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Muscular responses to testosterone replacement vary by administration route: a systematic review and meta‐analysis
dc.contributor.authorSkinner, Jared W.
dc.contributor.authorOtzel, Dana M.
dc.contributor.authorBowser, Andrew
dc.contributor.authorNargi, Daniel
dc.contributor.authorAgarwal, Sanjay
dc.contributor.authorPeterson, Mark D.
dc.contributor.authorZou, Baiming
dc.contributor.authorBorst, Stephen E.
dc.contributor.authorYarrow, Joshua F.
dc.date.accessioned2018-06-11T17:59:13Z
dc.date.available2019-08-01T19:53:23Zen
dc.date.issued2018-06
dc.identifier.citationSkinner, Jared W.; Otzel, Dana M.; Bowser, Andrew; Nargi, Daniel; Agarwal, Sanjay; Peterson, Mark D.; Zou, Baiming; Borst, Stephen E.; Yarrow, Joshua F. (2018). "Muscular responses to testosterone replacement vary by administration route: a systematic review and meta‐analysis." Journal of Cachexia, Sarcopenia and Muscle 9(3): 465-481.
dc.identifier.issn2190-5991
dc.identifier.issn2190-6009
dc.identifier.urihttps://hdl.handle.net/2027.42/144237
dc.description.abstractBackgroundInconsistent fat‐free mass (FFM) and muscle strength responses have been reported in randomized clinical trials (RCTs) administering testosterone replacement therapy (TRT) to middle‐aged and older men. Our objective was to conduct a meta‐analysis to determine whether TRT improves FFM and muscle strength in middle‐aged and older men and whether the muscular responses vary by TRT administration route.MethodsSystematic literature searches of MEDLINE/PubMed and the Cochrane Library were conducted from inception through 31 March 2017 to identify double‐blind RCTs that compared intramuscular or transdermal TRT vs. placebo and that reported assessments of FFM or upper‐extremity or lower‐extremity strength. Studies were identified, and data were extracted and validated by three investigators, with disagreement resolved by consensus. Using a random effects model, individual effect sizes (ESs) were determined from 31 RCTs reporting FFM (sample size: n = 1213 TRT, n = 1168 placebo) and 17 reporting upper‐extremity or lower‐extremity strength (n = 2572 TRT, n = 2523 placebo). Heterogeneity was examined, and sensitivity analyses were performed.ResultsWhen administration routes were collectively assessed, TRT was associated with increases in FFM [ES = 1.20 ± 0.15 (95% CI: 0.91, 1.49)], total body strength [ES = 0.90 ± 0.12 (0.67, 1.14)], lower‐extremity strength [ES = 0.77 ± 0.16 (0.45, 1.08)], and upper‐extremity strength [ES = 1.13 ± 0.18 (0.78, 1.47)] (P < 0.001 for all). When administration routes were evaluated separately, the ES magnitudes were larger and the per cent changes were 3–5 times greater for intramuscular TRT than for transdermal formulations vs. respective placebos, for all outcomes evaluated. Specifically, intramuscular TRT was associated with a 5.7% increase in FFM [ES = 1.49 ± 0.18 (1.13, 1.84)] and 10–13% increases in total body strength [ES = 1.39 ± 0.12 (1.15, 1.63)], lower‐extremity strength [ES = 1.39 ± 0.17 (1.07, 1.72)], and upper‐extremity strength [ES = 1.37 ± 0.17 (1.03, 1.70)] (P < 0.001 for all). In comparison, transdermal TRT was associated with only a 1.7% increase in FFM [ES = 0.98 ± 0.21 (0.58, 1.39)] and only 2–5% increases in total body [ES = 0.55 ± 0.17 (0.22, 0.88)] and upper‐extremity strength [ES = 0.97 ± 0.24 (0.50, 1.45)] (P < 0.001). Interestingly, transdermal TRT produced no change in lower‐extremity strength vs. placebo [ES = 0.26 ± 0.23 (−0.19, 0.70), P = 0.26]. Subanalyses of RCTs limiting enrolment to men ≥60 years of age produced similar results.ConclusionsIntramuscular TRT is more effective than transdermal formulations at increasing LBM and improving muscle strength in middle‐aged and older men, particularly in the lower extremities.
dc.publisherAcademic Press, Inc
dc.publisherWiley Periodicals, Inc.
dc.subject.otherLean mass
dc.subject.otherStrength
dc.subject.otherMuscle
dc.subject.otherAgeing
dc.subject.otherAndrogen
dc.subject.otherMusculoskeletal
dc.subject.otherFat‐free mass
dc.titleMuscular responses to testosterone replacement vary by administration route: a systematic review and meta‐analysis
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelInternal Medicine
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/144237/1/jcsm12291.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/144237/2/jcsm12291_am.pdf
dc.identifier.doi10.1002/jcsm.12291
dc.identifier.sourceJournal of Cachexia, Sarcopenia and Muscle
dc.identifier.citedreferenceDel Fabbro E, Garcia JM, Dev R, Hui D, Williams J, Engineer D, et al. Testosterone replacement for fatigue in hypogonadal ambulatory males with advanced cancer: a preliminary double‐blind placebo‐controlled trial. Support Care Cancer 2013; 21: 2599 – 2607.
dc.identifier.citedreferenceSvartberg J, Aasebo U, Hjalmarsen A, Sundsfjord J, Jorde R. Testosterone treatment improves body composition and sexual function in men with COPD, in a 6‐month randomized controlled trial. Respir Med 2004; 98: 906 – 913.
dc.identifier.citedreferenceSvartberg J, Agledahl I, Figenschau Y, Sildnes T, Waterloo K, Jorde R. Testosterone treatment in elderly men with subnormal testosterone levels improves body composition and BMD in the hip. Int J Impot Res 2008; 20: 378 – 387.
dc.identifier.citedreferenceTenover JS. Effects of testosterone supplementation in the aging male. J Clin Endocrinol Metab 1992; 75: 1092 – 1098.
dc.identifier.citedreferenceTravison TG, Basaria S, Storer TW, Jette AM, Miciek R, Farwell WR, et al. Clinical meaningfulness of the changes in muscle performance and physical function associated with testosterone administration in older men with mobility limitation. J Gerontol A Biol Sci Med Sci 2011; 66: 1090 – 1099.
dc.identifier.citedreferenceBasaria 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: 109 – 122.
dc.identifier.citedreferenceDias JP, Melvin D, Simonsick EM, Carlson O, Shardell MD, Ferrucci L, et al. Effects of aromatase inhibition vs. testosterone in older men with low testosterone: randomized‐controlled trial. Andrology 2016; 4: 33 – 40.
dc.identifier.citedreferenceMalkin CJ, Pugh PJ, West JN, van Beek EJ, Jones TH, Channer KS. Testosterone therapy in men with moderate severity heart failure: a double‐blind randomized placebo controlled trial. Eur Heart J 2006; 27: 57 – 64.
dc.identifier.citedreferenceSih R, Morley JE, Kaiser FE, Perry HM 3rd, Patrick P, Ross C. Testosterone replacement in older hypogonadal men: a 12‐month randomized controlled trial. J Clin Endocrinol Metab 1997; 82: 1661 – 1667.
dc.identifier.citedreferenceSinclair M, Grossmann M, Hoermann R, Angus PW, Gow PJ. Testosterone therapy increases muscle mass in men with cirrhosis and low testosterone: a randomised controlled trial. J Hepatol 2016; 65: 906 – 913.
dc.identifier.citedreferenceBaillargeon J, Urban RJ, Ottenbacher KJ, Pierson KS, Goodwin JS. Trends in androgen prescribing in the United States, 2001 to 2011. JAMA Intern Med 2013; 173: 1465 – 1466.
dc.identifier.citedreferenceNian Y, Ding M, Hu S, He H, Cheng S, Yi L, et al. Testosterone replacement therapy improves health‐related quality of life for patients with late‐onset hypogonadism: a meta‐analysis of randomized controlled trials. Andrologia 2017; 49.
dc.identifier.citedreferenceTracz MJ, Sideras K, Bolona 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: 2011 – 2016.
dc.identifier.citedreferenceCorona G, Giagulli VA, Maseroli E, Vignozzi L, Aversa A, Zitzmann M, et al. Therapy of endocrine desease: testosterone supplementation and body composition: results from a meta‐analysis study. Eur J Endocrinol 2016; 174: R99 – R116.
dc.identifier.citedreferenceGuo C, Gu W, Liu M, Peng BO, Yao X, Yang B, et al. Efficacy and safety of testosterone replacement therapy in men with hypogonadism: a meta‐analysis study of placebo‐controlled trials. Exp Ther Med 2016; 11: 853 – 863.
dc.identifier.citedreferenceCorona G, Rastrelli G, Morgentaler A, Sforza A, Mannucci E, Maggi M. Meta‐analysis of results of testosterone therapy on sexual function based on International Index of Erectile Function Scores. Eur Urol 2017.
dc.identifier.citedreferenceAlbert SG, Morley JE. Testosterone therapy, association with age, initiation and mode of therapy with cardiovascular events: a systematic review. Clin Endocrinol (Oxf) 2016; 85: 436 – 443.
dc.identifier.citedreferenceSt‐Onge MP, Wang Z, Horlick M, Wang J, Heymsfield SB. Dual‐energy X‐ray absorptiometry lean soft tissue hydration: independent contributions of intra‐ and extracellular water. Am J Physiol Endocrinol Metab 2004; 287: E842 – E847.
dc.identifier.citedreferenceJohannsson G, Gibney J, Wolthers T, Leung KC, Ho KK. Independent and combined effects of testosterone and growth hormone on extracellular water in hypopituitary men. J Clin Endocrinol Metab 2005; 90: 3989 – 3994.
dc.identifier.citedreferenceParis MT, Lafleur B, Dubin JA, Mourtzakis M. Development of a bedside viable ultrasound protocol to quantify appendicular lean tissue mass. J Cachexia Sarcopenia Muscle 2017; 8: 713 – 726.
dc.identifier.citedreferenceNijholt W, Scafoglieri A, Jager‐Wittenaar H, Hobbelen JSM, van der Schans CP. The reliability and validity of ultrasound to quantify muscles in older adults: a systematic review. J Cachexia Sarcopenia Muscle 2017; 8: 702 – 712.
dc.identifier.citedreferenceSinha‐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: 3024 – 3033.
dc.identifier.citedreferenceBhasin S, Travison TG, Storer TW, Lakshman K, Kaushik M, Mazer NA, et al. Effect of testosterone supplementation with and without a dual 5alpha‐reductase inhibitor on fat‐free mass in men with suppressed testosterone production: a randomized controlled trial. JAMA 2012; 307: 931 – 939.
dc.identifier.citedreferenceYarrow JF, McCoy SC, Borst SE. Intracrine and myotrophic roles of 5alpha‐reductase and androgens: a review. Med Sci Sports Exerc 2012; 44: 818 – 826.
dc.identifier.citedreferenceMazer N, Bell D, Wu J, Fischer J, Cosgrove M, Eilers B. Comparison of the steady‐state pharmacokinetics, metabolism, and variability of a transdermal testosterone patch versus a transdermal testosterone gel in hypogonadal men. J Sex Med 2005; 2: 213 – 226.
dc.identifier.citedreferenceWang C, Berman N, Longstreth JA, Chuapoco B, Hull L, Steiner B, et al. Pharmacokinetics of transdermal testosterone gel in hypogonadal men: application of gel at one site versus four sites: a General Clinical Research Center Study. J Clin Endocrinol Metab 2000; 85: 964 – 969.
dc.identifier.citedreferenceStraight CR, Brady AO, Evans E. Sex‐specific relationships of physical activity, body composition, and muscle quality with lower‐extremity physical function in older men and women. Menopause 2015; 22: 297 – 303.
dc.identifier.citedreferenceVisser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well‐functioning older persons. J Gerontol A Biol Sci Med Sci 2005; 60: 324 – 333.
dc.identifier.citedreferenceSchaap LA, Koster A, Visser M. Adiposity, muscle mass, and muscle strength in relation to functional decline in older persons. Epidemiol Rev 2013; 35: 51 – 65.
dc.identifier.citedreferencevon Haehling S, Morley JE, Coats AJ, Anker SD. Ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2015. J Cachexia Sarcopenia Muscle 2015; 6: 315 – 316.
dc.identifier.citedreferenceTravison TG, Araujo AB, O’Donnell AB, Kupelian V, McKinlay JB. A population‐level decline in serum testosterone levels in American men. J Clin Endocrinol Metab 2007; 92: 196 – 202.
dc.identifier.citedreferencevan den Beld AW, de Jong FH, Grobbee DE, Pols HA, Lamberts SW. Measures of bioavailable serum testosterone and estradiol and their relationships with muscle strength, bone density, and body composition in elderly men. J Clin Endocrinol Metab 2000; 85: 3276 – 3282.
dc.identifier.citedreferenceBaumgartner RN, Waters DL, Gallagher D, Morley JE, Garry PJ. Predictors of skeletal muscle mass in elderly men and women. Mech Ageing Dev 1999; 107: 123 – 136.
dc.identifier.citedreferenceSpitzer M, Huang G, Basaria S, Travison TG, Bhasin S. Risks and benefits of testosterone therapy in older men. Nat Rev Endocrinol 2013; 9: 414 – 424.
dc.identifier.citedreferenceCheung AS, Gray H, Schache AG, Hoermann R, Lim Joon D, Zajac JD, et al. Androgen deprivation causes selective deficits in the biomechanical leg muscle function of men during walking: a prospective case‐control study. J Cachexia Sarcopenia Muscle 2017; 8: 102 – 112.
dc.identifier.citedreferenceNeto 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 (Dordr) 2015; 37: 9742.
dc.identifier.citedreferenceIsidori 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: 280 – 293.
dc.identifier.citedreferenceOttenbacher KJ, Ottenbacher ME, Ottenbacher AJ, Acha AA, Ostir GV. Androgen treatment and muscle strength in elderly men: a meta‐analysis. J Am Geriatr Soc 2006; 54: 1666 – 1673.
dc.identifier.citedreferenceBhasin 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: 2536 – 2559.
dc.identifier.citedreferenceBorst 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 Physiol Endocrinol Metab 2015; 308: E1035 – E1042.
dc.identifier.citedreferenceSnyder 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: 2647 – 2653.
dc.identifier.citedreferenceNair KS, Rizza RA, O’Brien P, Dhatariya K, Short KR, Nehra A, et al. DHEA in elderly women and DHEA or testosterone in elderly men. N Engl J Med 2006; 355: 1647 – 1659.
dc.identifier.citedreferenceHildreth 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: 1891 – 1900.
dc.identifier.citedreferenceStorer 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: 583 – 593.
dc.identifier.citedreferenceFerrando AA, Sheffield‐Moore M, Yeckel CW, Gilkison C, Jiang J, Achacosa A, et al. Testosterone administration to older men improves muscle function: molecular and physiological mechanisms. Am J Physiol Endocrinol Metab 2002; 282: E601 – E607.
dc.identifier.citedreferenceBorst SE, Yarrow JF, Conover CF, Nseyo U, Meuleman JR, Lipinska JA, et al. Musculoskeletal and prostate effects of combined testosterone and finasteride administration in older hypogonadal men: a randomized, controlled trial. Am J Physiol Endocrinol Metab 2014; 306: E433 – E442.
dc.identifier.citedreferencePage ST, Amory JK, Bowman FD, Anawalt BD, Matsumoto AM, Bremner WJ, et al. Exogenous testosterone (T) alone or with finasteride increases physical performance, grip strength, and lean body mass in older men with low serum T. J Clin Endocrinol Metab 2005; 90: 1502 – 1510.
dc.identifier.citedreferenceDobs AS, Meikle AW, Arver S, Sanders SW, Caramelli KE, Mazer NA. Pharmacokinetics, efficacy, and safety of a permeation‐enhanced testosterone transdermal system in comparison with bi‐weekly injections of testosterone enanthate for the treatment of hypogonadal men. J Clin Endocrinol Metab 1999; 84: 3469 – 3478.
dc.identifier.citedreferenceBorst 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.
dc.identifier.citedreferenceMorgentaler A, Dobs AS, Kaufman JM, Miner MM, Shabsigh R, Swerdloff RS, et al. Long acting testosterone undecanoate therapy in men with hypogonadism: results of a pharmacokinetic clinical study. J Urol 2008; 180: 2307 – 2313.
dc.identifier.citedreferenceStorer TW, Woodhouse L, Magliano L, Singh AB, Dzekov C, Dzekov J, et al. Changes in muscle mass, muscle strength, and power but not physical function are related to testosterone dose in healthy older men. J Am Geriatr Soc 2008; 56: 1991 – 1999.
dc.identifier.citedreferenceVerhagen AP, de Vet HC, de Bie RA, Kessels AG, Boers M, Bouter LM, et al. The Delphi list: a criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by Delphi consensus. J Clin Epidemiol 1998; 51: 1235 – 1241.
dc.identifier.citedreferenceHedges LV, Olkin I. Statistical Methods for Meta‐Analysis. Orlando, FL: Academic Press, Inc; 1985.
dc.identifier.citedreferenceDerSimonian R, Laird N. Meta‐analysis in clinical trials. Control Clin Trials 1986; 7: 177 – 188.
dc.identifier.citedreferenceSawilowsky SS. New effect size rules of thumb. J Mod Appl Stat Methods 2009; 8: 597 – 599.
dc.identifier.citedreferenceMantel N. Chi‐square tests with one degree of freedom; extensions of the Mantel‐Haenszel procedure. J Am Stat Assoc 1963; 58: 690 – 700.
dc.identifier.citedreferenceViechtbauer W. Conducting meta‐analyses in R with the metafor package. J Stat Softw 2010; 36: 1 – 48.
dc.identifier.citedreferenceAgledahl I, Hansen JB, Svartberg J. Impact of testosterone treatment on postprandial triglyceride metabolism in elderly men with subnormal testosterone levels. Scand J Clin Lab Invest 2008; 68: 641 – 648.
dc.identifier.citedreferenceAllan CA, Strauss BJ, Burger HG, Forbes EA, McLachlan RI. Testosterone therapy prevents gain in visceral adipose tissue and loss of skeletal muscle in nonobese aging men. J Clin Endocrinol Metab 2008; 93: 139 – 146.
dc.identifier.citedreferenceBehre 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: 198 – 207.
dc.identifier.citedreferenceBlackman MR, Sorkin JD, Munzer T, Bellantoni MF, Busby‐Whitehead J, Stevens TE, et al. Growth hormone and sex steroid administration in healthy aged women and men: a randomized controlled trial. JAMA 2002; 288: 2282 – 2292.
dc.identifier.citedreferenceBrockenbrough AT, Dittrich MO, Page ST, Smith T, Stivelman JC, Bremner WJ. Transdermal androgen therapy to augment EPO in the treatment of anemia of chronic renal disease. Am J Kidney Dis 2006; 47: 251 – 262.
dc.identifier.citedreferenceCaminiti G, Volterrani M, Iellamo F, Marazzi G, Massaro R, Miceli M, et al. Effect of long‐acting testosterone treatment on functional exercise capacity, skeletal muscle performance, insulin resistance, and baroreflex sensitivity in elderly patients with chronic heart failure a double‐blind, placebo‐controlled, randomized study. J Am Coll Cardiol 2009; 54: 919 – 927.
dc.identifier.citedreferenceCasaburi R, Bhasin S, Cosentino L, Porszasz J, Somfay A, Lewis MI, et al. Effects of testosterone and resistance training in men with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2004; 170: 870 – 878.
dc.identifier.citedreferenceClague JE, Wu FC, Horan MA. Difficulties in measuring the effect of testosterone replacement therapy on muscle function in older men. Int J Androl 1999; 22: 261 – 265.
dc.identifier.citedreferenceCrawford BA, Liu PY, Kean MT, Bleasel JF, Handelsman DJ. Randomized placebo‐controlled trial of androgen effects on muscle and bone in men requiring long‐term systemic glucocorticoid treatment. J Clin Endocrinol Metab 2003; 88: 3167 – 3176.
dc.identifier.citedreferenceDhindsa S, Ghanim H, Batra M, Kuhadiya ND, Abuaysheh S, Sandhu S, et al. Insulin resistance and inflammation in hypogonadotropic hypogonadism and their reduction after testosterone replacement in men with type 2 diabetes. Diabetes Care 2016; 39: 82 – 91.
dc.identifier.citedreferenceFrederiksen L, Hojlund K, Hougaard DM, Brixen K, Andersen M. Testosterone therapy increased muscle mass and lipid oxidation in aging men. Age (Dordr) 2012; 34: 145 – 156.
dc.identifier.citedreferenceGianatti EJ, Dupuis P, Hoermann R, Strauss BJ, Wentworth JM, Zajac JD, et al. Effect of testosterone treatment on glucose metabolism in men with type 2 diabetes: a randomized controlled trial. Diabetes Care 2014; 37: 2098 – 2107.
dc.identifier.citedreferenceGiannoulis MG, Sonksen PH, Umpleby M, Breen L, Pentecost C, Whyte M, et al. The effects of growth hormone and/or testosterone in healthy elderly men: a randomized controlled trial. J Clin Endocrinol Metab 2006; 91: 477 – 484.
dc.identifier.citedreferenceHoyos CM, Yee BJ, Phillips CL, Machan EA, Grunstein RR, Liu PY. Body compositional and cardiometabolic effects of testosterone therapy in obese men with severe obstructive sleep apnoea: a randomised placebo‐controlled trial. Eur J Endocrinol 2012; 167: 531 – 541.
dc.identifier.citedreferenceKatznelson L, Robinson MW, Coyle CL, Lee H, Farrell CE. Effects of modest testosterone supplementation and exercise for 12 weeks on body composition and quality of life in elderly men. Eur J Endocrinol 2006; 155: 867 – 875.
dc.identifier.citedreferenceKenny 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: 1134 – 1143.
dc.identifier.citedreferenceKenny AM, Prestwood KM, Gruman CA, Marcello KM, Raisz LG. Effects of transdermal testosterone on bone and muscle in older men with low bioavailable testosterone levels. J Gerontol A Biol Sci Med Sci 2001; 56: M266 – M272.
dc.identifier.citedreferenceKvorning T, Christensen LL, Madsen K, Nielsen JL, Gejl KD, Brixen K, et al. Mechanical muscle function and lean body mass during supervised strength training and testosterone therapy in aging men with low‐normal testosterone levels. J Am Geriatr Soc 2013; 61: 957 – 962.
dc.identifier.citedreferenceMagnussen LV, Glintborg D, Hermann P, Hougaard DM, Hojlund 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: 980 – 989.
dc.identifier.citedreferenceMarin P, Holmang S, Gustafsson C, Jonsson L, Kvist H, Elander A, et al. Androgen treatment of abdominally obese men. Obes Res 1993; 1: 245 – 251.
dc.identifier.citedreferenceMerza Z, Blumsohn A, Mah PM, Meads DM, McKenna SP, Wylie K, et al. Double‐blind placebo‐controlled study of testosterone patch therapy on bone turnover in men with borderline hypogonadism. Int J Androl 2006; 29: 381 – 391.
dc.identifier.citedreferenceSheffield‐Moore M, Dillon EL, Casperson SL, Gilkison CR, Paddon‐Jones D, Durham WJ, et al. A randomized pilot study of monthly cycled testosterone replacement or continuous testosterone replacement versus placebo in older men. J Clin Endocrinol Metab 2011; 96: E1831 – E1837.
dc.identifier.citedreferenceSrinivas‐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: 639 – 650.
dc.identifier.citedreferenceSteidle 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: 2673 – 2681.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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