Abstract
Late onset hypogonadism (LOH, also referred to as age-associated testosterone deficiency syndrome, TDS) is a clinical and biochemical syndrome associated with advancing age and characterized by symptoms and a deficiency in serum testosterone levels. It may result in a significantly reduced quality of life and adversely affect the function of multiple organ systems. Although the treatment of LOH is primarily based on hormone replacement, other treatment modalities (medical or non-medical treatment) can also be considered for various accompanying symptoms. The efficacy of exercise in the treatment of LOH has already been evaluated in several studies, and many of them show beneficial effects for some specific symptoms and diseases. This study was designed to evaluate the relationship between exercise and plasma testosterone levels, and the potential beneficial effects of exercise for each specific symptom of LOH, and finally to consider the appropriate exercise treatment for LOH.
REFERENCES
1). Lunenfeld B, Saad F, Hoesl CE. ISA, ISSAM and EAU recommendations for the investigation, treatment and monitoring of late-onset hypogonadism in males: scientific background and rationale. Aging Male. 2005; 8:59–74.
2). Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS, et al. Task Force, Endocrine Society. Testosterone therapy in men with androgen deficiency syndromes: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2010; 95:2536–59.
3). Cattabiani C, Basaria S, Ceda GP, Luci M, Vignali A, Lauretani F, et al. Relationship between Testosterone deficiency and Cardiovascular risk and Mortality in Adult Men. J Endocrinol Invest 2011.
4). Vingren JL, Kraemer WJ, Ratamess NA, Anderson JM, Volek JS, Maresh CM. Testosterone physiology in resistance exercise and training: the up-stream regulatory elements. Sports Med. 2010; 40:1037–53.
5). Häkkinen K, Pakarinen A, Newton RU, Kraemer WJ. Acute hormone responses to heavy resistance lower and upper extremity exercise in young versus old men. Eur J Appl Physiol Occup Physiol. 1998; 77:312–9.
6). Linnamo V, Pakarinen A, Komi PV, Kraemer WJ, Häkkinen K. Acute hormonal responses to submaximal and maximal heavy resistance and explosive exercises in men and women. J Strength Cond Res. 2005; 19:566–71.
7). Kraemer WJ, Marchitelli L, Gordon SE, Harman E, Dziados JE, Mello R, et al. Hormonal and growth factor responses to heavy resistance exercise protocols. J Appl Physiol. 1990; 69:1442–50.
8). Häkkinen K, Pakarinen A, Kraemer WJ, Newton RU, Alen M. Basal concentrations and acute responses of serum hormones and strength development during heavy resistance training in middle-aged and elderly men and women. J Gerontol A Biol Sci Med Sci. 2000; 55:B95–105.
9). Pullinen T, Mero A, Huttunen P, Pakarinen A, Komi PV. Resistance exercise-induced hormonal responses in men, women, and pubescent boys. Med Sci Sports Exerc. 2002; 34:806–13.
10). Smilios I, Pilianidis T, Karamouzis M, Tokmakidis SP. Hormonal responses after various resistance exercise protocols. Med Sci Sports Exerc. 2003; 35:644–54.
11). Ratamess NA, Kraemer WJ, Volek JS, Maresh CM, Vanheest JL, Sharman MJ, et al. Androgen receptor content following heavy resistance exercise in men. J Steroid Biochem Mol Biol. 2005; 93:35–42.
12). Häkkinen K, Pakarinen A. Acute hormonal responses to two different fatiguing heavy-resistance protocols in male athletes. J Appl Physiol. 1993; 74:882–7.
13). Yarrow JF, Borsa PA, Borst SE, Sitren HS, Stevens BR, White LJ. Neuroendocrine responses to an acute bout of eccentric-enhanced resistance exercise. Med Sci Sports Exerc. 2007; 39:941–7.
14). Raastad T, Bj⊘ro T, Hallén J. Hormonal responses to high- and moderate-intensity strength exercise. Eur J Appl Physiol. 2000; 82:121–8.
15). Goto K, Ishii N, Kizuka T, Takamatsu K. The impact of metabolic stress on hormonal responses and muscular adaptations. Med Sci Sports Exerc. 2005; 37:955–63.
16). Migiano MJ, Vingren JL, Volek JS, Maresh CM, Fragala MS, Ho JY, et al. Endocrine response patterns to acute unilateral and bilateral resistance exercise in men. J Strength Cond Res. 2010; 24:128–34.
17). Hansen S, Kvorning T, Kjaer M, Sj⊘gaard G. The effect of short-term strength training on human skeletal muscle: the importance of physiologically elevated hormone levels. Scand J Med Sci Sports. 2001; 11:347–54.
18). Durand RJ, Castracane VD, Hollander DB, Tryniecki JL, Bamman MM, O'Neal S, et al. Hormonal responses from concentric and eccentric muscle contractions. Med Sci Sports Exerc. 2003; 35:937–43.
19). Krylow AM, Sandercock TG. Dynamic force responses of muscle involving eccentric contraction. J Biomech. 1997; 30:27–33.
20). La Vignera S, Condorelli R, Vicari E, D'Agata R, Calogero A. Physical activity and erectile dysfunction in middle-aged men: a brief review. J Androl 2011.
21). Esposito K, Giugliano F, Di Palo C, Giugliano G, Marfella R, D'Andrea F, et al. Effect of lifestyle changes on erectile dysfunction in obese men: a randomized controlled trial. JAMA. 2004; 291:2978–84.
22). Ferri A, Scaglioni G, Pousson M, Capodaglio P, Van Hoecke J, Narici MV. Strength and power changes of the human plantar flexors and knee extensors in response to resistance training in old age. Acta Physiol Scand. 2003; 177:69–78.
23). Grimby G, Aniansson A, Hedberg M, Henning GB, Grangård U, Kvist H. Training can improve muscle strength and endurance in 78- to 84-yr-old men. J Appl Physiol. 1992; 73:2517–23.
24). Häkkinen K, Kraemer WJ, Newton RU, Alen M. Changes in electromyographic activity, muscle fibre and force production characteristics during heavy resistance/power strength training in middle-aged and older men and women. Acta Physiol Scand. 2001; 171:51–62.
25). Häkkinen K, Newton RU, Gordon SE, McCormick M, Volek JS, Nindl BC, et al. Changes in muscle morphology, electromyographic activity, and force production characteristics during progressive strength training in young and older men. J Gerontol A Biol Sci Med Sci. 1998; 53:B415–23.
26). Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ. High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA. 1990; 263:3029–34.
27). Frontera WR, Meredith CN, O'Reilly KP, Knuttgen HG, Evans WJ. Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol. 1988; 64:1038–44.
28). Lexell J, Downham DY, Larsson Y, Bruhn E, Morsing B. Heavy-resistance training in older Scandinavian men and women: short- and longterm effects on arm and leg muscles. Scand J Med Sci Sports. 1995; 5:329–41.
29). Hunter GR, Bryan DR, Wetzstein CJ, Zuckerman PA, Bamman MM. Resistance training and intra-abdominal adipose tissue in older men and women. Med Sci Sports Exerc. 2002; 34:1023–8.
30). Bassett DR, Schneider PL, Huntington GE. Physical activity in an Old Order Amish community. Med Sci Sports Exerc. 2004; 36:79–85.
31). Foldvari M, Clark M, Laviolette LC, Bernstein MA, Kaliton D, Castaneda C, et al. Association of muscle power with functional status in community-dwelling elderly women. J Gerontol A Biol Sci Med Sci. 2000; 55:M192–9.
32). Izquierdo M, Ibañez J, Gorostiaga E, Garrues M, Zúñiga A, Antón A, et al. Maximal strength and power characteristics in isometric and dynamic actions of the upper and lower extremities in middle-aged and older men. Acta Physiol Scand. 1999; 167:57–68.
33). Metter EJ, Conwit R, Tobin J, Fozard JL. Age-associated loss of power and strength in the upper extremities in women and men. J Gerontol A Biol Sci Med Sci. 1997; 52:B267–76.
34). Earles DR, Judge JO, Gunnarsson OT. Velocity training induces power-specific adaptations in highly functioning older adults. Arch Phys Med Rehabil. 2001; 82:872–8.
35). Fiatarone MA, O'Neill EF, Ryan ND, Clements KM, Solares GR, Nelson ME, et al. Exercise training and nutritional supplementation for physical frailty in very elderly people. N Engl J Med. 1994; 330:1769–75.
36). Newton RU, Hakkinen K, Hakkinen A, McCormick M, Volek J, Kraemer WJ. Mixed-methods resistance training increases power and strength of young and older men. Med Sci Sports Exerc. 2002; 34:1367–75.
37). Fielding RA, LeBrasseur NK, Cuoco A, Bean J, Mizer K, Fiatarone Singh MA. High-velocity resistance training increases skeletal muscle peak power in older women. J Am Geriatr Soc. 2002; 50:655–62.
38). Ivey FM, Tracy BL, Lemmer JT, NessAiver M, Metter EJ, Fozard JL, et al. Effects of strength training and detraining on muscle quality: age and gender comparisons. J Gerontol A Biol Sci Med Sci. 2000; 55:B152–7.
39). Adams KJ, Swank AM, Berning JM, Sevene-Adams PG, Barnard KL, Shimp-Bowerman J. Progressive strength training in sedentary, older African American women. Med Sci Sports Exerc. 2001; 33:1567–76.
40). Vincent KR, Braith RW, Feldman RA, Magyari PM, Cutler RB, Persin SA, et al. Resistance exercise and physical performance in adults aged 60 to 83. J Am Geriatr Soc. 2002; 50:1100–7.
41). Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR. American College of Sports Medicine. American College of Sports Medicine Position Stand: physical activity and bone health. Med Sci Sports Exerc. 2004; 36:1985–96.
42). Michel BA, Lane NE, Björkengren A, Bloch DA, Fries JF. Impact of running on lumbar bone density: a 5-year longitudinal study. J Rheumatol. 1992; 19:1759–63.
43). Kelley GA, Kelley KS, Tran ZV. Exercise and bone mineral density in men: a meta-analysis. J Appl Physiol. 2000; 88:1730–6.
45). Vincent KR, Braith RW. Resistance exercise and bone turnover in elderly men and women. Med Sci Sports Exerc. 2002; 34:17–23.
46). Hurley BF, Hagberg JM. Optimizing health in older persons: aerobic or strength training? Exerc Sport Sci Rev. 1998; 26:61–89.
47). Kay SJ, Fiatarone Singh MA. The influence of physical activity on abdominal fat: a systematic review of the literature. Obes Rev. 2006; 7:183–200.
48). Toth MJ, Beckett T, Poehlman ET. Physical activity and the progressive change in body composition with aging: current evidence and research issues. Med Sci Sports Exerc. 1999; 31(11 Suppl):S590–6.
50). Hunter GR, McCarthy JP, Bamman MM. Effects of resistance training on older adults. Sports Med. 2004; 34:329–48.
51). Campbell WW, Crim MC, Young VR, Evans WJ. Increased energy requirements and changes in body composition with resistance training in older adults. Am J Clin Nutr. 1994; 60:167–75.
52). Hunter GR, Wetzstein CJ, McLafferty CL Jr, Zuckerman PA, Landers KA, Bamman MM. High-resistance versus variable-resistance training in older adults. Med Sci Sports Exerc. 2001; 33:1759–64.
53). Joseph LJ, Davey SL, Evans WJ, Campbell WW. Differential effect of resistance training on the body composition and lipoprotein-lipid profile in older men and women. Metabolism. 1999; 48:1474–80.
54). Sial S, Coggan AR, Hickner RC, Klein S. Training-induced alterations in fat and carbohydrate metabolism during exercise in elderly subjects. Am J Physiol. 1998; 274:E785–90.
55). Hagberg JM, Graves JE, Limacher M, Woods DR, Leggett SH, Cononie C, et al. Cardiovascular responses of 70- to 79-yr-old men and women to exercise training. J Appl Physiol. 1989; 66:2589–94.
56). Seals DR, Hagberg JM, Hurley BF, Ehsani AA, Holloszy JO. Effects of endurance training on glucose tolerance and plasma lipid levels in older men and women. JAMA. 1984; 252:645–9.
57). Huang G, Shi X, Davis-Brezette JA, Osness WH. Resting heart rate changes after endurance training in older adults: a meta-analysis. Med Sci Sports Exerc. 2005; 37:1381–6.
58). Seals DR, Hagberg JM, Hurley BF, Ehsani AA, Holloszy JO. Endurance training in older men and women. I. Cardiovascular responses to exercise. J Appl Physiol. 1984; 57:1024–9.
59). Martin WH 3rd, Kohrt WM, Malley MT, Korte E, Stoltz S. Exercise training enhances leg vasodilatory capacity of 65-yr-old men and women. J Appl Physiol. 1990; 69:1804–9.
60). Blumenthal JA, Babyak MA, Moore KA, Craighead WE, Herman S, Khatri P, et al. Effects of exercise training on older patients with major depression. Arch Intern Med. 1999; 159:2349–56.
61). Mather AS, Rodriguez C, Guthrie MF, McHarg AM, Reid IC, McMurdo ME. Effects of exercise on depressive symptoms in older adults with poorly responsive depressive disorder: randomised controlled trial. Br J Psychiatry. 2002; 180:411–5.
62). Netz Y, Wu MJ, Becker BJ, Tenenbaum G. Physical activity and psychological wellbeing in advanced age: a meta-analysis of intervention studies. Psychol Aging. 2005; 20:272–84.
63). McAuley E, Blissmer B, Marquez DX, Jerome GJ, Kramer AF, Katula J. Social relations, physical activity, and wellbeing in older adults. Prev Med. 2000; 31:608–17.
65). McAuley E, Blissmer B, Katula J, Duncan TE, Mihalko SL. Physical activity, self-esteem, and self-efficacy relationships in older adults: a randomized controlled trial. Ann Behav Med. 2000; 22:131–9.
66). Whitmer RA, Gunderson EP, Quesenberry CP Jr, Zhou J, Yaffe K. Body mass index in midlife and risk of Alzheimer disease and vascular dementia. Curr Alzheimer Res. 2007; 4:103–9.
67). Yaffe K, Haan M, Blackwell T, Cherkasova E, Whitmer RA, West N. Metabolic syndrome and cognitive decline in elderly Latinos: findings from the Sacramento Area Latino Study of Aging study. J Am Geriatr Soc. 2007; 55:758–62.
68). Laurin D, Verreault R, Lindsay J, MacPherson K, Rockwood K. Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch Neurol. 2001; 58:498–504.
69). Tabbarah M, Crimmins EM, Seeman TE. The relationship between cognitive and physical performance: MacArthur Studies of Successful Aging. J Gerontol A Biol Sci Med Sci. 2002; 57:M228–35.
70). Colcombe S, Kramer AF. Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci. 2003; 14:125–30.
71). Fabre C, Chamari K, Mucci P, Massé-Biron J, Préfaut C. Improvement of cognitive function by mental and/or individualized aerobic training in healthy elderly subjects. Int J Sports Med. 2002; 23:415–21.
72). Oswald WD, Rupprecht R, Gunzelmann T, Tritt K. The SIMA-project: effects of 1 year cognitive and psychomotor training on cognitive abilities of the elderly. Behav Brain Res. 1996; 78:67–72.
73). Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, et al. Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci. 2006; 61:1166–70.
74). Kramer AF, Erickson KI, Colcombe SJ. Exercise, cognition, and the aging brain. J Appl Physiol. 2006; 101:1237–42.
75). Spirduso WW, Cronin DL. Exercise dose-response effects on quality of life and independent living in older adults. Med Sci Sports Exerc. 2001; 33(6 Suppl):S598–608.
76). Taylor AH, Cable NT, Faulkner G, Hillsdon M, Narici M, Van Der Bij AK. Physical activity and older adults: a review of health benefits and the effectiveness of interventions. J Sports Sci. 2004; 22:703–25.
77). Martinsen EW, Hoffart A, Solberg O. Comparing aerobic with nonaerobic forms of exercise in the treatment of clinical depression: a randomized trial. Compr Psychiatry. 1989; 30:324–31.
78). Singh NA, Clements KM, Fiatarone MA. A randomized controlled trial of progressive resistance training in depressed elders. J Gerontol A Biol Sci Med Sci. 1997; 52:M27–35.
79). Singh NA, Clements KM, Singh MA. The efficacy of exercise as a longterm antidepressant in elderly subjects: a randomized, controlled trial. J Gerontol A Biol Sci Med Sci. 2001; 56:M497–504.
80). Martinsen EW, Medhus A, Sandvik L. Effects of aerobic exercise on depression: a controlled study. Br Med J (Clin Res Ed). 1985; 291:109.
81). Singh NA, Clements KM, Fiatarone MA. A randomized controlled trial of the effect of exercise on sleep. Sleep. 1997; 20:95–101.
82). Chandler JM, Duncan PW, Kochersberger G, Studenski S. Is lower extremity strength gain associated with improvement in physical performance and disability in frail, community-dwelling elders? Arch Phys Med Rehabil. 1998; 79:24–30.
83). Greendale GA, Salem GJ, Young JT, Damesyn M, Marion M, Wang MY, et al. A randomized trial of weighted vest use in ambulatory older adults: strength, performance, and quality of life outcomes. J Am Geriatr Soc. 2000; 48:305–11.
84). Tsutsumi T, Don BM, Zaichkowsky LD, Takenaka K, Oka K, Ohno T. Comparison of high and moderate intensity of strength training on mood and anxiety in older adults. Percept Mot Skills. 1998; 87:1003–11.
85). Gillespie LD, Gillespie WJ, Robertson MC, Lamb SE, Cumming RG, Rowe BH. Interventions for preventing falls in elderly people. Cochrane Database Syst Rev 2003: CD000340.
86). Said CM, Goldie PA, Patla AE, Culham E, Sparrow WA, Morris ME. Balance during obstacle crossing following stroke. Gait Posture. 2008; 27:23–30.
87). Campbell AJ, Robertson MC, Gardner MM, Norton RN, Buchner DM. Psychotropic medication withdrawal and a home-based exercise program to prevent falls: a randomized, controlled trial. J Am Geriatr Soc. 1999; 47:850–3.
88). Norton R, Galgali G, Campbell AJ, Reid IR, Robinson E, Butler M, et al. Is physical activity protective against hip fracture in frail older people? Age Ageing. 2001; 30:262–4.
89). Wolf SL, Sattin RW, Kutner M, O'Grady M, Greenspan AI, Gregor RJ. Intense tai chi exercise training and fall occurrences in older, transitionally frail adults: a randomized, controlled trial. J Am Geriatr Soc. 2003; 51:1693–701.
90). Rider RA, Daly J. Effects of flexibility training on enhancing spinal mobility in older women. J Sports Med Phys Fitness. 1991; 31:213–7.
91). DHHS. 2008 Physical Activity Guidelines for Americans. Rockville (MD): U.S. Department of Health and Human Services;2008.
92). American College of Sports Medicine. Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh MA, Minson CT, Nigg CR, et al. American College of Sports Medicine position stand. Exercise and physical activity for older adults. Med Sci Sports Exerc. 2009; 41:1510–30.