Male Osteoporosis
Keywords:
Male osteoporosis, osteoporosis, fracture risk, hypogonadism, pharmacological treatmentAbstract
Osteoporosis is a chronic condition characterized by impaired bone remodelling that results in reduced bone mineral density, excessive bone loss and increased fracture risk. Osteoporosis in men is a fairly common condition, affecting 2-8% of men worldwide and more than 30% by the age of 85. Despite these compelling figures, the condition is under-estimated, under-diagnosed and under-treated. As a result and since the condition is almost always a “silent disease”, the first presentation is often a fragility fracture. Although the mechanisms and conditions that cause osteoporosis in men are similar to those in women, male osteoporosis has some unique features. Risk factors in men are very heterogenous and hypogonadism represents a common underlying cause. Other common aetiological factors are poor vitamin D and calcium levels, chronic underlying haematological, gastroenterological and rheumatological conditions and use of offending drugs or substances. The evidence for diagnosis, screening and treatment of male osteoporosis is quite poor and most of the current knowledge is extrapolated from the female counterpart. Identification and prompt therapy of underlying conditions leading to osteoporosis is essential before additional anti-resorptive or anabolic treatment is considered. This review discusses the current evidence on pathophysiology, aetiology, diagnosis, screening and treatment of osteoporosis in men.
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References
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4. Ji MX, Yu Q. Primary osteoporosis in postmenopausal women. Chronic Dis Transl Med. 2015 Mar 21;1(1):9-13.
5. Wright NC, Looker AC, Saag KG, Curtis JR, Delzell ES, Randall S, et al. The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res. 2014
6. Robling AG, Bonewald LF. The Osteocyte: New Insights. Annu Rev Physiol. 2020 Feb 10;82:485-506.
7. Bonjour JP, Theintz G, Buchs B, Slosman D, Rizzoli R. Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence. J Clin Endocrinol Metab. 1991 Sep;73(3):555-63.
8. Finkelstein JS, Neer RM, Biller BM, Crawford JD, Klibanski A. Osteopenia in men with a history of delayed puberty. N Engl J Med. 1992 Feb 27;326(9):600-4.
9. Finkelstein JS, Klibanski A, Neer RM. A longitudinal evaluation of bone mineral density in adult men with histories of delayed puberty. J Clin Endocrinol Metab. 1996 Mar;81(3):1152-5.
10. Finkelstein JS, Klibanski A, Neer RM, Greenspan SL, Rosenthal DI, Crowley WF Jr. Osteoporosis in men with idiopathic hypogonadotropic hypogonadism. Ann Intern Med. 1987 Mar;106(3):354-61.
11. Guo CY, Jones TH, Eastell R. Treatment of isolated hypogonadotropic hypogonadism effect on bone mineral density and bone turnover. J Clin Endocrinol Metab. 1997 Feb;82(2):658-65.
12. Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel L, Amin S, Rouleau PA, Khosla S. A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res. 2008 Feb;23(2):205-14.
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21. Barrett-Connor E, Mueller JE, von Mühlen DG, Laughlin GA, Schneider DL, Sartoris DJ. Low levels of estradiol are associated with vertebral fractures in older men, but not women: the Rancho Bernardo Study. J Clin Endocrinol Metab. 2000 Jan;85(1):219-23.
22. Diamond T, Smerdely P, Kormas N, Sekel R, Vu T, Day P. Hip fracture in elderly men: the importance of subclinical vitamin D deficiency and hypogonadism. Med J Aust. 1998 Aug 3;169(3):138-41.
23. Wicherts IS, van Schoor NM, Boeke AJ, Visser M, Deeg DJ, Smit J, Knol DL, Lips P. Vitamin D status predicts physical performance and its decline in older persons. J Clin Endocrinol Metab. 2007 Jun;92(6):2058-65.
24. Looker AC, Mussolino ME. Serum 25-hydroxyvitamin D and hip fracture risk in older U.S. white adults. J Bone Miner Res. 2008 Jan;23(1):143-50.
25. Daly RM, Brown M, Bass S, Kukuljan S, Nowson C. Calcium- and vitamin D3-fortified milk reduces bone loss at clinically relevant skeletal sites in older men: a 2-year randomized controlled trial. J Bone Miner Res. 2006 Mar;21(3):397-405.
26. Meier C, Woitge HW, Witte K, Lemmer B, Seibel MJ. Supplementation with oral vitamin D3 and calcium during winter prevents seasonal bone loss: a randomized controlled open-label prospective trial. J Bone Miner Res. 2004 Aug;19(8):1221-30.
27. Cranney A, Weiler HA, O’Donnell S, Puil L. Summary of evidence-based review on vitamin D efficacy and safety in relation to bone health. Am J Clin Nutr. 2008 Aug;88(2):513S-519S.
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29. Jutberger H, Lorentzon M, Barrett-Connor E, Johansson H, Kanis JA, Ljunggren O, Karlsson MK, Rosengren BE, Redlund-Johnell I, Orwoll E, Ohlsson C, Mellström D. Smoking predicts incident fractures in elderly men: Mr OS Sweden. J Bone Miner Res. 2010 May;25(5):1010-6.
30. Drake MT, Murad MH, Mauck KF, Lane MA, Undavalli C, Elraiyah T, Stuart LM, Prasad C, Shahrour A, Mullan RJ, Hazem A, Erwin PJ, Montori VM. Clinical review. Risk factors for low bone mass-related fractures in men: a systematic review and meta-analysis. J Clin Endocrinol Metab. 2012 Jun;97(6):1861-70.
31. Haentjens P, Magaziner J, Colón-Emeric CS, Vanderschueren D, Milisen K, Velkeniers B, Boonen S. Meta-analysis: excess mortality after hip fracture among older women and men. Ann Intern Med. 2010 Mar 16;152(6):380-90.
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40. Katznelson L, Finkelstein JS, Schoenfeld DA, Rosenthal DI, Anderson EJ, Klibanski A. Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism. J Clin Endocrinol Metab. 1996 Dec;81(12):4358-65.
41. Benito M, Vasilic B, Wehrli FW, Bunker B, Wald M, Gomberg B, Wright AC, Zemel B, Cucchiara A, Snyder PJ. Effect of testosterone replacement on trabecular architecture in hypogonadal men. J Bone Miner Res. 2005 Oct;20(10):1785-91.
42. Finkelstein JS, Klibanski A, Neer RM, Doppelt SH, Rosenthal DI, Segre GV, Crowley WF Jr. Increases in bone density during treatment of men with idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 1989 Oct;69(4):776-83. 43. Wang C, Cunningham G, Dobs A, Iranmanesh A, Matsumoto AM, Snyder PJ, Weber T, Berman N, Hull L, Swerdloff RS. 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 May;89(5):2085-98.
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2. Osteoporosis or Low Bone Mass in Older Adults: United States, 2017–2018; NCHS Data Brief, March 2021. Available at: www.cdc.gov/nchs/products/databriefs/db405.htm (Accessed on October 18, 2022).
3. Trajanoska K, Schoufour JD, de Jonge EAL, Kieboom BCT, Mulder M, Stricker BH, Voortman T, Uitterlinden AG, Oei EHG, Ikram MA, Zillikens MC, Rivadeneira F, Oei L. Fracture incidence and secular trends between 1989 and 2013 in a population based cohort: The Rotterdam Study. Bone. 2018 Sep;114:116-124.
4. Ji MX, Yu Q. Primary osteoporosis in postmenopausal women. Chronic Dis Transl Med. 2015 Mar 21;1(1):9-13.
5. Wright NC, Looker AC, Saag KG, Curtis JR, Delzell ES, Randall S, et al. The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res. 2014
6. Robling AG, Bonewald LF. The Osteocyte: New Insights. Annu Rev Physiol. 2020 Feb 10;82:485-506.
7. Bonjour JP, Theintz G, Buchs B, Slosman D, Rizzoli R. Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence. J Clin Endocrinol Metab. 1991 Sep;73(3):555-63.
8. Finkelstein JS, Neer RM, Biller BM, Crawford JD, Klibanski A. Osteopenia in men with a history of delayed puberty. N Engl J Med. 1992 Feb 27;326(9):600-4.
9. Finkelstein JS, Klibanski A, Neer RM. A longitudinal evaluation of bone mineral density in adult men with histories of delayed puberty. J Clin Endocrinol Metab. 1996 Mar;81(3):1152-5.
10. Finkelstein JS, Klibanski A, Neer RM, Greenspan SL, Rosenthal DI, Crowley WF Jr. Osteoporosis in men with idiopathic hypogonadotropic hypogonadism. Ann Intern Med. 1987 Mar;106(3):354-61.
11. Guo CY, Jones TH, Eastell R. Treatment of isolated hypogonadotropic hypogonadism effect on bone mineral density and bone turnover. J Clin Endocrinol Metab. 1997 Feb;82(2):658-65.
12. Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel L, Amin S, Rouleau PA, Khosla S. A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res. 2008 Feb;23(2):205-14.
13. Gennari L, Bilezikian JP. New and developing pharmacotherapy for osteoporosis in men. Expert Opin Pharmacother. 2018 Feb;19(3):253-264.
14. Orwoll ES, Klein RF. Osteoporosis in men. Endocr Rev. 1995 Feb;16(1):87-116.
15. Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel L, Amin S, Rouleau PA, Khosla S. A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res. 2008 Feb;23(2):205-14.
16. Scane AC, Francis RM, Sutcliffe AM, Francis MJ, Rawlings DJ, Chapple CL. Case-control study of the pathogenesis and sequelae of symptomatic vertebral fractures in men. Osteoporos Int. 1999;9(1):91-7.
17. Kanis JA, Oden A, Johansson H, Borgström F, Ström O, McCloskey E. FRAX and its applications to clinical practice. Bone. 2009 May;44(5):734-43.
18. Lewis CE, Ewing SK, Taylor BC, Shikany JM, Fink HA, Ensrud KE, Barrett-Connor E, Cummings SR, Orwoll E; Osteoporotic Fractures in Men (MrOS) Study Research Group. Predictors of non-spine fracture in elderly men: the MrOS study. J Bone Miner Res. 2007 Feb;22(2):211-9.
19. Finkelstein JS, Lee H, Leder BZ, Burnett-Bowie SA, Goldstein DW, Hahn CW, Hirsch SC, Linker A, Perros N, Servais AB, Taylor AP, Webb ML, Youngner JM, Yu EW. Gonadal steroid-dependent effects on bone turnover and bone mineral density in men. J Clin Invest. 2016 Mar 1;126(3):1114-25.
20. Szulc P, Munoz F, Claustrat B, Garnero P, Marchand F, Duboeuf F, Delmas PD. Bioavailable estradiol may be an important determinant of osteoporosis in men: the MINOS study. J Clin Endocrinol Metab. 2001 Jan;86(1):192-9.
21. Barrett-Connor E, Mueller JE, von Mühlen DG, Laughlin GA, Schneider DL, Sartoris DJ. Low levels of estradiol are associated with vertebral fractures in older men, but not women: the Rancho Bernardo Study. J Clin Endocrinol Metab. 2000 Jan;85(1):219-23.
22. Diamond T, Smerdely P, Kormas N, Sekel R, Vu T, Day P. Hip fracture in elderly men: the importance of subclinical vitamin D deficiency and hypogonadism. Med J Aust. 1998 Aug 3;169(3):138-41.
23. Wicherts IS, van Schoor NM, Boeke AJ, Visser M, Deeg DJ, Smit J, Knol DL, Lips P. Vitamin D status predicts physical performance and its decline in older persons. J Clin Endocrinol Metab. 2007 Jun;92(6):2058-65.
24. Looker AC, Mussolino ME. Serum 25-hydroxyvitamin D and hip fracture risk in older U.S. white adults. J Bone Miner Res. 2008 Jan;23(1):143-50.
25. Daly RM, Brown M, Bass S, Kukuljan S, Nowson C. Calcium- and vitamin D3-fortified milk reduces bone loss at clinically relevant skeletal sites in older men: a 2-year randomized controlled trial. J Bone Miner Res. 2006 Mar;21(3):397-405.
26. Meier C, Woitge HW, Witte K, Lemmer B, Seibel MJ. Supplementation with oral vitamin D3 and calcium during winter prevents seasonal bone loss: a randomized controlled open-label prospective trial. J Bone Miner Res. 2004 Aug;19(8):1221-30.
27. Cranney A, Weiler HA, O’Donnell S, Puil L. Summary of evidence-based review on vitamin D efficacy and safety in relation to bone health. Am J Clin Nutr. 2008 Aug;88(2):513S-519S.
28. Moinuddin MM, Jameson KA, Syddall HE, Sayer AA, Martin HJ, Robinson S, Cooper C, Dennison EM. Cigarette smoking, birthweight and osteoporosis in adulthood: results from the hertfordshire cohort study. Open Rheumatol J. 2008;2:33-7.
29. Jutberger H, Lorentzon M, Barrett-Connor E, Johansson H, Kanis JA, Ljunggren O, Karlsson MK, Rosengren BE, Redlund-Johnell I, Orwoll E, Ohlsson C, Mellström D. Smoking predicts incident fractures in elderly men: Mr OS Sweden. J Bone Miner Res. 2010 May;25(5):1010-6.
30. Drake MT, Murad MH, Mauck KF, Lane MA, Undavalli C, Elraiyah T, Stuart LM, Prasad C, Shahrour A, Mullan RJ, Hazem A, Erwin PJ, Montori VM. Clinical review. Risk factors for low bone mass-related fractures in men: a systematic review and meta-analysis. J Clin Endocrinol Metab. 2012 Jun;97(6):1861-70.
31. Haentjens P, Magaziner J, Colón-Emeric CS, Vanderschueren D, Milisen K, Velkeniers B, Boonen S. Meta-analysis: excess mortality after hip fracture among older women and men. Ann Intern Med. 2010 Mar 16;152(6):380-90.
32. Cummings SR, Cawthon PM, Ensrud KE, Cauley JA, Fink HA, Orwoll ES; Osteoporotic Fractures in Men (MrOS) Research Groups; Study of Osteoporotic Fractures Research Groups. BMD and risk of hip and nonvertebral fractures in older men: a prospective study and comparison with older women. J Bone Miner Res. 2006 Oct;21(10):1550-6.
33. Kanis JA, McCloskey EV, Johansson H, Oden A, Melton LJ 3rd, Khaltaev N. A reference standard for the description of osteoporosis. Bone. 2008 Mar;42(3):467-75.
34. Adult Official Positions of the ISCD as updated in 2019 (available on iscd.org)
35. Guidelines for the diagnosis and management of osteoporosis, Hellenic Society for the Study of Bone Metabolism, updated 2018 (available at eemmo.gr)
36. World Health Organization. WHO Fracture Risk Assesment Tool. Available from: http://www.shef.ac.uk/FRAX.
37. Kukuljan S, Nowson CA, Sanders KM, Nicholson GC, Seibel MJ, Salmon J, Daly RM. Independent and combined effects of calcium-vitamin D3 and exercise on bone structure and strength in older men: an 18-month factorial design randomized controlled trial. J Clin Endocrinol Metab. 2011 Apr;96(4):955-63.
38. Fortinsky RH, Iannuzzi-Sucich M, Baker DI, Gottschalk M, King MB, Brown CJ, Tinetti ME. Fall-risk assessment and management in clinical practice: views from healthcare providers. J Am Geriatr Soc. 2004 Sep;52(9):1522-6.
39. Body JJ, Bergmann P, Boonen S, Boutsen Y, Bruyere O, Devogelaer JP, Goemaere S, Hollevoet N, Kaufman JM, Milisen K, Rozenberg S, Reginster JY. Non-pharmacological management of osteoporosis: a consensus of the Belgian Bone Club. Osteoporos Int. 2011 Nov;22(11):2769-88.
40. Katznelson L, Finkelstein JS, Schoenfeld DA, Rosenthal DI, Anderson EJ, Klibanski A. Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism. J Clin Endocrinol Metab. 1996 Dec;81(12):4358-65.
41. Benito M, Vasilic B, Wehrli FW, Bunker B, Wald M, Gomberg B, Wright AC, Zemel B, Cucchiara A, Snyder PJ. Effect of testosterone replacement on trabecular architecture in hypogonadal men. J Bone Miner Res. 2005 Oct;20(10):1785-91.
42. Finkelstein JS, Klibanski A, Neer RM, Doppelt SH, Rosenthal DI, Segre GV, Crowley WF Jr. Increases in bone density during treatment of men with idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 1989 Oct;69(4):776-83. 43. Wang C, Cunningham G, Dobs A, Iranmanesh A, Matsumoto AM, Snyder PJ, Weber T, Berman N, Hull L, Swerdloff RS. 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 May;89(5):2085-98.
43. Amory JK, Watts NB, Easley KA, Sutton PR, Anawalt BD, Matsumoto AM, Bremner WJ, Tenover JL. Exogenous testosterone or testosterone with finasteride increases bone mineral density in older men with low serum testosterone. J Clin Endocrinol Metab. 2004 Feb;89(2):503-10.
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