Skip to main content

Advertisement

Log in

Clinical analysis of the etiological spectrum of bilateral adrenal lesions: A large retrospective, single-center study

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

To investigate the clinical characteristics, endocrinological function, and etiology of bilateral adrenal lesions in hospitalized patients.

Methods

A retrospective study of 777 patients with bilateral adrenal lesions was conducted at the Chinese People’s Liberation Army General Hospital between January 2013 and January 2018. Patients’ demographic features, hormonal profiles, imaging findings, and histopathological findings were reviewed from database records.

Results

Of the 777 patients with bilateral adrenal lesions, 495 were men. The mean age at diagnosis was 52.0 ± 13.0 years. Overall, 511 (65.8%) cases were benign, followed by adrenal metastases (n = 224, 28.8%), pheochromocytoma (n = 26, 3.3%), adrenal lymphoma (n = 9, 1.2%), and adrenal corticocarcinoma (ACC; n = 7, 0.9%). Hormonal evaluation revealed that 34.3% of bilateral adrenal lesions were functional. The primary etiologies of functional lesions were primary aldosteronism (16.6%, 129/777), and primary bilateral macronodular adrenocortical hyperplasia (PBMAH; 8.8%, 68/777). Patients with lymphoma and metastases were significantly older than those with benign nonfunctional lesions (60.4 ± 11.0 years vs. 54.5 ± 10.4 years and 57.9 ± 10.8 years vs. 54.5 ± 10.4 years, respectively; both P < 0.001). Lesions in patients with adrenal lymphoma, ACC, pheochromocytoma, metastases, congenital adrenal hyperplasia, tuberculosis, and Cushing’s syndrome were significantly larger than benign nonfunctional lesions (all P < 0.001).

Conclusion

Benign adrenal lesions and metastases from the lungs are the most common causes of bilateral adrenal lesions. Primary aldosteronism and PBMAH are the most prevalent functional lesions. Moreover, patients with lymphoma or metastases are older and their masses are larger.

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

Access this article

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. M. Sherlock, A. Scarsbrook, A. Abbas, S. Fraser, P. Limumpornpetch, R. Dineen, P.M. Stewart, Adrenal incidentaloma. Endocr. Rev. 41(6), 775–820 (2020). https://doi.org/10.1210/endrev/bnaa008

    Article  PubMed Central  Google Scholar 

  2. J. Patrova, I. Jarocka, H. Wahrenberg, H. Falhammar, Clinical outcomes in adrenal incidentaloma: experience from one center. Endocr. Pr. 21(8), 870–877 (2015). https://doi.org/10.4158/EP15618.OR

    Article  Google Scholar 

  3. N. Lomte, T. Bandgar, S. Khare, S. Jadhav, A. Lila, M. Goroshi, R. Kasaliwal, K. Khadilkar, N.S. Shah, Bilateral adrenal masses: a single-centre experience. Endocr. Connect 5(2), 92–100 (2016). https://doi.org/10.1530/EC-16-0015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. L.L. Li, G. Yang, L. Zhao, J.T. Dou, W.J. Gu, Z.H. Lv, J.M. Lu, Y.M. Mu, Baseline Demographic and Clinical Characteristics of Patients with Adrenal Incidentaloma from a Single Center in China: A Survey. Int J Endocrinol. 3093290 (2017). https://doi.org/10.1155/2017/3093290

  5. O. Mete, L.A. Erickson, C.C. Juhlin, R.R. Krijger, H. Sasano, M. Volante, M.G. Papotti, Overview of the 2022 WHO classification of adrenal cortical tumors. Endocr. Pathol. 33(1), 155–196 (2022). https://doi.org/10.1007/s12022-022-09710-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. J. Maskur, M. Gruber, M. Peitzsch, D. Kaden, G. Di Dalmazi, M. Bidlingmaier, S. Zopp, K. Langton, J. Fazel, F. Beuschlein, S.R. Bornstein, M. Reincke, G. Eisenhofer, Plasma steroid profiles in subclinical compared with overt adrenal cushing syndrome. J. Clin. Endocrinol. Metab. 104(10), 4331–4340 (2019). https://doi.org/10.1210/jc.2018-02348

    Article  Google Scholar 

  7. L.K. Nieman, B.M. Biller, J.W. Findling, J. Newell-Price, M.O. Savage, P.M. Stewart, V.M. Montori, The diagnosis of cushing’s syndrome: an endocrine society clinical practice guideline. J. Clin. Endocrinol. Metab. 93(5), 1526–1540 (2008). https://doi.org/10.1210/jc.2008-0125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. R. Garcia-Carbonero, F. Matute Teresa, E. Mercader-Cidoncha, M. Mitjavila-Casanovas, M. Robledo, I. Tena, C. Alvarez-Escola, M. Arístegui, M.R. Bella-Cueto, C. Ferrer-Albiach, F.A. Hanzu, Multidisciplinary practice guidelines for the diagnosis, genetic counseling and treatment of pheochromocytomas and paragangliomas. Clin. Transl. Oncol. 23(10), 1995–2019 (2021). https://doi.org/10.1007/s12094-021-02622-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. J.W. Funder, R.M. Carey, F. Mantero, M.H. Murad, M. Reincke, H. Shibata, M. Stowasser, W.F. Young, The management of primary aldosteronism: case detection, diagnosis, and treatment: an endocrine society clinical practice guideline. J. Clin. Endocrinol. Metab. 101(5), 1889–1916 (2016). https://doi.org/10.1210/jc.2015-4061

    Article  CAS  PubMed  Google Scholar 

  10. J. Wei, S.Y. Li, Q.L. Liu, Y.C. Zhu, N.W. Wu, Y. Tang, Q.R. Li, K.Y. Ren, Q.Y. Zhang, Y.R. Yu, Z.M. An, J. Chen, J.W. Li, ACTH-independent Cushing’s syndrome with bilateral cortisol-secreting adrenal adenomas: a case report and review of literatures. BMC Endocr. Disord. 18(1), 22 (2018). https://doi.org/10.1186/s12902-018-0250-6

    Article  PubMed  PubMed Central  Google Scholar 

  11. H.L. Claahsen-van der Grinten, P.W. Speiser, S.F. Ahmed, W. Arlt, R.J. Auchus, H. Falhammar, C.E. Flück, L. Guasti, A. Huebner, B.B.M. Kortmann, N. Krone, D.P. Merke, M.L. Miller, A. Nordenström, N. Reisch, D.E. Sandberg, N.M.M.L. Stikkelbroeck, P. Touraine, A. Utari, S.A. Wudy, P.C. White, Congenital adrenal hyperplasia-current insights in pathophysiology, diagnostics, and management. Endocr. Rev. 43(1), 91–159 (2022). https://doi.org/10.1210/endrev/bnab016

    Article  PubMed  Google Scholar 

  12. J. Zeng, F. Yan, Y. Chen, L. Zang, K. Chen, Z. Lyu, J. Dou, Y. Mu, M. Lin, G. Yang, Primary adrenal lymphoma: two case series from China. Front Endocrinol. (Lausanne) 12, 778984 (2022). https://doi.org/10.3389/fendo.2021.778984

    Article  Google Scholar 

  13. M. Fassnacht, O.M. Dekkers, T. Else, E. Baudin, A. Berruti, R. de Krijger, H.R. Haak, R. Mihai, G. Assie, M. Terzolo, 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(4), G1–G46 (2018). https://doi.org/10.1530/EJE-18-0608

    Article  CAS  PubMed  Google Scholar 

  14. Y.C. Huang, Y.L. Tang, X.M. Zhang, N.L. Zeng, R. Li, T.W. Chen, Evaluation of primary adrenal insufficiency secondary to tuberculous adrenalitis with computed tomography and magnetic resonance imaging: Current status. World J. Radio. 7(10), 336–342 (2015). https://doi.org/10.4329/wjr.v7.i10.336

    Article  Google Scholar 

  15. M. Marty, D. Gaye, P. Perez, C. Auder, M.L. Nunes, A. Ferriere, M. Haissaguerre, A. Tabarin, Diagnostic accuracy of computed tomography to identify adenomas among adrenal incidentalomas in an endocrinological population. Eur. J. Endocrinol. 178(5), 439–446 (2018). https://doi.org/10.1530/EJE-17-1056

    Article  CAS  PubMed  Google Scholar 

  16. G.W. Boland, M.J. Lee, G.S. Gazelle, E.F. Halpern, M.M. McNicholas, P.R. Mueller, Characterization of adrenal masses using unenhanced CT: an analysis of the CT literature. AJR Am. J. Roentgenol. 171(1), 201–204 (1998). https://doi.org/10.2214/ajr.171.1.9648789

    Article  CAS  PubMed  Google Scholar 

  17. D.H. Szolar, M. Korobkin, P. Reittner, A. Berghold, T. Bauernhofer, H. Trummer, H. Schoellnast, K.W. Preidler, H. Samonigg, Adrenocortical carcinomas and adrenal pheochromocytomas: mass and enhancement loss evaluation at delayed contrast-enhanced CT. Radiology 234(2), 479–485 (2005). https://doi.org/10.1148/radiol.2342031876

    Article  PubMed  Google Scholar 

  18. I. Platzek, D. Sieron, V. Plodeck, A. Borkowetz, M. Laniado, R.T. Hoffmann, Chemical shift imaging for evaluation of adrenal masses: a systematic review and meta-analysis. Eur. Radio. 29(2), 806–817 (2019). https://doi.org/10.1007/s00330-018-5626-5

    Article  Google Scholar 

  19. Q. Tian, S.T. Zhang, H.W. Gao, R. Lu, J. Yang, H.N. Wang, T.P. Hong, The etiological analysis of 260 hospitalized cases with bilateral adrenal lesions. Zhonghua Yi Xue Za Zhi 99(16), 1246–1250 (2019). https://doi.org/10.3760/cma.j.issn.0376-2491

    Article  CAS  PubMed  Google Scholar 

  20. J.D. Pasternack, C.D. Seib, N. Seiser, J.B. Tyrell, C. Liu, R.M. Cisco, J.E. Gosnell, W.T. Shen, I. Suh, Q.Y. Duh, Differences between bilateral adrenal incidentalomas and unilateral lesions. JAMA Surg. 150(10), 974–978 (2015). https://doi.org/10.1001/jamasurg.2015.1683

    Article  Google Scholar 

  21. K. Duan, K.G. Hernandez, O. Mete, Clinicopathological correlates of adrenal Cushing’s syndrome. J. Clin. Pathol. 68(3), 175–186 (2015). https://doi.org/10.1136/jclinpath-2014-202612

    Article  CAS  PubMed  Google Scholar 

  22. K.Y. Lam, C.Y. Lo, Metastatic tumours of the adrenal glands: a 30-year experience in a teaching hospital. Clin. Endocrinol. (Oxf.) 56(1), 95–101 (2002). https://doi.org/10.1046/j.0300-0664.2001.01435.x

    Article  Google Scholar 

  23. J.H. Song, F.S. Chaudhry, W.W. Mayo-Smith, The incidental adrenal mass on CT: prevalence of adrenal disease in 1,049 consecutive adrenal masses in patients with no known malignancy. AJR Am. J. Roentgenol. 190(5), 1163–1168 (2008). https://doi.org/10.2214/AJR.07.2799

    Article  PubMed  Google Scholar 

  24. C.C. Juhlin, J. Bertherat, T.J. Giordano, G.D. Hammer, H. Sasano, O. Mete, What did we learn from the molecular biology of adrenal cortical neoplasia? From histopathology to translational genomics. Endocr. Pathol. 32(1), 102–133 (2021). https://doi.org/10.1007/s12022-021-09667-0

    Article  CAS  PubMed  Google Scholar 

  25. O. Mete, K. Duan, The many faces of primary aldosteronism and cushing syndrome: a refection of adrenocortical tumor heterogeneity. Front Med (Lausanne) 5, 54 (2018). https://doi.org/10.3389/fmed.2018.00054

    Article  Google Scholar 

  26. G.A. Alencar, A.M. Lerario, M.Y. Nishi, B.M. Mariani, M.Q. Almeida, J. Tremblay, P. Hamet, I. Bourdeau, M.C.N. Zerbini, M.A.A. Pereira, G.C. Gomes, M. Souza Rocha, J.L. Chambo, A. Lacroix, B.B. Mendonca, M.C.B.V. Fragoso, ARMC5 mutations are a frequent cause of primary macronodular adrenal Hyperplasia. J. Clin. Endocrinol. Metab. 99(8), E1501–9 (2014). https://doi.org/10.1210/jc.2013-4237

    Article  CAS  PubMed  Google Scholar 

  27. F.R. Faucz, M. Zilbermint, M.B. Lodish, E. Szarek, G. Trivellin, N. Sinaii, A. Berthon, R. Libé, G. Assié, S. Espiard, L. Drougat, B. Ragazzon, J. Bertherat, C.A. Stratakis, Macronodular adrenal hyperplasia due to mutations in an armadillo repeat containing 5 (ARMC5) gene: a clinical and genetic investigation. J. Clin. Endocrinol. Metab. 99(6), E1113–1119 (2014). https://doi.org/10.1210/jc.2013-4280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. G. Assié, R. Libé, S. Espiard, M. Rizk-Rabin, A. Guimier, W. Luscap, O. Barreau, L. Lefèvre, M. Sibony, L. Guignat, S. Rodriguez, K. Perlemoine, F. René-Corail, F. Letourneur, B. Trabulsi, A. Poussier, N. Chabbert-Buffet, F. Borson-Chazot, L. Groussin, X. Bertagna, C.A. Stratakis, B. Ragazzon, J. Bertherat, ARMC5 mutations in macronodular adrenal hyperplasia with Cushing’s syndrome. N. Engl. J. Med 369(22), 2105–2114 (2013). https://doi.org/10.1056/NEJMoa1304603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. A. Lacroix, Heredity and cortisol regulation in bilateral macronodular adrenal hyperplasia. N. Engl. J. Med 369(22), 2147–2149 (2013). https://doi.org/10.1056/NEJMe1312792

    Article  CAS  PubMed  Google Scholar 

  30. C.A. Stratakis, L.S. Kirschner, J.A. Carney, Clinical and molecular features of the Carney complex: diagnostic criteria and recommendations for patient evaluation. J. Clin. Endocrinol. Metab. 86(9), 4041–4046 (2001). https://doi.org/10.1210/jcem.86.9.7903

    Article  CAS  PubMed  Google Scholar 

  31. C.A. Stratakis, S.A. Boikos, Genetics of adrenal tumors associated with Cushing’s syndrome: a new classification for bilateral adrenocortical hyperplasias. Nat. Clin. Pr. Endocrinol. Metab. 3(11), 748–757 (2007). https://doi.org/10.1038/ncpendmet0648

    Article  CAS  Google Scholar 

  32. G. Goh, U.I. Scholl, J.M. Healy, M. Choi, M.L. Prasad, C. Nelson-Williams, J.W. Kunstman, R. Korah, A. Suttorp, D. Dietrich, M. Haase, H.S. Willenberg, P. Stålberg, P. Hellman, G. Akerström, P. Björklund, T. Carling, R.P. Lifton, Recurrent activating mutation in PRKACA in cortisol-producing adrenal tumors. Nat. Genet 46(6), 613–617 (2014). https://doi.org/10.1038/ng.2956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. G. Raverot, F. Brucker-Davis, F. Archambeaud-Mouveroux, H. Lefebvre, M.-L. Nunes, A. Tabarin, A. Lienhardt, O. Chabre, M. Houang, M. Bottineau, S. Stror, L. Groussin, L. Guignat, L. Cabanes, A. Feydy, F. Bonnet, M.O. North, N. Dupin, S. Grabar, D. Duboc, J. Bertherat, Frequency and Incidence of Carney Complex Manifestations: A Prospective Multicenter Study With a Three-Year Follow-Up. J. Clin. Endocrinol. Metab. 105(3), dgaa002 (2020). https://doi.org/10.1210/clinem/dgaa002

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank all the patient, doctors, nurses, and technicians involved at two centers for their dedication to the study.

Author information

Authors and Affiliations

Authors

Contributions

F.Y. and J.Z.: collected data and wrote the manuscript draft. Y.C., Y.C., Y.P., L.Z., K.C., W.G., J.D., Q.G., X.W., J.B., Z.L., J.D.: contributed to discussion and revision. G.Y. and Y.M.: designed the study and revised the submission. All authors contributed to the discussion and approved the final manuscript for the version to be submitted.

Corresponding authors

Correspondence to Guoqing Yang or Yiming Mu.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and was approved by the Ethics Committee (No. 2019-229).

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

Yan, F., Zeng, J., Chen, Y. et al. Clinical analysis of the etiological spectrum of bilateral adrenal lesions: A large retrospective, single-center study. Endocrine 77, 372–379 (2022). https://doi.org/10.1007/s12020-022-03077-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-022-03077-w

Keywords

Navigation