Publication: Country Level Diversity of the HIV-1 Pandemic between 1990 and 2015
Issued Date
2021-01-01
Resource Type
ISSN
10985514
0022538X
0022538X
Other identifier(s)
2-s2.0-85099298902
Rights
Mahidol University
Rights Holder(s)
SCOPUS
Bibliographic Citation
Journal of Virology. Vol.95, No.2 (2021)
Suggested Citation
Joris Hemelaar, Shanghavie Loganathan, Ramyiadarsini Elangovan, Jason Yun, Leslie Dickson-Tetteh, Shona Kirtley, Alash’le G. Abimiku, Simon Agwale, Chris Archibald, Boaz Avidor, María Gabriela Barbás, Francoise Barre-Sinoussi, Banson Barugahare, El Hadj Belabbes, Silvia Bertagnolio, Deborah Birx, Aleksei F. Bobkov, James Brandful, Helba Bredell, Catherine A. Brennan, James Brooks, Marie Bruckova, Luigi Buonaguro, Franco Buonaguro, Stefano Buttò, Anne Buvé, Mary Campbell, Jean Carr, Alex Carrera, Manuel Gómez Carrillo, Connie Celum, Beth Chaplin, Macarthur Charles, Dimitrios Chatzidimitriou, Zhiwei Chen, Katsumi Chijiwa, David Cooper, Philip Cunningham, Anoumou Dagnra, Cillian F. de Gascun, Julia Del Amo, Elena Delgado, Ursula Dietrich, Dominic Dwyer, Dennis Ellenberger, Barbara Ensoli, Max Essex, Hervé Fleury, Peter N. Fonjungo, Vincent Foulongne, Deepak A. Gadkari, Feng Gao, Federico García, Roger Garsia, Guy Michel Gershy-Damet, Judith R. Glynn, Ruth Goodall, Zehava Grossman, Monick Lindenmeyer Guimarães, Beatrice Hahn, Raph L. Hamers, Osamah Hamouda, Ray Handema, Xiang He, Joshua Herbeck, David D. Ho, Africa Holguin, Mina Hosseinipour, Gillian Hunt, Masahiko Ito, Mohamed Ali Bel Hadj Kacem, Erin Kahle, Pontiano Kaleebu, Marcia Kalish, Adeeba Kamarulzaman, Chun Kang, Phyllis Kanki, Edward Karamov, Jean Claude Karasi, Kayitesi Kayitenkore, Tony Kelleher, Dwip Kitayaporn, Leondios G. Kostrikis, Claudia Kucherer, Claudia Lara, Thomas Leitner, Kirsi Liitsola, Jai Lingappa, Marek Linka, Ivette Lorenzana de Rivera, Vladimir Lukashov, Shlomo Maayan, Luzia Mayr, Francine McCutchan, Nicolas Meda, Elisabeth Menu, Fred Mhalu, Doreen Mloka, John L. Mokili, Brigitte Montes Country Level Diversity of the HIV-1 Pandemic between 1990 and 2015. Journal of Virology. Vol.95, No.2 (2021). doi:10.1128/JVI.01580-20 Retrieved from: https://repository.li.mahidol.ac.th/handle/20.500.14594/75811
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Title
Country Level Diversity of the HIV-1 Pandemic between 1990 and 2015
Author(s)
Joris Hemelaar
Shanghavie Loganathan
Ramyiadarsini Elangovan
Jason Yun
Leslie Dickson-Tetteh
Shona Kirtley
Alash’le G. Abimiku
Simon Agwale
Chris Archibald
Boaz Avidor
María Gabriela Barbás
Francoise Barre-Sinoussi
Banson Barugahare
El Hadj Belabbes
Silvia Bertagnolio
Deborah Birx
Aleksei F. Bobkov
James Brandful
Helba Bredell
Catherine A. Brennan
James Brooks
Marie Bruckova
Luigi Buonaguro
Franco Buonaguro
Stefano Buttò
Anne Buvé
Mary Campbell
Jean Carr
Alex Carrera
Manuel Gómez Carrillo
Connie Celum
Beth Chaplin
Macarthur Charles
Dimitrios Chatzidimitriou
Zhiwei Chen
Katsumi Chijiwa
David Cooper
Philip Cunningham
Anoumou Dagnra
Cillian F. de Gascun
Julia Del Amo
Elena Delgado
Ursula Dietrich
Dominic Dwyer
Dennis Ellenberger
Barbara Ensoli
Max Essex
Hervé Fleury
Peter N. Fonjungo
Vincent Foulongne
Deepak A. Gadkari
Feng Gao
Federico García
Roger Garsia
Guy Michel Gershy-Damet
Judith R. Glynn
Ruth Goodall
Zehava Grossman
Monick Lindenmeyer Guimarães
Beatrice Hahn
Raph L. Hamers
Osamah Hamouda
Ray Handema
Xiang He
Joshua Herbeck
David D. Ho
Africa Holguin
Mina Hosseinipour
Gillian Hunt
Masahiko Ito
Mohamed Ali Bel Hadj Kacem
Erin Kahle
Pontiano Kaleebu
Marcia Kalish
Adeeba Kamarulzaman
Chun Kang
Phyllis Kanki
Edward Karamov
Jean Claude Karasi
Kayitesi Kayitenkore
Tony Kelleher
Dwip Kitayaporn
Leondios G. Kostrikis
Claudia Kucherer
Claudia Lara
Thomas Leitner
Kirsi Liitsola
Jai Lingappa
Marek Linka
Ivette Lorenzana de Rivera
Vladimir Lukashov
Shlomo Maayan
Luzia Mayr
Francine McCutchan
Nicolas Meda
Elisabeth Menu
Fred Mhalu
Doreen Mloka
John L. Mokili
Brigitte Montes
Shanghavie Loganathan
Ramyiadarsini Elangovan
Jason Yun
Leslie Dickson-Tetteh
Shona Kirtley
Alash’le G. Abimiku
Simon Agwale
Chris Archibald
Boaz Avidor
María Gabriela Barbás
Francoise Barre-Sinoussi
Banson Barugahare
El Hadj Belabbes
Silvia Bertagnolio
Deborah Birx
Aleksei F. Bobkov
James Brandful
Helba Bredell
Catherine A. Brennan
James Brooks
Marie Bruckova
Luigi Buonaguro
Franco Buonaguro
Stefano Buttò
Anne Buvé
Mary Campbell
Jean Carr
Alex Carrera
Manuel Gómez Carrillo
Connie Celum
Beth Chaplin
Macarthur Charles
Dimitrios Chatzidimitriou
Zhiwei Chen
Katsumi Chijiwa
David Cooper
Philip Cunningham
Anoumou Dagnra
Cillian F. de Gascun
Julia Del Amo
Elena Delgado
Ursula Dietrich
Dominic Dwyer
Dennis Ellenberger
Barbara Ensoli
Max Essex
Hervé Fleury
Peter N. Fonjungo
Vincent Foulongne
Deepak A. Gadkari
Feng Gao
Federico García
Roger Garsia
Guy Michel Gershy-Damet
Judith R. Glynn
Ruth Goodall
Zehava Grossman
Monick Lindenmeyer Guimarães
Beatrice Hahn
Raph L. Hamers
Osamah Hamouda
Ray Handema
Xiang He
Joshua Herbeck
David D. Ho
Africa Holguin
Mina Hosseinipour
Gillian Hunt
Masahiko Ito
Mohamed Ali Bel Hadj Kacem
Erin Kahle
Pontiano Kaleebu
Marcia Kalish
Adeeba Kamarulzaman
Chun Kang
Phyllis Kanki
Edward Karamov
Jean Claude Karasi
Kayitesi Kayitenkore
Tony Kelleher
Dwip Kitayaporn
Leondios G. Kostrikis
Claudia Kucherer
Claudia Lara
Thomas Leitner
Kirsi Liitsola
Jai Lingappa
Marek Linka
Ivette Lorenzana de Rivera
Vladimir Lukashov
Shlomo Maayan
Luzia Mayr
Francine McCutchan
Nicolas Meda
Elisabeth Menu
Fred Mhalu
Doreen Mloka
John L. Mokili
Brigitte Montes
Other Contributor(s)
Groupe d’étude Haïtien sur le Sarcome de Kaposi et les Infections Opportunistes
National Center for AIDS/STD Control and Prevention
Amsterdam Institute for Global Health and Development
Chinese Academy of Medical Sciences & Peking Union Medical College
Duke University Medical Center
Université de Bordeaux
Muhimbili University of Health and Allied Sciences
Universidad Nacional Autónoma de Honduras
University of Lome
Georg-Speyer-Haus
Centre MURAZ
Uganda Virus Research Institute
Uganda Ministry of Health
D.I. Ivanovsky Institute of Virology
N. F. Gamaleya Institute of Epidemiology and Microbiology, Ministry of Health of the Russian Federation
Institut Pasteur - Alger
Université de Tunis El Manar, Hôpital Charles Nicolle
Harvard T.H. Chan School of Public Health
Centre Hospitalier Universitaire de Montpellier
National Institute for Communicable Diseases
London School of Hygiene & Tropical Medicine
Vanderbilt University Medical Center
Universiti Malaya
Prins Leopold Instituut voor Tropische Geneeskunde
University of Washington School of Medicine
Universidad de Granada
Agence de la santé publique du Canada
The University of Edinburgh
Organisation Mondiale de la Santé
Rockefeller University
The Kirby Institute
Fundacao Oswaldo Cruz
St. Vincent's Hospital Sydney
The University of North Carolina at Chapel Hill
NYU Grossman School of Medicine
University College London
Kyushu University Hospital
Centers for Disease Control and Prevention
Hospital Ramon y Cajal
Karolinska Universitetssjukhuset
Royal Prince Alfred Hospital
University of Ghana
Istituto Nazionale Tumori IRCCS - Fondazione G Pascale, Napoli
Robert Koch Institut
Aristotle University of Thessaloniki
University of Maryland, Baltimore (UMB)
HJF
Seoul National University
National Institute of Public Health Prague
Istituto Superiore Di Sanita
University of Yamanashi
Tel Aviv Sourasky Medical Center
University of Pennsylvania
Los Alamos National Laboratory
University College Dublin
Westmead Hospital
University of Oxford Medical Sciences Division
Universiteit van Amsterdam
Emory University School of Medicine
National AIDS Research Institute India
Israel Ministry of Health
Institut Pasteur, Paris
Abbott Laboratories
Instituto de Salud Carlos III
Universidad de Buenos Aires
University of Cape Town
Hadassah University Medical Centre
Office of the Global AIDS Coordinator
Gede Foundation
National Institute for Health
National Reference Laboratory
Ministerio de Salud
HIV/AIDS Collaboration
National Center for AIDS/STD Control and Prevention
Amsterdam Institute for Global Health and Development
Chinese Academy of Medical Sciences & Peking Union Medical College
Duke University Medical Center
Université de Bordeaux
Muhimbili University of Health and Allied Sciences
Universidad Nacional Autónoma de Honduras
University of Lome
Georg-Speyer-Haus
Centre MURAZ
Uganda Virus Research Institute
Uganda Ministry of Health
D.I. Ivanovsky Institute of Virology
N. F. Gamaleya Institute of Epidemiology and Microbiology, Ministry of Health of the Russian Federation
Institut Pasteur - Alger
Université de Tunis El Manar, Hôpital Charles Nicolle
Harvard T.H. Chan School of Public Health
Centre Hospitalier Universitaire de Montpellier
National Institute for Communicable Diseases
London School of Hygiene & Tropical Medicine
Vanderbilt University Medical Center
Universiti Malaya
Prins Leopold Instituut voor Tropische Geneeskunde
University of Washington School of Medicine
Universidad de Granada
Agence de la santé publique du Canada
The University of Edinburgh
Organisation Mondiale de la Santé
Rockefeller University
The Kirby Institute
Fundacao Oswaldo Cruz
St. Vincent's Hospital Sydney
The University of North Carolina at Chapel Hill
NYU Grossman School of Medicine
University College London
Kyushu University Hospital
Centers for Disease Control and Prevention
Hospital Ramon y Cajal
Karolinska Universitetssjukhuset
Royal Prince Alfred Hospital
University of Ghana
Istituto Nazionale Tumori IRCCS - Fondazione G Pascale, Napoli
Robert Koch Institut
Aristotle University of Thessaloniki
University of Maryland, Baltimore (UMB)
HJF
Seoul National University
National Institute of Public Health Prague
Istituto Superiore Di Sanita
University of Yamanashi
Tel Aviv Sourasky Medical Center
University of Pennsylvania
Los Alamos National Laboratory
University College Dublin
Westmead Hospital
University of Oxford Medical Sciences Division
Universiteit van Amsterdam
Emory University School of Medicine
National AIDS Research Institute India
Israel Ministry of Health
Institut Pasteur, Paris
Abbott Laboratories
Instituto de Salud Carlos III
Universidad de Buenos Aires
University of Cape Town
Hadassah University Medical Centre
Office of the Global AIDS Coordinator
Gede Foundation
National Institute for Health
National Reference Laboratory
Ministerio de Salud
HIV/AIDS Collaboration
Abstract
The global diversity of HIV forms a major challenge to the development of an HIV vaccine, as well as diagnostic, drug resistance, and viral load assays, which are essential to reaching the UNAIDS 90:90:90 targets. We sought to determine country level HIV-1 diversity globally between 1990 and 2015. We assembled a global HIV-1 molecular epidemiology database through a systematic literature search and a global survey. We searched PubMed, EMBASE (Ovid), CINAHL (Ebscohost), and Global Health (Ovid) for HIV-1 subtyping studies published from 1 January 1990 to 31 December 2015. We collected additional unpublished data through a global survey of experts. Prevalence studies with original HIV-1 subtyping data collected between 1990 and 2015 were included. This resulted in a database with 383,519 subtyped HIV-1 samples from 116 countries over four time periods (1990 to 1999, 2000 to 2004, 2005 to 2009, and 2010 to 2015). We analyzed country-specific numbers of distinct HIV-1 subtypes, circulating recombinant forms (CRFs), and unique recombinant forms (URFs) in each time period. We also analyzed country-specific proportions of infections due to HIV-1 recombinants, CRFs, and URFs and calculated the Shannon diversity index for each country. Finally, we analyzed global temporal trends in each of these measures of HIV-1 diversity. We found extremely wide variation in complexity of country level HIV diversity around the world. Central African countries such as Chad, Democratic Republic of the Congo, Angola, and Republic of the Congo have the most diverse HIV epidemics. The number of distinct HIV-1 subtypes and recombinants was greatest in Western Europe (Spain and France) and North America (United States) (up to 39 distinct HIV-1 variants in Spain). The proportion of HIV-1 infections due to recombinants was highest in Southeast Asia (>95% of infections in Viet Nam, Cambodia, and Thailand), China, and West and Central Africa, mainly due to high proportions of CRF01_AE and CRF02_AG. Other CRFs played major roles (>75% of HIV-1 infections) in Estonia (CRF06_cpx), Iran (CRF35_AD), and Algeria (CRF06_cpx). The highest proportions of URFs (>30%) were found in Myanmar, Republic of the Congo, and Argentina. Global temporal analysis showed consistent increases over time in country level numbers of distinct HIV-1 variants and proportions of CRFs and URFs, leading to increases in country level HIV-1 diversity. Our study provides epidemiological evidence that the HIV pandemic is diversifying at country level and highlights the increasing challenge to prevention and treatment efforts. HIV-1 molecular epidemiological surveillance needs to be continued and improved. IMPORTANCE This is the first study to analyze global country level HIV-1 diversity from 1990 to 2015. We found extremely wide variation in complexity of country level HIV diversity around the world. Central African countries have the most diverse HIV epidemics. The number of distinct HIV-1 subtypes and recombinants was greatest in Western Europe and North America. The proportion of HIV-1 infections due to recombinants was highest in South-East Asia, China, and West and Central Africa. The highest proportions of URFs were found in Myanmar, Republic of the Congo, and Argentina. Our study provides epidemiological evidence that the HIV pandemic is diversifying at country level and highlights the increasing challenge to HIV vaccine development and diagnostic, drug resistance, and viral load assays.