Prevention of Bone Loss and Management of Fracture Risk in HIV-Infected Individuals: Case Studies and Recommendations for Different Patient Subgroups

• Puhan MA , Van Natta ML, Palella FJ, Addessi A, Meinert C: Excess mortality in patients with AIDS in the era of highly active antiretroviral therapy: temporal changes and risk factors. Clin. Infect. Dis.51(8) , 947–956 (2010).
   PubMed Web of Science ®Google Scholar
• Palella FJ Jr, Baker RK, Moorman AC et al.: Mortality in the highly active antiretroviral therapy era: changing causes of death and disease in the HIV outpatient study. J. Acquir. Immune Defic. Syndr.43(1) , 27–34 (2006).
   PubMed Web of Science ®Google Scholar
• Braitstein P , BrinkhofMW, DabisF et al.: Mortality of HIV-1-infected patients in the first year of antiretroviral therapy: comparison between low-income and high-income countries.Lancet367(9513) , 817–824 (2006).
   PubMed Web of Science ®Google Scholar
• Smit C , GeskusR, WalkerS et al.: Effective therapy has altered the spectrum of cause-specific mortality following HIV seroconversion.AIDS20(5) , 741–749 (2006).
   PubMed Web of Science ®Google Scholar
• Mocroft A , MadgeS, JohnsonAM et al.: A comparison of exposure groups in the EuroSIDA study: starting highly active antiretroviral therapy (HAART), response to HAART, and survival.J. Acquir. Immune Defic. Syndr.22(4) , 369–378 (1999).
   PubMed Web of Science ®Google Scholar
• Stone B , DockrellD, BowmanC, McCloskeyE: HIV and bone disease.Arch. Biochem. Biophys.503(1) , 66–77 (2010).
   PubMed Web of Science ®Google Scholar
• Mallon PW : HIV and bone mineral density.Curr. Opin. Infect. Dis.23(1) , 1–8 (2010).
   PubMed Web of Science ®Google Scholar
• Fausto A , BongiovanniM, CicconiP et al.: Potential predictive factors of osteoporosis in HIV-positive subjects.Bone38(6) , 893–897 (2006).
   PubMed Web of Science ®Google Scholar
• Dolan SE , KanterJR, GrinspoonS: Longitudinal analysis of bone density in human immunodeficiency virus-infected women.J. Clin. Endocrinol. Metab.91(8) , 2938–2945 (2006).
   PubMed Web of Science ®Google Scholar
• Mondy K , YarasheskiK, PowderlyWG et al.: Longitudinal evolution of bone mineral density and bone markers in human immunodeficiency virus-infected individuals.Clin. Infect. Dis.36(4) , 482–490 (2003).
   PubMed Web of Science ®Google Scholar
• Knobel H , GuelarA, VallecilloG, NoguesX, DiezA: Osteopenia in HIV-infected patients: is it the disease or is it the treatment?AIDS15(6) , 807–808 (2001).
   PubMed Web of Science ®Google Scholar
• Moore AL , VashishtA, SabinCA et al.: Reduced bone mineral density in HIV-positive individuals.AIDS15(13) , 1731–1733 (2001).
   PubMed Web of Science ®Google Scholar
• Teichmann J , StephanE, LangeU et al.: Osteopenia in HIV-infected women prior to highly active antiretroviral therapy.J. Infect.46(4) , 221–227 (2003).
   PubMed Web of Science ®Google Scholar
• Yin MT , ShiQ, HooverDR et al.: Fracture incidence in HIV-infected women: results from the Women‘s Interagency HIV Study.AIDS24(17) , 2679–2686 (2010).
   PubMed Web of Science ®Google Scholar
• Cazanave C , DuponM, Lavignolle-AurillacV et al.: Reduced bone mineral density in HIV-infected patients: prevalence and associated factors.AIDS22(3) , 395–402 (2008).
   PubMed Web of Science ®Google Scholar
• Vikulina T , FanX, YamaguchiM et al.: Alterations in the immuno-skeletal interface drive bone destruction in HIV-1 transgenic rats.Proc. Natl Acad. Sci. USA107(31) , 13848–13853 (2010).
   PubMed Web of Science ®Google Scholar
• Brown TT , McComseyGA, KingMS, QaqishRB, BernsteinBM, da Silva BA: Loss of bone mineral density after antiretroviral therapy initiation, independent of antiretroviral regimen. J. Acquir. Immune Defic. Syndr.51(5) , 554–561 (2009).
   PubMed Web of Science ®Google Scholar
• Grund B , PengG, GibertCL et al.: Continuous antiretroviral therapy decreases bone mineral density.AIDS23(12) , 1519–1529 (2009).
   PubMed Web of Science ®Google Scholar
• Stellbrink HJ , OrkinC, ArribasJR et al.: Comparison of changes in bone density and turnover with abacavir–lamivudine versus tenofovir-emtricitabine in HIV-infected adults: 48-week results from the ASSERT study.Clin. Infect. Dis.51(8) , 963–972 (2010).
   PubMed Web of Science ®Google Scholar
• Brown TT , QaqishRB: Antiretroviral therapy and the prevalence of osteopenia and osteoporosis: a meta-analytic review.AIDS20(17) , 2165–2174 (2006).
   PubMed Web of Science ®Google Scholar
• Carr A , MillerJ, EismanJA, CooperDA: Osteopenia in HIV-infected men: association with asymptomatic lactic acidemia and lower weight pre-antiretroviral therapy.AIDS15(6) , 703–709 (2001).
   PubMed Web of Science ®Google Scholar
• Yin MT , LuD, CremersS et al.: Short-term bone loss in HIV-infected premenopausal women.J. Acquir. Immune Defic. Syndr.53(2) , 202–208 (2010).
   PubMed Web of Science ®Google Scholar
• Loiseau-Peres S , DelaunayC, PouponS et al.: Osteopenia in patients infected by the human immunodeficiency virus. A case control study.Joint Bone Spine69(5) , 482–485 (2002).
   PubMed Web of Science ®Google Scholar
• Arnsten JH , FreemanR, HowardAA, Floris-MooreM, LoY, KleinRS: Decreased bone mineral density and increased fracture risk in aging men with or at risk for HIV infection.AIDS21(5) , 617–623 (2007).
   PubMed Web of Science ®Google Scholar
• Young B , DaoC, BuchaczK, BakerR, Brooks J; HIV Outpatient Study Investigators: Increased rates of bone fracture among HIV-infected persons in the HIV Outpatient Study compared with the US general population, 2000 to 2006. Clin. Infect. Dis.52(8) , 1061–1068 (2011).
   PubMed Web of Science ®Google Scholar
• Prior J , BurdgeD, MaanE et al.: Fragility fractures and bone mineral density in HIV positive women: a case-control population-based study.Osteoporos. Int.18(10) , 1345–1353 (2007).
   PubMed Web of Science ®Google Scholar
• Triant VA , BrownTT, LeeH, GrinspoonSK: Fracture prevalence among human immunodeficiency virus (HIV)-infected versus non-HIV-infected patients in a large U.S. healthcare system.J. Clin. Endocrinol. Metab.93(9) , 3499–3504 (2008).
   PubMed Web of Science ®Google Scholar
• Womak J , GouletJ, GilbertC et al.: Increased risk of fragility fractures among HIV infected compared to uninfected male veterans.PLoS One6 , E17217 (2011).
   PubMed Web of Science ®Google Scholar
• Cassetti I , MadrugaJV, SuleimanJM et al.: The safety and efficacy of tenofovir DF in combination with lamivudine and efavirenz through 6 years in antiretroviral-naive HIV-1-infected patients.HIV Clin. Trials8(3) , 164–172 (2007).
   PubMed Web of Science ®Google Scholar
• Rivas P , GorgolasM, Garcia-DelgadoR, Diaz-CurielM, GoyenecheaA, Fernandez-GuerreroML: Evolution of bone mineral density in AIDS patients on treatment with zidovudine/lamivudine plus abacavir or lopinavir/ritonavir.HIV Med.9(2) , 89–95 (2008).
   PubMed Web of Science ®Google Scholar
• Tebas P , UmblejaT, DubeMP, ParkerRA, MulliganK, RoubenoffR: Initiation of ART is associated with bone loss independent of the three specific ART regimens: results of ACTG A5005s. Presented at: 14th Conference of Retroviruses and Opportunistic Infections. Los Angeles, CA, USA, 25–28 February 2007.
   Google Scholar
• McComsey GA , KitchD, DaarES et al.: Bone and limb fat outcomes of ACTG A5224s, a substudy of ACTG A5202: a prospective, randomized, partially blinded Phase III trial of ABC/3TC or TDF/FTC with EFV or ATV/r for initial treatment of HIV-1 infection. Presented at: 17th Conference of Retroviruses and Opportunistic Infections. San Francisco, CA, USA, 16–19 February 2010.
   Google Scholar
• Bonjoch A , FiguerasM, EstanyC et al.: High prevalence of and progression to low bone mineral density in HIV-infected patients: a longitudinal cohort study.AIDS24(18) , 2827–2833 (2010).
   PubMed Web of Science ®Google Scholar
• Duvivier C , KoltaS, AssoumouL et al.: Greater decrease in bone mineral density with protease inhibitor regimens compared with nonnucleoside reverse transcriptase inhibitor regimens in HIV-1 infected naive patients.AIDS23(7) , 817–824 (2009).
   PubMed Web of Science ®Google Scholar
• Fernandez-Rivera J , GarciaR, LozanoF et al.: Relationship between low bone mineral density and highly active antiretroviral therapy including protease inhibitors in HIV-infected patients.HIV Clin. Trials.4(5) , 337–346 (2003).
   PubMed Web of Science ®Google Scholar
• Malizia AP , CotterE, ChewN, PowderlyWG, DoranPP: HIV protease inhibitors selectively induce gene expression alterations associated with reduced calcium deposition in primary human osteoblasts.AIDS Res. Hum. Retroviruses23(2) , 243–250 (2007).
   PubMed Web of Science ®Google Scholar
• Tebas P , PowderlyWG, ClaxtonS et al.: Accelerated bone mineral loss in HIV-infected patients receiving potent antiretroviral therapy.AIDS14(4) , F63–F67 (2000).
   PubMed Web of Science ®Google Scholar
• Amiel C , OstertagA, SlamaL et al.: BMD is reduced in HIV-infected men irrespective of treatment.J. Bone Miner. Res.19(3) , 402–409 (2004).
   PubMed Web of Science ®Google Scholar
• Hansen A , ObelN, NielsenH, PedersenC, GerstoftJ: Bone mineral density changes in protease inhibitor-sparing vs. nucleoside reverse transcriptase inhibitor-sparing highly active antiretroviral therapy: data from a randomized trial.HIV Med.12(3) , 157–165 (2010).
   PubMed Web of Science ®Google Scholar
• Parsonage MJ , WilkinsEG, SnowdenN, IssaBG, SavageMW: The development of hypophosphataemic osteomalacia with myopathy in two patients with HIV infection receiving tenofovir therapy.HIV Med.6(5) , 341–346 (2005).
   PubMed Web of Science ®Google Scholar
• Woodward CL , HallAM, WilliamsIG et al.: Tenofovir-associated renal and bone toxicity.HIV Med.10(8) , 482–487 (2009).
   PubMed Web of Science ®Google Scholar
• Rozenberg S , AssoumouL, BentataM et al.: Change in bone mineral density in HIV-1-infcted men with -2.5 >=T-score < -1 over 2 years.Antivir. Ther.15(Suppl. 4) , A12 (2010).
   Google Scholar
• Jacobson DL , SpiegelmanD, KnoxTK, WilsonIB: Evolution and predictors of change in total bone mineral density over time in HIV-infected men and women in the nutrition for healthy living study.J. Acquir. Immune Defic. Syndr.49(3) , 298–308 (2008).
   PubMed Web of Science ®Google Scholar
• Martin A , BlochM, AminJ et al.: Simplification of antiretroviral therapy with tenofovir-emtricitabine or abacavir–lamivudine: a randomized, 96-week trial.Clin. Infect. Dis.49(10) , 1591–1601 (2009).
   PubMed Web of Science ®Google Scholar
• Buchacz K , YoungB, BakerRK et al.: Renal function in patients receiving tenofovir with ritonavir/lopinavir or ritonavir/atazanavir in the HIV Outpatient Study (HOPS) cohort.J. Acquir. Immune Defic. Syndr.43(5) , 626–628 (2006).
   PubMed Web of Science ®Google Scholar
• Cooper RD , WiebeN, SmithN, KeiserP, NaickerS, TonelliM: Systematic review and meta-analysis: renal safety of tenofovir disoproxil fumarate in HIV-infected patients.Clin. Infect. Dis.51(5) , 496–505 (2010).
   PubMed Web of Science ®Google Scholar
• Gallant JE , StaszewskiS, PozniakAL et al.: Efficacy and safety of tenofovir DF vs stavudine in combination therapy in antiretroviral-naive patients: a 3-year randomized trial.JAMA292(2) , 191–201 (2004).
   PubMed Web of Science ®Google Scholar
• Schooley RT , RuaneP, MyersRA et al.: Tenofovir DF in antiretroviral-experienced patients: results from a 48-week, randomized, double-blind study.AIDS16(9) , 1257–1263 (2002).
   PubMed Web of Science ®Google Scholar
• Squires K , PozniakAL, PieroneG Jr et al.: Tenofovir disoproxil fumarate in nucleoside-resistant HIV-1 infection: a randomized trial. Ann. Intern. Med.139(5 Pt 1) , 313–320 (2003).
   PubMed Web of Science ®Google Scholar
• Wasserman P , RubinDS: Highly prevalent vitamin D deficiency and insufficiency in an urban cohort of HIV-infected men under care.AIDS Patient Care STDS24(4) , 223–227 (2010).
   PubMed Web of Science ®Google Scholar
• Mueller NJ , FuxCA, LedergerberB et al.: High prevalence of severe vitamin D deficiency in combined antiretroviral therapy-naive and successfully treated Swiss HIV patients.AIDS24(8) , 1127–1134 (2010).
   PubMed Web of Science ®Google Scholar
• Mehta S , GiovannucciE, MugusiFM et al.: Vitamin D status of HIV-infected women and its association with HIV disease progression, anemia, and mortality.PLoS One5(1) , E8770 (2010).
   PubMed Web of Science ®Google Scholar
• Welz T , ChildsK, IbrahimF et al.: Efavirenz is associated with severe vitamin D deficiency and increased alkaline phosphatase.AIDS24(12) , 1923–1928 (2010).
   PubMed Web of Science ®Google Scholar
• Arnsten JH , FreemanR, HowardAA, Floris-MooreM, SantoroN, SchoenbaumEE: HIV infection and bone mineral density in middle-aged women.Clin. Infect. Dis.42(7) , 1014–1020 (2006).
   PubMed Web of Science ®Google Scholar
• Teichmann J , LangeU, DischerT, LohmeyerJ, StrackeH, BretzelRG: Bone mineral density in human immunodeficiency virus-1 infected men with hypogonadism prior to highly-active-antiretroviral-therapy (HAART).Eur. J. Med. Res.14(2) , 59–64 (2009).
   PubMed Web of Science ®Google Scholar
• Cranney A , WeilerHA, O‘DonnellS, PuilL: Summary of evidence-based review on vitamin D efficacy and safety in relation to bone health.Am. J. Clin. Nutr.88(2) , 513S–519S (2008).
   PubMed Web of Science ®Google Scholar
• Chung M , BalkEM, BrendelM et al.: Vitamin D and Calcium: A Systematic Review of Health Outcomes. Agency for Healthcare Research and Quality, MD, USA (2009).
   Google Scholar
• Mallon PW , MillerJ, CooperDA, CarrA: Prospective evaluation of the effects of antiretroviral therapy on body composition in HIV-1-infected men starting therapy.AIDS17(7) , 971–979 (2003).
   PubMed Web of Science ®Google Scholar
• Viljakainen HT , SaarnioE, HytinanttiT et al.: Maternal vitamin D status determines bone variables in the newborn.J. Clin. Endocrinol. Metab.95(4) , 1749–1757 (2010).
   PubMed Web of Science ®Google Scholar
• National Collaborating Centre for Women‘s and Children‘s Health: Antenatal Care: Routine Care for the Healthy Pregnant Woman. Royal College of Obstetricians and Gynaecologists Press, UK (2008).
   Google Scholar
• Institute of Medicine of the National Academies: Dietary Reference Intakes for Calcium and Vitamin D. Ross CA, Taylor CL, Yaktine AL, Del Velle HB (Eds). The National Academies Press, Washington, DC, USA (2011).
   Google Scholar
• Ross AC , MansonJE, AbramsSA et al.: The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know.J. Clin. Endocrinol. Metab.96(1) , 53–58 (2011).
   PubMed Web of Science ®Google Scholar
• Gazzard BG , AndersonJ, BabikerA et al.: British HIV Association guidelines for the treatment of HIV-1-infected adults with antiretroviral therapy 2008.HIV Med.9(8) , 563–608 (2008).
   PubMed Web of Science ®Google Scholar
• Siberry G , WilliamsP, MendezH et al.: Safety of tenofovir use during pregnancy: associations with low birth weight and early growth in HIV-exposed uninfected infants. Presented at: XVIII International AIDS Conference. Vienna, Austria, 18–23 July 2010.
   Google Scholar
• Rosenvinge MM , GedelaK, CopasAJ et al.: Tenofovir-linked hyperparathyroidism is independently associated with the presence of vitamin D deficiency.Acquir. Immune Defic. Syndr.54(5) , 496–499 (2010).
   PubMed Web of Science ®Google Scholar
• Childs KE , FishmanSL, ConstableC et al.: Short communication: inadequate vitamin D exacerbates parathyroid hormone elevations in tenofovir users.AIDS Res. Hum. Retroviruses26(8) , 855–859 (2010).
   PubMed Web of Science ®Google Scholar
• WHO Scientific Group on the Prevention and Management of Osteoporosis: Prevention and Management of Osteoporosis: Report of a WHO Scientific Group. WHO Press, Switzerland (2003).
   Google Scholar
• Adams JS , HewisonM: Update in vitamin D.J. Clin. Endocrinol. Metab.95(2) , 471–478 (2010).
   PubMed Web of Science ®Google Scholar
• Dawson-Hughes B , MithalA, BonjourJP et al.: IOF position statement: vitamin D recommendations for older adults.Osteoporos. Int.21(7) , 1151–1154 (2010).
   PubMed Web of Science ®Google Scholar
• Hanley DA , CranneyA, JonesG, WhitingSJ, LeslieWD: Vitamin D in adult health and disease: a review and guideline statement from Osteoporosis Canada (summary).CMAJ182(12) , 1315–1319 (2010).
   PubMed Web of Science ®Google Scholar
• Hewison M : Antibacterial effects of vitamin D.Nat. Rev. Endocrinol. DOI: 10.1038/nrendo.2010.226 (2011) (Epub ahead of print).
   PubMed Web of Science ®Google Scholar
• Chapuy MC , PreziosiP, MaamerM et al.: Prevalence of vitamin D insufficiency in an adult normal population.Osteoporos. Int.7(5) , 439–443 (1997).
   PubMed Web of Science ®Google Scholar
• Heaney RP , DowellMS, HaleCA, BendichA: Calcium absorption varies within the reference range for serum 25-hydroxyvitamin D.J. Am. Coll. Nutr.22(2) , 142–146 (2003).
   PubMed Web of Science ®Google Scholar
• Heaney RP , DaviesKM, ChenTC, HolickMF, Barger-LuxMJ: Human serum 25-hydroxycholecalciferol response to extended oral dosing with colecalciferol.Am. J. Clin. Nutr.77(1) , 204–210 (2003).
   PubMed Web of Science ®Google Scholar
• Hathcock JN , ShaoA, ViethR, HeaneyR: Risk assessment for vitamin D.Am. J. Clin. Nutr.85(1) , 6–18 (2007).
   PubMed Web of Science ®Google Scholar
• McComsey GA , KendallMA, TebasP et al.: Alendronate with calcium and vitamin D supplementation is safe and effective for the treatment of decreased bone mineral density in HIV.AIDS21(18) , 2473–2482 (2007).
   PubMed Web of Science ®Google Scholar
• Pazianas M , AbrahamsenB: Safety of bisphosphonates.Bone24(3) , 245–248 (2011).
   Google Scholar
• Nolan D , UptonR, McKinnonE et al.: Stable or increasing bone mineral density in HIV-infected patients treated with nelfinavir or indinavir.AIDS15(10) , 1275–1280 (2001).
   PubMed Web of Science ®Google Scholar
• Paul TV , AshaHS, ThomasN et al.: Hypovitaminosis D and bone mineral density in human immunodeficiency virus-infected men from India, with or without antiretroviral therapy.Endocr. Pract.16(4) , 547–553 (2010).
   PubMed Web of Science ®Google Scholar
• Bruera D , LunaN, DavidDO, BergoglioLM, ZamudioJ: Decreased bone mineral density in HIV-infected patients is independent of antiretroviral therapy.AIDS17(13) , 1917–1923 (2003).
   PubMed Web of Science ®Google Scholar
• Anastos K , LuD, ShiO et al.: The association of bone mineral density with HIV infection and antiretroviral treatment in women.Antivir. Ther.12(7) , 1049–1058 (2007).
   PubMed Web of Science ®Google Scholar
• Calmy A , FuxCA, NorrisR et al.: Low bone mineral density, renal dysfunction, and fracture risk in HIV infection: a cross-sectional study. 200(11) , 1746–1754 (2009).
   Google Scholar
• Collin F , DuvalX, LemoingV et al.: Ten-year incidence and risk factors of bone fractures in a cohort of treated HIV1-infected adults.AIDS23(8) , 1021–1024 (2009).
   PubMed Web of Science ®Google Scholar

Websites

• WHO Fracture Risk Assessment tool (FRAX®) www.sheffield.ac.uk/FRAX
   Google Scholar
• European AIDS Clinical Society: Prevention and management of non-infectious comorbidities in HIV. Version 5.2 (2010) www.europeanaidsclinicalsociety.org/guidelinespdf/2_Non_Infectious_Co_Morbidities_in_HIV.pdf
   Google Scholar
• The Scottish Government: Improving maternal and infant nutrition: a framework for action. Scottish Government, UK (2011) www.scotland.gov.uk/Publications/2011/01/13095228/0
   Google Scholar