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Atherosclerosis and osteoporosis: age-dependent degenerative processes or related entities?

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Abstract

Osteoporosis and atherosclerosis, two multifactorial and degenerative entities, are major public health problems. These diseases accompany the aging process and share common risk factors. Furthermore, several common pathophysiological factors have been suggested. These include similar molecular pathways involving bone and vascular mineralization, estrogen deficiency, parathyroid hormone, homocysteine, lipid oxidation products, inflammatory process, as well as vitamin D and K. Moreover, the use of statins, biphosphonates, beta-blockers and experimental dual-purpose therapies based on the biological linkage of the above entities may simultaneously benefit bone loss and vascular disease. This review considers a potential link between osteoporosis and atherosclerosis beyond aging. These common factors may lead to appropriate treatment strategies.

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References

  1. Frye MA, Melton LJ 3rd, Bryant SC et al (1992) Osteoporosis and calcification of the aorta. Bone Miner 19:185–194

    PubMed  CAS  Google Scholar 

  2. Vogt MT, San Valentin R, Forrest KY et al (1997) Bone mineral density and aortic calcification: the Study of Osteoporotic fractures. J Am Geriatr Soc 45:140–145

    PubMed  CAS  Google Scholar 

  3. Sinnott B, Syed I, Sevrukov A et al (2006) Coronary calcification and osteoporosis in men and postmenopausal women are independent processes associated with aging. Calcif Tissue Int 78:195–202

    PubMed  CAS  Google Scholar 

  4. Dent CE, Engelbrecht HE, Godfrey RC (1968) Osteoporosis of lumbar vertebrae and calcification of abdominal aorta in women living in Durban. Br Med J 4:76–79

    PubMed  CAS  Google Scholar 

  5. Reid IR, Ames RW, Evans MC et al (1994) Determinants of the rate of bone loss in normal postmenopausal women. J Clin Endocrinol Metab 79:950–954

    PubMed  CAS  Google Scholar 

  6. Tekin GO, Kekilli E, Yagmur J et al (2008) Evaluation of cardiovascular risk factors and bone mineral density in postmenopausal women undergoing coronary angiography. Int J Cardiol [Epub ahead of print]

  7. Von der Recke P, Hansen MA, Hassager C (1999) The association between low bone mass at the menopause and cardiovascular mortality. Am J Med 106:273–278

    PubMed  Google Scholar 

  8. Kado DM, Browner WS, Blackwell T et al (2000) Rate of bone loss is associated with mortality in older women: a prospective study. J Bone Miner Res 15:1974–1980

    PubMed  CAS  Google Scholar 

  9. Browner WS, Seeley DG, Vogt TM et al (1991) Non-trauma mortality in elderly women with low bone mineral density. Study of Osteoporotic Fractures Research Group. Lancet 338:355–358

    PubMed  CAS  Google Scholar 

  10. Marcovitz PA, Tran HH, Franklin BA et al (2005) Usefulness of bone mineral density to predict significant coronary artery disease. Am J Cardiol 96:1059–1063

    PubMed  Google Scholar 

  11. Sennerby U, Farahmand B, Ahlbom A et al (2007) Cardiovascular diseases and future risk of hip fracture in women. Osteoporos Int 18:1355–1362

    PubMed  CAS  Google Scholar 

  12. Kiel DP, Kauppila LI, Cupples LA et al (2001) Bone loss and the progression of abdominal aortic calcification over a 25 year period: the Framingham Heart Study. Calcif Tissue Int 68:271–276

    PubMed  CAS  Google Scholar 

  13. Schulz E, Arfai K, Liu X et al (2004) Aortic calcification and the risk of osteoporosis and fractures. J Clin Endocrinol Metab 89:4246–4253

    PubMed  CAS  Google Scholar 

  14. Hyder JA, Allison MA, Criqui MH et al (2007) Association between systemic calcified atherosclerosis and bone density. Calif Tissue Int 80:301–306

    CAS  Google Scholar 

  15. Mangiafico RA, Alagona C, Pennisi P et al (2008) Increased augmentation index and central aortic blood pressure in osteoporotic postmenopausal women. Osteoporos Int 19:49–56

    PubMed  CAS  Google Scholar 

  16. Barengolts EI, Berman M, Kukreja SC et al (1998) Osteoporosis and coronary atherosclerosis in asymptomatic postmenopausal women. Calcif Tissue Int 62:209–213

    PubMed  CAS  Google Scholar 

  17. Uyama O, Yoshimoto Y, Yamamoto Y et al (1997) Bone changes and carotid atherosclerosis in postmenopausal women. Stroke 28:1730–1732

    PubMed  CAS  Google Scholar 

  18. Jorgensen L, Joakimsen O, Mathiesen EB et al (2006) Carotid plaque echogenicity and risk of nonvertebral fractures in women: a longitudinal population-based study. Calcif Tissue Int 79:207–213

    PubMed  CAS  Google Scholar 

  19. Shaffer JR, Kammerer CM, Rainwater DL et al (2007) Decreased bone mineral density is correlated with increased subclinical atherosclerosis in older, but not younger, Mexican American women and men: the San Antonio Family Osteoporosis Study. Calcif Tissue Int 81:430–441

    PubMed  CAS  Google Scholar 

  20. Van der Klift M, Pols HA, Hak AE et al (2002) Bone mineral density and the risk of peripheral arterial disease: the Rotterdam Study. Calcif Tissue Int 70:443–449

    PubMed  Google Scholar 

  21. Jorgensen L, Engstad T, Jacobsen BK (2001) Bone mineral density in acute stroke patients: low bone mineral density may predict first stroke in women. Stroke 32:47–51

    PubMed  CAS  Google Scholar 

  22. Browner WS, Pressman AR, Nevitt MC et al (1993) Association between low bone density and stroke in elderly women: the study of osteoporotic fractures. Stroke 24:940–946

    PubMed  CAS  Google Scholar 

  23. NIH (2001) Consensus development panel on osteoporosis prevention, diagnosis, and therapy. JAMA 285:785–795

    Google Scholar 

  24. Jorgensen L, Joakimsen O, Rosvold Berntsen GK et al (2004) Low bone mineral density is related to echogenic carotid artery plaques: a population-based study. Am J Epidemiol 160:549–556

    PubMed  Google Scholar 

  25. Farhat GN, Strotmeyer ES, Newman AB et al (2006) Volumetric and areal bone mineral density measures are associated with cardiovascular disease in older men and women: the health, aging and body composition study. Calcif Tissue Int 79:102–111

    PubMed  CAS  Google Scholar 

  26. Johansson C, Black D, Johnell O et al (1998) Bone mineral density is a predictor of survival. Calcif Tissue Int 63:190–196

    PubMed  CAS  Google Scholar 

  27. Cappuccio FP, Meilahn E, Zmuda JM et al (1999) High blood pressure and bone-mineral loss in elderly white women: a prospective study. Study of Osteoporotic Fractures Research Group. Lancet 354:971–975

    PubMed  CAS  Google Scholar 

  28. Selby PL (1988) Osteopenia and diabetes. Diabetic Med 5:423–428

    Article  PubMed  CAS  Google Scholar 

  29. Stevenson JC, Lees B, Devenport M et al (1989) Determinants of bone density in normal women: risk factors for future osteoporosis? Br Med J 298:924–928

    CAS  Google Scholar 

  30. Kanders B, Dempster DW, Lindsay R (1988) Interaction of calcium nutrition and physical activity on bone mass in young women. J Bone Miner Res 3:145–149

    Article  PubMed  CAS  Google Scholar 

  31. Hofbauer LC, Brueck CC, Shanahan CM et al (2007) Vascular calcification and osteoporosis-from clinical observation towards molecular understanding. Osteoporos Int 18:251–259

    PubMed  CAS  Google Scholar 

  32. Schmid K, McSharry WO, Pameijer CH et al (1980) Chemical and physiochemical studies on the mineral deposits of the human atherosclerotic aorta. Atherosclerosis 37:199–210

    PubMed  CAS  Google Scholar 

  33. Shanahan CM, Cary NR, Metcalfe JC et al (1994) High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J Clin Invest 93:2393–2402

    PubMed  CAS  Google Scholar 

  34. Luo G, Ducy P, McKee MD et al (1997) Spontaneous calcification of arteries and cartilage in mice lacking GLA protein. Nature 386:78–81

    PubMed  CAS  Google Scholar 

  35. Hamerman D (2005) Osteoporosis and atherosclerosis: biological linkages and the emergence of dual-purpose therapies. QJM 98:467–484

    PubMed  CAS  Google Scholar 

  36. Chen D, Zhao M, Mundy GR (2004) Bone morphogenetic proteins. Growth Factors 22:233–241

    PubMed  CAS  Google Scholar 

  37. Galvin KM, Donovan MJ, Lynch CA et al (2000) A role for Smad6 in development and homeostasis of the cardiovascular system. Nature Genetics 24:171–174

    PubMed  CAS  Google Scholar 

  38. Shao JS, Cheng SL, Pingsterhaus JM et al (2005) Msx2 promotes cardiovascular calcification by activating paracrine Wnt signals. J Clin Invest 115:1210–1220

    PubMed  CAS  Google Scholar 

  39. Hsu H, Lacey DL, Dunstan CR et al (1999) Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc Natl Acad Sci USA 96:3540–3545

    PubMed  CAS  Google Scholar 

  40. Collinp-Osdoby P, Rothe L, Anderson F et al (2001) Receptor activator of NF-kB and osteoprotegerin expression by human microvascular endothelial cells, regulation by inflammatory cytokines, and role in human osteoclastogenesis. J Biol Chem 276:20659–20672

    Google Scholar 

  41. Bucay N, Sarosi I, Dunstan CR et al (1998) Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev 12:1260–1268

    PubMed  CAS  Google Scholar 

  42. Browner WS, Lui LY, Cummings SR (2001) Association of serum osteoprotegerin levels with diabetes, stroke, bone density, fractures and mortality in elderly women. J Clin Endocrinol Metab 86:631–637

    PubMed  CAS  Google Scholar 

  43. Schoppet M, Sattler AM, Schaefer JR et al (2003) Increased osteoprotegerin serum levels in men with coronary artery disease. J Clin Endocrinol Metab 88:1024–1028

    PubMed  CAS  Google Scholar 

  44. Collins T, Cybulsky MI (2001) NF-kB: pivotal mediator or innocent bystander in atherogenesis? J Clin Invest 107:255–264

    PubMed  CAS  Google Scholar 

  45. Tamai K, Semenov M, Kato Y et al (2000) LDL-receptor related proteins in Wnt signal transduction. Nature 407:530–535

    PubMed  CAS  Google Scholar 

  46. Bienz M (1998) TCF: transcriptional activator or repressor? Curr Opin Cell Biol 10:366–372

    PubMed  CAS  Google Scholar 

  47. Mikhaylova L, Malmquist J, Nurminskaya M (2007) Regulation of in vitro vascular calcification by BMP4, VEGF and Wnt3a. Calcif Tissue Int 81:372–381

    PubMed  CAS  Google Scholar 

  48. Manolagas SC, Almeida M (2007) Gone with the Wnts: beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol 21:2605–2614

    PubMed  CAS  Google Scholar 

  49. Mani A, Radhakrishnan J, Wang H (2007) LRP6 mutation in a family with early coronary disease and metabolic risk factors. Science 315:1278–1282

    PubMed  CAS  Google Scholar 

  50. Banerjee C, McCabe LR, Choi JY et al (1997) Runt homology domain proteins in osteoblast differentiation: AML3/CBFA1 is a major component of a bone specific complex. J Cell Biochem 66:1–8

    PubMed  CAS  Google Scholar 

  51. Byon CH, Javed A, Dai Q et al (2008) Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx-2 by Akt signalling. J Biol Chem [Epub ahead of print]

  52. Odelberg SJ, Kollhoff A, Keating MT (2000) Dedifferentiation of mammalian myotubes induced by msx1. Cell 103:1099–1109

    PubMed  CAS  Google Scholar 

  53. Cheng SL, Shao JS, Charlton-Kachigian N et al (2003) Msx2 promotes osteogenesis and suppresses adipogenic differentiation of multipotent mesenchymal progenitors. J Biol Chem 278:45969–45977

    PubMed  CAS  Google Scholar 

  54. Christiansen C, Lindsay R (1990) Estrogen, bone loss and preservation. Osteoporos Int 1:7–13

    PubMed  CAS  Google Scholar 

  55. Mendelsohn ME, Karas RH (1999) The protective effects of estrogen on the cardiovascular system. N Engl J Med 340:1801–1811

    PubMed  CAS  Google Scholar 

  56. Losordo DW, Kearney M, Kim EA et al (1994) Variable expression of the estrogen receptor in normal and atherosclerotic coronary arteries of premenopausal women. Circulation 89:1501–1510

    PubMed  CAS  Google Scholar 

  57. Barrett-Connor E, Mueller JE, von Mühlen DG et al (2000) Low levels of esrtadiol are associated with vertebral fractures in older men, but not women: The Rancho Bernardo Study. J Clin Endocrinol Metab 85:219–223

    PubMed  CAS  Google Scholar 

  58. Khosla S, Atkinson EJ, Melton LJ 3rd et al (1997) Effects of age and estrogen status on serum parathyroid hormone levels and biochemical markers of bone turnover in women: a population-based study. J Clin Endocrinol Metab 82:1522–1527

    PubMed  CAS  Google Scholar 

  59. Stefenelli T, Mayr H, Bergler-Klein J et al (1993) Primary hyperparathyroidism: incidence of cardiac abnormalities and partial reversibility after successful parathyroidectomy. Am J Med 95:197–202

    PubMed  CAS  Google Scholar 

  60. Hak AE, Polderman KH, Westendorp IC et al (2000) Increased plasma homocysteine after menopause. Atherosclerosis 149:163–168

    PubMed  CAS  Google Scholar 

  61. Zhu X, Bonet B, Knopp RH (2000) Estradiol 17beta inhibition of LDL oxidation and endothelian cell cytotoxicity is opposed by progestins to different degrees. Atherosclerosis 148:31–41

    PubMed  CAS  Google Scholar 

  62. Christen WG, Ajani UA, Glynn RJ et al (2000) Blood levels of homocysteine and increased risks of cardiovascular disease: causal or casual? Arch Intern Med 160:422–434

    PubMed  CAS  Google Scholar 

  63. Miyao M, Morita H, Hosoi T et al (2000) Association of methylenetetrahydrofolate reductase (MTHFR) polymorphism with bone mineral density in postmenopausal Japanese women. Calcif Tissue Int 66:190–194

    PubMed  CAS  Google Scholar 

  64. Van der Mooren MJ, Wouters MG, Blom HJ et al (1994) Hormone replacement therapy may reduce high serum homocysteine in postmenopausal women. Eur J Clin Invest 24:733–736

    PubMed  Google Scholar 

  65. Parhami F, Jackson SM, Tintut Y et al (1999) Atherogenic diet and minimally oxidized low density lipoprotein inhibit osteogenic and promote adipogenic differentiation of marrow stromal cells. J Bone Miner Res 14:2067–2078

    PubMed  CAS  Google Scholar 

  66. Demer LL (2002) Vascular calcification and osteoporosis: inflammatory responses to oxidized lipids. Int J Epidemiol 31:737–741

    PubMed  Google Scholar 

  67. Kühn H, Belkner J, Suzuki H et al (1994) Oxidative modification of human lipoprotein by lipoxygenases of different positional specificities. J Lipid Res 35:1749–1759

    PubMed  Google Scholar 

  68. Klein RF, Allard J, Avnur Z et al (2004) Regulation of bone mass in mice by the lipoxygenase gene Alox15. Science 303:229–232

    PubMed  CAS  Google Scholar 

  69. Cornicelli JA, Trivedi BK (1999) 15-Lipoxygenase and its inhibitions: a novel therapeutic target for vascular disease. Curr Pharm Des 5:11–20

    PubMed  CAS  Google Scholar 

  70. Lawson JA, Rokach J, FitzGerald GA (1999) Isoprostanes: formation, analysis and use as indices of lipid peroxidation in vivo. J Biol Chem 274:24441–24444

    PubMed  CAS  Google Scholar 

  71. Tintut Y, Parhami F, Tsingotjidou A et al (2002) 8-Isoprostaglandin E2 enhances receptor-activated NFkappa B ligand (RANKL)-dependent osteoclastic potential of marrow hematopoietic precursors via the cAMP pathway. J Biol Chem 277:14221–14226

    PubMed  CAS  Google Scholar 

  72. Mangiafico RA, Malaponte G, Pennisi P et al (2007) Increased formation of 8-iso-prostaglandin F(2alpha) is associated with altered bone metabolism and lower bone mass in hypercholesterolaemic subjects. J Intern Med 261:587–596

    PubMed  CAS  Google Scholar 

  73. Pai JK, Pischon T, Ma J et al (2004) Inflammatory markers and the risk of coronary heart disease in men and women. N Eng J Med 351:2599–2610

    CAS  Google Scholar 

  74. Papanicolaou DA, Wilder RL, Manolagas SC et al (1998) The pathophysiologic roles of interleukin-6 in human disease. Ann Intern Med 128:127–137

    PubMed  CAS  Google Scholar 

  75. Koh JM, Khang YH, Jung CH et al (2005) Higher circulating hsCRP levels are associated with lower bone mineral density in healthy pre- and postmenopausal women: evidence for a link between systemic inflammation and osteoporosis. Osteoporos Int 16:1263–1271

    PubMed  CAS  Google Scholar 

  76. Kim BJ, Yu YM, Kim EN et al (2007) Relationship between serum hsCRP concentration and biochemical bone turnover markers in healthy pre- and postmenopausal women. Clin Endocrinol (Oxf) 67:152–158

    CAS  Google Scholar 

  77. Gallagher JC, Riggs BL, Eisman J et al (1979) Intestinal calcium absorption and serum vitamin D metabolites in normal subjects and osteoporotic patients. J Clin Invest 64:729–736

    PubMed  CAS  Google Scholar 

  78. Merke J, Milde P, Lewicka S et al (1989) Identification and regulation of 1,25-dihydroxyvitamin D3 receptor activity and biosynthesis of 1,25-dihydroxyvitamin D3. Studies in cultured bovine aortic endothelial cells and human dermal capillaries. J Clin Invest 83:1903–1915

    PubMed  CAS  Google Scholar 

  79. Merke J, Hofmann W, Goldschmidt D et al (1987) Demonstration of 1,25(OH)2 vitamin D3 receptors and actions in vascular smooth muscle cells in vitro. Calcif Tissue Int 41:112–114

    PubMed  CAS  Google Scholar 

  80. Kammerer CM, Dualan AA, Samollow PB et al (2004) Bone mineral density, carotid artery intimal medial thickness, and the vitamin D receptor BsmI Polymorphism in Mexican American Women. Calcif Tissue Int 75:292–298

    PubMed  CAS  Google Scholar 

  81. Gong G, Stern HS, Cheng SC et al (1999) The association of bone mineral density with vitamin D receptor gene polymorphisms. Osteoporos Int 9:55–64

    PubMed  CAS  Google Scholar 

  82. Van Schooten FJ, Hirvonen A, Maas LM et al (1998) Putative susceptibility markers of coronary artery disease: association between VDR genotype, smoking, and aromatic DNA adduct levels in human right atrial tissue. FASEB J 12:1409–1417

    PubMed  Google Scholar 

  83. Ortlepp JR, Lauscher J, Hoffmann R et al (2001) The vitamin D receptor gene variant is associated with the prevalence of type 2 diabetes mellitus and coronary artery disease. Diabet Med 18:842–845

    PubMed  CAS  Google Scholar 

  84. Ortlepp JR, von Korff A, Hanrath P et al (2003) Vitamin D receptor gene polymorphism BsmI is not associated with the prevalence and severity of CAD in a large-scale angiographic cohort of 3441 patients. Eur J Clin Invest 33:106–109

    PubMed  CAS  Google Scholar 

  85. Braam LA, Knapen MH, Geusens P et al (2003) Vitamin K1 supplementation retards bone loss in postmenopausal women between 50 and 60 years of age. Calcif Tissue Int 73:21–26

    PubMed  CAS  Google Scholar 

  86. Price PA, Williamson MK, Lothringer JW (1981) Origin of the vitamin K-dependent bone protein found in plasma and its clearance by kidney and bone. J Biol Chem 256:12760–12766

    PubMed  CAS  Google Scholar 

  87. Jie KG, Bots ML, Vermeer C et al (1996) Vitamin K status and bone mass in women with and without aortic atherosclerosis: a population-based study. Calcif Tissue Int 59:352–356

    PubMed  CAS  Google Scholar 

  88. Baigent C, Keech A, Kearney PM et al (2005) Cholesterol Treatment Trialists’ (CTT) Collaborators. Efficacy and safety of cholesterol-lowering treatment: prospective meta-analysis of data from 90,056 participants in 14 randomised trials of statins. Lancet 366:1267–1278

    PubMed  CAS  Google Scholar 

  89. Athyros VG, Kakafika AI, Papageorgiou AA et al (2007) GREACE Study Collaborative Group. Atorvastatin decreases triacylglycerol-associated risk of vascular events in coronary heart disease patients. Lipids 42:999–1009

    PubMed  CAS  Google Scholar 

  90. Paraskevas KI, Athyros VG, Briana DD et al (2007) Statins exert multiple beneficial effects on patients undergoing percutaneous revascularization procedures. Curr Drug Targets 8:942–951

    PubMed  CAS  Google Scholar 

  91. Meier CR, Schlienger RG, Kraenzlin ME et al (2000) HMG-CoA reductase inhibitors and the risk of fractures. JAMA 283:3205–3210

    PubMed  CAS  Google Scholar 

  92. Paraskevas KI, Tzovaras AA, Briana DD et al (2007) Emerging indications for statins: a pluripotent family of agents with several potential applications. Curr Pharm Des 13:3622–3636

    PubMed  CAS  Google Scholar 

  93. Liao JK (2002) Isoprenoids as mediators of the biological effects of statins. J Clin Invest 110:285–288

    PubMed  CAS  Google Scholar 

  94. Alegret M, Silvestre JS (2006) Pleiotropic effects of statins and related pharmacological experimental approaches. Methods Find Exp Clin Pharmacol 28:627–656

    PubMed  CAS  Google Scholar 

  95. Hughes A, Rogers MJ, Idris AI et al (2007) A comparison between the effects of hydrophobic and hydrophilic statins on osteoclast function in vitro and ovariectomy-induced bone loss in vivo. Calcif Tissue Int 81:403–413

    PubMed  CAS  Google Scholar 

  96. Chan MH, Mak TW, Chiu RW et al (2001) Simvastatin increases serum osteocalcin concentration in patients treated for hypercholesterolaemia. J Clin Endocrinol Metab 86:4556–4559

    PubMed  CAS  Google Scholar 

  97. Pérez-Castrillón JL, Vega G, Abad L et al (2007) Effects of Atorvastatin on vitamin D levels in patients with acute ischemic heart disease. Am J Cardiol 99:903–905

    PubMed  Google Scholar 

  98. Mundy G, Garrett R, Harris S et al (1999) Stimulation of bone formation in vitro and in rodents by statins. Science 286:1946–1949

    PubMed  CAS  Google Scholar 

  99. Bauer DC, Mundy GR, Jamal SA et al (2004) Use of statins and fracture: results of 4 prospective studies and cumulative meta-analysis of observational studies and controlled trials. Arch Intern Med 164:146–152

    PubMed  CAS  Google Scholar 

  100. Reid IR, Hague W, Emberson J et al (2001) Effect of pravastatin on frequency of fracture in the LIPID study: secondary analysis of a randomised controlled trial. Long-term Intervention with Pravastatin in Ischaemic Disease. Lancet 357:509–512

    PubMed  CAS  Google Scholar 

  101. Pedersen TR, Kjekshus J (2000) Statin drugs and the risk of fracture. 4S Study Group. JAMA 284:1921–1922

    PubMed  CAS  Google Scholar 

  102. Uzzan B, Cohen R, Nicolas P et al (2007) Effects of statins on bone mineral density: a meta-analysis of clinical studies. Bone 40:1581–1587

    PubMed  CAS  Google Scholar 

  103. Ylitalo R (2000) Bisphosphonates and atherosclerosis. Gen Pharmacol 35:287–296

    PubMed  CAS  Google Scholar 

  104. Luckman SP, Hughes DE, Coxon FP et al (1998) Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras. J Bone Miner Res 13:581–589

    PubMed  CAS  Google Scholar 

  105. Koshiyama H, Nakamura Y, Tanaka S (2000) Decrease in carotid intima-media thickness after 1-year therapy with etidronate for osteopenia associated with type 2 diabetes. J Clin Endocrinol Metab 85:2793–2796

    PubMed  CAS  Google Scholar 

  106. Bonnet N, Gadois C, McCloskey E et al (2007) Protective effect of beta blockers in postmenopausal women: influence on fractures, bone density, micro and macroarchitecture. Bone 40:1209–1216

    PubMed  CAS  Google Scholar 

  107. Chenu C (2004) Role of innervation in the control of bone remodeling. J Musculoskelet Neuronal Interact 2:132–134

    Google Scholar 

  108. Togari A (2002) Adrenergic regulation of bone metabolism: possible involvement of sympathetic innervation of osteoblastic and osteoclastic cells. Microsc Res Tech 58:77–84

    PubMed  CAS  Google Scholar 

  109. Meisinger C, Heier M, Lang O et al (2007) Beta-blocker use and risk of fractures in men and women from the general population: the MONICA/KORA Augsburg cohort study. Osteoporos Int 18:1189–1195

    PubMed  CAS  Google Scholar 

  110. Reid IR, Ames RW, Orr-Walker BJ et al (2000) Hydrochlorothiazide reduces loss of cortical bone in normal postmenopausal women: a randomized controlled trial. Am J Med 109:362–370

    PubMed  CAS  Google Scholar 

  111. Bolland MJ, Ames RW, Horne AM et al (2007) The effect of treatment with a thiazide diuretic for 4 years on bone density in normal postmenopausal women. Osteoporos Int 18:479–486

    PubMed  CAS  Google Scholar 

  112. Dvorak MM, De Joussineau C, Carter DH et al (2007) Thiazide diuretics directly induce osteoblast differentiation and mineralized nodule formation by targeting a sodium chloride cotransporter in bone. J Am Soc Nephrol 18:2509–2516

    PubMed  CAS  Google Scholar 

  113. Shimizu H, Nakagami H, Osako MK et al (2008) Angiotensin II accelerates osteoporosis by activating osteoclasts. FASEB J 6 [Epub ahead of print]

  114. Lynn H, Kwok T, Wong SY et al (2006) Angiotensin converting enzyme inhibitor use is associated with higher bone mineral density in elderly Chinese. Bone 38:584–588

    PubMed  CAS  Google Scholar 

  115. Stimpel M, Jee WS, Ma Y et al (1995) Impact of antihypertensive therapy on postmenopausal osteoporosis: effects of the angiotensin converting enzyme inhibitor moexipril, 17beta-estradiol and their combination on the ovariectomy-induced cancellous bone loss in young rats. J Hypertens 13:1852–1856

    PubMed  CAS  Google Scholar 

  116. Pérez-Castrillón JL, Silva J, Justo I et al (2003) Effect of quinapril, quinapril-hydrochlorothiazide, and enalapril on bone mass of hypertensive subjects: relationship with angiotensin converting enzyme polymorphisms. Am J Hypertens 16:453–459

    PubMed  Google Scholar 

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This review was written independently; no company or institution supported it financially. Some of the authors have attended conferences, given lectures and participated in advisory boards or other trials sponsored by various pharmaceutical companies.

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Correspondence to D. P. Mikhailidis.

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Anagnostis, P., Karagiannis, A., Kakafika, A.I. et al. Atherosclerosis and osteoporosis: age-dependent degenerative processes or related entities?. Osteoporos Int 20, 197–207 (2009). https://doi.org/10.1007/s00198-008-0648-5

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