Body composition changes with testosterone replacement therapy following spinal cord injury and aging: A mini review

References

• Walston JD. Sarcopenia in older adults. Curr Opin Rheumatol. 2012;24(6):623–7. doi: 10.1097/BOR.0b013e328358d59b
   PubMed Web of Science ®Google Scholar
• Bauman WA, Spungen AM. Disorders of carbohydrate and lipid-metabolism in veterans with paraplegia or quadriplegia - a model of premature aging. Metab-Clin Exp. 1994;43(6):749–56. doi: 10.1016/0026-0495(94)90126-0
   PubMed Web of Science ®Google Scholar
• Wilmet E, Ismail AA, Heilporn A, Welraeds D, Bergmann P. Longitudinal study of the bone mineral content and of soft tissue composition after spinal cord section. Paraplegia. 1995;33(11):674–7.
   PubMedGoogle Scholar
• Castro MJ, Apple DF, Staron RS, Campos GER, Dudley GA. Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury. J Appl Physiol. 1999;86(1):350–8. doi: 10.1152/jappl.1999.86.1.350
   PubMed Web of Science ®Google Scholar
• Spungen AM, Bauman WA, Wang J, Pierson RN, Jr. Measurement of body fat in individuals with tetraplegia: a comparison of eight clinical methods. Paraplegia. 1995;33(7):402–8.
   PubMedGoogle Scholar
• Buchholz AC, McGillivray CF, Pencharz PB. Physical activity levels are low in free-living adults with chronic paraplegia. Obes Res. 2003;11(4):563–70. doi: 10.1038/oby.2003.79
   PubMedGoogle Scholar
• Gorgey AS, Dudley GA. Skeletal muscle atrophy and increased intramuscular fat after incomplete spinal cord injury. Spinal Cord. 2007;45(4):304–9. doi: 10.1038/sj.sc.3101968
   PubMed Web of Science ®Google Scholar
• Shah PK, Gregory CM, Stevens JE, Pathare NC, Jayaraman A, Behrman AL, et al. Non-invasive assessment of lower extremity muscle composition after incomplete spinal cord injury. Spinal Cord. 2008;46(8):565–70. doi: 10.1038/sc.2008.10
   PubMed Web of Science ®Google Scholar
• Elder CP, Apple DF, Bickel CS, Meyer RA, Dudley GA. Intramuscular fat and glucose tolerance after spinal cord injury - a cross-sectional study. Spinal Cord. 2004;42(12):711–6. doi: 10.1038/sj.sc.3101652
   PubMed Web of Science ®Google Scholar
• Ryan TE, Brizendine JT, Young HJ, Erickson ML, McCully KK. Skeletal Muscle Metabolism and Glucose Tolerance after Spinal Cord Injury: Influence of Intramuscular Fat and Injury Duration. Med Sci Sports Exerc. 2012;44:688-.
   Web of Science ®Google Scholar
• Miljkovic I, Zmuda JM. Epidemiology of Myosteatosis. Curr Opin Clin Nutr Metab Care. 2010;13(3):260–4. doi: 10.1097/MCO.0b013e328337d826
   PubMed Web of Science ®Google Scholar
• Addison O, Marcus RL, LaStayo PC, Ryan AS. Intermuscular Fat: A Review of the Consequences and Causes. Int J Endocrinol. 2014;2014:309570. doi: 10.1155/2014/309570
   PubMed Web of Science ®Google Scholar
• Buchholz AC, McGillivray CF, Pencharz PB. Differences in resting metabolic rate between paraplegic and able-bodied subjects are explained by differences in body composition. Am J Clin Nutr. 2003;77(2):371–8. doi: 10.1093/ajcn/77.2.371
   PubMed Web of Science ®Google Scholar
• Gater DR. Obesity After Spinal Cord Injury. Phys Med Rehabil Clin N Am. 2007;18(2):333–51. doi: 10.1016/j.pmr.2007.03.004
   PubMedGoogle Scholar
• Edwards LA, Bugaresti JM, Buchholz AC. Visceral adipose tissue and the ratio of visceral to subcutaneous adipose tissue are greater in adults with than in those without spinal cord injury, despite matching waist circumferences. Am J Clin Nutr. 2008;87(3):600–7. doi: 10.1093/ajcn/87.3.600
   PubMed Web of Science ®Google Scholar
• Gorgey AS, Mather KJ, Gater DR. Central adiposity associations to carbohydrate and lipid metabolism in individuals with complete motor spinal cord injury. Metabolism. 2011;60(6):843–51. doi: 10.1016/j.metabol.2010.08.002
   PubMed Web of Science ®Google Scholar
• Bouloumie A, Curat CA, Sengenes C, Lolmede K, Miranville A, Busse R. Role of macrophage tissue infiltration in metabolic diseases. Curr Opin Clin Nutr Metab Care. 2005;8(4):347–54. doi: 10.1097/01.mco.0000172571.41149.52
   PubMed Web of Science ®Google Scholar
• Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH. Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Engl J Med. 1997;336(14):973–9. doi: 10.1056/NEJM199704033361401
   PubMed Web of Science ®Google Scholar
• Koenig W, Sund M, Frohlich M, Fischer HG, Lowel H, Doring A, et al. C-reactive protein, a sensitive marker of inflammation, predicts future risk of coronary heart disease in initially healthy middle-aged men - Results from the MONICA (Monitoring Trends and Determinants in Cardiovascular Disease) Augsburg Cohort Study, 1984 to 1992. Circulation. 1999;99(2):237–42. doi: 10.1161/01.CIR.99.2.237
   PubMed Web of Science ®Google Scholar
• Srikanthan P, Horwich TB, Tseng CH. Relation of Muscle Mass and Fat Mass to Cardiovascular Disease Mortality. Am J Cardiol. 117(8):1355–60. doi: 10.1016/j.amjcard.2016.01.033
   PubMed Web of Science ®Google Scholar
• Bassil N, Alkaade S, Morley JE. The benefits and risks of testosterone replacement therapy: a review. Ther Clin Risk Manag. 2009;5:427–48.
   PubMedGoogle Scholar
• Winter AG, Zhao F, Lee RK. Androgen deficiency and metabolic syndrome in men. Transl Androl and Urol. 2014;3(1):50–8.
   PubMedGoogle Scholar
• Sinha-Hikim I, Cornford M, Gaytan H, Lee ML, Bhasin S. Effects of Testosterone Supplementation on Skeletal Muscle Fiber Hypertrophy and Satellite Cells in Community-Dwelling Older Men. J Clin Endocrinol Metab. 2006;91(8):3024–33. doi: 10.1210/jc.2006-0357
   PubMed Web of Science ®Google Scholar
• Neto WK, Gama EF, Rocha LY, Ramos CC, Taets W, Scapini KB, et al. Effects of testosterone on lean mass gain in elderly men: systematic review with meta-analysis of controlled and randomized studies. Age. 2015;37(1):9742. doi: 10.1007/s11357-014-9742-0
   PubMedGoogle Scholar
• Sinha-Hikim I, Taylor WE, Gonzalez-Cadavid NF, Zheng W, Bhasin S. Androgen receptor in human skeletal muscle and cultured muscle satellite cells: up-regulation by androgen treatment. J Clin Endocrinol Metab. 2004;89(10):5245–55. doi: 10.1210/jc.2004-0084
   PubMed Web of Science ®Google Scholar
• De Pergola G. The adipose tissue metabolism: role of testosterone and dehydroepiandrosterone. International journal of obesity and related metabolic disorders. Int J Obes (Lond). 2000;24 Suppl 2:S59–63. doi: 10.1038/sj.ijo.0801280
   PubMed Web of Science ®Google Scholar
• Maggio M, Lauretani F, Ceda GP. Sex hormones and sarcopenia in older persons. Curr Opin Clin Nutr Metab Care. 2013;16(1):3–13.
   PubMed Web of Science ®Google Scholar
• O'Connell MD, Wu FC. Androgen effects on skeletal muscle: implications for the development and management of frailty. Asian J Androl. 2014;16(2):203–12. doi: 10.4103/1008-682X.122581
   PubMed Web of Science ®Google Scholar
• Ungureanu MC, Costache, II, Preda C, Mogos V, Vulpoi C, Leustean L. Myths and controversies in hypogonadism treatment of aging males. Rev Med Chir Soc Med Nat Iasi. 2015;119(2):325–33.
   PubMed Web of Science ®Google Scholar
• Lamberts SWJ, van den Beld AW, van der Lely A-J. The Endocrinology of Aging. Science. 1997;278(5337):419–24. doi: 10.1126/science.278.5337.419
   PubMed Web of Science ®Google Scholar
• Volpi E, Nazemi R, Fujita S. Muscle tissue changes with aging. Curr Opin Clin Nutr Metab Care. 2004;7(4):405–10. doi: 10.1097/01.mco.0000134362.76653.b2
   PubMed Web of Science ®Google Scholar
• Stanworth RD, Jones TH. Testosterone for the aging male; current evidence and recommended practice. Clin Interv Aging. 2008;3(1):25–44.
   PubMed Web of Science ®Google Scholar
• Yuki A, Otsuka R, Kozakai R, Kitamura I, Okura T, Ando F, et al. Relationship between low free testosterone levels and loss of muscle mass. Sci Rep. 2013;3:1818. doi: 10.1038/srep01818
   PubMed Web of Science ®Google Scholar
• Clark MJ, Schopp LH, Mazurek MO, Zaniletti I, Lammy AB, Martin TA, et al. Testosterone levels among men with spinal cord injury: relationship between time since injury and laboratory values. Am J Phys Med Rehabil. 2008;87(9):758–67. doi: 10.1097/PHM.0b013e3181837f4f
   PubMed Web of Science ®Google Scholar
• Bauman WA, La Fountaine MF, Spungen AM. Age-related prevalence of low testosterone in men with spinal cord injury. Journal Spinal Cord Med. 2014;37(1):32–9. doi: 10.1179/2045772313Y.0000000122
   PubMed Web of Science ®Google Scholar
• Milanović Z, Pantelić S, Trajković N, Sporiš G, Kostić R, James N. Age-related decrease in physical activity and functional fitness among elderly men and women. Clin Interv Aging. 2013;8:549–56. doi: 10.2147/CIA.S44112
   PubMed Web of Science ®Google Scholar
• Tsitouras PD, Zhong YG, Spungen AM, Bauman WA. Serum testosterone and growth hormone/insulin-like growth factor-I in adults with spinal cord injury. Horm Metab Res. 1995;27(6):287–92. doi: 10.1055/s-2007-979961
   PubMed Web of Science ®Google Scholar
• Durga A, Sepahpanah F, Regozzi M, Hastings J, Crane DA. Prevalence of Testosterone Deficiency After Spinal Cord Injury. Pm&R. 2011;3(10):929–32.
   Web of Science ®Google Scholar
• Ginis KAM, Latimer AE, Arbour-Nicitopoulos KP, Buchholz AC, Bray SR, Craven BC, et al. Leisure Time Physical Activity in a Population-Based Sample of People With Spinal Cord Injury Part I: Demographic and Injury-Related Correlates. Arch Phys Med Rehabil. 2010;91(5):722–8. doi: 10.1016/j.apmr.2009.12.027
   PubMed Web of Science ®Google Scholar
• McNicholas TA, Dean JD, Mulder H, Carnegie C, Jones NA. A novel testosterone gel formulation normalizes androgen levels in hypogonadal men, with improvements in body composition and sexual function. BJU International. 2003;91(1):69–74. doi: 10.1046/j.1464-410X.2003.04016.x
   PubMed Web of Science ®Google Scholar
• Wang C, Harnett M, Dobs AS, Swerdloff RS. Pharmacokinetics and safety of long-acting testosterone undecanoate injections in hypogonadal men: an 84-week phase III clinical trial. J Androl. 2010;31(5):457–65. doi: 10.2164/jandrol.109.009597
   PubMedGoogle Scholar
• Hadgraft J, Lane ME. Transdermal delivery of testosterone. Eur J Pharm Biopharm. 2015;92:42–8. doi: 10.1016/j.ejpb.2015.02.015
   PubMed Web of Science ®Google Scholar
• Ullah MI, Riche DM, Koch CA. Transdermal testosterone replacement therapy in men. Drug Des Devel Ther. 2014;8:101–12.
   PubMed Web of Science ®Google Scholar
• Bauman WA, Cirnigliaro CM, La Fountaine MF, Jensen AM, Wecht JM, Kirshblum SC, et al. A small-scale clinical trial to determine the safety and efficacy of testosterone replacement therapy in hypogonadal men with spinal cord injury. Horm Metab Res. 2011;43(8):574–9. doi: 10.1055/s-0031-1280797
   PubMed Web of Science ®Google Scholar
• Bauman WA, La Fountaine MF, Cirnigliaro CM, Kirshblum SC, Spungen AM. Testicular responses to hCG stimulation at varying doses in men with spinal cord injury. Spinal Cord. 2017.
   Google Scholar
• Rastrelli G, Carter EL, Ahern T, Finn JD, Antonio L, O'Neill TW, et al. Development of and Recovery from Secondary Hypogonadism in Aging Men: Prospective Results from the EMAS. J Clin Endocrinol Metab. 2015;100(8):3172–82. doi: 10.1210/jc.2015-1571
   PubMed Web of Science ®Google Scholar
• McBride JA, Carson CC, Coward RM. Testosterone deficiency in the aging male. Ther Adv Urol. 2016;8(1):47–60. doi: 10.1177/1756287215612961
   PubMed Web of Science ®Google Scholar
• Hildreth KL, Barry DW, Moreau KL, Vande Griend J, Meacham RB, Nakamura T, et al. Effects of Testosterone and Progressive Resistance Exercise in Healthy, Highly Functioning Older Men With Low-Normal Testosterone Levels. J Clin Endocrinol Metab. 2013;98(5):1891–900. doi: 10.1210/jc.2012-3695
   PubMed Web of Science ®Google Scholar
• Wang C, Swerdloff RS, Iranmanesh A, Dobs A, Snyder PJ, Cunningham G, et al. Transdermal Testosterone Gel Improves Sexual Function, Mood, Muscle Strength, and Body Composition Parameters in Hypogonadal Men1. J Clin Endocrinol Metab. 2000;85(8):2839–53.
   PubMed Web of Science ®Google Scholar
• Steidle C, Schwartz S, Jacoby K, Sebree T, Smith T, Bachand R. AA2500 Testosterone Gel Normalizes Androgen Levels in Aging Males with Improvements in Body Composition and Sexual Function. J Clin Endocrinol Metab. 2003;88(6):2673–81. doi: 10.1210/jc.2002-021058
   PubMed Web of Science ®Google Scholar
• Frederiksen L, Højlund K, Hougaard DM, Brixen K, Andersen M. Testosterone therapy increased muscle mass and lipid oxidation in aging men. AGE. 2012;34(1):145–56. doi: 10.1007/s11357-011-9213-9
   PubMedGoogle Scholar
• Magnussen LV, Glintborg D, Hermann P, Hougaard DM, Højlund K, Andersen M. Effect of testosterone on insulin sensitivity, oxidative metabolism and body composition in aging men with type 2 diabetes on metformin monotherapy. Diabetes Obes Metab. 2016;18(10):980–9. doi: 10.1111/dom.12701
   PubMed Web of Science ®Google Scholar
• Srinivas-Shankar U, Roberts SA, Connolly MJ, O'Connell MD, Adams JE, Oldham JA, et al. Effects of testosterone on muscle strength, physical function, body composition, and quality of life in intermediate-frail and frail elderly men: a randomized, double-blind, placebo-controlled study. J Clin Endocrinol Metab. 2010;95(2):639–50. doi: 10.1210/jc.2009-1251
   PubMed Web of Science ®Google Scholar
• Behre HM, Tammela TL, Arver S, Tolra JR, Bonifacio V, Lamche M, et al. A randomized, double-blind, placebo-controlled trial of testosterone gel on body composition and health-related quality-of-life in men with hypogonadal to low-normal levels of serum testosterone and symptoms of androgen deficiency over 6 months with 12 months open-label follow-up. Aging Male. 2012;15(4):198–207. doi: 10.3109/13685538.2012.699562
   PubMed Web of Science ®Google Scholar
• Kenny AM, Kleppinger A, Annis K, Rathier M, Browner B, Judge JO, et al. Effects of Transdermal Testosterone on Bone and Muscle in Older Men with Low Bioavailable Testosterone Levels, Low Bone Mass and Physical Frailty. J Am Geriatr Soc. 2010;58(6):1134–43. doi: 10.1111/j.1532-5415.2010.02865.x
   PubMed Web of Science ®Google Scholar
• Snyder PJ, Peachey H, Hannoush P, Berlin JA, Loh L, Lenrow DA, et al. Effect of testosterone treatment on body composition and muscle strength in men over 65 years of age. J Clin Endocrinol Metab. 1999;84(8):2647–53.
   PubMed Web of Science ®Google Scholar
• Wang C, Cunningham G, Dobs A, Iranmanesh A, Matsumoto AM, Snyder PJ, et al. Long-term testosterone gel (AndroGel) treatment maintains beneficial effects on sexual function and mood, lean and fat mass, and bone mineral density in hypogonadal men. J Clin Endocrinol Metab. 2004;89(5):2085–98. doi: 10.1210/jc.2003-032006
   PubMed Web of Science ®Google Scholar
• Storer TW, Basaria S, Traustadottir T, Harman SM, Pencina K, Li Z, et al. Effects of Testosterone Supplementation for 3 Years on Muscle Performance and Physical Function in Older Men. J Clin Endocrinol Metab. 2017;102(2):583–93.
   PubMed Web of Science ®Google Scholar
• Bhasin S, Parker RA, Sattler F, Haubrich R, Alston B, Umbleja T, et al. 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. 2007;92(3):1049–57. doi: 10.1210/jc.2006-2060
   PubMed Web of Science ®Google Scholar
• Behre HM, Kliesch S, Leifke E, Link TM, Nieschlag E. Long-Term Effect of Testosterone Therapy on Bone Mineral Density in Hypogonadal Men. J Clin Endocrinol Metab. 1997;82(8):2386–90. doi: 10.1210/jcem.82.8.4163
   PubMed Web of Science ®Google Scholar
• Snyder PJ, Peachey H, Hannoush P, Berlin JA, Loh L, Holmes JH, et al. Effect of testosterone treatment on bone mineral density in men over 65 years of age. J Clin Endocrinol Metab. 1999;84(6):1966–72.
   PubMed Web of Science ®Google Scholar
• Basurto L, Zarate, A., Gomez, R., Vargas, C., Saucedo, R., Galván, R. Effect of testosterone therapy on lumbar spine and hip mineral density in elderly men. Aging Male. 2008;11(3):140–5. doi: 10.1080/13685530802273715
   PubMed Web of Science ®Google Scholar
• Tracz MJ, Sideras K, Boloña ER, Haddad RM, Kennedy CC, Uraga MV, et al. Testosterone Use in Men and Its Effects on Bone Health. A Systematic Review and Meta-Analysis of Randomized Placebo-Controlled Trials. J Clin Endocrinol Metab. 2006;91(6):2011–6. doi: 10.1210/jc.2006-0036
   PubMed Web of Science ®Google Scholar
• Snyder PJ, Kopperdahl DL, Stephens-Shields AJ, Ellenberg SS, Cauley JA, Ensrud KE. et al. Effect of testosterone treatment on volumetric bone density and strength in older men with low testosterone: A controlled clinical trial. JAMA Intern Med. 2017;177(4):471–9. doi: 10.1001/jamainternmed.2016.9539
   PubMed Web of Science ®Google Scholar
• Borst SE, Yarrow JF. Injection of testosterone may be safer and more effective than transdermal administration for combating loss of muscle and bone in older men. Am J of Physiol Endocrinol Metab. 2015;308(12):E1035–E42. doi: 10.1152/ajpendo.00111.2015
   PubMed Web of Science ®Google Scholar
• Isidori AM, Giannetta E, Greco EA, Gianfrilli D, Bonifacio V, Isidori A, et al. Effects of testosterone on body composition, bone metabolism and serum lipid profile in middle-aged men: a meta-analysis. Clin Endocrinol (Oxf). 2005;63(3):280–93. doi: 10.1111/j.1365-2265.2005.02339.x
   PubMed Web of Science ®Google Scholar
• Yarrow JF, Conover CF, Beggs LA, Beck DT, Otzel DM, Balaez A, et al. Testosterone dose dependently prevents bone and muscle loss in rodents after spinal cord injury. J Neurotrauma. 2014;31(9):834–45. doi: 10.1089/neu.2013.3155
   PubMed Web of Science ®Google Scholar
• Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS, et al. Testosterone Therapy in Men with Androgen Deficiency Syndromes: An Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab. 2010;95(6):2536–59. doi: 10.1210/jc.2009-2354
   PubMed Web of Science ®Google Scholar
• Dohle GR, Arver, S., Bettocchi, C., Kliesch, S., Punab, M., De Ronde W. Guidelines on male hypogonadism. In: Urology EAo, editor. first ed. Arnhem (The Netherlands) 2012.
   Google Scholar
• Moore PD, Gorgey AS, Wade RC, Khalil RE, Lavis TD, Khan R, et al. Neuromuscular electrical stimulation and testosterone did not influence heterotopic ossification size after spinal cord injury: A case series. World J Clin Cases. 2016;4(7):172–6. doi: 10.12998/wjcc.v4.i7.172
   PubMed Web of Science ®Google Scholar
• Aversa A, Bruzziches R, Francomano D, Rosano G, Isidori AM, Lenzi A, et al. Effects of Testosterone Undecanoate on Cardiovascular Risk Factors and Atherosclerosis in Middle-Aged Men with Late-Onset Hypogonadism and Metabolic Syndrome: Results from a 24-month, Randomized, Double-Blind, Placebo-Controlled Study. J Sex Med. 2010;7(10):3495–503. doi: 10.1111/j.1743-6109.2010.01931.x
   PubMed Web of Science ®Google Scholar
• Bauman WA, Spungen AM. Coronary heart disease in individuals with spinal cord injury: assessment of risk factors. Spinal Cord. 2008;46(7):466–76. doi: 10.1038/sj.sc.3102161
   PubMed Web of Science ®Google Scholar
• Gilbert O, Croffoot JR, Taylor AJ, Nash M, Schomer K, Groah S. Serum lipid concentrations among persons with spinal cord injury - A systematic review and meta-analysis of the literature. Atherosclerosis. 2014;232(2):305–12. doi: 10.1016/j.atherosclerosis.2013.11.028
   PubMed Web of Science ®Google Scholar
• Kressler J, Cowan RE, Bigford GE, Nash MS. Reducing Cardiometabolic Disease in Spinal Cord Injury. Phys Med Rehabil Clin N Am. 2014;25(3):573-+. doi: 10.1016/j.pmr.2014.04.006
   PubMed Web of Science ®Google Scholar
• Corona G, Giagulli VA, Maseroli E, Vignozzi L, Aversa A, Zitzmann M, et al. Testosterone supplementation and body composition: results from a meta-analysis of observational studies. J Endocrinol Invest. 2016;39(9):967–81. doi: 10.1007/s40618-016-0480-2
   PubMed Web of Science ®Google Scholar
• Bauman WA, La Fountaine MF, Cirnigliaro CM, Kirshblum SC, Spungen AM. Lean tissue mass and energy expenditure are retained in hypogonadal men with spinal cord injury after discontinuation of testosterone replacement therapy. J Spinal Cord Med. 2015;38(1):38–47. doi: 10.1179/2045772314Y.0000000206
   PubMed Web of Science ®Google Scholar
• Barbonetti A, Caterina Vassallo MR, Cotugno M, Felzani G, Francavilla S, Francavilla F. Low testosterone and non-alcoholic fatty liver disease: Evidence for their independent association in men with chronic spinal cord injury. J Spinal Cord Med. 2016;39(4):443–9. doi: 10.1179/2045772314Y.0000000288
   PubMed Web of Science ®Google Scholar
• Paschos P, Paletas K. Non alcoholic fatty liver disease and metabolic syndrome. Hippokratia. 2009;13(1):9–19.
   PubMed Web of Science ®Google Scholar
• Basaria S, Coviello AD, Travison TG, Storer TW, Farwell WR, Jette AM, et al. Adverse Events Associated with Testosterone Administration. N Engl J Med. 2010;363(2):109–22. doi: 10.1056/NEJMoa1000485
   PubMed Web of Science ®Google Scholar
• Alexander GC, Iyer G, Lucas E, Lin D, Singh S. Cardiovascular Risks of Exogenous Testosterone Use Among Men: A Systematic Review and Meta-Analysis. Am J Med. 2017;130(3):293–305. doi: 10.1016/j.amjmed.2016.09.017
   PubMed Web of Science ®Google Scholar
• U.S. Food and Drug Administration. FDA Drug Safety Communications: FDA cautions about using testosterone products for low testosterone due to aging; requires labeling change to inform of possible increased risk of heart attack and stroke with use. 2015 [Available from: http://www.fda.gov/downloads/Drugs/DrugSafety/UCM436270.pdf.] Accessed June 2, 2017.
   Google Scholar
• Traish A. Testosterone therapy in men with testosterone deficiency: Are we beyond the point of no return? Investig Clin Urol. 2016;57(6):384–400. doi: 10.4111/icu.2016.57.6.384
   PubMed Web of Science ®Google Scholar
• Shores MM, Smith NL, Forsberg CW, Anawalt BD, Matsumoto AM. Testosterone treatment and mortality in men with low testosterone levels. J Clin Endocrinol Metab. 2012;97(6):2050–8. doi: 10.1210/jc.2011-2591
   PubMed Web of Science ®Google Scholar
• Sharma R, Oni OA, Gupta K, Chen G, Sharma M, Dawn B, et al. Normalization of testosterone level is associated with reduced incidence of myocardial infarction and mortality in men. Eur Heart J. 2015;36(40):2706–15. doi: 10.1093/eurheartj/ehv346
   PubMed Web of Science ®Google Scholar
• Cheetham T, An J, Jacobsen SJ, Niu F, Sidney, S, Quesenberry, CP, et al. Association of testosterone replacement with cardiovascular outcomes among men with androgen deficiency. JAMA Intern Med. 2017;177(4):491–9. doi: 10.1001/jamainternmed.2016.9546
   PubMed Web of Science ®Google Scholar
• Corona G, Maseroli E, Rastrelli G, Isidori AM, Sforza A, Mannucci E, et al. Cardiovascular risk associated with testosterone-boosting medications: a systematic review and meta-analysis. Expert Opin Drug Saf. 2014;13(10):1327–51. doi: 10.1517/14740338.2014.950653
   PubMed Web of Science ®Google Scholar
• Onasanya O, Iyer G, Lucas E, Lin D, Singh S, Alexander GC. Association between exogenous testosterone and cardiovascular events: an overview of systematic reviews. Lancet Diabetes Endocrinol. 2016;4(11):943–56. doi: 10.1016/S2213-8587(16)30215-7
   PubMed Web of Science ®Google Scholar
• Xu L, Freeman G, Cowling BJ, Schooling CM. Testosterone therapy and cardiovascular events among men: a systematic review and meta-analysis of placebo-controlled randomized trials. BMC Medicine. 2013;11(1):108. doi: 10.1186/1741-7015-11-108
   PubMed Web of Science ®Google Scholar
• Vigen R, O'Donnell CI, Baron AE, Grunwald GK, Maddox TM, Bradley SM, et al. Association of testosterone therapy with mortality, myocardial infarction, and stroke in men with low testosterone levels. JAMA. 2013;310(17):1829–36. doi: 10.1001/jama.2013.280386
   PubMed Web of Science ®Google Scholar
• Finkle WD, Greenland S, Ridgeway GK, Adams JL, Frasco MA, Cook MB, et al. Increased Risk of Non-Fatal Myocardial Infarction Following Testosterone Therapy Prescription in Men. PLoS One. 2014;9(1):e85805. doi: 10.1371/journal.pone.0085805
   PubMed Web of Science ®Google Scholar
• Maggi M, Wu FC, Jones TH, Jackson G, Behre HM, Hackett G, et al. Testosterone treatment is not associated with increased risk of adverse cardiovascular events: results from the Registry of Hypogonadism in Men (RHYME). Int J Clin Pract. 2016;70(10):843–52. doi: 10.1111/ijcp.12876
   PubMed Web of Science ®Google Scholar
• Borst SE, Shuster JJ, Zou B, Ye F, Jia H, Wokhlu A, et al. Cardiovascular risks and elevation of serum DHT vary by route of testosterone administration: a systematic review and meta-analysis. BMC Med. 2014;12:211. doi: 10.1186/s12916-014-0211-5
   PubMed Web of Science ®Google Scholar
• Layton JB, Meier CR, Sharpless JL, Sturmer T, Jick SS, Brookhart MA. Comparative Safety of Testosterone Dosage Forms. JAMA Intern Med. 2015;175(7):1187–96. doi: 10.1001/jamainternmed.2015.1573
   PubMed Web of Science ®Google Scholar
• Albert SG, Morley JE. Testosterone therapy, association with age, initiation and mode of therapy with cardiovascular events: a systematic review. Clin Endocrinol (Oxf). 2016;85(3):436–43. doi: 10.1111/cen.13084
   PubMed Web of Science ®Google Scholar
• Snyder PJ, Peachey H, Berlin JA, Hannoush P, Haddad G, Dlewati A, et al. Effects of testosterone replacement in hypogonadal men. J Clin Endocrinol Metab. 2000;85(8):2670–7.
   PubMed Web of Science ®Google Scholar
• Sharma R, Oni OA, Chen G, Sharma M, Dawn B, Sharma R, et al. Association Between Testosterone Replacement Therapy and the Incidence of DVT and Pulmonary Embolism: A Retrospective Cohort Study of the Veterans Administration Database. Chest. 2016;150(3):563–71. doi: 10.1016/j.chest.2016.05.007
   PubMed Web of Science ®Google Scholar
• Martinez C, Suissa S, Rietbrock S, Katholing A, Freedman B, Cohen AT, et al. Testosterone treatment and risk of venous thromboembolism: population based case-control study. BMJ. 2016;355:i5968. doi: 10.1136/bmj.i5968
   PubMed Web of Science ®Google Scholar
• Roy CN, Snyder PJ, Stephens-Shields AJ, Artz AS, Bhasin S, Cohen HJ, et al. Association of testosterone levels with anemia in older men: A controlled clinical trial. JAMA Intern Med. 2017;177(4):480–90. doi: 10.1001/jamainternmed.2016.9540
   PubMed Web of Science ®Google Scholar
• Calof OM, Singh AB, Lee ML, Kenny AM, Urban RJ, Tenover JL, et al. Adverse events associated with testosterone replacement in middle-aged and older men: a meta-analysis of randomized, placebo-controlled trials. J Gerontol A Biol Sci Med Sci. 2005;60(11):1451–7. doi: 10.1093/gerona/60.11.1451
   PubMed Web of Science ®Google Scholar
• Grech A, Breck J, Heidelbaugh J. Adverse effects of testosterone replacement therapy: an update on the evidence and controversy. Ther Adv Drug Saf. 2014;5(5):190–200. doi: 10.1177/2042098614548680
   PubMedGoogle Scholar
• Boyle P, Koechlin A, Bota M, d'Onofrio A, Zaridze DG, Perrin P, et al. Endogenous and exogenous testosterone and the risk of prostate cancer and increased prostate-specific antigen (PSA) level: a meta-analysis. BJU Int. 2016;118(5):731–41. doi: 10.1111/bju.13417
   PubMed Web of Science ®Google Scholar
• Debruyne FM, Behre HM, Roehrborn CG, Maggi M, Wu FC, Schroder FH, et al. Testosterone treatment is not associated with increased risk of prostate cancer or worsening of lower urinary tract symptoms: prostate health outcomes in the Registry of Hypogonadism in Men. BJU Int. 2017;119(2):216–24. doi: 10.1111/bju.13578
   PubMed Web of Science ®Google Scholar
• Gurakar A, Caraceni P, Fagiuoli S, Van Thiel DH. Androgenic/anabolic steroid-induced intrahepatic cholestasis: a review with four additional case reports. J Okla State Med Assoc. 1994;87(9):399–404.
   PubMedGoogle Scholar
• La Fountaine MF, Wecht JM, Cirnigliaro CM, Kirshblum SC, Spungen AM, Bauman WA. Testosterone replacement therapy improves QTaVI in hypogonadal men with spinal cord injury. Neuroendocrinology. 2013;97(4):341–6. doi: 10.1159/000347070
   PubMed Web of Science ®Google Scholar
• La Fountaine MF, Wecht JM, Cirnigliaro CM, Kirshblum SC, Spungen AM, Bauman WA. QT/RR Coherence Is Associated with Testosterone Levels in Men with Chronic Spinal Cord Injury. Neuroendocrinology. 2011;93(3):174–80. doi: 10.1159/000323773
   PubMed Web of Science ®Google Scholar
• Berger RD, Kasper EK, Baughman KL, Marban E, Calkins H, Tomaselli GF. Beat-to-beat QT interval variability: novel evidence for repolarization lability in ischemic and nonischemic dilated cardiomyopathy. Circulation. 1997;96(5):1557–65. doi: 10.1161/01.CIR.96.5.1557
   PubMed Web of Science ®Google Scholar
• Atiga WL, Calkins, H., Lawrence, J.H., Tomaseli, G.F., Smith, J.M., Berger, R.D. Beat-to-beat repolarization lability identifies patients at risk for sudden cardiac death. J Cardiovasc Electrophysiol. 1998;9:899–908. doi: 10.1111/j.1540-8167.1998.tb00130.x
   PubMed Web of Science ®Google Scholar
• Yekutiel M, Brooks ME, Ohry A, Yarom J, Carel R. The prevalence of hypertension, ischemic heart-disease and diabetes in traumatic spinal-cord injured patients and amputees. Paraplegia. 1989;27(1):58–62.
   PubMedGoogle Scholar
• Bauman WA, Kahn NN, Grimm DR, Spungen AM. Risk factors for atherogenesis and cardiovascular autonomic function in persons with spinal cord injury. Spinal Cord. 1999;37(9):601–16. doi: 10.1038/sj.sc.3100911
   PubMed Web of Science ®Google Scholar
• Krassioukov A, Claydon VE. The clinical problems in cardiovascular control following spinal cord injury: an overview. Prog Brain Res. 2006;152:223–9. doi: 10.1016/S0079-6123(05)52014-4
   PubMed Web of Science ®Google Scholar
• Myers J, Lee M, Kiratli J. Cardiovascular Disease in Spinal Cord Injury. Am J Phys Med Rehabil. 2007;86(2):142–52. doi: 10.1097/PHM.0b013e31802f0247
   PubMed Web of Science ®Google Scholar
• Budoff MJ, Ellenberg SS, Lewis CE, Mohler III ER, Wenger NK, Bhasin S, et al. Testosterone treatment and coronary artery plaque volume in older men with low testosterone. JAMA. 2017;317(7):708–16. doi: 10.1001/jama.2016.21043
   PubMed Web of Science ®Google Scholar
• Arbab-Zadeh A, Fuster V. The Myth of “The Vulnerable Plaque”: Transitioning from a Focus on Individual Lesions to Atherosclerotic Disease Burden for Coronary Artery Disease Risk Assessment. J Am Coll Cardiol. 2015;65(8):846–55. doi: 10.1016/j.jacc.2014.11.041
   PubMed Web of Science ®Google Scholar
• Gorgey AS, Khalil RE, Gill R, O'Brien LC, Lavis T, Castillo T, et al. Effects of Testosterone and Evoked Resistance Exercise after Spinal Cord Injury (TEREX-SCI): study protocol for a randomised controlled trial. BMJ Open. 2017;7(4):e014125. doi: 10.1136/bmjopen-2016-014125
   PubMed Web of Science ®Google Scholar
• Spungen AM, Wang J, Pierson RN, Bauman WA. Soft tissue body composition differences in monozygotic twins discordant for spinal cord injury. J Appl Physiol. 2000;88(4):1310–5. doi: 10.1152/jappl.2000.88.4.1310
   PubMed Web of Science ®Google Scholar
• DeFronzo RA. The Triumvirate: β-Cell, Muscle, Liver: A Collusion Responsible for NIDDM. Diabetes. 1988;37(6):667–87. doi: 10.2337/diab.37.6.667
   PubMed Web of Science ®Google Scholar
• Griffin L, Decker MJ, Hwang JY, Wang B, Kitchen K, Ding Z, et al. Functional electrical stimulation cycling improves body composition, metabolic and neural factors in persons with spinal cord injury. J Electromyogr Kinesiol. 2009;19(4):614–22. doi: 10.1016/j.jelekin.2008.03.002
   PubMed Web of Science ®Google Scholar
• LaVela SL, Weaver FM, Goldstein B, Chen K, Miskevics S, Rajan S, et al. Diabetes mellitus in individuals with spinal cord injury or disorder. J Spinal Cord Med. 2006;29(4):387–95. doi: 10.1080/10790268.2006.11753887
   PubMed Web of Science ®Google Scholar
• Lai YJ, Lin CL, Chang YJ, Lin MC, Lee ST, Sung FC, et al. Spinal cord injury increases the risk of Type 2 diabetes: a population-based cohort study. Spine Journal. 2014;14(9):1957–64. doi: 10.1016/j.spinee.2013.12.011
   PubMed Web of Science ®Google Scholar