Skip to main content

Advertisement

SpringerLink
Log in

Surgery for Adrenocortical Carcinoma: Do We Have Enough Evidence to Perform Robotic Approach? A Systematic Review

  • Review Article
  • Published:
Indian Journal of Surgery Aims and scope Submit manuscript

Abstract

Surgery is the treatment of choice for adrenocortical carcinoma (stage I–III). In recent years, many authors demonstrated the safety and feasibility of minimally invasive approaches when applied to highly selected cases. The aim of the present study is to provide an overview about technical details and surgical and oncological outcomes of robotic approach compared to traditional open or laparoscopic surgery in patients with adrenocortical carcinoma. A literature search, according to the PRISMA guidelines, was performed via PubMed, Scopus, and Cochrane Library. The search thread was robotic adrenalectomy, minimally invasive surgery, and adrenocortical carcinoma. Only studies involving patients with adrenocortical carcinoma comparing robotic approach with laparoscopic and open adrenalectomy and reporting relevant clinical outcomes were included. Among all reports identified, only three studies matching the inclusion criteria were finally selected for the analysis. All of them were retrospective and demonstrated the superiority of robotic approach over laparoscopy for adrenocortical carcinoma as regards open conversion rate with no significant differences in terms of length of stay, readmissions, and 90-day mortality. A study reported significantly higher odds of positive margins for laparoscopic adrenalectomy that seems to be associated with significantly shorter overall survival. The most relevant reports strictly concerning the robotic approach to adrenocortical carcinoma revealed the safety and feasibility of robotic surgery with better outcomes in terms of open conversion rate and negative resection margins that are powerful predictors for overall survival. Multicenter case series analysis is still needed to confirm the real advantages of robotic approach in the treatment of adrenocortical carcinoma.

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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Shariq OA, McKenzie TJ (2021) Adrenocortical carcinoma: current state of the art, ongoing controversies, and future directions in diagnosis and treatment. Ther Adv Chronic Dis 12:20406223211033104

    Article  PubMed  PubMed Central  Google Scholar 

  2. Wajchenberg BL, Albergaria Pereira MA, Medonca BB, Latronico AC, Campos Carneiro P, Alves VA et al (2000) Adrenocortical carcinoma: clinical and laboratory observations. Cancer 88:711–736

    Article  CAS  PubMed  Google Scholar 

  3. Kerkhofs TM, Verhoeven RH, Van der Zwan JM, Dieleman J, Kerstens MN et al (2013) Adrenocortical carcinoma: a population-based study on incidence and survival in the Netherlands since 1993. Eur J Cancer 49:2579–2586

    Article  PubMed  Google Scholar 

  4. Sharma E, Dahal S, Sharma P, Bhandari A, Gupta V, Amgai B et al (2018) The characteristics and trends in adrenocortical carcinoma: a United States population based study. J Clin Med Res 10:636–640

    Article  PubMed  PubMed Central  Google Scholar 

  5. Lughezzani G, Sun M, Perrotte P, Jeldres C, Alasker A, Isbarn H et al (2010) The European Network for the Study of Adrenal Tumors staging system is prognostically superior to the international union against cancer-staging system: a North American validation. Eur J Cancer 46:713–719

    Article  PubMed  Google Scholar 

  6. Miller BS, Gauger PG, Hammer GD, Giordano TJ, Doherty GM (2010) Proposal for modification of the ENSAT staging system for adrenocortical carcinoma using tumor grade. Langenbecks Arch Surg 395:955–961

    Article  PubMed  Google Scholar 

  7. Cavallaro G, Tarallo M, Chiappini A, Crocetti D, Polistena A, Petramala L et al (2021) Surgical management of adrenocortical carcinoma: current highlights. Biomedicines 9:909

    Article  PubMed  PubMed Central  Google Scholar 

  8. Gaujoux S, Mihai R, Carnaille B, Dousset B, Fiori C, Porpiglia F et al (2017) European Society of Endocrine Surgeons (ESES) and European Network for the Study of Adrenal Tumours (ENSAT) recommendations for the surgical management of adrenocortical carcinoma. Br J Surg 104:358–376

    Article  CAS  PubMed  Google Scholar 

  9. Gagner M, Lacroix A, Bolté E (1992) Laparoscopic adrenalectomy in Cushing’s syndrome and pheochromocytoma. N Engl J Med 327:1033

    Article  CAS  PubMed  Google Scholar 

  10. Yiannakopoulou E (2016) Robotic assisted adrenalectomy: surgical techniques, feasibility, indications, oncological outcome and safety. Int J Surg 28:169–172

    Article  Google Scholar 

  11. Brix D, Allolio B, Fenske W, Agha A, Dralle H, Jurowich C et al, German Adrenocortical Carcinoma Registry Group (2010) Laparoscopic versus open adrenalectomy for adrenocortical carcinoma: surgical and oncologic outcome in 152 patients. Eur Urol 58:609–615

  12. Lombardi CP, Raffaelli M, De Crea C, Boniardi M, De Toma G, Marzano LA (2012) Open versus endoscopic adrenalectomy in the treatment of localized (stage I/II) adrenocortical carcinoma: results of a multiinstitutional Italian survey. Surgery 152:1158–1164

    Article  PubMed  Google Scholar 

  13. Stefanidis D, Goldfarb M, Kercher KW, Hope WW, Richardson W, Fanelli RD (2013) SAGES guidelines for minimally invasive treatment of adrenal pathology. Surg Endosc. https://doi.org/10.1007/s00464-013-3169-z

  14. Hue JJ, Bingmer K, Zhao H, Ammori JB, Wilhelm SM, Towe CW (2021) Reassessing the impact of tumor size on operative approach in adrenocortical carcinoma. J Surg Oncol 123:1238–1245

    Article  PubMed  Google Scholar 

  15. Delozier OM, Stiles ZE, Deschner BW, Drake JA, Deneve JL, Glazer ES et al (2021) Implications of conversion during attempted minimally invasive adrenalectomy for adrenocortical carcinoma. Ann Surg Oncol 28:492–501

    Article  PubMed  Google Scholar 

  16. Higgins JP, Altman DG, Gøtzsche PC, Jüni P, Moher D, Oxman AD et al, Cochrane Bias Methods Group; Cochrane Statistical Methods Group (2011) The Cochrane Collaboration’s tool for assessing risk of bias in randomized trials. BMJ 343:d5928

  17. Mishra K, Maurice MJ, Bukavina L, Abouassaly R (2019) Comparative efficacy of laparoscopic versus robotic adrenalectomy for adrenal malignancy. Urology 123:146–150

    Article  PubMed  Google Scholar 

  18. Hue JJ, Ahorukomeye P, Bingmer K, Drapalik L, Ammori JB, Wilhelm SM et al (2021) A comparison of robotic and laparoscopic minimally invasive adrenalectomy for adrenal malignancies. Surg Endosc 36:5374–5381

    Article  PubMed  Google Scholar 

  19. Tseng J, Diperi T, Gonsalves N, Chen Y, Ben-Shlomo A, Shouhed D et al (2022) Operative approach and case volume are associated with negative resection margins for adrenocortical carcinoma. Surg Endosc. https://doi.org/10.1007/s00464-022-09167-0

  20. Zafar SS, Abaza R (2008) Robot-assisted laparoscopic adrenalectomy for adrenocortical carcinoma: initial report and review of the literature. J Endourol 22:985–989

    Article  PubMed  Google Scholar 

  21. Brunaud L, Ayav A, Zarnegar R, Rouers A, Klein M, Boissel P et al (2008) Prospective evaluation of 100 robotic-assisted unilateral adrenalectomies. Surgery 144:995–1001

    Article  PubMed  Google Scholar 

  22. Giulianotti PC, Buchs NC, Addeo P, Bianco FM, Ayloo SM, Caravaglios G et al (2011) Robot-assisted adrenalectomy: a technical option for the surgeon? Int J Med Robot 7:27–32

    Article  CAS  PubMed  Google Scholar 

  23. Nordenström E, Westerdahl J, Hallgrimsson P, Bergenfelz A (2011) A prospective study of 100 robotically assisted laparoscopic adrenalectomies. J Robot Surg 5:127–131

    Article  PubMed  Google Scholar 

  24. Raman SR, Shakov E, Carnevale N, Yiengpruksawan A (2012) Robotic adrenalectomy by an open surgeon: are outcomes different? J Robot Surg 6:207–212

    Article  PubMed  Google Scholar 

  25. Hu X, Yang WX, Shao YX, Dou WC, Xiong SC, Li X (2020) Minimally invasive versus open adrenalectomy in patients with adrenocortical carcinoma: a meta-analysis. Ann Surg Oncol 27:3858–3869

    Article  PubMed  Google Scholar 

  26. Lee CW, Salem AI, Schneider DF, Leverson GE, Tran TB, Poultsides GA et al (2017) Minimally invasive resection of adrenocortical carcinoma: a multi-institutional study of 201 patients. J Gastrointest Surg 21:352–362

    Article  PubMed  Google Scholar 

  27. Bilimoria KY, Shen WT, Elaraj D, Bentrem DJ, Winchester DJ, Kebebew E et al (2008) Adrenocortical carcinoma in the United States: treatment utilization and prognostic factors. Cancer 113:3130–3136

    Article  PubMed  Google Scholar 

  28. Tierney JF, Chivukula SV, Poirier J, Pappas SG, Schadde E, Hertl M et al (2019) National treatment practice for adrenocortical carcinoma: have they changed and have we made any progress? J Clin Endocrinol Metab 104:5948–5956

    Article  PubMed  Google Scholar 

  29. Pommier RF, Brennan MF (1992) An eleven-year experience with adrenocortical carcinoma. Surgery 112:963–970

    CAS  PubMed  Google Scholar 

  30. Kebebew E, Reiff E, Duh QY, Clark OH, McMillan A (2006) Extent of disease at presentation and outcome for adrenocortical carcinoma: have we made progress? World J Surg 30:872–878

    Article  PubMed  Google Scholar 

  31. Fassnacht M, Dekkers OM, Else T, Baudin E, Berruti A, de Krijger R et al (2018) European Society of Endocrinology clinical practice guidelines on the management of adrenocortical carcinoma in adults, in collaboration with the European Network for the Study of Adrenal Tumors. Eur J Endocrinol 179:G1–G46

    Article  CAS  PubMed  Google Scholar 

  32. Miller BS, Gauger PG, Hammer GD, Doherty GM (2012) Resection of adrenocortical carcinoma is less complete and local recurrence occurs sooner and more often after laparoscopic adrenalectomy than after open adrenalectomy. Surgery 152:1150–1157

    Article  PubMed  Google Scholar 

  33. Mpaili E, Moris D, Tsilimigras DI, Oikonomou D, Pawlik TM, Schizas D et al (2018) Laparoscopic versus open adrenalectomy for localized/locally advanced primary adrenocortical carcinoma (ENSAT I-III) in adults: is margin-free resection the key surgical factor that dictates outcome? A review of the literature. J Laparoendosc Adv Surg Tech 28:408–414

    Article  Google Scholar 

  34. Calcatera NA, Hsiung-Wang C, Suss NR, Winchester DJ, Moo-Young TA, Prinz RA (2017) Minimally invasive adrenalectomy for adrenocortical carcinoma: five-year trends and predictors of conversion. World J Surg 42:473–481

    Article  Google Scholar 

  35. Hupe MC, Imkamp F, Merseburger AS (2017) Minimally invasive approaches to adrenal tumors: an up-to-date summary including patient position and port placement of laparoscopic, retroperitoneoscopic, robot-assisted, and single-site adrenalectomy. Curr Opin Urol 27:56–61

    Article  PubMed  Google Scholar 

  36. Brunaud L, Bresler L, Ayav A, Zarnegar R, Raphoz AL, Levan T et al (2008) Robotic-assisted adrenalectomy: what advantages compared to lateral transperitoneal laparoscopic adrenalectomy? Am J Surg 195:433–438

    Article  PubMed  Google Scholar 

  37. Piccoli M, Pecchini F, Serra F, Nigro C, Colli G, Gozzo D et al (2021) Robotic versus laparoscopic adrenalectomy: pluriannual experience in a high-volume center evaluating indications and results. J Laparoendosc Adv Surg Tech 31:375–381

    Article  Google Scholar 

  38. Greilsamer T, Nomine-Criqui C, Thy M, Ullmann T, Zarnegar R, Bresler L et al (2019) Robotic-assisted unilateral adrenalectomy: risk factors for perioperative complications in 303 consecutive patients. Surg Endosc 33:802–810

    Article  PubMed  Google Scholar 

  39. Brunaud L, Bresler L, Zarnegar R, Ayav A, Cormier L, Tretou S et al (2004) Does robotic adrenalectomy improve patient quality of life when compared to laparoscopic adrenalectomy? World J Surg 28:1180–1185

    Article  PubMed  Google Scholar 

  40. Rieder JM, Nisbet AA, Wuerstle MC, Tran VQ, Kwon EO, Chien GW (2010) Differences in left and right laparoscopic adrenalectomy. JSLS 14:369–373

    Article  PubMed  PubMed Central  Google Scholar 

  41. Ludwig AT, Wagner KR, Lowry PS, Papaconstantinou HT, Lairmore TC (2010) Robot-assisted posterior retroperitoneoscopic adrenalectomy. J Endourol 24:1307–1314

    Article  PubMed  Google Scholar 

  42. Materazzi G, Rossi L (2021) Robot-assisted adrenalectomy: state of the art. Updates Surg 73:1131–1146

    Article  PubMed  Google Scholar 

  43. Economopoulos KP, Mylonas KS, Stamou AA, Theocharidis V, Sergentanis TN, Psaltopoulou T et al (2017) Laparoscopic versus robotic adrenalectomy: a comprehensive meta-analysis. Int J Surg 38:95–104

    Article  PubMed  Google Scholar 

  44. Tang K, Li H, Xia D, Yu G, Guo X, Guan W et al (2015) Robot-assisted versus laparoscopic adrenalectomy: a systematic review and meta-analysis. J Laparoendosc Adv Surg Tech 25:187–195

    Article  Google Scholar 

  45. Moore EC, Berber E (2019) Fluorescence techniques in adrenal surgery. Gland Surg 8:S22–S27

    Article  PubMed  PubMed Central  Google Scholar 

  46. Colvin J, Zaidi N, Berber E (2016) The utility of indocyanine green fluorescence imaging during robotic adrenalectomy. J Surg Oncol 114:153–156

    Article  PubMed  Google Scholar 

  47. Winter JM, Talamini MA, Stanfield CL, Chang DC, Hundt JD, Dackiw AP et al (2006) Thirty robotic adrenalectomies: a single institution’s experience. Surg Endosc 20:119–124

    Article  CAS  PubMed  Google Scholar 

  48. Morelli L, Tartaglia D, Bronzoni J, Palmeri M, Guadagni S, Di Franco G et al (2016) Robotic assisted versus pure laparoscopic surgery of the adrenal glands: a case-control study comparing surgical techniques. Langenbecks Arch Surg 401:999–1006

    Article  PubMed  Google Scholar 

  49. Agcaoglu O, Aliyev S, Karabulut K, Mitchell J, Siperstein A, Berber E (2012) Robotic versus laparoscopic resection of large adrenal tumors. Ann Surg Oncol 19:2288–2294

    Article  PubMed  Google Scholar 

  50. Goitein D, Mintz Y, Gross D, Reissman P (2004) Laparoscopic adrenalectomy: ascending the learning curve. Surg Endosc 18:771–773

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research received no external funding.

Author information

Authors and Affiliations

  1. General Surgery Unit, Luxemburg Hospital Center, Luxembourg, Luxembourg

    Alessia Fassari

  2. Department of Translational and Precision Medicine, Sapienza University, Rome, Italy

    Luigi Petramala

  3. Department of Clinical, Internal, Anesthesiologic and Cardiovascular Sciences, Sapienza University, Rome, Italy

    Claudio Letizia

  4. Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University, Rome, Italy

    Giuseppe Cavallaro

Authors
  1. Alessia Fassari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luigi Petramala
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claudio Letizia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Giuseppe Cavallaro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giuseppe Cavallaro.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fassari, A., Petramala, L., Letizia, C. et al. Surgery for Adrenocortical Carcinoma: Do We Have Enough Evidence to Perform Robotic Approach? A Systematic Review. Indian J Surg (2023). https://doi.org/10.1007/s12262-023-03958-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12262-023-03958-y

Keywords

Search

Navigation