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. 2022 Oct 7;378(6615):eabq5358.
doi: 10.1126/science.abq5358. Epub 2022 Oct 7.

The evolving SARS-CoV-2 epidemic in Africa: Insights from rapidly expanding genomic surveillance

Houriiyah Tegally #  1   2 , James E San  1   2 , Matthew Cotten  3   4 , Monika Moir  1 , Bryan Tegomoh  5   6 , Gerald Mboowa  7 , Darren P Martin  8   9 , Cheryl Baxter  1   10 , Arnold W Lambisia  11 , Amadou Diallo  12 , Daniel G Amoako  13   14 , Moussa M Diagne  12 , Abay Sisay  15   16 , Abdel-Rahman N Zekri  17 , Abdou Salam Gueye  18 , Abdoul K Sangare  19 , Abdoul-Salam Ouedraogo  20 , Abdourahmane Sow  21 , Abdualmoniem O Musa  22   23   24 , Abdul K Sesay  25 , Abe G Abias  26 , Adam I Elzagheid  27 , Adamou Lagare  28 , Adedotun-Sulaiman Kemi  29 , Aden Elmi Abar  30 , Adeniji A Johnson  31   32 , Adeola Fowotade  33   34 , Adeyemi O Oluwapelumi  35   36 , Adrienne A Amuri  37   38 , Agnes Juru  39 , Ahmed Kandeil  40 , Ahmed Mostafa  40 , Ahmed Rebai  41 , Ahmed Sayed  42 , Akano Kazeem  43   44 , Aladje Balde  45   46 , Alan Christoffels  7   47 , Alexander J Trotter  48 , Allan Campbell  49 , Alpha K Keita  50   51 , Amadou Kone  52 , Amal Bouzid  41   53 , Amal Souissi  41 , Ambrose Agweyu  11 , Amel Naguib  54 , Ana V Gutierrez  48 , Anatole Nkeshimana  55 , Andrew J Page  48 , Anges Yadouleton  56 , Anika Vinze  57 , Anise N Happi  43 , Anissa Chouikha  58   59 , Arash Iranzadeh  8   9 , Arisha Maharaj  1 , Armel L Batchi-Bouyou  60   61 , Arshad Ismail  13 , Augustina A Sylverken  62   63 , Augustine Goba  64   65 , Ayoade Femi  43   44 , Ayotunde E Sijuwola  43 , Baba Marycelin  66   67 , Babatunde L Salako  29   32 , Bamidele S Oderinde  66 , Bankole Bolajoko  43 , Bassirou Diarra  52 , Belinda L Herring  18 , Benjamin Tsofa  11 , Bernard Lekana-Douki  68   69 , Bernard Mvula  70 , Berthe-Marie Njanpop-Lafourcade  18 , Blessing T Marondera  71 , Bouh Abdi Khaireh  72   73 , Bourema Kouriba  19 , Bright Adu  74 , Brigitte Pool  75 , Bronwyn McInnis  17 , Cara Brook  76   77 , Carolyn Williamson  9   10   78 , Cassien Nduwimana  55 , Catherine Anscombe  79   80 , Catherine B Pratt  81 , Cathrine Scheepers  13   82 , Chantal G Akoua-Koffi  83   84 , Charles N Agoti  11   85 , Chastel M Mapanguy  60   86 , Cheikh Loucoubar  12 , Chika K Onwuamah  87 , Chikwe Ihekweazu  88 , Christian N Malaka  89 , Christophe Peyrefitte  12 , Chukwa Grace  43   44 , Chukwuma E Omoruyi  33   34 , Clotaire D Rafaï  90 , Collins M Morang'a  91 , Cyril Erameh  92 , Daniel B Lule  3 , Daniel J Bridges  93 , Daniel Mukadi-Bamuleka  37 , Danny Park  57 , David A Rasmussen  94   95 , David Baker  48 , David J Nokes  11   96 , Deogratius Ssemwanga  3   97 , Derek Tshiabuila  2 , Dominic S Y Amuzu  91 , Dominique Goedhals  98 , Donald S Grant  64   65   99 , Donwilliams O Omuoyo  11 , Dorcas Maruapula  100 , Dorcas W Wanjohi  7 , Ebenezer Foster-Nyarko  48 , Eddy K Lusamaki  37   38   51 , Edgar Simulundu  101 , Edidah M Ong'era  11 , Edith N Ngabana  37   38 , Edward O Abworo  102 , Edward Otieno  11 , Edwin Shumba  71 , Edwine Barasa  11 , El Bara Ahmed  103   104 , Elhadi A Ahmed  23 , Emmanuel Lokilo  37 , Enatha Mukantwari  105 , Eromon Philomena  43 , Essia Belarbi  106 , Etienne Simon-Loriere  107 , Etilé A Anoh  83 , Eusebio Manuel  108 , Fabian Leendertz  106 , Fahn M Taweh  109 , Fares Wasfi  58 , Fatma Abdelmoula  41   110 , Faustinos T Takawira  39 , Fawzi Derrar  111 , Fehintola V Ajogbasile  43 , Florette Treurnicht  112   113 , Folarin Onikepe  43   44 , Francine Ntoumi  60   114 , Francisca M Muyembe  37   38 , Frank E Z Ragomzingba  115 , Fred A Dratibi  116   18 , Fred-Akintunwa Iyanu  43 , Gabriel K Mbunsu  38 , Gaetan Thilliez  48 , Gemma L Kay  48 , George O Akpede  92 , Gert U van Zyl  117   118 , Gordon A Awandare  91 , Grace S Kpeli  119   120 , Grit Schubert  106 , Gugu P Maphalala  121 , Hafaliana C Ranaivoson  77 , Hannah E Omunakwe  122 , Harris Onywera  7 , Haruka Abe  123 , Hela Karray  124 , Hellen Nansumba  125 , Henda Triki  58 , Herve Albéric Adje Kadjo  126 , Hesham Elgahzaly  127 , Hlanai Gumbo  39 , Hota Mathieu  128 , Hugo Kavunga-Membo  37 , Ibtihel Smeti  41 , Idowu B Olawoye  43 , Ifedayo M O Adetifa  88   129 , Ikponmwosa Odia  92 , Ilhem Boutiba Ben Boubaker  130   131 , Iluoreh Ahmed Muhammad  43 , Isaac Ssewanyana  125 , Isatta Wurie  132 , Iyaloo S Konstantinus  133 , Jacqueline Wemboo Afiwa Halatoko  134 , James Ayei  26 , Janaki Sonoo  135 , Jean-Claude C Makangara  37   38 , Jean-Jacques M Tamfum  37   38 , Jean-Michel Heraud  12   77 , Jeffrey G Shaffer  136 , Jennifer Giandhari  2 , Jennifer Musyoki  11 , Jerome Nkurunziza  137 , Jessica N Uwanibe  43 , Jinal N Bhiman  13   113 , Jiro Yasuda  123 , Joana Morais  138   139 , Jocelyn Kiconco  97 , John D Sandi  64   65 , John Huddleston  140 , John K Odoom  74 , John M Morobe  11 , John O Gyapong  119 , John T Kayiwa  3 , Johnson C Okolie  43 , Joicymara S Xavier  1   141   142 , Jones Gyamfi  119 , Joseph F Wamala  143 , Joseph H K Bonney  74 , Joseph Nyandwi  55   144 , Josie Everatt  13 , Joweria Nakaseegu  97 , Joyce M Ngoi  91 , Joyce Namulondo  97 , Judith U Oguzie  43   44 , Julia C Andeko  68 , Julius J Lutwama  3 , Juma J H Mogga  143 , Justin O'Grady  48 , Katherine J Siddle  57 , Kathleen Victoir  145 , Kayode T Adeyemi  43   44 , Kefentse A Tumedi  146 , Kevin S Carvalho  147 , Khadija Said Mohammed  11 , Koussay Dellagi  145 , Kunda G Musonda  148 , Kwabena O Duedu  119   120 , Lamia Fki-Berrajah  124 , Lavanya Singh  2 , Lenora M Kepler  94   95 , Leon Biscornet  75 , Leonardo de Oliveira Martins  48 , Lucious Chabuka  149 , Luicer Olubayo  8 , Lul Deng Ojok  26 , Lul Lojok Deng  26 , Lynette I Ochola-Oyier  11 , Lynn Tyers  9 , Madisa Mine  150 , Magalutcheemee Ramuth  135 , Maha Mastouri  151   152 , Mahmoud ElHefnawi  153 , Maimouna Mbanne  12 , Maitshwarelo I Matsheka  146 , Malebogo Kebabonye  154 , Mamadou Diop  12 , Mambu Momoh  64   65   155 , Maria da Luz Lima Mendonça  147 , Marietjie Venter  156 , Marietou F Paye  57 , Martin Faye  12 , Martin M Nyaga  157 , Mathabo Mareka  158 , Matoke-Muhia Damaris  159 , Maureen W Mburu  11 , Maximillian G Mpina  160   161   162 , Michael Owusu  163 , Michael R Wiley  81   164 , Mirabeau Y Tatfeng  165 , Mitoha Ondo'o Ayekaba  161 , Mohamed Abouelhoda  166   167 , Mohamed Amine Beloufa  111 , Mohamed G Seadawy  168   169 , Mohamed K Khalifa  170 , Mooko Marethabile Matobo  158 , Mouhamed Kane  12 , Mounerou Salou  171 , Mphaphi B Mbulawa  154 , Mulenga Mwenda  93 , Mushal Allam  172 , My V T Phan  3 , Nabil Abid  151   173 , Nadine Rujeni  174   175 , Nadir Abuzaid  176 , Nalia Ismael  177 , Nancy Elguindy  54 , Ndeye Marieme Top  12 , Ndongo Dia  12 , Nédio Mabunda  177 , Nei-Yuan Hsiao  9   78 , Nelson Boricó Silochi  161 , Ngiambudulu M Francisco  138 , Ngonda Saasa  178 , Nicholas Bbosa  3 , Nickson Murunga  11 , Nicksy Gumede  18 , Nicole Wolter  13   113 , Nikita Sitharam  1 , Nnaemeka Ndodo  88 , Nnennaya A Ajayi  179 , Noël Tordo  180 , Nokuzola Mbhele  9 , Norosoa H Razanajatovo  77 , Nosamiefan Iguosadolo  43 , Nwando Mba  88 , Ojide C Kingsley  181 , Okogbenin Sylvanus  92 , Oladiji Femi  182 , Olubusuyi M Adewumi  31   32 , Olumade Testimony  43   44 , Olusola A Ogunsanya  43 , Oluwatosin Fakayode  183 , Onwe E Ogah  184 , Ope-Ewe Oludayo  43 , Ousmane Faye  12 , Pamela Smith-Lawrence  154 , Pascale Ondoa  71 , Patrice Combe  185 , Patricia Nabisubi  186   187 , Patrick Semanda  125 , Paul E Oluniyi  43 , Paulo Arnaldo  177 , Peter Kojo Quashie  91 , Peter O Okokhere  92   188 , Philip Bejon  11 , Philippe Dussart  77 , Phillip A Bester  189 , Placide K Mbala  37   38 , Pontiano Kaleebu  3   97 , Priscilla Abechi  43   44 , Rabeh El-Shesheny  40   190 , Rageema Joseph  9 , Ramy Karam Aziz  191   192 , René G Essomba  193   194 , Reuben Ayivor-Djanie  91   119   120 , Richard Njouom  195 , Richard O Phillips  63 , Richmond Gorman  63 , Robert A Kingsley  48 , Rosa Maria D E S A Neto Rodrigues  196   197 , Rosemary A Audu  29 , Rosina A A Carr  119   120 , Saba Gargouri  124 , Saber Masmoudi  41 , Sacha Bootsma  143 , Safietou Sankhe  12 , Sahra Isse Mohamed  198 , Saibu Femi  43 , Salma Mhalla  131   199 , Salome Hosch  160   200 , Samar Kamal Kassim  127 , Samar Metha  57 , Sameh Trabelsi  201 , Sara Hassan Agwa  127 , Sarah Wambui Mwangi  7 , Seydou Doumbia  52 , Sheila Makiala-Mandanda  37   38 , Sherihane Aryeetey  63 , Shymaa S Ahmed  54 , Side Mohamed Ahmed  103 , Siham Elhamoumi  57 , Sikhulile Moyo  100   202 , Silvia Lutucuta  138 , Simani Gaseitsiwe  100   202 , Simbirie Jalloh  64   65 , Soa Fy Andriamandimby  77 , Sobajo Oguntope  43 , Solène Grayo  180 , Sonia Lekana-Douki  68 , Sophie Prosolek  48 , Soumeya Ouangraoua  203   204 , Stephanie van Wyk  1 , Stephen F Schaffner  57 , Stephen Kanyerezi  186   187 , Steve Ahuka-Mundeke  37   38 , Steven Rudder  48 , Sureshnee Pillay  2 , Susan Nabadda  125 , Sylvie Behillil  205 , Sylvie L Budiaki  158 , Sylvie van der Werf  205 , Tapfumanei Mashe  39   206 , Thabo Mohale  13 , Thanh Le-Viet  48 , Thirumalaisamy P Velavan  114   207 , Tobias Schindler  160   161   200 , Tongai G Maponga  117 , Trevor Bedford  140   208 , Ugochukwu J Anyaneji  2 , Ugwu Chinedu  43   44 , Upasana Ramphal  2   10   209 , Uwem E George  43 , Vincent Enouf  205 , Vishvanath Nene  102 , Vivianne Gorova  210   211 , Wael H Roshdy  54 , Wasim Abdul Karim  1 , William K Ampofo  212 , Wolfgang Preiser  117   118 , Wonderful T Choga  100   213 , Yahaya Ali Ahmed  18 , Yajna Ramphal  1 , Yaw Bediako  91   214 , Yeshnee Naidoo  2 , Yvan Butera  174   215   216 , Zaydah R de Laurent  11 ; Africa Pathogen Genomics Initiative (Africa PGI)‡; Ahmed E O Ouma  7 , Anne von Gottberg  13   113 , George Githinji  11   217 , Matshidiso Moeti  18 , Oyewale Tomori  43 , Pardis C Sabeti  57 , Amadou A Sall  12 , Samuel O Oyola  102 , Yenew K Tebeje  7 , Sofonias K Tessema  7 , Tulio de Oliveira  1   2   10   218 , Christian Happi  43   44 , Richard Lessells  2 , John Nkengasong  7 , Eduan Wilkinson #  1   2
Affiliations

The evolving SARS-CoV-2 epidemic in Africa: Insights from rapidly expanding genomic surveillance

Houriiyah Tegally et al. Science. .

Abstract

Investment in severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) sequencing in Africa over the past year has led to a major increase in the number of sequences that have been generated and used to track the pandemic on the continent, a number that now exceeds 100,000 genomes. Our results show an increase in the number of African countries that are able to sequence domestically and highlight that local sequencing enables faster turnaround times and more-regular routine surveillance. Despite limitations of low testing proportions, findings from this genomic surveillance study underscore the heterogeneous nature of the pandemic and illuminate the distinct dispersal dynamics of variants of concern-particularly Alpha, Beta, Delta, and Omicron-on the continent. Sustained investment for diagnostics and genomic surveillance in Africa is needed as the virus continues to evolve while the continent faces many emerging and reemerging infectious disease threats. These investments are crucial for pandemic preparedness and response and will serve the health of the continent well into the 21st century.

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Figures

Fig. 1.
Fig. 1.. Epidemiological progression of the COVID-19 pandemic on the African continent.
(A) Total reported new case counts per million inhabitants in Africa (Data Source: Our World in Data; OWID; log-transformed) along with the distribution of VOCs, the Eta VOI and other lineages through time (size of circles proportional to the number of genomes sampled per month for each category). (B to F) Breakdown of reported new cases per million (Data Source: Our World in Data; OWID; log-transformed) and monthly sampling of VOCs, regional variant or lineage of interest and other lineages for three selected countries for North, Southern, West, Central and East Africa respectively. For each region, a different variant or lineage of interest is shown, relevant to that region (C.36, C.1.2, Eta, B.1.620 and A.23.1, respectively).
Fig. 2.
Fig. 2.. Sequencing strategies and outputs in Africa.
(A) Geographical representation of all countries (shaded in gray) and institutions (red dots) in Africa with their own on-site sequencing facilities. The inset graph shows the number of countries in Africa able to carry out sequencing locally over time. (B) Key regional sequencing hubs and networks in Africa showing countries (shaded in bright colors) and institutions (red dots) that have sequenced for other countries (shaded in corresponding light colors and linking curves) on the continent. CERI: Centre for Epidemic Response and Innovation; KRISP: KwaZulu-Natal Research Innovation and Sequencing Platform; NICD: National Institute for Communicable Diseases; KEMRI-WT: Kenya Medical Research Institute - Wellcome Trust; ILRI: International Livestock Research Institute; MRC/UVRI: Medical Research Council/Uganda Virus Research Institute; INRB: Institut National de Recherche Biomédicale; ACEGID: African Centre of Excellence for Genomics of Infectious Diseases; NMIMR: Noguchi Memorial Institute for Medical Research; MRCG: Medical Research Council Unit - The Gambia; IPD: Institut Pasteur de Dakar. (C) Geographical representation of the total number of SARS-CoV-2 whole genomes produced over the course of the pandemic in each country, as well as the proportion of those sequences that were produced locally, regionally or abroad. (D) Correlation of the proportion of COVID-19 positive cases that have been sequenced and the corresponding number of epidemiological weeks since the start of the pandemic that are represented with genomes for each African country. The color of each circle represents the number of cases and its size the number of genomes. (E) Comparison of sequencing turn-around times (lag times from sample collection to sequence submission) for the three strategies of sequencing in Africa, showing a significant difference in the means (p-value<0.0001). The box and whisker plot denote the lower quartile, median and upper quartile (box), the minimum and maximum values (whisker), and outliers (black dots). (F) Pearson correlations of the total number of sequencing laboratories per country against key sequencing outputs.
Fig. 3.
Fig. 3.. Genome gap analysis.
(A) Shows the mean N count per genome by month of submission to GISAID. The dates for the detection of important SARS-CoV-2 lineages are indicated at the top of the figure. (B) Illustrates the mean N count per genome stratified by sequencing technology. (C) Shows the mean N count per genome stratified by the sequencing primers sets used. For panels A to C, error bars indicate 95% confidence intervals. (D) Mean N count per genome by lineage. The mean N data were stratified by SARS-CoV-2 lineages to investigate lineage-specific frequency of genome gaps, an indirect measure of primer mismatch. All lineages present at least 100 times in the genome data were presented.
Fig. 4.
Fig. 4.. Inferred viral dissemination patterns of VOCs within Africa.
(A) Genomic prevalence of VOCs Alpha, Beta, Delta and Omicron in Africa over time. (B) Inferred viral exchange patterns to, from and within the Africa continent for the four VOCs (Omicron as BA.1 and BA.2) based on case-sensitive phylogeographic inference. Introductions and viral transitions within Africa are shown in solid lines and exports from Africa are shown in dotted lines and these are colored by continent. The shaded areas around the lines represent uncertainty of this analysis from ten replicates (+/− s.d.). (C) Dissemination patterns of the VOCs within Africa, from inferred ancestral state reconstructions performed on Africa enriched datasets, annotated and colored by region in Africa. The countries of origin of viral exchange routes are also shown with dots and the curves go from country of origin to destination country in an anti-clockwise direction.
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