Sudan virus disease super-spreading, Uganda, 2022.


Journal

BMC infectious diseases
ISSN: 1471-2334
Titre abrégé: BMC Infect Dis
Pays: England
ID NLM: 100968551

Informations de publication

Date de publication:
23 May 2024
Historique:
received: 05 12 2023
accepted: 08 05 2024
medline: 24 5 2024
pubmed: 24 5 2024
entrez: 23 5 2024
Statut: epublish

Résumé

On 20 September 2022, Uganda declared its fifth Sudan virus disease (SVD) outbreak, culminating in 142 confirmed and 22 probable cases. The reproductive rate (R) of this outbreak was 1.25. We described persons who were exposed to the virus, became infected, and they led to the infection of an unusually high number of cases during the outbreak. In this descriptive cross-sectional study, we defined a super-spreader person (SSP) as any person with real-time polymerase chain reaction (RT-PCR) confirmed SVD linked to the infection of ≥ 13 other persons (10-fold the outbreak R). We reviewed illness narratives for SSPs collected through interviews. Whole-genome sequencing was used to support epidemiologic linkages between cases. Two SSPs (Patient A, a 33-year-old male, and Patient B, a 26-year-old male) were identified, and linked to the infection of one probable and 50 confirmed secondary cases. Both SSPs lived in the same parish and were likely infected by a single ill healthcare worker in early October while receiving healthcare. Both sought treatment at multiple health facilities, but neither was ever isolated at an Ebola Treatment Unit (ETU). In total, 18 secondary cases (17 confirmed, one probable), including three deaths (17%), were linked to Patient A; 33 secondary cases (all confirmed), including 14 (42%) deaths, were linked to Patient B. Secondary cases linked to Patient A included family members, neighbours, and contacts at health facilities, including healthcare workers. Those linked to Patient B included healthcare workers, friends, and family members who interacted with him throughout his illness, prayed over him while he was nearing death, or exhumed his body. Intensive community engagement and awareness-building were initiated based on narratives collected about patients A and B; 49 (96%) of the secondary cases were isolated in an ETU, a median of three days after onset. Only nine tertiary cases were linked to the 51 secondary cases. Sequencing suggested plausible direct transmission from the SSPs to 37 of 39 secondary cases with sequence data. Extended time in the community while ill, social interactions, cross-district travel for treatment, and religious practices contributed to SVD super-spreading. Intensive community engagement and awareness may have reduced the number of tertiary infections. Intensive follow-up of contacts of case-patients may help reduce the impact of super-spreading events.

Sections du résumé

BACKGROUND BACKGROUND
On 20 September 2022, Uganda declared its fifth Sudan virus disease (SVD) outbreak, culminating in 142 confirmed and 22 probable cases. The reproductive rate (R) of this outbreak was 1.25. We described persons who were exposed to the virus, became infected, and they led to the infection of an unusually high number of cases during the outbreak.
METHODS METHODS
In this descriptive cross-sectional study, we defined a super-spreader person (SSP) as any person with real-time polymerase chain reaction (RT-PCR) confirmed SVD linked to the infection of ≥ 13 other persons (10-fold the outbreak R). We reviewed illness narratives for SSPs collected through interviews. Whole-genome sequencing was used to support epidemiologic linkages between cases.
RESULTS RESULTS
Two SSPs (Patient A, a 33-year-old male, and Patient B, a 26-year-old male) were identified, and linked to the infection of one probable and 50 confirmed secondary cases. Both SSPs lived in the same parish and were likely infected by a single ill healthcare worker in early October while receiving healthcare. Both sought treatment at multiple health facilities, but neither was ever isolated at an Ebola Treatment Unit (ETU). In total, 18 secondary cases (17 confirmed, one probable), including three deaths (17%), were linked to Patient A; 33 secondary cases (all confirmed), including 14 (42%) deaths, were linked to Patient B. Secondary cases linked to Patient A included family members, neighbours, and contacts at health facilities, including healthcare workers. Those linked to Patient B included healthcare workers, friends, and family members who interacted with him throughout his illness, prayed over him while he was nearing death, or exhumed his body. Intensive community engagement and awareness-building were initiated based on narratives collected about patients A and B; 49 (96%) of the secondary cases were isolated in an ETU, a median of three days after onset. Only nine tertiary cases were linked to the 51 secondary cases. Sequencing suggested plausible direct transmission from the SSPs to 37 of 39 secondary cases with sequence data.
CONCLUSION CONCLUSIONS
Extended time in the community while ill, social interactions, cross-district travel for treatment, and religious practices contributed to SVD super-spreading. Intensive community engagement and awareness may have reduced the number of tertiary infections. Intensive follow-up of contacts of case-patients may help reduce the impact of super-spreading events.

Identifiants

pubmed: 38783244
doi: 10.1186/s12879-024-09391-0
pii: 10.1186/s12879-024-09391-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

520

Informations de copyright

© 2024. The Author(s).

Références

WHO. Ebola Disease caused by Sudan virus – Uganda [Internet]. [cited 2022 Nov 12]. https://www.who.int/emergencies/disease-outbreak-news/item/2022-DON410 .
Kucharski AJ, John Edmunds W. Case fatality rate for Ebola virus disease in west Africa. 2014 [cited 2022 Nov 24]. https://doi.org/10.1016/S0140-6736(14)61706-2 .
Kadanali A, Karagoz G. An overview of Ebola virus disease. North Clin Istanbul [Internet]. 2015 [cited 2022 Nov 24];2(1):81. /pmc/articles/PMC5175058/.
U.S Centers for Disease Control and Prevention. What is Ebola Disease? | Ebola (Ebola Virus Disease) | CDC [Internet]. 2023 [cited 2023 Oct 25]. https://www.cdc.gov/vhf/ebola/about.html .
World Health Organization (WHO). Ebola virus disease [Internet]. [cited 2022 Dec 19]. https://www.who.int/news-room/fact-sheets/detail/ebola-virus-disease .
U.S Centers for Disease Control and Prevention. Transmission | Ebola Hemorrhagic Fever | CDC [Internet]. [cited 2022 Nov 12]. https://www.cdc.gov/vhf/ebola/transmission/index.html .
Dietz K. The estimation of the basic reproduction number for infectious diseases. http://dx.doi.org/101177/096228029300200103 [Internet]. 2016 Jul 2 [cited 2022 Nov 24];2(1):23–41. https://journals.sagepub.com/doi/abs/10.1177/096228029300200103 .
Fine PEM. Herd Immunity: History, Theory, Practice. 1993;15(2).
Luo D, Zheng R, Wang D, Zhang X, Yin Y, Wang K et al. Effect of sexual transmission on the West Africa Ebola outbreak in 2014: a mathematical modelling study. Sci Reports 2019 91 [Internet]. 2019 Feb 7 [cited 2022 Nov 16];9(1):1–11. https://www.nature.com/articles/s41598-018-38397-3 .
Camacho A, Kucharski AJ, Funk S, Breman J, Piot P, Edmunds WJ. Potential for large outbreaks of Ebola virus disease. Epidemics. 2014;9:70–8.
doi: 10.1016/j.epidem.2014.09.003 pubmed: 25480136 pmcid: 4255970
Legrand J, Grais RF, Boelle PY, Valleron AJ, Flahault A. Understanding the dynamics of Ebola epidemics. Epidemiol Infect [Internet]. 2007 [cited 2023 Jan 17];135(4):610–21. https://www.cambridge.org/core/journals/epidemiology-and-infection/article/understanding-the-dynamics-of-ebola-epidemics/BAEEC049DE2893FA58DD8F38E19F62D8 .
Ferrari MJ, Bjørnstad ON, Dobson AP. Estimation and inference of R0 of an infectious pathogen by a removal method. Math Biosci. 2005;198(1):14–26.
doi: 10.1016/j.mbs.2005.08.002 pubmed: 16216286
Ndanguza D, Tchuenche JM, Haario H. Statistical data analysis of the 1995 Ebola outbreak in the Democratic Republic of Congo. Afrika Mat 2011 241 [Internet]. 2011 Jul 28 [cited 2022 Nov 16];24(1):55–68. https://link.springer.com/article/ https://doi.org/10.1007/s13370-011-0039-5 .
Chowell G, Hengartner NW, Castillo-Chavez C, Fenimore PW, Hyman JM. The basic reproductive number of Ebola and the effects of public health measures: the cases of Congo and Uganda. J Theor Biol. 2004;229(1):119–26.
doi: 10.1016/j.jtbi.2004.03.006 pubmed: 15178190
Usan S, Line EK, Edemark ILH, Cott S, Avies FD. Outbreak of Tuberculosis among Regular Patrons of a Neighborhood Bar. https://doi.org/10.1056/nejm199507273330404 [Internet]. 1995 Jul 27 [cited 2022 Dec 21];333(4):222–7. https://www.nejm.org/doi/full/ .
Urtis AMBC, Uth R, Ogel V, Tephen S, Onough MCD, Ames J et al. Extensive Transmission of Mycobacterium tuberculosis from a Child. https://doi.org/101056/NEJM199911113412002 [Internet]. 1999 Nov 11 [cited 2022 Dec 21];341(20):1491–5. https://www.nejm.org/doi/full/ https://doi.org/10.1056/NEJM199911113412002 .
Khan AS, Kikwit for the C de L contre les E à, Tshioko FK. Kikwit for the C de L contre les E à, Heymann DL, Kikwit for the C de L contre les E à, The Reemergence of Ebola Hemorrhagic Fever, Democratic Republic of the Congo, 1995. J Infect Dis [Internet]. 1999 Feb 1 [cited 2022 Dec 21];179(Supplement_1):S76–86. https://academic.oup.com/jid/article/179/Supplement_1/S76/882543 .
Witteck A, Yerly S, Vernazza P. Unusually high HIV infectiousness in an HIV-, HCV- and HSV-2-coinfected heterosexual man. 2009 [cited 2022 Dec 21];139:207–9. Available from: https://doi.org/10.4414/smw.2009.12575 .
Lakdawala SS, Menachery VD. Catch me if you can: Superspreading of COVID-19. Trends Microbiol. 2021;29(10):919–29.
doi: 10.1016/j.tim.2021.05.002 pubmed: 34059436 pmcid: 8112283
Chau NVV, Hong NTT, Ngoc NM, Thanh TT, Khanh PNQ, Nguyet LA et al. Superspreading Event of SARS-CoV-2 Infection at a Bar, Ho Chi Minh City, Vietnam. Emerg Infect Dis [Internet]. 2021 Jan 1 [cited 2022 Dec 21];27(1):310. /pmc/articles/PMC7774544/.
Wang SX, Li YM, Sun BC, Zhang SW, Zhao WH, Wei MT, et al. The SARS outbreak in a general hospital in Tianjin, China - the case of super-spreader. Epidemiol Infect. 2006;134(4):786–91.
doi: 10.1017/S095026880500556X pubmed: 16371174
Lau MSY, Dalziel BD, Funk S, McClelland A, Tiffany A, Riley S et al. Spatial and temporal dynamics of superspreading events in the 2014–2015 West Africa Ebola epidemic. Proc Natl Acad Sci U S A [Internet]. 2017 Feb 28 [cited 2022 Nov 14];114(9):2337–42. https://www.pnas.org/doi/abs/ https://doi.org/10.1073/pnas.1614595114 .
Stein RA. Super-spreaders in infectious diseases. Int J Infect Dis. 2011;15(8):e510–3.
doi: 10.1016/j.ijid.2010.06.020 pubmed: 21737332 pmcid: 7110524
World Health Organization. Ebola virus disease in Uganda- WHO | Regional Office for Africa [Internet]. 2022 [cited 2023 Mar 13]. https://www.afro.who.int/countries/uganda/news/uganda-declares-ebola-virus-disease-outbreak .
Reliefweb U. Ebola Outbreak - Sep 2022 | ReliefWeb [Internet]. [cited 2022 Nov 12]. https://reliefweb.int/disaster/ep-2022-000315-uga .
Aceng JR, Bosa HK, Kamara N, Atwine D, Mwebesa H, Nyika H et al. Continental concerted efforts to control the seventh outbreak of Ebola Virus disease in Uganda: The first 90 days of the response. J Public Health Africa [Internet]. 2023 Sep 29 [cited 2023 Nov 7];14(9). https://www.publichealthinafrica.org/jphia/article/view/2735 .
GitHub. GitHub - imperialebola2018/chainchecker [Internet]. 2022 [cited 2022 Dec 4]. https://github.com/imperialebola2018/chainchecker .
Balinandi S, Whitmer S, Mulei S, Nassuna C, Pimundu G, Muyigi T et al. Molecular characterization of the 2022 Sudan virus disease outbreak in Uganda. Dutch RE, editor. J Virol [Internet]. 2023 Sep 26 [cited 2023 Oct 2]; https://doi.org/10.1128/jvi.00590-23 .
Lau MSY, Dalziel BD, Funk S, McClelland A, Tiffany A, Riley S et al. Spatial and temporal dynamics of superspreading events in the 2014–2015 West Africa Ebola epidemic. Proc Natl Acad Sci U S A [Internet]. 2017 Feb 28 [cited 2022 Nov 22];114(9):2337–42. https://www.pnas.org/doi/abs/ https://doi.org/10.1073/pnas.1614595114 .
Wong G, Liu W, Liu Y, Zhou B, Bi Y, Gao GF. MERS, SARS, and Ebola: The Role of Super-Spreaders in Infectious Disease. Cell Host Microbe [Internet]. 2015 Oct 10 [cited 2022 Nov 22];18(4):398. /pmc/articles/PMC7128246/.
Mohindra R, Ghai A, Brar R, Khandelwal N, Biswal M, Suri V et al. Superspreaders: A Lurking Danger in the Community. J Prim Care Community Heal [Internet]. 2021 Jan 15 [cited 2022 Nov 24];12. https://journals.sagepub.com/doi/ https://doi.org/10.1177/2150132720987432 .
Althaus CL, Ebola. The real lessons from HIV scale-up. Lancet Infect Dis [Internet]. 2015 May 1 [cited 2023 Aug 14];15(5):507–8. http://www.thelancet.com/article/S1473309915701350/fulltext .
After Ebola in West Africa — Unpredictable Risks, Preventable Epidemics. N Engl J Med [Internet]. 2016 Aug 11 [cited 2023 Aug 14];375(6):587–96. https://www.nejm.org/doi/full/ https://doi.org/10.1056/NEJMsr1513109 .
Edholm CJ, Emerenini BO, Murillo AL, Saucedo O, Shakiba N, Wang X et al. Searching for Superspreaders: Identifying Epidemic Patterns Associated with Superspreading Events in Stochastic Models. Assoc Women Math Ser [Internet]. 2018 [cited 2022 Nov 14];14:1–29. https://link.springer.com/chapter/ https://doi.org/10.1007/978-3-319-98083-6_1 .
Baize S, Pannetier D, Oestereich L, Rieger T, Koivogui L, Magassouba N et al. Emergence of Zaire Ebola Virus Disease in Guinea. N Engl J Med [Internet]. 2014 Oct 9 [cited 2023 Jan 18];371(15):1418–25. https://www.nejm.org/doi/full/ https://doi.org/10.1056/nejmoa1404505 .
Gire SK, Goba A, Andersen KG, Sealfon RSG, Park DJ, Kanneh L et al. Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak. Science (80-) [Internet]. 2014 Sep 12 [cited 2023 Aug 14];345(6202):1369–72. https://www.science.org/doi/ https://doi.org/10.1126/science.1259657 .
Lekone PE, Finkenstädt BF. Statistical Inference in a Stochastic Epidemic SEIR Model with Control Intervention: Ebola as a Case Study. Biometrics [Internet]. 2006 Dec 1 [cited 2023 Sep 12];62(4):1170–7. https://onlinelibrary.wiley.com/doi/full/ https://doi.org/10.1111/j.1541-0420.2006.00609.x .
White LF, Pagano M. A likelihood-based method for real-time estimation of the serial interval and reproductive number of an epidemic. Stat Med [Internet]. 2008 Jul 20 [cited 2023 Sep 12];27(16):2999–3016. https://onlinelibrary.wiley.com/doi/full/ https://doi.org/10.1002/sim.3136 .
Van Bemmel K. The Quest for Treatment. The Violated Body of Nodding Syndrome in Northern Uganda. Jpss [Internet]. 2016;2(2):63–78. http://www.jpss.ug/files/Mental_Health_Volume_2_2016/JPSS Mental Health 2016 The Quest for Treatment. The Violated Body of Nodding Syndrome.pdf.
Francesconi P, Yoti Z, Declich S, Onek PA, Fabiani M, Olango J et al. Ebola Hemorrhagic Fever Transmission and Risk Factors of Contacts, Uganda. Emerg Infect Dis [Internet]. 2003 [cited 2023 Jan 18];9(11):1430. /pmc/articles/PMC3035551/.
Bausch DG, Towner JS, Dowell SF, Kaducu F, Lukwiya M, Sanchez A et al. Assessment of the Risk of Ebola Virus Transmission from Bodily Fluids and Fomites. J Infect Dis [Internet]. 2007 Nov 15 [cited 2023 Jan 18];196(Supplement_2):S142–7. https://academic.oup.com/jid/article/196/Supplement_2/S142/858852 .
Dowell SF, Mukunu R, Ksiazek TG, Khan AS, Rollin PE, Peters CJ. Transmission of Ebola Hemorrhagic Fever: A Study of Risk Factors in Family Members, Kikwit, Democratic Republic of the Congo, 1995. J Infect Dis [Internet]. 1999 Feb 1 [cited 2023 Jan 18];179(Supplement_1):S87–91. https://academic.oup.com/jid/article/179/Supplement_1/S87/882673 .
Buseh AG, Stevens PE, Bromberg M, Kelber ST. The Ebola epidemic in West Africa: challenges, opportunities, and policy priority areas. Nurs Outlook. 2015;63(1):30–40.
doi: 10.1016/j.outlook.2014.12.013 pubmed: 25645480 pmcid: 7111626
Muzembo BA, Ntontolo NP, Ngatu NR, Khatiwada J, Ngombe KL, Numbi OL et al. Local perspectives on Ebola during its tenth outbreak in DR Congo: A nationwide qualitative study. PLoS One [Internet]. 2020 Oct 1 [cited 2023 Aug 10];15(10):e0241120. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0241120 .
Blevins JB, Jalloh MF, Robinson DA. Faith and global health practice in Ebola and HIV emergencies. Am J Public Health [Internet]. 2019 Feb 6 [cited 2023 Aug 10];109(3):379–84. https://doi.org/10.2105/AJPH.2018.304870 .
Marshall K. Roles of religious actors in the West African Ebola response. https://doi.org/101080/0961452420171327573 [Internet]. 2017 Jul 4 [cited 2023 Aug 10];27(5):622–33. https://www.tandfonline.com/doi/abs/ https://doi.org/10.1080/09614524.2017.1327573 .
Hewlett BL, Hewlett BS. Providing Care and Facing Death: Nursing During Ebola Outbreaks in Central Africa. http://dx.doi.org/101177/1043659605278935 [Internet]. 2005 Oct 1 [cited 2023 Aug 10];16(4):289–97. https://journals.sagepub.com/doi/abs/10.1177/1043659605278935 .
Nyakarahuka L, Skjerve E, Nabadda D, Sitali DC, Mumba C, Mwiine FN et al. Knowledge and attitude towards Ebola and Marburg virus diseases in Uganda using quantitative and participatory epidemiology techniques. PLoS Negl Trop Dis [Internet]. 2017 Sep 11 [cited 2023 Aug 10];11(9):e0005907. https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0005907 .
Gidado S, Oladimeji AM, Roberts AA, Nguku P, Nwangwu IG, Waziri NE et al. Public knowledge, perception and source of information on Ebola Virus Disease – Lagos, Nigeria; September, 2014. PLOS Curr Outbreaks. 2015;7(OUTBREAKS).
Gire SK, Goba A, Andersen KG, Sealfon RSG, Park DJ, Kanneh L et al. Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak. Science (80-) [Internet]. 2014 Sep 12 [cited 2023 Jan 18];345(6202):1369–72. https://www.science.org/doi/ https://doi.org/10.1126/science.1259657 .
Sierra Leone. a traditional healer and a funeral [Internet]. [cited 2023 Jan 18]. https://www.who.int/news/item/01-09-2015-sierra-leone-a-traditional-healer-and-a-funeral .
Barbarossa MV, Dénes A, Kiss G, Nakata Y, Röst G, Vizi Z. Transmission Dynamics and Final Epidemic Size of Ebola Virus Disease Outbreaks with Varying Interventions. PLoS One [Internet]. 2015 Jul 21 [cited 2023 Sep 11];10(7):e0131398. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0131398 .
Baron RC, McCormick JB, Zubeir OA. Ebola virus disease in southern Sudan: Hospital dissemination and intrafamilial spread. Bull World Health Organ. 1983;61(6):997–1003.
pubmed: 6370486 pmcid: 2536233

Auteurs

Allan Komakech (A)

Uganda National Institute of Public Health, Kampala, Uganda. akomackech@musph.ac.ug.
Clarke International University, Kampala, Uganda. akomackech@musph.ac.ug.

Shannon Whitmer (S)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

Jonathan Izudi (J)

Department of Community Health, Faculty of Medicine, Mbarara University of Science and Technology (MUST), Mbarara, Uganda.
Data Science and Evaluations Unit, African Population and Health Research Center, Nairobi, Kenya.

Charles Kizito (C)

Kikandwa Health Center III, Kassanda, Uganda.

Mackline Ninsiima (M)

Uganda National Institute of Public Health, Kampala, Uganda.

Sherry R Ahirirwe (SR)

Uganda National Institute of Public Health, Kampala, Uganda.

Zainah Kabami (Z)

Uganda National Institute of Public Health, Kampala, Uganda.

Alex R Ario (AR)

Uganda National Institute of Public Health, Kampala, Uganda.

Daniel Kadobera (D)

Uganda National Institute of Public Health, Kampala, Uganda.

Benon Kwesiga (B)

Uganda National Institute of Public Health, Kampala, Uganda.

Samuel Gidudu (S)

Uganda National Institute of Public Health, Kampala, Uganda.

Richard Migisha (R)

Uganda National Institute of Public Health, Kampala, Uganda.

Issa Makumbi (I)

National Public Health Emergency Operations Center, Kampala, Uganda.

Daniel Eurien (D)

BAYLOR Uganda, Kampala, Uganda.

Joshua Kayiwa (J)

National Public Health Emergency Operations Center, Kampala, Uganda.

Lilian Bulage (L)

Uganda National Institute of Public Health, Kampala, Uganda.

Doreen N Gonahasa (DN)

Uganda National Institute of Public Health, Kampala, Uganda.

Irene Kyamwine (I)

Uganda National Institute of Public Health, Kampala, Uganda.

Paul E Okello (PE)

Uganda National Institute of Public Health, Kampala, Uganda.

Hildah T Nansikombi (HT)

Uganda National Institute of Public Health, Kampala, Uganda.

Immaculate Atuhaire (I)

Uganda National Institute of Public Health, Kampala, Uganda.

Alice Asio (A)

Uganda National Institute of Public Health, Kampala, Uganda.

Sarah Elayeete (S)

Uganda National Institute of Public Health, Kampala, Uganda.

Edirisa J Nsubuga (EJ)

Uganda National Institute of Public Health, Kampala, Uganda.

Veronica Masanja (V)

Uganda National Institute of Public Health, Kampala, Uganda.

Stella M Migamba (SM)

Uganda National Institute of Public Health, Kampala, Uganda.

Patience Mwine (P)

Uganda National Institute of Public Health, Kampala, Uganda.

Petranilla Nakamya (P)

Uganda National Institute of Public Health, Kampala, Uganda.

Rose Nampeera (R)

Uganda National Institute of Public Health, Kampala, Uganda.

Andrew Kwiringira (A)

Uganda National Institute of Public Health, Kampala, Uganda.

Rebecca Akunzirwe (R)

Uganda National Institute of Public Health, Kampala, Uganda.

Helen Nelly Naiga (HN)

Uganda National Institute of Public Health, Kampala, Uganda.

Saudah K Namubiru (SK)

Uganda National Institute of Public Health, Kampala, Uganda.

Brian Agaba (B)

Uganda National Institute of Public Health, Kampala, Uganda.

Jane Frances Zalwango (JF)

Uganda National Institute of Public Health, Kampala, Uganda.

Marie Gorreti Zalwango (MG)

Uganda National Institute of Public Health, Kampala, Uganda.

Patrick King (P)

Uganda National Institute of Public Health, Kampala, Uganda.

Brenda Nakafeero Simbwa (BN)

Uganda National Institute of Public Health, Kampala, Uganda.

Robert Zavuga (R)

Uganda National Institute of Public Health, Kampala, Uganda.

Mercy Wendy Wanyana (MW)

Uganda National Institute of Public Health, Kampala, Uganda.

Thomas Kiggundu (T)

Uganda National Institute of Public Health, Kampala, Uganda.

Lawrence Oonyu (L)

Uganda National Institute of Public Health, Kampala, Uganda.

Alex Ndyabakira (A)

Kampala Capital City Authority, Kampala, Uganda.

Mariam Komugisha (M)

Uganda National Institute of Public Health, Kampala, Uganda.

Brian Kibwika (B)

Uganda National Institute of Public Health, Kampala, Uganda.

Innocent Ssemanda (I)

Uganda National Institute of Public Health, Kampala, Uganda.

Yasin Nuwamanya (Y)

Uganda National Institute of Public Health, Kampala, Uganda.

Adams Kamukama (A)

Uganda National Institute of Public Health, Kampala, Uganda.

Dorothy Aanyu (D)

Uganda National Institute of Public Health, Kampala, Uganda.

Dominic Kizza (D)

Uganda National Institute of Public Health, Kampala, Uganda.

Daniel Okello Ayen (DO)

Kampala Capital City Authority, Kampala, Uganda.

Sophia Mulei (S)

Uganda Virus Research Institute, Entebbe, Uganda.

Stephen Balinandi (S)

Uganda Virus Research Institute, Entebbe, Uganda.

Luke Nyakarahuka (L)

Uganda Virus Research Institute, Entebbe, Uganda.
Department of Biosecurity, Ecosystems, and Veterinary Public Health, Makerere University, Kampala, Uganda.

Jimmy Baluku (J)

Uganda Virus Research Institute, Entebbe, Uganda.

Jackson Kyondo (J)

Uganda Virus Research Institute, Entebbe, Uganda.

Alex Tumusiime (A)

Uganda Virus Research Institute, Entebbe, Uganda.

Dativa Aliddeki (D)

Africa Centres for Disease Control and Prevention, Addis Ababa, Ethiopia.

Ben Masiira (B)

, African Field Epidemiology Network, Kampala, Uganda.

Esther Muwanguzi (E)

World Health Organization, Geneva, Switzerland.

Ivan Kimuli (I)

World Health Organization, Geneva, Switzerland.

Daniel Bulwadda (D)

, Infectious Diseases Institute, Kampala, Uganda.

Herbert Isabirye (H)

, Infectious Diseases Institute, Kampala, Uganda.

Deborah Aujo (D)

Ministry of Health, Kampala, Uganda.

Arthur Kasambula (A)

Ministry of Health, Kampala, Uganda.

Solome Okware (S)

World Health Organization, Geneva, Switzerland.

Emmanuel Ochien (E)

World Health Organization, Geneva, Switzerland.

Innocent Komakech (I)

World Health Organization, Geneva, Switzerland.

Charles Okot (C)

World Health Organization, Geneva, Switzerland.

Mary Choi (M)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

Caitlin M Cossaboom (CM)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

Carrie Eggers (C)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

John D Klena (JD)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

Modupe O Osinubi (MO)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

Katrin S Sadigh (KS)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

Mary C Worrell (MC)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

Amy L Boore (AL)

United States Centers for Disease Control and Prevention, Kampala, Uganda.

Trevor Shoemaker (T)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

Joel M Montgomery (JM)

United States Centers for Disease Control and Prevention, Atlanta, GA, USA.

Susan N Nabadda (SN)

National Health Laboratory and Diagnostic Services, Kampala, Uganda.

Michael Mwanga (M)

Ministry of Health, Kampala, Uganda.

Allan N Muruta (AN)

Ministry of Health, Kampala, Uganda.

Julie R Harris (JR)

United States Centers for Disease Control and Prevention, Kampala, 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