Reviews in Endocrine and Metabolic Disorders

, Volume 18, Issue 4, pp 443–457 | Cite as

Is there any role for minimally invasive surgery in NET?

  • M. Thomaschewski
  • H. Neeff
  • T. Keck
  • H. P. H. Neumann
  • T. Strate
  • E. von Dobschuetz


Neuroendocrine tumors (NET) represent the variability of almost benign lesions either secreting hormones occurring as a single lesion up to malignant lesions with metastatic potential. Treatment of NET is usually performed by surgical resection. Due to the rarity of NET, surgical treatment is mainly based on the experience and recommendations of experts and less on the basis of prospective randomized studies. In addition, the development and establishment of new surgical procedures is made more difficult by their rarity. The development of laparoscopic-assisted surgery has significantly improved the treatment of many diseases. Due to the well-known advantages of laparoscopic surgery, this method has also been increasingly used to treat NET. However, due to limited comparative data, the assumed superiority of laparoscopic surgery in the area NET remains often unclear or not yet proven. This review focuses on the present usage of laparoscopic techniques in the area of NET. Relating to the current literature, this review presents the evidence of various laparoscopic procedures for treatment of adrenal, pancreatic and intestine NET as well as extraadrenal pheochromocytoma and neuroendocrine liver metastases. Further, this review focuses on recent new developments of minimally invasive surgery in the area of NET. Here, robotic-assisted surgery and single-port surgery are promising approaches.


Neuroendocrine tumors Laparoscopy Minimally invasive surgery Adrenal Liver Pancreas Robotic surgery 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Gagner M, Lacroix A, Bolte E. Laparoscopic adrenalectomy in Cushing's syndrome and pheochromocytoma. N Engl J Med. 1992;327(14):1033. Scholar
  2. 2.
    Walz MK. Minimally invasive adrenal gland surgery. Transperitoneal or retroperitoneal approach? Chirurg. 2012;83(6):536–45. Scholar
  3. 3.
    Conzo G, Pasquali D, Della Pietra C, Napolitano S, Esposito D, Iorio S, et al. Laparoscopic adrenal surgery: ten-year experience in a single institution. BMC Surg. 2013;13(Suppl 2):S5.–2482-13-S2-S5.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Elfenbein DM, Scarborough JE, Speicher PJ, Scheri RP. Comparison of laparoscopic versus open adrenalectomy: results from American College of Surgeons-National Surgery Quality Improvement Project. J Surg Res. 2013;184(1):216–20. Scholar
  5. 5.
    Tiberio GA, Baiocchi GL, Arru L, Agabiti Rosei C, De Ponti S, Matheis A, et al. Prospective randomized comparison of laparoscopic versus open adrenalectomy for sporadic pheochromocytoma. Surg Endosc. 2008;22(6):1435–9. Scholar
  6. 6.
    Walz MK, Peitgen K, Krause U, Eigler FW. Dorsal retroperitoneoscopic adrenalectomy--a new surgical technique. Zentralbl Chir. 1995;120(1):53–8.PubMedGoogle Scholar
  7. 7.
    Walz MK, Alesina PF, Wenger FA, Deligiannis A, Szuczik E, Petersenn S, et al. Posterior retroperitoneoscopic adrenalectomy--results of 560 procedures in 520 patients. Surgery. 2006;140(6):943–948. discussion 8–50. Scholar
  8. 8.
    Berber E, Tellioglu G, Harvey A, Mitchell J, Milas M, Siperstein A. Comparison of laparoscopic transabdominal lateral versus posterior retroperitoneal adrenalectomy. Surgery. 2009;146(4):621–625. discussion 5–6. Scholar
  9. 9.
    Mazzaglia PJ, Vezeridis MP. Laparoscopic adrenalectomy: balancing the operative indications with the technical advances. J Surg Oncol. 2010;101(8):739–44. Scholar
  10. 10.
    Tai CK, Li SK, Hou SM, Fan CW, Fung TC, Wah MK. Laparoscopic adrenalectomy: Comparison of lateral transperitoneal and lateral retroperitoneal approaches. Surg Laparosc Endosc Percutan Tech. 2006;16(3):141–5.PubMedCrossRefGoogle Scholar
  11. 11.
    Ramacciato G, Nigri GR, Petrucciani N, Di Santo V, Piccoli M, Buniva P, et al. Minimally invasive adrenalectomy: a multicenter comparison of transperitoneal and retroperitoneal approaches. Am Surg. 2011;77(4):409–16.PubMedGoogle Scholar
  12. 12.
    Kiriakopoulos A, Petralias A, Linos D. Posterior retroperitoneoscopic versus laparoscopic adrenalectomy in sporadic and MENIIA pheochromocytomas. Surg Endosc. 2015;29(8):2164–70. Scholar
  13. 13.
    Dickson PV, Alex GC, Grubbs EG, Ayala-Ramirez M, Jimenez C, Evans DB, et al. Posterior retroperitoneoscopic adrenalectomy is a safe and effective alternative to transabdominal laparoscopic adrenalectomy for pheochromocytoma. Surgery. 2011;150(3):452–8. Scholar
  14. 14.
    Rubinstein M, Gill IS, Aron M, Kilciler M, Meraney AM, Finelli A, et al. Prospective, randomized comparison of transperitoneal versus retroperitoneal laparoscopic adrenalectomy. J Urol. 2005;174(2):442–445. discussion 5. Scholar
  15. 15.
    Bonjer HJ, Lange JF, Kazemier G, de Herder WW, Steyerberg EW, Bruining HA. Comparison of three techniques for adrenalectomy. Br J Surg. 1997;84(5):679–82.PubMedCrossRefGoogle Scholar
  16. 16.
    Walz MK, Groeben H, Alesina PF. Single-access retroperitoneoscopic adrenalectomy (SARA) versus conventional retroperitoneoscopic adrenalectomy (CORA): a case-control study. World J Surg. 2010;34(6):1386–90. Scholar
  17. 17.
    Kiriakopoulos A, Economopoulos KP, Poulios E, Linos D. Impact of posterior retroperitoneoscopic adrenalectomy in a tertiary care center: a paradigm shift. Surg Endosc. 2011;25(11):3584–9. Scholar
  18. 18.
    Grau-Talens EJ, Garcia-Olives F, Ruperez-Arribas MP. Transcylindrical cholecystectomy: new technique for minimally invasive cholecystectomy. World J Surg. 1998;22(5):453–8.PubMedCrossRefGoogle Scholar
  19. 19.
    Liatsikos E, Kallidonis P, Kyriazis I, Al-Aown A, Stolzenburg JU. Urologic laparoendoscopic single-site surgery. Nat Rev Urol. 2009;6(12):654–9. Scholar
  20. 20.
    Colleselli D, Janetschek G. Current trends in partial adrenalectomy. Curr Opin Urol. 2015;25(2):89–94. Scholar
  21. 21.
    Wang L, Cai C, Liu B, Yang Q, Wu Z, Xiao L, et al. Perioperative outcomes and cosmesis analysis of patients undergoing laparoendoscopic single-site adrenalectomy: a comparison of transumbilical, transperitoneal subcostal, and retroperitoneal subcostal approaches. Urology. 2013;82(2):358–64. Scholar
  22. 22.
    Yuge K, Miyajima A, Hasegawa M, Miyazaki Y, Maeda T, Takeda T, et al. Initial experience of transumbilical laparoendoscopic single-site surgery of partial adrenalectomy in patient with aldosterone-producing adenoma. BMC Urol. 2010;10:19. Scholar
  23. 23.
    St Julien J, Ball D, Schulick R. Robot-assisted cortical-sparing adrenalectomy in a patient with Von Hippel-Lindau disease and bilateral pheochromocytomas separated by 9 years. J Laparoendosc Adv Surg Tech A. 2006;16(5):473–7. Scholar
  24. 24.
    Nordenstrom E, Westerdahl J, Hallgrimsson P, Bergenfelz A. A prospective study of 100 roboticallyassisted laparoscopic adrenalectomies. J Robot Surg. 2011;5(2):127–31. Scholar
  25. 25.
    Brandao LF, Autorino R, Laydner H, Haber GP, Ouzaid I, De Sio M, et al. Robotic versus laparoscopic adrenalectomy: a systematic review and meta-analysis. Eur Urol. 2014;65(6):1154–61. Scholar
  26. 26.
    Economopoulos KP, Mylonas KS, Stamou AA, Theocharidis V, Sergentanis TN, Psaltopoulou T, et al. Laparoscopic versus robotic adrenalectomy: A comprehensive meta-analysis. Int J Surg. 2017;38:95–104. Scholar
  27. 27.
    Brunaud L, Ayav A, Zarnegar R, Rouers A, Klein M, Boissel P, et al. Prospective evaluation of 100 robotic-assisted unilateral adrenalectomies. Surgery. 2008;144(6):995–1001. discussion. Scholar
  28. 28.
    Berber E, Mitchell J, Milas M, Siperstein A. Robotic posterior retroperitoneal adrenalectomy: operative technique. Arch Surg. 2010;145(8):781–4. Scholar
  29. 29.
    Ludwig AT, Wagner KR, Lowry PS, Papaconstantinou HT, Lairmore TC. Robot-assisted posterior retroperitoneoscopic adrenalectomy. J Endourol. 2010;24(8):1307–14. Scholar
  30. 30.
    Okoh AK, Yigitbas H, Berber E. Robotic posterior retroperitoneal adrenalectomy. J Surg Oncol. 2015;112(3):302–4. Scholar
  31. 31.
    Taskin HE, Aliyev S, Aksoy E, Hamrahian A, Siperstein A, Berber E. Bilateral posterior retroperitoneal robotic adrenalectomy for ACTH-independent Cushing syndrome. Surg Laparosc Endosc Percutan Tech. 2014;24(3):e113–5. Scholar
  32. 32.
    Kahramangil B, Berber E. Comparison of posterior retroperitoneal and transabdominal lateral approaches in robotic adrenalectomy: an analysis of 200 cases. Surg Endosc. 2017;
  33. 33.
    Lenders JW, Duh QY, Eisenhofer G, Gimenez-Roqueplo AP, Grebe SK, Murad MH, et al. Pheochromocytoma and paraganglioma: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2014;99(6):1915–42. Scholar
  34. 34.
    Pacak K. Preoperative management of the pheochromocytoma patient. J Clin Endocrinol Metab. 2007;92(11):4069–79. Scholar
  35. 35.
    Kinney MA, Narr BJ, Warner MA. Perioperative management of pheochromocytoma. J Cardiothorac Vasc Anesth. 2002;16(3):359–69.PubMedCrossRefGoogle Scholar
  36. 36.
    Groeben H, Nottebaum BJ, Alesina PF, Traut A, Neumann HP, Walz MK. Perioperative alpha-receptor blockade in phaeochromocytoma surgery: an observational case series. Br J Anaesth. 2017;118(2):182–9. Scholar
  37. 37.
    Livingstone M, Duttchen K, Thompson J, Sunderani Z, Hawboldt G, Sarah Rose M, et al. Hemodynamic Stability During Pheochromocytoma Resection: Lessons Learned Over the Last Two Decades. Ann Surg Oncol. 2015;22(13):4175–80. Scholar
  38. 38.
    Kiernan CM, Du L, Chen X, Broome JT, Shi C, Peters MF, et al. Predictors of hemodynamic instability during surgery for pheochromocytoma. Ann Surg Oncol. 2014;21(12):3865–71. Scholar
  39. 39.
    Walz MK, Alesina PF, Wenger FA, Koch JA, Neumann HP, Petersenn S, et al. Laparoscopic and retroperitoneoscopic treatment of pheochromocytomas and retroperitoneal paragangliomas: results of 161 tumors in 126 patients. World J Surg. 2006;30(5):899–908. Scholar
  40. 40.
    Rao N, Ramachandran R, Tandon N, Singh P, Kumar R. Laparoscopic adrenalectomy for pheochromocytoma-does size matter? A single surgeon comparative study. Transl Androl Urol. 2016;5(5):780–3.  10.21037/tau.2016.08.10.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Carter YM, Mazeh H, Sippel RS, Chen H. Safety and feasibility of laparoscopic resection for large (>/= 6 CM) pheochromocytomas without suspected malignancy. Endocr Pract. 2012;18(5):720–6. Scholar
  42. 42.
    Sessa L, Nomine-Criqui C, Germain A, Ayav A, Bresler L, Brunaud L. Robotic transperitoneal left adrenalectomy for a 10cm pheochromocytoma (with video). J Visc Surg. 2016;153(4):307–8. Scholar
  43. 43.
    Shen WT, Grogan R, Vriens M, Clark OH, Duh QY. One hundred two patients with pheochromocytoma treated at a single institution since the introduction of laparoscopic adrenalectomy. Arch Surg. 2010;145(9):893–7. Scholar
  44. 44.
    Goers TA, Abdo M, Moley JF, Matthews BD, Quasebarth M, Brunt LM. Outcomes of resection of extra-adrenal pheochromocytomas/paragangliomas in the laparoscopic era: a comparison with adrenal pheochromocytoma. Surg Endosc. 2013;27(2):428–33. Scholar
  45. 45.
    Gagner M, Pomp A. Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc. 1994;8(5):408–10.PubMedCrossRefGoogle Scholar
  46. 46.
    Cuschieri A. Laparoscopic surgery of the pancreas. J R Coll Surg Edinb. 1994;39(3):178–84.PubMedGoogle Scholar
  47. 47.
    Nigri GR, Rosman AS, Petrucciani N, Fancellu A, Pisano M, Zorcolo L, et al. Metaanalysis of trials comparing minimally invasive and open distal pancreatectomies. Surg Endosc. 2011;25(5):1642–51. Scholar
  48. 48.
    Schloricke E, Hoffmann M, Kujath P, Shetty GM, Scheer F, Liedke MO, et al. Laparoscopic Pylorus- and Spleen-Preserving Duodenopancreatectomy for a Multifocal Neuroendocrine Tumor. Viszeralmedizin. 2015;31(5):364–9. Scholar
  49. 49.
    Mabrut JY, Fernandez-Cruz L, Azagra JS, Bassi C, Delvaux G, Weerts J, et al. Laparoscopic pancreatic resection: results of a multicenter European study of 127 patients. Surgery. 2005;137(6):597–605.PubMedCrossRefGoogle Scholar
  50. 50.
    Wellner UF, Kusters S, Sick O, Busch C, Bausch D, Bronsert P, et al. Hybrid laparoscopic versus open pylorus-preserving pancreatoduodenectomy: retrospective matched case comparison in 80 patients. Langenbecks Arch Surg. 2014;399(7):849–56. Scholar
  51. 51.
    Drymousis P, Raptis DA, Spalding D, Fernandez-Cruz L, Menon D, Breitenstein S, et al. Laparoscopic versus open pancreas resection for pancreatic neuroendocrine tumours: a systematic review and meta-analysis. HPB (Oxford). 2014;16(5):397–406. Scholar
  52. 52.
    Fernandez-Cruz L, Blanco L, Cosa R, Rendon H. Is laparoscopic resection adequate in patients with neuroendocrine pancreatic tumors? World J Surg. 2008;32(5):904–17. Scholar
  53. 53.
    Partelli S, Bartsch DK, Capdevila J, Chen J, Knigge U, Niederle B, et al. ENETS Consensus Guidelines for Standard of Care in Neuroendocrine Tumours: Surgery for Small Intestinal and Pancreatic Neuroendocrine Tumours. Neuroendocrinology. 2017;
  54. 54.
    Falconi M, Zerbi A, Crippa S, Balzano G, Boninsegna L, Capitanio V, et al. Parenchyma-preserving resections for small nonfunctioning pancreatic endocrine tumors. Ann Surg Oncol. 2010;17(6):1621–7. Scholar
  55. 55.
    Zhao YP, Zhan HX, Zhang TP, Cong L, Dai MH, Liao Q, et al. Surgical management of patients with insulinomas: Result of 292 cases in a single institution. J Surg Oncol. 2011;103(2):169–74. Scholar
  56. 56.
    Partelli S, Tamburrino D, Lopez C, Albers M, Milanetto AC, Pasquali C, et al. Active Surveillance versus Surgery of Nonfunctioning Pancreatic Neuroendocrine Neoplasms </=2 cm in MEN1 Patients. Neuroendocrinology. 2016;103(6):779–86. Scholar
  57. 57.
    Fendrich V, Waldmann J, Bartsch DK, Langer P. Surgical management of pancreatic endocrine tumors. Nat Rev Clin Oncol. 2009;6(7):419–28. Scholar
  58. 58.
    Yoo YJ, Yang SJ, Hwang HK, Kang CM, Kim H, Lee WJ. Overestimated Oncologic Significance of Lymph Node Metastasis in G1 Nonfunctioning Neuroendocrine Tumor in the Left Side of the Pancreas. Medicine (Baltimore). 2015;94(36):e1404. Scholar
  59. 59.
    Gagner M, Pomp A, Herrera MF. Early experience with laparoscopic resections of islet cell tumors. Surgery. 1996;120(6):1051–4.PubMedCrossRefGoogle Scholar
  60. 60.
    Dedieu A, Rault A, Collet D, Masson B, Sa CA. Laparoscopic enucleation of pancreatic neoplasm. Surg Endosc. 2011;25(2):572–6. Scholar
  61. 61.
    Zhang RC, Zhou YC, Mou YP, Huang CJ, Jin WW, Yan JF, et al. Laparoscopic versus open enucleation for pancreatic neoplasms: clinical outcomes and pancreatic function analysis. Surg Endosc. 2016;30(7):2657–65. Scholar
  62. 62.
    Karaliotas C, Sgourakis G. Laparoscopic versus open enucleation for solitary insulinoma in the body and tail of the pancreas. J Gastrointest Surg. 2009;13(10):1869. Scholar
  63. 63.
    Sa Cunha A, Beau C, Rault A, Catargi B, Collet D, Masson B. Laparoscopic versus open approach for solitary insulinoma. Surg Endosc. 2007;21(1):103–8. Scholar
  64. 64.
    Costi R, Randone B, Mal F, Basato S, Levard H, Gayet B. A critical appraisal of laparoscopic pancreatic enucleations: right-sided procedures (Pancreatic Head, Uncus) are not mini-invasive surgery. Surg Laparosc Endosc Percutan Tech. 2013;23(6):524–31. Scholar
  65. 65.
    Venkat R, Edil BH, Schulick RD, Lidor AO, Makary MA, Wolfgang CL. Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg. 2012;255(6):1048–59. Scholar
  66. 66.
    Sulpice L, Farges O, Goutte N, Bendersky N, Dokmak S, Sauvanet A, et al. Laparoscopic Distal Pancreatectomy for Pancreatic Ductal Adenocarcinoma: Time for a Randomized Controlled Trial? Results of an All-inclusive National Observational Study. Ann Surg. 2015;262(5):868–873. discussion 73–4. Scholar
  67. 67.
    de Rooij T, Jilesen AP, Boerma D, Bonsing BA, Bosscha K, van Dam RM, et al. A nationwide comparison of laparoscopic and open distal pancreatectomy for benign and malignant disease. J Am Coll Surg. 2015;220(3):263–270 e1. Scholar
  68. 68.
    de Rooij T, Tol JA, van Eijck CH, Boerma D, Bonsing BA, Bosscha K, et al. Outcomes of distal pancreatectomy for pancreatic ductal adenocarcinoma in the Netherlands: a Nationwide retrospective analysis. Ann Surg Oncol. 2016;23(2):585–91. Scholar
  69. 69.
    de Rooij T, van Hilst J, Busch OR, Dijkgraaf MG, Kooby DA, Abu Hilal M, et al. Laparoscopic distal pancreatectomy for pancreatic ductal adenocarcinoma: time for a randomized controlled trial? Results of an all-inclusive National Observational Study. Ann Surg. 2016;
  70. 70.
    de Rooij T, van Hilst J, Vogel JA, van Santvoort HC, de Boer MT, Boerma D, et al. Minimally invasive versus open distal pancreatectomy (LEOPARD): study protocol for a randomized controlled trial. Trials. 2017;18(1):166. PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Lopez CL, Albers MB, Bollmann C, Manoharan J, Waldmann J, Fendrich V, et al. Minimally invasive versus open pancreatic surgery in patients with multiple endocrine neoplasia type 1. World J Surg. 2016;40(7):1729–36. Scholar
  72. 72.
    Wang M, Meng L, Cai Y, Li Y, Wang X, Zhang Z, et al. Learning curve for laparoscopic Pancreaticoduodenectomy: a CUSUM analysis. J Gastrointest Surg. 2016;20(5):924–35. Scholar
  73. 73.
    Song KB, Kim SC, Hwang DW, Lee JH, Lee DJ, Lee JW, et al. Matched case-control analysis comparing laparoscopic and open pylorus-preserving Pancreaticoduodenectomy in patients with Periampullary tumors. Ann Surg. 2015;262(1):146–55. Scholar
  74. 74.
    Mendoza AS, 3rd, Han HS, Yoon YS, Cho JY, Choi Y. Laparoscopy-assisted pancreaticoduodenectomy as minimally invasive surgery for periampullary tumors: a comparison of short-term clinical outcomes of laparoscopy-assisted pancreaticoduodenectomy and open pancreaticoduodenectomy. J Hepatobiliary Pancreat Sci 2015;22(12):819–824. doi:
  75. 75.
    Wang M, Zhang H, Wu Z, Zhang Z, Peng B. Laparoscopic pancreaticoduodenectomy: single-surgeon experience. Surg Endosc. 2015;29(12):3783–94. Scholar
  76. 76.
    Keutgen XM, Hammel P, Choyke PL, Libutti SK, Jonasch E, Kebebew E. Evaluation and management of pancreatic lesions in patients with von Hippel-Lindau disease. Nat Rev Clin Oncol. 2016;13(9):537–49. Scholar
  77. 77.
    von Ducker L, Walz MK, Voss C, Arnold G, Eng C, Neumann HP. Laparoscopic organ-sparing resection of von Hippel-Lindau disease-associated pancreatic neuroendocrine tumors. World J Surg. 2011;35(3):563–7. Scholar
  78. 78.
    Melvin WS, Needleman BJ, Krause KR, Schneider C, Wolf RK, Michler RE, et al. Computer-enhanced robotic telesurgery. Initial experience in foregut surgery. Surg Endosc. 2002;16(12):1790–2. Scholar
  79. 79.
    Chen S, Zhan Q, Chen JZ, Jin JB, Deng XX, Chen H, et al. Robotic approach improves spleen-preserving rate and shortens postoperative hospital stay of laparoscopic distal pancreatectomy: a matched cohort study. Surg Endosc. 2015;29(12):3507–18. Scholar
  80. 80.
    Daouadi M, Zureikat AH, Zenati MS, Choudry H, Tsung A, Bartlett DL, et al. Robot-assisted minimally invasive distal pancreatectomy is superior to the laparoscopic technique. Ann Surg. 2013;257(1):128–32. Scholar
  81. 81.
    Lee SY, Allen PJ, Sadot E, D'Angelica MI, DeMatteo RP, Fong Y, et al. Distal pancreatectomy: a single institution's experience in open, laparoscopic, and robotic approaches. J Am Coll Surg. 2015;220(1):18–27. Scholar
  82. 82.
    Zhang J, Jin J, Chen S, Gu J, Zhu Y, Qin K, et al. Minimally invasive distal pancreatectomy for PNETs: laparoscopic or robotic approach? Oncotarget. 2017;8(20):33872–83.  10.18632/oncotarget.17513. PubMedPubMedCentralGoogle Scholar
  83. 83.
    Lai EC, Tang CN. Robotic distal pancreatectomy versus conventional laparoscopic distal pancreatectomy: a comparative study for short-term outcomes. Front Med. 2015;9(3):356–60. Scholar
  84. 84.
    Ryan CE, Ross SB, Sukharamwala PB, Sadowitz BD, Wood TW, Rosemurgy AS. Distal pancreatectomy and splenectomy: a robotic or LESS approach. JSLS. 2015;19(1):e2014 00246. Scholar
  85. 85.
    Joyce D, Morris-Stiff G, Falk GA, El-Hayek K, Chalikonda S, Walsh RM. Robotic surgery of the pancreas. World J Gastroenterol. 2014;20(40):14726–32. Scholar
  86. 86.
    Giulianotti PC, Addeo P, Buchs NC, Ayloo SM, Bianco FM. Robotic extended pancreatectomy with vascular resection for locally advanced pancreatic tumors. Pancreas. 2011;40(8):1264–70. Scholar
  87. 87.
    Boone BA, Zenati M, Hogg ME, Steve J, Moser AJ, Bartlett DL, et al. Assessment of quality outcomes for robotic pancreaticoduodenectomy: identification of the learning curve. JAMA Surg. 2015;150(5):416–22. Scholar
  88. 88.
    Hoffmann KM, Furukawa M, Jensen RT. Duodenal neuroendocrine tumors: classification, functional syndromes, diagnosis and medical treatment. Best Pract Res Clin Gastroenterol. 2005;19(5):675–97. Scholar
  89. 89.
    Delle Fave G, O'Toole D, Sundin A, Taal B, Ferolla P, Ramage JK, et al. ENETS consensus guidelines update for gastroduodenal neuroendocrine neoplasms. Neuroendocrinology. 2016;103(2):119–24. Scholar
  90. 90.
    Tsujimoto H, Ichikura T, Nagao S, Sato T, Ono S, Aiko S, et al. Minimally invasive surgery for resection of duodenal carcinoid tumors: endoscopic full-thickness resection under laparoscopic observation. Surg Endosc. 2010;24(2):471–5. Scholar
  91. 91.
    Abe N, Takeuchi H, Shibuya M, Ohki A, Yanagida O, Masaki T, et al. Successful treatment of duodenal carcinoid tumor by laparoscopy-assisted endoscopic full-thickness resection with lymphadenectomy. Asian J Endosc Surg. 2012;5(2):81–5. Scholar
  92. 92.
    Shamiyeh A, Gabriel M. Laparoscopic resection of gastrointestinal neuroendocrine tumors with special contribution of radionuclide imaging. World J Gastroenterol. 2014;20(42):15608–15. Scholar
  93. 93.
    Jayakrishnan TT, Groeschl RT, George B, Thomas JP, Clark Gamblin T, Turaga KK. Review of the impact of antineoplastic therapies on the risk for cholelithiasis and acute cholecystitis. Ann Surg Oncol. 2014;21(1):240–7. Scholar
  94. 94.
    Capurso G, Rinzivillo M, Bettini R, Boninsegna L, Delle Fave G, Falconi M. Systematic review of resection of primary midgut carcinoid tumour in patients with unresectable liver metastases. Br J Surg. 2012;99(11):1480–6. Scholar
  95. 95.
    Connor SJ, Hanna GB, Frizelle FA. Appendiceal tumors: retrospective clinicopathologic analysis of appendiceal tumors from 7,970 appendectomies. Dis Colon rectum. 1998;41(1):75–80.PubMedCrossRefGoogle Scholar
  96. 96.
    Alexandraki KI, Kaltsas GA, Grozinsky-Glasberg S, Chatzellis E, Grossman AB. Appendiceal neuroendocrine neoplasms: diagnosis and management. Endocr Relat Cancer. 2016;23(1):R27–41. Scholar
  97. 97.
    Suarez-Grau JM, Garcia-Ruiz S, Rubio-Chaves C, Bustos-Jimenez M, Docobo-Durantez F, Padillo-Ruiz FJ. Appendiceal carcinoid tumors. Evaluation of long-term outcomes in a tertiary level. Cir Cir. 2014;82(2):142–9.PubMedGoogle Scholar
  98. 98.
    Bucher P, Mathe Z, Demirag A, Morel P. Appendix tumors in the era of laparoscopic appendectomy. Surg Endosc. 2004;18(7):1063–6. PubMedCrossRefGoogle Scholar
  99. 99.
    Dralle H. Surgical strategies for accidental detection of appendix carcinoids. Chirurg. 2011;82(7):598–606. Scholar
  100. 100.
    Abraham NS, Young JM, Solomon MJ. Meta-analysis of short-term outcomes after laparoscopic resection for colorectal cancer. Br J Surg. 2004;91(9):1111–24. Scholar
  101. 101.
    Kuhry E, Schwenk WF, Gaupset R, Romild U, Bonjer HJ. Long-term results of laparoscopic colorectal cancer resection. Cochrane Database Syst Rev. 2008;2:CD003432. Scholar
  102. 102.
    Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, et al. Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol. 2005;6(7):477–84. Scholar
  103. 103.
    Jayne DG, Guillou PJ, Thorpe H, Quirke P, Copeland J, Smith AM, et al. Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC trial group. J Clin Oncol. 2007;25(21):3061–8. Scholar
  104. 104.
    Palanivelu C, Rangarajan M, Annapoorni S, Senthilkumar R, Anand NV. Laparoscopic right hemicolectomy for goblet-cell carcinoid of the appendix: report of a rare case and literature survey. J Laparoendosc Adv Surg Tech A. 2008;18(3):417–21. Scholar
  105. 105.
    Tomioka K, Fukoe Y, Lee Y, Lee M, Wada Y, Aoki T, et al. Primary neuroendocrine carcinoma of the appendix: a case report and review of the literature. Anticancer Res. 2013;33(6):2635–8.PubMedGoogle Scholar
  106. 106.
    Scherubl H, Kloppel G. Rectal carcinoids on the rise - update. Z Gastroenterol. 2009;47(4):365–71. PubMedCrossRefGoogle Scholar
  107. 107.
    Konishi T, Watanabe T, Nagawa H, Oya M, Ueno M, Kuroyanagi H, et al. Treatment of colorectal carcinoids: a new paradigm. World J Gastrointest Surg. 2010;2(5):153–6. Scholar
  108. 108.
    Moore JS, Cataldo PA, Osler T, Hyman NH. Transanal endoscopic microsurgery is more effective than traditional transanal excision for resection of rectal masses. Dis Colon rectum. 2008;51(7):1026–1030. discussion 30-1. Scholar
  109. 109.
    Quaresima S, Balla A, Franceschilli L, La Torre M, Iafrate C, Shalaby M, et al. Transanal minimally invasive surgery for rectal lesions. JSLS. 2016;20(3)
  110. 110.
    Atallah S, Albert M, Larach S. Transanal minimally invasive surgery: a giant leap forward. Surg Endosc. 2010;24(9):2200–5. Scholar
  111. 111.
    Martin-Perez B, Andrade-Ribeiro GD, Hunter L, Atallah S. A systematic review of transanal minimally invasive surgery (TAMIS) from 2010 to 2013. Tech Coloproctol. 2014;18(9):775–88. Scholar
  112. 112.
    Verseveld M, Barendse RM, Gosselink MP, Verhoef C, de Graaf EJ, Doornebosch PG. Transanal minimally invasive surgery: impact on quality of life and functional outcome. Surg Endosc. 2016;30(3):1184–7. Scholar
  113. 113.
    Lee L, Burke JP, deBeche-Adams T, Nassif G, Martin-Perez B, Monson JR, et al. Transanal minimally invasive surgery for local excision of benign and malignant rectal neoplasia: outcomes from 200 consecutive cases with midterm follow up. Ann Surg. 2017;
  114. 114.
    Hahnloser D, Cantero R, Salgado G, Dindo D, Rega D, Delrio P. Transanal minimal invasive surgery for rectal lesions: should the defect be closed? Color Dis. 2015;17(5):397–402. Scholar
  115. 115.
    Janebdar H, Malik A. Transanal minimally invasive surgery (TAMIS) for excision of rectal carcinoid - video vignette. Color Dis. 2017;
  116. 116.
    McDermott FD, Heeney A, Courtney D, Mohan H, Winter D. Rectal carcinoids: a systematic review. Surg Endosc. 2014;28(7):2020–6. Scholar
  117. 117.
    Ramage JK, Goretzki PE, Manfredi R, Komminoth P, Ferone D, Hyrdel R, et al. Consensus guidelines for the management of patients with digestive neuroendocrine tumours: well-differentiated colon and rectum tumour/carcinoma. Neuroendocrinology. 2008;87(1):31–9. PubMedCrossRefGoogle Scholar
  118. 118.
    Scherubl H, de Mestier L, Cadiot G. Therapy of rectal carcinoids of 11 to 19 mm: a matter of debate. Gastrointest Endosc. 2014;80(3):532–3. Scholar
  119. 119.
    Breukink SO, van der Zaag-Loonen HJ, Bouma EM, Pierie JP, Hoff C, Wiggers T, et al. Prospective evaluation of quality of life and sexual functioning after laparoscopic total mesorectal excision. Dis Colon rectum. 2007;50(2):147–55. PubMedCrossRefGoogle Scholar
  120. 120.
    Bonjer HJ, Deijen CL, Abis GA, Cuesta MA, van der Pas MH, de Lange-de Klerk ES, et al. A randomized trial of laparoscopic versus open surgery for rectal cancer. N Engl J Med. 2015;372(14):1324–32. Scholar
  121. 121.
    Jeong SY, Park JW, Nam BH, Kim S, Kang SB, Lim SB, et al. Open versus laparoscopic surgery for mid-rectal or low-rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): survival outcomes of an open-label, non-inferiority, randomised controlled trial. Lancet Oncol. 2014;15(7):767–74. Scholar
  122. 122.
    Takatsu Y, Fukunaga Y, Nagasaki T, Akiyoshi T, Konishi T, Fujimoto Y, et al. Short- and long-term outcomes of laparoscopic Total mesenteric excision for neuroendocrine tumors of the rectum. Dis Colon rectum. 2017;60(3):284–9. PubMedGoogle Scholar
  123. 123.
    Kim MJ, Park SC, Park JW, Chang HJ, Kim DY, Nam BH, et al. Robot-assisted versus laparoscopic surgery for rectal cancer: a phase II open label prospective randomized controlled trial. Ann Surg. 2017;
  124. 124.
    Frilling A, Li J, Malamutmann E, Schmid KW, Bockisch A, Broelsch CE. Treatment of liver metastases from neuroendocrine tumours in relation to the extent of hepatic disease. Br J Surg. 2009;96(2):175–84. Scholar
  125. 125.
    Glazer ES, Tseng JF, Al-Refaie W, Solorzano CC, Liu P, Willborn KA, et al. Long-term survival after surgical management of neuroendocrine hepatic metastases. HPB (Oxford). 2010;12(6):427–33. Scholar
  126. 126.
    Frilling A, Clift AK. Therapeutic strategies for neuroendocrine liver metastases. Cancer. 2015;121(8):1172–86. Scholar
  127. 127.
    Watzka FM, Fottner C, Miederer M, Schad A, Weber MM, Otto G, et al. Surgical therapy of neuroendocrine neoplasm with hepatic metastasis: patient selection and prognosis. Langenbeck's Arch Surg. 2015;400(3):349–58. Scholar
  128. 128.
    Kandil E, Saeed A, Buell J. Surgical approaches for liver metastases in carcinoid tumors. Gland Surg. 2015;4(5):442–6. PubMedPubMedCentralGoogle Scholar
  129. 129.
    Fairweather M, Swanson R, Wang J, Brais LK, Dutton T, Kulke MH, et al. Management of Neuroendocrine Tumor Liver Metastases: long-term outcomes and prognostic factors from a large prospective database. Ann Surg Oncol. 2017;
  130. 130.
    Conrad C, Ogiso S, Inoue Y, Shivathirthan N, Gayet B. Laparoscopic parenchymal-sparing liver resection of lesions in the central segments: feasible, safe, and effective. Surg Endosc. 2015;29(8):2410–7. Scholar
  131. 131.
    Zorzi D, Laurent A, Pawlik TM, Lauwers GY, Vauthey JN, Abdalla EK. Chemotherapy-associated hepatotoxicity and surgery for colorectal liver metastases. Br J Surg. 2007;94(3):274–86. Scholar
  132. 132.
    Jaeck D, Oussoultzoglou E, Bachellier P, Lemarque P, Weber JC, Nakano H, et al. Hepatic metastases of gastroenteropancreatic neuroendocrine tumors: safe hepatic surgery. World J Surg. 2001;25(6):689–92.PubMedCrossRefGoogle Scholar
  133. 133.
    Kianmanesh R, Sauvanet A, Hentic O, Couvelard A, Levy P, Vilgrain V, et al. Two-step surgery for synchronous bilobar liver metastases from digestive endocrine tumors: a safe approach for radical resection. Ann Surg. 2008;247(4):659–65. Scholar
  134. 134.
    Schnitzbauer AA, Lang SA, Goessmann H, Nadalin S, Baumgart J, Farkas SA, et al. Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling 2-staged extended right hepatic resection in small-for-size settings. Ann Surg. 2012;255(3):405–14. Scholar
  135. 135.
    Kandil E, Noureldine SI, Koffron A, Yao L, Saggi B, Buell JF. Outcomes of laparoscopic and open resection for neuroendocrine liver metastases. Surgery. 2012;152(6):1225–31. Scholar
  136. 136.
    Abu Hilal M, Di Fabio F, Abu Salameh M, Pearce NW. Oncological efficiency analysis of laparoscopic liver resection for primary and metastatic cancer: a single-center UK experience. Arch Surg. 2012;147(1):42–8. Scholar
  137. 137.
    Cipriani F, Rawashdeh M, Stanton L, Armstrong T, Takhar A, Pearce NW, et al. Propensity score-based analysis of outcomes of laparoscopic versus open liver resection for colorectal metastases. Br J Surg. 2016;103(11):1504–12. Scholar
  138. 138.
    Massironi S, Conte D, Sciola V, Pirola L, Paggi S, Fraquelli M, et al. Contrast-enhanced ultrasonography in evaluating hepatic metastases from neuroendocrine tumours. Dig Liver Dis. 2010;42(9):635–41. Scholar
  139. 139.
    Spolverato G, Bagante F, Aldrighetti L, Poultsides GA, Bauer TW, Fields RC, et al. Management and outcomes of patients with recurrent neuroendocrine liver metastasis after curative surgery: an international multi-institutional analysis. J Surg Oncol. 2017;

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of SurgeryUniversity of Lübeck and University Medical Center Schleswig-Holstein, Campus LübeckLübeckGermany
  2. 2.Department of Visceral and General SurgeryUniversity Medical Center FreiburgFreiburgGermany
  3. 3.Section for Preventive Medicine, Department of Nephrology and General MedicineUniversity Medical Center, Albert-Ludwigs-UniversityFreiburgGermany
  4. 4.Department of General, Visceral and Thoracic SurgeryAcademic Teaching Hospital University of HamburgReinbekGermany
  5. 5.Section of Endocrine Surgery, Department of General, Visceral and Thoracic SurgeryAcademic Teaching Hospital University of HamburgReinbekGermany

Personalised recommendations