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1.
Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Lwin KM, Ariey F, Hanpithakpong W, Lee SJ, Ringwald P, Kamolrat S, Imwong M, Chotivanich K, Lim P, Herdman T, An SS, Yeung S, Singhasivanon P, Day NPJ, Lindegardh N, Socheat D, White NJ, 2009. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361: 455–467.
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2.
Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, Sreng S, Anderson JM, Mao S, Sam B, Sopha C, Chuor CM, Nguon C, Sovannaroth S, Pukrittayakamee S, Jittamala P, Chotivanich K, Chutasmit K, Suchatsoonthorn C, Runcharoen R, Hien TT, Thuy-Nhien NT, Thanh NV, Phu NH, Htut Y, Han KT, Aye KH, Mokuolu OA, Olaosebikan RR, Folaranmi OO, Mayxay M, Khantavong M, Hongvanthong B, Newton PN, Onyamboko MA, Fanello CI, Tshefu AK, Mishra N, Valecha N, Phyo AP, Nosten F, Yi P, Tripura R, Borrmann S, Bashraheil M, Peshu J, Faiz MA, Ghose A, Hossain MA, Samad R, Rahman MR, Hasan MM, Islam A, Miotto O, Amato R, Macinnis B, Stalker J, Kwiatkowski DP, Bozdech Z, Jeeyapant A, Cheah PY, Sakulthaew T, Chalk J, Intharabut B, Silamut K, Lee SJ, Vihokhern B, Kunasol C, Imwong M, Tarning J, Taylor WJ, Yeung S, Woodrow CJ, Flegg JA, Das D, Smith J, Venkatesan M, Plowe CV, Stepniewska K, Guerin PJ, Dondrop AM, Day NP, White NJ, 2014. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 371: 411–423.
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3.
World Health Organization, 2016. Artemisinin and Artemisinin-Based Combination Therapy Resistance. Available at: http://apps.who.int/iris/bitstream/10665/208820/1/WHO_HTM_GMP_2016.5_eng.pdf/. Accessed June 10, 2016.
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4.
Saunders DL, Vanachayangkul P, Lon C, 2014. Dihydroartemisinin–piperaquine failure in Cambodia. N Engl J Med 371: 484–485.
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5.
Hawkes M, Conroy AL, Opoka RO, Namasopo S, Zhong K, Liles WC, John CC, Kain KC, 2015. Slow clearance of Plasmodium falciparum in severe pediatric malaria, Uganda, 2011–2013. Emerg Infect Dis 21: 1237–1239.
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6.
Trape JF, 2001. The public health impact of chloroquine resistance in Africa. Am J Trop Med Hyg 64: S12–S17.
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7.
Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC, Khim N, Kim S, Duru V, Bouchier C, Ma L, Lim P, Leang R, Duong S, Sreng S, Suon S, Chuor CM, Bout DM, Ménard S, Rogers WO, Genton B, Fandeur T, Miotto O, Ringwald P, Le Bras J, Berry A, Barale JC, Fairhurst RM, Benoit-Vical F, Mercereau-Puijalon O, Ménard D, 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505: 50–55.
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8.
Zhang DD, Lo SC, Cross JV, Templeton DJ, Hannink M, 2004. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol 24: 10941–10953.
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9.
Mbengue A, Bhattacharjee S, Pandharkar T, Liu H, Estiu G, Stahelin RV, Rizk S, Njimoh DL, Ryan Y, Chotivanich K, Nguon C, Ghorbal M, Lopez-Rubio JJ, Pfrender M, Emrich S, Mohandas N, Dondorp AM, Wiest O, Haldar K, 2015. A molecular mechanism of artemisinin resistance in Plasmodium falciparum malaria. Nature 520: 683–687.
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10.
Witkowski B, Amaratunga C, Khim N, Sreng S, Chim P, Kim S, Lim P, Mao S, Sopha C, Sam B, 2013. Novel phenotypic assays for the detection of artemisinin-resistant Plasmodium falciparum malaria in Cambodia: in-vitro and ex-vivo drug-response studies. Lancet Infect Dis 13: 1043–1049.
-
11.
Miotto O, Amato R, Ashley EA, MacInnis B, Almagro-Garcia J, Amaratunga C, Lim P, Mead D, Oyola SO, Dhorda M, Imwong M, Woodrow C, Manske M, Stalker J, Drury E, Campino S, Amenga-Etego L, Thanh TN, Tran HT, Ringwald P, Bethell D, Nosten F, Phyo AP, Pukrittayakamee S, Chotivanich K, Chuor CM, Nguon C, Suon S, Sreng S, Newton PN, Mayxay M, Khanthavong M, Hongvanthong B, Htut Y, Han KT, Kyaw MP, Faiz MA, Fanello CI, Onyamboko M, Mokuolu OA, Jacob CG, Takala-Harrison S, Plowe CV, Day NP, Dondorp AM, Spencer CC, McVean G, Fairhurst RM, White NJ, Kwiatkowski DP, 2015. Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nat Genet 47: 226–234.
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12.
Amato R, Miotto O, Woodrow CJ, Almagro-Garcia J, Sinha I, Campino S, Mead D, Drury E, Kekre M, Sanders M, Amambua-Ngwa A, Amaratunga C, Amenga-Etego L, Andrianaranjaka V, Apinjoh T, Ashley E, Auburn S, Awandare GA, Baraka V, Barry A, Boni MF, Borrmann S, Bousema T, Branch O, Bull PC, Chotivanich K, Conway DJ, Craig A, Day NP, Djimde A, Dondorp AM, Drakeley C, Duffy P, Echeverry DF, Egwang TG, Fairhurst RM, Faiz A, Fanello CI, Hodgson A, Imwong M, Lim P, Lon C, Marfurt J, Marsh K, Mayxay M, Michon P, Mobegi V, Mokuolu OA, Montgomery J, Mueller I, Phone-Kyaw M, Newton PN, Nosten F, Noviyanti R, Nzila A, Ocholla H, Oduro A, Onyamboko M, Ouedraogo JB, Phyo AP, Plowe C, Pukrittayakamee S, Randrianarivelojosia M, Ringwald P, Ruiz L, Saunders D, Shayo A, Siba P, Takala-Harrison S, Thanh TN, Thathy V, Verra F, Wendler J, White NJ, Ye H, Cornelius VJ, Giacomantonio R, Muddyman D, Henrichs C, Malangone C, Jyothi D, Pearson RD, Rayner JC, McVean G, Rockett KA, Miles A, Vauterin P, Jeffery B, Manske M, Stalker J, MacInnis B, Kwiatkowski DP; MalariaGEN Corsortium 2016. Genomic epidemiology of artemisinin resistant malaria. eLife 5: e08714.
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13.
Taylor SM, Parobek CM, DeConti DK, Kayentao K, Coulibaly SO, Greenwood BM, Tagbor H, Williams J, Bojang K, Njie F, Desai M, Kariuki S, Gutman J, Mathanga DP, Mårtensson A, Ngasala B, Conrad MD, Rosenthal PJ, Tshefu AK, Moormann AM, Vulule JM, Doumbo OK, Ter Kuile FO, Meshnick SR, Bailey JA, Juliano JJ, 2015. Absence of putative artemisinin resistance mutations among Plasmodium falciparum in sub-Saharan Africa: a molecular epidemiologic study. J Infect Dis 211: 680–688.
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14.
Kamau E, Campino S, Amenga-Etego L, Drury E, Ishengoma D, Johnson K, Mumba D, Kekre M, Yavo W, Mead D, Bouyou-Akotet M, Apinjoh T, Golassa L, Randrianarivelojosia M, Andagalu B, Maiga-Ascofare O, Amambua-Ngwa A, Tindana P, Ghansah A, MacInnis B, Kwiatkowski D, Djimde AA, 2015. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. J Infect Dis 211: 1352–1355.
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Zeile I, Gahutu JB, Shyirambere C, Steininger C, Musemakweri A, Sebahungu F, Karema C, Harms G, Eggelte TA, Mockenhaupt FP, 2012. Molecular markers of Plasmodium falciparum drug resistance in southern highland Rwanda. Acta Trop 121: 50–54.
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Artemisinin Resistance–Associated K13 Polymorphisms of Plasmodium falciparum in Southern Rwanda, 2010–2015
Costanza Tacoli
Costanza Tacoli
Institute of Tropical Medicine and International Health, Charité–Universitätsmedzin Berlin, Berlin, Germany.
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Prabhanjan P. Gai
Prabhanjan P. Gai
Institute of Tropical Medicine and International Health, Charité–Universitätsmedzin Berlin, Berlin, Germany.
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Claude Bayingana
Claude Bayingana
University Teaching Hospital of Butare, Butare, Rwanda.
School of Medicine and Pharmacy, University of Rwanda, Butare, Rwanda.
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School of Medicine and Pharmacy, University of Rwanda, Butare, Rwanda.
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Kevin Sifft
Kevin Sifft
Institute of Tropical Medicine and International Health, Charité–Universitätsmedzin Berlin, Berlin, Germany.
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Dominik Geus
Dominik Geus
Institute of Tropical Medicine and International Health, Charité–Universitätsmedzin Berlin, Berlin, Germany.
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Jules Ndoli
Jules Ndoli
University Teaching Hospital of Butare, Butare, Rwanda.
School of Medicine and Pharmacy, University of Rwanda, Butare, Rwanda.
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School of Medicine and Pharmacy, University of Rwanda, Butare, Rwanda.
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Augustin Sendegeya
Augustin Sendegeya
University Teaching Hospital of Butare, Butare, Rwanda.
School of Medicine and Pharmacy, University of Rwanda, Butare, Rwanda.
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School of Medicine and Pharmacy, University of Rwanda, Butare, Rwanda.
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Jean Bosco Gahutu
Jean Bosco Gahutu
University Teaching Hospital of Butare, Butare, Rwanda.
School of Medicine and Pharmacy, University of Rwanda, Butare, Rwanda.
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School of Medicine and Pharmacy, University of Rwanda, Butare, Rwanda.
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Frank P. Mockenhaupt
Frank P. Mockenhaupt
Institute of Tropical Medicine and International Health, Charité–Universitätsmedzin Berlin, Berlin, Germany.
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Emerging artemisinin resistance is a threat to global malaria control. Mutations in the Plasmodium falciparum Kelch 13 (K13) propeller domain confer artemisinin resistance and constitute molecular markers for its detection and monitoring. We sequenced 222 P. falciparum isolates obtained from community children in the Huye District of southern Rwanda in 2010, 2014, and 2015 to investigate the presence of K13 polymorphisms. No polymorphisms were observed in 2010 but they were present in 2.5% and 4.5% in 2014 and 2015, respectively. In 2015, two isolates showed candidate K13 resistance mutations (P574L and A675V), which are common in southeast Asia and associated with delayed parasite clearance. K13 polymorphisms in southern Rwanda are infrequent but include variants associated with artemisinin resistance. Establishing correlations with local treatment response and in vitro resistance assays are needed in addition to further monitoring K13 polymorphisms in the study area.
Author Notes
Financial support: This study was supported by the German Federal Ministry of Education and Research (grant 01DG13006A, MOPACUR) and by the German Federal Ministry for Economic Cooperation and Development via the ESTHER program. Costanza Tacoli is financially supported by grant GRK2046 from the German Research Foundation (DFG), and Prabhanjan P. Gai by DFG grant GRK1673 and a stipend of the Sonnenfeld-Foundation, Berlin. The funding bodies had no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.
Authors' addresses: Costanza Tacoli, Prabhanjan P. Gai, Kevin Sifft, Dominik Geus, and Frank P. Mockenhaupt, Institute of Tropical Medicine and International Health, Charité–Universitätsmedizin Berlin, Berlin, Germany, E-mails: costanza.tacoli@charite.de, prabhanjan.gai@charite.de, kevin-christian.sifft@charite.de, dominiktw@hotmail.de, and frank.mockenhaupt@charite.de. Claude Bayingana, Jules Ndoli, Augustin Sendegeya, and Jean Bosco Gahutu, University Teaching Hospital of Butare, Butare, Rwanda, E-mails: cbayrw2000@yahoo.fr, jndoli1971@gmail.com, augdr2002@gmail.com, and j.b.gahutu@ur.ac.rw.
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1.
Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Lwin KM, Ariey F, Hanpithakpong W, Lee SJ, Ringwald P, Kamolrat S, Imwong M, Chotivanich K, Lim P, Herdman T, An SS, Yeung S, Singhasivanon P, Day NPJ, Lindegardh N, Socheat D, White NJ, 2009. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361: 455–467.
-
2.
Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, Sreng S, Anderson JM, Mao S, Sam B, Sopha C, Chuor CM, Nguon C, Sovannaroth S, Pukrittayakamee S, Jittamala P, Chotivanich K, Chutasmit K, Suchatsoonthorn C, Runcharoen R, Hien TT, Thuy-Nhien NT, Thanh NV, Phu NH, Htut Y, Han KT, Aye KH, Mokuolu OA, Olaosebikan RR, Folaranmi OO, Mayxay M, Khantavong M, Hongvanthong B, Newton PN, Onyamboko MA, Fanello CI, Tshefu AK, Mishra N, Valecha N, Phyo AP, Nosten F, Yi P, Tripura R, Borrmann S, Bashraheil M, Peshu J, Faiz MA, Ghose A, Hossain MA, Samad R, Rahman MR, Hasan MM, Islam A, Miotto O, Amato R, Macinnis B, Stalker J, Kwiatkowski DP, Bozdech Z, Jeeyapant A, Cheah PY, Sakulthaew T, Chalk J, Intharabut B, Silamut K, Lee SJ, Vihokhern B, Kunasol C, Imwong M, Tarning J, Taylor WJ, Yeung S, Woodrow CJ, Flegg JA, Das D, Smith J, Venkatesan M, Plowe CV, Stepniewska K, Guerin PJ, Dondrop AM, Day NP, White NJ, 2014. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 371: 411–423.
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3.
World Health Organization, 2016. Artemisinin and Artemisinin-Based Combination Therapy Resistance. Available at: http://apps.who.int/iris/bitstream/10665/208820/1/WHO_HTM_GMP_2016.5_eng.pdf/. Accessed June 10, 2016.
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4.
Saunders DL, Vanachayangkul P, Lon C, 2014. Dihydroartemisinin–piperaquine failure in Cambodia. N Engl J Med 371: 484–485.
-
5.
Hawkes M, Conroy AL, Opoka RO, Namasopo S, Zhong K, Liles WC, John CC, Kain KC, 2015. Slow clearance of Plasmodium falciparum in severe pediatric malaria, Uganda, 2011–2013. Emerg Infect Dis 21: 1237–1239.
-
6.
Trape JF, 2001. The public health impact of chloroquine resistance in Africa. Am J Trop Med Hyg 64: S12–S17.
-
7.
Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC, Khim N, Kim S, Duru V, Bouchier C, Ma L, Lim P, Leang R, Duong S, Sreng S, Suon S, Chuor CM, Bout DM, Ménard S, Rogers WO, Genton B, Fandeur T, Miotto O, Ringwald P, Le Bras J, Berry A, Barale JC, Fairhurst RM, Benoit-Vical F, Mercereau-Puijalon O, Ménard D, 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505: 50–55.
-
8.
Zhang DD, Lo SC, Cross JV, Templeton DJ, Hannink M, 2004. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol 24: 10941–10953.
-
9.
Mbengue A, Bhattacharjee S, Pandharkar T, Liu H, Estiu G, Stahelin RV, Rizk S, Njimoh DL, Ryan Y, Chotivanich K, Nguon C, Ghorbal M, Lopez-Rubio JJ, Pfrender M, Emrich S, Mohandas N, Dondorp AM, Wiest O, Haldar K, 2015. A molecular mechanism of artemisinin resistance in Plasmodium falciparum malaria. Nature 520: 683–687.
-
10.
Witkowski B, Amaratunga C, Khim N, Sreng S, Chim P, Kim S, Lim P, Mao S, Sopha C, Sam B, 2013. Novel phenotypic assays for the detection of artemisinin-resistant Plasmodium falciparum malaria in Cambodia: in-vitro and ex-vivo drug-response studies. Lancet Infect Dis 13: 1043–1049.
-
11.
Miotto O, Amato R, Ashley EA, MacInnis B, Almagro-Garcia J, Amaratunga C, Lim P, Mead D, Oyola SO, Dhorda M, Imwong M, Woodrow C, Manske M, Stalker J, Drury E, Campino S, Amenga-Etego L, Thanh TN, Tran HT, Ringwald P, Bethell D, Nosten F, Phyo AP, Pukrittayakamee S, Chotivanich K, Chuor CM, Nguon C, Suon S, Sreng S, Newton PN, Mayxay M, Khanthavong M, Hongvanthong B, Htut Y, Han KT, Kyaw MP, Faiz MA, Fanello CI, Onyamboko M, Mokuolu OA, Jacob CG, Takala-Harrison S, Plowe CV, Day NP, Dondorp AM, Spencer CC, McVean G, Fairhurst RM, White NJ, Kwiatkowski DP, 2015. Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nat Genet 47: 226–234.
-
12.
Amato R, Miotto O, Woodrow CJ, Almagro-Garcia J, Sinha I, Campino S, Mead D, Drury E, Kekre M, Sanders M, Amambua-Ngwa A, Amaratunga C, Amenga-Etego L, Andrianaranjaka V, Apinjoh T, Ashley E, Auburn S, Awandare GA, Baraka V, Barry A, Boni MF, Borrmann S, Bousema T, Branch O, Bull PC, Chotivanich K, Conway DJ, Craig A, Day NP, Djimde A, Dondorp AM, Drakeley C, Duffy P, Echeverry DF, Egwang TG, Fairhurst RM, Faiz A, Fanello CI, Hodgson A, Imwong M, Lim P, Lon C, Marfurt J, Marsh K, Mayxay M, Michon P, Mobegi V, Mokuolu OA, Montgomery J, Mueller I, Phone-Kyaw M, Newton PN, Nosten F, Noviyanti R, Nzila A, Ocholla H, Oduro A, Onyamboko M, Ouedraogo JB, Phyo AP, Plowe C, Pukrittayakamee S, Randrianarivelojosia M, Ringwald P, Ruiz L, Saunders D, Shayo A, Siba P, Takala-Harrison S, Thanh TN, Thathy V, Verra F, Wendler J, White NJ, Ye H, Cornelius VJ, Giacomantonio R, Muddyman D, Henrichs C, Malangone C, Jyothi D, Pearson RD, Rayner JC, McVean G, Rockett KA, Miles A, Vauterin P, Jeffery B, Manske M, Stalker J, MacInnis B, Kwiatkowski DP; MalariaGEN Corsortium 2016. Genomic epidemiology of artemisinin resistant malaria. eLife 5: e08714.
-
13.
Taylor SM, Parobek CM, DeConti DK, Kayentao K, Coulibaly SO, Greenwood BM, Tagbor H, Williams J, Bojang K, Njie F, Desai M, Kariuki S, Gutman J, Mathanga DP, Mårtensson A, Ngasala B, Conrad MD, Rosenthal PJ, Tshefu AK, Moormann AM, Vulule JM, Doumbo OK, Ter Kuile FO, Meshnick SR, Bailey JA, Juliano JJ, 2015. Absence of putative artemisinin resistance mutations among Plasmodium falciparum in sub-Saharan Africa: a molecular epidemiologic study. J Infect Dis 211: 680–688.
-
14.
Kamau E, Campino S, Amenga-Etego L, Drury E, Ishengoma D, Johnson K, Mumba D, Kekre M, Yavo W, Mead D, Bouyou-Akotet M, Apinjoh T, Golassa L, Randrianarivelojosia M, Andagalu B, Maiga-Ascofare O, Amambua-Ngwa A, Tindana P, Ghansah A, MacInnis B, Kwiatkowski D, Djimde AA, 2015. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. J Infect Dis 211: 1352–1355.
-
15.
United States Agency of International Development, 2016. President's Malaria Initiative Series: FY 2016 Rwanda Malaria Operational Plan. Available at: https://www.pmi.gov/where-we-work/rwanda. Accessed June 10, 2016.
-
16.
Zeile I, Gahutu JB, Shyirambere C, Steininger C, Musemakweri A, Sebahungu F, Karema C, Harms G, Eggelte TA, Mockenhaupt FP, 2012. Molecular markers of Plasmodium falciparum drug resistance in southern highland Rwanda. Acta Trop 121: 50–54.
-
17.
Gahutu J-B, Steininger C, Shyirambere C, Zeile I, Cwinya-Ay N, Danquah I, Larsen CH, Eggelte TA, Uwimana A, Karema C, Musemakweri A, Harms G, Mockenhaupt FP, 2011. Prevalence and risk factors of malaria among children in southern highland Rwanda. Malar J 10: 134.
-
18.
Rubio JM, Post RJ, van Leeuwen WM, Henry MC, Lindergard G, Hommel M, 2002. Alternative polymerase chain reaction method to identify Plasmodium species in human blood samples: the semi-nested multiplex malaria PCR (SnM-PCR). Trans R Soc Trop Med Hyg 96: S199–S204.
-
19.
Takala-Harrison S, Jacob CG, Arze C, Cummings MP, Silva JC, Dondorp AM, Fukuda MM, Hien TT, Mayxay M, Noedl H, Nosten F, Kyaw MP, Nhien NT, Imwong M, Bethell D, Se Y, Lon C, Tyner SD, Saunders DL, Ariey F, Mercereau-Puijalon O, Menard D, Newton PN, Khanthavong M, Hongvanthong B, Starzengruber P, Fuehrer HP, Swoboda P, Khan WA, Phyo AP, Nyunt MM, Nyunt MH, Brown TS, Adams M, Pepin CS, Bailey J, Tan JC, Ferdig MT, Clark TG, Miotto O, MacInnis B, Kwiatkowski DP, White NJ, Ringwald P, Plowe CV, 2015. Independent emergence of artemisinin resistance mutations among Plasmodium falciparum in southeast Asia. J Infect Dis 211: 670–679.
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