Low testosterone is associated with poor health status in men with human immunodeficiency virus infection: A retrospective study

Andrology

Volumn 3, Issue 2, 2015, Pages 298-308

  Rochira, V ^a,b   Diazzi, C ^a,b   Santi, D ^a,b   Brigante, G ^a   Ansaloni, A ^a   Decaroli, M C ^a   De Vincentis, S ^a   Stentarelli, C ^a   Zona, S ^a   Guaraldi, G ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b AUSL Modena   (Italy)

Author keywords

Comorbidities; Frailty; Highly active antiretroviral therapy; Human immunodeficiency virus infection; Male hypogonadism; Poor health status; Serum testosterone

Indexed keywords

LUTEINIZING HORMONE; TESTOSTERONE;

ADULT; ANTHROPOMETRY; ARTICLE; BONE DENSITY; CARDIOVASCULAR DISEASE; CEREBROVASCULAR ACCIDENT; CHRONIC KIDNEY DISEASE; COMORBIDITY; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE ASSOCIATION; DYSLIPIDEMIA; FRAILTY; FREE LIOTHYRONINE INDEX; HEALTH STATUS; HEART INFARCTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS ASSOCIATED NONACQUIRED IMMUNODEFICIENCY SYNDROME; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPERGONADOTROPIC HYPOGONADISM; HYPERTENSION; HYPOGONADISM; LIPODYSTROPHY; MAJOR CLINICAL STUDY; MALE; MALIGNANT NEOPLASTIC DISEASE; METABOLIC SYNDROME X; MIDDLE AGED; NONALCOHOLIC FATTY LIVER; OBESITY; OSTEOPOROSIS; OUTCOME ASSESSMENT; PREVALENCE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; RISK FACTOR; TESTOSTERONE BLOOD LEVEL; VIRUS HEPATITIS; VITAMIN D DEFICIENCY; WASTING SYNDROME; WEAKNESS; METABOLISM; PATHOPHYSIOLOGY;

ADULT; HEALTH STATUS; HIV INFECTIONS; HUMANS; MALE; MIDDLE AGED; RETROSPECTIVE STUDIES; TESTOSTERONE;

EID: 84928284569     PISSN: 20472919     EISSN: 20472927     Source Type: Journal    
DOI: 10.1111/andr.310     Document Type: Article

References (55)

1. Agledahl I, Skjaerpe PA, Hansen JB & Svartberg J. (2008) Low serum testosterone in men is inversely associated with non-fasting serum triglycerides: the Tromsø study. Nutr Metab Cardiovasc Dis 18, 256-262.
2. Basaria S, Coviello AD, Travison TG, Storer TW, Farwell WR, Jette AM & Bhasin S. (2010) Adverse events associated with testosterone administration. N Engl J Med 363, 109-122.
3. Bhasin S, Storer TW, Javanbakht M, Berman N, Yarasheski KE, Phillips J, Dike M, Sinha-Hikim I, Shen R, Hays RD & Beall G. (2000) Testosterone replacement and resistance exercise in HIV-infected men with weight loss and low testosterone levels. JAMA 283, 763-770.
4. Bhasin S, Parker RA, Sattler F, Haubrich R, Alston B, Umbleja T & Shikuma CM & AIDS Clinical Trials Group Protocol A5079 Study Team. (2007) Effects of testosterone supplementation on whole body and regional fat mass and distribution in human immunodeficiency virus-infected men with abdominal obesity. J Clin Endocrinol Metab 92, 1049-1057.
5. Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS & Montori VM. (2010) Testosterone therapy in men with androgen deficiency syndromes: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 95, 2536-2559.
6. Brand JS, Rovers MM, Yeap BB, Schneider HJ, Tuomainen TP, Haring R, Corona G, Onat A, Maggio M, Bouchard C, Tong PC, Chen RY, Akishita M, Gietema JA, Gannagé-Yared MH, Undén AL, Hautanen A, Goncharov NP, Kumanov P, Chubb SA, Almeida OP, Wittchen HU, Klotsche J, Wallaschofski H, Völzke H, Kauhanen J, Salonen JT, Ferrucci L & van der Schouw YT (2014) Testosterone, sex hormone-binding globulin and the metabolic syndrome in men: an individual participant data meta-analysis of observational studies. PLoS ONE 9, e100409.
7. Brothers TD, Kirkland S, Guaraldi G, Falutz J, Theou O, Johnston BL & Rockwood K. (2014) Frailty in people aging with human immunodeficiency virus (HIV) infection. J Infect Dis 210, 1170-1179.
8. Corona G, Monami M, Rastrelli G, Aversa A, Sforza A, Lenzi A, Forti G, Mannucci E & Maggi M. (2011a) Type 2 diabetes mellitus and testosterone: a meta-analysis study. Int J Androl 34, 528-540.
9. Corona G, Rastrelli G, Vignozzi L, Mannucci E & Maggi M. (2011b) Testosterone, cardiovascular disease and the metabolic syndrome. Best Pract Res Clin Endocrinol Metab 25, 337-353.
10. Corona G, Rastrelli G, Morelli A, Vignozzi L, Mannucci E & Maggi M. (2011c) Hypogonadism and metabolic syndrome. J Endocrinol Invest 34, 557-567.
11. Corona G, Rastrelli G, Monami M, Melani C, Balzi D, Sforza A, Forti G, Mannucci E & Maggi M. (2011d) Body mass index regulates hypogonadism-associated CV risk: results from a cohort of subjects with erectile dysfunction. J Sex Med 8, 2098-2105.
12. Corona G, Rastrelli G, Maseroli E, Fralassi N, Sforza A, Forti G, Mannucci E & Maggi M. (2014a) Low testosterone syndrome protects subjects with high cardiovascular risk burden from major adverse cardiovascular events. Andrology 2, 741-747.
13. Corona G, Rastrelli G, Filippi S, Vignozzi L, Mannucci E & Maggi M. (2014b) Erectile dysfunction and central obesity: an Italian perspective. Asian J Androl 16, 581-591.
14. Corona G, Maseroli E, Rastrelli G, Isidori AM, Sforza A, Mannucci E & Maggi M. (2014c) Cardiovascular risk associated with testosterone-boosting medications: a systematic review and meta-analysis. Expert Opin Drug Saf 13, 1327-1351.
15. Deeks SG & Phillips AN. (2009) HIV infection, antiretroviral treatment, ageing, and non-AIDS related morbidity. BMJ 338, a3172.
16. Deeks SG, Lewin SR & Havlir DV. (2013) The end of AIDS: HIV infection as a chronic disease. Lancet 382, 1525-1533.
17. Finkle WD, Greenland S, Ridgeway GK, Adams JL, Frasco MA, Cook MB, Fraumeni JF, Jr & Hoover RN. (2014) Increased risk of non-fatal myocardial infarction following testosterone therapy prescription in men. PLoS ONE 9, e85805.
18. Guaraldi G, Orlando G, Zona S, Menozzi M, Carli F, Garlassi E, Berti A, Rossi E, Roverato A & Palella F. (2011) Premature age-related comorbidities among HIV-infected persons compared with the general population. Clin Infect Dis 53, 1120-1126.
19. Guaraldi G, Silva AR & Stentarelli C. (2014a) Multimorbidity and functional status assessment. Curr Opin HIV AIDS 9, 386-397.
20. Guaraldi G, Prakash M, Moecklinghoff C & Stellbrink HJ. (2014b) Morbidity in older HIV-infected patients: impact of long-term antiretroviral use. AIDS Rev 16, 75-89.
21. Handelsman DJ. (2011) An old emperor finds new clothing: rejuvenation in our time. Asian J Androl 13, 125-129.
22. Iglesias P, Carrero JJ & Díez JJ. (2012) Gonadal dysfunction in men with chronic kidney disease: clinical features, prognostic implications and therapeutic options. J Nephrol 25, 31-42.
23. Kim S, Kwon H, Park JH, Cho B, Kim D, Oh SW, Lee CM & Choi HC. (2012) A low level of serum total testosterone is independently associated with nonalcoholic fatty liver disease. BMC Gastroenterol 12, 69.
24. Knapp PE, Storer TW, Herbst KL, Singh AB, Dzekov C, Dzekov J, LaValley M, Zhang A, Ulloor J & Bhasin S. (2008) Effects of a supraphysiological dose of testosterone on physical function, muscle performance, mood, and fatigue in men with HIV-associated weight loss. Am J Physiol Endocrinol Metab 294, E1135-E1143.
25. Lee DM, Tajar A, Pye SR, Boonen S, Vanderschueren D, Bouillon R, O'Neill TW, Bartfai G, Casanueva FF, Finn JD, Forti G, Giwercman A, Han TS, Huhtaniemi IT, Kula K, Lean ME, Pendleton N, Punab M, Wu FC & EMAS study group. (2012) Association of hypogonadism with vitamin D status: the European Male Ageing Study. Eur J Endocrinol 166, 77-85.
26. Martin J & Volberding P. (2010) HIV and premature aging: a field still in its infancy. Ann Intern Med 153, 477-479.
27. Miller KK. (2013) Endocrine effects of anorexia nervosa. Endocrinol Metab Clin North Am 42, 515-528.
28. Monroe AK, Dobs AS, Palella FJ, Kingsley LA, Witt MD & Brown TT. (2014) Morning free and total testosterone in HIV-infected men: implications for the assessment of hypogonadism. AIDS Res Ther 11, 6.
29. Moreno-Pérez O, Escoin C, Serna-Candel C, Portilla J, Boix V, Alfayate R, González-Sánchez V, Mauri M, Sánchez-Payá J & Picó A. (2010) The determination of total testosterone and free testosterone (RIA) are not applicable to the evaluation of gonadal function in HIV-infected males. J Sex Med 7, 2873-2883.
30. Morley JE & Melmed S. (1979) Gonadal dysfunction in systemic disorders. Metabolism 28, 1051-1073.
31. Muraleedharan V & Hugh Jones T. (2014) Testosterone and mortality. Clin Endocrinol (Oxf) 81, 477-487.
32. Ofotokun I & Weitzmann MN. (2010) HIV-1 infection and antiretroviral therapies: risk factors for osteoporosis and bone fracture. Curr Opin Endocrinol Diabetes Obes 17, 523-529.
33. Palella FJ, Jr, Delaney KM, Moorman AC, Loveless MO, Fuhrer J, Satten GA, Aschman DJ & Holmberg SD. (1998) Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl J Med 338, 853-860.
34. Palella FJ, Cole FR, Chmiel JS, Riddler SA, Visscher B, Dobs A & Williams C. (2004) Anthropometrics and examiner-reported body habitus abnormalities in the Multicenter AIDS Cohort Study. Clin Infect Dis 8, 903-907.
35. Ravindrarajah R, Lee DM, Pye SR, Gielen E, Boonen S, Vanderschueren D, Pendleton N, Finn JD, Tajar A, O'Connell MD, Rockwood K, Bartfai G, Casanueva FF, Forti G, Giwercman A, Han TS, Huhtaniemi IT, Kula K, Lean ME, Punab M, Wu FC, O'Neill TW & European Male Aging Study Group. (2013) The ability of three different models of frailty to predict all-cause mortality: results from the European Male Aging Study (EMAS). Arch Gerontol Geriatr 57, 360-368.
36. Rochira V & Guaraldi G. (2014) Hypogonadism in the HIV-infected male. Endocrinol Metab Clin North Am 43, 709-730.
37. Rochira V, Zirilli L, Orlando G, Santi D, Brigante G, Diazzi C, Carli F, Carani C & Guaraldi G. (2011) Premature decline of serum total testosterone in HIV-infected men in the HAART-era. PLoS ONE 6, e28512.
38. Rockwood K & Mitnitski A. (2007) Frailty in relation to the accumulation of deficits. J Gerontol A Biol Sci Med Sci 62, 722-727.
39. Rockwood K & Mitnitski A. (2011) Frailty defined by deficit accumulation and geriatric medicine defined by frailty. Clin Geriatr Med 27, 17-26.
40. Samaras K (2011) Endocrine disease in HIV infection. Best Pract Res Clin Endocrinol Metab 25, vii-viii.
41. Searle SD, Mitnitski A, Gahbauer EA, Gill TM & Rockwood K. (2008) A standard procedure for creating a frailty index. BMC Geriatr 8, 24.
42. Spratt DI, Cox P, Orav J, Moloney J & Bigos T. (1993) Reproductive axis suppression in acute illness is related to disease severity. J Clin Endocrinol Metab 76, 1548-1554.
43. Stanworth RD, Kapoor D, Channer KS & Jones TH. (2011) Dyslipidaemia is associated with testosterone, oestradiol and androgen receptor CAG repeat polymorphism in men with type 2 diabetes. Clin Endocrinol (Oxf) 74, 624-630.
44. Svartberg J, von Mühlen D, Schirmer H, Barrett-Connor E, Sundfjord J & Jorde R. (2004) Association of endogenous testosterone with blood pressure and left ventricular mass in men. The Tromsø Study. Eur J Endocrinol 150, 65-71.
45. Tajar A, Forti G, O'Neill TW, Lee DM, Silman AJ, Finn JD, Bartfai G, Boonen S, Casanueva FF, Giwercman A, Han TS, Kula K, Labrie F, Lean ME, Pendleton N, Punab M, Vanderschueren D, Huhtaniemi IT & Wu FC & the EMAS Group. (2010) Characteristics of secondary, primary, and compensated hypogonadism in aging men: evidence from the European Male Ageing Study. J Clin Endocrinol Metab 95, 1810-1818.
46. Tajar A, O'Connell MD, Mitnitski AB, O'Neill TW, Searle SD, Huhtaniemi IT, Finn JD, Bartfai G, Boonen S, Casanueva FF, Forti G, Giwercman A, Han TS, Kula K, Labrie F, Lean ME, Pendleton N, Punab M, Silman AJ, Vanderschueren D, Rockwood K, Wu FC & European Male Aging Study Group. (2011) Frailty in relation to variations in hormone levels of the hypothalamic-pituitary-testicular axis in older men: results from the European male aging study. J Am Geriatr Soc 59, 814-821.
47. Thacher TD & Clarke BL. (2011) Vitamin D insufficiency. Mayo Clin Proc 86, 50-60.
48. Travison TG, Araujo AB, Kupelian V, O'Donnell AB & McKinlay JB. (2007) The relative contributions of aging, health, and lifestyle factors to serum testosterone decline in men. J Clin Endocrinol Metab 92, 549-555.
49. Vigen R, O'Donnell CI, Barón AE, Grunwald GK, Maddox TM, Bradley SM, Barqawi A, Woning G, Wierman ME, Plomondon ME, Rumsfeld JS & Ho PM. (2013) Association of testosterone therapy with mortality, myocardial infarction, and stroke in men with low testosterone levels. JAMA 310, 1829-1836.
50. Vlachopoulos C, Ioakeimidis N, Terentes-Printzios D, Aznaouridis K, Rokkas K, Aggelis A, Synodinos A, Lazaros G & Stefanadis C. (2013) Plasma total testosterone and incident cardiovascular events in hypertensive patients. Am J Hypertens 26, 373-381.
51. Wang C, Jackson G, Jones TH, Matsumoto AM, Nehra A, Perelman MA, Swerdloff RS, Traish A, Zitzmann M & Cunningham G. (2011) Low testosterone associated with obesity and the metabolic syndrome contributes to sexual dysfunction and cardiovascular disease risk in men with type 2 diabetes. Diabetes Care 34, 1669-1675.
52. Warner MH & Beckett GJ. (2010) Mechanisms behind the non-thyroidal illness syndrome: an update. J Endocrinol 205, 1-13.
53. Woolf PD, Hamill RW, McDonald JV, Lee LA & Kelly M. (1985) Transient hypogonadotropic hypogonadism caused by critical illness. J Clin Endocrinol Metab 60, 444-450.
54. Wu FC, Tajar A, Beynon JM, Pye SR, Silman AJ, Finn JD, O'Neill TW, Bartfai G, Casanueva FF, Forti G, Giwercman A, Han TS, Kula K, Lean ME, Pendleton N, Punab M, Boonen S, Vanderschueren D, Labrie F & Huhtaniemi IT & EMAS Group. (2010) Identification of late-onset hypogonadism in middle-aged and elderly men. N Engl J Med 363, 123-135.
55. Xu L, Freeman G, Cowling BJ & Schooling CM. (2013) Testosterone therapy and cardiovascular events among men: a systematic review and meta-analysis of placebo-controlled randomized trials. BMC Med 11, 108.