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Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

High efficacy of artemether-lumefantrine and declining efficacy of artesunate + sulfadoxine-pyrimethamine against Plasmodium falciparum in Sudan (2010–2015): evidence from in vivo and molecular marker studies

Authors: Ahmed A. Adeel, Fahad Awad Ali Elnour, Khalid Abdalmutalab Elmardi, Mona B. Abd-Elmajid, Mai Mahmoud Elhelo, Mousab S. Ali, Mariam A. Adam, Hoda Atta, Ghasem Zamani, Marian Warsame, Amy Barrette, Hanan El Mohammady, Rania A. Nada

Published in: Malaria Journal | Issue 1/2016

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Abstract

Background

The present paper reports on studies that evaluated artesunate + sulfadoxine-pyrimethamine (AS + SP) which is the first-line drug and artemether-lumefantrine (AL) which is a second-line drug against uncomplicated falciparum malaria in Sudan. This evaluation was performed in twenty studies covering six sentinel sites during five successive annual malaria transmission seasons from 2010 to 2015.

Methods

The standard World Health Organization protocol was used for a follow-up period of 28 days. The frequency distribution of molecular markers for antifolate resistance in dihydrofolate reductase (dhfr) and dihydropteroate synthase (dhps) genes was studied in pre-treatment samples in four sites in 2011.

Results

In the nine studies of AL conducted at five sites (n = 595), high PCR-corrected cure rates were found, ranging from 96.8 to 100 %. Among the eleven studies of AS + SP (n = 1013), a decline in the PCR-corrected cure rates was observed in Gedaref in Eastern Sudan: 91.0 % in the 2011–12 season and 86.5 % in the 2014–15 season. In the remaining sites, the AS + SP cure rates ranged between 95.6 and 100 %. The rate of clearance of microscopic gametocytaemia after treatment was not significantly different with AL or AS + SP on days 7, 14, 21 and 28 of follow-up. A total of 371 pre-treatment samples were analysed for molecular markers of SP resistance. The temporal changes and geographical differences in the frequency distribution of SP-resistance genotypes showed evidence of regional differentiation and selection of resistant strains.

Conclusion

The findings of this study call for a need to review the Sudan malaria treatment policy. Epidemiological factors could play a major role in the emergence of drug-resistant malaria in eastern Sudan.

Australian New Zealand Clinical Trials Registry

Trial registration numbers 2011–2012: ACTRN12611001253998, 2013–2015: ACTRN12613000945729
Literature
1.
go back to reference WHO. World malaria report, 2014. Geneva: World Health Organization; 2014. WHO. World malaria report, 2014. Geneva: World Health Organization; 2014.
2.
go back to reference Malik EM, Mohamed TA, Elmardi KA, Mowien RM, Elhassan AH, Elamin SB, et al. From chloroquine to artemisinin-based combination therapy: the Sudanese experience. Malar J. 2006;5:65.CrossRefPubMedPubMedCentral Malik EM, Mohamed TA, Elmardi KA, Mowien RM, Elhassan AH, Elamin SB, et al. From chloroquine to artemisinin-based combination therapy: the Sudanese experience. Malar J. 2006;5:65.CrossRefPubMedPubMedCentral
4.
go back to reference A-Elbasit I, Elbashir M, Khalil I, Alifrangis M, Giha H. The efficacy of sulfadoxine-pyrimethamine alone and in combination with chloroquine for malaria treatment in rural Eastern Sudan: the interrelation between resistance, age and gametocytogenesis. Trop Med Int Health. 2006;11:604–12.CrossRefPubMed A-Elbasit I, Elbashir M, Khalil I, Alifrangis M, Giha H. The efficacy of sulfadoxine-pyrimethamine alone and in combination with chloroquine for malaria treatment in rural Eastern Sudan: the interrelation between resistance, age and gametocytogenesis. Trop Med Int Health. 2006;11:604–12.CrossRefPubMed
6.
go back to reference Kublin JG, Dzinjalamala FK, Kamwendo DD, Malkin EM, Cortese JF, Martino LM, et al. Molecular markers for failure of sulfadoxine-pyrimethamine and chlorproguanil-dapsone treatment of Plasmodium falciparum malaria. J Infect Dis. 2002;185:380–8.CrossRefPubMed Kublin JG, Dzinjalamala FK, Kamwendo DD, Malkin EM, Cortese JF, Martino LM, et al. Molecular markers for failure of sulfadoxine-pyrimethamine and chlorproguanil-dapsone treatment of Plasmodium falciparum malaria. J Infect Dis. 2002;185:380–8.CrossRefPubMed
7.
go back to reference Vestergaard LS, Ringwald P. Responding to the challenge of antimalarial drug resistance by routine monitoring to update national malaria treatment policies. Am J Trop Med Hyg. 2007;77:153–9.PubMed Vestergaard LS, Ringwald P. Responding to the challenge of antimalarial drug resistance by routine monitoring to update national malaria treatment policies. Am J Trop Med Hyg. 2007;77:153–9.PubMed
8.
go back to reference Kublin JG, Cortese JF, Njunju EM, Rabia AG, Mukadam RA, Wirima JJ, et al. Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J Infect Dis. 2003;187:1870–5.CrossRefPubMed Kublin JG, Cortese JF, Njunju EM, Rabia AG, Mukadam RA, Wirima JJ, et al. Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J Infect Dis. 2003;187:1870–5.CrossRefPubMed
9.
go back to reference Laufer MK, Plowe CV. Withdrawing antimalarial drugs: impact on parasite resistance and implications for malaria treatment policies. Drug Resist Update. 2004;7:279–88.CrossRef Laufer MK, Plowe CV. Withdrawing antimalarial drugs: impact on parasite resistance and implications for malaria treatment policies. Drug Resist Update. 2004;7:279–88.CrossRef
14.
go back to reference Reeder JC, Rieckmann KH, Genton B, Lorry K, Wines B, Cowman AF. Point mutations in the dihydrofolate reductase and dihydropteroate synthetase genes and in vitro susceptibility to pyrimethamine and cycloguanil of Plasmodium falciparum isolates from Papua New Guinea. Am J Trop Med Hyg. 1996;55:209–13.PubMed Reeder JC, Rieckmann KH, Genton B, Lorry K, Wines B, Cowman AF. Point mutations in the dihydrofolate reductase and dihydropteroate synthetase genes and in vitro susceptibility to pyrimethamine and cycloguanil of Plasmodium falciparum isolates from Papua New Guinea. Am J Trop Med Hyg. 1996;55:209–13.PubMed
15.
go back to reference Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8.
17.
go back to reference Al-Saai S, Kheir A, Abdel-Muhsin AM, Al-Ghazali A, Nwakanma D, Swedberg G, et al. Distinct haplotypes of dhfr and dhps among Plasmodium falciparum isolates in an area of high level of sulfadoxine-pyrimethamine (SP) resistance in eastern Sudan. Infect Genet Evol. 2009;9:778–83.CrossRefPubMed Al-Saai S, Kheir A, Abdel-Muhsin AM, Al-Ghazali A, Nwakanma D, Swedberg G, et al. Distinct haplotypes of dhfr and dhps among Plasmodium falciparum isolates in an area of high level of sulfadoxine-pyrimethamine (SP) resistance in eastern Sudan. Infect Genet Evol. 2009;9:778–83.CrossRefPubMed
19.
go back to reference A-Elbasit IE, Khalil IF, Elbashir MI, Masuadi EM, Bygbjerg IC, Alifrangis M, et al. High frequency of Plasmodium falciparum CICNI/SGEAA and CVIET haplotypes without association with resistance to sulfadoxine/pyrimethamine and chloroquine combination in the Daraweesh area, in Sudan. Eur J Clin Microbiol Infect Dis. 2008;27:725–32.CrossRefPubMed A-Elbasit IE, Khalil IF, Elbashir MI, Masuadi EM, Bygbjerg IC, Alifrangis M, et al. High frequency of Plasmodium falciparum CICNI/SGEAA and CVIET haplotypes without association with resistance to sulfadoxine/pyrimethamine and chloroquine combination in the Daraweesh area, in Sudan. Eur J Clin Microbiol Infect Dis. 2008;27:725–32.CrossRefPubMed
21.
go back to reference Makanga M, Bassat Q, Falade CO, Premji ZG, Krudsood S, Hunt P, et al. Efficacy and safety of artemether-lumefantrine in the treatment of acute, uncomplicated Plasmodium falciparum malaria: a pooled analysis. Am J Trop Med Hyg. 2011;85:793–804.CrossRefPubMedPubMedCentral Makanga M, Bassat Q, Falade CO, Premji ZG, Krudsood S, Hunt P, et al. Efficacy and safety of artemether-lumefantrine in the treatment of acute, uncomplicated Plasmodium falciparum malaria: a pooled analysis. Am J Trop Med Hyg. 2011;85:793–804.CrossRefPubMedPubMedCentral
24.
go back to reference Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2009;361:455–67.CrossRefPubMedPubMedCentral Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2009;361:455–67.CrossRefPubMedPubMedCentral
26.
go back to reference Clyde DF. The problem of drug-resistant malaria. Am J Trop Med Hyg. 1971;21:736–43. Clyde DF. The problem of drug-resistant malaria. Am J Trop Med Hyg. 1971;21:736–43.
27.
go back to reference Ezzet F, van Vugt M, Nosten F, Looareesuwan S, White NJ. Pharmacokinetics and pharmacodynamics of lumefantrine (benflumetol) in acute falciparum malaria. Antimicrob Agents Chemother. 2000;44:697–704.CrossRefPubMedPubMedCentral Ezzet F, van Vugt M, Nosten F, Looareesuwan S, White NJ. Pharmacokinetics and pharmacodynamics of lumefantrine (benflumetol) in acute falciparum malaria. Antimicrob Agents Chemother. 2000;44:697–704.CrossRefPubMedPubMedCentral
28.
go back to reference White NJ. Why is it that antimalarial drug treatments do not always work? Ann Trop Med Parasitol. 1998;92:449–58.CrossRefPubMed White NJ. Why is it that antimalarial drug treatments do not always work? Ann Trop Med Parasitol. 1998;92:449–58.CrossRefPubMed
29.
go back to reference Gadalla NB, Abdallah TM, Atwal S, Sutherland CJ, Adam I. Selection of pfdhfr/pfdhps alleles and declining artesunate/sulphadoxine-pyrimethamine efficacy against Plasmodium falciparum 8 years after deployment in eastern Sudan. Malar J. 2013;12:255.CrossRefPubMedPubMedCentral Gadalla NB, Abdallah TM, Atwal S, Sutherland CJ, Adam I. Selection of pfdhfr/pfdhps alleles and declining artesunate/sulphadoxine-pyrimethamine efficacy against Plasmodium falciparum 8 years after deployment in eastern Sudan. Malar J. 2013;12:255.CrossRefPubMedPubMedCentral
30.
go back to reference Theander TG. Unstable malaria in Sudan: the influence of the dry season. Malaria in areas of unstable and seasonal transmission. Lessons from Daraweesh. Trans R Soc Trop Med Hyg. 1998;92:589–92.CrossRefPubMed Theander TG. Unstable malaria in Sudan: the influence of the dry season. Malaria in areas of unstable and seasonal transmission. Lessons from Daraweesh. Trans R Soc Trop Med Hyg. 1998;92:589–92.CrossRefPubMed
31.
go back to reference Djimdé AA, Doumbo OK, Traore O, Guindo AB, Kayentao K, Diourte Y, et al. Clearance of drug-resistant parasites as a model for protective immunity in Plasmodium falciparum malaria. Am J Trop Med Hyg. 2003;69:558–63.PubMed Djimdé AA, Doumbo OK, Traore O, Guindo AB, Kayentao K, Diourte Y, et al. Clearance of drug-resistant parasites as a model for protective immunity in Plasmodium falciparum malaria. Am J Trop Med Hyg. 2003;69:558–63.PubMed
32.
go back to reference Barnes KI, Watkins WM, White NJ. Antimalarial dosing regimens and drug resistance. Trends Parasitol. 2008;24:127–34.CrossRefPubMed Barnes KI, Watkins WM, White NJ. Antimalarial dosing regimens and drug resistance. Trends Parasitol. 2008;24:127–34.CrossRefPubMed
34.
go back to reference van den Broek I, Kitz C. Al Attas S, Libama F, Balasegaram M, Guthmann JP. Efficacy of three artemisinin combination therapies for the treatment of uncomplicated Plasmodium falciparum malaria in the Republic of Congo. Malar J. 2006;5:113.CrossRefPubMedPubMedCentral van den Broek I, Kitz C. Al Attas S, Libama F, Balasegaram M, Guthmann JP. Efficacy of three artemisinin combination therapies for the treatment of uncomplicated Plasmodium falciparum malaria in the Republic of Congo. Malar J. 2006;5:113.CrossRefPubMedPubMedCentral
36.
go back to reference Roper C, Pearce R, Nair S, Sharp B, Nosten F, Anderson T. Intercontinental spread of pyrimethamine-resistant malaria. Science. 2004;305:1124.CrossRefPubMed Roper C, Pearce R, Nair S, Sharp B, Nosten F, Anderson T. Intercontinental spread of pyrimethamine-resistant malaria. Science. 2004;305:1124.CrossRefPubMed
37.
go back to reference Watkins WM, Mosobo M. Treatment of Plasmodium falciparum malaria with pyrimethamine-sulfadoxine: selective pressure for resistance is a function of long elimination half-life. Trans R Soc Trop Med Hyg. 1993;87:75–8.CrossRefPubMed Watkins WM, Mosobo M. Treatment of Plasmodium falciparum malaria with pyrimethamine-sulfadoxine: selective pressure for resistance is a function of long elimination half-life. Trans R Soc Trop Med Hyg. 1993;87:75–8.CrossRefPubMed
38.
go back to reference Abdel-Hameed AA. Malaria case management at the community level in Gezira. Sudan. Afr J Med Med Sci. 2001;30(Suppl):43–6.PubMed Abdel-Hameed AA. Malaria case management at the community level in Gezira. Sudan. Afr J Med Med Sci. 2001;30(Suppl):43–6.PubMed
39.
go back to reference Yousif MA, Adeel AA. Antimalarials prescribing patterns in Gezira State: precepts and practices. East Mediterr Health J. 2000;6:939–47.PubMed Yousif MA, Adeel AA. Antimalarials prescribing patterns in Gezira State: precepts and practices. East Mediterr Health J. 2000;6:939–47.PubMed
40.
go back to reference Awad A, Eltayeb I, Matowe L, Thalib L. Self-medication with antibiotics and antimalarials in the community of Khartoum State, Sudan. J Pharm Pharm Sci. 2005;8:326–31.PubMed Awad A, Eltayeb I, Matowe L, Thalib L. Self-medication with antibiotics and antimalarials in the community of Khartoum State, Sudan. J Pharm Pharm Sci. 2005;8:326–31.PubMed
41.
go back to reference Bayoumi RA, Babiker HA, Ibrahim SM, Ghalib HW, Saeed BO, Khider S, et al. Chloroquine-resistant Plasmodium falciparum in eastern Sudan. Acta Trop. 1989;46:157–65.CrossRefPubMed Bayoumi RA, Babiker HA, Ibrahim SM, Ghalib HW, Saeed BO, Khider S, et al. Chloroquine-resistant Plasmodium falciparum in eastern Sudan. Acta Trop. 1989;46:157–65.CrossRefPubMed
42.
go back to reference Lienhardt C, Ghebray R, Candolfi E. Does chloroquine resistance occur in refugee camps in eastern Sudan? Trans R Soc Trop Med Hyg. 1989;83:486–7.CrossRefPubMed Lienhardt C, Ghebray R, Candolfi E. Does chloroquine resistance occur in refugee camps in eastern Sudan? Trans R Soc Trop Med Hyg. 1989;83:486–7.CrossRefPubMed
43.
go back to reference Jima D, Tesfaye G, Medhin A, Kebede A, Argaw D, Babaniyi O. Efficacy of sulfadoxine-pyrimethamine for the treatment of uncomplicated falciparum malaria in Ethiopia. East Afr Med J. 2005;82:391–5.PubMed Jima D, Tesfaye G, Medhin A, Kebede A, Argaw D, Babaniyi O. Efficacy of sulfadoxine-pyrimethamine for the treatment of uncomplicated falciparum malaria in Ethiopia. East Afr Med J. 2005;82:391–5.PubMed
44.
go back to reference Pearce RJ, Pota H, Evehe MS, el Ba H, Mombo-Ngoma G, Malisa AL, et al. Multiple origins and regional dispersal of resistant dhps in African Plasmodium falciparum malaria. PLoS Med. 2009;6:e1000055.CrossRefPubMedPubMedCentral Pearce RJ, Pota H, Evehe MS, el Ba H, Mombo-Ngoma G, Malisa AL, et al. Multiple origins and regional dispersal of resistant dhps in African Plasmodium falciparum malaria. PLoS Med. 2009;6:e1000055.CrossRefPubMedPubMedCentral
45.
go back to reference Basco LK, Tahar R, Ringwald P. Molecular basis of in vivo resistance to sulfadoxine-pyrimethamine in African adult patients infected with Plasmodium falciparum malaria parasites. Antimicrob Agents Chemother. 1998;42:1811–4.PubMedPubMedCentral Basco LK, Tahar R, Ringwald P. Molecular basis of in vivo resistance to sulfadoxine-pyrimethamine in African adult patients infected with Plasmodium falciparum malaria parasites. Antimicrob Agents Chemother. 1998;42:1811–4.PubMedPubMedCentral
46.
go back to reference Cowman AF, Morry MJ, Biggs BA, Cross GA, Foote SJ. Amino acid changes linked to pyrimethamine resistance in the dihydrofolate reductase-thymidylate synthase gene of Plasmodium falciparum. Proc Natl Acad Sci USA. 1988;85:9109–13.CrossRefPubMedPubMedCentral Cowman AF, Morry MJ, Biggs BA, Cross GA, Foote SJ. Amino acid changes linked to pyrimethamine resistance in the dihydrofolate reductase-thymidylate synthase gene of Plasmodium falciparum. Proc Natl Acad Sci USA. 1988;85:9109–13.CrossRefPubMedPubMedCentral
47.
go back to reference de Pecoulas PE, Basco LK, Le Bras J, Mazabraud A. Association between antifol resistance in vitro and DHFR gene point mutation in Plasmodium falciparum isolates. Trans R Soc Trop Med Hyg. 1996;90:181–2.CrossRefPubMed de Pecoulas PE, Basco LK, Le Bras J, Mazabraud A. Association between antifol resistance in vitro and DHFR gene point mutation in Plasmodium falciparum isolates. Trans R Soc Trop Med Hyg. 1996;90:181–2.CrossRefPubMed
48.
go back to reference Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase Chin reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.PubMed Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase Chin reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.PubMed
49.
go back to reference Naidoo I, Roper C. Mapping ‘partially resistant’, ‘fully resistant’, and ‘super resistant’ malaria. Trends Parasitol. 2013;29:505–15.CrossRefPubMed Naidoo I, Roper C. Mapping ‘partially resistant’, ‘fully resistant’, and ‘super resistant’ malaria. Trends Parasitol. 2013;29:505–15.CrossRefPubMed
50.
go back to reference Sridaran S, McClintock SK, Syphard LM, Herman KM, Barnwell JW, Udhayakumar V. Anti-folate drug resistance in Africa: meta-analysis of reported dihydrofolate reductase (dhfr) and dihydropteroate synthase (dhps) mutant genotype frequencies in African Plasmodium falciparum parasite populations. Malar J. 2010;9:247.CrossRefPubMedPubMedCentral Sridaran S, McClintock SK, Syphard LM, Herman KM, Barnwell JW, Udhayakumar V. Anti-folate drug resistance in Africa: meta-analysis of reported dihydrofolate reductase (dhfr) and dihydropteroate synthase (dhps) mutant genotype frequencies in African Plasmodium falciparum parasite populations. Malar J. 2010;9:247.CrossRefPubMedPubMedCentral
51.
go back to reference Nzila AM, Mberu EK, Sulo J, Dayo H, Winstanley PA, Sibley CH, et al. Towards an understanding of the mechanism of pyrimethamine-sulfadoxine resistance in Plasmodium falciparum: genotyping of dihydrofolate reductase and dihydropteroate synthase of Kenyan parasites. Antimicrob Agents Chemother. 2000;44:991–6.CrossRefPubMedPubMedCentral Nzila AM, Mberu EK, Sulo J, Dayo H, Winstanley PA, Sibley CH, et al. Towards an understanding of the mechanism of pyrimethamine-sulfadoxine resistance in Plasmodium falciparum: genotyping of dihydrofolate reductase and dihydropteroate synthase of Kenyan parasites. Antimicrob Agents Chemother. 2000;44:991–6.CrossRefPubMedPubMedCentral
52.
go back to reference Mberu EK, Mosobo MK, Nzila AM, Kokwaro GO, Sibley CH, Watkins WM. The changing in vitro susceptibility pattern to pyrimethamine/sulfadoxine in Plasmodium falciparum field isolates from Kilifi, Kenya. Am J Trop Med Hyg. 2000;62:396–401.PubMed Mberu EK, Mosobo MK, Nzila AM, Kokwaro GO, Sibley CH, Watkins WM. The changing in vitro susceptibility pattern to pyrimethamine/sulfadoxine in Plasmodium falciparum field isolates from Kilifi, Kenya. Am J Trop Med Hyg. 2000;62:396–401.PubMed
53.
go back to reference Osman ME, Mockenhaupt FP, Bienzle U, Elbashir MI, Giha HA. Field-based evidence for linkage of mutations associated with chloroquine (pfcrt/pfmdr1) and sulfadoxine-pyrimethamine (pfdhfr/pfdhps) resistance and for the fitness cost of multiple mutations in P. falciparum. Infect Genet Evol. 2007;7:52–9.CrossRefPubMed Osman ME, Mockenhaupt FP, Bienzle U, Elbashir MI, Giha HA. Field-based evidence for linkage of mutations associated with chloroquine (pfcrt/pfmdr1) and sulfadoxine-pyrimethamine (pfdhfr/pfdhps) resistance and for the fitness cost of multiple mutations in P. falciparum. Infect Genet Evol. 2007;7:52–9.CrossRefPubMed
54.
go back to reference Menegon M, Talha AA, Severini C, Elbushra SM, Mohamedani AA, Malik EM, et al. Frequency distribution of antimalarial drug resistance alleles among Plasmodium falciparum isolates from Gezira State, central Sudan, and Gedarif State, eastern Sudan. Am J Trop Med Hyg. 2010;83:250–7.CrossRefPubMedPubMedCentral Menegon M, Talha AA, Severini C, Elbushra SM, Mohamedani AA, Malik EM, et al. Frequency distribution of antimalarial drug resistance alleles among Plasmodium falciparum isolates from Gezira State, central Sudan, and Gedarif State, eastern Sudan. Am J Trop Med Hyg. 2010;83:250–7.CrossRefPubMedPubMedCentral
55.
go back to reference Abdel-Muhsin AM, Mackinnon MJ, Ali E, el Nassir KA, Suleiman S, Ahmed S, et al. Evolution of drug-resistance genes in Plasmodium falciparum in an area of seasonal malaria transmission in Eastern Sudan. J Infect Dis. 2004;189:1239–44.CrossRefPubMed Abdel-Muhsin AM, Mackinnon MJ, Ali E, el Nassir KA, Suleiman S, Ahmed S, et al. Evolution of drug-resistance genes in Plasmodium falciparum in an area of seasonal malaria transmission in Eastern Sudan. J Infect Dis. 2004;189:1239–44.CrossRefPubMed
56.
go back to reference Malisa A, Pearce R, Abdullah S, Mutayoba B, Mshinda H, Kachur P, et al. Molecular monitoring of resistant dhfr and dhps allelic haplotypes in Morogoro and Mvomero districts in south eastern Tanzania. Afr Health Sci. 2011;11:142–50.PubMedPubMedCentral Malisa A, Pearce R, Abdullah S, Mutayoba B, Mshinda H, Kachur P, et al. Molecular monitoring of resistant dhfr and dhps allelic haplotypes in Morogoro and Mvomero districts in south eastern Tanzania. Afr Health Sci. 2011;11:142–50.PubMedPubMedCentral
57.
go back to reference Hailemeskel E, Kassa M, Taddesse G, Mohammed H, Woyessa A, Tasew G, et al. Prevalence of sulfadoxine-pyrimethamine resistance-associated mutations in dhfr and dhps genes of Plasmodium falciparum three years after SP withdrawal in Bahir Dar. Northwest Ethiopia. Acta Trop. 2013;128:636–41.CrossRefPubMed Hailemeskel E, Kassa M, Taddesse G, Mohammed H, Woyessa A, Tasew G, et al. Prevalence of sulfadoxine-pyrimethamine resistance-associated mutations in dhfr and dhps genes of Plasmodium falciparum three years after SP withdrawal in Bahir Dar. Northwest Ethiopia. Acta Trop. 2013;128:636–41.CrossRefPubMed
58.
go back to reference Mula P, Fernández-Martínez A, de Lucio A, Ramos JM, Reyes F, González V, et al. Detection of high levels of mutations involved in anti-malarial drug resistance in Plasmodium falciparum and Plasmodium vivax at a rural hospital in southern Ethiopia. Malar J. 2011;10:214.CrossRefPubMedPubMedCentral Mula P, Fernández-Martínez A, de Lucio A, Ramos JM, Reyes F, González V, et al. Detection of high levels of mutations involved in anti-malarial drug resistance in Plasmodium falciparum and Plasmodium vivax at a rural hospital in southern Ethiopia. Malar J. 2011;10:214.CrossRefPubMedPubMedCentral
59.
go back to reference Al-Farsi HM, Al-Hashami ZS, Bin Dajem SM, Al-Sheikh AA, Al-Qahtani A, Beja-Pereira A, et al. Source of drug resistant Plasmodium falciparum in a potential malaria elimination site in Saudi Arabia. Infect Genet Evol. 2012;12:1253–9.CrossRefPubMed Al-Farsi HM, Al-Hashami ZS, Bin Dajem SM, Al-Sheikh AA, Al-Qahtani A, Beja-Pereira A, et al. Source of drug resistant Plasmodium falciparum in a potential malaria elimination site in Saudi Arabia. Infect Genet Evol. 2012;12:1253–9.CrossRefPubMed
Metadata
Title
High efficacy of artemether-lumefantrine and declining efficacy of artesunate + sulfadoxine-pyrimethamine against Plasmodium falciparum in Sudan (2010–2015): evidence from in vivo and molecular marker studies
Authors
Ahmed A. Adeel
Fahad Awad Ali Elnour
Khalid Abdalmutalab Elmardi
Mona B. Abd-Elmajid
Mai Mahmoud Elhelo
Mousab S. Ali
Mariam A. Adam
Hoda Atta
Ghasem Zamani
Marian Warsame
Amy Barrette
Hanan El Mohammady
Rania A. Nada
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1339-x

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