Prospective evaluation of bone markers, parathormone and 1,25-(OH) 2 vitamin D in HIV-positive patients after the initiation of tenofovir/emtricitabine with atazanavir/ritonavir or efavirenz

BMC Infectious Diseases

Volumn 12, Issue , 2012, Pages

  Focà, Emanuele ^a   Motta, Davide ^a   Borderi, Marco ^b   Gotti, Daria ^a   Albini, Laura ^a   Calabresi, Alessandra ^a   Izzo, Ilaria ^a   Bellagamba, Rita ^c   Narciso, Pasquale ^c   Sighinolfi, Laura ^d   Clò, Alberto ^b   Gibellini, Davide ^b   Quiros Roldan, Eugenia ^a   Brianese, Nigritella ^a   Cesana, Bruno M ^a   Re, Maria C ^b   Torti, Carlo ^a,e  

^a UNIVERSITY OF BRESCIA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^d S ANNA HOSPITAL   (Italy)

^e UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Antiretroviral therapy; Bone turnover; HIV; Osteoporosis; Vitamin D

Indexed keywords

ATAZANAVIR PLUS RITONAVIR; CALCITRIOL; CARBOXY TERMINAL TELOPEPTIDE; CYSTATIN C; EFAVIRENZ; EMTRICITABINE PLUS TENOFOVIR DISOPROXIL; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PARATHYROID HORMONE; VIRUS RNA; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; BIOLOGICAL MARKER; ERGOCALCIFEROL;

ADULT; ARTICLE; BONE TURNOVER; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; GLOMERULUS FILTRATION RATE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; KIDNEY FUNCTION; MAJOR CLINICAL STUDY; MALE; OSTEOLYSIS; PROSPECTIVE STUDY; RISK ASSESSMENT; SEASONAL VARIATION; SIDE EFFECT; SUMMER; TREND STUDY; VIRUS LOAD; BLOOD; BONE; CLINICAL TRIAL; COMPARATIVE STUDY; CONTROLLED CLINICAL TRIAL; DRUG EFFECT; METHODOLOGY; MIDDLE AGED; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL;

ADULT; ANTI-HIV AGENTS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; BIOLOGICAL MARKERS; BONE AND BONES; ERGOCALCIFEROLS; FEMALE; HIV INFECTIONS; HUMANS; MALE; MIDDLE AGED; PARATHYROID HORMONE; PROSPECTIVE STUDIES;

EID: 84857013805     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/1471-2334-12-38     Document Type: Article

References (42)

1. Brown TT, Qaqish RB. Antiretroviral therapy and the prevalence of osteopenia and osteoporosis: a meta-analytic review. AIDS 2006, 20:2165-2174. 10.1097/QAD.0b013e32801022eb, 17086056.
2. Young J, Bucher HC, Guenthard HF, Rickenbach M, Fux CA, Hirschel B, Cavassini M, Vernazza P, Bernasconi E, Battegay M. Virological and immunological responses to efavirenz or boosted lopinavir as first-line therapy for patients with HIV. Antivir Ther 2009, 14:771-779. 10.3851/IMP1291, 19812439.
3. Womack JA, Goulet JL, Gibert C, Brandt C, Chang CC, Gulanski B, Fraenkel L, Mattocks K, Rimland D, Rodriguez-Barradas MC, Tate J, Yin MT, Justice AC. Increased risk of fragility fractures among HIV infected compared to uninfected male veterans. PLoS One 2011, 6:e17217. 10.1371/journal.pone.0017217, 3040233, 21359191.
4. Borderi M, Gibellini D, Vescini F, De Crignis E, Cimatti L, Biagetti C, Tampellini L, Re MC. Metabolic bone disease in HIV infection. AIDS 2009, 23:1297-1310. 10.1097/QAD.0b013e32832ce85a, 19550284.
5. Watts NB, Bilezikian JP, Camacho PM, Greenspan SL, Harris ST, Hodgson SF, Kleerekoper M, Luckey MM, McClung MR, Pollack RP, Petak SM. American Association of Clinical Endocrinologists Medical Guidelines for Clinical Practice for the diagnosis and treatment of postmenopausal osteoporosis. Endocr Pract 2010, 16(Suppl 3):1-37.
6. Vega D, Maalouf NM, Sakhaee K. CLINICAL Review: the role of receptor activator of nuclear factor-kappaB (RANK)/RANK ligand/osteoprotegerin: clinical implications. J Clin Endocrinol Metab 2007, 92:4514-4521. 10.1210/jc.2007-0646, 17895323.
7. Rivas P, Górgolas M, García-Delgado R, Díaz-Curiel M, Goyenechea A, Fernández-Guerrero ML. Evolution of bone mineral density in AIDS patients on treatment with zidovudine/lamivudine plus abacavir or lopinavir/ritonavir. HIV Med 2008, 9:89-95. 10.1111/j.1468-1293.2007.00525.x, 18093130.
8. van Vonderen MGA, Lips P, van Agtmael MA, Hassink EAM, Brinkman K, Geerlings SE, Sutinen J, Ristola M, Danner SA, Reiss P. First line zidovudine/lamivudine/lopinavir/ritonavir leads to greater bone loss compared to nevirapine/lopinavir/ritonavir. AIDS 2009, 23:1367-1376. 10.1097/QAD.0b013e32832c4947, 19424051.
9. Moyle G, Newey C, Baldwin C, Torti C, Mandalia S, Gazzard B. Osteopenia: a consequence of HIV not HAART?. Antivir Ther 2000, 5:43.
10. Fernández-Rivera J, García R, Lozano F, Macías J, García-García JA, Mira JA, Corzo JE, Gómez-Mateos J, Rueda A, Sánchez-Burson J, Pineda JA. Relationship between low bone mineral density and highly active antiretroviral therapy including protease inhibitors in HIV-infected patients. HIV Clin Trials 2003, 4:337-46. 10.1310/4X0H-UVMJ-BHYW-CPFB, 14583850.
11. Aukrust P, Haug CJ, Ueland T, Lien E, Müller F, Espevik T, Bollerslev J, Frøland SS. 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, 84:145-150. 10.1210/jc.84.1.145, 9920075.
12. Hernández Quero J, Ortego Centeno N, Muñoz-Torres M, Martinez Pérez MA, Higuera Torres-Puchol JM. Alterations in bone turnover in HIV-positive patients. Infection 1993, 21:220-222. 10.1007/BF01728893, 7901171.
13. Serrano S, Mariñoso ML, Soriano JC, Rubiés-Prat J, Aubia J, Coll J, Bosch J, Del Rio L, Vila J, Goday A. Bone remodelling in human immunodeficiency virus-1-infected patients. A histomorphometric study. Bone 1995, 16:185-191. 10.1016/8756-3282(94)00028-X, 7756046.
14. Brown TT, Ross AC, Storer N, Labbato D, McComsey G. Bone turnover, osteoprotegerin/RANKL and inflammation with antiretroviral initiation: tenofovir versus non-tenofovir regimens. Antivir Ther 2011, 16:1063-1072. 10.3851/IMP1874, 22024522.
15. Stellbrink H-J, Orkin C, Arribas JR, Compston J, Gerstoft J, Van Wijngaerden E, Lazzarin A, Rizzardini G, Sprenger HG, Lambert J, Sture G, Leather D, Hughes S, Zucchi P, Pearce H. 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 2010, 51:963-972. 10.1086/656417, 20828304.
16. Piso RJ, Rothen M, Rothen JP, Stahl M. Markers of bone turnover are elevated in patients with antiretroviral treatment independent of the substance used. J Acquir Immune Defic Syndr 2011, 56:320-4. 10.1097/QAI.0b013e31820cf010, 21350365.
17. Panel on Antiretroviral Guidelines for Adults and Adolescents Guidelines for the use of antiretroviral agents in HIV-1-infected adults and adolescents. 2011, 1-167. Department ofHealth and Human Services, Available at [http://www.aidsinfo.nih.gov/ContentFiles/AdultandAdolescentGL.pdf]. Accessed December 15th, 2011, Panel on Antiretroviral Guidelines for Adults and Adolescents.
18. Antinori A, Marcotullio S, Ammassari A, Andreoni M, Angarano G, Carosi G, Cinque P, d' Arminio Monforte A, Di Perri G, Ensoli B, Ferrazzi E, Galli M, Mastroianni C, Matteelli A, Mazzotta F, Moroni M, Palù G, Puoti M, Puro V, Rizzardini G, Sagnelli E, Suter F, Vella S, Lazzarin A. Italian guidelines for the use of antiretroviral agents and the diagnostic-clinical management of HIV-1 infected persons. New Microbiol 2011, 34:109-46.
19. Albini L, Cesana BM, Motta D, Focà E, Gotti D, Calabresi A, Izzo I, Bellagamba R, Fezza R, Narciso P, Sighinolfi L, Maggi P, Quiros-Roldan E, Manili L, Guaraldi G, Lapadula G, Torti C. A randomized, pilot trial to evaluate glomerular filtration rate by creatinine or cystatin C in naïve HIV-infected patients after tenofovir/emtricitabine in combination with atazanavir/ritonavir or efavirenz. J Acquir Immune Defic Syndr 2012, 59:18-30. 10.1097/QAI.0b013e31823a6124, 21992924.
20. Stevens LA, Schmid CH, Greene T, Zhang YL, Beck GJ, Froissart M, Hamm LL, Lewis JB, Mauer M, Navis GJ, Steffes MW, Eggers PW, Coresh J, Levey AS. Comparative performance of the CKD Epidemiology Collaboration (CKD-EPI) and the Modification of Diet in Renal Disease (MDRD) Study equations for estimating GFR levels above 60 mL/min/1.73 m2. Am J Kidney Dis 2010, 56:486-95. 10.1053/j.ajkd.2010.03.026, 2926290, 20557989.
21. Stevens LA, Coresh J, Schmid CH, Feldman HI, Froissart M, Kusek J, Rossert J, Van Lente F, Bruce RD, Zhang YL, Greene T, Levey AS. Estimating GFR using serum cystatin C alone and in combination with serum creatinine: a pooled analysis of 3,418 individuals with CKD. Am J Kidney Dis 2008, 51:395-406. 10.1053/j.ajkd.2007.11.018, 2390827, 18295055.
22. Dubois D, Dubois E. A formula to estimate the approximate surface area if height and weight be known. Arch Intern Med 1916, 17:863-871.
23. European Medicines Agency (EMEA) ICH Topic E 6 (R1) Guideline for Good Clinical Practice. 2002, CPMP/ICH/135/95, European Medicines Agency (EMEA).
24. Webb AR, Kline L, Holick MF. Influence of season and latitude on the cutaneous synthesis of vitamin D3: exposure to winter sunlight in Boston and Edmonton will not promote vitamin D3 synthesis in human skin. J Clin Endocrinol Metab 1988, 67:373-378. 10.1210/jcem-67-2-373, 2839537.
25. Kanis JA, . the World Health Organization Scientific Group Assessment of osteoporosis at the primary healthcare level. Technical Report 2007, University of Sheffield, Sheffield: WHO Collaborating Centre, the World Health Organization Scientific Group.
26. Odden MC, Scherzer R, Bacchetti P, Szczech LA, Sidney S, Grunfeld C, Shlipak MG. Cystatin C level as a marker of kidney function in human immunodeficiency virus infection: the FRAM study. Arch Intern Med 2007, 167:2213-2219. 10.1001/archinte.167.20.2213, 3189482, 17998494.
27. Filler G, Bökenkamp A, Hofmann W, Le Bricon T, Martínez-Brú C, Grubb A. Cystatin C as a marker of GFR-history, indications, and future research. Clin Biochem 2005, 38:1-8. 10.1016/j.clinbiochem.2004.09.025, 15607309.
28. van Vonderen M, Mallon P, Murray B, Doran P, van Agtmael M, Danner S, Lips P, Reiss S, . MEDICLAS Study Group Changes in Bone Biomarkers in ARV-naïve HIV + Men Randomized to NVP/LPV/r or AZT/3TC/LPV/r Help Explain Limited Loss of Bone Mineral Density over the First 12 Months after ART Initiation. 18th Conference on Retroviruses and Opportunistic Infections, Boston MA Feb 24-Mar 2 2011 833. MEDICLAS Study Group.
29. Keller C, Katz R, Cushman M, Fried LF, Shlipak M. Association of kidney function with inflammatory and procoagulant markers in a diverse cohort: a cross-sectional analysis from the Multi-Ethnic Study of Atherosclerosis (MESA). BMC Nephrol 2008, 9:9. 10.1186/1471-2369-9-9, 2533297, 18681974.
30. Barraclough K, Er L, Ng F, Harris M, Montaner J, Levin A. A comparison of the predictive performance of different methods of kidney function estimation in a well-characterized HIV-infected population. Nephron Clin Pract 2009, 111:c39-c48. 10.1159/000178978, 19052469.
31. Bennett KK, DeGruttola VG, Marschner IC, Havlir DV, Richman DD. Baseline predictors of CD4 T-lymphocyte recovery with combination antiretroviral therapy. J Acquir Immune Defic Syndr 2002, 31:20-26. 10.1097/00126334-200209010-00003, 12352146.
32. Sabin CA, Smith CJ, d' Arminio Monforte A, Battegay M, Gabiano C, Galli L, Geelen S, Gibb D, Guiguet M, Judd A, Leport C, Dabis F, Pantazis N, Porter K, Raffi F, Thorne C, Torti C, Walker S, Warszawski J, Wintergerst U, Chene G, Lundgren J. Collaboration of Observational HIV Epidemiological Research Europe (COHERE) Study Group Response to combination antiretroviral therapy: variation by age. AIDS 2008, 22:1463-73. Collaboration of Observational HIV Epidemiological Research Europe (COHERE) Study Group.
33. Ofotokun I, Weitzmann N, Vunnava A, Sheth A, Villinger F, Zhou J, Williams E, Sanford S, Rivas M, Lennox J. HAART-induced Immune Reconstitution: A Driving Force Behind Bone Resorption in HIV/AIDS. 18th Conference on Retroviruses and Opportunistic Infections, Boston MA 2011, 78.
34. Onen NF, Overton ET, Seyfried W, Stumm ER, Snell M, Mondy K, Tebas P. Aging and HIV infection: a comparison between older HIV-infected persons and the general population. HIV clin trials 2010, 11:100-109. 10.1310/hct1102-100, 20542846.
35. Fausto A, Bongiovanni M, Cicconi P, Menicagli L, Ligabò EV, Melzi S, Bini T, Sardanelli F, Cornalba G, d' Arminio Monforte A. Potential predictive factors of osteoporosis in HIV-positive subjects. Bone 2006, 38:893-897. 10.1016/j.bone.2005.11.001, 16377270.
36. McComsey GA, Kitch D, Daar ES, Tierney C, Jahed NC, Tebas P, Myers L, Melbourne K, Ha B, Sax PE. 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 A5224s, a substudy of ACTG. J Infect Dis 2011, 203:1791-1801. 10.1093/infdis/jir188, 21606537.
37. Rosenvinge MM, Gedela K, Copas AJ, Wilkinson A, Sheehy CA, Bano G, Hay PE, Pakianathan MR, Sadiq ST. Tenofovir-linked hyperparathyroidism is independently associated with the presence of vitamin D deficiency. J Acquir Immune Defic Syndr 2010, 54:496-499. 10.1097/QAI.0b013e3181caebaa, 20672448.
38. Masià M, Padillla S, Robledano C, López N, Ramos JM, Gutiérrez F. Early changes in parathyroid hormone concentrations in patients initiating antiretroviral therapy with tenofovir. AIDS Res Hum Retrovir
39. Haug CJ, Aukrust P, Haug E, Mørkrid L, Müller F, Frøland SS. Severe deficiency of 1,25-dihydroxyvitamin D3 in human immunodeficiency virus infection: association with immunological hyperactivity and only minor changes in calcium homeostasis. J Clin Endocrinol Metab 1998, 83:3832-3838. 10.1210/jc.83.11.3832, 9814454.
40. Mueller NJ, Fux CA, Ledergerber B, Elzi L, Schmid P, Dang T, Magenta L, Calmy A, Vergopoulos A, Bischoff-Ferrari HA. High prevalence of severe vitamin D deficiency in combined antiretroviral therapy-naive and successfully treated Swiss HIV patients. AIDS 2010, 24:1127-1134. 10.1097/QAD.0b013e328337b161, 20168200.
41. Hollis BW. Assessment and interpretation of circulating 25-hydroxyvitamin D and 1,25-dihydroxyvitamin D in the clinical enviroment. Endocrinol Metab Clin North Am 2010, 39:271-286. 10.1016/j.ecl.2010.02.012, 2903449, 20511051.
42. Vasikaran S, Eastell R, Bruyère O, Foldes AJ, Garnero P, Griesmacher A, McClung M, Morris HA, Silverman S, Trenti T, Wahl DA, Cooper C, Kanis JA. Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int 2011, 22:391-420. 10.1007/s00198-010-1501-1, 21184054.