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Surveillance of Molecular Markers of Plasmodium falciparum Resistance to Sulphadoxine-Pyrimethamine 5 Years after the Change of Malaria Treatment Policy in Ghana
Nancy O. Duah
Nancy O. Duah
Noguchi Memorial Institute for Medical Research, Legon, Accra, Ghana; Centre for Tropical Clinical Pharmacology and Therapeutics, University of Ghana Medical School, Korle-Bu, Accra, Ghana; United States Naval Medical Research Unit No. 3, Cairo, Egypt
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Neils B. Quashie
Neils B. Quashie
Noguchi Memorial Institute for Medical Research, Legon, Accra, Ghana; Centre for Tropical Clinical Pharmacology and Therapeutics, University of Ghana Medical School, Korle-Bu, Accra, Ghana; United States Naval Medical Research Unit No. 3, Cairo, Egypt
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Benjamin K. Abuaku
Benjamin K. Abuaku
Noguchi Memorial Institute for Medical Research, Legon, Accra, Ghana; Centre for Tropical Clinical Pharmacology and Therapeutics, University of Ghana Medical School, Korle-Bu, Accra, Ghana; United States Naval Medical Research Unit No. 3, Cairo, Egypt
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Peter J. Sebeny
Peter J. Sebeny
Noguchi Memorial Institute for Medical Research, Legon, Accra, Ghana; Centre for Tropical Clinical Pharmacology and Therapeutics, University of Ghana Medical School, Korle-Bu, Accra, Ghana; United States Naval Medical Research Unit No. 3, Cairo, Egypt
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Karl C. Kronmann
Karl C. Kronmann
Noguchi Memorial Institute for Medical Research, Legon, Accra, Ghana; Centre for Tropical Clinical Pharmacology and Therapeutics, University of Ghana Medical School, Korle-Bu, Accra, Ghana; United States Naval Medical Research Unit No. 3, Cairo, Egypt
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Kwadwo A. Koram
Kwadwo A. Koram
Noguchi Memorial Institute for Medical Research, Legon, Accra, Ghana; Centre for Tropical Clinical Pharmacology and Therapeutics, University of Ghana Medical School, Korle-Bu, Accra, Ghana; United States Naval Medical Research Unit No. 3, Cairo, Egypt
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In 2005, sulphadoxine-pyrimethamine (SP) became the drug of choice for intermittent preventive treatment of Plasmodium falciparum malaria in pregnancy (IPTp) in Ghana. Reports suggest the use of SP by others to treat uncomplicated malaria. Because of the increased use of SP, the prevalence of mutations in the genes, dihydrofolate reductase (dhfr), and dihydropteroate synthetase (dhps), linked to SP resistance in P. falciparum were determined. Blood samples from 945 children with uncomplicated malaria collected at nine sites from 2003 to 2010 were analyzed using polymerase chain reaction and restriction fragment length polymorphism. Prevalence of the dhfr triple and dhfr plus dhps quadruple mutations showed significant increase in trend from 2003 to 2010 (χ2 = 18.78, P < 0.001, χ2 = 15.11, P < 0.001, respectively). For dhps double mutant G437 + E540 the prevalence was low (1.12%) caused by the very low prevalence of E540. Our findings show the wide use of SP in Ghana and therefore its use for IPTp needs to be closely monitored.
Author Notes
Financial support: The molecular aspect of this work was funded by the Global Emerging Infections Surveillance and Response System (GEIS), a Division of the Armed Forces Health Surveillance Center (AFHSC) [Project no. C0437_10_N3]. The field work aspect was funded by the Global Fund for TB, Aids, and Malaria/National Malaria Control Program and the WHO/Multilateral Initiative in Malaria (MIM) [Project no. 980034].
Disclosure: Karl C. Kronmann and Peter Sebeny are military service members. This work was prepared as part of their official duties. Title 17 U.S.C. §105 provides that ‘Copyright protection under this title is not available for any work of the United States Government.’ Title 17 U.S.C. §101 defines a U.S. Government work as a work prepared by a military service member or employee of the U.S. Government as part of that person's official duties.
Authors' addresses: Nancy O. Duah, Benjamin K. Abuaku, and Kwadwo A. Koram, Noguchi Memorial Institute for Medical Research, Legon, Accra, Ghana, E-mails: nduah@noguchi.mimcom.org, babuaku@noguchi.mimcom.org, and kkoram@noguchi.mimcom.org. Neils B. Quashie, Noguchi Memorial Institute for Medical Research, Legon, Accra, Ghana, E-mail: nquashie@noguchi.mimcom.org. Peter J. Sebeny, Infectious Diseases Directorate, Naval Medical Research Center, Silver Spring, MD, E-mail: Peter.Sebeny@med.navy.mil. Karl C. Kronmann, U.S. Naval Medical Research Unit No. 3, Cairo, Egypt, E-mail: karl.kronmann@med.navy.mil.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
WHO, 2010. WHO calls on malaria-endemic countries to strengthen monitoring of drug efficacy. Available at: http://www.wpro.who.int/mediacentre/releases/2010/20101118/en/index.html. Accessed June 3, 2012.
-
2.
WHO, 2003. Lives at risk: malaria in pregnancy. Available at: http://www.who.int/features/2003/04b/en/. Accessed November 20, 2011.
-
3.
WHO, 2010. Malaria Fact Sheet No. 94. Available at: http://www.who.int/mediacentre/factsheets/fs094/en/index.html. Accessed November 20, 2011.
-
4.
MOH, 2009. Anti-Malaria Drug Policy for Ghana. Ghana: Ministry of Health.
-
5.
Koram KA, Abuaku B, Duah N, Quashie N, 2005. Comparative efficacy of antimalarial drugs including ACTs in the treatment of uncomplicated malaria among children under 5 years in Ghana. Acta Trop 95: 194–203.
-
6.
Ghana Statistical Service (GSS), Ghana Health Service (GHS) and ICF Macro, 2009. Ghana Demographic and Health Survey 2008. Accra, Ghana: GSS, GHS, and ICF Macro. Available at: http://pdf.usaid.gov/pdf_docs/PNADQ630.pdf.
-
7.
Faye B, Ndiaye M, Ndiaye JL, Annie A, Tine RC, Lo AC, Sow D, De Sousa A, Gaye O, 2011. Prevalence of molecular markers of Plasmodium falciparum resistance to sulfadoxine-pyrimethamine during the intermittent preventive treatment in infants coupled with the expanded program immunization in Senegal. Parasitol Res 109: 133–138.
-
8.
Raman J, Little F, Roper C, Kleinschmidt I, Cassam Y, Maharaj R, Barnes KI, 2010. Five years of large-scale dhfr and dhps mutation surveillance following the phased implementation of artesunate plus sulfadoxine-pyrimethamine in Maputo Province, Southern Mozambique. Am J Trop Med Hyg 82: 788–794.
-
9.
Peterson DS, Milhous WK, Wellems TE, 1990. Molecular basis of differential resistance to cycloguanil and pyrimethamine in Plasmodium falciparum malaria. Proc Natl Acad Sci USA 87: 3018–3022.
-
10.
Peterson DS, Walliker D, Wellems TE, 1988. Evidence that a point mutation in dihydrofolate reductase-thymidylate synthase confers resistance to pyrimethamine in falciparum malaria. Proc Natl Acad Sci USA 85: 9114–9118.
-
11.
Wang P, Read M, Sims PF, Hyde JE, 1997. Sulfadoxine resistance in the human malaria parasite Plasmodium falciparum is determined by mutations in dihydropteroate synthetase and an additional factor associated with folate utilization. Mol Microbiol 23: 979–986.
-
12.
Figueiredo P, Benchimol C, Lopes D, Bernardino L, Rosario VE, Varandas L, Nogueira F, 2008. Prevalence of pfmdr1, pfcrt, pfdhfr and pfdhps mutations associated with drug resistance, in Luanda, Angola. Malar J 7: 236.
-
13.
Mens PF, van Overmeir C, Bonnet M, Dujardin JC, d'Alessandro U, 2008. Real-time PCR/MCA assay using fluorescence resonance energy transfer for the genotyping of resistance related DHPS-540 mutations in Plasmodium falciparum. Malar J 7: 48.
-
14.
Mockenhaupt FP, Bousema JT, Eggelte TA, Schreiber J, Ehrhardt S, Wassilew N, Otchwemah RN, Sauerwein RW, Bienzle U, 2005. Plasmodium falciparum dhfr but not dhps mutations associated with sulphadoxine-pyrimethamine treatment failure and gametocyte carriage in northern Ghana. Trop Med Int Health 10: 901–908.
-
15.
Kublin JG, Dzinjalamala FK, Kamwendo DD, Malkin EM, Cortese JF, Martino LM, Mukadam RA, Rogerson SJ, Lescano AG, Molyneux ME, Winstanley PA, Chimpeni P, Taylor TE, Plowe CV, 2002. Molecular markers for failure of sulfadoxine-pyrimethamine and chlorproguanil-dapsone treatment of Plasmodium falciparum malaria. J Infect Dis 185: 380–388.
-
16.
Plowe CV, Cortese JF, Djimde A, Wellems TE, 1997. Mutations in Plasmodium falciparum dihydrofolate reductase and dihydropteroate synthase and epidemiologic patterns of pyrimethamine-sulfadoxine use and resistance. J Infect Dis 176: 1590–1596.
-
17.
Wang P, Lee CS, Bayoumi R, Djimde A, Doumbo O, Swedberg G, Dao LD, Mshinda H, Tanner M, Watkins WM, Sims PF, Hyde JE, 1997. Resistance to antifolates in Plasmodium falciparum monitored by sequence analysis of dihydropteroate synthetase and dihydrofolate reductase alleles in a large number of field samples of diverse origins. Mol Biochem Parasitol 89: 161–177.
-
18.
Sirawaraporn W, Sathitkul T, Sirawaraporn R, Yuthavong Y, Santi DV, 1997. Antifolate-resistant mutants of Plasmodium falciparum dihydrofolate reductase. Proc Natl Acad Sci USA 94: 1124–1129.
-
19.
Pearce RJ, Pota H, Evehe MS, Ba el-H, Mombo-Ngoma G, Malisa AL, Ord R, Inojosa W, Matondo A, Diallo DA, Mbacham W, van den Broek IV, Swarthout TD, Getachew A, Dejene S, Grobusch MP, Njie F, Dunyo S, Kweku M, Owusu-Agyei S, Chandramohan D, Bonnet M, Guthmann JP, Clarke S, Barnes KI, Streat E, Katokele ST, Uusiku P, Agboghoroma CO, Elegba OY, Cisse B, A-Elbasit IE, Giha HA, Kachur SP, Lynch C, Rwakimari JB, Chanda P, Hawela M, Sharp B, Naidoo I, Roper C, 2009. Multiple origins and regional dispersal of resistant dhps in African Plasmodium falciparum malaria. PLoS Med 6: e1000055.
-
20.
Alam MT, de Souza DK, Vinayak S, Griffing SM, Poe AC, Duah NO, Ghansah A, Asamoa K, Slutsker L, Wilson MD, Barnwell JW, Udhayakumar V, Koram KA, 2011. Selective sweeps and genetic lineages of Plasmodium falciparum drug-resistant alleles in Ghana. J Infect Dis 203: 220–227.
-
21.
Quashie NB, Duah NO, Abuaku B, Koram KA, 2007. The in-vitro susceptibilities of Ghanaian Plasmodium falciparum to antimalarial drugs. Ann Trop Med Parasitol 101: 391–398.
-
22.
Duah NO, Wilson MD, Ghansah A, Abuaku B, Edoh D, Quashie NB, Koram KA, 2007. Mutations in Plasmodium falciparum chloroquine resistance transporter and multidrug resistance genes, and treatment outcomes in Ghanaian children with uncomplicated malaria. J Trop Pediatr 53: 27–31.
-
23.
GHS, 2004. Final Draft: Antimalaria Drug Policy for Ghana. Ghana: Ghana Health Service.
-
24.
Dicko A, Sagara I, Djimde AA, Toure SO, Traore M, Dama S, Diallo AI, Barry A, Dicko M, Coulibaly OM, Rogier C, de Sousa A, Doumbo OK, 2010. Molecular markers of resistance to sulphadoxine-pyrimethamine one year after implementation of intermittent preventive treatment of malaria in infants in Mali. Malar J 9: 9.
-
25.
WHO, 2010. Policy recommendation on Intermittent Preventive Treatment during infancy with sulphadoxine-pyrimethamine (SP-IPTi) for Plasmodium falciparum malaria control in Africa. Available at: http://www.who.int/malaria/news/WHO_policy_recommendation_IPTi_032010.pdf. Accessed June 3, 2012.
-
26.
Naidoo I, Roper C, 2011. Drug resistance maps to guide intermittent preventive treatment of malaria in African infants. Parasitol 138: 1469–1479.
-
27.
Bereczky S, Martensson A, Gil JP, Farnert A, 2005. Short report: rapid DNA extraction from archive blood spots on filter paper for genotyping of Plasmodium falciparum. Am J Trop Med Hyg 72: 249–251.
-
28.
Duraisingh MT, Curtis J, Warhurst DC, 1998. Plasmodium falciparum: detection of polymorphisms in the dihydrofolate reductase and dihydropteroate synthetase genes by PCR and restriction digestion. Exp Parasitol 89: 1–8.
-
29.
Omar SA, Adagu IS, Warhurst DC, 2001. Can pretreatment screening for dhps and dhfr point mutations in Plasmodium falciparum infections be used to predict sulfadoxine-pyrimethamine treatment failure? Trans R Soc Trop Med Hyg 95: 315–319.
-
30.
Alifrangis M, Enosse S, Khalil IF, Tarimo DS, Lemnge MM, Thompson R, Bygbjerg IC, Ronn AM, 2003. Prediction of Plasmodium falciparum resistance to sulfadoxine/pyrimethamine in vivo by mutations in the dihydrofolate reductase and dihydropteroate synthetase genes: a comparative study between sites of differing endemicity. Am J Trop Med Hyg 69: 601–606.
-
31.
Staedke SG, Sendagire H, Lamola S, Kamya MR, Dorsey G, Rosenthal PJ, 2004. Relationship between age, molecular markers, and response to sulphadoxine-pyrimethamine treatment in Kampala, Uganda. Trop Med Int Health 9: 624–629.
-
32.
Tahar R, Basco L, 2006. Molecular epidemiology of malaria in Cameroon. XXII. Geographic mapping and distribution of Plasmodium falciparum dihydrofolate reductase (dhfr) mutant alleles. Am J Trop Med Hyg 75: 396–401.
-
33.
Gama BE, Pereira-Carvalho G, Kosi F, Oliverira A, Fortes F, Rosenthal PJ, Rosario V, Daniel-Ribeiro C, Ferreira-da-Cruz M, 2011. Molecular markers of antifolate resistance in Plasmodium falciparum isolates from Luanda, Angola. Malar J 10: 248.
-
34.
Alifrangis M, Lusingu JP, Mmbando B, Dalgaard MB, Vestergaard LS, Ishengoma D, Khalil IF, Theander TG, Lemnge MM, Bygbjerg IC, 2009. Five-year surveillance of molecular markers of Plasmodium falciparum antimalarial drug resistance in Korogwe District, Tanzania: accumulation of the 581G mutation in the P. falciparum dihydropteroate synthase gene. Am J Trop Med Hyg 80: 523–527.
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