HIV-1 subtype B spread through cross-border clusters in the Balkans: a molecular analysis in view of incidence trends.
Journal
AIDS (London, England)
ISSN: 1473-5571
Titre abrégé: AIDS
Pays: England
ID NLM: 8710219
Informations de publication
Date de publication:
01 01 2023
01 01 2023
Historique:
pubmed:
22
9
2022
medline:
15
12
2022
entrez:
21
9
2022
Statut:
ppublish
Résumé
To analyze phylogenetic relations and assess the role of cross-border clusters in the spread of HIV-1 subtype B across the Balkans, given the general trends of new HIV diagnoses in seven Balkan countries. Retrospective phylogenetic and trend analysis. In-depth phylogenetic, phylodynamic and phylogeographic analysis performed on 2415 HIV-1 subtype B sequences from 1999 to 2019 using maximal likelihood and Bayesian methods. The joinpoint regression analysis of new HIV diagnoses by country and modes of transmission using 2004-2019 ECDC data. Ninety-three HIV-1 Subtype B transmission clusters (68% of studied sequences) were detected of which four cross-border clusters (11% of studied sequences). Phylodynamic analysis showed activity of cross-border clusters up until the mid-2000s, with a subsequent stationary growth phase. Phylogeography analyses revealed reciprocal spread patterns between Serbia, Slovenia and Montenegro and several introductions to Romania from these countries and Croatia. The joinpoint analysis revealed a reduction in new HIV diagnoses in Romania, Greece and Slovenia, whereas an increase in Serbia, Bulgaria, Croatia and Montenegro, predominantly among MSM. Differing trends of new HIV diagnoses in the Balkans mirror differences in preventive policies implemented in participating countries. Regional spread of HIV within the countries of former Yugoslavia has continued to play an important role even after country break-up, whereas the spread of subtype B through multiple introductions to Romania suggested the changing pattern of travel and migration linked to European integration of Balkan countries in the early 2000s.
Identifiants
pubmed: 36129113
doi: 10.1097/QAD.0000000000003394
pii: 00002030-202301010-00013
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
125-135Informations de copyright
Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.
Références
UN Joint Programme on HIV/AIDS (UNAIDS). The Reference Data, 2020. Available at: https://www.unaids.org/en/resources/documents/2020/unaids-data [Accessed 10 August 2022].
European Centre for Disease Prevention and Control/WHO Regional Office for Europe. HIV/AIDS Surveillance in Europe 2020 – 2019 data. Available at: https://www.ecdc.europa.eu/en/publications-data/hivaids-surveillance-europe-2020-2019-data [Accessed 10 August 2022].
Gökengin D, Oprea C, Uysal S, Begovac J. The growing HIV epidemic in Central Europe: a neglected issue? . J Virus Erad 2016; 2:156–161.
Stanojevic M, Alexiev I, Beshkov D, Gökengin D, Mezei M, Minarovits J, et al. HIV-1 molecular epidemiology in the Balkans: a melting pot for high genetic diversity . AIDS Rev 2012; 14:28–36.
Beloukas A, Psarris A, Giannelou P, Kostaki E, Hatzakis A, Paraskevis D. Molecular epidemiology of HIV-1 infection in Europe: an overview . Infect Genet Evol 2016; 46:180–189.
Alexiev IM, Campbell E, Knyazev S, Pan Y, Grigorova L, Dimitrova R, et al. Molecular epidemiology of the HIV-1 subtype B sub-epidemic in Bulgaria . Viruses 2020; 12:441.
Paraschiv S, Otelea D, Batan I, Baicus C, Magiorkinis G, Paraskevis D. Molecular typing of the recently expanding subtype B HIV-1 epidemic in Romania: evidence for local spread among MSMs in Bucharest area . Infect Genet Evol 2012; 12:1052–1057.
Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint regression with applications to cancer rates . Stat Med 2000; 19:335–351.
Cayuela A, Rodríguez-Domínguez S, López-Campos JL, Otero Candelera R, Rodríguez Matutes C. Joinpoint regression analysis of lung cancer mortality, Andalusia 1975-2000 . Ann Oncol 2004; 15:793–796.
WHO. HIVResNet HIV drug resistance laboratory operational framework, second edition . Geneva: World Health Organization; 2020.
Struck D, Lawyer G, Ternes AM, Schmit JC, Bercoff DP. COMET: adaptive context-based modeling for ultrafast HIV-1 subtype identification . Nucleic Acids Res 2014; 42:e144.
Peña ACP, Faria NR, Imbrechts S, Libin P, Abecasis AB, Deforche K, et al. Automated subtyping of HIV-1 genetic sequences for clinical and surveillance purposes: performance evaluation of the new REGA version 3 and seven other tools . Infect Genet Evol 2013; 19:337–348.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms . Mol Biol Evol 2018; 35:1547–1549.
Wensing AM, Calvez V, Günthard HF, Johnson VA, Paredes R, Pillay D, et al. 2017 update of the drug resistance mutations in HIV-1 . Top Antivir Med 2016; 24:132–133.
Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis . Nucleic Acids Res 2016; 44:W232–W235.
Posada D. Selection of models of DNA evolution with jModelTest . Methods Mol Biol 2009; 537:93–112.
Novitsky V, Steingrimsson JA, Howison M, Gillani FS, Li Y, Manne A, et al. Empirical comparison of analytical approaches for identifying molecular HIV-1 clusters . Sci Rep 2020; 10:18547.
Jovanović L, Šiljić M, Ćirković V, Salemović D, Pešić-Pavlović I, Todorović M, et al. Exploring evolutionary and transmission dynamics of HIV epidemic in Serbia: bridging socio-demographic with phylogenetic approach . Front Microbiol 2019; 10:287.
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation . Mol Biol Evol 2018; 35:518–522.
Kostaki E, Magiorkinis G, Psichogiou M, Flampouris A, Iliopoulos P, Papachristou E, et al. Detailed molecular surveillance of the HIV-1 outbreak among people who inject drugs (PWID) in Athens during a period of four years . Curr HIV Res 2017; 15:396–404.
Paraskevis D, Kostaki E, Gargalianos P, Xylomenos G, Lazanas M, Chini M, et al. Transmission dynamics of HIV-1 drug resistance among treatment-naïve individuals in Greece: the added value of molecular epidemiology to public health . Genes 2017; 8:322.
Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, et al. The EMBL-EBI search and sequence analysis tools APIs in 2019 . Nucleic Acids Res 2019; 47:W636–W641.
Paraskevis D, Beloukas A, Stasinos K, Pantazis N, de Mendoza C, Bannert N, et al. HIV-1 molecular transmission clusters in nine European countries and Canada: association with demographic and clinical factors . BMC Med 2019; 17:4.
Drummond AJ, Rambaut A, Shapiro B, Pybus OG. Bayesian coalescent inference of past population dynamics from molecular sequences . Mol Biol Evol 2005; 22:1185–1192.
Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7 . Mol Biol Evol 2012; 29:1969–1973.
Veo C, Della Ventura C, Moreno A, Rovida F, Percivalle E, Canziani S, et al. Evolutionary dynamics of the Lineage 2 West Nile Virus that caused the largest European epidemic: Italy 2011-2018 . Viruses 2019; 11:814.
Stadler T, Kühnert D, Bonhoeffer S, Drummond AJ. Birth-death skyline plot reveals temporal changes of epidemic spread in HIV and hepatitis C virus (HCV) . Proc Natl Acad Sci U S A 2013; 110:228–233.
Siljic M, Salemovic D, Jevtovic D, Pesic-Pavlovic I, Zerjav S, Nikolic V, et al. Molecular typing of the local HIV-1 epidemic in Serbia . Infect Genet Evol 2013; 19:378–385.
Barido-Sottani J, Bošková V, Plessis LD, Kühnert D, Magnus C, Mitov V, et al. Taming the BEAST-A Community Teaching Material Resource for BEAST 2 . Syst Biol 2018; 67:170.e26–174.e26.
Bbosa N, Ssemwanga D, Nsubuga RN, Salazar-Gonzalez JF, Salazar MG, Nanyonjo M, et al. Phylogeography of HIV-1 suggests that Ugandan fishing communities are a sink for, not a source of, virus from general populations . Sci Rep 2019; 9:1051.
Pérez-Parra S, Chueca N, Álvarez M, Pasquau J, Omar M, Collado A, et al. Phylodynamic and phylogeographic profiles of subtype B HIV-1 epidemics in South Spain . PLoS One 2016; 11:e0168099.
Bielejec F, Baele G, Vrancken B, Suchard MA, Rambaut A, Lemey P. SpreaD3: interactive visualization of spatiotemporal history and trait evolutionary processes . Mol Biol Evol 2016; 33:2167–2169.
Paraskevis D, Pybus O, Magiorkinis G, Hatzakis A, Wensing AM, van de Vijver DA, et al. Tracing the HIV-1 subtype B mobility in Europe: a phylogeographic approach . Retrovirology 2009; 6:49.
Kostaki EG, Gova M, Adamis G, Xylomenos G, Chini M, Mangafas N, et al. A nationwide study about the dispersal patterns of the predominant HIV-1 subtypes A1 and B in Greece: inference of the molecular transmission clusters . Viruses 2020; 12:1183.
Billings E, Heipertz RA, Varleva T, Sanders-Buell E, O'Sullivan AM, et al. HIV-1 genetic diversity and demographic characteristics in Bulgaria . PLoS One 2019; 14:e0217063.
Alexiev I, Shankar A, Wensing AM, Beshkov D, Elenkov I, Stoycheva M, et al. Low HIV-1 transmitted drug resistance in Bulgaria against a background of high clade diversity . J Antimicrob Chemother 2015; 70:1874–1880.
Oroz M, Begovac J, Planinić A, Rokić F, Lunar MM, Zorec TM, et al. Analysis of HIV-1 diversity, primary drug resistance and transmission networks in Croatia . Sci Rep 2019; 9:17307.
Grgic I, Lepej SZ, Lunar MM, Poljak M, Vince A, Vrakela IB, et al. The prevalence of transmitted drug resistance in newly diagnosed HIV-infected individuals in Croatia: the role of transmission clusters of men who have sex with men carrying the T215S surveillance drug resistance mutation . AIDS Res Hum Retrovirus 2013; 29:329–336.
Lunar MM, Židovec Lepej S, Tomažič J, Vovko TD, Pečavar B, Turel G, et al. HIV-1 transmitted drug resistance in Slovenia and its impact on predicted treatment effectiveness: 2011–2016 update . PLoS One 2018; 13:e0196670.
European Centre for Disease Prevention and Control. HIV: Combination prevention. Monitoring implementation of the Dublin Declaration on partnership to fight HIV/AIDS in Europe and Central Asia: 2018 progress report . Stockholm: ECDC; 2020
Nikolopoulos GK, Pavlitina E, Muth SQ, Schneider J, Psichogiou M, Williams LD, et al. A network intervention that locates and intervenes with recently HIV-infected persons: the Transmission Reduction Intervention Project (TRIP) . Sci Rep 2016; 6:38100.
National Aids Committee, Department For Aids Monitoring From Romania. Statistic data on HIV/AIDS infection in Romania. CNLAS; Bucharest: 2013. Available at: http://www.cnlas.ro/date-statistice.html .
Temereanca A, Oprea C, Wertheim JO, Ianache I, Ceausu E, Cernescu C, et al. HIV transmission clusters among injecting drug users in Romania . Rom Biotechnol Lett 2017; 22:12307–12315.
Gokengin D, Oprea C, Begovac J, Horban A, Zeka AN, Sedlacek D, et al. HIV care in Central and Eastern Europe: how close are we to the target? . Int J Infect Dis 2018; 70:121–130.
Frentz D, Wensing AM, Albert J, Paraskevis D, Abecasis AB, Hamouda O, et al. Limited cross-border infections in patients newly diagnosed with HIV in Europe . Retrovirology 2013; 10:36.
Hauser A, Hofmann A, Meixenberger K, Altmann B, Hanke K, Bremer V, et al. Increasing proportions of HIV-1 non-B subtypes and of NNRTI resistance between 2013 and 2016 in Germany: results from the national molecular surveillance of new HIV-diagnoses . PLoS One 2018; 13:e0206234.
Magiorkinis G, Angelis K, Mamais I, Katzourakis A, Hatzakis A, Albert J, et al. The global spread of HIV-1 subtype B epidemic . Infect Genet Evol 2016; 46:169–179.
Michalopoulos LM, Ncube N, Simona SJ, Kansankala B, Sinkala E, Raidoo J. A qualitative study of migrant-related stressors, psychosocial outcomes and HIV risk behaviour among truck drivers in Zambia . Afr J AIDS Res 2016; 15:219–226.
Botão C, Horth RZ, Frank H, Cummings B, Inguane C, Sathane I, et al. Prevalence of HIV and associated risk factors among long distance truck drivers in Inchope, Mozambique, 2012 . AIDS Behav 2016; 20:811–820.
Jochelson K, Mothibeli M, Leger JP. Human immunodeficiency virus and migrant labor in South Africa . Int J Health Serv 1991; 21:157–173.
Abecasis AB, Wensing AM, Paraskevis D, Vercauteren J, Theys K, Van de Vijver DA, et al. HIV-1 subtype distribution and its demographic determinants in newly diagnosed patients in Europe suggest highly compartmentalized epidemics . Retrovirology 2013; 10:7.
Ragonnet-Cronin ML, Shilaih M, Günthard HF, Hodcroft EB, Böni J, Fearnhill E, et al. A direct comparison of two densely sampled HIV epidemics: the UK and Switzerland . Sci Rep 2016; 6:32251.
Delgado E, Cuevas MT, Domínguez F, Vega Y, Cabello M, Fernández-García A, et al. Phylogeny and phylogeography of a recent HIV-1 subtype F outbreak among men who have sex with men in Spain deriving from a cluster with a wide geographic circulation in Western Europe . PLoS One 2015; 10:e0143325.
Hassan AS, Pybus OG, Sanders EJ, Albert J, Esbjörnsson J. Defining HIV-1 transmission clusters based on sequence data . AIDS 2017; 31:1211–1222.
Hué S, Clewley JP, Cane PA, Pillay D. HIV-1 pol gene variation is sufficient for reconstruction of transmissions in the era of antiretroviral therapy . AIDS 2004; 18:719–728.
Lemey P, Vandamme AM. Exploring full-genome sequences for phylogenetic support of HIV-1 transmission events . AIDS 2005; 19:1551–1552.
Kaye M, Chibo D, Birch C. Phylogenetic investigation of transmission pathways of drug-resistant HIV-1 utilizing pol sequences derived from resistance genotyping . J Acquir Immune Defic Syndr 2008; 49:9–16.