Bone disorders associated with the human immunodeficiency virus: Pathogenesis and management

Pharmacotherapy

Volumn 24, Issue 10 II, 2004, Pages 1331-1346

  Qaqish, Roula B ^a   Sims, Keri A ^b  

^a ABBOTT LABORATORIES   (United States)

^b ST LOUIS COLLEGE OF PHARMACY   (United States)

Author keywords

Antiretroviral therapy; Bone; HIV; Osteonecrosis; Osteopenia; Osteoporosis

Indexed keywords

ALENDRONIC ACID; AMPRENAVIR; ANTIRETROVIRUS AGENT; BISPHOSPHONIC ACID DERIVATIVE; CALCIUM; EFAVIRENZ; ESTROGEN; INDINAVIR; LAMIVUDINE; LOPINAVIR; NELFINAVIR; NEVIRAPINE; PROGESTERONE; RITONAVIR; SAQUINAVIR; SELECTIVE ESTROGEN RECEPTOR MODULATOR; STAVUDINE; TENOFOVIR; TESTOSTERONE; VITAMIN D;

ALCOHOL CONSUMPTION; BONE DENSITY; BONE DISEASE; BONE NECROSIS; CALCIUM INTAKE; CLINICAL TRIAL; DISEASE SEVERITY; DUAL ENERGY X RAY ABSORPTIOMETRY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HORMONE SUBSTITUTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LIPODYSTROPHY; NONHUMAN; OSTEOLYSIS; OSTEOPENIA; OSTEOPOROSIS; PATHOGENESIS; PREVALENCE; REVIEW; RISK FACTOR; SMOKING; TREATMENT WITHDRAWAL; VITAMIN SUPPLEMENTATION;

ANTI-HIV AGENTS; BONE DISEASES; CALCIUM; DIPHOSPHONATES; HIV INFECTIONS; HUMANS; VITAMIN D;

EID: 4644351563     PISSN: 02770008     EISSN: None     Source Type: Journal    
DOI: 10.1592/phco.24.14.1331.43150     Document Type: Review

References (82)

1. Murphy EL, Coller AC, Kalish LA, et al. Highly active antiretroviral therapy decreases mortality and morbidity in patients with advanced HIV disease. Ann Intern Med 2001;344:1764-72.
2. Palella FJ, Delaney KM, Moorman AC, et al. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. N Engl J Med 1998;338:853-60.
3. Porter K, Babiker A, Bhaskaran K, et al. Determinants of survival following HIV-1 seroconversion after the introduction of HAART. Lancet 2003;362:1267-74.
4. Cummings SR, Bates D, Black DM. Clinical use of bone densitometry: scientific review. JAMA 2002;288:1889-97.
5. Osteoporosis Task Force. American Association of Clinical Endocrinologists 2001 medical guidelines for clinical practice for the prevention and management of postmenopausal osteoporosis - revised. Available from www.aace.com/clin/guidelines/osteoporosis2001Revised.pdf. Accessed November 13, 2003.
6. Ross P, Davis J, Epstein R, et al. Pre-existing fractures and bone mass predict vertebral fracture incidence in women. Ann Intern Med 1991;114:919-23.
7. Cummings S, Black D, Nevitt M, et al. Bone density at various sites for prediction of hip fractures. The study of osteoporotic fractures research group. Lancet 1993;341:72-5.
8. Lindsay R, Cosman F. Osteoporosis. In: Braunwald E, Fauci AS, Kasper DL, Hauser SL, Longo DL, Jameson JL, eds. Harrison's principles of internal medicine, 15th ed. New York: McGraw-Hill Professional, 2001:2226-37.
9. Nacher M, Serrano S, González A, et al. Osteoblasts in HIV-infected patients: HIV-1 infection and cell function. AIDS 2001;15:2239-43.
10. Fauci AS. Host factors and pathogenesis of HIV induced disease. Nature 1996;384:529-34.
11. Manolagas SC, Jilka RL. Bone marrow, cytokines, and bone remodeling: emerging insights into the pathophysiology of osteoporosis. N Engl J Med 1995;332:305-11.
12. Fakruddin JM, Laurence J. HIV-1 modulates TRANCE expression in vitro and in vivo: potential mechanism for the osteopenia of HIV disease. Presented at the 9th conference on retroviruses and opportunistic infections, Seattle, February 24-28, 2002.
13. Kong YY, Penninger JM. Molecular control of bone remodeling and osteoporosis. Exp Gerontol 2000;35:947-56.
14. Grcevic D, Katavic V, Kresimir I, Kovacic N, Lorenzo JA, Marusic A. Cellular and molecular interactions between immune system and bone. Croat Med J 2001;42:384-92.
15. Aubin JE, Bonnelye E. Osteoprotegerin and its ligand: a new paradigm for regulation of osteoclastogenesis and bone resorption. Medscape Women's Health ejournal 2000;5:1-10.
16. Romas E, Martin TJ. Cytokines in the pathogenesis of osteoporosis. Osteoporos Int 1997;7(suppl 3):S47-53.
17. Horwood NJ, Kartsogiannis V, Quinn JMW, Romas E, Martin TJ, Gillepsie MT. Activated T cells support osteoclast formation in vitro. Biochem Biophys Res Commun 1999;265:144-50.
18. McDermott AY, Shevitz A, Knox T, Roubenoff R, Kehayias J, Gorbach S. Effect of highly active antiretroviral therapy on fat, lean, and bone mass in HIV-seropositive men and women. Am J Clin Nutr 2001;74:679-86.
19. Moore AL, Vashisht A, Sabin CA, et al. Reduced bone mineral density in HIV-positive individuals. AIDS 2001;15:1731-3.
20. Tebas P, Powderly WG, Claxton S, et al. Accelerated bone mineral loss in HIV-infected patients receiving potent antiretroviral therapy. AIDS 2000;14:F63-7.
21. Carr A, Miller J, Eisman JA, Cooper DA. Osteopenia in HIV-infected men: association with asymptomatic lactic academia and lower weight pre-antiretroviral therapy. AIDS 2001;15:703-9.
22. Dube MP, Qian D, Edmondson-Melancon H, et al. Prospective, intensive study of metabolic changes associated with 48 weeks of amprenavir-based antiretroviral therapy. Clin Infect Dis 2002;35:475-81.
23. Huang JS, Rietschel P, Hadigan CM, Rosenthal DI, Grinspoon S. Increased abdominal visceral fat is associated with reduced bone density in HIV-infected men with lipodystrophy. AIDS 2001;15:975-82.
24. Brown T, Ruppe M, Kassner R, et al. Reduced bone mineral density in human immunodeficiency virus-infected patients and its association with central adiposity and postload hyperglycemia. J Clin Endocrinol Metab 2004;89:1200-6.
25. Gilead Sciences. Data on file. Foster City, CA; 2004.
26. Struble K, Murray J, Schneider B, Soon G. Bone fracture (fx) rates in HIV+ patients receiving PI vs non-PI regimens [abstr]. In: Program and abstracts of the 41st interscience conference on antimicrobial agents and chemotherapy. Washington, DC: American Society for Microbiology, 2001:1-1329.
27. McComsey G, Huang J, Woolley I, et al. Fragility fractures in HIV-infected subjects: an area for improvement. Presented at the 11th conference on retroviruses and opportunistic infections, San Francisco, February 8-11, 2004.
28. O'Connel MB, Elliott ME. Osteoporosis and osteomalacia. In: DiPiro JT, Talbert RL, Yee GC, Matzke GR, Wells BG, Posey LM, eds. Pharmacotherapy: a pathophysiologic approach, 5th ed. New York: McGraw-Hill, 2002:1599-621.
29. Serrano S, Marinoso ML, Soriano JC, et al. Bone remodeling in human immunodeficiency virus-1-infected patients: a histomorphometric study. Bone 1995;16:185-91.
30. Paton NI, Macallan DC, Griffin GE, Pazianas M. Bone mineral density in patients with human immunodeficiency virus infection. Calcif Tissue Int 1997;61:30-2.
31. Pérez-Mas JR, Díaz I, Mun̄oz J, et al. Osteopenia in antiretroviral-naīve HIV-1-infected patients. Presented at the XIV international AIDS conference, Barcelona, Spain, July 7-12, 2002.
32. McGowan I, Cheng A, Coleman S, Johnson A, Genant H. Assessment of bone mineral density (bmd) in HIV-infected antiretroviral-therapy-naïve patients. Presented at the 8th conference on retroviruses and opportunistic infections, Chicago, February 4-8, 2001.
33. Teichmann J, Stephan E, Lange U, et al. Osteopenia in HIV-infected women prior to highly active antiretroviral therapy. J Infect 2003;46:221-7.
34. Aukrust P, Haug CJ, Ueland T, et al. Decreased bone formative and enhanced resorptive markers in human immunodeficiency virus infection: indication of normalization of the bone-remodeling process during highly active antiretroviral therapy. J Clin Endocrinol Metab 1999;84:145-50.
35. Hernandez Quero J, Ortego Centeno N, Munoz-Torres M, Martinez Ferez MA, Higuera Torres-Puchol JM. Alterations in bone turnover in HIV-positive patients. Infection 1993;21:220-2.
36. Billaud E, Allavena C, Maugars Y, et al. Osteopenia and osteoporosis in HIV-infected patients [abstr]. In: Program and abstracts of the 40th interscience conference on antimicrobial agents and chemotherapy. Washington, DC: American Society for Microbiology, 2000:1304.
37. Bernat G, Galindo MJ, Alcacer F, Guix J, Tasta T. Factors related to osteopenia in HIV-infected patients [abstr]. In: Program and abstracts of the 40th interscience conference on antimicrobial agents and chemotherapy. Washington, DC: American Society for Microbiology, 2000:1303.
38. Nolan D, Upton R, McKinnon E, et al. Stable or increasing bone mineral density in HIV-infected patients treated with nelfinavir or indinavir. AIDS 2001;15:1275-80.
39. Negredo E, Gel S, Arisa ER, et al. Bone mineral density in HIV-1-infected patients. Presented at the 8th conference on retroviruses and opportunistic infections, Chicago, February 4-8, 2001.
40. Knobel H, Guelar A, Vallecillo G, Nogues X, Diez A. Osteopenia in HIV-infected patients: is it the disease or is it the treatment? AIDS 2001;15:807-8.
41. Fairfield WP, Finkelstein JS, Klibanski A, Grinspoon SK. Osteopenia in eugonadal men with acquired immune deficiency syndrome wasting syndrome. J Clin Endocrinol Metab 2001;86:2020-6.
42. Negredo E, Arisa ER, Gel S, et al. A prospective comparative trial of BMD in HIV-infected patients [abstr]. In: Program and abstracts of the 41st interscience conference on antimicrobial agents and chemotherapy. Washington, DC: American Society for Microbiology, 2001:1-217.
43. Tsiodras S, Brodovicz K, Coplan P, et al. Osteoporosis in HIV-infected patients treated with HAART is independent of protease inhibitor use [abstr]. In: Program and abstracts of the 41st interscience conference on antimicrobial agents and chemotherapy. Washington, DC: American Society for Microbiology, 2001:1-1328.
44. Borderi M, Calza L, Tampellini L, et al. Reduced bone mineral density and lipoatrophy in HIV-infected patients receiving a protease inhibitor-based regimen. Presented at the 3rd European workshop on lipodystrophy and metabolic disorders, Marbella, Spain, April 25-27, 2002.
45. Amiel C, Ostertag A, Slama L, et al. BMD is reduced in HIV-infected men irrespective of treatment. J Bone Miner Res 2004;19:402-9.
46. Fernandez-Rivera J, Pineda JA, Garcia R, et al. High prevalence of osteopenia in HIV-infected patients under highly active antiretroviral therapy (HAART): preliminary results. Presented at the 3rd European workshop on lipodystrophy and metabolic disorders, Marbella, Spain, April 25-27, 2002.
47. Arnsten JH, Freeman R, Santoro N, Kunins H, Schoenbaum EE. Bone mineral density and protease inhibitor use in older HIV-infected women. Presented at the 9th conference on retroviruses and opportunistic infections, Seattle, February 24-28, 2002.
48. Arnsten JH, Freeman R, Santoro N, Schoenbaum EE. HIV infection and protease inhibitor use are not associated with reduced bone mineral density in older HIV-infected women. Presented at the 10th conference on retroviruses and opportunistic infections, Boston, February 10-14, 2003.
49. Jacobson D, Knox T, Shevitz A, Gorbach S. Low bone mineral density in HIV-infected women. Presented at the 10th conference on retroviruses and opportunistic infections, Boston, February 10-14, 2003.
50. Seminari E, Galli L, Rubinacci A, et al. Osteopenia/osteoporosis in highly-experienced HIV-infected patients [abstr]. Antivir Ther 2003;8:L95.
51. Madeddu GR, Spanu A, Solinas P, et al. Bone mass loss risk and vitamin D metabolism impairment in HIV patients treated with highly active antiretroviral therapy. Presented at the 9th European AIDS conference, Warsaw, Poland, October 25-29, 2003.
52. Mondy K, Yarasheski K, Powderly WG, et al. Longitudinal evolution of bone mineral density and bone markers in human immunodeficiency virus-infected individuals. Clin Infect Dis 2003;36:482-90.
53. Bruera D, Luna N, David DO, Bergoglio LM, Zamudio J. Decreased bone mineral density in HIV-infected patients is independent of antiretroviral therapy. AIDS 2003;17:1917-23.
54. Fakruddin JM, Laurence J. HIV envelope gp120-mediated regulation of osteoclastogenesis via RANKL secretion and its modulation by certain HIV protease inhibitors through interferon-γ/RANKL cross-talk. J Biol Chem 2003;278: 48251-8.
55. Jain RG, Lenhard JM. Select HIV protease inhibitors alter bone and fat metabolism ex vivo. J Biol Chem 2002;277:19247-50.
56. Wang MWH, Teitelbaum SL, Tebas P, Powderly WG, Ross FP. Indinavir administration leads to bone loss in mice. Presented at the 9th conference on retroviruses and opportunistic infections, Seattle, February 24-28, 2002.
57. Schwarzwald H, Ellis KJ, Evans DL, Kline NE, McMeans A, Kline MW. Effect of HAART on bone density in HIV-infected children. Presented at the 10th conference on retroviruses and opportunistic infections, Boston, February 10-14, 2003.
58. Gallant J, Staszewski S, Pozniak AL, et al. Long-term efficacy and safety of tenofovir disoproxil fumarate (TDF): a 144-week comparison versus stavudine (d4T) in antiretroviral-naive patients [abstr]. In: Programs and abstracts of the 15th international AIDS conference, Bangkok, Thailand, July 11-16, 2004.
59. Tsekes G, Chrysos G, Douskas G, et al. Body composition changes in protease inhibitor-naïve HIV-infected patients treated with two nucleoside reverse transcriptase inhibitors. HIV Med 2002;3:85-90.
60. Lawal A, Engelson ES, Wang J, Heymsfield SB, Kotler DP. Equivalent osteopenia in HIV-infected individuals studied before and during the era of highly active antiretroviral therapy. AIDS 2001;15:278-80.
61. Torralba M, Azriel SA, Rubio RR, et al. Bone mineral density (BMD) and body shape abnormalities (BSA) in HIV patients who have been on stable first line treatment for prolonged periods. Presented at the XIV international AIDS conference, Barcelona, Spain, July 7-12, 2002.
62. Ramos JT, Garcia L, Rojo P, et al. High prevalence of metabolic abnormalities in HIV-infected children treated with HAART. Presented at the 10th conference on retroviruses and opportunistic infections, Boston, February 10-14, 2003.
63. Milinkovic A, Martinez E, Vidal S, et al. Reduced bone mineral density is associated with lipoatrophy in HIV-infected patients receiving HAART. Presented at the 3rd European workshop on lipodystrophy and metabolic disorders, Marbella, Spain, April 25-27, 2002.
64. Hoy J, Hudson J, Law M, Cooper DA. Osteopenia in a randomized, multicenter study of protease inhibitor (PI) substitution in patients with the lipodystrophy syndrome and well-controlled HIV viremia. Presented at the 7th conference on retroviruses and opportunistic infections, San Francisco, January 30-February 2, 2000.
65. Schambelan M, Benson CA, Carr A, et al. Management of metabolic complications associated with antiretroviral therapy for HIV-1 infection: recommendations of an International AIDS Society-USA panel. J Acquir Immune Defic Syndr 2002;31:257-75.
66. Arpadi SM, Horlick M, Thornton J, Cuff PA, Wang J, Kotler DP. Bone mineral content is lower in prepubertal HIV-infected children. J Acquir Immune Defic Syndr 2002;29:450-4.
67. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis and Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA 2001;285:785-95.
68. Hully S, Furberg C, Barrett-Connor E, et al. Noncardiovascular disease outcomes during 6.8 years of hormone therapy: heart and estrogen/progestin replacement study follow-up (HERS II). JAMA 2002;288:58-66.
69. Rossouw JE, Anderson GL, Prentice RL, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the women's health initiative randomized controlled trial. JAMA 2002;228:321-33.
70. Hodsman AB, Hanley DA, Josse R. Do bisphosphonates reduce the risk of osteoporotic fractures? An evaluation of the evidence to date. Can Med AssocJ 2002;166:1426-30.
71. Orwoll E, Ettinger M, Weiss S, et al. Alendronate for the treatment of osteoporosis in men. N Engl J Med 2000;343:604-10.
72. Claxton S, Demarco D, Powderly WG, Yarasheski KE. Circulating leptin and lactate levels are not associated with osteopenia in HIV-infected men. Presented at the 8th conference on retroviruses and opportunistic infections, Chicago, February 4-8, 2001.
73. Mondy K, Powderly WG, Claxton SA, et al. Alendronate, vitamin D and calcium for the treatment of osteopenia/osteoporosis associated with HIV infection. Presented at the 10th conference on retroviruses and opportunistic infections, Boston, February 10-14, 2003.
74. Guaraldi G, Orlando G, Madeddu G, et al. Alendronate reduces bone turnover in HIV-associated osteopenia and Osteoporosis. Presented at the 11th conference on retroviruses and opportunistic infections, San Francisco, February 8-11, 2004.
75. Miller KD, Masur H, Jones EC, et al. High prevalence of osteonecrosis of the femoral head in HIV-infected adults. Ann Intern Med 2002;137:17-25.
76. Mont MA, Hungerford DS. Non-traumatic avascular necrosis of the femoral head. J Bone Joint Surg Am 1995;77:459-74.
77. Scribner AN, Troia-Cancio PV, Cox BA, et al. Osteonecrosis in HIV: a case-control study. J Acquir Immune Defic Syndr 2000;25:19-25.
78. Glesby MJ, Hoover DR, Vaamonde CM. Osteonecrosis in patients infected with human immunodeficiency virus: a case-control study. J Infect Dis 2001;184:519-23.
79. Gerster J, Camus J, Chave J, et al. Multiple site avascular necrosis in HIV-infected patients. J Rheumatol 1991;18:300-2.
80. Monier P, McKown K, Bronze M. Osteonecrosis complicating highly active antiretroviral therapy in patients infected with HIV. Clin Infect Dis 2000;31:1488-92.
81. Panel on Clinical Practices for Treatment of HIV Infection. Guidelines for the use of antiretroviral agents in HIV-1-infected adults and adolescents. Washington, DC: U.S. Department of Health and Human Services, 2004.
82. Forum for Collaborative HIV Research. Bone metabolism and HIV disease meeting report. Washington, DC: Center for Health Services Research and Policy at the George Washington University School of Public Health and Health Services, 2000.