Is the virulence of HIV changing? A meta-analysis of trends in prognostic markers of HIV disease progression and transmission

AIDS

Volumn 26, Issue 2, 2012, Pages 193-205

  Herbeck, Joshua T ^a   Müller, Viktor ^b   Maust, Brandon S ^a   Ledergerber, Bruno ^c   Tortie, Carlo ^d   Di Giambenedetto, Simona ^e   Gras, Luuk ^f   Günthard, Huldrych F ^c   Jacobsonh, Lisa P ^g   Mullins, James I ^a   Gottlieb, Geoffrey S ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d UNIVERSITY OF BRESCIA   (Italy)

^e CATHOLIC UNIVERSITY   (Italy)

^f STICHTING HIV MONITORING   (Netherlands)

^g JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

CD4 lymphocyte count; Disease progression; HIV infections epidemiology; HIV infections virology; HIV pathogenicity; Viral load trends; Virulence

Indexed keywords

ANTIRETROVIRUS AGENT; VIRUS RNA;

ARTICLE; CD4+ T LYMPHOCYTE; DISEASE COURSE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; PRIORITY JOURNAL; PROGNOSIS; TREND STUDY; VIRUS LOAD; VIRUS TRANSMISSION; VIRUS VIRULENCE;

BIOLOGICAL MARKERS; CD4 LYMPHOCYTE COUNT; DISEASE PROGRESSION; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; MALE; PROGNOSIS; RNA, VIRAL; VIRAL LOAD; VIRULENCE;

EID: 84155168018     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32834db418     Document Type: Article

References (73)

1. Biggar RJ. AIDS incubation in 1891 HIV seroconverters from different exposure groups. International Registry of Seroconverters. AIDS 1990; 4:1059-1066.
2. Carre N, Prins M, Meyer L, Brettle RP, Robertson JR, McArdle H, et al. Has the rate of progression to AIDS changed in recent years? AIDS 1997; 11:1611-1618.
3. Vanhems P, Lambert J, Guerra M, Hirschel B, Allard R. Association between the rate of CD4R T cell decrease and the year of human immunodeficiency virus (HIV) type 1 seroconversion among persons enrolled in the Swiss HIV Cohort Study. J Infect Dis 1999; 180:1803-1808.
4. Easterbrook PJ, Yu LM, Goetghebeur E, Boag F, McLean K, Gazzard B. Ten-year trends in CD4 cell counts at HIV and AIDS diagnosis in a London HIV clinic. AIDS 2000; 14:561-571.
5. Hendriks JC, Craib KJ, Veugelers PJ, van Druten HA, Coutinho RA, Schechter MT, et al. Secular trends in the survival of HIVinfected homosexual men in Amsterdam and Vancouver estimated from a death-included CD4-staged Markov model. Int J Epidemiol 2000; 29:565-572.
6. Holmberg S, Conley L, Luby S, Cohn S, Wong L, Vlahov D. Recent infection with human immunodeficiency virus and possible rapid loss of CD4 T lymphocytes. J Acquir Immune Defic Syndr Hum Retrovirol 1995; 9:291-296.
7. Galai N, Lepri A, Viahov D, Pezzotti P, Sinicco A, Rezza G. Temporal trends of initial CD4 cells counts following human immunodeficiency virus seroconversion in Italy, 1985-1992. The Human Immunodeficiency Virus Italian Seroconversion Study. Am J Epidemiol 1996; 143:278-282.
8. CASCADE. Time from HIV-1 seroconversion to AIDS and death before widespread use of highly-active antiretroviral therapy: a collaborative re-analysis. Collaborative Group on AIDS Incubation andHIV Survival including the CASCADE EU Concerted Action. Concerted Action on Seroconversion to AIDS and Death in Europe. Lancet 2000; 355:1131-1137.
9. CASCADE. Differences in CD4 cell counts at seroconversion and decline among 5739 HIV-1-infected individuals with well estimated dates of seroconversion. J Acquir Immune Defic Syndr 2003; 34:76-83.
10. Müller V, Ledergerber B, Perrin L, Klimkait T, Furrer H, Telenti A, et al. Stable virulence levels in the HIV epidemic of Switzerland over two decades. AIDS 2006; 20:889-894.
11. Herbeck JT, Gottlieb GS, Li X, Hu Z, Detels R, Phair J, et al. Lack of evidence for changing virulence of HIV-1 in North America. PLoS One 2008; 3:e1525.
12. Troude P, Chaix ML, Tran L, Deveau C, Seng R, Delfraissy JF, et al. No evidence of a change in HIV-1 virulence since 1996 in France. AIDS 2009; 23:1261-1267.
13. van Griensven GJ, Hessol NA, Koblin BA, Byers RH, O'Malley PM, Albercht-van Lent N, et al. Epidemiology of human immunodeficiency virus type 1 infection among homosexual men participating in hepatitis B vaccine trials in Amsterdam, New York City, and San Francisco, 1978-1990. Am J Epidemiol 1993; 137:909-915.
14. Veugelers PJ, Page KA, Tindall B, Schechter MT, Moss AR, Winkelstein WW Jr, et al. Determinants of HIV disease progression among homosexual men registered in the Tricontinental Seroconverter Study. Am J Epidemiol 1994; 140:747-758.
15. Sinicco A, Fora R, Raiteri R, Sciandra M, Bechis G, Calvo MM, et al. Is the clinical course of HIV-1 changing? Cohort study. Br Med J 1997; 315:1232-1237.
16. Dorrucci M, Phillips A, Longo B, Rezza G. Changes over time in postseroconversion CD4 cell counts in the Italian HIVSeroconversion Study: 1985-2002. AIDS 2005; 19:331-335.
17. Gali Y, Berkhout B, Vanham G, Bakker M, Back NK, Arien KK. Survey of the temporal changes in HIV-1 replicative fitness in the Amsterdam Cohort. Virology 2007; 364:140-146.
18. Dorrucci M, Rezza G, Porter K, Phillips A. Temporal trends in postseroconversion CD4 cell count and HIV load: the Concerted Action on Seroconversion to AIDS and Death in Europe Collaboration, 1985-2002. J Infect Dis 2007; 195:525-534.
19. Crum-Cianflone N, Eberly L, Zhang Y, Ganesan A, Weintrob A, Marconi V, et al. Is HIV becoming more virulent? Initial CD4 cell counts among HIV seroconverters during the course of the HIV epidemic: 1985-2007. Clin Infect Dis 2009; 48:1285-1292.
20. Gras L, Jurriaans S, Bakker M, van Sighem A, Bezemer D, Fraser C, et al. Viral load levels measured at set-point have risen over the last decade of the HIV epidemic in the Netherlands. PLoS One 2009; 4:e7365.
21. Müller V, Maggiolo F, Suter F, Ladisa N, De Luca A, Antinori A, et al. Increasing clinical virulence in two decades of the Italian HIV epidemic. PLoS Pathog. 2009; 5: e1000454.
22. Crum-Cianflone NF, Ren Q, Eberly LE, Ganesan A, Weintrob A, Marconi V, et al. Are HIV-positive persons progressing faster after diagnosis over the epidemic? J Acquir Immune Defic Syndr 2010; 54:e6-e7.
23. Potard V, Weiss L, Lamontagne F, Rouveix E, Beck-Wirth G, Drogoul-Vey MP, et al. Trends in postinfection CD4 cell counts and plasma HIV-1 RNA levels in HIV-1-infected patients in France between 1997 and 2005. J Acquir Immune Defic Syndr 2009; 52:422-426.
24. Webber MP, SchoenbaumEE, Gourevitch MN, Buono D, Chang CJ, Klein RS. Temporal trends in the progression of human immunodeficiency virus disease in a cohort of drug users. Epidemiology 1998; 9:613-617.
25. Gail MH, Rosenberg PS, Goedert JJ. Therapy may explain recent deficits in AIDS incidence. J Acquir Immune Defic Syndr 1990; 3:296-306.
26. SFBulletin. Update: acquired immunodeficiency syndrome in homosexual and bisexual men-San Francisco. In: San Francisco Epidemiologic Bulletin. Edited by San Francisco Department of Public Health; 1988.
27. Taylor JMG, Kuo J-M, Detels R. Is the incubation period of AIDS lengthening? J Acquir Immune Defic Syndr 1991; 4:69-75.
28. O'Brien T, Hoover D, Rosenberg P, Chen B, Detels R, Kingsley L. Evaluation of secular trends in CD4R lymphocyte loss among human immunodeficiency virus type 1 (HIV-1)-infected men with known dates of seroconversion.AmJ Epidemiol 1995; 142:636-642.
29. Hessol NA, Koblin BA, van Griensven GJ, Bacchetti P, Liu JY, Stevens CE, et al. Progression of human immunodeficiency virus type 1 (HIV-1) infection among homosexual men in hepatitis B vaccine trial cohorts in Amsterdam, New York City, and San Francisco, 1978-1991. Am J Epidemiol 1994; 139:1077-1087.
30. Keet IPM, Veugelers PJ, Koot M, de Weerd MH, Roos MTL, Miedema F, et al. Temporal trends of the natural history of HIV- 1 infection following seroconversion between 1984 and 1993.. AIDS 1996; 10:1601-1602.
31. Muñoz A, Xu J. Models for the incubation of AIDS and variations according to age and period. Stat Med 1996; 15:2459-2473.
32. Arien KK, Troyer RM, Gali Y, Colebunders RL, Arts EJ, Vanham G. Replicative fitness of historical and recent HIV-1 isolates suggests HIV-1 attenuation over time. AIDS 2005; 19:1555-1564.
33. Müller V, von Wyl V, Yerly S, Boni J, Klimkait T, Burgisser P, et al. African descent is associated with slower CD4 cell count decline in treatment-naive patients of the Swiss HIV Cohort Study. AIDS 2009; 23: 1269-1276.
34. de Wolf F, Spijkerman I, Schellekens PT, Langendam M, Kuiken C, Bakker M, et al. AIDS prognosis based on HIV-1 RNA, CD4R T-cell count and function: markers with reciprocal predictive value over time after seroconversion. AIDS 1997; 11:1799-1806.
35. Mellors JW, Kingsley LA, Rinaldo CR Jr, Todd JA, Hoo BS, Kokka RP, et al. Quantitation of HIV-1 RNA in plasma predicts outcome after seroconversion. Ann Intern Med 1995; 122:573-579.
36. Mellors JW, Munoz A, Giorgi JV, Margolick JB, Tassoni CJ, Gupta P, et al. Plasma viral load and CD4R lymphocytes as prognostic markers of HIV-1 infection. Ann Intern Med 1997; 126:946-954.
37. Mellors JW, Margolick JB, Phair JP, Rinaldo CR, Detels R, Jacobson LP, et al. Prognostic value of HIV-1 RNA, CD4 cell count, and CD4 cell slope for progression to AIDS and death in untreated HIV-1 infection J Am Med Assoc 2007; 297:2349-2350.
38. Lingappa JR, Hughes JP, Wang RS, Baeten JM, Celum C, Gray GE, et al. Estimating the impact of plasma HIV-1 RNA reductions on heterosexual HIV-1 transmission risk. PLoS One 2010; 5:e12598.
39. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, et al. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med 2000; 342:921-929.
40. Fideli US, Allen SA, Musonda R, Trask S, Hahn BH, Weiss H, et al. Virologic and immunologic determinants of heterosexual transmission of human immunodeficiency virus type 1 in Africa. AIDS Res Hum Retroviruses 2001; 17:901-910.
41. Fraser C, Hollingsworth TD, Chapman R, de Wolf F, Hanage WP. Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc Natl Acad Sci U S A 2007; 104:17441-17446.
42. SHCS. Cohort profile: the Swiss HIV Cohort Study. Int J Epidemiol 2010; 39:1179-1189.
43. Anastos K, Gange SJ, Lau B, Weiser B, Detels R, Giorgi JV, et al. Association of race and gender with HIV-1 RNA levels and immunologic progression. J Acquir Immune Defic Syndr 2000; 24:218-226.
44. Easterbrook PJ, Farzadegan H, Hoover DR, Palenicek J, Chmiel JS, Kaslow RA, et al. Racial differences in rate of CD4 decline in HIV-1-infected homosexual men. AIDS 1996; 10:1147-1155.
45. May M, Wood R, Myer L, Taffe P, Rauch A, Battegay M, et al. CD4(R) T cell count decreases by ethnicity among untreated patients with HIV infection in South Africa and Switzerland. J Infect Dis 2009; 200:1729-1735.
46. Viechtbauer W. The metafor package: a meta-analysis package for R (Version 1.3-0).. J Stat Software 2010; 36:1-48.
47. Team RDC. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2009.
48. Laird N, Mosteller F. Some statistical methods for combining experimental results. Int J Technol Assess Health Care 1990; 6:5-30.
49. Thompson SG, Higgins JP. How should meta-regression analyses be undertaken and interpreted? Stat Med 2002; 21:1559-1573.
50. Lyles RH, Munoz A, Yamashita TE, Bazmi H, Detels R, Rinaldo CR, et al. Natural history of human immunodeficiency virus type 1 viremia after seroconversion and proximal to AIDS in a large cohort of homosexual men. Multicenter AIDS Cohort Study. J Infect Dis 2000; 181:872-880.
51. Gupta SB, Jacobson LP, Margolick JB, Rinaldo CR, Phair JP, Jamieson BD, et al. Estimating the benefit of an HIV-1 vaccine that reduces viral load set point. J Infect Dis 2007; 195:546-550.
52. Janssen RS. Implementing HIV screening. Clin Infect Dis 2007; 45 (Suppl 4):S226-S231.
53. Janssen RS, Satten GA, Stramer SL, Rawal BD, O'Brien TR, Weiblen BJ, et al. New testing strategy to detect early HIV-1 infection for use in incidence estimates and for clinical and prevention purposes. JAMA 1998; 280:42-48.
54. Ghosn J, Deveau C, Chaix ML, Goujard C, Galimand J, Zitoun Y, et al. Despite being highly diverse, immunovirological status strongly correlates with clinical symptoms during primary HIV-1 infection: a cross-sectional study based on 674 patients enrolled in the ANRS CO 06 PRIMO cohort. J Antimicrob Chemother 2010; 65:741-748.
55. Kelley CF, Barbour JD, Hecht FM. The relation between symptoms, viral load, and viral load set point in primary HIV infection. J Acquir Immune Defic Syndr 2007; 45:445-448.
56. Quinn TC. The epidemiology of the acquired immunodeficiency syndrome in the 1990 s. Emerg Med Clin North Am 1995; 13:1-25.
57. Ward JW, Duchin JS. The epidemiology of HIV and AIDS in the United States. AIDS Clin Rev 1997-1998; 1-45.
58. Hamers FF, Batter V, Downs AM, Alix J, Cazein F, Brunet JB. The HIV epidemic associated with injecting drug use in Europe: geographic and time trends. AIDS 1997; 11:1365-1374.
59. Kouyos RD, von Wyl V, Yerly S, Boni J, Taffe P, Shah C, et al. Molecular epidemiology reveals long-term changes in HIV type 1 subtype B transmission in Switzerland. J Infect Dis 2010; 201:1488-1497.
60. Pilcher CD, Tien HC, Eron JJ Jr, Vernazza PL, Leu SY, Stewart PW, et al. Brief but efficient: acute HIV infection and the sexual transmission of HIV. J Infect Dis 2004; 189:1785-1792.
61. Gray RH, Wawer MJ, Brookmeyer R, Sewankambo NK, Serwadda D, Wabwire-Mangen F, et al. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 2001; 357:1149-1153.
62. Hecht FM, Hartogensis W, Bragg L, Bacchetti P, Atchison R, Grant R, et al. HIV RNA level in early infection is predicted by viral load in the transmission source. AIDS 2010; 24:941-945.
63. Hollingsworth TD, Laeyendecker O, Shirreff G, Donnelly CA, Serwadda D, Wawer MJ, et al. HIV-1 transmitting couples have similar viral load set-points in Rakai, Uganda. PLoS Pathog 2010; 6:e1000876.
64. Alizon S, von Wyl V, Stadler T, Kouyos RD, Yerly S, Hirschel B, et al. Phylogenetic approach reveals that virus genotype largely determines HIV set-point viral load. PLoS Pathog 2010; 6:e1001123.
65. Müller V, Fraser C, Herbeck J. A strong case for viral genetic factors in HIV virulence. Viruses 2011; 3:204-206.
66. Allen TM, Altfeld M, Yu XG, O'Sullivan KM, Lichterfeld M, Le Gall S, et al. Selection, transmission, and reversion of an antigen-processing cytotoxic T-lymphocyte escape mutation in human immunodeficiency virus type 1 infection. J Virol 2004; 78:7069-7078.
67. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, Feeney M, et al. HIV evolution: CTL escape mutation and reversion after transmission. Nat Med 2004; 10:282-289.
68. Bhattacharya T, Daniels M, Heckerman D, Foley B, Frahm N, Kadie C, et al. Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science 2007; 315:1583-1586.
69. Kawashima Y, Pfafferott K, Frater J, Matthews P, Payne R, Addo M, et al. Adaptation of HIV-1 to human leukocyte antigen class I. Nature 2009; 458:641-645.
70. Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, et al. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med 1996; 2:405-411.
71. Carrington M, O'Brien SJ. The influence of HLA genotype on AIDS. Annu Rev Med 2003; 54:535-551.
72. Bunnik EM, Euler Z, Welkers MR, Boeser-Nunnink BD, Grijsen ML, Prins JM, et al. Adaptation of HIV-1 envelope gp120 to humoral immunity at a population level. Nat Med 2010; 16:995-997.
73. Curlin ME, Zioni R, Hawes SE, Liu Y, Deng W, Gottlieb GS, et al. HIV-1 envelope subregion length variation during disease progression. PLoS Pathog 2010; 6:e1001228.