Polymorphisms in pfcrt and pfmdr1: parasite risk factors that affect treatment outcomes for falciparum malaria after artemether-lumefantrine and artesunate-amodiaquine-Corrected version

Meera Venkatesan, Nahla B. Gadalla, Kasia Stepniewska, Prabin Dahal, Christian Nsanzabana, Clarissa Moriera, Ric N. Price , Andreas Mårtensson, Philip Rosenthal, Grant Dorsey, Colin J. Sutherland, Philippe Guérin, Timothy M. E. Davis, Didier Ménard, Ishag Adam, George Ademowo, Cesar Arze, Frederick N. Baliraine, Nicole Berens-Riha, Anders Björkman, Steffen Borrmann, Francesco Checchi, Meghna Desai, Mehul Dhorda , Abdoulaye A. Djimdé, Badria B. El-Sayed, Teferi Eshetu, Frederick Eyase, Catherine Falade, Jean-François Faucher, Gabrielle Fröberg, Anastasia Grivoyannis, SallyHamour, Sandrine Houzé, Jacob Johnson, Erasmus Kamugisha, Simon Kariuki, Jean-René Kiechel, Fred Kironde, Poul-Erik Kofoed, Jacques LeBras Maja Malmberg, Leah Mwai, Billy Ngasala, Francois Nosten Samuel L. Nsobya, Alexis Nzila Mary Oguike, Sabina Dahlström Otienoburu, Bernhards Ogutu, Jean-Bosco Ouédraogo, Patrice Piola, Lars Rombo, Birgit Schramm, A.Fabrice Somé, Julie Thwing, Johan Ursing, Rina P. M. Wong, Ahmed Zeynudin, Issaka Zongo , Carol Hopkins Sibley Christopher V. Plowe

[1]  B. Genton,et al.  A molecular marker of artemisinin-resistant Plasmodium falciparum malaria , 2013, Nature.

[2]  Charles Akugbey Narh,et al.  Increased pfmdr1 gene copy number and the decline in pfcrt and pfmdr1 resistance alleles in Ghanaian Plasmodium falciparum isolates after the change of anti-malarial drug treatment policy , 2013, Malaria Journal.

[3]  R. Price,et al.  Nonlinear Mixed-Effects Modelling of In Vitro Drug Susceptibility and Molecular Correlates of Multidrug Resistant Plasmodium falciparum , 2013, PloS one.

[4]  E. Ashley,et al.  Efficacy of artesunate-amodiaquine and artemether-lumefantrine fixed-dose combinations for the treatment of uncomplicated Plasmodium falciparum malaria among children aged six to 59 months in Nimba County, Liberia: an open-label randomized non-inferiority trial , 2013, Malaria Journal.

[5]  Andreas Mårtensson,et al.  Plasmodium falciparum Drug Resistance Phenotype as Assessed by Patient Antimalarial Drug Levels and Its Association With pfmdr1 Polymorphisms , 2012, The Journal of infectious diseases.

[6]  L. Quaye,et al.  Therapeutic efficacy of artemether-lumefantrine combination in the treatment of uncomplicated malaria among children under five years of age in three ecological zones in Ghana , 2012, Malaria Journal.

[7]  A. Wieser,et al.  Open-label trial with artemether-lumefantrine against uncomplicated Plasmodium falciparum malaria three years after its broad introduction in Jimma Zone, Ethiopia , 2012, Malaria Journal.

[8]  Kayla R. Stover,et al.  Artemether-Lumefantrine: An Option for Malaria , 2012, The Annals of pharmacotherapy.

[9]  F. Kironde,et al.  Efficacy of artemether-lumefantrine in treatment of malaria among under-fives and prevalence of drug resistance markers in Igombe-Mwanza, north-western Tanzania , 2012, Malaria Journal.

[10]  C. Happi,et al.  In vitro amodiaquine resistance and its association with mutations in pfcrt and pfmdr1 genes of Plasmodium falciparum isolates from Nigeria. , 2011, Acta tropica.

[11]  A. Nzila,et al.  Declining Responsiveness of Plasmodium falciparum Infections to Artemisinin-Based Combination Treatments on the Kenyan Coast , 2011, PloS one.

[12]  P. Rosenthal,et al.  Prolonged selection of pfmdr1 polymorphisms after treatment of falciparum malaria with artemether-lumefantrine in Uganda. , 2011, The Journal of infectious diseases.

[13]  Badria B. El-Sayed,et al.  Increased pfmdr1 Copy Number and Sequence Polymorphisms in Plasmodium falciparum Isolates from Sudanese Malaria Patients Treated with Artemether-Lumefantrine , 2011, Antimicrobial Agents and Chemotherapy.

[14]  F. Ou,et al.  Randomized trials of artemisinin-piperaquine, dihydroartemisinin-piperaquine phosphate and artemether-lumefantrine for the treatment of multi-drug resistant falciparum malaria in Cambodia-Thailand border area , 2011, Malaria Journal.

[15]  L. Ranford-Cartwright,et al.  Rational deployment of antimalarial drugs in Africa: should first-line combination drugs be reserved for paediatric malaria cases? , 2011, Parasitology.

[16]  M. Petzold,et al.  Efficacy and effectiveness of artemether-lumefantrine after initial and repeated treatment in children <5 years of age with acute uncomplicated Plasmodium falciparum malaria in rural Tanzania: a randomized trial. , 2011, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[17]  Z. Premji,et al.  Effectiveness of artemether-lumefantrine provided by community health workers in under-five children with uncomplicated malaria in rural Tanzania: an open label prospective study , 2011, Malaria Journal.

[18]  S. Ward,et al.  Association between the pfmdr1 gene and in vitro artemether and lumefantrine sensitivity in Thai isolates of Plasmodium falciparum. , 2010, The American journal of tropical medicine and hygiene.

[19]  R. Durand,et al.  Chloroquine Clinical Failures in P. falciparum Malaria Are Associated with Mutant Pfmdr-1, Not Pfcrt in Madagascar , 2010, PloS one.

[20]  Teferi Eshetu,et al.  Different mutation patterns of Plasmodium falciparum among patients in Jimma University Hospital, Ethiopia , 2010, Malaria Journal.

[21]  P. Rosenthal,et al.  Selection of Known Plasmodium falciparum Resistance-Mediating Polymorphisms by Artemether-Lumefantrine and Amodiaquine- Sulfadoxine-Pyrimethamine but Not Dihydroartemisinin- Piperaquine in Burkina Faso , 2010, Antimicrobial Agents and Chemotherapy.

[22]  O. Müller,et al.  Selection of pfmdr1 and pfcrt alleles in amodiaquine treatment failure in north-western Burkina Faso. , 2010, Acta tropica.

[23]  S. Krudsood,et al.  The clinical efficacy of artemether/lumefantrine (Coartem®) , 2009, Malaria Journal.

[24]  Paul Garner,et al.  Artemisinin-based combination therapy for treating uncomplicated malaria. , 2009, The Cochrane database of systematic reviews.

[25]  J. Vulule,et al.  In‐vivo efficacy of amodiaquine‐artesunate in children with uncomplicated Plasmodium falciparum malaria in western Kenya , 2009, Tropical medicine & international health : TM & IH.

[26]  Z. Premji,et al.  In vivo selection of Plasmodium falciparum parasites carrying the chloroquine-susceptible pfcrt K76 allele after treatment with artemether-lumefantrine in Africa. , 2009, The Journal of infectious diseases.

[27]  S. Meshnick,et al.  Pfmdr1 copy number and arteminisin derivatives combination therapy failure in falciparum malaria in Cambodia , 2009, Malaria Journal.

[28]  D. Wirth,et al.  Selection of Plasmodium falciparum Multidrug Resistance Gene 1 Alleles in Asexual Stages and Gametocytes by Artemether-Lumefantrine in Nigerian Children with Uncomplicated Falciparum Malaria , 2008, Antimicrobial Agents and Chemotherapy.

[29]  David L. Smith,et al.  Benefits of using multiple first-line therapies against malaria , 2008, Proceedings of the National Academy of Sciences.

[30]  O. Ademowo,et al.  High efficacy of two artemisinin‐based combinations (artemether–lumefantrine and artesunate plus amodiaquine) for acute uncomplicated malaria in Ibadan, Nigeria , 2008, Tropical medicine & international health : TM & IH.

[31]  A. Dicko,et al.  Efficacy, safety, and selection of molecular markers of drug resistance by two ACTs in Mali. , 2008, The American journal of tropical medicine and hygiene.

[32]  H. Tinto,et al.  Chloroquine‐resistance molecular markers (Pfcrt T76 and Pfmdr‐1 Y86) and amodiaquine resistance in Burkina Faso , 2008, Tropical medicine & international health : TM & IH.

[33]  P. Rosenthal,et al.  Randomized comparison of amodiaquine plus sulfadoxine-pyrimethamine, artemether-lumefantrine, and dihydroartemisinin-piperaquine for the treatment of uncomplicated Plasmodium falciparum malaria in Burkina Faso. , 2007, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[34]  Diego F. Echeverry,et al.  Short report: polymorphisms in the pfcrt and pfmdr1 genes of Plasmodium falciparum and in vitro susceptibility to amodiaquine and desethylamodiaquine. , 2007, The American journal of tropical medicine and hygiene.

[35]  A. Mårtensson,et al.  Selection of pfmdr1 mutations after amodiaquine monotherapy and amodiaquine plus artemisinin combination therapy in East Africa. , 2007, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[36]  S. Krishna,et al.  The role of pfmdr1 in Plasmodium falciparum tolerance to artemether‐lumefantrine in Africa , 2007, Tropical medicine & international health : TM & IH.

[37]  Georgina S. Humphreys,et al.  Amodiaquine and Artemether-Lumefantrine Select Distinct Alleles of the Plasmodium falciparum mdr1 Gene in Tanzanian Children Treated for Uncomplicated Malaria , 2006, Antimicrobial Agents and Chemotherapy.

[38]  C. Roper,et al.  Artesunate + amodiaquine and artesunate + sulphadoxine–pyrimethamine for treatment of uncomplicated malaria in Democratic Republic of Congo: a clinical trial with determination of sulphadoxine and pyrimethamine‐resistant haplotypes , 2006, Tropical medicine & international health : TM & IH.

[39]  D. Fidock,et al.  Decreasing pfmdr1 copy number in plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin. , 2006, The Journal of infectious diseases.

[40]  D. Wirth,et al.  Association between mutations in Plasmodium falciparum chloroquine resistance transporter and P. falciparum multidrug resistance 1 genes and in vivo amodiaquine resistance in P. falciparum malaria-infected children in Nigeria. , 2006, The American journal of tropical medicine and hygiene.

[41]  C. Obonyo,et al.  Amodiaquine resistant Plasmodium falciparum malaria in vivo is associated with selection of pfcrt 76T and pfmdr1 86Y. , 2006, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[42]  R. Price,et al.  Molecular and pharmacological determinants of the therapeutic response to artemether-lumefantrine in multidrug-resistant Plasmodium falciparum malaria. , 2006, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[43]  P. Rosenthal,et al.  Selection of Plasmodium falciparum pfmdr1 Alleles following Therapy with Artemether-Lumefantrine in an Area of Uganda where Malaria Is Highly Endemic , 2006, Antimicrobial Agents and Chemotherapy.

[44]  Abdullah S. Ali,et al.  Efficacy of artesunate plus amodiaquine versus that of artemether-lumefantrine for the treatment of uncomplicated childhood Plasmodium falciparum malaria in Zanzibar, Tanzania. , 2005, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[45]  N. Ford,et al.  Malaria in the Nuba Mountains of Sudan: baseline genotypic resistance and efficacy of the artesunate plus sulfadoxine-pyrimethamine and artesunate plus amodiaquine combinations. , 2005, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[46]  R. Hallett,et al.  Amodiaquine alone, amodiaquine+sulfadoxine-pyrimethamine, amodiaquine+artesunate, and artemether-lumefantrine for outpatient treatment of malaria in Tanzanian children: a four-arm randomised effectiveness trial , 2005, The Lancet.

[47]  C. Karema,et al.  Is amodiaquine failing in Rwanda? Efficacy of amodiaquine alone and combined with artesunate in children with uncomplicated malaria , 2004, Tropical medicine & international health : TM & IH.

[48]  François Nosten,et al.  Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number , 2004, The Lancet.

[49]  A. Nzila,et al.  Short report: association between chloroquine and amodiaquine resistance and allelic variation in the Plasmodium falciparum multiple drug resistance 1 gene and the chloroquine resistance transporter gene in isolates from the upper Nile in southern Sudan. , 2003, The American journal of tropical medicine and hygiene.

[50]  S. Meshnick,et al.  Resistance to Antimalarials in Southeast Asia and Genetic Polymorphisms in pfmdr1 , 2003, Antimicrobial Agents and Chemotherapy.

[51]  Jahar B Choudhury,et al.  Non‐parametric confidence interval estimation for competing risks analysis: application to contraceptive data , 2002, Statistics in medicine.

[52]  D. Warhurst A molecular marker for chloroquine-resistant falciparum malaria. , 2001, The New England journal of medicine.

[53]  M. Duraisingh,et al.  The tyrosine-86 allele of the pfmdr1 gene of Plasmodium falciparum is associated with increased sensitivity to the anti-malarials mefloquine and artemisinin. , 2000, Molecular and biochemical parasitology.

[54]  N. White,et al.  Pharmacokinetics and Pharmacodynamics of Lumefantrine (Benflumetol) in Acute Falciparum Malaria , 2000, Antimicrobial Agents and Chemotherapy.

[55]  K. Kirk,et al.  Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum , 2000, Nature.

[56]  C. Drakeley,et al.  Evidence for selection for the tyrosine-86 allele of the pfmdr 1 gene of Plasmodium falciparum by chloroquine and amodiaquine , 1997, Parasitology.

[57]  C G Thomas,et al.  Pharmacokinetics of artemether after oral administration to healthy Thai males and patients with acute, uncomplicated falciparum malaria. , 1994, British journal of clinical pharmacology.

[58]  David A. Schoenfeld,et al.  Partial residuals for the proportional hazards regression model , 1982 .

[59]  P. Kofoed,et al.  Similar efficacy and tolerability of double-dose chloroquine and artemether-lumefantrine for treatment of Plasmodium falciparum infection in Guinea-Bissau: a randomized trial. , 2011, The Journal of infectious diseases.

[60]  Organización Mundial de la Salud Methods and techniques for clinical trials on antimalarial drug efficacy: genotyping to identify parasite populations , 2008 .

[61]  R. Price,et al.  Intrahost selection of Plasmodium falciparum pfmdr1 alleles after antimalarial treatment on the northwestern border of Thailand. , 2007, The Journal of infectious diseases.