24599

    Article  PubMed  Google Scholar 

  18. Takahashi H, Kahramangil B, Berber E (2018) Local recurrence after microwave thermosphere ablation of malignant liver tumors: results of a surgical series. Surgery 163:709–713. https://doi.org/10.1016/j.surg.2017.10.026

    Article  PubMed  Google Scholar 

  19. Mazzaglia PJ, Berber E, Milas M, Siperstein AE (2007) Laparoscopic radiofrequency ablation of neuroendocrine liver metastases: a 10-year experience evaluating predictors of survival. Surgery 142:10–19. https://doi.org/10.1016/j.surg.2007.01.036

    Article  PubMed  Google Scholar 

  20. Akyildiz HY, Mitchell J, Milas M, Siperstein A, Berber E (2010) Laparoscopic radiofrequency thermal ablation of neuroendocrine hepatic metastases: long-term follow-up. Surgery 148:1288–1293. https://doi.org/10.1016/j.surg.2010.09.014

    Article  PubMed  Google Scholar 

  21. Gillams A, Cassoni A, Conway G, Lees W (2005) Radiofrequency ablation of neuroendocrine liver metastases: the Middlesex experience. Abdom Imaging 30:435–441. https://doi.org/10.1007/s00261-004-0258-4

    Article  CAS  PubMed  Google Scholar 

  22. Wessels FJ, Schell SR (2001) Radiofrequency ablation treatment of refractory carcinoid hepatic metastases. J Surg Res 95:8–12. https://doi.org/10.1006/jsre.2000.5988

    Article  CAS  PubMed  Google Scholar 

  23. Hellman P, Ladjevardi S, Skogseid B, Akerström G, Elvin A (2002) Radiofrequency tissue ablation using cooled tip for liver metastases of endocrine tumors. World J Surg 26:1052–1056. https://doi.org/10.1007/s00268-002-6663-3

    Article  PubMed  Google Scholar 

  24. Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, Abdalla EK, Fleming JB, Vauthey J-N, 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. https://doi.org/10.1200/JCO.2007.15.4377

    Article  PubMed  Google Scholar 

  25. Karabulut K, Akyildiz HY, Lance C, Aucejo F, McLennan G, Agcaoglu O, Siperstein A, Berber E (2011) Multimodality treatment of neuroendocrine liver metastases. Surgery 150:316–325. https://doi.org/10.1016/j.surg.2011.05.008

    Article  PubMed  Google Scholar 

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Acknowledgements

Dr. Emin Kose is a recipient of International Postdoctoral Research Fellowship Program scholarship awarded by The Scientific and Technological Research Council of Turkey (TUBITAK).

Funding

No financial support was received for this study.

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Authors and Affiliations

  1. Department of Endocrine Surgery, Cleveland Clinic, 9500 Euclid Ave/F20, Cleveland, OH, 44195, USA

    Emin Kose, Bora Kahramangil, Husnu Aydin, Mustafa Donmez, Allan Siperstein & Eren Berber

  2. Department of General Surgery, Cleveland Clinic, Cleveland, OH, USA

    Hideo Takahashi, Federico Aucejo & Eren Berber

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  1. Emin Kose
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Correspondence to Eren Berber.

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Disclosures

Dr. Eren Berber is consultant for Ethicon, Medtronics and Aesculap Inc. and has received honoraria for consulting activities. Drs. Emin Kose, Bora Kahramangil, Husnu Aydin, Mustafa Donmez, Hideo Takahashi, Federico Aucejo, and Allan Siperstein have no conflicts of interest or financial ties to disclose.

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Kose, E., Kahramangil, B., Aydin, H. et al. Outcomes of laparoscopic tumor ablation for neuroendocrine liver metastases: a 20-year experience. Surg Endosc 34, 249–256 (2020). https://doi.org/10.1007/s00464-019-06759-1

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