Skip to main content

Advertisement

SpringerLink
Log in

Prevalence of causes of secondary osteoporosis and contribution to lower bone mineral density in HIV-infected patients

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

Eighty-one percent of human immunodeficiency virus (HIV)-infected patients had one or more of seven evaluated causes of secondary osteoporosis, and this rate increases with age. The type and number of causes were associated with a lower bone mineral density (BMD), and with an increased rate of osteopenia/osteoporosis, regardless of age and body mass index.

Introduction

The objective of this study was to determine whether factors of secondary osteoporosis were associated with lower BMD in HIV.

Methods

This was a cross-sectional study of 285 HIV-infected patients (25 % females) evaluating the impact of seven different factors of reduced BMD: hyperthyroidism, diabetes, chronic viral hepatitis, chronic kidney disease (CKD), hypovitaminosis D, secondary hyperparathyroidism, and hypogonadism. Dual-energy X-ray absorptiometry scan of the femoral neck was obtained at the clinical visit.

Results

Mean age was 45.7 years; osteopenia and osteoporosis were diagnosed in 38 and 6 %, respectively. Overall, 230 patients (81 %) had secondary factors; 107 (38 %) had only 1 cause, 94 (33 %) had 2, and 28 (10 %) had 3 or more, predominantly vitamin D deficiency in 61 %, hepatitis C virus coinfection in 45 %, and secondary hyperparathyroidism in 27 %. The number of secondary factors was closely related to a lower BMD, which is statistically significant for patients having ≥2 causes (0.77 vs 0.73 g/cm2, p = 0.02). The rate of osteopenia ranged from 36 % without any cause to 57 % with three or more, osteoporosis from 0 to 19 %, and Z-score <−2 SD from 0 to 27 %, respectively. In a multivariate linear regression, adjusting by age, body mass index, and HIV-related factors, the number of secondary factors was independently associated with a lower BMD (ß coefficient −0.134; p = 0.02), mainly due to patients with hepatitis C virus (HCV) coinfection, secondary hyperparathyroidism, and CKD.

Conclusions

A high prevalence of secondary causes of osteoporosis is observed in HIV-infected patients, and its type and cumulative number determine a lower BMD, after adjusting by age and body mass index.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Mocroft A, Brettle R, Kirk O, Blaxhult A, Parkin JM, Antunes F, Francioli P, D'Arminio Monforte A, Fox Z, Lundgren JD, EuroSIDA study group (2002) Changes in the cause of death among HIV positive subjects across Europe: results from the EuroSIDA study. AIDS 16:1663–1671

    Article  CAS  PubMed  Google Scholar 

  2. Tebas P, Powderly WG, Claxton S, Marin D, Tantisiriwat W, Teitelbaum SL, Yarasheski KE (2000) Accelerated bone mineral loss in HIV-infected patients receiving potent antiretroviral therapy. AIDS 14:F63–F67

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Arnsten JH, Freeman R, Howard AA, Floris-Moore M, Santoro N, Schoenbaum EE (2006) HIV infection and bone mineral density in middle aged women. Clin Infect Dis 42:1014–1020

    Article  CAS  PubMed  Google Scholar 

  4. Jones S, Restrepo D, Kasowitz A, Korenstein D, Wallenstein S, Schneider A, Keller MJ (2008) Risk factors for decreased bone density and effects of HIV on bone in the elderly. Osteoporos Int 19:913–918

    Article  CAS  PubMed  Google Scholar 

  5. Dolan SE, Huang JS, Killilea KM, Sullivan MP, Aliabadi N, Grinspoon S (2004) Reduced bone density in HIV-infected women. AIDS 18:475–483

    Article  PubMed  Google Scholar 

  6. Brown TT, Qaqish RB (2006) Antiretroviral therapy and the prevalence of osteopenia and osteoporosis: a meta-analytic review. AIDS 20:2165–2174

    Article  PubMed  Google Scholar 

  7. Triant VA, Brown TT, Lee H, Grinspoon SK (2008) Fracture prevalence among human immunodeficiency virus (HIV)-infected versus non-HIV-infected patients in a large U.S. healthcare system. J Clin Endocrinol Metab 93:3499–3504

    Article  CAS  PubMed  Google Scholar 

  8. Young B, Dao CN, Buchacz K, Baker R, Brooks JT (2011) Increased rates of bone fracture among HIV-infected persons in the HIV Outpatient Study (HOPS) compared with the US general population, 2000–2006. Clin Infect Dis 52:1061–1068

    Article  PubMed  Google Scholar 

  9. Brown TT, McComsey GA, King MS, Qaqish RB, Bernstein BM, da Silva BA (2009) Loss of bone mineral density after antiretroviral therapy initiation, independent of antiretroviral regimen. J Acquir Immune Defic Syndr 51:554–561

    Article  CAS  PubMed  Google Scholar 

  10. Duvivier C, Kolta S, Assoumou L, Ghosn J, Rozenberg S, Murphy RL, Katlama C, Costagliola D; ANRS 121 Hippocampe study group (2009) Greater decrease in bone mineral density with protease inhibitor regimens compared with nonnucleoside reverse transcriptase inhibitor regimens in HIV-1 infected naive patients. AIDS 23:817–824

    Google Scholar 

  11. Mondy K, Yarasheski K, Powderly WG, Whyte M, Claxton S, DeMarco D, Hoffmann M, Tebas P (2003) Longitudinal evolution of bone mineral density and bone markers in human immunodeficiency virus-infected individuals. Clin Infect Dis 36:482–490

    Article  PubMed  Google Scholar 

  12. Inaba M (2004) Secondary osteoporosis: thyrotoxicosis, rheumatoid arthritis, and diabetes mellitus. J Bone Miner Metab 22:287–292

    Article  PubMed  Google Scholar 

  13. Crum NF, Furtek KJ, Olson PE, Amling CL, Wallace MR (2005) A review of hypogonadism and erectile dysfunction among HIV-infected men during the pre- and post- HAART eras: diagnosis, pathogenesis, and management. AIDS Patient Care STDs 19:655–671

    Article  PubMed  Google Scholar 

  14. Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Work Group (2009) KDIGO clinical practice guideline for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int Suppl 113:S1–S130

    Google Scholar 

  15. Kanis JA (2002) Diagnosis of osteoporosis and assessment of fracture risk. Lancet 359:1929–1936

    Article  PubMed  Google Scholar 

  16. Lewiecki EM, Watts NB, McClung MR, Petak SM, Bachrach LK, Shepherd JA, Downs RW Jr; International Society for Clinical Densitometry (2004) Official positions of the International Society for Clinical Densitometry. J Clin Endocrinol Metab 89:3651–3655

    Article  Google Scholar 

  17. World Health Organization (2007) Assessment of osteoporosis at the primary health care level. WHO, Geneva. www.who.int/chp/topics/rheumatic/en/index.html. Accessed May 2013

  18. Kanis JA, McCloskey EV, Johansson H, Oden A, Melton LJ III, Khaltaev N (2008) A reference standard for the description of osteoporosis. Bone 42:467–475

    Article  CAS  PubMed  Google Scholar 

  19. Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J, Ensrud K, Genant HK, Palermo L, Scott J, Vogt TM (1993) Bone density at various sites for prediction of hip fractures. The Study of Osteoporotic Fractures Research Group. Lancet 341: 72–75

    Google Scholar 

  20. Edwards BJ, Langman CB, Bunta AD, Vicuna M, Favus M (2008) Secondary contributors to bone loss in osteoporosis related hip fractures. Osteoporos Int 19:991–999

    Article  CAS  PubMed  Google Scholar 

  21. Deutschmann HA, Weger M, Weger W, Kotanko P, Deutschmann MJ, Skrabal F (2002) Search for occult secondary osteoporosis: impact of identified possible risk factors on bone mineral density. J Intern Med 252:389–397

    Article  CAS  PubMed  Google Scholar 

  22. Johnson BE, Lucasey B, Robinson RG, Lukert BP (1989) Contributing diagnoses in osteoporosis. The value of a complete medical evaluation. Arch Intern Med 149:1069–1072

    Article  CAS  PubMed  Google Scholar 

  23. Tannenbaum C, Clark J, Schwartzman K, Wallenstein S, Lapinski R, Meier D, Luckey M (2002) Yield of laboratory testing to identify secondary contributors to osteoporosis in otherwise healthy women. J Clin Endocrinol Metab 87:4431–4437

    Article  CAS  PubMed  Google Scholar 

  24. Bours SPG, van Geel TA, Geusens P, Janssen MJ, Janzing HM, Hoffland GA, Willems PC, van den Bergh JP (2011) Contributors to secondary osteoporosis and metabolic bone diseases in patients presenting with a clinical fracture. J Clin Endocrinol Metab 96:1360–1367

    Article  CAS  PubMed  Google Scholar 

  25. Khosla S, Amin S, Orwoll E (2008) Osteoporosis in men. Endocr Rev 29:441–464

    Article  CAS  PubMed  Google Scholar 

  26. Bolland MJ, Grey AB, Gamble GD, Reid IR (2007) Clinical review: low body weight mediates the relationship between HIV infection and low bone mineral density: a meta-analysis. J Clin Endocrinol Metab 92:4522–4528

    Article  CAS  PubMed  Google Scholar 

  27. Chew NS, Doran PP, Powderly WG (2007) Osteopenia and osteoporosis in HIV: pathogenesis and treatment. Curr Opin HIV AIDS 2:318–323

    Article  PubMed  Google Scholar 

  28. Kanis JA, Johansson H, Oden A, Johnell O, De Laet C, Eisman JA, McCloskey EV, Mellstrom D, Melton LJ 3rd, Pols HA, Reeve J, Silman AJ, Tenenhouse A (2004) A family history of fracture and fracture risk: a meta-analysis. Bone 35:1029–1037

    Article  CAS  PubMed  Google Scholar 

  29. Ramayo E, Gonzalez-Moreno MP, Macias J, Cruz-Ruíz M, Mira JA, Villar-Rueda AM, García-García JA, Gómez-Mateos JM, Lozano F, Pineda JA (2005) Relationship between osteopenia, free testosterone, and vitamin D metabolite levels in HIV-infected patients with and without highly active antiretroviral therapy. AIDS Res Hum Retrovir 21:915–921

    Article  CAS  PubMed  Google Scholar 

  30. Liu H, Paige NM, Goldzweig CL, Wong E, Zhou A, Suttorp MJ, Munjas B, Orwoll E, Shekelle P (2008) Screening for osteoporosis in men: a systematic review for an American College of Physicians guideline. Ann Intern Med 148:685–701

    Article  PubMed  Google Scholar 

  31. Rouillard S, Lane NE (2001) Hepatic osteodystrophy. Hepatology 33:301–307

    Article  CAS  PubMed  Google Scholar 

  32. Lin JC, Hsieh TY, Wu CC, Chen PJ, Chueh TH, Chang WK, Chu HC (2012) Association between chronic hepatitis C virus infection and bone mineral density. Calcif Tissue Int 91:423–429

    Article  CAS  PubMed  Google Scholar 

  33. Lo Re V, Guaraldi G, Leonard MD, Localio AR, Lin J, Orlando G, Zirilli L, Rochira V, Kostman JR, Tebas P (2009) Viral hepatitis is associated with reduced bone mineral density in HIV-infected women but not men. AIDS 23:2191–2198

    Article  PubMed Central  PubMed  Google Scholar 

  34. McComsey GA, Kitch D, Daar ES, Tierney C, Jahed NC, Tebas P, Myers L, Melbourne K, Ha B, Sax PE (2011) Bone mineral density and fractures in antiretroviral-naive persons randomized to receive abacavir-lamivudine or tenofovir disoproxil fumarate-emtricitabine along with efavirenz or atazanavir-ritonavir: AIDS Clinical Trials Group A5224 s, a substudy of ACTG A5202. J Infect Dis 203:1791–1801

    Article  CAS  PubMed  Google Scholar 

  35. Liu AY, Vittinghoff E, Sellmeyer DE, Irvin R, Mulligan K, Mayer K, Thompson M, Grant R, Pathak S, O'Hara B, Gvetadze R, Chillag K, Grohskopf L, Buchbinder SP (2011) Bone mineral density in HIV-negative men participating in a tenofovir pre-exposure prophylaxis randomized clinical trial in San Francisco. PloS One 6:e23688. doi:10.1371/journal.pone.0023688

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Isidro ML, Ruano B (2010) Bone disease in diabetes. Curr Diabetes Rev 6:144–155

    Article  PubMed  Google Scholar 

  37. Ma L, Oei L, Jiang L, Estrada K, Chen H, Wang Z, Yu Q, Zillikens MC, Gao X, Rivadeneira F (2012) Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies. Eur J Epidemiol 27:319–332

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Sta RM, Li-Yu JT (2007) Investigation of the relationship between type 2 diabetes and osteoporosis using Bayesian inference. J Clin Densitom 10:386–390

    Article  Google Scholar 

  39. The Endocrine Society. Summary from the 2nd Annual Andropause Consensus Meeting (Chevy Chase, MD): The Endocrine Society Continuing Medical Education Services, 2001

  40. Teichmann J, Lange U, Discher T, Lohmeyer J, Stracke H, Bretzel RG (2009) Bone mineral density in human immunodeficiency virus-1 infected men with hypogonadism prior to highly active antiretrovial therapy. Eur J Med Res 14:59–64

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Grinspoon S (2005) Androgen deficiency and HIV infection. Clin Infect Dis 41:1804–1805

    Article  CAS  PubMed  Google Scholar 

  42. Nickolas TL, Leonard MB, Shane E (2008) Chronic kidney disease and bone fracture: a growing concern. Kidney Int 74:721–731

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Ana Abad for the important contribution in database management.

Conflicts of interest

None.

Author information

Authors and Affiliations

  1. Department of Infectious Diseases, Ramon y Cajal Hospital, Cra. de Colmenar, Km 9.1, 28034, Madrid, Spain

    J. L. Casado, S. Bañon, R. Andrés, M. J. Perez-Elías, A. Moreno & S. Moreno

Authors
  1. J. L. Casado
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Bañon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Andrés
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. J. Perez-Elías
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. L. Casado.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Casado, J.L., Bañon, S., Andrés, R. et al. Prevalence of causes of secondary osteoporosis and contribution to lower bone mineral density in HIV-infected patients. Osteoporos Int 25, 1071–1079 (2014). https://doi.org/10.1007/s00198-013-2506-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-013-2506-3

Keywords

Search

Navigation