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Published in: Surgical Endoscopy 10/2017

01-10-2017

Short- and long-term outcomes of laparoscopic organ-sparing resection in pancreatic neuroendocrine tumors: a single-center experience

Authors: Javier A. Cienfuegos, Joseba Salguero, Jorge M. Núñez-Córdoba, Miguel Ruiz-Canela, Alberto Benito, Sira Ocaña, Gabriel Zozaya, Pablo Martí-Cruchaga, Fernando Pardo, José Luis Hernández-Lizoáin, Fernando Rotellar

Published in: Surgical Endoscopy | Issue 10/2017

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Abstract

Background

Laparoscopic organ-sparing pancreatectomy (LOSP) is an ideal therapeutic option in selected cases of pancreatic neuroendocrine tumors (PNETs). Nevertheless, given the low frequency of PNETs, there is scarce evidence regarding short and particularly long-term outcomes of LOSP in this clinical setting.

Methods

All patients with PNETs who underwent surgery (under a LOSP policy) were retrospectively reviewed from a prospective database maintained at our center. Preoperative characteristics, operative data, pathological features and postoperative outcomes were analyzed.

Results

Between December 2003 and December 2015, 36 patients with PNETs underwent laparoscopic resections. Ten were functional tumors, 26 non-functional and 16 were “incidental” cases. The following procedures were performed: one enucleation, eight central pancreatectomies (LCP), one resection of the uncinate process and 26 distal pancreatectomies (DP) (15 of them laparoscopic vessels-preserving). There were no conversions to open surgery, and no drains were routinely left. Mean operative time was 288 min (SD 99). Hospital stay was 6 days. Eighteen patients (50%) experienced some complication of which most were mild (Clavien–Dindo I/II). Three postoperative bleedings occurred: two grade B/one grade C; two required laparoscopic reoperation. Thirteen (36.1%) patients developed peripancreatic fluid collections: two were symptomatic and were managed with transgastric drainage (one presented post-puncture abscesification requiring surgical drainage and splenectomy). Four patients (11%)—one DP and three LCP—developed new-onset pancreatogenic diabetes mellitus (NODM) in the long term. According to the European Neuroendocrine Tumor Society, 19 cases were stage I, seven IIA, two IIIA, one IIIB and seven stage IV. Over a mean follow-up of 51 months, two patients died, one due to recurrence of the tumor and another due to cirrhosis.

Conclusions

The existing different surgical options must be individually considered according to the location and particular characteristics of every tumor. Results from this single-center study document the effectiveness of LOSP in selected cases of PNETs.
Literature
5.
go back to reference Liu TC, Hamilton N, Hawkins W, Gao F, Cao D (2013) Comparison of WHO Classifications (2004, 2010), the Hochwald grading system, and AJCC and ENETS staging systems in predicting prognosis in locoregional well-differentiated pancreatic neuroendocrine tumors. Am J Surg Pathol 37:853–859. doi:10.1097/PAS.0b013e31827fcc18 CrossRefPubMedPubMedCentral Liu TC, Hamilton N, Hawkins W, Gao F, Cao D (2013) Comparison of WHO Classifications (2004, 2010), the Hochwald grading system, and AJCC and ENETS staging systems in predicting prognosis in locoregional well-differentiated pancreatic neuroendocrine tumors. Am J Surg Pathol 37:853–859. doi:10.​1097/​PAS.​0b013e31827fcc18​ CrossRefPubMedPubMedCentral
6.
go back to reference Cherenfant J, Stocker SJ, Gage MK, Du H, Thurow TA, Odeleye M, Schimpke SW, Kaul KL, Hall CR, Lamzabi I, Gattuso P, Winchester DJ, Marsh RW, Roggin KK, Bentrem DJ, Baker MS, Prinz RA, Talamonti MS (2013) Predicting aggressive behavior in nonfunctioning pancreatic neuroendocrine tumors. Surgery 154:783–785. doi:10.1016/j.surg.2013.07.004 Cherenfant J, Stocker SJ, Gage MK, Du H, Thurow TA, Odeleye M, Schimpke SW, Kaul KL, Hall CR, Lamzabi I, Gattuso P, Winchester DJ, Marsh RW, Roggin KK, Bentrem DJ, Baker MS, Prinz RA, Talamonti MS (2013) Predicting aggressive behavior in nonfunctioning pancreatic neuroendocrine tumors. Surgery 154:783–785. doi:10.​1016/​j.​surg.​2013.​07.​004
7.
go back to reference Cherenfant J, Talamonti MS, Hall CR, Thurow TA, Gage MK, Stocker SJ, Lapin B, Wang E, Silverstein JC, Mangold K, Odeleye M, Kaul KL, Lamzabi I, Gattuso P, Winchester DJ, Marsh RW, Roggin KK, Bentrem DJ, Baker MS, Prinz RA (2014) Comparison of tumor markers for predicting outcomes after resection of nonfunctioning pancreatic neuroendocrine tumors. Surgery 156:1501–1504. doi:10.1016/j.surg.2014.08.043 CrossRef Cherenfant J, Talamonti MS, Hall CR, Thurow TA, Gage MK, Stocker SJ, Lapin B, Wang E, Silverstein JC, Mangold K, Odeleye M, Kaul KL, Lamzabi I, Gattuso P, Winchester DJ, Marsh RW, Roggin KK, Bentrem DJ, Baker MS, Prinz RA (2014) Comparison of tumor markers for predicting outcomes after resection of nonfunctioning pancreatic neuroendocrine tumors. Surgery 156:1501–1504. doi:10.​1016/​j.​surg.​2014.​08.​043 CrossRef
10.
go back to reference Venkat R, Edil BH, Schulick RD, Lidor AO, Makary MA, Wolfgang CL (2012) Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg 255:1048–1059. doi:10.1097/SLA.0b013e318251ee09 CrossRefPubMed Venkat R, Edil BH, Schulick RD, Lidor AO, Makary MA, Wolfgang CL (2012) Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg 255:1048–1059. doi:10.​1097/​SLA.​0b013e318251ee09​ CrossRefPubMed
11.
go back to reference Hwang HK, Kang CM, Chung YE, Kim KA, Choi SH, Lee WJ (2013) Robot-assisted spleen-preserving distal pancreatectomy: a single surgeon’s experiences and proposal of clinical application. Surg Endosc 27:774–781. doi:10.1007/s00464-012-2551-6 CrossRefPubMed Hwang HK, Kang CM, Chung YE, Kim KA, Choi SH, Lee WJ (2013) Robot-assisted spleen-preserving distal pancreatectomy: a single surgeon’s experiences and proposal of clinical application. Surg Endosc 27:774–781. doi:10.​1007/​s00464-012-2551-6 CrossRefPubMed
12.
go back to reference Klimstra DS, Modlin IR, Adsay NV, Chetty R, Deshpande V, Gonen M, Jensen RT, Kidd M, Kulke MH, Lloyd RV, Moran C, Moss SF, Oberg K, O’Toole D, Rindi G, Robert ME, Suster S, Tang LH, Tzen CY, Washington MK, Wiedenmann B, Yao J (2010) Pathology reporting of neuroendocrine tumors: application of the Delphic consensus process to the development of a minimum pathology data set. Am J Surg Pathol 34:300–313. doi:10.1097/PAS.0b013e3181ce1447 CrossRefPubMed Klimstra DS, Modlin IR, Adsay NV, Chetty R, Deshpande V, Gonen M, Jensen RT, Kidd M, Kulke MH, Lloyd RV, Moran C, Moss SF, Oberg K, O’Toole D, Rindi G, Robert ME, Suster S, Tang LH, Tzen CY, Washington MK, Wiedenmann B, Yao J (2010) Pathology reporting of neuroendocrine tumors: application of the Delphic consensus process to the development of a minimum pathology data set. Am J Surg Pathol 34:300–313. doi:10.​1097/​PAS.​0b013e3181ce1447​ CrossRefPubMed
14.
go back to reference Kloppel G, Rindi G, Perren A, Komminoth P, Klimstra DS (2010) The ENETS and AJCC/UICC TNM classifications of the neuroendocrine tumors of the gastrointestinal tract and the pancreas: a statement. Virchows Arch 456:595–597. doi:10.1007/s00428-010-0924-6 CrossRefPubMed Kloppel G, Rindi G, Perren A, Komminoth P, Klimstra DS (2010) The ENETS and AJCC/UICC TNM classifications of the neuroendocrine tumors of the gastrointestinal tract and the pancreas: a statement. Virchows Arch 456:595–597. doi:10.​1007/​s00428-010-0924-6 CrossRefPubMed
15.
go back to reference Gagner M, Pomp A (1994) Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc 8:408–410CrossRefPubMed Gagner M, Pomp A (1994) Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc 8:408–410CrossRefPubMed
17.
go back to reference Fernandez-Cruz L, Cosa R, Blanco L, Levi S, Lopez-Boado MA, Navarro S (2007) Curative laparoscopic resection for pancreatic neoplasms: a critical analysis from a single institution. J Gastrointest Surg 11:1602–1607. doi:10.1007/s11605-007-0266-0 CrossRef Fernandez-Cruz L, Cosa R, Blanco L, Levi S, Lopez-Boado MA, Navarro S (2007) Curative laparoscopic resection for pancreatic neoplasms: a critical analysis from a single institution. J Gastrointest Surg 11:1602–1607. doi:10.​1007/​s11605-007-0266-0 CrossRef
18.
go back to reference Fox AM, Pitzul K, Bhojani F, Kaplan M, Moulton CA, Wei AC, McGilvray I, Cleary S, Okrainec A (2012) Comparison of outcomes and costs between laparoscopic distal pancreatectomy and open resection at a single center. Surg Endosc 26:1220–1230. doi:10.1007/s00464-011-2061-y CrossRefPubMed Fox AM, Pitzul K, Bhojani F, Kaplan M, Moulton CA, Wei AC, McGilvray I, Cleary S, Okrainec A (2012) Comparison of outcomes and costs between laparoscopic distal pancreatectomy and open resection at a single center. Surg Endosc 26:1220–1230. doi:10.​1007/​s00464-011-2061-y CrossRefPubMed
20.
go back to reference Nakamura M, Wakabayashi G, Miyasaka Y, Tanaka M, Morikawa T, Unno M, Tajima H, Kumamoto Y, Satoi S, Kwon M, Toyama H, Ku Y, Yoshitomi H, Nara S, Shimada K, Yokoyama T, Miyagawa S, Toyama Y, Yanaga K, Fujii T, Kodera Y, JHBPS SG of JSEPS, Tomiyama Y, Miyata H, Takahara T, Beppu T, Yamaue H, Miyazaki M, Takada T (2015) Multicenter comparative study of laparoscopic and open distal pancreatectomy using propensity score-matching. J Hepatobiliary Pancreat Sci. doi:10.1002/jhbp.268 Nakamura M, Wakabayashi G, Miyasaka Y, Tanaka M, Morikawa T, Unno M, Tajima H, Kumamoto Y, Satoi S, Kwon M, Toyama H, Ku Y, Yoshitomi H, Nara S, Shimada K, Yokoyama T, Miyagawa S, Toyama Y, Yanaga K, Fujii T, Kodera Y, JHBPS SG of JSEPS, Tomiyama Y, Miyata H, Takahara T, Beppu T, Yamaue H, Miyazaki M, Takada T (2015) Multicenter comparative study of laparoscopic and open distal pancreatectomy using propensity score-matching. J Hepatobiliary Pancreat Sci. doi:10.​1002/​jhbp.​268
21.
22.
go back to reference Mehrabi A, Hafezi M, Arvin J, Esmaeilzadeh M, Garoussi C, Emami G, Kossler-Ebs J, Muller-Stich BP, Buchler MW, Hackert T, Diener MK (2015) A systematic review and meta-analysis of laparoscopic versus open distal pancreatectomy for benign and malignant lesions of the pancreas: it’s time to randomize. Surgery 157:45–55. doi:10.1016/j.surg.2014.06.081 CrossRefPubMed Mehrabi A, Hafezi M, Arvin J, Esmaeilzadeh M, Garoussi C, Emami G, Kossler-Ebs J, Muller-Stich BP, Buchler MW, Hackert T, Diener MK (2015) A systematic review and meta-analysis of laparoscopic versus open distal pancreatectomy for benign and malignant lesions of the pancreas: it’s time to randomize. Surgery 157:45–55. doi:10.​1016/​j.​surg.​2014.​06.​081 CrossRefPubMed
23.
go back to reference Nigri GR, Rosman AS, Petrucciani N, Fancellu A, Pisano M, Zorcolo L, Ramacciato G, Melis M (2011) Metaanalysis of trials comparing minimally invasive and open distal pancreatectomies. Surg Endosc 25:1642–1651. doi:10.1007/s00464-010-1456-5 CrossRefPubMed Nigri GR, Rosman AS, Petrucciani N, Fancellu A, Pisano M, Zorcolo L, Ramacciato G, Melis M (2011) Metaanalysis of trials comparing minimally invasive and open distal pancreatectomies. Surg Endosc 25:1642–1651. doi:10.​1007/​s00464-010-1456-5 CrossRefPubMed
25.
go back to reference Drymousis P, Raptis DA, Spalding D, Fernandez-Cruz L, Menon D, Breitenstein S, Davidson B, Frilling A (2014) Laparoscopic versus open pancreas resection for pancreatic neuroendocrine tumours: a systematic review and meta-analysis. HPB (Oxford) 16:397–406. doi:10.1111/hpb.12162 CrossRef Drymousis P, Raptis DA, Spalding D, Fernandez-Cruz L, Menon D, Breitenstein S, Davidson B, Frilling A (2014) Laparoscopic versus open pancreas resection for pancreatic neuroendocrine tumours: a systematic review and meta-analysis. HPB (Oxford) 16:397–406. doi:10.​1111/​hpb.​12162 CrossRef
27.
go back to reference DiNorcia J, Ahmed L, Lee MK, Reavey PL, Yakaitis EA, Lee JA, Schrope BA, Chabot JA, Allendorf JD (2010) Better preservation of endocrine function after central versus distal pancreatectomy for mid-gland lesions. Surgery 148:1246–1247. doi:10.1016/j.surg.2010.09.003 CrossRef DiNorcia J, Ahmed L, Lee MK, Reavey PL, Yakaitis EA, Lee JA, Schrope BA, Chabot JA, Allendorf JD (2010) Better preservation of endocrine function after central versus distal pancreatectomy for mid-gland lesions. Surgery 148:1246–1247. doi:10.​1016/​j.​surg.​2010.​09.​003 CrossRef
31.
34.
go back to reference Rotellar F, Pardo F, Cervera M, Gil A, Valenti V, Pastor C, Cienfuegos JA (2006) Laparoscopic distal pancreatectomy with or without splenectomy. Surgical technique. SurgEndosc 20(Suppl 1):S245 Rotellar F, Pardo F, Cervera M, Gil A, Valenti V, Pastor C, Cienfuegos JA (2006) Laparoscopic distal pancreatectomy with or without splenectomy. Surgical technique. SurgEndosc 20(Suppl 1):S245
35.
go back to reference Rotellar F, Pardo F, Montiel C, Benito A, Regueira FM, Poveda I, Marti-Cruchaga P, Cienfuegos JA (2008) Totally laparoscopic Roux-en-Y duct-to-mucosa pancreaticojejunostomy after middle pancreatectomy: a consecutive nine-case series at a single institution. Ann Surg 247:938–944. doi:10.1097/SLA.0b013e3181724e4a CrossRefPubMed Rotellar F, Pardo F, Montiel C, Benito A, Regueira FM, Poveda I, Marti-Cruchaga P, Cienfuegos JA (2008) Totally laparoscopic Roux-en-Y duct-to-mucosa pancreaticojejunostomy after middle pancreatectomy: a consecutive nine-case series at a single institution. Ann Surg 247:938–944. doi:10.​1097/​SLA.​0b013e3181724e4a​ CrossRefPubMed
36.
go back to reference Rotellar F, Pardo F, Benito A, Marti-Cruchaga P, Zozaya G, Cienfuegos JA (2011) Laparoscopic resection of the uncinate process of the pancreas: the inframesocolic approach and hanging maneuver of the mesenteric root. Surg Endosc 25:3426–3427. doi:10.1007/s00464-011-1740-z CrossRefPubMed Rotellar F, Pardo F, Benito A, Marti-Cruchaga P, Zozaya G, Cienfuegos JA (2011) Laparoscopic resection of the uncinate process of the pancreas: the inframesocolic approach and hanging maneuver of the mesenteric root. Surg Endosc 25:3426–3427. doi:10.​1007/​s00464-011-1740-z CrossRefPubMed
37.
go back to reference Fernández-Cruz L, Cosa R, Blanco L, Levi S, Lopez-Boado MA, Navarro S (2007) Curative laparoscopic resection for pancreatic neoplasms: a critical analysis from a single institution. J Gastrointest Surg 11:1607–1621. doi:10.1007/s11605-007-0266-0 CrossRefPubMed Fernández-Cruz L, Cosa R, Blanco L, Levi S, Lopez-Boado MA, Navarro S (2007) Curative laparoscopic resection for pancreatic neoplasms: a critical analysis from a single institution. J Gastrointest Surg 11:1607–1621. doi:10.​1007/​s11605-007-0266-0 CrossRefPubMed
39.
go back to reference Rindi G, Falconi M, Klersy C, Albarello L, Boninsegna L, Buchler MW, Capella C, Caplin M, Couvelard A, Doglioni C, Delle Fave G, Fischer L, Fusai G, de Herder WW, Jann H, Komminoth P, de Krijger RR, La Rosa S, Luong TV, Pape U, Perren A, Ruszniewski P, Scarpa A, Schmitt A, Solcia E, Wiedenmann B (2012) TNM staging of neoplasms of the endocrine pancreas: results from a large international cohort study. J Natl Cancer Inst 104:764–777. doi:10.1093/jnci/djs208 CrossRefPubMed Rindi G, Falconi M, Klersy C, Albarello L, Boninsegna L, Buchler MW, Capella C, Caplin M, Couvelard A, Doglioni C, Delle Fave G, Fischer L, Fusai G, de Herder WW, Jann H, Komminoth P, de Krijger RR, La Rosa S, Luong TV, Pape U, Perren A, Ruszniewski P, Scarpa A, Schmitt A, Solcia E, Wiedenmann B (2012) TNM staging of neoplasms of the endocrine pancreas: results from a large international cohort study. J Natl Cancer Inst 104:764–777. doi:10.​1093/​jnci/​djs208 CrossRefPubMed
41.
go back to reference Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefPubMedPubMedCentral Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefPubMedPubMedCentral
42.
go back to reference Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M, Definition ISG on PF (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13CrossRefPubMed Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M, Definition ISG on PF (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13CrossRefPubMed
43.
go back to reference Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Yeo CJ, Buchler MW (2007) Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 142:20–25CrossRefPubMed Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Yeo CJ, Buchler MW (2007) Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 142:20–25CrossRefPubMed
44.
go back to reference Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Traverso LW, Yeo CJ, Buchler MW (2007) Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 142:761–768CrossRefPubMed Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Traverso LW, Yeo CJ, Buchler MW (2007) Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 142:761–768CrossRefPubMed
45.
go back to reference Ricci C, Casadei R, Taffurelli G, Campana D, Ambrosini V, Pagano N, Santini D, De Giorgio R, Ingaldi C, Tomassetti P, Zani E, Minni F (2016) Validation of the 2010 WHO classification and a new prognostic proposal: a single centre retrospective study of well-differentiated pancreatic neuroendocrine tumours. Pancreatol Off J Int Assoc Pancreatol. et al Ricci C, Casadei R, Taffurelli G, Campana D, Ambrosini V, Pagano N, Santini D, De Giorgio R, Ingaldi C, Tomassetti P, Zani E, Minni F (2016) Validation of the 2010 WHO classification and a new prognostic proposal: a single centre retrospective study of well-differentiated pancreatic neuroendocrine tumours. Pancreatol Off J Int Assoc Pancreatol. et al
48.
go back to reference Ellison TA, Wolfgang CL, Shi C, Cameron JL, Murakami P, Mun LJ, Singhi AD, Cornish TC, Olino K, Meriden Z, Choti M, Diaz LA, Pawlik TM, Schulick RD, Hruban RH, Edil BH (2014) A single institution’s 26-year experience with nonfunctional pancreatic neuroendocrine tumors: a validation of current staging systems and a new prognostic nomogram. Ann Surg 259:204–212. doi:10.1097/SLA.0b013e31828f3174 CrossRefPubMedPubMedCentral Ellison TA, Wolfgang CL, Shi C, Cameron JL, Murakami P, Mun LJ, Singhi AD, Cornish TC, Olino K, Meriden Z, Choti M, Diaz LA, Pawlik TM, Schulick RD, Hruban RH, Edil BH (2014) A single institution’s 26-year experience with nonfunctional pancreatic neuroendocrine tumors: a validation of current staging systems and a new prognostic nomogram. Ann Surg 259:204–212. doi:10.​1097/​SLA.​0b013e31828f3174​ CrossRefPubMedPubMedCentral
49.
go back to reference Strosberg JR, Cheema A, Weber JM, Ghayouri M, Han G, Hodul PJ, Kvols LK (2012) Relapse-free survival in patients with nonmetastatic, surgically resected pancreatic neuroendocrine tumors: an analysis of the AJCC and ENETS staging classifications. Ann Surg 256:321–325. doi:10.1097/SLA.0b013e31824e6108 CrossRefPubMed Strosberg JR, Cheema A, Weber JM, Ghayouri M, Han G, Hodul PJ, Kvols LK (2012) Relapse-free survival in patients with nonmetastatic, surgically resected pancreatic neuroendocrine tumors: an analysis of the AJCC and ENETS staging classifications. Ann Surg 256:321–325. doi:10.​1097/​SLA.​0b013e31824e6108​ CrossRefPubMed
50.
go back to reference Fischer L, Bergmann F, Schimmack S, Hinz U, Priess S, Muller-Stich BP, Werner J, Hackert T, Buchler MW (2014) Outcome of surgery for pancreatic neuroendocrine neoplasms. Br J Surg. doi:10.1002/bjs.9603 PubMed Fischer L, Bergmann F, Schimmack S, Hinz U, Priess S, Muller-Stich BP, Werner J, Hackert T, Buchler MW (2014) Outcome of surgery for pancreatic neuroendocrine neoplasms. Br J Surg. doi:10.​1002/​bjs.​9603 PubMed
51.
go back to reference Kim MJ, Choi DW, Choi SH, Heo JS, Park HJ, Choi KK, Jang KT, Sung JY (2012) Surgical strategies for non-functioning pancreatic neuroendocrine tumours. Br J Surg 99:1562–1568. doi:10.1002/bjs.8892 CrossRefPubMed Kim MJ, Choi DW, Choi SH, Heo JS, Park HJ, Choi KK, Jang KT, Sung JY (2012) Surgical strategies for non-functioning pancreatic neuroendocrine tumours. Br J Surg 99:1562–1568. doi:10.​1002/​bjs.​8892 CrossRefPubMed
52.
go back to reference Birnbaum DJ, Gaujoux S, Cherif R, Dokmak S, Fuks D, Couvelard A, Vullierme MP, Ronot M, Ruszniewski P, Belghiti J, Sauvanet A (2014) Sporadic nonfunctioning pancreatic neuroendocrine tumors: prognostic significance of incidental diagnosis. Surgery 155:13–21. doi:10.1016/j.surg.2013.08.007 CrossRefPubMed Birnbaum DJ, Gaujoux S, Cherif R, Dokmak S, Fuks D, Couvelard A, Vullierme MP, Ronot M, Ruszniewski P, Belghiti J, Sauvanet A (2014) Sporadic nonfunctioning pancreatic neuroendocrine tumors: prognostic significance of incidental diagnosis. Surgery 155:13–21. doi:10.​1016/​j.​surg.​2013.​08.​007 CrossRefPubMed
53.
go back to reference Hochwald SN, Zee S, Conlon KC, Colleoni R, Louie O, Brennan MF, Klimstra DS (2002) Prognostic factors in pancreatic endocrine neoplasms: an analysis of 136 cases with a proposal for low-grade and intermediate-grade groups. J Clin Oncol 20:2633–2642CrossRefPubMed Hochwald SN, Zee S, Conlon KC, Colleoni R, Louie O, Brennan MF, Klimstra DS (2002) Prognostic factors in pancreatic endocrine neoplasms: an analysis of 136 cases with a proposal for low-grade and intermediate-grade groups. J Clin Oncol 20:2633–2642CrossRefPubMed
55.
go back to reference Pericleous S, Middleton N, McKay SC, Bowers KA, Hutchins RR (2012) Systematic review and meta-analysis of case-matched studies comparing open and laparoscopic distal pancreatectomy: is it a safe procedure? Pancreas 41:993–1000. doi:10.1097/MPA.0b013e31824f3669 CrossRefPubMed Pericleous S, Middleton N, McKay SC, Bowers KA, Hutchins RR (2012) Systematic review and meta-analysis of case-matched studies comparing open and laparoscopic distal pancreatectomy: is it a safe procedure? Pancreas 41:993–1000. doi:10.​1097/​MPA.​0b013e31824f3669​ CrossRefPubMed
58.
go back to reference Strosberg JR, Weber JM, Feldman M, Coppola D, Meredith K, Kvols LK (2013) Prognostic validity of the American Joint Committee on Cancer staging classification for midgut neuroendocrine tumors. J Clin Oncol 31:420–425. doi:10.1200/JCO.2012.44.5924 CrossRefPubMed Strosberg JR, Weber JM, Feldman M, Coppola D, Meredith K, Kvols LK (2013) Prognostic validity of the American Joint Committee on Cancer staging classification for midgut neuroendocrine tumors. J Clin Oncol 31:420–425. doi:10.​1200/​JCO.​2012.​44.​5924 CrossRefPubMed
61.
go back to reference Huttner FJ, Koessler-Ebs J, Hackert T, Ulrich A, Buchler MW, Diener MK (2015) Meta-analysis of surgical outcome after enucleation versus standard resection for pancreatic neoplasms. Br J Surg. doi:10.1002/bjs.9819 Huttner FJ, Koessler-Ebs J, Hackert T, Ulrich A, Buchler MW, Diener MK (2015) Meta-analysis of surgical outcome after enucleation versus standard resection for pancreatic neoplasms. Br J Surg. doi:10.​1002/​bjs.​9819
62.
64.
65.
go back to reference Jain G, Chakravartty S, Patel AG (2013) Spleen-preserving distal pancreatectomy with and without splenic vessel ligation: a systematic review. HPB (Oxford) 15:403–410. doi:10.1111/hpb.12003 CrossRef Jain G, Chakravartty S, Patel AG (2013) Spleen-preserving distal pancreatectomy with and without splenic vessel ligation: a systematic review. HPB (Oxford) 15:403–410. doi:10.​1111/​hpb.​12003 CrossRef
66.
68.
go back to reference Baldwin KM, Katz SC, Espat NJ, Somasundar P (2011) Laparoscopic spleen-preserving distal pancreatectomy in elderly subjects: splenic vessel sacrifice may be associated with a higher rate of splenic infarction. HPB (Oxford) 13:621–625. doi:10.1111/j.1477-2574.2011.00341.x CrossRef Baldwin KM, Katz SC, Espat NJ, Somasundar P (2011) Laparoscopic spleen-preserving distal pancreatectomy in elderly subjects: splenic vessel sacrifice may be associated with a higher rate of splenic infarction. HPB (Oxford) 13:621–625. doi:10.​1111/​j.​1477-2574.​2011.​00341.​x CrossRef
69.
go back to reference Zhou ZQ, Kim SC, Song KB, Park KM, Lee JH, Lee YJ (2014) Laparoscopic spleen-preserving distal pancreatectomy: comparative study of spleen preservation with splenic vessel resection and splenic vessel preservation. World J Surg 38:2973–2979. doi:10.1007/s00268-014-2671-3 CrossRefPubMed Zhou ZQ, Kim SC, Song KB, Park KM, Lee JH, Lee YJ (2014) Laparoscopic spleen-preserving distal pancreatectomy: comparative study of spleen preservation with splenic vessel resection and splenic vessel preservation. World J Surg 38:2973–2979. doi:10.​1007/​s00268-014-2671-3 CrossRefPubMed
70.
go back to reference Mabrut JY, Fernandez-Cruz L, Azagra JS, Bassi C, Delvaux G, Weerts J, Fabre JM, Boulez J, Baulieux J, Peix JL, Gigot JF, Surgery H and PS (HBPS) of the RBS of, (BGES) BG for ES, Coelio C (2005) Laparoscopic pancreatic resection: results of a multicenter European study of 127 patients. Surgery 137:597–605CrossRefPubMed Mabrut JY, Fernandez-Cruz L, Azagra JS, Bassi C, Delvaux G, Weerts J, Fabre JM, Boulez J, Baulieux J, Peix JL, Gigot JF, Surgery H and PS (HBPS) of the RBS of, (BGES) BG for ES, Coelio C (2005) Laparoscopic pancreatic resection: results of a multicenter European study of 127 patients. Surgery 137:597–605CrossRefPubMed
72.
go back to reference Gianduzzo TR, Colombo JR Jr, Haber GP, Magi-Galluzzi C, Dall’Oglio MF, Ulchaker J, Gill IS (2009) KTP laser nerve sparing radical prostatectomy: comparison of ultrasonic and cold scissor dissection on cavernous nerve function. J Urol 181:2760–2766. doi:10.1016/j.juro.2009.01.095 CrossRefPubMed Gianduzzo TR, Colombo JR Jr, Haber GP, Magi-Galluzzi C, Dall’Oglio MF, Ulchaker J, Gill IS (2009) KTP laser nerve sparing radical prostatectomy: comparison of ultrasonic and cold scissor dissection on cavernous nerve function. J Urol 181:2760–2766. doi:10.​1016/​j.​juro.​2009.​01.​095 CrossRefPubMed
73.
go back to reference Yoon YS, Lee KH, Han HS, Cho JY, Ahn KS (2009) Patency of splenic vessels after laparoscopic spleen and splenic vessel-preserving distal pancreatectomy. Br J Surg 96:633–640. doi:10.1002/bjs.6609 CrossRefPubMed Yoon YS, Lee KH, Han HS, Cho JY, Ahn KS (2009) Patency of splenic vessels after laparoscopic spleen and splenic vessel-preserving distal pancreatectomy. Br J Surg 96:633–640. doi:10.​1002/​bjs.​6609 CrossRefPubMed
74.
go back to reference Fendrich V, Merz MK, Waldmann J, Langer P, Heverhagen AE, Dietzel K, Bartsch DK (2011) Neuroendocrine pancreatic tumors are risk factors for pancreatic fistula after pancreatic surgery. Dig Surg 28:263–269. doi:10.1159/000328667 CrossRefPubMed Fendrich V, Merz MK, Waldmann J, Langer P, Heverhagen AE, Dietzel K, Bartsch DK (2011) Neuroendocrine pancreatic tumors are risk factors for pancreatic fistula after pancreatic surgery. Dig Surg 28:263–269. doi:10.​1159/​000328667 CrossRefPubMed
75.
go back to reference Heeger K, Falconi M, Partelli S, Waldmann J, Crippa S, Fendrich V, Bartsch DK (2014) Increased rate of clinically relevant pancreatic fistula after deep enucleation of small pancreatic tumors. Langenbecks Arch Surg 399:315–321. doi:10.1007/s00423-014-1171-0 CrossRefPubMed Heeger K, Falconi M, Partelli S, Waldmann J, Crippa S, Fendrich V, Bartsch DK (2014) Increased rate of clinically relevant pancreatic fistula after deep enucleation of small pancreatic tumors. Langenbecks Arch Surg 399:315–321. doi:10.​1007/​s00423-014-1171-0 CrossRefPubMed
76.
go back to reference Atema JJ, Jilesen AP, Busch OR, van Gulik TM, Gouma DJ, Nieveen van Dijkum EJ (2015) Pancreatic fistulae after pancreatic resections for neuroendocrine tumours compared with resections for other lesions. HPB (Oxford) 17:38–45. doi:10.1111/hpb.12319 CrossRef Atema JJ, Jilesen AP, Busch OR, van Gulik TM, Gouma DJ, Nieveen van Dijkum EJ (2015) Pancreatic fistulae after pancreatic resections for neuroendocrine tumours compared with resections for other lesions. HPB (Oxford) 17:38–45. doi:10.​1111/​hpb.​12319 CrossRef
77.
79.
go back to reference Tosoian JJ, Hicks CW, Cameron JL, Valero V 3rd, Eckhauser FE, Hirose K, Makary MA, Pawlik TM, Ahuja N, Weiss MJ, Wolfgang CL (2015) Tracking early readmission after pancreatectomy to index and nonindex institutions: a more accurate assessment of readmission. JAMA Surg 150:152–158. doi:10.1001/jamasurg.2014.2346 CrossRefPubMedPubMedCentral Tosoian JJ, Hicks CW, Cameron JL, Valero V 3rd, Eckhauser FE, Hirose K, Makary MA, Pawlik TM, Ahuja N, Weiss MJ, Wolfgang CL (2015) Tracking early readmission after pancreatectomy to index and nonindex institutions: a more accurate assessment of readmission. JAMA Surg 150:152–158. doi:10.​1001/​jamasurg.​2014.​2346 CrossRefPubMedPubMedCentral
80.
go back to reference Strobel O, Cherrez A, Hinz U, Mayer P, Kaiser J, Fritz S, Schneider L, Klauss M, Buchler MW, Hackert T (2015) Risk of pancreatic fistula after enucleation of pancreatic tumours. Br J Surg. doi:10.1002/bjs.9843 PubMed Strobel O, Cherrez A, Hinz U, Mayer P, Kaiser J, Fritz S, Schneider L, Klauss M, Buchler MW, Hackert T (2015) Risk of pancreatic fistula after enucleation of pancreatic tumours. Br J Surg. doi:10.​1002/​bjs.​9843 PubMed
81.
go back to reference Tjaden C, Hinz U, Hassenpflug M, Fritz F, Fritz S, Grenacher L, Buchler MW, Hackert T (2016) Fluid collection after distal pancreatectomy: a frequent finding. HPB (Oxford) 18:35–40CrossRef Tjaden C, Hinz U, Hassenpflug M, Fritz F, Fritz S, Grenacher L, Buchler MW, Hackert T (2016) Fluid collection after distal pancreatectomy: a frequent finding. HPB (Oxford) 18:35–40CrossRef
85.
go back to reference Fernandez-Cruz L, Jimenez Chavarria E, Taura P, Closa D, Boado MA, Ferrer J (2013) Prospective randomized trial of the effect of octreotide on pancreatic juice output after pancreaticoduodenectomy in relation to histological diagnosis, duct size and leakage. HPB (Oxford) 15:392–399. doi:10.1111/j.1477-2574.2012.00608.x CrossRef Fernandez-Cruz L, Jimenez Chavarria E, Taura P, Closa D, Boado MA, Ferrer J (2013) Prospective randomized trial of the effect of octreotide on pancreatic juice output after pancreaticoduodenectomy in relation to histological diagnosis, duct size and leakage. HPB (Oxford) 15:392–399. doi:10.​1111/​j.​1477-2574.​2012.​00608.​x CrossRef
86.
go back to reference Alghamdi AA, Jawas AM, Hart RS (2007) Use of octreotide for the prevention of pancreatic fistula after elective pancreatic surgery: a systematic review and meta-analysis. Can J surgeryJournal Can Chir 50:459–466 Alghamdi AA, Jawas AM, Hart RS (2007) Use of octreotide for the prevention of pancreatic fistula after elective pancreatic surgery: a systematic review and meta-analysis. Can J surgeryJournal Can Chir 50:459–466
87.
go back to reference Li-Ling J, Irving M (2001) Somatostatin and octreotide in the prevention of postoperative pancreatic complications and the treatment of enterocutaneous pancreatic fistulas: a systematic review of randomized controlled trials. Br J Surg 88:190–199CrossRefPubMed Li-Ling J, Irving M (2001) Somatostatin and octreotide in the prevention of postoperative pancreatic complications and the treatment of enterocutaneous pancreatic fistulas: a systematic review of randomized controlled trials. Br J Surg 88:190–199CrossRefPubMed
89.
go back to reference Lillemoe KD, Kaushal S, Cameron JL, Sohn TA, Pitt HA, Yeo CJ (1999) Distal pancreatectomy: indications and outcomes in 235 patients. Ann Surg 229:693–700CrossRefPubMedPubMedCentral Lillemoe KD, Kaushal S, Cameron JL, Sohn TA, Pitt HA, Yeo CJ (1999) Distal pancreatectomy: indications and outcomes in 235 patients. Ann Surg 229:693–700CrossRefPubMedPubMedCentral
92.
go back to reference Dumitrascu T, Scarlat A, Ionescu M, Popescu I (2012) Central pancreatectomy versus spleen-preserving distal pancreatectomy: a comparative analysis of early and late postoperative outcomes. Dig Surg 29:400–407. doi:10.1159/000343927 CrossRefPubMed Dumitrascu T, Scarlat A, Ionescu M, Popescu I (2012) Central pancreatectomy versus spleen-preserving distal pancreatectomy: a comparative analysis of early and late postoperative outcomes. Dig Surg 29:400–407. doi:10.​1159/​000343927 CrossRefPubMed
95.
go back to reference Menge BA, Tannapfel A, Belyaev O, Drescher R, Muller C, Uhl W, Schmidt WE, Meier JJ (2008) Partial pancreatectomy in adult humans does not provoke beta-cell regeneration. Diabetes 57:142–149. doi:10.2337/db07-1294 CrossRefPubMed Menge BA, Tannapfel A, Belyaev O, Drescher R, Muller C, Uhl W, Schmidt WE, Meier JJ (2008) Partial pancreatectomy in adult humans does not provoke beta-cell regeneration. Diabetes 57:142–149. doi:10.​2337/​db07-1294 CrossRefPubMed
Metadata
Title
Short- and long-term outcomes of laparoscopic organ-sparing resection in pancreatic neuroendocrine tumors: a single-center experience
Authors
Javier A. Cienfuegos
Joseba Salguero
Jorge M. Núñez-Córdoba
Miguel Ruiz-Canela
Alberto Benito
Sira Ocaña
Gabriel Zozaya
Pablo Martí-Cruchaga
Fernando Pardo
José Luis Hernández-Lizoáin
Fernando Rotellar
Publication date
01-10-2017
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 10/2017
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-016-5411-y

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