{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,28]],"date-time":"2026-04-28T04:37:06Z","timestamp":1777351026335,"version":"3.51.4"},"reference-count":35,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2022,2,11]],"date-time":"2022-02-11T00:00:00Z","timestamp":1644537600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Fogarty International grant","award":["D43 TW010354"],"award-info":[{"award-number":["D43 TW010354"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>The predictive factors of HIV-1 drug resistance and its distribution are poorly documented in female sex workers (FSWs) in the Democratic Republic of the Congo (DRC). However, the identification of predictive factors can lead to the development of improved and effective antiretroviral therapy (ART). The objective of the current study was to determine the predictive factors of HIV-1 drug resistance and its distribution based on FSWs in the studied regions in the Democratic Republic of the Congo (DRC). HIV-positive FSWs who were diagnosed as part of the DRC Integrated Biological and Behavioral Surveillance Survey (IBBS) were included in this study. A total of 325 FSWs participated. The HIV-1 viral load (VL) was measured according to the Abbott m2000sp and m2000rt protocols. The homogeneity chi-square test was conducted to determine the homogeneity of HIV-1 drug resistance distribution. Using a significance level of 0.05, multivariate analyses were performed to identify factors associated with HIV-1 drug resistance to ART. HIV drug resistance mutation (HIVDRM) distribution was homogeneous in the three study regions (p = 0.554) but differed based on the HIV-1 VLs of the FSWs. FSWs with high HIV-1 VLs harbored more HIVDRMs (p = 0.028) of predominantly pure HIV-1 strains compared with those that had low HIV-1 VLs. Sexually transmitted infection (STI) history (aOR [95%CI] = 8.51 [1.62, 44.74]), high HIV-1 VLs (aOR [95%CI] = 5.39 [1.09, 26.74]), and HIV-1\u2013syphilis coinfection (aOR [95%CI] = 9.71 [1.84, 51.27]) were associated with HIV drug resistance among FSWs in the DRC. A history of STIs (e.g., abnormal fluid) in the 12 months prior to the survey, a high HIV-1 VL, and HIV-1\u2013syphilis coinfection were associated with HIV-1 drug resistance among FSWs in the DRC. Efforts should be made to systematically test for other infections which increase the HIV-1 VL, in the case of HIV-1 coinfection, in order to maintain ART effectiveness across the DRC.<\/jats:p>","DOI":"10.3390\/ijerph19042021","type":"journal-article","created":{"date-parts":[[2022,2,13]],"date-time":"2022-02-13T21:08:43Z","timestamp":1644786523000},"page":"2021","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Predictive Factors of HIV-1 Drug Resistance and Its Distribution among Female Sex Workers in the Democratic Republic of the Congo (DRC)"],"prefix":"10.3390","volume":"19","author":[{"given":"Godefroid Mulakilwa Ali","family":"Musema","sequence":"first","affiliation":[{"name":"Kinshasa School of Public Health, University of Kinshasa, Kinshasa P.O. Box 11850, Democratic Republic of the Congo"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3828-6214","authenticated-orcid":false,"given":"Pierre Zalagile","family":"Akilimali","sequence":"additional","affiliation":[{"name":"Kinshasa School of Public Health, University of Kinshasa, Kinshasa P.O. Box 11850, Democratic Republic of the Congo"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Takaisi Kikuni Ntonbo","family":"za Balega","sequence":"additional","affiliation":[{"name":"Pharmaceutical Sciences Faculty, University of Kinshasa, Kinshasa P.O. Box 11850, Democratic Republic of the Congo"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"D\u00e9sir\u00e9","family":"Tshala-Katumbay","sequence":"additional","affiliation":[{"name":"Department of Neurology, School of Medicine and School of Public Health, Oregon Health & Science University, Portland, OR 97239, USA"},{"name":"Department of Neurology, School of Medicine, University of Kinshasa, Kinshasa P.O. Box 11850, Democratic Republic of the Congo"},{"name":"Institut National de Recherches Biom\u00e9dicales, Kinshasa P.O. Box 11850, Democratic Republic of the Congo"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paul-Samson Dikasa","family":"Lusamba","sequence":"additional","affiliation":[{"name":"Kinshasa School of Public Health, University of Kinshasa, Kinshasa P.O. Box 11850, Democratic Republic of the Congo"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,2,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12981-020-00290-3","article-title":"The HIV care continuum and HIV-1 drug resistance among female sex workers: A key population in Guinea-Bissau","volume":"17","author":"Lindman","year":"2020","journal-title":"AIDS Res. Ther."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Yuan, D., Du, Z., Zhou, J., Ye, L., Su, L., Yang, H., Yuan, F., Li, Y., Liu, H., and Zhai, W. (2019). HIV-1 subtype diversity, drug resistance, and genetic transmission networks in men who have sex with men with virologic failure in antiretroviral therapy in Sichuan, China, 2011 to 2017. Medicine, 98.","DOI":"10.1097\/MD.0000000000017585"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Palumbo, P.J., Zhang, Y., Fogel, J.M., Guo, X., Clarke, W., Breaud, A., Richardson, P., Piwowar-Manning, E., Hart, S., and Hamilton, E.L. (2019). HIV drug resistance in persons who inject drugs enrolled in an HIV prevention trial in Indonesia, Ukraine, and Vietnam: HPTN 074. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0223829"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"34","DOI":"10.2174\/1874613601610010034","article-title":"HIV Infection and AIDS in Sub-Saharan Africa: Current Status, Challenges and Opportunities","volume":"10","author":"Kharsany","year":"2016","journal-title":"Open AIDS J."},{"key":"ref_5","unstructured":"Joint United Nations Program on HIV and AIDS (2017, December 15). UNAIDS-Data. Available online: http:\/\/www.unaids.org\/sites\/default\/files\/media_asset\/20170720_Data_book_2017_en.pdf."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.1016\/S0140-6736(18)32279-7","article-title":"Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990\u20132017: A systematic analysis for the Global Burden of Disease Study 2017","volume":"392","author":"James","year":"2018","journal-title":"Lancet"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1736","DOI":"10.1016\/S0140-6736(18)32203-7","article-title":"Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980\u20132017: A systematic analysis for the Global Burden of Disease Study 2017; GBD 2017 Causes of Death Collaborators","volume":"392","author":"Roth","year":"2018","journal-title":"Lancet"},{"key":"ref_8","unstructured":"Minist\u00e8re de la Sant\u00e9 Publique, R\u00e9publique D\u00e9mocratique du Congo (2006). Programme National de Lutte contre le VIH\/Sida et les IST (PNLS). Rapport de l\u2019Enqu\u00eate de Surveillance Comportementale (ESC) et de S\u00e9ropr\u00e9valence (BSS), Minist\u00e8re de la Sant\u00e9 Publique, R\u00e9publique D\u00e9mocratique du Congo."},{"key":"ref_9","unstructured":"Minist\u00e8re de la Sant\u00e9 Publique, R\u00e9publique D\u00e9mocratique du Congo (2014). Programme National de Lutte contre le VIH\/Sida et les IST (PNLS). Rapport de l\u2019Enqu\u00eate Int\u00e9gr\u00e9e de Surveillance Comportementale et de S\u00e9ropr\u00e9valence (IBSS), Minist\u00e8re de la Sant\u00e9 Publique, R\u00e9publique D\u00e9mocratique du Congo."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1080\/17290376.2012.743825","article-title":"Female sex workers in Africa: Epidemiology overview, data gaps, ways forward","volume":"9","author":"Ngugi","year":"2012","journal-title":"SAHARA-J J. Soc. Asp. HIV\/AIDS"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1089\/aid.2013.0009","article-title":"Dynamics of HIV Type 1 Recombination Following Superinfection","volume":"29","author":"Koning","year":"2013","journal-title":"AIDS Res. Hum. Retrovir."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1089\/aid.2011.0024","article-title":"HIV Type 1 Subtype Distribution, Multiple Infections, Sexual Networks, and Partnership Histories in Female Sex Workers in Kampala, Uganda","volume":"28","author":"Ssemwanga","year":"2012","journal-title":"AIDS Res. Hum. Retrovir."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12889-015-2553-0","article-title":"A systematic review of the clinical and social epidemiological research among sex workers in Uganda","volume":"15","author":"Muldoon","year":"2015","journal-title":"BMC Public Health"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Etta, E.M., Mavhandu, L., Manhaeve, C., Mcgonigle, K., Jackson, P., Rekosh, D., Hammarskjold, M.-L., Bessong, P.O., and Tebit, D. (2017). High level of HIV-1 drug resistance mutations in patients with unsuppressed viral loads in rural northern South Africa. AIDS Res. Ther., 14.","DOI":"10.1186\/s12981-017-0161-z"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1621","DOI":"10.3851\/IMP2267","article-title":"Therapy failure resulting from superinfection by a drug resistant HIV variant","volume":"17","author":"Pingen","year":"2012","journal-title":"Antivir. Ther."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1071\/SH04024","article-title":"HIV-1 co-infection, superinfection and recombination","volume":"1","author":"Steain","year":"2004","journal-title":"Sex. Health"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Kwon, E.H., Musema, G.M.A., Boelter, J., Townsend, S., Tshala-Katumbay, D., Kayembe, P.K., West, J., and Wood, C. (2020). HIV-1 subtypes and drug resistance mutations among female sex workers varied in different cities and regions of the Democratic Republic of Congo. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0228670"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Williams, J.R., Alary, M., Lowndes, C.M., Behanzin, L., Labb\u00e9, A.-C., Anagonou, S., Ndour, M., Minani, I., Ahoussinou, C., and Zannou, D.M. (2014). Positive Impact of Increases in Condom Use among Female Sex Workers and Clients in a Medium HIV Prevalence Epidemic: Modelling Results from Project SIDA1\/2\/3 in Cotonou, Benin. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0102643"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1097\/00002030-200404090-00009","article-title":"Transactional sex is the driving force in the dynamics of HIV in Accra, Ghana","volume":"18","author":"Sobela","year":"2004","journal-title":"AIDS"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1097\/00002030-200404090-00013","article-title":"The central role of clients of female sex workers in the dynamics of heterosexual HIV transmission in sub-Saharan Africa","volume":"18","author":"Alary","year":"2004","journal-title":"AIDS"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Coetzee, J., Hunt, G., Jaffer, M., Otwombe, K., Scott, L., Bongwe, A., Ledwaba, J., Molema, S., Jewkes, R., and Gray, G.E. (2017). HIV-1 viraemia and drug resistance amongst female sex workers in Soweto, South Africa: A cross sectional study. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0188606"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1016\/S1473-3099(10)70093-1","article-title":"Effect of treating co-infections on HIV-1 viral load: A systematic review","volume":"10","author":"Modjarrad","year":"2010","journal-title":"Lancet Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1111\/ddg.12382","article-title":"Characteristics and coinfection with syphilis in newly HIV-infected patients at the University Hospital Dresden 1987\u20132012","volume":"12","author":"Schmitt","year":"2014","journal-title":"J. Dtsch. Dermatol. Ges."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"93","DOI":"10.21106\/ijtmrph.140","article-title":"HIV-1-Syphilis Co-infection Associated with High Viral Load in Female Sex Workers in the Democratic Republic of the Congo","volume":"4","author":"Musema","year":"2020","journal-title":"Int. J. Transl. Med Res. Public Heal."},{"key":"ref_25","unstructured":"World Health Organization (2012). HIV Drug Resistance Report 2012, WHO."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.jcv.2018.03.012","article-title":"Rare emergence of drug resistance in HIV-1 treatment-na\u00efve patients receiving elvitegravir\/cobicistat\/emtricitabine\/tenofovir alafenamide for 144 weeks","volume":"103","author":"Margot","year":"2018","journal-title":"J. Clin. Virol."},{"key":"ref_27","unstructured":"World Health Organization (WHO) (2016). Consolidated Guidelines on the Use of Antiretroviral Drugs for Treating and Preventing HIV Infection: Recommendations for a Public Health Approach, WHO."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1136\/sextrans-2018-053854","article-title":"Sustained virological response and drug resistance among female sex workers living with HIV on antiretroviral therapy in Kampala, Uganda: A cross-sectional study","volume":"95","author":"Namale","year":"2019","journal-title":"Sex. Transm. Infect."},{"key":"ref_29","first-page":"470","article-title":"Prevalence of & knowledge, attitude & practices towards HIV & sexually transmitted infections (STIs) among female sex workers (FSWs) in Andhra Pradesh","volume":"134","author":"Hemalatha","year":"2011","journal-title":"Indian J. Med. Res."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Diabat\u00e9, S., Chamberland, A., Geraldo, N., Tremblay, C., and Alary, M. (2018). Gonorrhea, Chlamydia and HIV incidence among female sex workers in Cotonou, Benin: A longitudinal study. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0197251"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"928","DOI":"10.1111\/tmi.12717","article-title":"Drug resistance mutations after the first 12 months on antiretroviral therapy and determinants of virological failure in Rwanda","volume":"21","author":"Ndahimana","year":"2016","journal-title":"Trop. Med. Int. Health"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1136\/sti.75.1.3","article-title":"From epidemiological synergy to public health policy and practice: The contribution of other sexually transmitted diseases to sexual transmission of HIV infection","volume":"75","author":"Fleming","year":"1999","journal-title":"Sex. Transm. Infect."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1136\/bmj.313.7053.341","article-title":"Fluctuations of HIV load in semen of HIV positive patients with newly acquired sexually transmitted diseases","volume":"313","author":"Atkins","year":"1996","journal-title":"BMJ"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"F85","DOI":"10.1097\/00002030-199712000-00001","article-title":"The associations between cervicovaginal HIV shedding, sexually transmitted diseases and immunosuppression in female sex workers in Abidjan, Cote d\u2019Ivoire","volume":"11","author":"Ghys","year":"1997","journal-title":"AIDS."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Rich, S.N., Cook, R.L., Yaghjyan, L., Francois, K., Puttkammer, N., Robin, E., Bae, J., Joseph, N., Pessoa-Brand\u00e3o, L., and Delcher, C. (2020). Risk factors for delayed viral suppression on first-line antiretroviral therapy among persons living with HIV in Haiti, 2013\u20132017. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0240817"}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/4\/2021\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:17:34Z","timestamp":1760134654000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/4\/2021"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,11]]},"references-count":35,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2022,2]]}},"alternative-id":["ijerph19042021"],"URL":"https:\/\/doi.org\/10.3390\/ijerph19042021","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,11]]}}}