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Published in:

01-05-2022 | Human Immunodeficiency Virus | Review

Osteoporosis and HIV Infection

Author: Emmanuel Biver

Published in: Calcified Tissue International | Issue 5/2022

Abstract

Life expectancy of people living with HIV (PLWH) is now close to that of the HIV-uninfected population. As a result, age-related comorbidities, including osteoporosis, are increasing in PLWH. This narrative review describes the epidemiology of bone fragility in PLWH, changes of bone features over the course of HIV infection and their determinants, as well as the available evidence regarding the management of osteoporosis in PLWH. The risk of fracture is higher and increases about 10 years earlier compared to the general population. The classical risk factors of bone fragility are very widespread and are major determinants of bone health in this population. The majority of bone loss occurs during virus replication and during immune reconstitution at antiretroviral therapies (ART) initiation, which both increase osteoclast activity. Abnormalities in bone formation and mineralization have also been shown in histomorphometric studies in untreated PLWH. Measurement of bone mineral density (BMD) is the first line tool for assessing fracture risk in postmenopausal women, men above 50 years, and other HIV-infected patients with clinical risk factors for osteoporosis. FRAX underestimates fracture probability in PLWH. In case of indication for anti-osteoporotic drug, bisphosphonates remain the reference option. Calcium and vitamin D supplementation should be considered as ART initiation, since it may attenuate bone loss at this stage. Bone-protective ART regimens improve BMD compared to other regimens, but to a lesser extent than bisphosphonate, and without available data on their influence on the incidence of fracture.

Scherrer AU, Traytel A, Braun DL, Calmy A, Battegay M, Cavassini M et al (2021) Cohort profile update: the Swiss HIV Cohort Study (SHCS). Int J Epidemiol. https://doi.org/10.1093/ije/dyab141CrossRef

Alvarez E, Belloso WH, Boyd MA, Inkaya A, Hsieh E, Kambugu A et al (2016) Which HIV patients should be screened for osteoporosis: an international perspective. Curr Opin HIV AIDS 11(3):268–276. https://doi.org/10.1097/coh.0000000000000269CrossRefPubMed

Kim JH, Noh J, Kim W, Seong H, Kim JH, Lee WJ et al (2021) Trends of age-related non-communicable diseases in people living with HIV and comparison with uninfected controls: a nationwide population-based study in South Korea. HIV Med 22(9):824–833. https://doi.org/10.1111/hiv.13139CrossRefPubMed

Marcus JL, Leyden WA, Alexeeff SE, Anderson AN, Hechter RC, Hu H et al (2020) Comparison of overall and comorbidity-free life expectancy between insured adults with and without HIV infection, 2000–2016. JAMA Netw Open 3(6):e207954. https://doi.org/10.1001/jamanetworkopen.2020.7954CrossRefPubMedPubMedCentral

Shiau S, Broun EC, Arpadi SM, Yin MT (2013) Incident fractures in HIV-infected individuals: a systematic review and meta-analysis. AIDS 27(12):1949–1957. https://doi.org/10.1097/QAD.0b013e328361d241CrossRefPubMed

Dong HV, Cortés YI, Shiau S, Yin MT (2014) Osteoporosis and fractures in HIV/hepatitis C virus coinfection: a systematic review and meta-analysis. AIDS 28(14):2119–2131. https://doi.org/10.1097/qad.0000000000000363CrossRefPubMed

O’Neill TJ, Rivera L, Struchkov V, Zaheen A, Thein HH (2014) The effect of HIV-hepatitis C co-infection on bone mineral density and fracture: a meta-analysis. PLoS ONE 9(7):e101493. https://doi.org/10.1371/journal.pone.0101493CrossRefPubMedPubMedCentral

Ilha T, Comim FV, Copes RM, Compston JE, Premaor MO (2018) HIV and vertebral fractures: a systematic review and metanalysis. Sci Rep 8(1):7838. https://doi.org/10.1038/s41598-018-26312-9CrossRefPubMedPubMedCentral

Pramukti I, Lindayani L, Chen YC, Yeh CY, Tai TW, Fetzer S et al (2020) Bone fracture among people living with HIV: a systematic review and meta-regression of prevalence, incidence, and risk factors. PLoS ONE 15(6):e0233501. https://doi.org/10.1371/journal.pone.0233501CrossRefPubMedPubMedCentral

10.

Starup-Linde J, Rosendahl SB, Storgaard M, Langdahl B (2020) Management of osteoporosis in patients living with HIV-A systematic review and meta-analysis. J Acquir Immune Defic Syndr 83(1):1–8. https://doi.org/10.1097/qai.0000000000002207CrossRefPubMed

11.

Chang CJ, Chan YL, Pramukti I, Ko NY, Tai TW (2021) People with HIV infection had lower bone mineral density and increased fracture risk: a meta-analysis. Arch Osteoporos 16(1):47. https://doi.org/10.1007/s11657-021-00903-yCrossRefPubMed

12.

Sharma A, Shi Q, Hoover DR, Anastos K, Tien PC, Young MA et al (2015) Increased fracture incidence in middle-aged HIV-infected and HIV-uninfected women: updated results from the women’s interagency HIV study. J Acquir Immune Defic Syndr 70(1):54–61. https://doi.org/10.1097/qai.0000000000000674CrossRefPubMedPubMedCentral

13.

Gonciulea A, Wang R, Althoff KN, Palella FJ, Lake J, Kingsley LA et al (2017) An increased rate of fracture occurs a decade earlier in HIV+ compared with HIV- men. AIDS 31(10):1435–1443. https://doi.org/10.1097/QAD.0000000000001493CrossRefPubMed

14.

Jespersen NA, Axelsen F, Dollerup J, Nørgaard M, Larsen CS (2021) The burden of non-communicable diseases and mortality in people living with HIV (PLHIV) in the pre-, early- and late-HAART era. HIV Med 22(6):478–490. https://doi.org/10.1111/hiv.13077CrossRefPubMedPubMedCentral

15.

Zhang T, Wilson IB, Zullo AR, Meyers DJ, Lee Y, Daiello LA et al (2021) Hip fracture rates in nursing home residents with and without HIV. J Am Med Dir Assoc. https://doi.org/10.1016/j.jamda.2021.08.040CrossRefPubMedPubMedCentral

16.

Byrne DD, Newcomb CW, Carbonari DM, Nezamzadeh MS, Leidl KB, Herlim M et al (2015) Increased risk of hip fracture associated with dually treated HIV/hepatitis B virus coinfection. J Viral Hepat 22(11):936–947. https://doi.org/10.1111/jvh.12398CrossRefPubMedPubMedCentral

17.

Battalora L, Armon C, Palella F, Li J, Overton ET, Hammer J et al (2021) Incident bone fracture and mortality in a large HIV cohort outpatient study, 2000–2017, USA. Arch Osteoporos 16(1):117. https://doi.org/10.1007/s11657-021-00949-yCrossRefPubMed

18.

Goh SSL, Lai PSM, Tan ATB, Ponnampalavanar S (2018) Reduced bone mineral density in human immunodeficiency virus-infected individuals: a meta-analysis of its prevalence and risk factors. Osteoporos Int 29(3):595–613. https://doi.org/10.1007/s00198-017-4305-8CrossRefPubMed

19.

Gregson CL, Madanhire T, Rehman A, Ferrand RA, Cappola AR, Tollman S et al (2021) Osteoporosis, rather than sarcopenia, is the predominant musculoskeletal disease in a rural South African community where HIV prevalence is high: a cross-sectional study. J Bone Miner Res. https://doi.org/10.1002/jbmr.4464CrossRefPubMed

20.

Rukuni R, Rehman AM, Mukwasi-Kahari C, Madanhire T, Kowo-Nyakoko F, McHugh G et al (2021) Effect of HIV infection on growth and bone density in peripubertal children in the era of antiretroviral therapy: a cross-sectional study in Zimbabwe. Lancet Child Adolesc Health 5(8):569–581. https://doi.org/10.1016/s2352-4642(21)00133-4CrossRefPubMedPubMedCentral

21.

Bolland MJ, Grey A, Reid IR (2015) Skeletal health in adults with HIV infection. Lancet Diabetes Endocrinol 3(1):63–74. https://doi.org/10.1016/S2213-8587(13)70181-5CrossRefPubMed

22.

Hoy JF, Grund B, Roediger M, Schwartz AV, Shepherd J, Avihingsanon A et al (2017) Immediate initiation of antiretroviral therapy for HIV infection accelerates bone loss relative to deferring therapy: findings from the START bone mineral density substudy, a randomized trial. J Bone Miner Res 32(9):1945–1955. https://doi.org/10.1002/jbmr.3183CrossRefPubMed

23.

Guo F, Song X, Li Y, Guan W, Pan W, Yu W et al (2021) Longitudinal change in bone mineral density among Chinese individuals with HIV after initiation of antiretroviral therapy. Osteoporos Int 32(2):321–332. https://doi.org/10.1007/s00198-020-05584-wCrossRefPubMed

24.

Han WM, Wattanachanya L, Apornpong T, Jantrapakde J, Avihingsanon A, Kerr SJ et al (2020) Bone mineral density changes among people living with HIV who have started with TDF-containing regimen: a five-year prospective study. PLoS ONE 15(3):e0230368. https://doi.org/10.1371/journal.pone.0230368CrossRefPubMedPubMedCentral

25.

Biver E, Calmy A, Delhumeau C, Durosier C, Zawadynski S, Rizzoli R (2014) Microstructural alterations of trabecular and cortical bone in long-term HIV-infected elderly men on successful antiretroviral therapy. AIDS 28(16):2417–2427CrossRefPubMed

26.

Warming L et al (2002) Changes in bone mineral density with age in men and women: a longitudinal study. Osteoporos Int 13(2):105–112CrossRefPubMed

27.

Khosla S et al (2005) Pathophysiology of age-related bone loss and osteoporosis. Endocrinol Metab Clin North Am 34(4):1015–1030CrossRefPubMed

28.

Finkelstein JS et al (2008) Bone mineral density changes during the menopause transition in a multiethnic cohort of women. J Clin Endocrinol Metab 93:861–868CrossRefPubMed

29.

Gnant M et al (2015) Adjuvant denosumab in breast cancer (ABCSG-18): a multicentre, randomised, double-blind, placebo-controlled trial. Lancet 386:433–443CrossRefPubMed

30.

Gnant M et al (2008) Adjuvant endocrine therapy plus zoledronic acid in premenopausal women with early-stage breast cancer: 5-year follow-up of the ABCSG-12 bone-mineral density substudy. Lancet Oncol 9:840–849CrossRefPubMed

31.

Messina OD et al (2021) Management of glucocorticoid-induced osteoporosis. Aging Clin Exp Res 33(4):793–804CrossRefPubMed

32.

Baranek B et al (2020) The effect of tenofovir disoproxil fumarate on bone mineral density: a systematic review and meta-analysis. Antivir Ther 25(1):21–32CrossRefPubMed

33.

Yin MT, Lund E, Shah J, Zhang CA, Foca M, Neu N et al (2014) Lower peak bone mass and abnormal trabecular and cortical microarchitecture in young men infected with HIV early in life. AIDS 28(3):345–353. https://doi.org/10.1097/qad.0000000000000070CrossRefPubMed

34.

Calmy A, Chevalley T, Delhumeau C, Toutous-Trellu L, Spycher-Elbes R, Ratib O et al (2013) Long-term HIV infection and antiretroviral therapy are associated with bone microstructure alterations in premenopausal women. Osteoporos Int 24(6):1843–1852. https://doi.org/10.1007/s00198-012-2189-1CrossRefPubMed

35.

Sellier P, Ostertag A, Collet C, Trout H, Champion K, Fernandez S et al (2016) Disrupted trabecular bone micro-architecture in middle-aged male HIV-infected treated patients. HIV Med 17(7):550–556. https://doi.org/10.1111/hiv.12380CrossRefPubMed

36.

Macdonald HM, Maan EJ, Berger C, Dunn RA, Côté HCF, Murray MCM et al (2020) Deficits in bone strength, density and microarchitecture in women living with HIV: a cross-sectional HR-pQCT study. Bone 138:115509. https://doi.org/10.1016/j.bone.2020.115509CrossRefPubMed

37.

Yin MT, Shu A, Zhang CA, Boutroy S, McMahon DJ, Ferris DC et al (2013) Trabecular and cortical microarchitecture in postmenopausal HIV-infected women. Calcif Tissue Int 92(6):557–565. https://doi.org/10.1007/s00223-013-9716-8CrossRefPubMedPubMedCentral

38.

Serrano S, Mariñoso ML, Soriano JC, Rubiés-Prat J, Aubia J, Coll J et al (1995) Bone remodelling in human immunodeficiency virus-1-infected patients. A histomorphometric study. Bone 16(2):185–191. https://doi.org/10.1016/8756-3282(94)00028-xCrossRefPubMed

39.

Ramalho J, Martins CSW, Galvão J, Furukawa LN, Domingues WV, Oliveira IB et al (2019) Treatment of human immunodeficiency virus infection with tenofovir disoproxil fumarate-containing antiretrovirals maintains low bone formation rate, but increases osteoid volume on bone histomorphometry. J Bone Miner Res 34(9):1574–1584. https://doi.org/10.1002/jbmr.3751CrossRefPubMed

40.

Biver E, Calmy A, Rizzoli R (2017) Bone health in HIV and hepatitis B or C infections. Ther Adv Musculoskelet Dis 9(1):22–34. https://doi.org/10.1177/1759720X16671927CrossRefPubMed

41.

Maffezzoni F, Porcelli T, Delbarba A, Pezzaioli LC, Properzi M, Cappelli C et al (2020) Hypogonadism and bone health in men with HIV. Lancet HIV 7(11):e782–e790. https://doi.org/10.1016/s2352-3018(20)30236-8CrossRefPubMed

42.

Sharma A, Hoover DR, Shi Q, Tien PC, Weber KM, Shah JG et al (2021) HIV and menopause are independently associated with lower bone mineral density: results from the women’s interagency HIV study. Clin Infect Dis. https://doi.org/10.1093/cid/ciab874CrossRefPubMedPubMedCentral

43.

Foreman SC, Wu PH, Kuang R, John MD, Tien PC, Link TM et al (2020) Factors associated with bone microstructural alterations assessed by HR-pQCT in long-term HIV-infected individuals. Bone 133:115210. https://doi.org/10.1016/j.bone.2019.115210CrossRefPubMed

44.

Womack JA, Murphy TE, Ramsey C, Bathulapalli H, Leo-Summers L, Smith AC et al (2021) Brief report: are serious falls associated with subsequent fragility fractures among veterans living with HIV? J Acquir Immune Defic Syndr 88(2):192–196. https://doi.org/10.1097/qai.0000000000002752CrossRefPubMed

45.

Mascarau R, Bertrand F, Labrousse A, Gennero I, Poincloux R, Maridonneau-Parini I et al (2020) HIV-1-infected human macrophages, by secreting RANK-L, contribute to enhanced osteoclast recruitment. Int J Mol Sci. https://doi.org/10.3390/ijms21093154CrossRefPubMedPubMedCentral

46.

Delpino MV, Quarleri J (2020) Influence of HIV infection and antiretroviral therapy on bone homeostasis. Front Endocrinol (Lausanne) 11:502. https://doi.org/10.3389/fendo.2020.00502CrossRef

47.

Raynaud-Messina B, Bracq L, Dupont M, Souriant S, Usmani SM, Proag A et al (2018) Bone degradation machinery of osteoclasts: an HIV-1 target that contributes to bone loss. Proc Natl Acad Sci U S A 115(11):E2556–E2565. https://doi.org/10.1073/pnas.1713370115CrossRefPubMedPubMedCentral

48.

Ofotokun I, Titanji K, Vikulina T, Roser-Page S, Yamaguchi M, Zayzafoon M et al (2015) Role of T-cell reconstitution in HIV-1 antiretroviral therapy-induced bone loss. Nat Commun 6:8282. https://doi.org/10.1038/ncomms9282CrossRefPubMed

49.

Ofotokun I, Titanji K, Vunnava A, Roser-Page S, Vikulina T, Villinger F et al (2016) Antiretroviral therapy induces a rapid increase in bone resorption that is positively associated with the magnitude of immune reconstitution in HIV infection. AIDS 30(3):405–414. https://doi.org/10.1097/qad.0000000000000918CrossRefPubMed

50.

Ogbuagu O, Ruane PJ, Podzamczer D, Salazar LC, Henry K, Asmuth DM et al (2021) Long-term safety and efficacy of emtricitabine and tenofovir alafenamide vs emtricitabine and tenofovir disoproxil fumarate for HIV-1 pre-exposure prophylaxis: week 96 results from a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet HIV 8(7):e397–e407. https://doi.org/10.1016/s2352-3018(21)00071-0CrossRefPubMed

51.

Mayer KH, Molina JM, Thompson MA, Anderson PL, Mounzer KC, De Wet JJ et al (2020) Emtricitabine and tenofovir alafenamide vs emtricitabine and tenofovir disoproxil fumarate for HIV pre-exposure prophylaxis (DISCOVER): primary results from a randomised, double-blind, multicentre, active-controlled, phase 3, non-inferiority trial. Lancet 396(10246):239–254. https://doi.org/10.1016/s0140-6736(20)31065-5CrossRefPubMed

52.

McComsey GA, Lupo S, Parks D, Poggio MC, De Wet J, Kahl LP et al (2018) Switch from tenofovir disoproxil fumarate combination to dolutegravir with rilpivirine improves parameters of bone health. AIDS 32(4):477–485. https://doi.org/10.1097/qad.0000000000001725CrossRefPubMed

53.

Maggiolo F, Rizzardini G, Raffi F, Pulido F, Mateo-Garcia MG, Molina JM et al (2019) Bone mineral density in virologically suppressed people aged 60 years or older with HIV-1 switching from a regimen containing tenofovir disoproxil fumarate to an elvitegravir, cobicistat, emtricitabine, and tenofovir alafenamide single-tablet regimen: a multicentre, open-label, phase 3b, randomised trial. Lancet HIV 6(10):e655–e666. https://doi.org/10.1016/s2352-3018(19)30195-xCrossRefPubMed

54.

Nishijima T, Mutoh Y, Kawasaki Y, Tomonari K, Kikuchi Y, Gatanaga H et al (2018) Cumulative exposure of TDF is associated with kidney tubulopathy whether it is currently used or discontinued. AIDS 32(2):179–188. https://doi.org/10.1097/qad.0000000000001667CrossRefPubMed

55.

Gupta SK, Post FA, Arribas JR, Eron JJ Jr, Wohl DA, Clarke AE et al (2019) Renal safety of tenofovir alafenamide vs. tenofovir disoproxil fumarate: a pooled analysis of 26 clinical trials. AIDS 33(9):1455–1465. https://doi.org/10.1097/qad.0000000000002223CrossRefPubMed

56.

Shukla S, Kumari S, Bal SK, Monaco DC, Ribeiro SP, Sekaly RP et al (2021) “Go”, “No Go,” or “Where to Go”; does microbiota dictate T cell exhaustion, programming, and HIV persistence? Curr Opin HIV AIDS 16(4):215–222. https://doi.org/10.1097/coh.0000000000000692CrossRefPubMed

57.

Imahashi M, Ode H, Kobayashi A, Nemoto M, Matsuda M, Hashiba C et al (2021) Impact of long-term antiretroviral therapy on gut and oral microbiotas in HIV-1-infected patients. Sci Rep 11(1):960. https://doi.org/10.1038/s41598-020-80247-8CrossRefPubMedPubMedCentral

58.

Dubé MP, Park SY, Ross H, Love TMT, Morris SR, Lee HY (2018) Daily HIV pre-exposure prophylaxis (PrEP) with tenofovir disoproxil fumarate-emtricitabine reduced Streptococcus and increased Erysipelotrichaceae in rectal microbiota. Sci Rep 8(1):15212. https://doi.org/10.1038/s41598-018-33524-6CrossRefPubMedPubMedCentral

59.

Fulcher JA, Li F, Cook RR, Zabih S, Louie A, Okochi H et al (2019) Rectal microbiome alterations associated with oral human immunodeficiency virus pre-exposure prophylaxis. Open Forum Infect Dis 6(11):ofz463. https://doi.org/10.1093/ofid/ofz463CrossRefPubMedPubMedCentral

60.

Perler BK, Reinhart EM, Montgomery M, Maynard M, Shapiro JM, Belenky P et al (2021) Evaluation of the microbiome in men taking pre-exposure prophylaxis for HIV prevention. AIDS Behav 25(7):2005–2013. https://doi.org/10.1007/s10461-020-03130-7CrossRefPubMed

61.

Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A, Anderson EE et al (2018) Extensive impact of non-antibiotic drugs on human gut bacteria. Nature 555(7698):623–628. https://doi.org/10.1038/nature25979CrossRefPubMedPubMedCentral

62.

Biver E, Calmy A, Aubry-Rozier B, Birkhauser M, Bischoff-Ferrari HA, Ferrari S et al (2019) Diagnosis, prevention, and treatment of bone fragility in people living with HIV: a position statement from the Swiss Association against Osteoporosis. Osteoporos Int 30(5):1125–1135. https://doi.org/10.1007/s00198-018-4794-0CrossRefPubMed

63.

Brown TT, Hoy J, Borderi M, Guaraldi G, Renjifo B, Vescini F et al (2015) Recommendations for evaluation and management of bone disease in HIV. Clin Infect Dis 60(8):1242–1251. https://doi.org/10.1093/cid/civ010CrossRefPubMedPubMedCentral

64.

Yin MT, Shiau S, Rimland D, Gibert CL, Bedimo RJ, Rodriguez-Barradas MC et al (2016) Fracture prediction with modified-FRAX in older HIV-infected and uninfected men. J Acquir Immune Defic Syndr 72(5):513–520. https://doi.org/10.1097/QAI.0000000000000998CrossRefPubMedPubMedCentral

65.

Yang J, Sharma A, Shi Q, Anastos K, Cohen MH, Golub ET et al (2018) Improved fracture prediction using different fracture risk assessment tool adjustments in HIV-infected women. AIDS 32(12):1699–1706. https://doi.org/10.1097/qad.0000000000001864CrossRefPubMed

66.

Mansueto P, Seidita A, Vitale G, Gangemi S, Iaria C, Cascio A (2015) Vitamin D deficiency in HIV infection: not only a bone disorder. Biomed Res Int 2015:735615. https://doi.org/10.1155/2015/735615CrossRefPubMedPubMedCentral

67.

EACS (2021) European AIDS Clinical Society guidelines. Version 11.0 October 2021. http://www.eacsociety.org/guidelines/eacs-guidelines/eacs-guidelines.html.

68.

Alvarez N, Aguilar-Jimenez W, Rugeles MT (2019) The potential protective role of vitamin D supplementation on HIV-1 infection. Front Immunol 10:2291. https://doi.org/10.3389/fimmu.2019.02291CrossRefPubMedPubMedCentral

69.

Rizzoli R, Boonen S, Brandi ML, Bruyère O, Cooper C, Kanis JA et al (2013) Vitamin D supplementation in elderly or postmenopausal women: a 2013 update of the 2008 recommendations from the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO). Curr Med Res Opin 29(4):305–313. https://doi.org/10.1185/03007995.2013.766162CrossRefPubMed

70.

Havens PL, Stephensen CB, Hazra R, Flynn PM, Wilson CM, Rutledge B et al (2012) Vitamin D3 decreases parathyroid hormone in HIV-infected youth being treated with tenofovir: a randomized, placebo-controlled trial. Clin Infect Dis 54(7):1013–1025. https://doi.org/10.1093/cid/cir968CrossRefPubMedPubMedCentral

71.

Giacomet V, Vigano A, Manfredini V, Cerini C, Bedogni G, Mora S et al (2013) Cholecalciferol supplementation in HIV-infected youth with vitamin D insufficiency: effects on vitamin D status and T-cell phenotype: a randomized controlled trial. HIV Clin Trials 14(2):51–60. https://doi.org/10.1310/hct1402-51CrossRefPubMed

72.

Havens PL, Stephensen CB, Van Loan MD, Schuster GU, Woodhouse LR, Flynn PM et al (2018) Vitamin D3 supplementation increases spine bone mineral density in adolescents and young adults with human immunodeficiency virus infection being treated with tenofovir disoproxil fumarate: a randomized, placebo-controlled trial. Clin Infect Dis 66(2):220–228. https://doi.org/10.1093/cid/cix753CrossRefPubMed

73.

Sudjaritruk T, Bunupuradah T, Aurpibul L, Kanjanavanit S, Chotecharoentanan T, Sricharoen N et al (2021) Impact of vitamin D and calcium supplementation on bone mineral density and bone metabolism among thai adolescents with perinatally acquired human immunodeficiency virus (HIV) infection: a randomized clinical trial. Clin Infect Dis 73(9):1555–1564. https://doi.org/10.1093/cid/ciab547CrossRefPubMed

74.

Overton ET, Chan ES, Brown TT, Tebas P, McComsey GA, Melbourne KM et al (2015) Vitamin D and calcium attenuate bone loss with antiretroviral therapy initiation: a randomized trial. Ann Intern Med 162(12):815–824. https://doi.org/10.7326/M14-1409CrossRefPubMedPubMedCentral

75.

Havers FP, Detrick B, Cardoso SW, Berendes S, Lama JR, Sugandhavesa P et al (2014) Change in vitamin d levels occurs early after antiretroviral therapy initiation and depends on treatment regimen in resource-limited settings. PLoS ONE 9(4):e95164. https://doi.org/10.1371/journal.pone.0095164CrossRefPubMedPubMedCentral

76.

Wohl DA, Orkin C, Doroana M, Pilotto JH, Sungkanuparph S, Yeni P et al (2014) Change in vitamin D levels and risk of severe vitamin D deficiency over 48 weeks among HIV-1-infected, treatment-naive adults receiving rilpivirine or efavirenz in a Phase III trial (ECHO). Antivir Ther 19(2):191–200. https://doi.org/10.3851/IMP2721CrossRefPubMed

77.

Arpadi SM, McMahon DJ, Abrams EJ, Bamji M, Purswani M, Engelson ES et al (2012) Effect of supplementation with cholecalciferol and calcium on 2-y bone mass accrual in HIV-infected children and adolescents: a randomized clinical trial. Am J Clin Nutr 95(3):678–685. https://doi.org/10.3945/ajcn.111.024786CrossRefPubMedPubMedCentral

78.

Rovner AJ, Stallings VA, Rutstein R, Schall JI, Leonard MB, Zemel BS (2017) Effect of high-dose cholecalciferol (vitamin D(3)) on bone and body composition in children and young adults with HIV infection: a randomized, double-blind, placebo-controlled trial. Osteoporos Int 28(1):201–209. https://doi.org/10.1007/s00198-016-3826-xCrossRefPubMed

79.

Eckard AR, Oriordan MA, Rosebush JC, Ruff JH, Chahroudi A, Labbato D et al (2017) Effects of vitamin D supplementation on bone mineral density and bone markers in HIV-infected youth. J Acquir Immune Defic Syndr 76(5):539–546. https://doi.org/10.1097/qai.0000000000001545CrossRefPubMedPubMedCentral

80.

Bang UC, Kolte L, Hitz M, Schierbeck LL, Nielsen SD, Benfield T et al (2013) The effect of cholecalciferol and calcitriol on biochemical bone markers in HIV type 1-infected males: results of a clinical trial. AIDS Res Hum Retroviruses 29(4):658–664. https://doi.org/10.1089/aid.2012.0263CrossRefPubMed

81.

Yin MT, RoyChoudhury A, Bucovsky M, Colon I, Ferris DC, Olender S et al (2019) A randomized placebo-controlled trial of low- versus moderate-dose vitamin D3 supplementation on bone mineral density in postmenopausal women with HIV. J Acquir Immune Defic Syndr 80(3):342–349. https://doi.org/10.1097/qai.0000000000001929CrossRefPubMedPubMedCentral

82.

Bolland MJ, Grey A, Horne AM, Briggs SE, Thomas MG, Ellis-Pegler RB et al (2012) Effects of intravenous zoledronate on bone turnover and bone density persist for at least five years in HIV-infected men. J Clin Endocrinol Metab 97(6):1922–1928. https://doi.org/10.1210/jc.2012-1424CrossRefPubMed

83.

Negredo E, Bonjoch A, Pérez-Álvarez N, Ornelas A, Puig J, Herrero C et al (2015) Comparison of two different strategies of treatment with zoledronate in HIV-infected patients with low bone mineral density: single dose versus two doses in 2 years. HIV Med 16(7):441–448. https://doi.org/10.1111/hiv.12260CrossRefPubMed

84.

Ofotokun I, Titanji K, Lahiri CD, Vunnava A, Foster A, Sanford SE et al (2016) A single-dose zoledronic acid infusion prevents antiretroviral therapy-induced bone loss in treatment-naive hiv-infected patients: a phase IIb trial. Clin Infect Dis 63(5):663–671. https://doi.org/10.1093/cid/ciw331CrossRefPubMedPubMedCentral

85.

McGinty T, Alvarez-Barco E, Tinago W, Macken A, O'Broin C, Cotter AG, et al (2021) Short-course alendronate for the prevention of ART-associated bone loss. In: [CROI Abstract 96]. Abstracts from the virtual CROI 2021 conference on retroviruses and opportunistic infections. vCROI 2021 Abstract eBook. 2021;483.

86.

Makras P, Petrikkos P, Anastasilakis AD, Kolynou A, Katsarou A, Tsachouridou O et al (2021) Denosumab versus zoledronate for the treatment of low bone mineral density in male HIV-infected patients. Bone Rep 15:101128. https://doi.org/10.1016/j.bonr.2021.101128CrossRefPubMedPubMedCentral

87.

Guaraldi G, Orlando G, Madeddu G, Vescini F, Ventura P, Campostrini S et al (2004) Alendronate reduces bone resorption in HIV-associated osteopenia/osteoporosis. HIV Clin Trials 5(5):269–277. https://doi.org/10.1310/md8v-5dlg-en3t-brhxCrossRefPubMed

88.

Negredo E, Martínez-López E, Paredes R, Rosales J, Pérez-Alvarez N, Holgado S et al (2005) Reversal of HIV-1-associated osteoporosis with once-weekly alendronate. AIDS 19(3):343–345PubMed

89.

Mondy K, Powderly WG, Claxton SA, Yarasheski KH, Royal M, Stoneman JS et al (2005) Alendronate, vitamin D, and calcium for the treatment of osteopenia/osteoporosis associated with HIV infection. J Acquir Immune Defic Syndr 38(4):426–431. https://doi.org/10.1097/01.qai.0000145352.04440.1eCrossRefPubMed

90.

McComsey GA, Kendall MA, Tebas P, Swindells S, Hogg E, Alston-Smith B et al (2007) Alendronate with calcium and vitamin D supplementation is safe and effective for the treatment of decreased bone mineral density in HIV. AIDS 21(18):2473–2482. https://doi.org/10.1097/QAD.0b013e3282ef961dCrossRefPubMed

91.

Rozenberg S, Lanoy E, Bentata M, Viard JP, Valantin MA, Missy P et al (2012) Effect of alendronate on HIV-associated osteoporosis: a randomized, double-blind, placebo-controlled, 96-week trial (ANRS 120). AIDS Res Hum Retroviruses 28(9):972–980. https://doi.org/10.1089/aid.2011.0224CrossRefPubMed

92.

Jacobson DL, Lindsey JC, Gordon C, Hazra R, Spiegel H, Ferreira F et al (2020) Alendronate improves bone mineral density in children and adolescents perinatally infected with human immunodeficiency virus with low bone mineral density for age. Clin Infect Dis 71(5):1281–1288. https://doi.org/10.1093/cid/ciz957CrossRefPubMed

93.

Lindsey JC, Jacobson DL, Spiegel HM, Gordon CM, Hazra R, Siberry GK (2021) Safety and efficacy of 48 and 96 weeks of alendronate in children and adolescents with perinatal human immunodeficiency virus infection and low bone mineral density for age. Clin Infect Dis 72(6):1059–1063. https://doi.org/10.1093/cid/ciaa861CrossRefPubMed

94.

Bolland MJ, Grey AB, Horne AM, Briggs SE, Thomas MG, Ellis-Pegler RB et al (2007) Annual zoledronate increases bone density in highly active antiretroviral therapy-treated human immunodeficiency virus-infected men: a randomized controlled trial. J Clin Endocrinol Metab 92(4):1283–1288. https://doi.org/10.1210/jc.2006-2216CrossRefPubMed

95.

Bolland MJ, Grey AB, Horne AM, Briggs SE, Thomas MG, Ellis-Pegler RB et al (2008) Effects of intravenous zoledronate on bone turnover and BMD persist for at least 24 months. J Bone Miner Res 23(8):1304–1308. https://doi.org/10.1359/jbmr.080312CrossRefPubMed

96.

Huang J, Meixner L, Fernandez S, McCutchan JA (2009) A double-blinded, randomized controlled trial of zoledronate therapy for HIV-associated osteopenia and osteoporosis. AIDS 23(1):51–57. https://doi.org/10.1097/QAD.0b013e32831c8adcCrossRefPubMed

97.

Hoy JF, Richardson R, Ebeling PR, Rojas J, Pocock N, Kerr SJ et al (2018) Zoledronic acid is superior to tenofovir disoproxil fumarate-switching for low bone mineral density in adults with HIV. AIDS 32(14):1967–1975. https://doi.org/10.1097/qad.0000000000001911CrossRefPubMed

98.

Carr A, Kerr SJ, Richardson R, Ebeling P, Pocock N, Rojas J et al (2019) Prolonged effect of zoledronic acid on bone mineral density and turnover in HIV-infected adults on tenofovir: a randomized. Open-Label Study J Bone Miner Res 34(12):2192–2197. https://doi.org/10.1002/jbmr.3834CrossRefPubMed

99.

Lei JJH, Pereira B, Moyle G, Boffito M, Milinkovic A (2021) The benefits of tenofovir discontinuation with or without bisphosphonate therapy in osteoporotic people living with HIV. HIV Med 22(9):816–823. https://doi.org/10.1111/hiv.13137CrossRefPubMed

100.

Venter WDF, Sokhela S, Simmons B, Moorhouse M, Fairlie L, Mashabane N et al (2020) Dolutegravir with emtricitabine and tenofovir alafenamide or tenofovir disoproxil fumarate versus efavirenz, emtricitabine, and tenofovir disoproxil fumarate for initial treatment of HIV-1 infection (ADVANCE): week 96 results from a randomised, phase 3, non-inferiority trial. Lancet HIV 7(10):e666–e676. https://doi.org/10.1016/s2352-3018(20)30241-1CrossRefPubMed

101.

Surial B, Mugglin C, Calmy A, Cavassini M, Günthard HF, Stöckle M et al (2021) Weight and metabolic changes after switching from tenofovir disoproxil fumarate to tenofovir alafenamide in people living with HIV: a cohort study. Ann Intern Med 174(6):758–767. https://doi.org/10.7326/m20-4853CrossRefPubMed

Title: Osteoporosis and HIV Infection
Author: Emmanuel Biver
Publication date: 01-05-2022
Publisher: Springer US
Keywords: Human Immunodeficiency Virus
Osteoporosis
Osteoporosis
Published in: Calcified Tissue International / Issue 5/2022
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI: https://doi.org/10.1007/s00223-022-00946-4

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