A year of genomic surveillance reveals how the SARS-CoV-2 pandemic unfolded in Africa

Eduan Wilkinson, Marta Giovanetti, Houriiyah Tegally, James E. San, Richard Lessells, Diego Cuadros, Darren P. Martin, David A. Rasmussen, Abdel Rahman N. Zekri, Abdoul K. Sangare, Abdoul Salam Ouedraogo, Abdul K. Sesay, Abechi Priscilla, Adedotun Sulaiman Kemi, Adewunmi M. Olubusuyi, Adeyemi O.O. Oluwapelumi, Adnène Hammami, Adrienne A. Amuri, Ahmad Sayed, Ahmed E.O. OumaAida Elargoubi, Nnennaya A. Ajayi, Ajogbasile F. Victoria, Akano Kazeem, Akpede George, Alexander J. Trotter, Ali A. Yahaya, Alpha K. Keita, Amadou Diallo, Amadou Kone, Amal Souissi, Amel Chtourou, Ana V. Gutierrez, Andrew J. Page, Anika Vinze, Arash Iranzadeh, Arnold Lambisia, Arshad Ismail, Audu Rosemary, Augustina Sylverken, Ayoade Femi, Azeddine Ibrahimi, Baba Marycelin, Bamidele S. Oderinde, Bankole Bolajoko, Beatrice Dhaala, Belinda L. Herring, Berthe Marie Njanpop-Lafourcade, Bronwyn Kleinhans, Bronwyn McInnis, Bryan Tegomoh, Cara Brook, Catherine B. Pratt, Cathrine Scheepers, Chantal G. Akoua-Koffi, Charles N. Agoti, Christophe Peyrefitte, Claudia Daubenberger, Collins M. Morang’a, D. James Nokes, Daniel G. Amoako, Daniel L. Bugembe, Danny Park, David Baker, Deelan Doolabh, Deogratius Ssemwanga, Derek Tshiabuila, Diarra Bassirou, Dominic S.Y. Amuzu, Dominique Goedhals, Donwilliams O. Omuoyo, Dorcas Maruapula, Ebenezer Foster-Nyarko, Eddy K. Lusamaki, Edgar Simulundu, Edidah M. Ong’era, Edith N. Ngabana, Edwin Shumba, Elmostafa El Fahime, Emmanuel Lokilo, Enatha Mukantwari, Eromon Philomena, Essia Belarbi, Etienne Simon-Loriere, Etilé A. Anoh, Fabian Leendertz, Faida Ajili, Fakayode O. Enoch, Fares Wasfi, Fatma Abdelmoula, Fausta S. Mosha, Faustinos T. Takawira, Fawzi Derrar, Feriel Bouzid, Folarin Onikepe, Fowotade Adeola, Francisca M. Muyembe, Frank Tanser, Fred A. Dratibi, Gabriel K. Mbunsu, Gaetan Thilliez, Gemma L. Kay, George Githinji, Gert van Zyl, Gordon A. Awandare, Grit Schubert, Gugu P. Maphalala, Hafaliana C. Ranaivoson, Hajar Lemriss, Happi Anise, Haruka Abe, Hela H. Karray, Hellen Nansumba, Hesham A. Elgahzaly, Hlanai Gumbo, Ibtihel Smeti, Ikhlas B. Ayed, Ikponmwosa Odia, Ilhem Boutiba Ben Boubaker, Imed Gaaloul, Inbal Gazy, Innocent Mudau, Isaac Ssewanyana, Iyaloo Konstantinus, Jean B. Lekana-Douk, Jean Claude C. Makangara, Jean Jacques M. Tamfum, Jean Michel Heraud, Jeffrey G. Shaffer, Jennifer Giandhari, Jingjing Li, Jiro Yasuda, Joana Q. Mends, Jocelyn Kiconco, John M. Morobe, John O. Gyapong, Johnson C. Okolie, John T. Kayiwa, Johnathan A. Edwards, Jones Gyamfi, Jouali Farah, Joweria Nakaseegu, Joyce M. Ngoi, Joyce Namulondo, Julia C. Andeko, Julius J. Lutwama, Justin O’Grady, Katherine Siddle, Kayode T. Adeyemi, Kefentse A. Tumedi, Khadija M. Said, Kim Hae-Young, Kwabena O. Duedu, Lahcen Belyamani, Lamia Fki-Berrajah, Lavanya Singh, Leonardo de O. Martins, Lynn Tyers, Magalutcheemee Ramuth, Maha Mastouri, Mahjoub Aouni, Mahmoud el Hefnawi, Maitshwarelo I. Matsheka, Malebogo Kebabonye, Mamadou Diop, Manel Turki, Marietou Paye, Martin M. Nyaga, Mathabo Mareka, Matoke Muhia Damaris, Maureen W. Mburu, Maximillian Mpina, Mba Nwando, Michael Owusu, Michael R. Wiley, Mirabeau T. Youtchou, Mitoha O. Ayekaba, Mohamed Abouelhoda, Mohamed G. Seadawy, Mohamed K. Khalifa, Mooko Sekhele, Mouna Ouadghiri, Moussa M. Diagne, Mulenga Mwenda, Mushal Allam, My V.T. Phan, Nabil Abid, Nadia Touil, Nadine Rujeni, Najla Kharrat, Nalia Ismael, Ndongo Dia, Nedio Mabunda, Nei Yuan Hsiao, Nelson B. Silochi, Ngoy Nsenga, Nicksy Gumede, Nicola Mulder, Nnaemeka Ndodo, Norosoa H. Razanajatovo, Nosamiefan Iguosadolo, Oguzie Judith, Ojide C. Kingsley, Okogbenin Sylvanus, Okokhere Peter, Oladiji Femi, Olawoye Idowu, Olumade Testimony, Omoruyi E. Chukwuma, Onwe E. Ogah, Chika K. Onwuamah, Oshomah Cyril, Ousmane Faye, Oyewale Tomori, Pascale Ondoa, Patrice Combe, Patrick Semanda, Paul E. Oluniyi, Paulo Arnaldo, Peter K. Quashie, Philippe Dussart, Phillip A. Bester, Placide K. Mbala, Reuben Ayivor-Djanie, Richard Njouom, Richard O. Phillips, Richmond Gorman, Robert A. Kingsley, Rosina A.A. Carr, Saâd El Kabbaj, Saba Gargouri, Saber Masmoudi, Safietou Sankhe, Salako B. Lawal, Samar Kassim, Sameh Trabelsi, Samar Metha, Sami Kammoun, Sanaâ Lemriss, Sara H.A. Agwa, Sébastien Calvignac-Spencer, Stephen F. Schaffner, Seydou Doumbia, Sheila M. Mandanda, Sherihane Aryeetey, Shymaa S. Ahmed, Siham Elhamoumi, Soafy Andriamandimby, Sobajo Tope, Sonia Lekana-Douki, Sophie Prosolek, Soumeya Ouangraoua, Steve A. Mundeke, Steven Rudder, Sumir Panji, Sureshnee Pillay, Susan Engelbrecht, Susan Nabadda, Sylvie Behillil, Sylvie L. Budiaki, Sylvie van der Werf, Tapfumanei Mashe, Tarik Aanniz, Thabo Mohale, Thanh Le-Viet, Tobias Schindler, Ugochukwu J. Anyaneji, Ugwu Chinedu, Upasana Ramphal, Uwanibe Jessica, Uwem George, Vagner Fonseca, Vincent Enouf, Vivianne Gorova, Wael H. Roshdy, William K. Ampofo, Wolfgang Preiser, Wonderful T. Choga, Yaw Bediako, Yeshnee Naidoo, Yvan Butera, Zaydah R. de Laurent, Amadou A. Sall, Ahmed Rebai, Anne von Gottberg, Bourema Kouriba, Carolyn Williamson, Daniel J. Bridges, Ihekweazu Chikwe, Jinal N. Bhiman, Madisa Mine, Matthew Cotten, Sikhulile Moyo, Simani Gaseitsiwe, Ngonda Saasa, Pardis C. Sabeti, Pontiano Kaleebu, Yenew K. Tebeje, Sofonias K. Tessema, Christian Happi, John Nkengasong, Tulio de Oliveira*

*Corresponding author for this work

    Research output: Contribution to journalArticlepeer-review

    109 Citations (SciVal)

    Abstract

    The progression of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic in Africa has so far been heterogeneous, and the full impact is not yet well understood. In this study, we describe the genomic epidemiology using a dataset of 8746 genomes from 33 African countries and two overseas territories. We show that the epidemics in most countries were initiated by importations predominantly from Europe, which diminished after the early introduction of international travel restrictions. As the pandemic progressed, ongoing transmission in many countries and increasing mobility led to the emergence and spread within the continent of many variants of concern and interest, such as B.1.351, B.1.525, A.23.1, and C.1.1. Although distorted by low sampling numbers and blind spots, the findings highlight that Africa must not be left behind in the global pandemic response, otherwise it could become a source for new variants.
    Original languageEnglish
    Pages (from-to)423-431
    Number of pages9
    JournalScience
    Volume374
    Issue number6566
    DOIs
    Publication statusPublished (VoR) - 22 Oct 2021

    Funding

    The University of Ghana (WACCBIP) team was funded by a Wellcome/African Academy of Sciences Developing Excellence in Leadership Training and Science (DELTAS) grant (DEL-15-007 and 107755/Z/15/Z: Awandare); National Institute of Health Research (NIHR) (17.63.91) grants using UK aid from the UK government for a global health research group for genomic surveillance of malaria in West Africa (Wellcome Sanger Institute, UK) and the global research unit for Tackling Infections to Benefit Africa (TIBA partnership, University of Edinburgh); and a World Bank African Centres of Excellent grant (WACCBIP-NCDs: Awandare). Project ADAGE PRFCOV19-GP2 (2020-2022) includes 40 researchers from the Center of Biotechnology of Sfax, the University of Sfax, the University of Monastir, the University Hospital Hédi Chaker of Sfax, the Military Hospital of Tunis, and Dacima Consulting. Ministry of Higher Education and Scientific Research and Ministry of Health of the Republic of Tunisia. The Uganda contributions were funded by the UK Medical Research Council (MRC/UKRI) and the UK Department for International Development (DFID) under the MRC/ DFID concordat agreement (grant agreement number NC_PC_19060) and by the Wellcome, DFID–Wellcome Epidemic Preparedness–Coronavirus (grant agreement number 220977/Z/ 20/Z) awarded to M.C. Work from Quadram Institute Bioscience was funded by The Biotechnology and Biological Sciences Research Council Institute Strategic Programme Microbes in the Food Chain BB/ R012504/1 and its constituent projects BBS/E/F/000PR10348, BBS/E/F/000PR10349, BBS/E/F/000PR10351, and BBS/E/F/ 000PR10352 and by the Quadram Institute Bioscience BBSRC–funded Core Capability Grant (project number BB/CCG1860/1). The Africa Pathogen Genomics Initiative (Africa PGI) at the Africa CDC is supported by the Bill & Melinda Gates Foundation (INV018978 and INV018278), Illumina Inc, the US Centers for Disease Control and Prevention (CDC), and Oxford Nanopore Technologies. Sequences generated in Zambia through PATH were funded by the Bill & Melinda Gates Foundation. The findings and conclusions contained within are those of the authors and do not necessarily reflect positions or policies of the Bill & Melinda Gates Foundation. Funding for sequencing in Côte d’Ivoire, Burkina Faso, and part of the sequencing in the DRC was granted by the German Federal Ministry of Education and Research (BMBF). Sequencing efforts from Morocco have been supported by Academie Hassan II of Science and Technology, Morocco. Funding for surveillance, sampling, and testing in Madagasar was provided by the WHO, the CDC (grant U5/ IP000812-05), the US Agency for International Development (USAID; cooperation agreement 72068719CA00001), and the Office of the Assistant Secretary for Preparedness and Response in the US Department of Health and Human Services (DHHS; grant number IDSEP190051-01-0200). Funding for sequencing was provided by the Bill & Melinda Gates Foundation (GCE/ID OPP1211841), Chan Zuckerberg Biohub, and the Innovative Genomics Institute at UC Berkeley. The Botswana Harvard AIDS Institute was supported by the following funding: H3ABioNet through funding from the National Institutes of Health Common Fund (U41HG006941)—H3ABioNet is an initiative of the Human Health and Heredity in Africa Consortium (H3Africa) program of the African Academy of Science (AAS); DHHS–NIH–National Institute of Allergy and Infectious Diseases (NIAID) (5K24AI131928-04 and 5K24AI131924-04); Sub-Saharan African Network for TB/HIV Research Excellence (SANTHE); a DELTAS Africa Initiative (grant DEL-15-0060—the DELTAS Africa Initiative is an independent funding scheme of the AAS’s Alliance for Accelerating Excellence in Science in Africa (AESA) and supported by the New Partnership for Africa’s Development Planning and Coordinating Agency (NEPAD Agency) with funding from the Wellcome Trust [grant 107752/Z/15/Z] and the UK government; and the South African Medical Research Council (SAMRC) and the Department of Technology and Innovation as part of the Network for Genomic Surveillance in South Africa (NGS-SA) and the Stellenbosch University Faculty of Medicine & Health Sciences, Strategic Equipment Fund. D.P.M. is funded by the Wellcome Trust (Wellcome Trust grant 222574/Z/21/Z). Sequencing activities at the NICD were supported by a conditional grant from the South African National Department of Health as part of the emergency COVID-19 response; a cooperative agreement between the National Institute for Communicable Diseases of the National Health Laboratory Service and the U.S. Centers for Disease Control and Prevention (grant number 5 U01IP001048-05-00); the African Society of Laboratory Medicine (ASLM) and Africa Centers for Disease Control and Prevention through a sub-award from the Bill and Melinda Gates Foundation grant number INV-018978; the UK Foreign, Commonwealth and Development Office and Wellcome (Grant no 221003/Z/20/Z); the South African Medical Research Council (Reference number SHIPNCD 76756); the UK Department of Health and Social Care, managed by the Fleming Fund and performed under the auspices of the SEQAFRICA project. Furthermore, pandemic surveillance in South Africa and Senegal was supported in part through NIH grant U01 AI151698 for the United World Antiviral Research Network (UWARN). Support for pandemic surveillance from the Tulio de Oliveira group to other African countries is funded by the Rockefeller Foundation. Sequencing efforts in the DRC were funded by the Bill & Melinda Gates Foundation under grant INV-018030 awarded to C.B.P. and further supported by funding from the Africa CDC through the ASLM (African Society of Laboratory Medicine) for Accelerating SARSCoV-2 Genomic Surveillance in Africa. Sequencing efforts in Rwanda were commissioned by the NIHR Global Health Research program (16/ 136/33) using UK aid from the UK government (funding to E.M. and N. R. through TIBA partnership) and additional funds from the government of Rwanda through RBC/National Reference Laboratory in collaboration with the Belgian Development Agency (ENABEL) for additional genomic sequencing at GIGA Research Institute–Liege/ Belgium. The sequencing effort in Equatorial Guinea was supported by a public-private partnership, the Bioko Island Malaria Elimination Project, composed of the government of Equatorial Guinea Ministries of Mines and Hydrocarbons, and Health and Social Welfare, Marathon EG Production Limited, Noble Energy, Atlantic Methanol Production Company, and EG LNG. Sample collection and typing in Mali were supported by Fondation Merieux–France, and sequence efforts have been supported by the Enable and Enhance Initiative of the German Federal Government’s Security Cooperation against Biological Threats in the G5 Sahel Region. The Nigeria work was made possible by support from Flu Lab and a cohort of generous donors through TED’s Audacious Project, including the ELMA Foundation, MacKenzie Scott, the Skoll Foundation, and Open Philanthropy. Further Nigeria funding came from grants from the NIAID (www.niaid.nih. gov), NIH-H3Africa (https://h3africa.org) (U01HG007480 and U54HG007480), and the World Bank grant (worldbank.org) (ACE IMPACT project) to C.H. Analysis for the Gabon strains was supported by the Science and Technology Research Partnership for Sustainable Development (SATREPS), Japan International Cooperation Agency (JICA), and Japan Agency for Medical Research and Development (AMED) (grant number JP20jm0110013) and a grant from AMED (grant number JP20wm0225003). Sequencing at KEMRI-Wellcome Trust Research Programme site in Kenya was supported by the National Institute for Health Research (NIHR) (project references 17/ 63/82 and 16/136/33), using UK aid from the UK Government to support global health research, and the UK Foreign, Commonwealth and Development Office and Wellcome Trust (grant# 102975; 220985).

    FundersFunder number
    Africa Pathogen Genomics Initiative
    African Society of Laboratory Medicine
    Atlantic Methanol Production Company
    Bioko Island Malaria Elimination Project
    Center of Biotechnology of Sfax
    DELTASDEL-15-007, 107755/Z/15/Z
    Department of Technology and Innovation
    Fleming FundU01 AI151698
    Fondation Merieux–France
    Health and Social Welfare
    Human Health and Heredity in Africa Consortium
    Innovative Genomics Institute at UC Berkeley
    KEMRI-Wellcome
    Marathon EG Production Limited
    Ministry of Health of the Republic of Tunisia
    NIH-H3AfricaU54HG007480, U01HG007480
    National Institute for Communicable Diseases
    National Institutes of Health Common FundU41HG006941
    Noble Energy
    Office of the Assistant Secretary for Preparedness and Response
    PGI
    Skoll Foundation
    Stellenbosch University Faculty of Medicine & Health Sciences
    Strategic Equipment Fund222574/Z/21/Z
    United World Antiviral Research Network
    University Hospital Hédi Chaker of Sfax
    WACCBIP
    Wellcome Sanger Institute
    Wellcome/African Academy of Sciences Developing Excellence in Leadership Training and Science
    World Bank African Centres of Excellent2020-2022, ADAGE PRFCOV19-GP2
    National Institutes of Health
    U.S. Department of Health and Human ServicesGCE/ID OPP1211841, IDSEP190051-01-0200
    Centers for Disease Control and Prevention5 U01IP001048-05-00
    National Institute of Allergy and Infectious DiseasesDEL-15-0060, K24AI131924, 5K24AI131928-04
    United States Agency for International Development72068719CA00001
    Bill and Melinda Gates FoundationINV018278, INV018978
    Rockefeller FoundationINV-018030
    World Bank Group
    World Health OrganizationU5/ IP000812-05
    National Department of Health
    Japan Agency for Medical Research and DevelopmentJP20jm0110013, JP20wm0225003
    Wellcome Trust220977/Z/ 20/Z, 107752/Z/15/Z
    Oxford Nanopore Technologies
    Ministère de l’Enseignement Supérieur et de la Recherche Scientifique
    Government of the United Kingdom
    UK Research and Innovation
    Université Monastir
    Medical Research Council
    National Institute for Health and Care Research17.63.91, 16/136/33, 17/ 63/82
    Department of Health and Social Care
    Department for International Development, UK GovernmentNC_PC_19060
    South African Medical Research Council
    Bundesministerium für Bildung und Forschung
    Japan International Cooperation Agency
    Belgisch Ontwikkelingsagentschap
    University of Ghana
    Science and Technology Research Partnership for Sustainable Development
    New Partnership for Africa's Development
    Quadram Institute BioscienceBBS/E/F/ 000PR10352, BB/ R012504/1, BBS/E/F/000PR10351, BB/CCG1860/1, BBS/E/F/000PR10349, BBS/E/F/000PR10348
    ELMA Foundation
    National Health Laboratory Service
    African Academy of Sciences
    Université de Sfax
    Foreign, Commonwealth and Development Office221003/Z/20/Z, SHIPNCD 76756, 102975, 220985

      Keywords

      • Africa/epidemiology COVID-19/*epidemiology/transmission/virology *Epidemiological Monitoring Genetic Variation *Genomics Humans *Pandemics SARS-CoV-2/*genetics/isolation & purification

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