Migration, hotspots, and dispersal of HIV infection in Rakai, Uganda.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
20 02 2020
Historique:
received: 09 07 2018
accepted: 18 01 2020
entrez: 22 2 2020
pubmed: 23 2 2020
medline: 6 5 2020
Statut: epublish

Résumé

HIV prevalence varies markedly throughout Africa, and it is often presumed areas of higher HIV prevalence (i.e., hotspots) serve as sources of infection to neighboring areas of lower prevalence. However, the small-scale geography of migration networks and movement of HIV-positive individuals between communities is poorly understood. Here, we use population-based data from ~22,000 persons of known HIV status to characterize migratory patterns and their relationship to HIV among 38 communities in Rakai, Uganda with HIV prevalence ranging from 9 to 43%. We find that migrants moving into hotspots had significantly higher HIV prevalence than migrants moving elsewhere, but out-migration from hotspots was geographically dispersed, contributing minimally to HIV burden in destination locations. Our results challenge the assumption that high prevalence hotspots are drivers of transmission in regional epidemics, instead suggesting that migrants with high HIV prevalence, particularly women, selectively migrate to these areas.

Identifiants

pubmed: 32080169
doi: 10.1038/s41467-020-14636-y
pii: 10.1038/s41467-020-14636-y
pmc: PMC7033206
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

976

Subventions

Organisme : NIAID NIH HHS
ID : K01 AI125086
Pays : United States
Organisme : NIAID NIH HHS
ID : P30 AI094189
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI143333
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD091003
Pays : United States

Références

Gushulak, B. D. & MacPherson, D. W. Globalization of infectious diseases: the impact of migration. Clin. Infect. Dis. 38, 1742–1748 (2004).
doi: 10.1086/421268 pubmed: 15227621
Tatem, A. J., Rogers, D. J. & Hay, S. I. Global transport networks and infectious disease spread. Adv. Parasitol. 62, 293–343 (2006).
doi: 10.1016/S0065-308X(05)62009-X pubmed: 16647974 pmcid: 3145127
Mokdad, A. H. et al. Global burden of diseases, injuries, and risk factors for young people’s health during 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 387, 2383–2401 (2016).
doi: 10.1016/S0140-6736(16)00648-6 pubmed: 27174305
Quinn, T. C. Population migration and the spread of types 1 and 2 human immunodeficiency viruses. Proc. Natl Acad. Sci. USA 91, 2407–2414 (1994).
doi: 10.1073/pnas.91.7.2407 pubmed: 8146131
McKinnon, L. R. & Karim, Q. A. Factors driving the HIV epidemic in Southern Africa. Curr. HIV/AIDS Rep. 13, 158–169 (2016).
doi: 10.1007/s11904-016-0314-z pubmed: 27137200
Tanser, F., Barnighausen, T., Vandormael, A. & Dobra, A. HIV treatment cascade in migrants and mobile populations. Curr. Opin. HIV. AIDS. 10, 430–438 (2015).
doi: 10.1097/COH.0000000000000192 pubmed: 26352396
Lurie, M. N. & Williams, B. G. Migration and health in Southern Africa: 100 years and still circulating. Health Psychol. Behav. Med. 2, 34–40 (2014).
doi: 10.1080/21642850.2013.866898 pubmed: 24653964 pmcid: 3956074
UNAIDS. UNAIDS report of the global AIDS epidemic 2013. (2013).
Nunn, A. J., Wagner, H. U., Kamali, A., Kengeya-Kayondo, J. F. & Mulder, D. W. Migration and HIV-1 seroprevalence in a rural Ugandan population. AIDS 9, 503–506 (1995).
doi: 10.1097/00002030-199509050-00013 pubmed: 7639976
Camlin, C. S. et al. Gender, migration and HIV in rural KwaZulu-Natal, South Africa. PLoS ONE 5, e11539 (2010).
doi: 10.1371/journal.pone.0011539 pubmed: 20634965 pmcid: 2902532
McGrath, N., Eaton, J. W., Newell, M. L. & Hosegood, V. Migration, sexual behaviour, and HIV risk: a general population cohort in rural South Africa. Lancet HIV. 2, e252–e259 (2015).
doi: 10.1016/S2352-3018(15)00045-4 pubmed: 26280016 pmcid: 4533230
Welz, T. et al. Continued very high prevalence of HIV infection in rural KwaZulu-Natal, South Africa: a population-based longitudinal study. AIDS 21, 1467–1472 (2007).
doi: 10.1097/QAD.0b013e3280ef6af2 pubmed: 17589193
Anglewicz, P. Migration, marital change, and HIV infection in Malawi. Demography 49, 239–265 (2012).
doi: 10.1007/s13524-011-0072-x pubmed: 22109083 pmcid: 3787875
Lurie, M. N. et al. The impact of migration on HIV-1 transmission in South Africa: a study of migrant and nonmigrant men and their partners. Sex. Transm. Dis. 30, 149–156 (2003).
doi: 10.1097/00007435-200302000-00011 pubmed: 12567174
Anglewicz, P., VanLandingham, M., Manda-Taylor, L. & Kohler, H. P. Migration and HIV infection in Malawi. AIDS 30, 2099–2105 (2016).
doi: 10.1097/QAD.0000000000001150 pubmed: 27163708 pmcid: 4965311
Sartorius, B., Kahn, K., Collinson, M. A., Sartorius, K. & Tollman, S. M. Dying in their prime: determinants and space-time risk of adult mortality in rural South Africa. Geospat Health 7, 237–249 (2013).
doi: 10.4081/gh.2013.83 pubmed: 23733287 pmcid: 3725424
Levira, F., Todd, J. & Masanja, H. Coming home to die? The association between migration and mortality in rural Tanzania before and after ART scale-up. Glob. Health Action 7, 22956 (2014).
doi: 10.3402/gha.v7.22956 pubmed: 24857612
Mee, P. et al. Determinants of the risk of dying of HIV/AIDS in a rural South African community over the period of the decentralised roll-out of antiretroviral therapy: a longitudinal study. Glob. Health Action 7, 24826 (2014).
doi: 10.3402/gha.v7.24826 pubmed: 25416322
GBD 2017 HIV collaborators. Global, regional, and national incidence, prevalence, and mortality of HIV, 1980-2017, and forecasts to 2030, for 195 countries and territories: a systematic analysis for the Global Burden of Diseases, Injuries, and Risk Factors Study 2017. Lancet HIV. 6, e831–e859 (2019).
doi: 10.1016/S2352-3018(19)30196-1 pmcid: 6934077
Havlir, D. V. et al. HIV testing and treatment with the use of a community health approach in Rural Africa. N. Engl. J. Med. 381, 219–229 (2019).
doi: 10.1056/NEJMoa1809866 pubmed: 31314966 pmcid: 6748325
Petersen, M. et al. Association of implementation of a universal testing and treatment intervention with HIV diagnosis, receipt of antiretroviral therapy, and viral suppression in East Africa. JAMA 317, 2196–2206 (2017).
doi: 10.1001/jama.2017.5705 pubmed: 28586888 pmcid: 5734234
Makhema, J. et al. Universal testing, expanded treatment, and incidence of HIV infection in Botswana. N. Engl. J. Med. 381, 230–242 (2019).
doi: 10.1056/NEJMoa1812281 pubmed: 31314967 pmcid: 6800102
Hayes, R. J. et al. Effect of universal testing and treatment on HIV incidence - HPTN 071 (PopART). N. Engl. J. Med. 381, 207–218 (2019).
doi: 10.1056/NEJMoa1814556 pubmed: 31314965 pmcid: 6587177
Abdool Karim, S. S. HIV-1 epidemic control - insights from test-and-treat trials. N. Engl. J. Med. 381, 286–288 (2019).
doi: 10.1056/NEJMe1907279 pubmed: 31314975
Global Burden of Disease Health Financing Collaborator Network. Spending on health and HIV/AIDS: domestic health spending and development assistance in 188 countries, 1995-2015. Lancet 391, 1799–1829 (2018).
doi: 10.1016/S0140-6736(18)30698-6
Cuadros, D. F. et al. Towards UNAIDS Fast-Track goals: targeting priority geographic areas for HIV prevention and care in Zimbabwe. AIDS 33, 305–314 (2019).
doi: 10.1097/QAD.0000000000002052 pubmed: 30557161
Kelly, S. L. et al. The global Optima HIV allocative efficiency model: targeting resources in efforts to end AIDS. Lancet HIV. 5, e190–e198 (2018).
doi: 10.1016/S2352-3018(18)30024-9 pubmed: 29540265
Dwyer-Lindgren, L. et al. Mapping HIV prevalence in sub-Saharan Africa between 2000 and 2017. Nature 570, 189–193 (2019).
doi: 10.1038/s41586-019-1200-9 pubmed: 31092927 pmcid: 6601349
Anderson, S. J. et al. Maximising the effect of combination HIV prevention through prioritisation of the people and places in greatest need: a modelling study. Lancet 384, 249–256 (2014).
doi: 10.1016/S0140-6736(14)61053-9 pubmed: 25042235
Cuadros, D. F., Graf, T., Oliviera, T., Bärnighausen, T. & Tanser, F. Assessing the role of geographical HIV hotspots in the spread of the epidemic. in Proc. Conference on Retroviruses and Opportunistic Infections (International AIDS Society is the publisher 2018).
Tanser, F., Barnighausen, T., Dobra, A. & Sartorius, B. Identifying ‘corridors of HIV transmission’ in a severely affected rural South African population: a case for a shift toward targeted prevention strategies. Int. J. Epidemiol. 47, 537–549 (2018).
doi: 10.1093/ije/dyx257 pubmed: 29300904
Chang, L. W. et al. Heterogeneity of the HIV epidemic in agrarian, trading, and fishing communities in Rakai, Uganda: an observational epidemiological study. Lancet HIV 3, e388–e396 (2016).
doi: 10.1016/S2352-3018(16)30034-0 pubmed: 27470029 pmcid: 4973864
Opio, A., Muyonga, M., Mulumba, N. & Cameron, D. W. HIV Infection in Fishing Communities of Lake Victoria Basin of Uganda – A Cross-Sectional Sero-Behavioral Survey. PLoS ONE, 8, e70770 (2013).
Woolhouse, M. E. et al. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc. Natl Acad. Sci. USA 94, 338–342 (1997).
doi: 10.1073/pnas.94.1.338 pubmed: 8990210
Azman, A. S. et al. Urban cholera transmission hotspots and their implications for reactive vaccination: evidence from Bissau city, Guinea Bissau. PLoS Negl. Trop. Dis. 6, e1901 (2012).
doi: 10.1371/journal.pntd.0001901 pubmed: 23145204 pmcid: 3493445
Azman, A. S. & Lessler, J. Reactive vaccination in the presence of disease hotspots. Proc. Biol. Sci. 282, 20141341 (2015).
doi: 10.1098/rspb.2014.1341 pubmed: 25392464 pmcid: 4262159
Dushoff, J. et al. Vaccinating to protect a vulnerable subpopulation. PLoS Med. 4, e174 (2007).
doi: 10.1371/journal.pmed.0040174 pubmed: 17518515 pmcid: 1872043
Grabowski, M. K. et al. The role of viral introductions in sustaining community-based HIV epidemics in rural Uganda: evidence from spatial clustering, phylogenetics, and egocentric transmission models. PLoS Med. 11, e1001610 (2014).
doi: 10.1371/journal.pmed.1001610 pubmed: 24595023 pmcid: 3942316
Grabowski, M. K. et al. HIV prevention efforts and incidence of HIV in Uganda. N. Engl. J. Med. 377, 2154–2166 (2017).
doi: 10.1056/NEJMoa1702150 pubmed: 29171817 pmcid: 5627523
Serwadda, D. et al. Slim disease: a new disease in Uganda and its association with HTLV-III infection. Lancet 2, 849–852 (1985).
doi: 10.1016/S0140-6736(85)90122-9 pubmed: 2864575
Uganda AIDS Commission. Consolidated Mid-Term Review Report of the National HIV/AIDS Strategic Plan 2011/12-2014/15. (2014).
Ratmann, O. et al. Quantifying HIV transmission flow between high-prevalence hotspots and surrounding communities: a population-based study in Rakai, Uganda. Lancet HIV.  https://doi.org/10.1016/S2352-3018(19)30378-9  (2020).
Bbosa, N. et al. Phylogeography of HIV-1 suggests that Ugandan fishing communities are a sink for, not a source of, virus from general populations. Scientific Reports, 9, 1051 (2019).
Lubega, M. et al. Risk denial and socio-economic factors related to high HIV transmission in a fishing community in Rakai, Uganda: a qualitative study. PLoS ONE 10, e0132740 (2015).
doi: 10.1371/journal.pone.0132740 pubmed: 26309179 pmcid: 4550390
Camlin, C. S., Kwena, Z. A. & Dworkin, S. L. Jaboya vs. jakambi: Status, negotiation, and HIV risks among female migrants in the “sex for fish” economy in Nyanza Province, Kenya. AIDS Educ. Prev. 25, 216–231 (2013).
doi: 10.1521/aeap.2013.25.3.216 pubmed: 23631716 pmcid: 3717412
Camlin, C. S., Kwena, Z. A., Dworkin, S. L., Cohen, C. R. & Bukusi, E. A. “She mixes her business”: HIV transmission and acquisition risks among female migrants in western Kenya. Soc. Sci. Med. 102, 146–156 (2014).
doi: 10.1016/j.socscimed.2013.11.004 pubmed: 24565152
Lubega, M. et al. Understanding the socio-structural context of high HIV transmission in Kasensero fishing community, South Western Uganda. BMC Public Health 15, 1033-015–102371 (2015).
doi: 10.1186/s12889-015-2371-4
Pickering, H., Okongo, M., Bwanika, K., Nnalusiba, B. & Whitworth, J. Sexual behaviour in a fishing community on Lake Victoria, Uganda. Health Transit. Rev. 7, 13–20 (1997).
pubmed: 10168579 pmcid: 10168579
Lurie, M., Harrison, A., Wilkinson, D. & Karim, S. A. Circular migration and sexual networking in rural KwaZulu/Natal: implications for the spread of HIV and other sexually transmitted infections. Health Trans. Rev. 7, 17–27 (1997).
Camlin, C. S., Snow, R. C. & Hosegood, V. Gendered patterns of migration in rural South Africa. Popul. Space Place 20, 528–551 (2014).
doi: 10.1002/psp.1794 pubmed: 25332690
Kwena, Z. A., Camlin, C. S., Shisanya, C. A., Mwanzo, I. & Bukusi, E. A. Short-term mobility and the risk of HIV infection among married couples in the fishing communities along Lake Victoria, Kenya. PLoS ONE 8, e54523 (2013).
doi: 10.1371/journal.pone.0054523 pubmed: 23336005 pmcid: 3545885
Schuyler, A. C. et al. Mobility among youth in Rakai, Uganda: Trends, characteristics, and associations with behavioural risk factors for HIV. Glob. Public. Health. 12, 1033–1050 (2017).
Olawore, O. et al. Migration and risk of HIV acquisition in Rakai, Uganda: a population-based cohort study. Lancet HIV. 5, e181–e189 (2018).
doi: 10.1016/S2352-3018(18)30009-2 pubmed: 29490875 pmcid: 6195205
Arroyo, M. A. et al. Higher HIV-1 incidence and genetic complexity along main roads in Rakai District, Uganda. J. Acquir. Immune Defic. Syndr. 43, 440–445 (2006).
doi: 10.1097/01.qai.0000243053.80945.f0 pubmed: 16980909
Wesolowski, A. et al. The use of census migration data to approximate human movement patterns across temporal scales. PLoS ONE 8, e52971 (2013).
doi: 10.1371/journal.pone.0052971 pubmed: 23326367 pmcid: 3541275
Grabowski, M. K. et al. The validity of self-reported ART use in persons living with HIV: a population-based study. AIDS. 32, 363–369 (2018).
Kagulire, S. C. et al. Field evaluation of five rapid diagnostic tests for screening of HIV-1 infections in rural Rakai, Uganda. Int. J. STD AIDS 22, 308–309 (2011).
doi: 10.1258/ijsa.2009.009352 pubmed: 21680664 pmcid: 3726838
Hill, M. O. Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432 (1973).
doi: 10.2307/1934352
Cole, S. R. & Hernan, M. A. Constructing inverse probability weights for marginal structural models. Am. J. Epidemiol. 168, 656–664 (2008).
doi: 10.1093/aje/kwn164 pubmed: 18682488 pmcid: 2732954

Auteurs

Mary Kate Grabowski (M)

Department of Pathology, Johns Hopkins School of Medicine, Baltimore, MD, 21287, USA. mgrabow2@jhu.edu.
Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, 627 North Washington St., Baltimore, MD, 21205, USA. mgrabow2@jhu.edu.
Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda. mgrabow2@jhu.edu.

Justin Lessler (J)

Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, 627 North Washington St., Baltimore, MD, 21205, USA.

Jeremiah Bazaale (J)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

Dorean Nabukalu (D)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

Justine Nankinga (J)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

Betty Nantume (B)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

Joseph Ssekasanvu (J)

Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, 627 North Washington St., Baltimore, MD, 21205, USA.

Steven J Reynolds (SJ)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.
Laboratory of Immunoregulation, Division of Intramural Research, National Institute for Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.
Division of Infectious Diseases, Department of Medicine, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA.

Robert Ssekubugu (R)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

Fred Nalugoda (F)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

Godfrey Kigozi (G)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

Joseph Kagaayi (J)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

John S Santelli (JS)

Heilbrunn Department of Population and Family Health, Columbia University, 60 Haven Avenue, New York, NY, 10032, USA.

Caitlin Kennedy (C)

Department of International Health, Johns Hopkins Bloomberg School of Public Health, 615 N. Wolfe St., Baltimore, MD, 21205, USA.

Maria J Wawer (MJ)

Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, 627 North Washington St., Baltimore, MD, 21205, USA.
Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

David Serwadda (D)

Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.
Makerere University School of Public Health, Kampala, Uganda.

Larry W Chang (LW)

Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, 627 North Washington St., Baltimore, MD, 21205, USA.
Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.
Division of Infectious Diseases, Department of Medicine, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA.
Department of International Health, Johns Hopkins Bloomberg School of Public Health, 615 N. Wolfe St., Baltimore, MD, 21205, USA.

Ronald H Gray (RH)

Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, 627 North Washington St., Baltimore, MD, 21205, USA.
Rakai Health Sciences Program, Old Bukoba Road, P.O. Box 279, Kalisizo, Uganda.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH