Advertisement

Current Osteoporosis Reports

, Volume 13, Issue 5, pp 302–309 | Cite as

Skeletal Effects of Smoking

  • Natalie E. Cusano
Therapeutics and Medical Management (E Shane and R Adler, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Therapeutics and Medical Management

Abstract

Smoking is a leading cause of preventable death and disability. Smoking has long been identified as a risk factor for osteoporosis, with data showing that older smokers have decreased bone mineral density and increased fracture risk compared to nonsmokers, particularly at the hip. The increase in fracture risk in smokers is out of proportion to the effects on bone density, indicating deficits in bone quality. Advanced imaging techniques have demonstrated microarchitectural deterioration in smokers, particularly in the trabecular compartment. The mechanisms by which smoking affects skeletal health remain unclear, although multiple pathways have been proposed. Smoking cessation may at least partially reverse the adverse effects of smoking on the skeleton.

Keywords

Smoking Skeleton Bone Osteoporosis Fractures 

Notes

Compliance with Ethics Guidelines

Conflict of Interest

The author of this paper declares she has no conflicts of interest.

Human and Animal Rights and Informed Consent

This article contains no studies with human or animal subjects performed by the author.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Jamal A, Agaku IT, O’Connor E, King BA, Kenemer JB, Neff L. Current cigarette smoking among adults—United States, 2005–2013. MMWR. 2014;63(47):1108–12.PubMedGoogle Scholar
  2. 2.
    Ng M, Freeman MK, Fleming TD, Robinson M, Dwyer-Lindgren L, Thomson B, et al. Smoking prevalence and cigarette consumption in 187 countries, 1980–2012. JAMA. 2014;311(2):183–92.PubMedCrossRefGoogle Scholar
  3. 3.
    Daniell HW. Osteoporosis and smoking. JAMA. 1972;221(5):509.PubMedCrossRefGoogle Scholar
  4. 4.
    Daniell HW. Osteoporosis of the slender smoker. Vertebral compression fractures and loss of metacarpal cortex in relation to postmenopausal cigarette smoking and lack of obesity. Arch Intern Med. 1976;136(3):298–304.PubMedCrossRefGoogle Scholar
  5. 5.
    Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J Bone Miner Res Off J Am Soc Bone Miner Res. 2007;22(3):465–75.CrossRefGoogle Scholar
  6. 6.
    Kanis JA, Johnell O, Oden A, Johansson H, De Laet C, Eisman JA, et al. Smoking and fracture risk: a meta-analysis. Osteoporosis Int J Established Result Cooperation Between Eur Found Osteoporosis Natl Osteoporosis Found USA. 2005;16(2):155–62.CrossRefGoogle Scholar
  7. 7.
    Kanis JA. Diagnosis of osteoporosis and assessment of fracture risk. Lancet. 2002;359(9321):1929–36.PubMedCrossRefGoogle Scholar
  8. 8.
    Law MR, Hackshaw AK. A meta-analysis of cigarette smoking, bone mineral density and risk of hip fracture: recognition of a major effect. BMJ. 1997;315(7112):841–6.PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Ward KD, Klesges RC. A meta-analysis of the effects of cigarette smoking on bone mineral density. Calcif Tissue Int. 2001;68(5):259–70.PubMedCrossRefGoogle Scholar
  10. 10.
    Kiel DP, Zhang Y, Hannan MT, Anderson JJ, Baron JA, Felson DT. The effect of smoking at different life stages on bone mineral density in elderly men and women. Osteoporosis Int J Established Result Cooperation Between Eur Found Osteoporosis Natl Osteoporosis Found USA. 1996;6(3):240–8.CrossRefGoogle Scholar
  11. 11.
    Vestergaard P, Mosekilde L. Fracture risk associated with smoking: a meta-analysis. J Intern Med. 2003;254(6):572–83.PubMedCrossRefGoogle Scholar
  12. 12.
    Osteoporosis prevention, diagnosis, and therapy. NIH consensus statement. 2000;29;17(1):1-36.Google Scholar
  13. 13.
    Leslie WD, Rubin MR, Schwartz AV, Kanis JA. Type 2 diabetes and bone. J Bone Miner Res Off J Am Soc Bone Miner Res. 2012;27(11):2231–7.CrossRefGoogle Scholar
  14. 14.
    Stein EM, Silva BC, Boutroy S, Zhou B, Wang J, Udesky J, et al. Primary hyperparathyroidism is associated with abnormal cortical and trabecular microstructure and reduced bone stiffness in postmenopausal women. J Bone Miner Res Off J Am Soc Bone Miner Res. 2013;28(5):1029–40.CrossRefGoogle Scholar
  15. 15.••
    Szulc P, Debiesse E, Boutroy S, Vilauphiou N, Chapurlat R. Poor trabecular microarchitecture in male current smokers: the cross-sectional STRAMBO study. Calcif Tissue Int. 2011;89(4):303–11. This paper provides important data on skeletal microarchitectural changes in adult male smokers.PubMedCrossRefGoogle Scholar
  16. 16.
    Lorentzon M, Mellstrom D, Haug E, Ohlsson C. Smoking is associated with lower bone mineral density and reduced cortical thickness in young men. J Clin Endocrinol Metab. 2007;92(2):497–503.PubMedCrossRefGoogle Scholar
  17. 17.••
    Rudang R, Darelid A, Nilsson M, Nilsson S, Mellstrom D, Ohlsson C, et al. Smoking is associated with impaired bone mass development in young adult men: a 5-year longitudinal study. J Bone Miner Res Off J Am Soc Bone Miner Res. 2012;27(10):2189–97. Paper presents evidence that smoking impairs bone quality in young men.CrossRefGoogle Scholar
  18. 18.
    Taes Y, Lapauw B, Vanbillemont G, Bogaert V, De Bacquer D, Goemaere S, et al. Early smoking is associated with peak bone mass and prevalent fractures in young, healthy men. J Bone Miner Res Off J Am Soc Bone Miner Res. 2010;25(2):379–87.CrossRefGoogle Scholar
  19. 19.
    Nelson HD, Nevitt MC, Scott JC, Stone KL, Cummings SR. Smoking, alcohol, and neuromuscular and physical function of older women. Study of Osteoporotic Fractures Research Group. JAMA. 1994;272(23):1825–31.PubMedCrossRefGoogle Scholar
  20. 20.
    Szulc P, Duboeuf F, Marchand F, Delmas PD. Hormonal and lifestyle determinants of appendicular skeletal muscle mass in men: the MINOS study. Am J Clin Nutr. 2004;80(2):496–503.PubMedGoogle Scholar
  21. 21.
    Fletcher PC, Hirdes JP. Risk factor for accidental injuries within senior citizens’ homes: analysis of the Canadian survey on ageing and independence. J Gerontol Nurs. 2005;31(2):49–57.PubMedCrossRefGoogle Scholar
  22. 22.
    Faulkner KA, Cauley JA, Studenski SA, Landsittel DP, Cummings SR, Ensrud KE, et al. Lifestyle predicts falls independent of physical risk factors. Osteoporosis Int J Established Result Cooperation Between Eur Found Osteoporosis Natl Osteoporosis Found USA. 2009;20(12):2025–34.CrossRefGoogle Scholar
  23. 23.
    Lord SR, Ward JA, Williams P, Anstey KJ. An epidemiological study of falls in older community-dwelling women: the Randwick falls and fractures study. Aust J Public Health. 1993;17(3):240–5.PubMedCrossRefGoogle Scholar
  24. 24.
    Grundstrom AC, Guse CE, Layde PM. Risk factors for falls and fall-related injuries in adults 85 years of age and older. Arch Gerontol Geriatr. 2012;54(3):421–8.PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.•
    Cairoli E, Eller-Vainicher C, Ulivieri FM, Zhukouskaya VV, Palmieri S, Morelli V, et al. Factors associated with bisphosphonate treatment failure in postmenopausal women with primary osteoporosis. Osteoporosis Int J Established Result Cooperation Between Eur Found Osteoporosis Natl Osteoporosis Found USA. 2014;25(4):1401–10. Paper provides data that smoking may cause bisphosphonate treatment failure.CrossRefGoogle Scholar
  26. 26.•
    Scolaro JA, Schenker ML, Yannascoli S, Baldwin K, Mehta S, Ahn J. Cigarette smoking increases complications following fracture: a systematic review. J Bone Joint Surg Am. 2014;96(8):674–81. Excellent review of the post-fracture complications of smoking.PubMedCrossRefGoogle Scholar
  27. 27.
    Antonova E, Le TK, Burge R, Mershon J. Tibia shaft fractures: costly burden of nonunions. BMC Musculoskelet Disord. 2013;14:42.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Mineur YS, Abizaid A, Rao Y, Salas R, DiLeone RJ, Gundisch D, et al. Nicotine decreases food intake through activation of POMC neurons. Science. 2011;332(6035):1330–2.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Krall EA, Dawson-Hughes B. Smoking and bone loss among postmenopausal women. J Bone Miner Res Off J Am Soc Bone Miner Res. 1991;6(4):331–8.CrossRefGoogle Scholar
  30. 30.
    Krall EA, Dawson-Hughes B. Smoking increases bone loss and decreases intestinal calcium absorption. J Bone Miner Res Off J Am Soc Bone Miner Res. 1999;14(2):215–20.CrossRefGoogle Scholar
  31. 31.
    Landin-Wilhelmsen K, Wilhelmsen L, Lappas G, Rosen T, Lindstedt G, Lundberg PA, et al. Serum intact parathyroid hormone in a random population sample of men and women: relationship to anthropometry, life-style factors, blood pressure, and vitamin D. Calcif Tissue Int. 1995;56(2):104–8.PubMedCrossRefGoogle Scholar
  32. 32.
    Brot C, Jorgensen NR, Sorensen OH. The influence of smoking on vitamin D status and calcium metabolism. Eur J Clin Nutr. 1999;53(12):920–6.PubMedCrossRefGoogle Scholar
  33. 33.
    Szulc P, Garnero P, Claustrat B, Marchand F, Duboeuf F, Delmas PD. Increased bone resorption in moderate smokers with low body weight: the Minos study. J Clin Endocrinol Metab. 2002;87(2):666–74.PubMedCrossRefGoogle Scholar
  34. 34.
    Wong PK, Christie JJ, Wark JD. The effects of smoking on bone health. Clin Sci (Lond). 2007;113(5):233–41.CrossRefGoogle Scholar
  35. 35.
    Winternitz WW, Quillen D. Acute hormonal response to cigarette smoking. J Clin Pharmacol. 1977;17(7):389–97.PubMedCrossRefGoogle Scholar
  36. 36.
    Wilkins JN, Carlson HE, Van Vunakis H, Hill MA, Gritz E, Jarvik ME. Nicotine from cigarette smoking increases circulating levels of cortisol, growth hormone, and prolactin in male chronic smokers. Psychopharmacology (Berlin). 1982;78(4):305–8.CrossRefGoogle Scholar
  37. 37.
    Seyler Jr LE, Fertig J, Pomerleau O, Hunt D, Parker K. The effects of smoking on ACTH and cortisol secretion. Life Sci. 1984;34(1):57–65.PubMedCrossRefGoogle Scholar
  38. 38.
    Baron JA, Comi RJ, Cryns V, Brinck-Johnsen T, Mercer NG. The effect of cigarette smoking on adrenal cortical hormones. J Pharmacol Exp Ther. 1995;272(1):151–5.PubMedGoogle Scholar
  39. 39.
    Field AE, Colditz GA, Willett WC, Longcope C, McKinlay JB. The relation of smoking, age, relative weight, and dietary intake to serum adrenal steroids, sex hormones, and sex hormone-binding globulin in middle-aged men. J Clin Endocrinol Metab. 1994;79(5):1310–6.PubMedGoogle Scholar
  40. 40.
    Yeh J, Barbieri RL. Twenty-four-hour urinary-free cortisol in premenopausal cigarette smokers and nonsmokers. Fertil Steril. 1989;52(6):1067–9.PubMedGoogle Scholar
  41. 41.
    McKinlay SM, Bifano NL, McKinlay JB. Smoking and age at menopause in women. Ann Intern Med. 1985;103(3):350–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Midgette AS, Baron JA. Cigarette smoking and the risk of natural menopause. Epidemiology. 1990;1(6):474–80.PubMedCrossRefGoogle Scholar
  43. 43.
    Bjarnason NH, Christiansen C. The influence of thinness and smoking on bone loss and response to hormone replacement therapy in early postmenopausal women. J Clin Endocrinol Metab. 2000;85(2):590–6.PubMedCrossRefGoogle Scholar
  44. 44.
    Michnovicz JJ, Hershcopf RJ, Naganuma H, Bradlow HL, Fishman J. Increased 2-hydroxylation of estradiol as a possible mechanism for the anti-estrogenic effect of cigarette smoking. N Engl J Med. 1986;315(21):1305–9.PubMedCrossRefGoogle Scholar
  45. 45.
    Briggs MH. Cigarette smoking and infertility in men. Med J Aust. 1973;1(12):616–7.PubMedGoogle Scholar
  46. 46.
    Shaarawy M, Mahmoud KZ. Endocrine profile and semen characteristics in male smokers. Fertil Steril. 1982;38(2):255–7.PubMedGoogle Scholar
  47. 47.
    English KM, Pugh PJ, Parry H, Scutt NE, Channer KS, Jones TH. Effect of cigarette smoking on levels of bioavailable testosterone in healthy men. Clin Sci (Lond). 2001;100(6):661–5.CrossRefGoogle Scholar
  48. 48.
    Wang W, Yang X, Liang J, Liao M, Zhang H, Qin X, et al. Cigarette smoking has a positive and independent effect on testosterone levels. Hormones (Athens). 2013;12(4):567–77.CrossRefGoogle Scholar
  49. 49.
    Duthie GG, Arthur JR, James WP. Effects of smoking and vitamin E on blood antioxidant status. Am J Clin Nutr. 1991;53(4 Suppl):1061S–3.PubMedGoogle Scholar
  50. 50.
    Valavanidis A, Vlachogianni T, Fiotakis K. Tobacco smoke: involvement of reactive oxygen species and stable free radicals in mechanisms of oxidative damage, carcinogenesis and synergistic effects with other respirable particles. Int J Environ Res Public Health. 2009;6(2):445–62.PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Callaway DA, Jiang JX. Reactive oxygen species and oxidative stress in osteoclastogenesis, skeletal aging and bone diseases. J Bone Miner Metab. 2015.Google Scholar
  52. 52.
    Melhus H, Michaelsson K, Holmberg L, Wolk A, Ljunghall S. Smoking, antioxidant vitamins, and the risk of hip fracture. J Bone Miner Res Off J Am Soc Bone Miner Res. 1999;14(1):129–35.CrossRefGoogle Scholar
  53. 53.•
    Yan C, Avadhani NG, Iqbal J. The effects of smoke carcinogens on bone. Curr Osteoporos Rep. 2011;9(4):202–9. Excellent review on the effects of nicotine and other cigarette toxins on bone tissue.PubMedCrossRefGoogle Scholar
  54. 54.
    Walker LM, Preston MR, Magnay JL, Thomas PB, El Haj AJ. Nicotinic regulation of c-fos and osteopontin expression in human-derived osteoblast-like cells and human trabecular bone organ culture. Bone. 2001;28(6):603–8.PubMedCrossRefGoogle Scholar
  55. 55.
    Wejheden C, Brunnberg S, Larsson S, Lind PM, Andersson G, Hanberg A. Transgenic mice with a constitutively active aryl hydrocarbon receptor display a gender-specific bone phenotype. Toxicol Sci. 2010;114(1):48–58.PubMedCrossRefGoogle Scholar
  56. 56.
    Singh SU, Casper RF, Fritz PC, Sukhu B, Ganss B, Girard Jr B, et al. Inhibition of dioxin effects on bone formation in vitro by a newly described aryl hydrocarbon receptor antagonist, resveratrol. J Endocrinol. 2000;167(1):183–95.PubMedCrossRefGoogle Scholar
  57. 57.•
    Ko CH, Chan RL, Siu WS, Shum WT, Leung PC, Zhang L, et al. Deteriorating effect on bone metabolism and microstructure by passive cigarette smoking through dual actions on osteoblast and osteoclast. Calcif Tissue Int. 2015;96(5):389–400. This paper provides evidence that passive smoking exposure may have direct effects on osteoblasts and osteoclasts.PubMedCrossRefGoogle Scholar
  58. 58.
    Nguyen TV, Kelly PJ, Sambrook PN, Gilbert C, Pocock NA, Eisman JA. Lifestyle factors and bone density in the elderly: implications for osteoporosis prevention. J Bone Miner Res Off J Am Soc Bone Miner Res. 1994;9(9):1339–46.CrossRefGoogle Scholar
  59. 59.
    Hollenbach KA, Barrett-Connor E, Edelstein SL, Holbrook T. Cigarette smoking and bone mineral density in older men and women. Am J Public Health. 1993;83(9):1265–70.PubMedCentralPubMedCrossRefGoogle Scholar
  60. 60.
    Cornuz J, Feskanich D, Willett WC, Colditz GA. Smoking, smoking cessation, and risk of hip fracture in women. Am J Med. 1999;106(3):311–4.PubMedCrossRefGoogle Scholar
  61. 61.
    Olofsson H, Byberg L, Mohsen R, Melhus H, Lithell H, Michaelsson K. Smoking and the risk of fracture in older men. J Bone Miner Res Off J Am Soc Bone Miner Res. 2005;20(7):1208–15.CrossRefGoogle Scholar
  62. 62.
    Anthonisen NR, Skeans MA, Wise RA, Manfreda J, Kanner RE, Connett JE, et al. The effects of a smoking cessation intervention on 14.5-year mortality: a randomized clinical trial. Ann Intern Med. 2005;142(4):233–9.PubMedCrossRefGoogle Scholar
  63. 63.
    Kenfield SA, Stampfer MJ, Rosner BA, Colditz GA. Smoking and smoking cessation in relation to mortality in women. JAMA. 2008;299(17):2037–47.PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Cao Y, Kenfield S, Song Y, Rosner B, Qiu W, Sesso HD, et al. Cigarette smoking cessation and total and cause-specific mortality: a 22-year follow-up study among US male physicians. Arch Intern Med. 2011;171(21):1956–9.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Medicine, Division of EndocrinologyColumbia University Medical CenterNew YorkUSA

Personalised recommendations