Skip to main content
SpringerLink
Log in

Open and minimally invasive pancreatic neoplasms enucleation: a systematic review

  • Review Article
  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Pancreatic enucleation (pEN) as parenchyma-sparing procedure for small pancreatic neoplasms is quickly becoming the most common surgical option in such setting. Nowadays, pEN is frequently carried out through a minimally invasive approach either laparoscopic or robotic. Its impact on overall perioperative complications and pancreatic fistula (POPF) is still under evaluation. The scope of our systematic review is to assess pEN’s perioperative outcomes and to evaluate the effect of the minimally invasive techniques over POPF and other surgical complications.

Methods

We performed a systematic literature search (time-frame January 1999–September 2018), considering exclusively those studies which included at least 5 cases of either open or minimally invasive pEN. Data regarding postoperative outcome and POPF were extracted and analyzed. We defined postoperative morbidities by the Clavien–Dindo classification while POPF according to the International Study Group of Pancreatic Fistula (ISGPF) definition.

Results

Sixty-three studies met the criteria selected, accounting for a study population of 2485 patients. 27.7% had a minimally invasive pEN. The overall postoperative morbidity rate was 46.1% with 11.9% rated as severe (Clavien–Dindo ≥ 3). Mortality rate was 0.69%. The minimally invasive approach to pEN led to a statistically significant reduction of both the overall POPF rate (28.7% vs. 45.9%, p < 0.001), and clinically significant B-C POPF (p < 0.027). The postoperative overall morbidity rate was clearly in favor of the minimally invasive approach (27.6% vs. 55.2%, p < 0.001).

Conclusions

Our review confirms that pEN is a safe and feasible technique for the treatment of small benign or low-grade pancreatic neoplasms and it can be implemented with an acceptable morbidity rate along with low mortality. The minimally invasive approach is gaining widespread acceptance due to its supposed non-inferiority compared with the traditional open approach. In our review, it showed to be even better in terms of POPF incidence rate and short-term postoperative outcome. Still, such data need to be corroborated by randomized clinical trials.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Crippa S, Bassi M, Salvia R, Falconi M, Butturini G, Pederzoli P (2007) Enucleation of pancreatic neoplasms. Br J Surg 94:1254–1259

    Article  CAS  PubMed  Google Scholar 

  2. Casadei R, Ricci C, Rega D, D’Ambra M, Pezzilli R, Tomassetti P, Campana D, Nori F, Minni F (2010) Pancreatic endocrine tumors less than 4 cm in diameter: resect or enucleate? A single-center experience. Pancreas 39:825–828

    Article  PubMed  Google Scholar 

  3. Kiely JM, Nakeeb A, Komorowski RA, Wilson SD, Pitt HA (2003) Cystic pancreatic neoplasms: enucleate or resect? J Gastrointest Surg 7:890–897

    Article  PubMed  Google Scholar 

  4. Talamini MA, Moesinger R, Yeo CJ, Poulose B, Hruban RH, Cameron JL, Pitt HA (1998) Cystadenomas of the pancreas: is enucleation an adequate operation? Ann Surg 227:896–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Nikfarjam M, Warshaw AL, Axelrod L, Deshpande V, Thayer SP, Ferrone CR, Fernandez-del Castillo C (2008) Improved contemporary surgical management of insulinomas. A 24-year experience at the Massachusetts General Hospital. Ann Surg 247:165–172

    Article  PubMed  PubMed Central  Google Scholar 

  6. Falconi M, Mantovani W, Crippa S, Mascetta G, Salvia R, Pederzoli P (2008) Pancreatic insufficiency after different resections for benign tumors. Br J Surg 95:85–91

    Article  CAS  PubMed  Google Scholar 

  7. Madan AK, Weldon CB, Long WP, Raafat JD (2004) Solid and papillary epithelial neoplasm of the pancreas. J Surg Oncol 15:193–198

    Article  Google Scholar 

  8. Sciaudone G, Perniceni T, Levy P, Bougaran J, Gayet B (2000) Enucleation of intraductal papillary-mucinous tumor of the head of the pancreas. Gastroenterol Clin Biol 24:17–20

    Google Scholar 

  9. Hackert T, Hinz U, Fritz S, Strobel O, Schneider L, Hartwig W, Büchler MW, Werner J (2011) Enucleation in pancreatic surgery: indications, technique, and outcome compared to standard pancreatic resections. Langenbecks Arch Surg 396:1197–1203

    Article  PubMed  Google Scholar 

  10. Kahl S, Malfertheiner P (2004) Exocrine and endocrine pancreatic insufficiency after pancreatic surgery. Best Pract Res Clin Gastroenterol 18:947–955

    Article  PubMed  Google Scholar 

  11. Pitt SC, Pitt HA, Baker MS, Christians K, Touzios JG, Kiely JM, Weber SM, Wilson SD, Howard TJ, Talamonti MS, Rikkers LF (2009) Small pancreatic and periampullary neuroendocrine tumors: resect or enucleate? J Gastrointest Surg 13:1692–1698

    Article  PubMed  PubMed Central  Google Scholar 

  12. Lillemoe KD, Kaushal S, Cameron JL, Sohn TA, Pitt HA, Yeo CH (1999) Distal pancreatectomy: indications and outcomes in 235 patients. Ann Surg 229:693–700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Mabrut JY, Boulez J, Peix JL, Gigot JF, Gouillat C, De La Roche E, Adham M, Ducerf C, Baulieux J (2003) Laparoscopic pancreatic resection. Ann Chir 128:425–432

    Article  PubMed  Google Scholar 

  14. Kuroki T, Eguchi S (2014) Laparoscopic parenchyma-sparing pancreatectomy. J Hepatobiliary Pancreat Sci 21:323–327

    Article  PubMed  Google Scholar 

  15. Crippa S, Zerbi A, Boninsegna L, Capitanio V, Partelli S, Balzano G, Pederzoli P, Di Carlo V, Falconi M (2012) Surgical management of insulinomas. Arch Surg 147:261–266

    Article  PubMed  Google Scholar 

  16. 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. Langebecks Arch Surg 399:315–321

    Article  Google Scholar 

  17. Faitot F, Gaujoux S, Barber L, Novaes M, Dokmak S, Aussilhou B, Couvelard A, Rebours V, Ruszniewski P, Belghiti J, Sauvanet A (2015) Reappraisal of pancreatic enucleations: a single-center experience of 126 procedures. Surgery 158:201–210

    Article  PubMed  Google Scholar 

  18. 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 tumors. BJS 102:1258–1266

    Article  CAS  Google Scholar 

  19. Wolk S, Distler M, Kerstin S, Weitz J, Saeger HD, Grutzmann R (2015) Evaluation of central pancreatectomy and pancreatic enucleation as a pancreatic resections—a comparison. Int J Surg 22:118–124

    Article  PubMed  Google Scholar 

  20. Xiao Z, Luo G, Liu Z, Jin K, Xu J, Liu C, Liu L, Ni Q, Long J, Yu X (2016) Roux en Y pancreaticojejunostomy reconstruction after deep enucleation of benign or borderline pancreatic lesions: a single-institution experience. HPB 18:145–152

    Article  PubMed  Google Scholar 

  21. Kaiser J, Fritz S, Klauss M, Bergmann F, Hinz U, Strobel O, Schneider L, Buchler MW, Hackert T (2016) Enucleation: a treatment alternative for branch duct intraductal papillary mucinous neoplasms. Surgery 161:602–610

    Article  PubMed  Google Scholar 

  22. Ayav A, Bresler L, Brunaud L, Boissel P (2005) Laparoscopic approach for solitary insulinoma: a multicentre study Langebecks. Arch Surg 390:134–140

    Article  CAS  Google Scholar 

  23. Ardbuckle JD, Kekis PB, Lim A, Jackson JE, Todd JF, Lynn J, Isla A (2009) Laparoscopic management of insulinomas. Br J Surg 96:185–190

    Article  Google Scholar 

  24. 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 11:1607–1622

    Article  PubMed  Google Scholar 

  25. Sa Cunha A, Beau C, Rault A, Catargi B, Collet D, Masson B (2007) Laparoscopic versus open approach for solitary insulinoma. Surg Endosc 21:103–108

    Article  PubMed  Google Scholar 

  26. Sweet MP, Izumisato Y, Way LW, Clark OH, Masharani U, Duh QY (2007) Laparoscopic enucleation of insulinomas. Arch Surg 142:1202–1204

    Article  PubMed  Google Scholar 

  27. Luo Y, Liu R, Hu MG, Mu YM, An LC, Huang ZQ (2009) Laparoscopic strategy for pancreatic insulinomas: a single-institution experience of 29 cases. J Gastrointest Surg 13:945–950

    Article  PubMed  Google Scholar 

  28. Fernandez-Cruz L, Molina V, Vallejos R, Jimenez Chavarria E, Lopez-Boaldo MA, Ferrer J (2012) Outcome after laparoscopic enucleation for non-functional neuroendocrine pancreatic tumors. HPB 14:171–176

    Article  PubMed  PubMed Central  Google Scholar 

  29. Costi R, Randone B, Mal F, Basato S, Levard H, Gayet B (2013) A critical appraisal of laparoscopic pancreatic enucleations: right-sided procedures (pancreatic head, uncus) are not mini-invasive surgery. Surg Laparosc Endosc Percutan Tech 23:524–531

    Article  PubMed  Google Scholar 

  30. Choi KS, Chung JC, Kim HC (2014) Feasibility and outcomes of laparoscopic enucleation for pancreatic neoplasms. Ann Surg Treat Res 87:285–289

    Article  PubMed  PubMed Central  Google Scholar 

  31. Haugvik SP, Pavlik Marangos I, Rosok BI, Pomianwska E, Gladhaug IP, Mathiasen O, Edwin B (2013) Long-term outcome of laparoscopic surgery for pancreatic neuroendocrine tumors. World J Surg 37:582–590

    Article  PubMed  Google Scholar 

  32. Thomas E, Matsuoka L, Alexopoulos S, Selby R, Parekh D (2015) Laparoscopic hand-assisted parenchymal sparing resections for presumed side-branch intraductal papillary mucinous neoplasms. J Laparosc Adv Surg Tech 25:668–671

    Article  Google Scholar 

  33. Boggi U, Napoli N, Costa F, Kauffmann EF, Menonna F, Iacopi S, Vistoli F, Amorese G (2016) Robotic assisted pancreatic resections. Word J Surg 40:2497–2506

    Article  Google Scholar 

  34. Sahakyan MA, Rosok BI, Kazaryan AM, Barkhatov L, Haugvik SP, Fretland AA, Ignjatovic D, Labori KJ, Edwin B (2017) Role of laparoscopic enucleation in the treatment of pancreatic lesions: case series and case-matched analysis. Surg Endosc 31:2310–2316

    Article  PubMed  Google Scholar 

  35. Tian F, Hong XF, Wu WM, Han XL, Wang MY, Cong L, Dai MH, Liao Q, Zhang TP, Zhao YP (2016) Propensity score-matched analysis of robotic versus open surgical enucleation for small pancreatic neuroendocrine tumors. Br J Surg 103:1358–1364

    Article  CAS  PubMed  Google Scholar 

  36. Song KB, Kim SC, Hwang DW, Lee JH, Lee DJ, Lee JW, Jun ES, Sin SH, Kim HE, Park KM, Lee YJ (2015) Enucleation for benign or low-grade malignant lesions of the pancreas: single-center experience with 65 consecutive patients. Surgery 158:1203–1210

    Article  PubMed  Google Scholar 

  37. Jin JB, Qin K, Li H, Wu ZC, Zhan Q, Deng XX, Chen H, Shen BY, Peng CB, Li HW (2016) Robotic enucleation for benign or bordeline tumors of the pancreas: a retrospective analysis and comparison from an high-volume center in Asia. World J Surg 40:3009–3020

    Article  PubMed  Google Scholar 

  38. Di Benedetto F, Magistri P, Ballarin R, Tarantino G, Bartolini I, Bencini L, Moraldi L, Annecchiarico M, Guerra F, Coratti A (2018) Ultrasound-guided robotic enucleation of pancreatic neuroendocrine tumors. Surg Innov 26:37–45. https://doi.org/10.1177/1553350618790711

    Article  PubMed  Google Scholar 

  39. Balzano G, Zerbi A, Veronesi P, Cristallo M, Di Carlo V (2003) Surgical treatment of benign and borderline neoplasms of the pancreatic body. Dig Surg 20:506–510

    Article  CAS  PubMed  Google Scholar 

  40. Fernandez-Cruz L, Pardo F, Cugat E, Artigas V, Olsina J, Rotellar F, Carrillo A, Diaz H, Targarona E, Miras M, Morales-Conde S, Morales-Mendes S, Pereira F, Calafell J (2006) Analisis del registro nacional espanol de la cirurgia laparoscopica del pancreas. Cir Esp 79:293–298

    Article  PubMed  Google Scholar 

  41. Casanova D, Polavieja MG, Naranjo A, Pardo F, Rotellar F, Gonzalez F, Luzuriaga C, Regano S, Freijanes J (2007) Surgical treatment of persistent hyperinsulinemic hypoglicemia (PHH) (insulinomas and nesidioblastosis). Langenbecks Arch Surg 392:663–670

    Article  PubMed  Google Scholar 

  42. Liu H, Peng C, Zhang S, Wu Y, Fang H, Sheng H, Peng S (2007) Strategy for the surgical management of insulinomas: analysis of 52 cases. Dig Surg 24:463–470

    Article  CAS  PubMed  Google Scholar 

  43. Hu M, Zhao G, Luo Y, Liu R (2011) Laparoscopic versus open treatment for benign pancreatic insulinomas: an analysis of 89 cases. Surg Endosc 25:2821–3837

    Article  Google Scholar 

  44. Tsang YP, Lang BHH, Shek TWH (2016) Assessing the short and long-term outcomes after resection of benign insulinoma. ANZ J Surg 86:706–710

    Article  PubMed  Google Scholar 

  45. Jilesen APJ, van Eijck CHJ, Busch ORC, van Gulik TM, Gouma DJ, van Dijkum EJMN (2016) Postoperative outcomes of enucleation and standard resections in patients with a pancreatic neuroendocrine tumor. World J Surg 40:715–728

    Article  PubMed  Google Scholar 

  46. Wei J, Liu X, Wu J, Xu W, Gao W, Jiang K, Zhang Z, Miao Y (2016) Diagnosis and surgical management of insulinomas in 33 consecutive patients at a single institution. Langenbecks Arch Surg 401:1019–1025

    Article  PubMed  Google Scholar 

  47. Uccelli F, Gavazzi F, Capretti G, Virdis M, Montorsi M, Zerbi A (2016) Parenchyma-sparing surgery for pancreatic endocrine tumors. Updates Surg 68:313–319

    Article  PubMed  Google Scholar 

  48. Turrini O, Schmidt CM, Pitt HA, Guiramand J, Aguilar-Saavedra JR, Aboudi S, Lillemoe KD, Delpero JR (2011) Side-branch intra-ductal papillary mucinous neoplasms of the pancreatic head/uncinate: resection or enucleation? HPB (Oxford) 13:126–131

    Article  Google Scholar 

  49. Blanc B, Sauvanet A, Couvelard A, Pessaux P, Dokmak S, Vullierme MP, Lévy P, Ruszniewski P, Belghiti J (2008) Limited pancreatic resections for intraductal papillary mucinous neoplasm. J Chir 145:568–578

    Article  CAS  Google Scholar 

  50. Falconi M, Zerbi A, Crippa S, Balzano G, Boninsegna L, Capitanio V, Bassi C, Di Carlo V, Pederzoli P (2010) Parenchyma-preserving resections for small non-functioning pancreatic endocrine tumors. Ann Surg Oncol 17:1621–1627

    Article  PubMed  Google Scholar 

  51. Pulvirenti A, Marchegiani G, Pea A, Allegrini V, Esposito A, Casetti L, Landoni L, Malleo G, Salvia R, Bassi C (2018) Clinical implications of the 2016 International Study Group on pancreatic surgery definition and grading of postoperative pancreatic fistula on 775 consecutive pancreatic resections. Ann Surg 268:1069–1075

    Article  PubMed  Google Scholar 

  52. Wang X, Tan CL, Zhang H, Chen YH, Yang M, Ke NW, Liu XB (2018) Short-term outcomes and risk factors for pancreatic fistula after pancreatic enucleation: a single-center experience of 142 patients. J Surg Oncol 117:182–190

    Article  CAS  PubMed  Google Scholar 

  53. Correa-Gallego C, Brennan MF, D’Angelica M, Fong Y, Dematteo RP, Kingham TP, Jarnagin WR, Allen PJ (2013) Operative drainage following pancreatic resection: analysis of 1122 patients resected over 5 years at a single institution. Ann Surg 258:1051–1058

    Article  PubMed  PubMed Central  Google Scholar 

  54. Diener MK, Seiler CM, Rossion I, Kleeff J, Glanemann M, Butturini G, Tomazic A, Bruns CJ, Busch OR, Farkas S, Belyaev O, Neoptolemos JP, Halloran C, Keck T, Niedergethmann M, Gellert K, Witzigmann H, Kollmar O, Langer P, Steger U, Neudecker J, Berrevoet F, Ganzera S, Heiss MM, Luntz SP, Bruckner T, Kieser M, Büchler MW (2011) Efficacy of stapler versus hand-sewn closure after distal pancreatectomy (DISPACT): a randomised, controlled multicentre trial. Lancet 377:1514–1522

    Article  PubMed  Google Scholar 

  55. Van Buren G 2nd, Bloomston M, Hughes SJ, Winter J, Behrman SW, Zyromski NJ, Vollmer C, Velanovich V, Riall T, Muscarella P, Trevino J, Nakeeb A, Schmidt CM, Behrns K, Ellison EC, Barakat O, Perry KA, Drebin J, House M, Abdel-Misih S, Silberfein EJ, Goldin S, Brown K, Mohammed S, Hodges SE, McElhany A, Issazadeh M, Jo E, Mo Q, Fisher WE (2014) A randomized prospective multicenter trial of pancreaticoduodenectomy with and without routine intraperitoneal drainage. Ann Surg 259:605–612

    Article  PubMed  Google Scholar 

  56. Chua TC, Yang TX, Gill JA, Samra JS (2016) Systematic review and meta-analysis of enucleation versus standardized resection for small pancreatic lesions. Ann Surg Oncol 23:592–599

    Article  PubMed  Google Scholar 

  57. Duconseil P, Marchese U, Ewald J, Giovannini M, Mokart D, Delpero JR, Turrini O (2018) A pancreatic zone at higher risk of fistula after enucleation. World J Surg Oncol. https://doi.org/10.1186/s12957-018-1476-5

    Article  PubMed  PubMed Central  Google Scholar 

  58. Harnoss JC, Ulrich AB, Harnoss JM, Diener MK, Buchler MW, Welsch T (2014) Use and results of consensus definitions in pancreatic surgery: a systematic review. Surgery 155:47–57

    Article  PubMed  Google Scholar 

  59. Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hilal M, Adham M, Allen P, Andersson R, Asbun HJ, Besselink MG, Conlon K, Del Chiaro M, Falconi M, Fernandez-Cruz L, Fernandez-Del Castillo C, Fingerhut A, Friess H, Gouma DJ, Hackert T, Izbicki J, Lillemoe KD, Neoptolemos JP, Olah A, Schulick R, Shrikhande SV, Takada T, Takaori K, Traverso W, Vollmer CR, Wolfgang CL, Yeo CJ, Salvia R, Buchler M, International Study Group on Pancreatic Surgery (ISGPS) (2017) The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery 161:584–591

    Article  PubMed  Google Scholar 

  60. Inchauste SM, Lanier BJ, Libutti SK, Phan GQ, Nilubol N, Steinberg SM, Kebebew E, Hughes MS (2012) Rate of clinically significant postoperative pancreatic fistula in pancreatic neuroendocrine tumors. World J Surg 36:1517–1526

    Article  PubMed  PubMed Central  Google Scholar 

  61. Beger HG, Siech M, Poch B, Mayer B, Schoenberg MH (2015) Limited surgery for benign tumors of the pancreas: a systematic review. World J Surg 39:1557–1566

    Article  CAS  PubMed  Google Scholar 

  62. Hüttner FJ, Koessler-Ebs J, Hackert T, Ulrich A, Büchler MW, Diener MK (2015) Meta-analysis of surgical outcome after enucleation versus standard resection for pancreatic neoplasms. Br J Surg 102:1026–1036

    Article  PubMed  Google Scholar 

  63. Zhang RC, Zhou YC, Mou YP, Huang CJ, Jin WW, Yan JF, Wang YX, Liao Y (2016) Laparoscopic versus open enucleation for pancreatic neoplasms: clinical outcomes and pancreatic function analysis. Surg Endosc 30:2657–2665

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of General Surgery, Hepato-pancreato-biliary Unit, Department of Medicine and Surgery, Parma University Hospital, Via Linati 6, 43121, Parma, Italy

    Raffaele Dalla Valle, Elena Cremaschi, Laura Lamecchi & Maurizio Iaria

  2. Department of Surgery, Poliambulanza Foundation, Brescia, Italy

    Francesca Guerini & Edoardo Rosso

Authors
  1. Raffaele Dalla Valle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena Cremaschi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura Lamecchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francesca Guerini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Edoardo Rosso
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maurizio Iaria
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maurizio Iaria.

Ethics declarations

Disclosures

Raffaele Dalla Valle, Elena Cremaschi, Laura Lamecchi, Francesca Guerini, Edoardo Rosso, and Maurizio Iaria have no conflict of interest or financial ties to disclose.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dalla Valle, R., Cremaschi, E., Lamecchi, L. et al. Open and minimally invasive pancreatic neoplasms enucleation: a systematic review. Surg Endosc 33, 3192–3199 (2019). https://doi.org/10.1007/s00464-019-06967-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-019-06967-9

Keywords

Search

Navigation