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Genomic epidemiology of the current wave of artemisinin resistant malaria

Roberto Amato, Olivo Miotto, Charles Woodrow, Jacob Almagro-Garcia, Ipsita Sinha, Susana Campino, Daniel Mead, Eleanor Drury, Mihir Kekre, Mandy Sanders, Alfred Amambua-Ngwa, Chanaki Amaratunga, Lucas Amenga-Etego, Tim J C Anderson, Voahangy Andrianaranjaka, Tobias Apinjoh, Elizabeth Ashley, Sarah Auburn, Gordon A Awandare, Vito Baraka, Alyssa Barry, Maciej F Boni, Steffen Borrmann, Teun Bousema, Oralee Branch, Peter C Bull, Kesinee Chotivanich, David J Conway, Alister Craig, Nicholas P Day, Abdoulaye Djimdé, Christiane Dolecek, Arjen M Dondorp, Chris Drakeley, Patrick Duffy, Diego F Echeverri-Garcia, Thomas G Egwang, Rick M Fairhurst, Abul Faiz Md., Caterina I Fanello, Tran Tinh Hien, Abraham Hodgson, Mallika Imwong, Deus Ishengoma, Pharath Lim, Chanthap Lon, Jutta Marfurt, Kevin Marsh, Mayfong Mayxay, Victor Mobegi, Olugbenga Mokuolu, Jacqui Montgomery, Ivo Mueller, Myat Phone Kyaw, Paul N Newton, Francois Nosten, Rintis Noviyanti, Alexis Nzila, Harold Ocholla, Abraham Oduro, Marie Onyamboko, Jean-Bosco Ouedraogo, Aung Pyae Phyo, Christopher V Plowe, Ric N Price, Sasithon Pukrittayakamee, Milijaona Randrianarivelojosia, Pascal Ringwald, Lastenia Ruiz, David Saunders, Alex Shayo, Peter Siba, Shannon Takala-Harrison, Thuy-Nhien Nguyen Thanh, Vandana Thathy, Federica Verra, Nicholas J White, Ye Htut, Victoria J Cornelius, Rachel Giacomantonio, Dawn Muddyman, Christa Henrichs, Cinzia Malangone, Dushyanth Jyothi, Richard D Pearson, Julian C Rayner, Gilean McVean, Kirk Rockett, Alistair Miles, Paul Vauterin, Ben Jeffery, Magnus Manske, Jim Stalker, Bronwyn MacInnis, Dominic P Kwiatkowski, MalariaGEN Plasmodium falciparum Community Project
doi: https://doi.org/10.1101/019737
Roberto Amato
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Olivo Miotto
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
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Charles Woodrow
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Jacob Almagro-Garcia
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Ipsita Sinha
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
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Susana Campino
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Daniel Mead
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Eleanor Drury
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Mihir Kekre
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Mandy Sanders
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Alfred Amambua-Ngwa
5Medical Research Council Unit, P. O. Box 273, Fajara,Banjul, The Gambia
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Chanaki Amaratunga
6National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland 20892, USA
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Lucas Amenga-Etego
7Navrongo Health Research Centre, Navrongo, Ghana
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Tim J C Anderson
8Texas Biomedical Research Institute, 7620 NW Loop 410, San Antonio, TX 78227, USA
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Voahangy Andrianaranjaka
9Malaria Research Unit, Institut Pasteur de Madagascar, B.P. 1274, Ambatofotsikely, Antananarivo 101, Madagascar
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Tobias Apinjoh
10University of Buea, Cameroon
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Elizabeth Ashley
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
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Sarah Auburn
11Global and Tropical Health Division, Menzies School of Health Research and Charles Darwin University, Darwin, Northern Territories 0811, Australia
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Gordon A Awandare
12West African Centre for Cell Biology of Infectious Pathogens, College of Basic and Applied Sciences, University of Ghana, Legon, Ghana
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Vito Baraka
13National Institute for Medical Research, Tanga - Centre, Tanga, Tanzania
14International Health Unit, Department of Epidemiology, University of Antwerp, Belgium
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Alyssa Barry
15Walter and Eliza Hall Institute, Australia
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Maciej F Boni
16Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Steffen Borrmann
17Kenya Medical Research Institute (KEMRI)/Wellcome Trust Collaborative Research Program, P.O. Box 230-80108, Kilifi, Kenya
18Institute for Tropical Medicine, University of Tübingen, Germany
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Teun Bousema
19London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
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Oralee Branch
20New York University School of Medicine, New York, NY 10010, USA
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Peter C Bull
17Kenya Medical Research Institute (KEMRI)/Wellcome Trust Collaborative Research Program, P.O. Box 230-80108, Kilifi, Kenya
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Kesinee Chotivanich
21Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
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David J Conway
5Medical Research Council Unit, P. O. Box 273, Fajara,Banjul, The Gambia
18Institute for Tropical Medicine, University of Tübingen, Germany
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Alister Craig
22Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK
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Nicholas P Day
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Abdoulaye Djimdé
23Malaria Research and Training Centre, Faculty of Medicine, University of Bamako, Bamako, Mali
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Christiane Dolecek
16Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Arjen M Dondorp
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Chris Drakeley
19London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
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Patrick Duffy
6National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland 20892, USA
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Diego F Echeverri-Garcia
24Department of Entomology, Purdue University, West Lafayette, IN 47907, USA
25International Center for Medical Research and Training, CIDEIM, Cali, Colombia
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Thomas G Egwang
26Med Biotech Laboratories, Plot 3438 / P.O. 9364 Bukasa Rd, Kampala, Uganda
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Rick M Fairhurst
6National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland 20892, USA
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Abul Faiz Md.
27Malaria Research Group & Dev Care Foundation, Dhaka, Bangladesh
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Caterina I Fanello
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
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Tran Tinh Hien
16Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Abraham Hodgson
7Navrongo Health Research Centre, Navrongo, Ghana
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Mallika Imwong
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
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Deus Ishengoma
12West African Centre for Cell Biology of Infectious Pathogens, College of Basic and Applied Sciences, University of Ghana, Legon, Ghana
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Pharath Lim
6National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland 20892, USA
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Chanthap Lon
28Department of Immunology and Medicine, US Army Medical Component, Armed Forces Research Institute of Medical Sciences (USAMC-AFRIMS), Bangkok, Thailand
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Jutta Marfurt
11Global and Tropical Health Division, Menzies School of Health Research and Charles Darwin University, Darwin, Northern Territories 0811, Australia
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Kevin Marsh
17Kenya Medical Research Institute (KEMRI)/Wellcome Trust Collaborative Research Program, P.O. Box 230-80108, Kilifi, Kenya
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Mayfong Mayxay
29Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Vientiane, Lao PDR
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Victor Mobegi
5Medical Research Council Unit, P. O. Box 273, Fajara,Banjul, The Gambia
19London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
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Olugbenga Mokuolu
30Department of Paediatrics and Child Health, University of Ilorin, Ilorin, Nigeria
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Jacqui Montgomery
31Dept of Biology and Entomology, Pennsylvania State University, University Park, PA 16802, USA
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Ivo Mueller
15Walter and Eliza Hall Institute, Australia
32Barcelona Centre for International Health Research, Spain
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Myat Phone Kyaw
33Department of Medical Research Lower Myanmar, Ministry of Health, Yangon, Myanmar
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Paul N Newton
29Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit, Vientiane, Lao PDR
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Francois Nosten
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
34Shoklo Malaria Research Unit, Mae Sot, Tak 63110, Thailand
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Rintis Noviyanti
35Eijkman Institute for Molecular Biology, Jakarta 10430, Indonesia
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Alexis Nzila
36King Fahd University of Petroleum and Minerals, Department of Biology, PO Box 468, Dhahran, 31261, Saudi Arabia
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Harold Ocholla
37Malawi Liverpool Wellcome Trust Clinical Research Programme, Malawi
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Abraham Oduro
7Navrongo Health Research Centre, Navrongo, Ghana
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Marie Onyamboko
38University of Kinshasa, DRC
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Jean-Bosco Ouedraogo
39Institut de Recherche en Sciences de la Santé, Direction Regionale de l’Ouést, Bobo-Dioulasso, Burkina Faso
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Aung Pyae Phyo
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
34Shoklo Malaria Research Unit, Mae Sot, Tak 63110, Thailand
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Christopher V Plowe
40University of Maryland School of Medicine, Baltimore, Maryland 21201, USA
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Ric N Price
11Global and Tropical Health Division, Menzies School of Health Research and Charles Darwin University, Darwin, Northern Territories 0811, Australia
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Sasithon Pukrittayakamee
21Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
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Milijaona Randrianarivelojosia
9Malaria Research Unit, Institut Pasteur de Madagascar, B.P. 1274, Ambatofotsikely, Antananarivo 101, Madagascar
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Pascal Ringwald
41Global Malaria Program, World Health Organization, Geneva, Switzerland
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Lastenia Ruiz
42Universidad Nacional de la Amazonia Peruana, Iquitos, Peru
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David Saunders
28Department of Immunology and Medicine, US Army Medical Component, Armed Forces Research Institute of Medical Sciences (USAMC-AFRIMS), Bangkok, Thailand
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Alex Shayo
43Department of Biotechnology and Bioinformatics, The University of Dodoma, P.O.BOX 338, Dodoma, Tanzania
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Peter Siba
44Papua New Guinea Institute of Medical Research, Madang, Papua New Guinea
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Shannon Takala-Harrison
40University of Maryland School of Medicine, Baltimore, Maryland 21201, USA
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Thuy-Nhien Nguyen Thanh
16Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Vandana Thathy
17Kenya Medical Research Institute (KEMRI)/Wellcome Trust Collaborative Research Program, P.O. Box 230-80108, Kilifi, Kenya
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Federica Verra
19London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
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Nicholas J White
3Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok 10400, Thailand
4Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK
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Ye Htut
33Department of Medical Research Lower Myanmar, Ministry of Health, Yangon, Myanmar
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Victoria J Cornelius
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
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Rachel Giacomantonio
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Dawn Muddyman
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Christa Henrichs
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
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Cinzia Malangone
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Dushyanth Jyothi
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Richard D Pearson
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Julian C Rayner
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Gilean McVean
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
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Kirk Rockett
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Alistair Miles
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Paul Vauterin
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
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Ben Jeffery
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
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Magnus Manske
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Jim Stalker
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Bronwyn MacInnis
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Dominic P Kwiatkowski
1MRC Centre for Genomics and Global Health, Wellcome Trust Centre for Human Genetics, Oxford OX3 7BN, UK
2Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK
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Abstract

Artemisinin resistant Plasmodium falciparum is advancing across Southeast Asia in a soft selective sweep involving at least 20 independent kelch13 mutations. In a large global survey, we find that kelch13 mutations which cause resistance in Southeast Asia are present at low frequency in Africa. We show that African kelch13 mutations have originated locally, and that kelch13 shows a normal variation pattern relative to other genes in Africa, whereas in Southeast Asia there is a great excess of non-synonymous mutations, many of which cause radical amino-acid changes. Thus, kelch13 is not currently undergoing strong selection in Africa, despite a deep reservoir of standing variation that could potentially allow resistance to emerge rapidly. The practical implications are that public health surveillance for artemisinin resistance should not rely on kelch13 data alone, and interventions to prevent resistance must account for local evolutionary conditions, shown by genomic epidemiology to differ greatly between geographical regions.

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Posted May 24, 2015.
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Genomic epidemiology of the current wave of artemisinin resistant malaria
Roberto Amato, Olivo Miotto, Charles Woodrow, Jacob Almagro-Garcia, Ipsita Sinha, Susana Campino, Daniel Mead, Eleanor Drury, Mihir Kekre, Mandy Sanders, Alfred Amambua-Ngwa, Chanaki Amaratunga, Lucas Amenga-Etego, Tim J C Anderson, Voahangy Andrianaranjaka, Tobias Apinjoh, Elizabeth Ashley, Sarah Auburn, Gordon A Awandare, Vito Baraka, Alyssa Barry, Maciej F Boni, Steffen Borrmann, Teun Bousema, Oralee Branch, Peter C Bull, Kesinee Chotivanich, David J Conway, Alister Craig, Nicholas P Day, Abdoulaye Djimdé, Christiane Dolecek, Arjen M Dondorp, Chris Drakeley, Patrick Duffy, Diego F Echeverri-Garcia, Thomas G Egwang, Rick M Fairhurst, Abul Faiz Md., Caterina I Fanello, Tran Tinh Hien, Abraham Hodgson, Mallika Imwong, Deus Ishengoma, Pharath Lim, Chanthap Lon, Jutta Marfurt, Kevin Marsh, Mayfong Mayxay, Victor Mobegi, Olugbenga Mokuolu, Jacqui Montgomery, Ivo Mueller, Myat Phone Kyaw, Paul N Newton, Francois Nosten, Rintis Noviyanti, Alexis Nzila, Harold Ocholla, Abraham Oduro, Marie Onyamboko, Jean-Bosco Ouedraogo, Aung Pyae Phyo, Christopher V Plowe, Ric N Price, Sasithon Pukrittayakamee, Milijaona Randrianarivelojosia, Pascal Ringwald, Lastenia Ruiz, David Saunders, Alex Shayo, Peter Siba, Shannon Takala-Harrison, Thuy-Nhien Nguyen Thanh, Vandana Thathy, Federica Verra, Nicholas J White, Ye Htut, Victoria J Cornelius, Rachel Giacomantonio, Dawn Muddyman, Christa Henrichs, Cinzia Malangone, Dushyanth Jyothi, Richard D Pearson, Julian C Rayner, Gilean McVean, Kirk Rockett, Alistair Miles, Paul Vauterin, Ben Jeffery, Magnus Manske, Jim Stalker, Bronwyn MacInnis, Dominic P Kwiatkowski, MalariaGEN Plasmodium falciparum Community Project
bioRxiv 019737; doi: https://doi.org/10.1101/019737
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Genomic epidemiology of the current wave of artemisinin resistant malaria
Roberto Amato, Olivo Miotto, Charles Woodrow, Jacob Almagro-Garcia, Ipsita Sinha, Susana Campino, Daniel Mead, Eleanor Drury, Mihir Kekre, Mandy Sanders, Alfred Amambua-Ngwa, Chanaki Amaratunga, Lucas Amenga-Etego, Tim J C Anderson, Voahangy Andrianaranjaka, Tobias Apinjoh, Elizabeth Ashley, Sarah Auburn, Gordon A Awandare, Vito Baraka, Alyssa Barry, Maciej F Boni, Steffen Borrmann, Teun Bousema, Oralee Branch, Peter C Bull, Kesinee Chotivanich, David J Conway, Alister Craig, Nicholas P Day, Abdoulaye Djimdé, Christiane Dolecek, Arjen M Dondorp, Chris Drakeley, Patrick Duffy, Diego F Echeverri-Garcia, Thomas G Egwang, Rick M Fairhurst, Abul Faiz Md., Caterina I Fanello, Tran Tinh Hien, Abraham Hodgson, Mallika Imwong, Deus Ishengoma, Pharath Lim, Chanthap Lon, Jutta Marfurt, Kevin Marsh, Mayfong Mayxay, Victor Mobegi, Olugbenga Mokuolu, Jacqui Montgomery, Ivo Mueller, Myat Phone Kyaw, Paul N Newton, Francois Nosten, Rintis Noviyanti, Alexis Nzila, Harold Ocholla, Abraham Oduro, Marie Onyamboko, Jean-Bosco Ouedraogo, Aung Pyae Phyo, Christopher V Plowe, Ric N Price, Sasithon Pukrittayakamee, Milijaona Randrianarivelojosia, Pascal Ringwald, Lastenia Ruiz, David Saunders, Alex Shayo, Peter Siba, Shannon Takala-Harrison, Thuy-Nhien Nguyen Thanh, Vandana Thathy, Federica Verra, Nicholas J White, Ye Htut, Victoria J Cornelius, Rachel Giacomantonio, Dawn Muddyman, Christa Henrichs, Cinzia Malangone, Dushyanth Jyothi, Richard D Pearson, Julian C Rayner, Gilean McVean, Kirk Rockett, Alistair Miles, Paul Vauterin, Ben Jeffery, Magnus Manske, Jim Stalker, Bronwyn MacInnis, Dominic P Kwiatkowski, MalariaGEN Plasmodium falciparum Community Project
bioRxiv 019737; doi: https://doi.org/10.1101/019737

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