Systematic review of surgical treatment of subclinical Cushing's syndrome

British Journal of Surgery

Volumn 102, Issue 4, 2015, Pages

  Iacobone, M ^a   Citton, M ^a   Scarpa, M ^a   Viel, G ^a   Boscaro, M ^b   Nitti, D ^a  

^a VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALECTOMY; ADULT; AGED; CUSHING SYNDROME; EPIDEMIOLOGY; FEMALE; HUMAN; LAPAROSCOPY; MALE; MIDDLE AGED; POSTOPERATIVE COMPLICATIONS; PROCEDURES; TREATMENT OUTCOME;

ADRENALECTOMY; ADULT; AGED; CUSHING SYNDROME; EPIDEMIOLOGIC METHODS; FEMALE; HUMANS; LAPAROSCOPY; MALE; MIDDLE AGED; POSTOPERATIVE COMPLICATIONS; TREATMENT OUTCOME;

EID: 84923093878     PISSN: 00071323     EISSN: 13652168     Source Type: Journal    
DOI: 10.1002/bjs.9742     Document Type: Review

References (74)

1. Chiodini I, Morelli V, Salcuni AS, Eller-Vainicher C, Torlontano M, Coletti F et al. Beneficial metabolic effects of prompt surgical treatment in patients with an adrenal incidentaloma causing biochemical hypercortisolism. J Clin Endocrinol Metab 2010; 95: 2736-2745.
2. Sippel RS, Chen H. Subclinical Cushing's syndrome in adrenal incidentalomas. Surg Clin North Am 2004; 84: 875-885.
3. Nieman LK, Biller BM, Findling JW, Newell-Price J, Savage MO, Stewart PM et al. The diagnosis of Cushing's syndrome: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab 2008; 93: 1526-1540.
4. Starker LF, Kunstman JW, Carling T. Subclinical Cushing syndrome: a review. Surg Clin North Am 2014; 94: 657-668.
5. Chiodini I. Clinical review: diagnosis and treatment of subclinical hypercortisolism. J Clin Endocrinol Metab 2011; 96: 1223-1236.
6. Arnaldi G, Boscaro M. Adrenal incidentaloma. Best Pract Res Clin Endocrinol Metab 2012; 26: 405-419.
7. Reincke M. Subclinical Cushing's syndrome. Endocrinol Metab Clin North Am 2000; 29: 43-56.
8. Grumbach MM, Biller BM, Braunstein GD, Campbell KK, Carney JA, Godley PA et al. Management of the clinically inapparent adrenal mass ('incidentaloma'). Ann Intern Med 2003; 138: 424-429.
9. Mantero F, Terzolo M, Arnaldi G, Osella G, Masini AM, Ali A et al. A survey on adrenal incidentaloma in Italy. Study Group on Adrenal Tumors of the Italian Society of Endocrinology. J Clin Endocrinol Metab 2000; 85: 637-644.
10. Terzolo M, Stigliano A, Chiodini I, Loli P, Furlani L, Arnaldi G et al.; Italian Association of Clinical Endocrinologists. AME position statement on adrenal incidentaloma. Eur J Endocrinol 2011; 164: 851-870.
11. Stewart PM. Is subclinical Cushing's syndrome an entity or a statistical fallout from diagnostic testing? Consensus surrounding the diagnosis is required before optimal treatment can be defined. J Clin Endocrinol Metab 2010; 95: 2618-2620.
12. NIH state-of-the-science statement on management of the clinically inapparent adrenal mass ('incidentaloma'). NIH Consens State Sci Statements 2002; 19: 1-25.
13. Iacobone M, Albiger N, Scaroni C, Mantero F, Fassina A, Viel G et al. The role of unilateral adrenalectomy in ACTH-independent macronodular adrenal hyperplasia (AIMAH). World J Surg 2008; 32: 882-889.
14. Beierwaltes WH, Sturman MF, Ryo U, Ice RD. Imaging functional nodules of the adrenal glands with 131-I-19-iodocholesterol. J Nucl Med 1974; 15: 246-251.
15. Charbonnel B, Chatal JF, Ozanne P. Does the corticoadrenal adenoma with 'pre-Cushing's syndrome' exist? J Nucl Med 1981; 22: 1059-1061.
16. Young WF Jr. Management approaches to adrenal incidentalomas. A view from Rochester, Minnesota. Endocrinol Metab Clin North Am 2000; 29: 159-185.
17. Barzon L, Scaroni C, Sonino N, Fallo F, Paoletta A, Boscaro M. Risk factors and long-term follow-up of adrenal incidentalomas. J Clin Endocrinol Metab 1999; 84: 520-526.
18. Barzon L, Sonino N, Fallo F, Palu G, Boscaro M. Prevalence and natural history of adrenal incidentalomas. Eur J Endocrinol 2003; 149: 273-285.
19. Terzolo M, Pia A, Reimondo G. Subclinical Cushing's syndrome: definition and management. Clin Endocrinol (Oxf) 2012; 76: 12-18.
20. Van Rossum EF, Russcher H, Lamberts SW. Genetic polymorphisms and multifactorial diseases: facts and fallacies revealed by the glucocorticoid receptor gene. Trends Endocrinol Metab 2005; 16: 445-450.
21. Manenschijn L, van den Akker EL, Lamberts SW, van Rossum EF. Clinical features associated with glucocorticoid receptor polymorphisms. An overview. Ann N Y Acad Sci 2009; 1179: 179-198.
22. Szappanos A, Patócs A, Tõke J, Boyle B, Sereg M, Majnik J et al. BclI polymorphism of the glucocorticoid receptor gene is associated with decreased bone mineral density in patients with endogenous hypercortisolism. Clin Endocrinol (Oxf) 2009; 71: 636-643.
23. Morelli V, Donadio F, Eller-Vainicher C, Cirello V, Olgiati L, Savoca C et al. Role of glucocorticoid receptor polymorphism in adrenal incidentalomas. Eur J Clin Invest 2010; 40: 803-811.
24. Tomlinson JW, Walker EA, Bujalska IJ, Draper N, Lavery GG, Cooper MS et al. 11Beta-hydroxysteroid dehydrogenase type 1: a tissue-specific regulator of glucocorticoid response. Endocr Rev 2004; 25: 831-866.
25. Hwang JY, Lee SH, Kim GS, Koh JM, Go MJ, Kim YJ et al. HSD11B1 polymorphisms predicted bone mineral density and fracture risk in postmenopausal women without a clinically apparent hypercortisolemia. Bone 2009; 45: 1098-1103.
26. Erbil Y, Ademoʇlu E, Ozbey N, Barbaros U, Yanik BT, Salmaslioʇlu A et al. Evaluation of the cardiovascular risk in patients with subclinical Cushing syndrome before and after surgery. World J Surg 2006; 30: 1665-1671.
27. Mitchell IC, Auchus RJ, Juneja K, Chang AY, Holt SA, Snyder WH III et al. 'Subclinical Cushing's syndrome' is not subclinical: improvement after adrenalectomy in 9 patients. Surgery 2007; 142: 900-905.
28. Terzolo M, Pia A, Alì A, Osella G, Reimondo G, Bovio S et al. Adrenal incidentaloma: a new cause of the metabolic syndrome? J Clin Endocrinol Metab 2002; 87: 998-1003.
29. Tauchmanovà L, Rossi R, Biondi B, Pulcrano M, Nuzzo V, Palmieri EA et al. Patients with subclinical Cushing's syndrome due to adrenal adenoma have increased cardiovascular risk. J Clin Endocrinol Metab 2002; 87: 4872-4878.
30. Rossi R, Tauchmanova L, Luciano A, Di Martino M, Battista C, Del Viscovo L et al. Subclinical Cushing's syndrome in patients with adrenal incidentaloma: clinical and biochemical features. J Clin Endocrinol Metab 2000; 85: 1440-1448.
31. Chiodini I, Morelli V, Masserini B, Salcuni AS, Eller-Vainicher C, Viti R et al. Bone mineral density, prevalence of vertebral fractures, and bone quality in patients with adrenal incidentalomas with and without subclinical hypercortisolism: an Italian multicenter study. J Clin Endocrinol Metab 2009; 94: 3207-3214.
32. Di Dalmazi G, Vicennati V, Garelli S, Casadio E, Rinaldi E, Giampalma E et al. Cardiovascular events and mortality in patients with adrenal incidentalomas that are either non-secreting or associated with intermediate phenotype or subclinical Cushing's syndrome: a 15-year retrospective study. Lancet Diabetes Endocrinol 2014; 2: 396-405.
33. Zeiger MA, Thompson GB, Duh QY, Hamrahian AH, Angelos P, Elaraj D et al.; American Association of Clinical Endocrinologists; American Association of Endocrine Surgeons. The American Association of Clinical Endocrinologists and American Association of Endocrine Surgeons medical guidelines for the management of adrenal incidentalomas. Endocr Pract 2009; 15(Suppl 1): 1-20.
34. Bernini G, Moretti A, Iacconi P, Miccoli P, Nami R, Lucani B et al. Anthropometric, haemodynamic, humoral and hormonal evaluation in patients with incidental adrenocortical adenomas before and after surgery. Eur J Endocrinol 2003; 148: 213-219.
35. Toniato A, Merante-Boschin I, Opocher G, Pelizzo MR, Schiavi F, Ballotta E. Surgical versus conservative management for subclinical Cushing syndrome in adrenal incidentalomas: a prospective randomized study. Ann Surg 2009; 249: 388-391.
36. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009; 339: b2535.
37. Dutch Cochrane Collaboration. Therapy Checklist (Dutch extended version) of the Dutch Cochrane Collaboration. http://www.cochrane.nl [accessed 13 July 2014].
38. Maehana T, Tanaka T, Itoh N, Masumori N, Tsukamoto T. Clinical outcomes of surgical treatment and longitudinal non-surgical observation of patients with subclinical Cushing's syndrome and nonfunctioning adrenocortical adenoma. Indian J Urol 2012; 28: 179-183.
39. He HC, Dai J, Shen ZJ, Zhu Y, Sun FK, Shao Y et al. Retroperitoneal adrenal-sparing surgery for the treatment of Cushing's syndrome caused by adrenocortical adenoma: 8-year experience with 87 patients. World J Surg 2012; 36: 1182-1188.
40. Giordano R, Marinazzo E, Berardelli R, Picu A, Maccario M, Ghigo E et al. Long-term morphological, hormonal, and clinical follow-up in a single unit on 118 patients with adrenal incidentalomas. Eur J Endocrinol 2010; 162: 779-785.
41. Midorikawa S, Sanada H, Hashimoto S, Suzuki T, Watanabe T. The improvement of insulin resistance in patients with adrenal incidentaloma by surgical resection. Clin Endocrinol (Oxf) 2001; 54: 797-804.
42. Morioka M, Fujii T, Matsuki T, Jo Y, Kobayashi T, Tanaka H et al. Preclinical Cushing's syndrome: report of seven cases and a review of the literature. Int J Urol 2000; 7: 126-132.
43. McLeod MK, Thompson NW, Gross MD, Bondeson AG, Bondeson L. Sub-clinical Cushing's syndrome in patients with adrenal gland incidentalomas. Pitfalls in diagnosis and management. Am Surg 1990; 56: 398-403.
44. Inoue M, Ide H, Kurihara K, Koseki T, Yu J, China T et al. Clinical usefulness of corticotropin releasing hormone testing in subclinical Cushing's syndrome for predicting cortisol replacement after adrenalectomy. Korean J Urol 2012; 53: 414-418.
45. Emral R, Uysal AR, Asik M, Gullu S, Corapcioglu D, Tonyukuk V et al. Prevalence of subclinical Cushing's syndrome in 70 patients with adrenal incidentaloma: clinical, biochemical and surgical outcomes. Endocr J 2003; 50: 399-408.
46. Ambrosi B, Peverelli S, Passini E, Re T, Ferrario R, Colombo P et al. Abnormalities of endocrine function in patients with clinically 'silent' adrenal masses. Eur J Endocrinol 1995; 132: 422-428.
47. Akaza I, Yoshimoto T, Iwashima F, Nakayama C, Doi M, Izumiyama H et al. Clinical outcome of subclinical Cushing's syndrome after surgical and conservative treatment. Hypertens Res 2011; 34: 1111-1115.
48. Tjan-Heijnen VC, Hermus AR, Kemink SA, Mudde AH, Pieters GF, Smals AG et al. Preclinical Cushing's syndrome in patients with an adrenal incidentaloma. Neth J Med 1998; 52: 111-115.
49. Reincke M, Nieke J, Krestin GP, Saeger W, Allolio B, Winkelmann W. Preclinical Cushing's syndrome in adrenal 'incidentalomas': comparison with adrenal Cushing's syndrome. J Clin Endocrinol Metab 1992; 75: 826-832.
50. Eller-Vainicher C, Morelli V, Salcuni AS, Torlontano M, Coletti F, Iorio L et al. Post-surgical hypocortisolism after removal of an adrenal incidentaloma: is it predictable by an accurate endocrinological work-up before surgery? Eur J Endocrinol 2010; 162: 91-99.
51. Sarkar R, Thompson NW, McLeod MK. The role of adrenalectomy in Cushing's syndrome. Surgery 1990; 108: 1079-1084.
52. Sereg M, Szappanos A, Toke J, Karlinger K, Feldman K, Kaszper E et al. Atherosclerotic risk factors and complications in patients with non-functioning adrenal adenomas treated with or without adrenalectomy: a long-term follow-up study. Eur J Endocrinol 2009; 160: 647-655.
53. Carney JA, Stratakis CA, Young WF Jr. Adrenal cortical adenoma: the fourth component of the Carney triad and an association with subclinical Cushing syndrome. Am J Surg Pathol 2013; 37: 1140-1149.
54. Muth A, Hammarstedt L, Hellström M, Sigurjónsdóttir HÁ, Almqvist E, Wängberg B; Adrenal Study Group of Western Sweden. Cohort study of patients with adrenal lesions discovered incidentally. Br J Surg 2011; 98: 1383-1391.
55. Mitchell J, Barbosa G, Tsinberg M, Milas M, Siperstein A, Berber E. Unrecognized adrenal insufficiency in patients undergoing laparoscopic adrenalectomy. Surg Endosc 2009; 23: 248-254.
56. Kasperlik-Załuska AA, Otto M, Cichocki A, Rosłonowska E, Słowinska-Srzednicka J, Zgliczyński W et al. 1161patients with adrenal incidentalomas: indications for surgery. Langenbecks Arch Surg 2008; 393: 121-126.
57. Shen WT, Lee J, Kebebew E, Clark OH, Duh QY. Selective use of steroid replacement after adrenalectomy: lessons from 331 consecutive cases. Arch Surg 2006; 141: 771-774.
58. Izaki H, Fukumori T, Takahashi M, Taue R, Kishimoto T, Tanimoto S et al. Indications for laparoscopic adrenalectomy for non-functional adrenal tumor with hypertension: usefulness of adrenocortical scintigraphy. Int J Urol 2006; 13: 677-681.
59. Eto M, Harano M, Koga H, Tanaka M, Naito S. Clinical outcomes and learning curve of a laparoscopic adrenalectomy in 103 consecutive cases at a single institute. Int J Urol 2006; 13: 671-676.
60. Terachi T, Yoshida O, Matsuda T, Orikasa S, Chiba Y, Takahashi K et al. Complications of laparoscopic and retroperitoneoscopic adrenalectomies in 370 cases in Japan: a multi-institutional study. Biomed Pharmacother 2000; 54(Suppl 1): 211s-214s.
61. Omura M, Saito J, Yamaguchi K, Kakuta Y, Nishikawa T. Prospective study on the prevalence of secondary hypertension among hypertensive patients visiting a general outpatient clinic in Japan. Hypertens Res 2004; 27: 193-202.
62. Alesina PF, Hommeltenberg S, Meier B, Petersenn S, Lahner H, Schmid KWet al. Posterior retroperitoneoscopic adrenalectomy for clinical and subclinical Cushing's syndrome. World J Surg 2010; 34: 1391-1397.
63. Miyazato M, Ishidoya S, Satoh F, Morimoto R, Kaiho Y, Yamada S et al. Surgical outcomes of laparoscopic adrenalectomy for patients with Cushing's and subclinical Cushing's syndrome: a single center experience. Int Urol Nephrol 2011; 43: 975-981.
64. Tsuiki M, Tanabe A, Takagi S, Naruse M, Takano K. Cardiovascular risks and their long-term clinical outcome in patients with subclinical Cushing's syndrome. Endocr J 2008; 55: 737-745.
65. Guerrieri M, Campagnacci R, Patrizi A, Romiti C, Arnaldi G, Boscaro M. Primary adrenal hypercortisolism: minimally invasive surgical treatment or medical therapy? A retrospective study with long-term follow-up evaluation. Surg Endosc 2010; 24: 2542-2546.
66. Iacobone M, Citton M, Viel G, Boetto R, Bonadio I, Mondi I et al. Adrenalectomy may improve cardiovascular and metabolic impairment and ameliorate quality of life in patients with adrenal incidentalomas and subclinical Cushing's syndrome. Surgery 2012; 152: 991-997.
67. Perysinakis I, Marakaki C, Avlonitis S, Katseli A, Vassilatou E, Papanastasiou L et al. Laparoscopic adrenalectomy in patients with subclinical Cushing syndrome. Surg Endosc 2013; 27: 2145-2148.
68. Mancia G, De Backer G, Dominiczak A, Cifkova R, Fagard R, Germano G et al.; Management of Arterial Hypertension of the European Society of Hypertension; European Society of Cardiology. 2007 guidelines for the management of arterial hypertension: the Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). J Hypertens 2007; 25: 1105-1187.
69. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). JAMA 2001; 285: 2486-2497.
70. Tabarin A, Bardet S, Bertherat J, Dupas B, Chabre O, Hamoir E et al.; French Society of Endocrinology Consensus. Exploration and management of adrenal incidentalomas. French Society of Endocrinology Consensus. Ann Endocrinol (Paris) 2008; 69: 487-500.
71. Valli N, Catargi B, Ronci N, Vergnot V, Leccia F, Ferriere JM et al. Biochemical screening for subclinical cortisol-secreting adenomas amongst adrenal incidentalomas. Eur J Endocrinol 2001; 144: 401-408.
72. Di Dalmazi G, Berr CM, Fassnacht M, Beuschlein F, Reincke M. Adrenal function after adrenalectomy for subclinical hypercortisolism and Cushing's syndrome: a systematic review of the literature. J Clin Endocrinol Metab 2014; 99: 2637-2645.
73. Huiras CM, Pehling GB, Caplan RH. Adrenal insufficiency after operative removal of apparently nonfunctioning adrenal adenomas. JAMA 1989; 261: 894-898.
74. Chiodini I, Torlontano M, Carnevale V, Guglielmi G, Cammisa M, Trischitta V et al. Bone loss rate in adrenal incidentalomas: a longitudinal study. J Clin Endocrinol Metab 2001; 86: 5337-5341.