Identifying recent HIV infections: From serological assays to genomics

Viruses

Volumn 7, Issue 10, 2015, Pages 5508-5524

  Moyo, Sikhulile ^a,b   Wilkinson, Eduan ^c   Novitsky, Vladimir ^b,d   Vandormael, Alain ^c   Gaseitsiwe, Simani ^b,d   Essex, Max ^b,d   Engelbrecht, Susan ^a,e   De Oliveira, Tulio ^c,f,g  

^a STELLENBOSCH UNIVERSITY   (South Africa)

^b BOTSWANA HARVARD AIDS INSTITUTE PARTNERSHIP   (Botswana)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

Molecular based assays; Recent HIV infection; Serology based assays; Viral diversity

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN G3;

ANTIBODY RESPONSE; BINDING AFFINITY; BINDING ASSAY; COST EFFECTIVENESS ANALYSIS; ENZYME IMMUNOASSAY; GENETIC ALGORITHM; GENETIC VARIABILITY; HAMMING DISTANCE; HIGH RESOLUTION MELTING ASSAY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; INFORMATION PROCESSING; INNO LIA ASSAY; MICROBIAL POPULATION DYNAMICS; MOLECULAR DIAGNOSIS; POLYMERASE CHAIN REACTION; REVIEW; SCORING SYSTEM; SEQUENCE ANALYSIS; SEROLOGY; VIRAL LOAD TESTING; VIRUS IDENTIFICATION; VIRUS LOAD; CROSS-SECTIONAL STUDY; HIV INFECTIONS; HUMAN; IMMUNOLOGY; LONGITUDINAL STUDY; PROCEDURES;

CROSS-SECTIONAL STUDIES; HIV INFECTIONS; HUMANS; LONGITUDINAL STUDIES; MOLECULAR DIAGNOSTIC TECHNIQUES; SEROLOGIC TESTS;

EID: 84945344556     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7102887     Document Type: Review

References (100)

1. Fiamma, A.; Lissouba, P.; Amy, O.E.; Singh, B.; Laeyendecker, O.; Quinn, T.C.; Taljaard, D.; Auvert, B. Can HIV incidence testing be used for evaluating HIV intervention programs? A reanalysis of the Orange Farm male circumcision trial (ANRS-1265). BMC Infect. Dis. 2010, 10. [CrossRef] [PubMed]
2. Gray, R.H.; Li, X.; Kigozi, G.; Serwadda, D.; Nalugoda, F.; Watya, S.; Reynolds, S.J.; Wawer, M. The impact of male circumcision on HIV incidence and cost per infection prevented: A stochastic simulation model from Rakai, Uganda. AIDS 2007, 21, 845–850. [CrossRef] [PubMed]
3. Hall, H.I.; Green, T.A.; Wolitski, R.J.; Holtgrave, D.R.; Rhodes, P.; Lehman, J.S.; Durden, T.; Fenton, K.A.; Mermin, J.H. Estimated future HIV prevalence, incidence, and potential infections averted in the United States: Amultiple scenario analysis. J. Acquir. Immune Defic. Syndr. 2010, 55, 271–276. [CrossRef] [PubMed]
4. Brenner, B.G.; Roger, M.; Routy, J.-P.; Moisi, D.; Ntemgwa, M.; Matte, C.; Baril, J.-G.; Thomas, R.; Rouleau, D.; Bruneau, J. High rates of forward transmission events after acute/early HIV-1 infection. J. Infect. Dis. 2007, 195, 951–959. [CrossRef] [PubMed]
5. Ahmed, S.; Lutalo, T.; Wawer, M.; Serwadda, D.; Sewankambo, N.; Nalugoda, F.; Makumbi, F.; Wabwire-Mangen, F.; Kiwanuka, N.; Kigozi, G. HIV incidence and sexually transmitted disease prevalence associated with condom use: A population study in Rakai, Uganda. AIDS 2001, 15, 2171–2179. [CrossRef] [PubMed]
6. Wawer, M.J.; Gray, R.H.; Sewankambo, N.K.; Serwadda, D.; Li, X.; Laeyendecker, O.; Kiwanuka, N.; Kigozi, G.; Kiddugavu, M.; Lutalo, T., et al. Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J. Infect. Dis. 2005, 191, 1403–1409. [CrossRef] [PubMed]
7. Abrahams, M.-R.; Anderson, J.A.; Giorgi, E.E.; Seoighe, C.; Mlisana, K.; Ping, L.-H.; Athreya, G.S.; Treurnicht, F.K.; Keele, B.F.; Wood, N., et al. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-poisson distribution of transmitted variants. J. Virol. 2009, 83, 3556–3567. [CrossRef] [PubMed]
8. Lagakos, S.; Gable, A. Methodological Challenges in Biomedical HIV Prevention Trials; National Academy Press: Washington, DC, USA, 2008.
9. Barnighausen, T.; Tanser, F.; Gqwede, Z.; Mbizana, C.; Herbst, K.; Newell, M. High HIV incidence in a community with high HIV prevalence in rural South Africa: Findings from a prospective population-based study. AIDS 2008, 22, 139–144. [CrossRef] [PubMed]
10. Kumwenda, N.; Hoffman, I.; Chirenje, M.; Kelly, C.; Coletti, A.; Ristow, A.; Martinson, F.; Brown, J.; Chilongozi, D.; Richardson, B. HIV incidence among women of reproductive age in Malawi and Zimbabwe. Sex. Transm. Dis. 2006, 33, 646–651. [CrossRef] [PubMed]
11. Ghys, P.; Kufa, E.; George, M. Measuring trends in prevalence and incidence of HIV infection in countries with generalised epidemics. Sex. Transm. Infect. 2006, 82 (Suppl. 1), i52–i56. [CrossRef] [PubMed]
12. Brookmeyer, R.; Konikoff, J.; Laeyendecker, O.; Eshleman, S.H. Estimation of HIV incidence using multiple biomarkers. Am. J. Epidemiol. 2013, 177, 264–272. [CrossRef] [PubMed]
13. Busch, M.P.; Pilcher, C.D.; Mastro, T.D.; Kaldor, J.; Vercauteren, G.; Rodriguez, W.; Rousseau, C.; Rehle, T.M.; Welte, A.; Averill, M.D. Beyond detuning: 10 Years of progress and new challenges in the development and application of assays for HIV incidence estimation. AIDS 2010, 24, 2763–2771. [CrossRef] [PubMed]
14. Guy, R.; Gold, J.; Calleja, J.M.; Kim, A.A.; Parekh, B.; Busch, M.; Rehle, T.; Hargrove, J.; Remis, R.S.; Kaldor, J.M.: Accuracy of serological assays for detection of recent infection with HIV and estimation of population incidence: A systematic review. Lancet Infect. Dis. 2009, 9, 747–759. [CrossRef]
15. Incidence Assay Critical Path Working Group. More and better information to tackle HIV epidemics: Towards improved HIV incidence assays. PLoS Med. 2011, 8, e1001045.
16. Le Vu, S.; Pillonel, J.; Semaille, C.; Bernillon, P.; le Strat, Y.; Meyer, L.; Desenclos, J.: Principles and uses of HIV incidence estimation from recent infection testing—A review. Eur. Surveill. 2008, 13, 537–545.
17. Murphy, G.; Parry, J.V. Assays for the detection of recent infections with human immunodeficiency virus type 1. Euro. Surveill. 2008, 13, 314–320.
18. Kouyos, R.D.; vonWyl, V.; Yerly, S.; Böni, J.; Rieder, P.; Joos, B.; Taffé, P.; Shah, C.; Bürgisser, P.; Klimkait, T.: Ambiguous nucleotide calls from population-based sequencing of HIV-1 are a marker for viral diversity and the age of infection. Clin. Infect. Dis. 2011, 52, 532–539. [CrossRef] [PubMed]
19. Ragonnet-Cronin, M.; Aris-Brosou, S.; Joanisse, I.; Merks, H.; Vallée, D.; Caminiti, K.; Rekart, M.; Krajden, M.; Cook, D.; Kim, J. Genetic diversity as a marker for timing infection in HIV-infected patients: Evaluation of a 6-month window and comparison with BED. J. Infect. Dis. 2012, 206, 756–764. [CrossRef] [PubMed]
20. Sharma, U.K.; Schito, M.; Welte, A.; Rousseau, C.; Fitzgibbon, J.; Keele, B.; Shapiro, S.; McMichael, A.; Burns, D.N. Workshop summary: Novel biomarkers for HIV incidence assay development. AIDS Res. Hum. Retrovir. 2012, 28, 532–539. [CrossRef] [PubMed]
21. Allam, O.; Samarani, S.; Ahmad, A. Hammering out HIV-1 incidence with Hamming distance. AIDS 2011, 25, 2047–2048. [CrossRef] [PubMed]
22. Chen, I.; Khaki, L.; Lindsey, J.C.; Fry, C.; Cousins, M.M.; Siliciano, R.F.; Violari, A.; Palumbo, P.; Eshleman, S.H. Association of pol diversity with antiretroviral treatment outcomes among HIV-infected African children. PLoS ONE 2013, 8, e81213. [CrossRef] [PubMed]
23. Welte, A.; McWalter, T.A.; Laeyendecker, O.; Hallett, T.B. Using tests for recent infection to estimate incidence: Problems and prospects for HIV. Eur. Surveill. 2010, 15. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19589 (accessed on 1 July 2015).
24. Mastro, T.D.; Kim, A.A.; Hallett, T.; Rehle, T.; Welte, A.; Laeyendecker, O.; Oluoch, T.; Garcia-Calleja, J.M. Estimating HIV incidence in populations using tests for recent infection: Issues, challenges and the way forward. J. HIV AIDS Surveill. Epidemiol. 2010, 2, 1–14. [PubMed]
25. Kassanjee, R.; McWalter, T.A.; Barnighausen, T.; Welte, A. A new general biomarker-based incidence estimator. Epidemiology 2012, 23, 721–728. [CrossRef] [PubMed]
26. Kassanjee, R.; Pilcher, C.D.; Keating, S.M.; Facente, S.N.; McKinney, E.; Price, M.A.; Martin, J.N.; Little, S.; Hecht, F.M.; Kallas, E.G., et al. Independent assessment of candidate HIV incidence assays on specimens in the CEPHIA repository. AIDS 2014, 28, 2439–2449. [CrossRef] [PubMed]
27. Duong, Y.T.; Qiu, M.; De, A.K.; Jackson, K.; Dobbs, T.; Kim, A.A.; Nkengasong, J.N.; Parekh, B.S. Detection of recent HIV-1 infection using a new limiting-antigen avidity assay: Potential for HIV-1 incidence estimates and avidity maturation studies. PLoS ONE 2012, 7, e33328. [CrossRef] [PubMed]
28. Cohen, M.S.; Gay, C.L.; Busch, M.P.; Hecht, F.M. The detection of acute HIV infection. J. Infect. Dis. 2010, 202, S270–S277. [CrossRef] [PubMed]
29. McMichael, A.J.; Borrow, P.; Tomaras, G.D.; Goonetilleke, N.; Haynes, B.F. The immune response during acute HIV-1 infection: Clues for vaccine development. Nat. Rev. Immunol. 2010, 10, 11–23. [CrossRef] [PubMed]
30. Powers, K.A.; Miller, W.C.; Pilcher, C.D.; Mapanje, C.; Martinson, F.E.; Fiscus, S.A.; Chilongozi, D.A.; Namakhwa, D.; Price, M.A.; Galvin, S.R., et al. Improved detection of acute HIV-1 infection in sub-Saharan Africa: Development of a risk score algorithm. AIDS 2007, 21, 2237–2242. [CrossRef] [PubMed]
31. Rosenberg, N.E.; Pilcher, C.D.; Busch, M.P.; Cohen, M.S. How can we better identify early HIV infections? Curr. Opin. HIV AIDS 2015, 10, 61–68. [CrossRef] [PubMed]
32. Aulagnier, M.; Janssens, W.; de Beer, I.; van Rooy, G.; Gaeb, E.; Hesp, C.; van der Gaag, J.; Rinke deWit, T.F. Incidence of HIV inWindhoek, Namibia: Demographic and socio-economic associations. PLoS ONE 2011, 6, e25860. [CrossRef] [PubMed]
33. Draenert, R.; Verrill, C.L.; Tang, Y.; Allen, T.M.; Wurcel, A.G.; Boczanowski, M.; Lechner, A.; Kim, A.Y.; Suscovich, T.; Brown, N.V., et al. Persistent recognition of autologous virus by high-avidity CD8 T cells in chronic, progressive human immunodeficiency virus type 1 infection. J. Virol. 2004, 78, 630–641. [CrossRef] [PubMed]
34. Parekh, B.S.; Kennedy, M.S.; Dobbs, T.; Pau, C.P.; Byers, R.; Green, T.; Hu, D.J.; Vanichseni, S.; Young, N.L.; Choopanya, K., et al. Quantitative detection of increasing HIV type 1 antibodies after seroconversion: A simple assay for detecting recent HIV infection and estimating incidence. AIDS Res. Hum. Retrovir. 2002, 18, 295–307. [CrossRef] [PubMed]
35. Suligoi, B.; Massi, M.; Galli, C.; Sciandra, M.; di Sora, F.; Pezzotti, P.; Recchia, O.; Montella, F.; Sinicco, A.; Rezza, G.: Identifying recent HIV infections using the avidity index and an automated enzyme immunoassay. J. Acquir. Immune Defic. Syndr. 2003, 32, 424–428. [CrossRef] [PubMed]
36. Laeyendecker, O.; Brookmeyer, R.; Cousins, M.M.; Mullis, C.E.; Konikoff, J.; Donnell, D.; Celum, C.; Buchbinder, S.P.; Seage, G.R., III; Kirk, G.D., et al. HIV incidence determination in the United States: A multiassay approach. J. Infect. Dis. 2013, 207, 232–239. [CrossRef] [PubMed]
37. World Health Organization. When and How to Use Assays for Recent Infection to Estimate HIV Incidence at a Population Level;World Health Organization: Geneva, Switzerland, 2011.
38. Janssen, R.S.; Satten, G.A.; Stramer, S.L.; Rawal, B.D.; O’Brien, T.R.; Weiblen, B.J.; Hecht, F.M.; Jack, N.; Cleghorn, F.R.; Kahn, J.O., et al. New testing strategy to detect early HIV-1 infection for use in incidence estimates and for clinical and prevention purposes. J. Am. Med. Assoc. 1998, 280, 42–48. [CrossRef]
39. Kothe, D.; Byers, R.H.; Caudill, S.P.; Satten, G.A.; Janssen, R.S.; Hannon, W.H.; Mei, J.V. Performance characteristics of a new less sensitive HIV-1 enzyme immunoassay for use in estimating HIV seroincidence. J. Acquir. Immune Defic. Syndr. 2003, 33, 625–634. [CrossRef] [PubMed]
40. Soroka, S.D.; Granade, T.C.; Candal, D.; Parekh, B.S. Modification of rapid human immunodeficiency virus (HIV) antibody assay protocols for detecting recent HIV seroconversion. Clin. Diagn. Lab. Immunol. 2005, 12, 918–921. [CrossRef] [PubMed]
41. Soroka, S.D.; Granade, T.C.; Phillips, S.; Parekh, B. The use of simple, rapid tests to detect antibodies to human immunodeficiency virus types 1 and 2 in pooled serum specimens. J. Clin. Virol. 2003, 27, 90–96. [CrossRef]
42. Young, C.L.; Hu, D.J.; Byers, R.; Vanichseni, S.; Young, N.L.; Nelson, R.; Mock, P.A.; Choopanya, K.; Janssen, R.; Mastro, T.D., et al. Evaluation of a sensitive/less sensitive testing algorithm using the bioMerieux Vironostika-LS assay for detecting recent HIV-1 subtype B or E infection in Thailand. AIDS Res. Hum. Retrovir. 2003, 19, 481–486. [CrossRef] [PubMed]
43. Calypte Biomedical Corporation. AwareTM BEDTM EIA HIV-1 Incidence (IgG-Capture HIV-EIA) Enzyme Immunoassay for Population Estimates of HIV-1 Incidence; Calypte Biomedical Corporation: Portland, OR, USA, 2008.
44. Marinda, E.T.; Hargrove, J.; Preiser, W.; Slabbert, H.; van Zyl, G.; Levin, J.; Moulton, L.H.; Welte, A.; Humphrey, J. Significantly diminished long-term specificity of the BED capture enzyme immunoassay among patients with HIV-1 with very low CD4 counts and those on antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 2010, 53, 496–499. [CrossRef] [PubMed]
45. Moyo, S.; LeCuyer, T.; Wang, R.; Gaseitsiwe, S.; Weng, J.; Musonda, R.; Bussmann, H.; Mine, M.; Engelbrecht, S.; Makhema, J., et al. Evaluation of the false recent classification rates of multiassay algorithms in estimating HIV type 1 subtype C incidence. AIDS Res. Hum. Retrovir. 2014, 29, 29–36. [CrossRef]
46. Karita, E.; Price, M.; Hunter, E.; Chomba, E.; Allen, S.; Fei, L.; Kamali, A.; Sanders, E.J.; Anzala, O.; Katende, M. Investigating the utility of the HIV-1 BED capture enzyme immunoassay using cross-sectional and longitudinal seroconverter specimens from Africa. AIDS 2007, 21, 403–408. [CrossRef] [PubMed]
47. Laeyendecker, O.; Brookmeyer, R.; Oliver, A.E.; Mullis, C.E.; Eaton, K.P.; Mueller, A.C.; Jacobson, L.P.; Margolick, J.B.; Brown, J.; Rinaldo, C.R., et al. Factors associated with incorrect identification of recent HIV infection using the BED capture immunoassay. AIDS Res. Hum. Retrovir. 2012, 28, 816–822. [CrossRef] [PubMed]
48. Longosz, A.F.; Serwadda, D.; Nalugoda, F.; Kigozi, G.; Franco, V.; Gray, R.H.; Quinn, T.C.; Eshleman, S.H.; Laeyendecker, O.: Impact of HIV subtype on performance of the limiting antigen-avidity enzyme immunoassay, the bio-rad avidity assay, and the BED capture immunoassay in Rakai, Uganda. AIDS Res. Hum. Retrovir. 2014, 30, 339–344. [CrossRef] [PubMed]
49. Hargrove, J.; van Schalkwyk, C.; Eastwood, H. Bed estimates of HIV incidence: Resolving the differences, making things simpler. PLoS ONE 2012, 7, e29736. [CrossRef] [PubMed]
50. Brookmeyer, R. On the statistical accuracy of biomarker assays for HIV incidence. J. Acquir. Immune Defic. Syndr. 2010, 54, 406–414. [CrossRef] [PubMed]
51. UNAIDS. UNAIDS Reference Group on estimates, modelling and projections—Statement on the use of the BED assay for the estimation of HIV-1 incidence for surveillance or epidemic monitoring. Wkly Epidemiol. Rec. 2006, 81, 40.
52. Wei, X.; Liu, X.; Dobbs, T.; Kuehl, D.; Nkengasong, J.N.; Hu, D.J.; Parekh, B.S. Development of two avidity-based assays to detect recent HIV type 1 seroconversion using a multisubtype gp41 recombinant protein. AIDS Res. Hum. Retrovir. 2010, 26, 61–71. [CrossRef] [PubMed]
53. Thomas, H.I.; Wilson, S.; O’Toole, C.M.; Lister, C.M.; Saeed, A.M.; Watkins, R.P.; Morgan-Capner, P. Differential maturation of avidity of IgG antibodies to gp41, p24 and p17 following infection with HIV- 1. Clin. Exp. Immunol. 1996, 103, 185–191. [CrossRef] [PubMed]
54. Broliden, P.A.; Morfeldt-Mansson, L.; Rosen, J.; Jondal, M.; Wahren, B. Fine specificity of IgG subclass response to group antigens in HIV-1-infected patients. Clin. Exp. Immunol. 1989, 76, 216–221. [PubMed]
55. Tomaras, G.D.; Haynes, B.F. HIV-1-specific antibody responses during acute and chronic HIV-1 infection. Curr. Opin. HIV AIDS 2009, 4, 373–379. [CrossRef] [PubMed]
56. Wilson, K.M.; Johnson, E.I.; Croom, H.A.; Richards, K.M.; Doughty, L.; Cunningham, P.H.; Kemp, B.E.; Branson, B.M.; Dax, E.M. Incidence immunoassay for distinguishing recent from established HIV-1 infection in therapy-naive populations. AIDS 2004, 18, 2253–2259. [CrossRef] [PubMed]
57. McDougal, J.S.; Kennedy, M.S.; Nicholson, J.K.; Spira, T.J.; Jaffe, H.W.; Kaplan, J.E.; Fishbein, D.B.; O’Malley, P.; Aloisio, C.H.; Black, C.M., et al. Antibody response to human immunodeficiency virus in homosexual men. Relation of antibody specificity, titer, and isotype to clinical status, severity of immunodeficiency, and disease progression. J. Clin. Investig. 1987, 80, 316–324. [CrossRef] [PubMed]
58. Beniguel, L.; Begaud, E.; Peruchon, S.; Cognasse, F.; Gabrie, P.; Marovich, M.; Lucht, F.; Genin, C.; Garraud, O. Isotype profiles of anti-gp160 antibodies from HIV-infected patients in plasma and culture supernatants. Immunol. Lett. 2004, 93, 57–62. [CrossRef] [PubMed]
59. Curtis, K.A.; Ambrose, K.M.; Kennedy, M.S.; Owen, S.M. Evaluation of dried blood spots with a multiplex assay for measuring recent HIV-1 infection. PLoS ONE 2014, 9, e107153. [CrossRef] [PubMed]
60. Tinguely, C.; Schild-Spycher, T.; Bahador, Z.; Gowland, P.; Stolz, M.; Niederhauser, C. Comparison of a conventional HIV 1/2 line immunoassay with a rapid confirmatory HIV 1/2 assay. J. Virol. Methods 2014, 206, 1–4. [CrossRef] [PubMed]
61. Schupbach, J.; Gebhardt, M.D.; Tomasik, Z.; Niederhauser, C.; Yerly, S.; Burgisser, P.; Matter, L.; Gorgievski, M.; Dubs, R.; Schultze, D., et al. Assessment of recent HIV-1 infection by a line immunoassay for HIV-1/2 confirmation. PLoS Med. 2007, 4, e343. [CrossRef] [PubMed]
62. Wendel, S.K.; Mullis, C.E.; Eshleman, S.H.; Blankson, J.N.; Moore, R.D.; Keruly, J.C.; Brookmeyer, R.; Quinn, T.C.; Laeyendecker, O. Effect of natural and ARV-induced viral suppression and viral breakthrough on anti-HIV antibody proportion and avidity in patients with HIV-1 subtype B infection. PLoS ONE 2013, 8, e55525. [CrossRef] [PubMed]
63. Rawal, B.D.; Degula, A.; Lebedeva, L.; Janssen, R.S.; Hecht, F.M.; Sheppard, H.W.; Busch, M.P. Development of a new less-sensitive enzyme immunoassay for detection of early HIV-1 infection. J. Acquir. Immune Defic. Syndr. 2003, 33, 349–355. [CrossRef] [PubMed]
64. Burgers, W.A.; Riou, C.; Mlotshwa, M.; Maenetje, P.; de Assis Rosa, D.; Brenchley, J.; Mlisana, K.; Douek, D.C.; Koup, R.; Roederer, M., et al. Association of HIV-specific and total CD8+ T memory phenotypes in subtype C HIV-1 infection with viral set point. J. Immunol. 2009, 182, 4751–4761. [CrossRef] [PubMed]
65. Laeyendecker, O.; Brookmeyer, R.; Mullis, C.; Donnell, D.; Lingappa, J.; Celum, C.; Baeten, J.M.; Campbell, M.S.; Essex, M.; de Bruyn, G., et al. Specificity of four laboratory approaches for cross-sectional HIV incidence determination: Analysis of samples from adults with known non-recent HIV infection from five African countries. AIDS Res. Hum. Retrovir. 2012, 28, 1177–1183. [CrossRef] [PubMed]
66. Hallett, T.B.; Ghys, P.; Barnighausen, T.; Yan, P.; Garnett, G.P. Errors in “BED”-derived estimates of HIV incidence will vary by place, time and age. PLoS ONE 2009, 4, e5720. [CrossRef] [PubMed]
67. UNAIDS. WHO/UNAIDS Technical Update on HIV Incidence Assays for Surveillance and Epidemic Monitoring; UNAIDS: Geneva, Swtizerland, 2013.
68. Rehle, T.; Johnson, L.; Hallett, T.; Mahy, M.; Kim, A.; Odido, H.; Onoya, D.; Jooste, S.; Shisana, O.; Puren, A., et al. A comparison of South African national HIV incidence estimates: A critical appraisal of different methods. PLoS ONE 2015, 10, e0133255. [CrossRef] [PubMed]
69. Cousins, M.M.; Laeyendecker, O.; Beauchamp, G.; Brookmeyer, R.; Towler, W.I.; Hudelson, S.E.; Khaki, L.; Koblin, B.; Chesney, M.; Moore, R.D.: Use of a high resolution melting (HRM) assay to compare gag, pol, and env diversity in adults with different stages of HIV infection. PLoS ONE 2011, 6, e27211. [CrossRef] [PubMed]
70. Cousins, M.M.; Konikoff, J.; Laeyendecker, O.; Celum, C.; Buchbinder, S.P.; Seage, G.R., III; Kirk, G.D.; Moore, R.D.; Mehta, S.H.; Margolick, J.B., et al. HIV diversity as a biomarker for HIV incidence estimation: including a high resolution melting diversity assay in a multi-assay algorithm. J. Clin. Microbiol. 2013, 52, 115–121. [CrossRef] [PubMed]
71. Cousins, M.M.; Donnell, D.; Eshleman, S.H.: Impact of mutation type and amplicon characteristics on genetic diversity measures generated using a high-resolution melting diversity assay. J. Mol. Diagn. 2013, 15, 130–137. [CrossRef] [PubMed]
72. Meixenberger, K.; Hauser, A.; Jansen, K.; Yousef, K.P.; Fiedler, S.; von Kleist, M.; Norley, S.; Somogyi, S.; Hamouda, O.; Bannert, N., et al. Assessment of ambiguous base calls in HIV-1 pol population sequences as a biomarker for identification of recent infections in HIV-1 incidence studies. J. Clin. Microbiol. 2014, 52, 2977–2983. [CrossRef] [PubMed]
73. Andersson, E.; Shao, W.; Bontell, I.; Cham, F.; Cuong, D.D.; Wondwossen, A.; Morris, L.; Hunt, G.; Sönnerborg, A.; Bertagnolio, S. Evaluation of sequence ambiguities of the HIV-1 pol gene as a method to identify recent HIV-1 infection in transmitted drug resistance surveys. Infect. Genet. Evol. 2013, 18, 125–131. [CrossRef] [PubMed]
74. Volz, E.M.; Ionides, E.; Romero-Severson, E.O.; Brandt, M.-G.; Mokotoff, E.; Koopman, J.S. HIV-1 transmission during early infection in men who have sex with men: A phylodynamic analysis. PLoS Med. 2013, 10, e1001568. [CrossRef] [PubMed]
75. Park, S.Y.; Love, T.M.; Nelson, J.; Thurston, S.W.; Perelson, A.S.; Lee, H.Y. Designing a genome-based HIV incidence assay with high sensitivity and specificity. AIDS 2011, 25, F13–F19. [CrossRef] [PubMed]
76. Xia, X.-Y.; Ge, M.; Hsi, J.H.; He, X.; Ruan, Y.-H.; Wang, Z.-X.; Shao, Y.-M.; Pan, X.-M. High-accuracy identification of incident HIV-1 infections using a sequence clustering based diversity measure. PLoS ONE 2014, 9, e100081. [CrossRef] [PubMed]
77. Laeyendecker, O.; Rothman, R.E.; Henson, C.; Horne, B.J.; Ketlogetswe, K.S.; Kraus, C.K.; Shahan, J.; Kelen, G.D.; Quinn, T.C. The effect of viral suppression on cross-sectional incidence testing in the Johns Hopkins hospital emergency department. J. Acquir. Immune Defic. Syndr. 2008, 48, 211–215. [CrossRef] [PubMed]
78. Konikoff, J.; Brookmeyer, R.; Longosz, A.F.; Cousins, M.M.; Celum, C.; Buchbinder, S.P.; Seage, G.R., III; Kirk, G.D.; Moore, R.D.; Mehta, S.H., et al. Performance of a limiting-antigen avidity enzyme immunoassay for cross-sectional estimation of HIV incidence in the United States. PLoS ONE 2013, 8, e82772. [CrossRef] [PubMed]
79. Joseph, S.B.; Swanstrom, R.; Kashuba, A.D.; Cohen, M.S. Bottlenecks in HIV-1 transmission: Insights from the study of founder viruses. Nat. Rev. Microbiol. 2015, 13, 414–425. [CrossRef] [PubMed]
80. Keele, B.F.; Giorgi, E.E.; Salazar-Gonzalez, J.F.; Decker, J.M.; Pham, K.T.; Salazar, M.G.; Sun, C.; Grayson, T.; Wang, S.; Li, H., et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 2008, 105, 7552–7557. [CrossRef] [PubMed]
81. Parker, Z.F.; Iyer, S.S.; Wilen, C.B.; Parrish, N.F.; Chikere, K.C.; Lee, F.-H.; Didigu, C.A.; Berro, R.; Klasse, P.J.; Lee, B., et al. Transmitted/founder and chronic HIV-1 envelope proteins are distinguished by differential utilization of CCR 5. J. Virol. 2013, 87, 2401–2411. [CrossRef] [PubMed]
82. Parrish, N.F.; Wilen, C.B.; Banks, L.B.; Iyer, S.S.; Pfaff, J.M.; Salazar-Gonzalez, J.F.; Salazar, M.G.; Decker, J.M.; Parrish, E.H.; Berg, A., et al. Transmitted/founder and chronic subtype C HIV-1 use CD4 and CCR5 receptors with equal efficiency and are not inhibited by blocking the integrin _4_ 7. PLoS Pathog. 2012, 8, e1002686. [CrossRef] [PubMed]
83. Novitsky, V.; Lagakos, S.; Herzig, M.; Bonney, C.; Kebaabetswe, L.; Rossenkhan, R.; Nkwe, D.; Margolin, L.; Musonda, R.; Moyo, S. Evolution of proviral gp120 over the first year of HIV-1 subtype C infection. Virology 2009, 383, 47–59. [CrossRef] [PubMed]
84. Kearney, M.; Maldarelli, F.; Shao, W.; Margolick, J.B.; Daar, E.S.; Mellors, J.W.; Rao, V.; Coffin, J.M.; Palmer, S. Human immunodeficiency virus type 1 population genetics and adaptation in newly infected individuals. J. Virol. 2009, 83, 2715–2727. [CrossRef] [PubMed]
85. Palmer, S.; Kearney, M.; Maldarelli, F.; Halvas, E.K.; Bixby, C.J.; Bazmi, H.; Rock, D.; Falloon, J.; Davey, R.T., Jr.; Dewar, R.L., et al. Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J. Clin. Microbiol. 2005, 43, 406–413. [CrossRef] [PubMed]
86. Cousins, M.M.; Ou, S.S.; Wawer, M.J.; Munshaw, S.; Swan, D.; Magaret, C.A.; Mullis, C.E.; Serwadda, D.; Porcella, S.F.; Gray, R.H., et al. Comparison of a high-resolution melting assay to next-generation sequencing for analysis of HIV diversity. J. Clin. Microbiol. 2012, 50, 3054–3059. [CrossRef] [PubMed]
87. Towler, W.I.; James, M.M.; Ray, S.C.; Wang, L.; Donnell, D.; Mwatha, A.; Guay, L.; Nakabiito, C.; Musoke, P.; Jackson, J.B., et al. Analysis of HIV diversity using a high-resolution melting assay. AIDS Res. Hum. Retrovir. 2010, 26, 913–918. [CrossRef] [PubMed]
88. James, M.M.; Wang, L.; Donnell, D.; Cousins, M.M.; Barlow-Mosha, L.; Fogel, J.M.; Towler, W.I.; Agwu, A.L.; Bagenda, D.; Mubiru, M., et al. Use of a high resolution melting assay to analyze HIV diversity in HIV-infected Ugandan children. Pediatr. Infect. Dis. J. 2012, 31, e222–e228. [CrossRef] [PubMed]
89. Delwart, E.L.; Sheppard, H.W.; Walker, B.D.; Goudsmit, J.; Mullins, J.I. Human immunodeficiency virus type 1 evolution in vivo tracked by DNA heteroduplex mobility assays. J. Virol. 1994, 68, 6672–6683. [PubMed]
90. Cousins, M.M.; Konikoff, J.; Sabin, D.; Khaki, L.; Longosz, A.F.; Laeyendecker, O.; Celum, C.; Buchbinder, S.P.; Seage, G.R., III; Kirk, G.D., et al. A comparison of two measures of HIV diversity in multi-assay algorithms for HIV incidence estimation. PLoS ONE 2014, 9, e101043. [CrossRef] [PubMed]
91. Shankarappa, R.; Margolick, J.B.; Gange, S.J.; Rodrigo, A.G.; Upchurch, D.; Farzadegan, H.; Gupta, P.; Rinaldo, C.R.; Learn, G.H.; He, X., et al. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 1999, 73, 10489–10502. [PubMed]
92. Lee, H.Y.; Perelson, A.S.; Park, S.-C.; Leitner, T. Dynamic correlation between intrahost HIV-1 quasispecies evolution and disease progression. PLoS Comput. Biol. 2008, 4, e1000240. [CrossRef] [PubMed]
93. Wolbers, M.; Babiker, A.; Sabin, C.; Young, J.; Dorrucci, M.; Chêne, G.; Mussini, C.; Porter, K.; Bucher, H.C. Pretreatment CD4 cell slope and progression to AIDS or death in HIV-infected patients initiating antiretroviral therapy—The CASCADE collaboration: A collaboration of 23 cohort studies. PLoS Med. 2010, 7, e1000239. [CrossRef] [PubMed]
94. Park, S.Y.; Goeken, N.; Lee, H.J.; Bolan, R.; Dube, M.P.; Lee, H.Y. Developing high-throughput HIV incidence assay with pyrosequencing platform. J. Virol. 2014, 88, 2977–2990. [CrossRef] [PubMed]
95. Stramer, S.L.; Glynn, S.A.; Kleinman, S.H.; Strong, D.M.; Sally, C.; Wright, D.J.; Dodd, R.Y.; Busch, M.P. Detection of HIV-1 and HCV infections among antibody-negative blood donors by nucleic acid-amplification testing. N. Engl. J. Med. 2004, 351, 760–768. [CrossRef] [PubMed]
96. Hallett, T.B. Estimating the HIV incidence rate: Recent and future developments. Curr. Opin. HIV AIDS 2011, 6, 102–107. [CrossRef] [PubMed]
97. Yang, J.; Xia, X.; He, X.; Yang, S.; Ruan, Y.; Zhao, Q.; Wang, Z.; Shao, Y.; Pan, X. A new pattern-based method for identifying recent HIV-1 infections from the viral env sequence. Sci. Chin. Life Sci. 2012, 55, 328–335. [CrossRef] [PubMed]
98. Ypma, R.J.; van Ballegooijen, W.M.; Wallinga, J. Relating phylogenetic trees to transmission trees of infectious disease outbreaks. Genetics 2013, 195, 1055–1062. [CrossRef] [PubMed]
99. Eshleman, S.H.; Hudelson, S.E.; Redd, A.D.; Wang, L.; Debes, R.; Chen, Y.Q.; Martens, C.A.; Ricklefs, S.M.; Selig, E.J.; Porcella, S.F., et al. Analysis of genetic linkage of HIV from couples enrolled in the HIV Prevention Trials Network 052 trial. J. Infect. Dis. 2011, 204, 1918–1926. [CrossRef] [PubMed]
100. Cohen, M.S.; Chen, Y.Q.; McCauley, M.; Gamble, T.; Hosseinipour, M.C.; Kumarasamy, N.; Hakim, J.G.; Kumwenda, J.; Grinsztejn, B.; Pilotto, J.H., et al. Prevention of HIV-1 infection with early antiretroviral therapy. N. Engl. J. Med. 2011, 365, 493–505. [CrossRef] [PubMed]