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Bone Biomechanical Property Deterioration Due to Tobacco Smoke Exposure

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Abstract

Tobacco smoking has been implicated in the development of osteoporosis and early onset of menopause in women smokers. We measured various biomechanical properties of femurs and tibiae obtained from smoke-exposed and control mice to determine cigarette smoke influences on bone mass, structure, and strength. Growing female C57BL mice were exposed to sidestream cigarette smoke in a whole-body exposure chamber, set at 30 ± 2 mg smoke particulates/m3 for 4 hours/day and 5 days/week for 12 consecutive weeks. Elevated levels of urinary cotinine and pulmonary ethoxyresorufin deethylase activity in smoke-exposed mice confirmed their effective exposure to cigarette smoke. There were no differences in body weight and physical size (length, medial-lateral and anterior-posterior widths, midshaft cortical area and thickness) of femurs and tibiae between smoke-exposed and control mice. The femoral mid-shaft yield load, stiffness, yield stress, and modulus were, respectively 8%, 13%, 10%, and 14% lower (P < 0.05) in smoke-exposed compared to control mice. The ultimate load and stress in mid-shaft femurs showed decreasing trends (P < 0.1) in smoke-exposed mice. In the femoral neck, the ultimate load and stiffness were 9% and 12% lower (P < 0.05) in smoke-exposed mice, respectively. Further, the ash-to-dry bone weight ratio was smaller (∼6%, P < 0.05), and micro-computed tomographic scanning of distal femoral bone volume/total volume (%) and trabecular thickness showed decreasing trends in smoke-exposed mice compared to the control group. We conclude that exposure to tobacco smoke deteriorates some of the biomechanical properties of bone in growing female mice.

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References

  1. Secker-Walker RH, Worden JK, Holland RR, Flynn BS, Detsky AS (1997) A mass media programme to prevent smoking among adolescents: costs and cost effectiveness. Tob Control 6:207-212

    PubMed  CAS  Google Scholar 

  2. Hodgson TA (1992) Cigarette smoking and lifetime medical expenditures. Milbank Q 70:81–125

    PubMed  CAS  Google Scholar 

  3. Tsevat J (1992) Impact and cost-effectiveness of smoking interventions. Am J Med 93:43S-47S

    Article  PubMed  CAS  Google Scholar 

  4. Taylor DH Jr, Hasselblad V, Henley SJ, Thun MJ, Sloan FA (2002) Benefits of smoking cessation for longevity. Am J Public Health 2002;92:990–996

    PubMed  Google Scholar 

  5. Nusselder WJ, Looman CW, Marang van de Mheen PJ, van de Mheen H, Mackenbach JP (2000) Smoking and the compression of morbidity. J Epidemiol Community Health 54(8):566–574

    PubMed  CAS  Google Scholar 

  6. Rogers RG, Powell Griner E (1991) Life expectancies of cigarette smokers and nonsmokers in the United States. Soc Sci Med 32:1151–1159

    Article  PubMed  CAS  Google Scholar 

  7. Burns DM (2003) Tobacco-related diseases. Semin Oncol Nurs 19:244–249

    Article  PubMed  Google Scholar 

  8. Bilello KS, Murin S, Matthay RA (2002) Epidemiology, etiology, and prevention of lung cancer. Clin Chest Med 23:1–25

    Article  PubMed  Google Scholar 

  9. Lowenfels AB, Maisonneuve P (2002) Epidemiologic and etiologic factors of pancreatic cancer. Hematol Oncol Clin North Am 16:1–16

    Article  PubMed  Google Scholar 

  10. Kesteloot H (2003) Social class, all-cause, cardiovascular and cancer mortality: the importance of cigarette smoking. Acta Cardiol 58:285–287

    PubMed  Google Scholar 

  11. Stabile LP, Siegfried JM (2003) Sex and gender differences in lung cancer. J Gend Specif Med 6:37–48

    PubMed  Google Scholar 

  12. Centers for Disease Control and Prevention (2003) Cigarette smoking-attributable morbidity —United States, 2000. MMWR Morb Mortal Wkly Rep 52:842–844

    Google Scholar 

  13. Daniell HW (1976) 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 136:298–304

    Article  PubMed  CAS  Google Scholar 

  14. Hopper JL, Seeman E (1994) Bone density in twins discordant for tobacco use. N Engl J Med 330:387–392

    Article  PubMed  CAS  Google Scholar 

  15. Krall EA, Dawson-Hughes B (1999) Smoking increases bone loss and decreases intestinal calcium absorption. J Bone Miner Res 14:215–220

    PubMed  CAS  Google Scholar 

  16. Law MR, Hackshaw AK (1997) A meta-analysis of cigarette smoking, bone mineral density and risk of hip fracture: recognition of a major efffect. BMJ 315:841–846

    PubMed  CAS  Google Scholar 

  17. Pocock NA, Eisman JA, Kelly PJ, Sambrook PN, Yeates MG (1989) Effects of tobacco use on axial and appendicular bone mineral density. Bone 10:329–331

    Article  PubMed  CAS  Google Scholar 

  18. Seeman E (1996) The effects of tobacco and alcohol use on bone. In: Marcus R, Feldman D, Kelsey J (eds), Osteoporosis. Academic Press, San Diego, pp 577–597

    Google Scholar 

  19. Cornuz J, Feskanich D, Willett WC, Colditz GA (1999) Smoking, smoking cessation, and risk of hip fracture in women. Am J Med 106:311–314

    Article  PubMed  CAS  Google Scholar 

  20. Oncken C, Prestwood K, Cooney JL, Unson C, Fall P, Kulldorff M, Raisz LG (2002) Effects of smoking cessation or reduction on hormone profiles and bone turnover in postmenopausal women. Nicotine Tob Res 4:451–458

    Article  PubMed  CAS  Google Scholar 

  21. Qandil R, Sandhu HS, Matthews DC (1997) Tobacco smoking and periodontal diseases. J Can Dent Assoc 63:187–195

    PubMed  CAS  Google Scholar 

  22. Moran S, Glazier G, Armstrong K (2003) Women smokers’ perceptions of smoking-related health risks. J Womens Health 12:363–371

    Google Scholar 

  23. Ward KD, Klesges RC (2001) A meta-analysis of the effects of cigarette smoking on bone mineral density. Calcif Tissue Int 68:259–270

    Google Scholar 

  24. Karamanidis D, Tamiolakis D, Koutsougeras G, Tripsanas CH, Retzos K, Karidis S, Liberis B (2001) Cigarette smoking and the degree of maturation of the vaginal squamous epithelium in postmenopausal women. Clin Exp Obstet Gynecol 28:274–276

    PubMed  CAS  Google Scholar 

  25. Hardy R, Kuh D, Wadsworth M (2000) Smoking, body mass index, socioeconomic status and the menopausal transition in a British national cohort. Int J Epidemiol 29:845–851

    Article  PubMed  CAS  Google Scholar 

  26. Mueller L, Ciervo CA (1998) Smoking in women. J Am Osteopath Assoc 98(12 suppl):S7-S10

    PubMed  CAS  Google Scholar 

  27. McKinlay SM (1996) The normal menopause transition: an overview. Maturitas 23:137–145

    Article  PubMed  CAS  Google Scholar 

  28. Lipsitz CM (1993) Have you come a long way, baby? Smoking trends in women. Md Med J 42:27–31

    PubMed  CAS  Google Scholar 

  29. Shulman A, Ellenbogen A, Maymon R, Bahary C (1990) Smoking out the oestrogens. Hum Reprod 5:231–233

    PubMed  CAS  Google Scholar 

  30. Lindquist O, Bengtsson C, Lapidus L (1985) Relationships between the menopause and risk factors for ischaemic heart disease. Acta Obstet Gynecol Scand Suppl 130:43–47

    PubMed  CAS  Google Scholar 

  31. Kato I, Toniolo P, Akhmedkhanov A, Koenig KL, Shore R, Zeleniuch-Jacquotte A (1998) Prospective study of factors influencing the onset of natural menopause. J Clin Epidemiol 51:1271–1276

    Article  PubMed  CAS  Google Scholar 

  32. McKinlay SM (1996) The normal menopause transition: an overview. Maturitas 23:137–145

    Article  PubMed  CAS  Google Scholar 

  33. Welch A, Camus J, Dalzell N, Oakes S, Reeve J, Khaw KT (2004) Broadband ultrasound attenuation (BUA) of the heel bone and its correlates in men and women in the EPIC-Norfolk cohort: a cross-sectional population-based study. Osteoporos Int 15:217–225

    Article  PubMed  Google Scholar 

  34. Hannan MT, Felson DT, Dawson-Hughes B, Tucker KL, Cupples LA, Wilson PW, Kiel DP (2000) Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res 15:710–720

    PubMed  CAS  Google Scholar 

  35. Payne JB, Reinhardt RA, Nummikoski PV, Dunning DG, Patil KD (2000) The association of cigarette smoking with alveolar bone loss in postmenopausal females. J Clin Periodontol 27:658–664

    Article  PubMed  CAS  Google Scholar 

  36. Galvin RJ, Ramp WEEK, Lenz LG (1988) Smokeless tobacco contains a non-nicotine inhibitor of bone metabolism. Toxicol Appl Pharmacol 95:292–300

    Article  PubMed  CAS  Google Scholar 

  37. Krall EA, Dawson-Hughes B (1991) Smoking and bone loss among postmenopausal women. J Bone Miner Res 6:331–338

    PubMed  CAS  Google Scholar 

  38. Michnovicz J, Hershcopf RJ, Naganuma H, Bradlow HL, Fishman J (1986) Increased 2-hydroxylation of estradiol as a possible mechanism for the anti-estrogenic effect of cigarette smoking. N Engl J Med 315:1305–1309

    Article  PubMed  CAS  Google Scholar 

  39. Bjarnason NH, Christiansen C (2000) The influence of thinness and smoking on bone loss and response to hormone replacement therapy in early postmenopausal women. J Clin Endocrinol Metab 85:590–596

    Article  PubMed  CAS  Google Scholar 

  40. Sirola J, Kroger H, Honkanen R, Sandini L, Tuppurainen M, Jurvelin JS, Saarikoski S (2003) Smoking may impair the bone protective effects of nutritional calcium: a population-based approach. J Bone Miner Res 18:1036–1042

    PubMed  CAS  Google Scholar 

  41. Need AG, Kemp A, Giles N, Morris HA, Horowitz M, Nordin B (2002) Relationships between intestinal calcium absorption, serum vitamin D metabolites and smoking in postmenopausal women. Osteoporos Int 13:83–88

    Article  PubMed  CAS  Google Scholar 

  42. Krall EA, Dawson-Hughes B (1999) Smoking increases bone loss and decreases intestinal calcium absorption. J Bone Miner Res 14:215–220

    PubMed  CAS  Google Scholar 

  43. Benowitz NL (1986) Clinical pharmacology of nicotine. Annu Rev Med 37:21–32

    Article  PubMed  CAS  Google Scholar 

  44. Fung YK, Mendlik MG, Haven MC, Akhter MP, Kimmel DB (1998) Short-term effects of nicotine on bone and calciotropic hormones in adult female rats. Pharmacol Toxicol 82:243–249

    PubMed  CAS  Google Scholar 

  45. Fung YK, Iwaniec UT, Cullen DM, Akhter MP, Haven MC, Timmins P (1999) Long-term effects of nicotine on bone and calcitropic hormones in adult female rats. Pharmacol Toxicol 85:181–187

    Article  PubMed  CAS  Google Scholar 

  46. Iwaniec UT, Fung YK, Cullen DM, Akhter MA, Haven MC, Schmid M (2000) Effects of nicotine on bone and calciotropic hormones in growing female rats. Calcif Tissue Int 67:68–74

    Article  PubMed  CAS  Google Scholar 

  47. Syversen U, Nordsletten L, Falch JA, Madsen JE, Nilsen OG, Waldum HL (1999) Effects of lifelong nicotine inhalation on bone mass and mechanical properties in female rat femurs. Calcif Tissue Int 65:246–249

    Article  PubMed  CAS  Google Scholar 

  48. Akhter MP, Iwaniec UT, Haynatzki GR, Fung YK, Cullen DM, Recker RR (2003) Effects of nicotine on bone mass and strength in aged female rats. J Orthop Res 21:14–19

    Article  PubMed  CAS  Google Scholar 

  49. Iwaniec UT, Fung YK, Akhter MA, Haven MC, Nespor S, Haynatzki GR, Cullen DM (2001) Effects of nicotine on bone mass, turnover, and strength in adult female rats. Calcif Tissue Int 68:358–364

    Article  PubMed  CAS  Google Scholar 

  50. Silcox DH III, Daftari T, Boden SD, Schimandle JH, Hutton WC, Whitesides TE Jr (1995) The effect of nicotine on spinal fusion. Spine 20:1549–1553

    PubMed  Google Scholar 

  51. Cesar-Neto JB, Duarte PM, Sallum EA, Barbieri D, Moreno H Jr, Nociti FH Jr (2003) A comparative study on the effect of nicotine administration and cigarette smoke inhalation on bone healing around titanium implants. J Periodontol 74:1454–1459

    Article  PubMed  CAS  Google Scholar 

  52. Akhter MP, Wells DJ, Short SJ, Cullen DM, Johnson ML, Haynatzki GR, Babij P, Allen KM, Yaworsky PJ, Bex F, Recker RR (2004) Bone biomechanical properties in LRP5 mutant mice. Bone 35:162–169

    Article  PubMed  CAS  Google Scholar 

  53. Akhter MP, Otero JK, Iwaniec UT, Cullen DM, Haynatzki GR, Recker RR (2004) Differences in vertebral structure and strength of inbred female mouse strains. J Musculoskelet Neuronal Interact 4:33–40

    PubMed  CAS  Google Scholar 

  54. Kodama Y, Dimai HP, Wegedal J, Sheng M, Malpe R, Kutilek S, Beamer W, Donahue LR, Rosen C, Baylink DJ, Farley J (1999) Cortical tibial bone volume in two strains of mice: effects of sciatic neurectomy and genetic regulation of bone response to mechanical loading. Bone 25:183–190

    Article  PubMed  CAS  Google Scholar 

  55. Klein RF, Mitchell SR, Phillips TJ, Belknap JK, Orwoll ES (1998) Quantitative trait loci affecting peak bone mineral density in mice. J Bone Miner Res 13:1648–1656

    PubMed  CAS  Google Scholar 

  56. Beamer WG, Donahue LR, Rosen CJ, Baylink DJ (1996) Genetic variability in adult bone density among inbred strains of mice. Bone 18:397–403

    Article  PubMed  CAS  Google Scholar 

  57. Robling AG, Turner CH (2002) Mechanotransduction in bone: genetic effects on mechanosensitivity in mice. Bone 31:562–569

    Article  PubMed  CAS  Google Scholar 

  58. Gairola CG, Drawdy ML, Block AE, Daugherty A (2001) Sidestream cigarette smoke accelerates atherogenesis in apolipoprotein E-/- mice. Atherosclerosis 156:49–55

    Article  PubMed  CAS  Google Scholar 

  59. Akhter MP, Iwaniec UT, Covey MA, Cullen DM, Kimmel DB, Recker RR (2000) Genetic variations in bone density, histomorphometry, and strength in mice. Calcif Tissue Int 67:337–349

    Article  PubMed  CAS  Google Scholar 

  60. Akhter MP, Raab DM, Turner CH, Kimmel DK, Recker RR (1992) Characterization of in vivo strain in the rat tibia during external application of a four-point bending load. J Biomech 25:1241–1246

    Article  PubMed  CAS  Google Scholar 

  61. Baumeister T, Avallone EA (1986) Marks’ standard handbook for mechanical engineers, 9th ed. McGraw-Hill, New York

    Google Scholar 

  62. Newby JR (1992) Mechanical testing handbook, vol 8. Material Information Society, American Society of Metals

  63. Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:598–604

    Article  Google Scholar 

  64. Akpe MP, Waibel PE, Larntz K, Metz AL, Noll SL, Walser MM (1987) Phosphorus availability bioassay using bone ash and bone densitometry as response criteria. Poult Sci 66:713–720

    PubMed  CAS  Google Scholar 

  65. Hill AD, Patterson KY, Veillon C, Morris ER (1986) Digestion of biological materials for mineral analyses using a combination of wet and dry ashing. Anal Chem 58:2340–2342

    Article  CAS  Google Scholar 

  66. Kapadia RD, Stroup GB, Badger AM, Koller B, Levin JM, Coatney RW, Dodds RA, Liang X, Lark MW, Gowen M (1998) Applications of microCT and MR microscopy to study pre-clinical models of osteoporosis and osteoarthritis. Technol Health Care 6:361–372

    PubMed  CAS  Google Scholar 

  67. Muller R, Hahn M, Vogel M, Delling G, Ruegsegger P (1996) Morphometric analysis of noninvasively assessed bone biopsies: comparison of high-resolution computed tomography and histologic sections. Bone 18:215–220

    PubMed  CAS  Google Scholar 

  68. Johnson KC, Hu J, Mao Y (2000) Passive and active smoking and breast cancer risk in Canada, 1994-97. The Canadian Cancer Registries Epidemiology Research Group. Cancer Causes Control 11:211–221

    CAS  Google Scholar 

  69. Gerstenfeld LC, Riva A, Hodgens K, Eyre DR, Landis WJ (1993) Post-translational control of collagen fibrillogenesis in mineralizing cultures of chick osteoblasts. J Bone Miner Res 8:1031–1043

    Article  PubMed  CAS  Google Scholar 

  70. Reddi AH, Sullivan NE (1979) Inhibition of mineralization by experimental lathyrism during matrix-induced endochondral bone differentiation. Proc Soc Exp Biol Med 162:445–448

    PubMed  CAS  Google Scholar 

  71. Weerd S, Thomas CMG, Kuster JETG, Cikot RJLM, Steegers EAP (2002) Variation of serum and urine cotinine in passive and active smokers and applicability in preconceptional smoking cessation counseling. Environ Res A 90:119–124

    Google Scholar 

  72. Witschi H, Espiritu I, Uyeminami D, Suffia M, Pinkerton KE (2004) Lung tumor response in strain a mice exposed to tobacco smoke: some dose-effect relationships. Inhalat Toxicol 16:27–32

    CAS  Google Scholar 

  73. Yang M, Kunugita N, Kitagawa K, Kang S-H, Coles B, Kadlubar FF, Katoh T, Matsuno K, Kawamoto T (2001) Individual differences in urinary cotinine levels in Japanese smokers relation to genetic polymorphism of drug-metabolizing enzymes. Cancer Epidemiol Biomarkers Prev 10:589–593

    PubMed  CAS  Google Scholar 

  74. Benowitz NL, Kuyt F, Jacob PI (1982) Circadian blood nicotine concentrations during cigarette smoking. Clin Pharmacol Ther 32:758–764

    Article  PubMed  CAS  Google Scholar 

  75. Broulik PD, Jarab J (1993) The effect of chronic nicotine administration on bone mineral content in mice. Horm Metab Res 25:219–221

    Article  PubMed  CAS  Google Scholar 

  76. Lee LL, Lee JS, Waldman SD, Casper RF, Grynpas MD (2002) Polycyclic aromatic hydrocarbons present in cigarette smoke cause bone loss in an ovariectomized rat model. Bone 30:917–923

    PubMed  CAS  Google Scholar 

  77. Yano R, Hayakawa D, Emura S, Chen H, Ozawa Y, Taguchi H, Shoumura S (2002) Effects of cigarette smoke exposure on the ultrastructure of the golden hamster parathyroid gland. Histol Histopathol 17:375–381

    PubMed  CAS  Google Scholar 

  78. Ueng SW, Lee MY, Li AF, Lin SS, Tai CL, Shih C (1997) Effect of intermittent cigarette smoke inhalation on tibial lengthening: experimental study on rabbits. J Trauma 42:231–238

    PubMed  CAS  Google Scholar 

  79. Nociti FH Jr, Cesar NJ, Carvalho MD, Sallum EA (2002) Bone density around titanium implants may be influenced by intermittent cigarette smoke inhalation: a histometric study in rats. Int J Oral Maxillofac Implants 17:347–352

    PubMed  Google Scholar 

  80. Selman M, Montano M, Ramos C, Vanda B, Becerril C, Delgado J, Sansores R, Barrios R, Pardo A (1996) Tobacco smoke-induced lung emphysema in guinea pigs is associated with increased interstitial collagenase. Am J Physiol 271:L734-L743

    PubMed  CAS  Google Scholar 

  81. Lang MR, Fiaux GW, Gillooly M, Stewart JA, Hulmes DJ, Lamb D (1994) Collagen content of alveolar wall tissue in emphysematous and non-emphysematous lungs. Thorax 49:319–326

    PubMed  CAS  Google Scholar 

  82. Akhter MP, Fan Z, Rho JY (2004) Bone intrinsic material properties in three inbred mouse strains. Calcif Tissue Int 75:416–420

    Article  PubMed  CAS  Google Scholar 

  83. Pierce JP, Gilpin E (1996) How long will today’s new adolescent smoker be addicted to cigarettes? Am J Public Health 86:253–256

    Article  PubMed  CAS  Google Scholar 

  84. Boyle P (1997) Cancer, cigarette smoking and premature death in Europe: a review including the Recommendations of European Cancer Experts Consensus Meeting, Helsinki, October 1996. Lung Cancer 17:1–60

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Daniel Wells, Nick Glass, Paul Hruby, and Gleb Haynatzki for their assistance. This study was supported partially by the State of Nebraska (LB595) and the University of Kentucky.

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Akhter, M.P., Lund, A.D. & Gairola, C.G. Bone Biomechanical Property Deterioration Due to Tobacco Smoke Exposure. Calcif Tissue Int 77, 319–326 (2005). https://doi.org/10.1007/s00223-005-0072-1

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