Skip to main content
Top
Published in: Calcified Tissue International 5/2005

01-11-2005 | Laboratory Investigations

Bone Biomechanical Property Deterioration Due to Tobacco Smoke Exposure

Authors: M. P. Akhter, A. D. Lund, C. G. Gairola

Published in: Calcified Tissue International | Issue 5/2005

Login to get access

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.
Literature
1.
go back to reference 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 6:207-212PubMed 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 6:207-212PubMed
2.
go back to reference Hodgson TA (1992) Cigarette smoking and lifetime medical expenditures. Milbank Q 70:81–125PubMed Hodgson TA (1992) Cigarette smoking and lifetime medical expenditures. Milbank Q 70:81–125PubMed
3.
4.
go back to reference Taylor DH Jr, Hasselblad V, Henley SJ, Thun MJ, Sloan FA (2002) Benefits of smoking cessation for longevity. Am J Public Health 2002;92:990–996PubMed Taylor DH Jr, Hasselblad V, Henley SJ, Thun MJ, Sloan FA (2002) Benefits of smoking cessation for longevity. Am J Public Health 2002;92:990–996PubMed
5.
go back to reference 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):566–574PubMed 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):566–574PubMed
6.
go back to reference Rogers RG, Powell Griner E (1991) Life expectancies of cigarette smokers and nonsmokers in the United States. Soc Sci Med 32:1151–1159CrossRefPubMed Rogers RG, Powell Griner E (1991) Life expectancies of cigarette smokers and nonsmokers in the United States. Soc Sci Med 32:1151–1159CrossRefPubMed
8.
go back to reference Bilello KS, Murin S, Matthay RA (2002) Epidemiology, etiology, and prevention of lung cancer. Clin Chest Med 23:1–25CrossRefPubMed Bilello KS, Murin S, Matthay RA (2002) Epidemiology, etiology, and prevention of lung cancer. Clin Chest Med 23:1–25CrossRefPubMed
9.
go back to reference Lowenfels AB, Maisonneuve P (2002) Epidemiologic and etiologic factors of pancreatic cancer. Hematol Oncol Clin North Am 16:1–16CrossRefPubMed Lowenfels AB, Maisonneuve P (2002) Epidemiologic and etiologic factors of pancreatic cancer. Hematol Oncol Clin North Am 16:1–16CrossRefPubMed
10.
go back to reference Kesteloot H (2003) Social class, all-cause, cardiovascular and cancer mortality: the importance of cigarette smoking. Acta Cardiol 58:285–287PubMed Kesteloot H (2003) Social class, all-cause, cardiovascular and cancer mortality: the importance of cigarette smoking. Acta Cardiol 58:285–287PubMed
11.
go back to reference Stabile LP, Siegfried JM (2003) Sex and gender differences in lung cancer. J Gend Specif Med 6:37–48PubMed Stabile LP, Siegfried JM (2003) Sex and gender differences in lung cancer. J Gend Specif Med 6:37–48PubMed
12.
go back to reference Centers for Disease Control and Prevention (2003) Cigarette smoking-attributable morbidity —United States, 2000. MMWR Morb Mortal Wkly Rep 52:842–844 Centers for Disease Control and Prevention (2003) Cigarette smoking-attributable morbidity —United States, 2000. MMWR Morb Mortal Wkly Rep 52:842–844
13.
go back to reference 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 136:298–304CrossRefPubMed 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 136:298–304CrossRefPubMed
14.
go back to reference Hopper JL, Seeman E (1994) Bone density in twins discordant for tobacco use. N Engl J Med 330:387–392CrossRefPubMed Hopper JL, Seeman E (1994) Bone density in twins discordant for tobacco use. N Engl J Med 330:387–392CrossRefPubMed
15.
go back to reference Krall EA, Dawson-Hughes B (1999) Smoking increases bone loss and decreases intestinal calcium absorption. J Bone Miner Res 14:215–220PubMed Krall EA, Dawson-Hughes B (1999) Smoking increases bone loss and decreases intestinal calcium absorption. J Bone Miner Res 14:215–220PubMed
16.
go back to reference 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 315:841–846PubMed 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 315:841–846PubMed
17.
go back to reference Pocock NA, Eisman JA, Kelly PJ, Sambrook PN, Yeates MG (1989) Effects of tobacco use on axial and appendicular bone mineral density. Bone 10:329–331CrossRefPubMed Pocock NA, Eisman JA, Kelly PJ, Sambrook PN, Yeates MG (1989) Effects of tobacco use on axial and appendicular bone mineral density. Bone 10:329–331CrossRefPubMed
18.
go back to reference 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 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
19.
go back to reference Cornuz J, Feskanich D, Willett WC, Colditz GA (1999) Smoking, smoking cessation, and risk of hip fracture in women. Am J Med 106:311–314CrossRefPubMed Cornuz J, Feskanich D, Willett WC, Colditz GA (1999) Smoking, smoking cessation, and risk of hip fracture in women. Am J Med 106:311–314CrossRefPubMed
20.
go back to reference 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 4:451–458PubMedCrossRef 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 4:451–458PubMedCrossRef
21.
go back to reference Qandil R, Sandhu HS, Matthews DC (1997) Tobacco smoking and periodontal diseases. J Can Dent Assoc 63:187–195PubMed Qandil R, Sandhu HS, Matthews DC (1997) Tobacco smoking and periodontal diseases. J Can Dent Assoc 63:187–195PubMed
22.
go back to reference Moran S, Glazier G, Armstrong K (2003) Women smokers’ perceptions of smoking-related health risks. J Womens Health 12:363–371 Moran S, Glazier G, Armstrong K (2003) Women smokers’ perceptions of smoking-related health risks. J Womens Health 12:363–371
23.
go back to reference Ward KD, Klesges RC (2001) A meta-analysis of the effects of cigarette smoking on bone mineral density. Calcif Tissue Int 68:259–270 Ward KD, Klesges RC (2001) A meta-analysis of the effects of cigarette smoking on bone mineral density. Calcif Tissue Int 68:259–270
24.
go back to reference 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 28:274–276PubMed 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 28:274–276PubMed
25.
go back to reference 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 29:845–851CrossRefPubMed 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 29:845–851CrossRefPubMed
26.
go back to reference Mueller L, Ciervo CA (1998) Smoking in women. J Am Osteopath Assoc 98(12 suppl):S7-S10PubMed Mueller L, Ciervo CA (1998) Smoking in women. J Am Osteopath Assoc 98(12 suppl):S7-S10PubMed
27.
28.
go back to reference Lipsitz CM (1993) Have you come a long way, baby? Smoking trends in women. Md Med J 42:27–31PubMed Lipsitz CM (1993) Have you come a long way, baby? Smoking trends in women. Md Med J 42:27–31PubMed
29.
go back to reference Shulman A, Ellenbogen A, Maymon R, Bahary C (1990) Smoking out the oestrogens. Hum Reprod 5:231–233PubMed Shulman A, Ellenbogen A, Maymon R, Bahary C (1990) Smoking out the oestrogens. Hum Reprod 5:231–233PubMed
30.
go back to reference Lindquist O, Bengtsson C, Lapidus L (1985) Relationships between the menopause and risk factors for ischaemic heart disease. Acta Obstet Gynecol Scand Suppl 130:43–47PubMed Lindquist O, Bengtsson C, Lapidus L (1985) Relationships between the menopause and risk factors for ischaemic heart disease. Acta Obstet Gynecol Scand Suppl 130:43–47PubMed
31.
go back to reference 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 51:1271–1276CrossRefPubMed 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 51:1271–1276CrossRefPubMed
32.
33.
go back to reference 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 15:217–225CrossRefPubMed 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 15:217–225CrossRefPubMed
34.
go back to reference 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 15:710–720PubMed 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 15:710–720PubMed
35.
go back to reference 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 27:658–664CrossRefPubMed 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 27:658–664CrossRefPubMed
36.
go back to reference Galvin RJ, Ramp WEEK, Lenz LG (1988) Smokeless tobacco contains a non-nicotine inhibitor of bone metabolism. Toxicol Appl Pharmacol 95:292–300CrossRefPubMed Galvin RJ, Ramp WEEK, Lenz LG (1988) Smokeless tobacco contains a non-nicotine inhibitor of bone metabolism. Toxicol Appl Pharmacol 95:292–300CrossRefPubMed
37.
go back to reference Krall EA, Dawson-Hughes B (1991) Smoking and bone loss among postmenopausal women. J Bone Miner Res 6:331–338PubMed Krall EA, Dawson-Hughes B (1991) Smoking and bone loss among postmenopausal women. J Bone Miner Res 6:331–338PubMed
38.
go back to reference 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 315:1305–1309PubMedCrossRef 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 315:1305–1309PubMedCrossRef
39.
go back to reference 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 85:590–596CrossRefPubMed 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 85:590–596CrossRefPubMed
40.
go back to reference 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 18:1036–1042PubMed 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 18:1036–1042PubMed
41.
go back to reference 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 13:83–88CrossRefPubMed 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 13:83–88CrossRefPubMed
42.
go back to reference Krall EA, Dawson-Hughes B (1999) Smoking increases bone loss and decreases intestinal calcium absorption. J Bone Miner Res 14:215–220PubMed Krall EA, Dawson-Hughes B (1999) Smoking increases bone loss and decreases intestinal calcium absorption. J Bone Miner Res 14:215–220PubMed
44.
go back to reference 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 82:243–249PubMed 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 82:243–249PubMed
45.
go back to reference 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 85:181–187PubMedCrossRef 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 85:181–187PubMedCrossRef
46.
go back to reference 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 67:68–74CrossRefPubMed 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 67:68–74CrossRefPubMed
47.
go back to reference 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 65:246–249CrossRefPubMed 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 65:246–249CrossRefPubMed
48.
go back to reference 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 21:14–19CrossRefPubMed 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 21:14–19CrossRefPubMed
49.
go back to reference 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 68:358–364CrossRefPubMed 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 68:358–364CrossRefPubMed
50.
go back to reference Silcox DH III, Daftari T, Boden SD, Schimandle JH, Hutton WC, Whitesides TE Jr (1995) The effect of nicotine on spinal fusion. Spine 20:1549–1553PubMed Silcox DH III, Daftari T, Boden SD, Schimandle JH, Hutton WC, Whitesides TE Jr (1995) The effect of nicotine on spinal fusion. Spine 20:1549–1553PubMed
51.
go back to reference 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 74:1454–1459CrossRefPubMed 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 74:1454–1459CrossRefPubMed
52.
go back to reference 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 35:162–169CrossRefPubMed 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 35:162–169CrossRefPubMed
53.
go back to reference 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 4:33–40PubMed 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 4:33–40PubMed
54.
go back to reference 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 25:183–190CrossRefPubMed 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 25:183–190CrossRefPubMed
55.
go back to reference 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 13:1648–1656PubMed 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 13:1648–1656PubMed
56.
go back to reference Beamer WG, Donahue LR, Rosen CJ, Baylink DJ (1996) Genetic variability in adult bone density among inbred strains of mice. Bone 18:397–403CrossRefPubMed Beamer WG, Donahue LR, Rosen CJ, Baylink DJ (1996) Genetic variability in adult bone density among inbred strains of mice. Bone 18:397–403CrossRefPubMed
57.
go back to reference Robling AG, Turner CH (2002) Mechanotransduction in bone: genetic effects on mechanosensitivity in mice. Bone 31:562–569CrossRefPubMed Robling AG, Turner CH (2002) Mechanotransduction in bone: genetic effects on mechanosensitivity in mice. Bone 31:562–569CrossRefPubMed
58.
go back to reference Gairola CG, Drawdy ML, Block AE, Daugherty A (2001) Sidestream cigarette smoke accelerates atherogenesis in apolipoprotein E-/- mice. Atherosclerosis 156:49–55CrossRefPubMed Gairola CG, Drawdy ML, Block AE, Daugherty A (2001) Sidestream cigarette smoke accelerates atherogenesis in apolipoprotein E-/- mice. Atherosclerosis 156:49–55CrossRefPubMed
59.
go back to reference 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 67:337–349CrossRefPubMed 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 67:337–349CrossRefPubMed
60.
go back to reference 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 25:1241–1246CrossRefPubMed 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 25:1241–1246CrossRefPubMed
61.
go back to reference Baumeister T, Avallone EA (1986) Marks’ standard handbook for mechanical engineers, 9th ed. McGraw-Hill, New York Baumeister T, Avallone EA (1986) Marks’ standard handbook for mechanical engineers, 9th ed. McGraw-Hill, New York
62.
go back to reference Newby JR (1992) Mechanical testing handbook, vol 8. Material Information Society, American Society of Metals Newby JR (1992) Mechanical testing handbook, vol 8. Material Information Society, American Society of Metals
63.
go back to reference Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:598–604CrossRef Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:598–604CrossRef
64.
go back to reference 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 66:713–720PubMed 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 66:713–720PubMed
65.
go back to reference 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 58:2340–2342CrossRef 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 58:2340–2342CrossRef
66.
go back to reference 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 6:361–372PubMed 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 6:361–372PubMed
67.
go back to reference 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 18:215–220PubMed 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 18:215–220PubMed
68.
go back to reference 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 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
69.
go back to reference 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 8:1031–1043PubMedCrossRef 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 8:1031–1043PubMedCrossRef
70.
go back to reference Reddi AH, Sullivan NE (1979) Inhibition of mineralization by experimental lathyrism during matrix-induced endochondral bone differentiation. Proc Soc Exp Biol Med 162:445–448PubMed Reddi AH, Sullivan NE (1979) Inhibition of mineralization by experimental lathyrism during matrix-induced endochondral bone differentiation. Proc Soc Exp Biol Med 162:445–448PubMed
71.
go back to reference 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 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
72.
go back to reference 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 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
73.
go back to reference 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 10:589–593PubMed 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 10:589–593PubMed
74.
go back to reference Benowitz NL, Kuyt F, Jacob PI (1982) Circadian blood nicotine concentrations during cigarette smoking. Clin Pharmacol Ther 32:758–764PubMedCrossRef Benowitz NL, Kuyt F, Jacob PI (1982) Circadian blood nicotine concentrations during cigarette smoking. Clin Pharmacol Ther 32:758–764PubMedCrossRef
75.
go back to reference Broulik PD, Jarab J (1993) The effect of chronic nicotine administration on bone mineral content in mice. Horm Metab Res 25:219–221PubMedCrossRef Broulik PD, Jarab J (1993) The effect of chronic nicotine administration on bone mineral content in mice. Horm Metab Res 25:219–221PubMedCrossRef
76.
go back to reference 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 30:917–923PubMed 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 30:917–923PubMed
77.
go back to reference 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 17:375–381PubMed 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 17:375–381PubMed
78.
go back to reference 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 42:231–238PubMed 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 42:231–238PubMed
79.
go back to reference 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 17:347–352PubMed 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 17:347–352PubMed
80.
go back to reference 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-L743PubMed 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-L743PubMed
81.
go back to reference 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 49:319–326PubMed 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 49:319–326PubMed
82.
go back to reference Akhter MP, Fan Z, Rho JY (2004) Bone intrinsic material properties in three inbred mouse strains. Calcif Tissue Int 75:416–420CrossRefPubMed Akhter MP, Fan Z, Rho JY (2004) Bone intrinsic material properties in three inbred mouse strains. Calcif Tissue Int 75:416–420CrossRefPubMed
83.
go back to reference Pierce JP, Gilpin E (1996) How long will today’s new adolescent smoker be addicted to cigarettes? Am J Public Health 86:253–256PubMedCrossRef Pierce JP, Gilpin E (1996) How long will today’s new adolescent smoker be addicted to cigarettes? Am J Public Health 86:253–256PubMedCrossRef
84.
go back to reference 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 17:1–60CrossRefPubMed 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 17:1–60CrossRefPubMed
Metadata
Title
Bone Biomechanical Property Deterioration Due to Tobacco Smoke Exposure
Authors
M. P. Akhter
A. D. Lund
C. G. Gairola
Publication date
01-11-2005
Publisher
Springer-Verlag
Published in
Calcified Tissue International / Issue 5/2005
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-005-0072-1

Other articles of this Issue 5/2005

Calcified Tissue International 5/2005 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.