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Open Versus Laparoscopic Surgery in the Management of Adrenocortical Carcinoma: A Systematic Review and Meta-analysis

  • Endocrine Tumors
  • Published:
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Abstract

Background

Laparoscopic surgery is considered a standard treatment for benign adrenal tumors; however, no consensus has been reached on the optimal resection technique for adrenocortical carcinomas. This study aims to evaluate the safety and efficacy of laparoscopic surgery and open surgery in the management of adrenocortical carcinoma.

Methods

The Cochrane, Embase, PubMed, Scopus, and Web of Science databases were searched for articles from inception to May 2022, by two independent reviewers using the preferred reporting items for systematic reviews and meta-analysis (PRISMA) guidelines. The review was registered prospectively on the PROSPERO database (CRD42022316050).

Results

From 183 studies screened, 11 studies met the eligibility criteria, with a total of 1617 patients with adrenocortical carcinoma undergoing either laparoscopic surgery (n = 472) or open surgery (n = 1145). Open surgery demonstrated a lower rate of positive resection margin compared with laparoscopic surgery (odds ratio [OR] 1.52, 95% confidence interval [CI] 1.10–2.10; I2 = 0%). Additionally, open surgery had more favorable overall survival (OR 0.56, 95% CI 0.44–0.72; I2 = 0%) and recurrence-free rates (OR 0.60, 95% CI 0.42–0.85; I2 = 38%) than laparoscopic surgery at 3 years. Hospital stay was shorter for laparoscopic surgery than open surgery (mean difference − 2.49 days, 95% CI − 2.95 to − 2.04; I2 = 45%).

Conclusions

Open surgery should still be considered the standard operative approach; however, laparoscopic surgery could be regarded as an effective and safe operation for selected adrenocortical carcinoma cases with appropriate laparoscopic expertise. Further randomized controlled studies with tumor stage- and resection margin-dependent survival analysis are necessary to ascertain the safety and efficacy of the treatment.

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Data Availability

The data set used for this meta-analysis will be shared upon request to the study authors.

References

  1. Sharma E, Dahal S, Sharma P, et al. The characteristics and trends in adrenocortical carcinoma: a United States population based study. J Clin Med Res. 2018;10(8):636–40.

    Article  Google Scholar 

  2. Ayala-Ramirez M, Jasim S, Feng L, et al. Adrenocortical carcinoma: clinical outcomes and prognosis of 330 patients at a tertiary care center. Eur J Endocrinol. 2013;169(6):891–9.

    Article  CAS  Google Scholar 

  3. Marincola Smith P, Kiernan CM, Tran TB, et al. Role of additional organ resection in adrenocortical carcinoma: analysis of 167 patients from the U.S. adrenocortical carcinoma database. Ann Surg Oncol. 2018;25(8):2308–15.

    Article  Google Scholar 

  4. Carnaille B. Adrenocortical carcinoma: Which surgical approach? Langenbecks Arch Surg. 2012;397(2):195–9.

    Article  Google Scholar 

  5. Smith CD, Weber CJ, Amerson JR. Laparoscopic adrenalectomy: new gold standard. World J Surg. 1999;23(4):389–96.

    Article  CAS  Google Scholar 

  6. Wang HS, Li CC, Chou YH, Wang CJ, Wu WJ, Huang CH. Comparison of laparoscopic adrenalectomy with open surgery for adrenal tumors. Kaohsiung J Med Sci. 2009;25(8):438–44.

    Article  CAS  Google Scholar 

  7. Yan Y, Cheng J, Chen K, Liu TF, Ning G. Better clinical benefits and potential cost saving of an enhanced recovery pathways for laparoscopic adrenalectomy. Gland Surg. 2022;11(1):23–34.

    Article  CAS  Google Scholar 

  8. Hazzan D, Shiloni E, Golijanin D, Jurim O, Gross D, Reissman P. Laparoscopic vs open adrenalectomy for benign adrenal neoplasm. Surg Endosc. 2001;15(11):1356–8.

    Article  CAS  Google Scholar 

  9. Pigg RA, Fazendin JM, Porterfield JR, Chen H, Lindeman B. Patient satisfaction is equivalent for inpatient and outpatient minimally-invasive adrenalectomy. J Surg Res. 2022;269:207–11.

    Article  Google Scholar 

  10. Miller BS, Gauger PG, Hammer GD, Doherty GM. Resection of adrenocortical carcinoma is less complete and local recurrence occurs sooner and more often after laparoscopic adrenalectomy than after open adrenalectomy. Surgery. 2012;152(6):1150–7.

    Article  Google Scholar 

  11. Kebebew E, Siperstein AE, Clark OH, Duh QY. Results of laparoscopic adrenalectomy for suspected and unsuspected malignant adrenal neoplasms. Arch Surg. 2002;137(8):948–51 (discussion 952–943).

    Article  Google Scholar 

  12. Leboulleux S, Deandreis D, Al Ghuzlan A, et al. Adrenocortical carcinoma: Is the surgical approach a risk factor of peritoneal carcinomatosis? Eur J Endocrinol. 2010;162(6):1147–53.

    Article  CAS  Google Scholar 

  13. Lombardi CP, Raffaelli M, De Crea C, Bellantone R. Role of laparoscopy in the management of adrenal malignancies. J Surg Oncol. 2006;94(2):128–31.

    Article  Google Scholar 

  14. Langenhuijsen J, Birtle A, Klatte T, Porpiglia F, Timsit MO. Surgical management of adrenocortical carcinoma: impact of laparoscopic approach, lymphadenectomy, and surgical volume on outcomes-a systematic review and meta-analysis of the current literature. Eur Urol Focus. 2016;1(3):241–50.

    Article  Google Scholar 

  15. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.

    Article  Google Scholar 

  16. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.

    Article  Google Scholar 

  17. Fassnacht M, Johanssen S, Quinkler M, et al. Limited prognostic value of the 2004 International Union Against Cancer staging classification for adrenocortical carcinoma: proposal for a Revised TNM Classification. Cancer. 2009;115(2):243–50.

    Article  Google Scholar 

  18. Lughezzani G, Sun M, Perrotte P, et al. 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. 2010;46(4):713–9.

    Article  Google Scholar 

  19. Hermanek P, Wittekind C. The pathologist and the residual tumor (R) classification. Pathol Res Pract. 1994;190(2):115–23.

    Article  CAS  Google Scholar 

  20. Guyot P, Ades AE, Ouwens MJ, Welton NJ. Enhanced secondary analysis of survival data: reconstructing the data from published Kaplan–Meier survival curves. BMC Med Res Methodol. 2012;12:9.

    Article  Google Scholar 

  21. Higgins JPT, Cochrane Collaboration. Cochrane handbook for systematic reviews of interventions. 2nd edn. Hoboken: Wiley; 2020.

    Google Scholar 

  22. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–60.

    Article  Google Scholar 

  23. Sterne JA, Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol. 2001;54(10):1046–55.

    Article  CAS  Google Scholar 

  24. Brix D, Allolio B, Fenske W, et al. Laparoscopic versus open adrenalectomy for adrenocortical carcinoma: surgical and oncologic outcome in 152 patients. Eur Urol. 2010;58(4):609–15.

    Article  Google Scholar 

  25. Kastelan D, Knezevic N, Zibar Tomsic K, et al. Open vs laparoscopic adrenalectomy for localized adrenocortical carcinoma. Clin Endocrinol (Oxf). 2020;93(4):404–8.

    Article  Google Scholar 

  26. Tseng J, Diperi T, Gonsalves N, et al. Operative approach and case volume are associated with negative resection margins for adrenocortical carcinoma. Surg Endosc. 2022. https://doi.org/10.1007/s00464-022-09167-0.

    Article  Google Scholar 

  27. Lombardi CP, Raffaelli M, De Crea C, et al. Open versus endoscopic adrenalectomy in the treatment of localized (stage I/II) adrenocortical carcinoma: results of a multiinstitutional Italian survey. Surgery. 2012;152(6):1158–64.

    Article  Google Scholar 

  28. Cooper AB, Habra MA, Grubbs EG, et al. Does laparoscopic adrenalectomy jeopardize oncologic outcomes for patients with adrenocortical carcinoma? Surg Endosc. 2013;27(11):4026–32.

    Article  Google Scholar 

  29. Donatini G, Caiazzo R, Do Cao C, et al. Long-term survival after adrenalectomy for stage I/II adrenocortical carcinoma (ACC): a retrospective comparative cohort study of laparoscopic versus open approach. Ann Surg Oncol. 2014;21(1):284–91.

    Article  Google Scholar 

  30. Fossa A, Rosok BI, Kazaryan AM, et al. Laparoscopic versus open surgery in stage I-III adrenocortical carcinoma—a retrospective comparison of 32 patients. Acta Oncol. 2013;52(8):1771–7.

    Article  Google Scholar 

  31. Mir MC, Klink JC, Guillotreau J, et al. Comparative outcomes of laparoscopic and open adrenalectomy for adrenocortical carcinoma: single, high-volume center experience. Ann Surg Oncol. 2013;20(5):1456–61.

    Article  Google Scholar 

  32. Porpiglia F, Fiori C, Daffara F, et al. Retrospective evaluation of the outcome of open versus laparoscopic adrenalectomy for stage I and II adrenocortical cancer. Eur Urol. 2010;57(5):873–8.

    Article  Google Scholar 

  33. Wu K, Liu Z, Liang J, et al. Laparoscopic versus open adrenalectomy for localized (stage 1/2) adrenocortical carcinoma: experience at a single, high-volume center. Surgery. 2018;164(6):1325–9.

    Article  Google Scholar 

  34. Zheng GY, Li HZ, Deng JH, Zhang XB, Wu XC. Open adrenalectomy versus laparoscopic adrenalectomy for adrenocortical carcinoma: a retrospective comparative study on short-term oncologic prognosis. Onco Targets Ther. 2018;11:1625–32.

    Article  Google Scholar 

  35. Margonis GA, Kim Y, Prescott JD, et al. Adrenocortical carcinoma: impact of surgical margin status on long-term outcomes. Ann Surg Oncol. 2016;23(1):134–41.

    Article  Google Scholar 

  36. Grubbs EG, Callender GG, Xing Y, et al. Recurrence of adrenal cortical carcinoma following resection: surgery alone can achieve results equal to surgery plus mitotane. Ann Surg Oncol. 2010;17(1):263–70.

    Article  Google Scholar 

  37. Hu X, Yang WX, Shao YX, Dou WC, Xiong SC, Li X. Minimally invasive versus open adrenalectomy in patients with adrenocortical carcinoma: a meta-analysis. Ann Surg Oncol. 2020;27(10):3858–69.

    Article  Google Scholar 

  38. Yeo CT, Pasieka JL, Assadzadeh GE, Harvey A. The adoption of the endoscopic retroperitoneal approach to the adrenal gland—conversion factors and learning points. Am J Surg. 2022;224(2):703–9.

    Article  Google Scholar 

  39. Fazendin J, Chen H, Lindeman B. Influence of fellowship educational experience on practice patterns for adrenalectomy: a survey of recent AAES fellowship graduates. Am J Surg. 2021;221(3):626–30.

    Article  Google Scholar 

  40. Autorino R, Bove P, De Sio M, et al. Open versus laparoscopic adrenalectomy for adrenocortical carcinoma: a meta-analysis of surgical and oncological outcomes. Ann Surg Oncol. 2016;23(4):1195–202.

    Article  Google Scholar 

  41. Amin MB, Greene FL, Edge SB, et al. The eighth edition AJCC cancer staging manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67(2):93–9.

    Article  Google Scholar 

  42. Tella SH, Kommalapati A, Yaturu S, Kebebew E. Predictors of survival in adrenocortical carcinoma: an analysis from the national cancer database. J Clin Endocrinol Metab. 2018;103(9):3566–73.

    Article  Google Scholar 

  43. Theophilus M, Platell C, Spilsbury K. Long-term survival following laparoscopic and open colectomy for colon cancer: a meta-analysis of randomized controlled trials. Colorectal Dis. 2014;16(3):O75-81.

    Article  CAS  Google Scholar 

  44. Vinuela EF, Gonen M, Brennan MF, Coit DG, Strong VE. Laparoscopic versus open distal gastrectomy for gastric cancer: a meta-analysis of randomized controlled trials and high-quality nonrandomized studies. Ann Surg. 2012;255(3):446–56.

    Article  Google Scholar 

  45. Nakanishi H, Miangul S, Oluwaremi TT, Sim BL, Hong SS, Than CA. Open versus laparoscopic surgery in the management of patients with gallbladder cancer: a systematic review and meta-analysis. Am J Surg. 2022;224(1 Pt B):348–57.

    Article  Google Scholar 

  46. Tsai KY, Chen HA, Wang WY, Huang MT. Long-term and short-term surgical outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma: Might laparoscopic approach be better in early HCC? Surg Endosc. 2019;33(4):1131–9.

    Article  Google Scholar 

  47. Miller BS, Ammori JB, Gauger PG, Broome JT, Hammer GD, Doherty GM. Laparoscopic resection is inappropriate in patients with known or suspected adrenocortical carcinoma. World J Surg. 2010;34(6):1380–5.

    Article  CAS  Google Scholar 

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Acknowledgment

The authors would like to thank M.L.S. Larry Prokop for the literature search.

Funding

This research did not receive any specific grants from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors

Contributions

HN, SM, and HC conceived and designed the study; reviewed the literature; collected, analyzed, and interpreted the data; and drafted and critically revised the manuscript. HN, SM, RW, JEH, NEG, FAA, RHM, CAT, BEJ, and HC reviewed the literature; collected, analyzed, and interpreted the data; and drafted the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Herbert Chen MD.

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Disclosure

Benjamin Johnson has a financial relationship with Intuitive Surgical for proctoring and educational events, however these were not related to this current paper. Hayato Nakanishi, Shahid Miangul, Rongzhi Wang, Joe El Haddad, Nour El Ghaza, Fatma Ali Makhzoum Abdulsalam, Reem H. Matar, Christian A. Than, and Herbert Chen declare they have no competing interests.

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This systematic review and meta-analysis does not require ethical approval.

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Nakanishi, H., Miangul, S., Wang, R. et al. Open Versus Laparoscopic Surgery in the Management of Adrenocortical Carcinoma: A Systematic Review and Meta-analysis. Ann Surg Oncol 30, 994–1005 (2023). https://doi.org/10.1245/s10434-022-12711-w

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