Skip to main content
Top
Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Increase in the prevalence of mutations associated with sulfadoxine–pyrimethamine resistance in Plasmodium falciparum isolates collected from early to late pregnancy in Nanoro, Burkina Faso

Authors: Esmée Ruizendaal, Marc C. Tahita, Ronald B. Geskus, Inge Versteeg, Susana Scott, Umberto d’Alessandro, Palpouguini Lompo, Karim Derra, Maminata Traore-Coulibaly, Menno D. de Jong, Henk D. F. H. Schallig, Halidou Tinto, Petra F. Mens

Published in: Malaria Journal | Issue 1/2017

Login to get access

Abstract

Background

Pregnant women are a high-risk group for Plasmodium falciparum infections, which may result in maternal anaemia and low birth weight newborns, among other adverse birth outcomes. Intermittent preventive treatment with sulfadoxine–pyrimethamine during pregnancy (IPTp-SP) is widely implemented to prevent these negative effects of malaria. However, resistance against SP by P. falciparum may decrease efficacy of IPTp-SP. Combinations of point mutations in the dhps (codons A437, K540) and dhfr genes (codons N51, C59, S108) of P. falciparum are associated with SP resistance. In this study the prevalence of SP resistance mutations was determined among P. falciparum found in pregnant women and the general population (GP) from Nanoro, Burkina Faso and the association of IPTp-SP dosing and other variables with mutations was studied.

Methods

Blood spots on filter papers were collected from pregnant women at their first antenatal care visit (ANC booking) and at delivery, from an ongoing trial and from the GP in a cross-sectional survey. The dhps and dhfr genes were amplified by nested PCR and products were sequenced to identify mutations conferring resistance (ANC booking, n = 400; delivery, n = 223; GP, n = 400). Prevalence was estimated with generalized estimating equations and for multivariate analyses mixed effects logistic regression was used.

Results

The prevalence of the triple dhfr mutation was high, and significantly higher in the GP and at delivery than at ANC booking, but it did not affect birth weight. Furthermore, quintuple mutations (triple dhfr and double dhps mutations) were found for the first time in Burkina Faso. IPTp-SP did not significantly affect the occurrence of any of the mutations, but high transmission season was associated with increased mutation prevalence in delivery samples. It is unclear why the prevalence of mutations was higher in the GP than in pregnant women at ANC booking.

Conclusion

The high number of mutants and the presence of quintuple mutants in Burkina Faso confirm concerns about the efficacy of IPTp-SP in the near future. Other drug combinations to tackle malaria in pregnancy should, therefore, be explored. An increase in mutation prevalence due to IPTp-SP dosing could not be confirmed.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO. World Malaria report 2015. Geneva: World Health Organization; 2015. WHO. World Malaria report 2015. Geneva: World Health Organization; 2015.
2.
go back to reference Adu B, Cherif MK, Bosomprah S, Diarra A, Arthur FKN, Dickson EK, et al. Antibody levels against GLURP R2, MSP1 block 2 hybrid and AS202.11 and the risk of malaria in children living in hyperendemic (Burkina Faso) and hypo-endemic (Ghana) areas. Malar J. 2016;15:123.CrossRefPubMedPubMedCentral Adu B, Cherif MK, Bosomprah S, Diarra A, Arthur FKN, Dickson EK, et al. Antibody levels against GLURP R2, MSP1 block 2 hybrid and AS202.11 and the risk of malaria in children living in hyperendemic (Burkina Faso) and hypo-endemic (Ghana) areas. Malar J. 2016;15:123.CrossRefPubMedPubMedCentral
3.
go back to reference Ryg-Cornejo V, Ly A, Hansen DS. Immunological processes underlying the slow acquisition of humoral immunity to malaria. Parasitology. 2016;143:199–207.CrossRefPubMed Ryg-Cornejo V, Ly A, Hansen DS. Immunological processes underlying the slow acquisition of humoral immunity to malaria. Parasitology. 2016;143:199–207.CrossRefPubMed
4.
go back to reference Fried M, Duffy PE. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science. 1996;272:1502–4.CrossRefPubMed Fried M, Duffy PE. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science. 1996;272:1502–4.CrossRefPubMed
5.
go back to reference Rogerson SJ, Hviid L, Duffy PE, Leke RFG, Taylor DW. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis. 2007;7:105–17.CrossRefPubMed Rogerson SJ, Hviid L, Duffy PE, Leke RFG, Taylor DW. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis. 2007;7:105–17.CrossRefPubMed
6.
go back to reference Maubert B, Fievet N, Tami G, Cot M, Boudin C, Deloron P. Development of antibodies against chondroitin sulfate A-adherent Plasmodium falciparum in pregnant women. Infect Immun. 1999;67:5367–71.PubMedPubMedCentral Maubert B, Fievet N, Tami G, Cot M, Boudin C, Deloron P. Development of antibodies against chondroitin sulfate A-adherent Plasmodium falciparum in pregnant women. Infect Immun. 1999;67:5367–71.PubMedPubMedCentral
7.
go back to reference Fried M, Nosten F, Brockman A, Brabin B, Duffy PE. Maternal antibodies block malaria. Nature. 1998;20:851–2.CrossRef Fried M, Nosten F, Brockman A, Brabin B, Duffy PE. Maternal antibodies block malaria. Nature. 1998;20:851–2.CrossRef
8.
go back to reference Duffy PE, Fried M. Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate a are associated with increased birth weight and the gestational age of newborns. Infect Immun. 2003;71:6620–3.CrossRefPubMedPubMedCentral Duffy PE, Fried M. Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate a are associated with increased birth weight and the gestational age of newborns. Infect Immun. 2003;71:6620–3.CrossRefPubMedPubMedCentral
9.
go back to reference Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, et al. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis. 2007;7:93–104.CrossRefPubMed Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, et al. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis. 2007;7:93–104.CrossRefPubMed
11.
go back to reference World Health Organization. Policy brief for the implementation of intermittent preventive treatment of malaria in pregnancy using sulfadoxine–pyrimethamine (IPTp-SP). Geneva: World Health Organization; 2013. World Health Organization. Policy brief for the implementation of intermittent preventive treatment of malaria in pregnancy using sulfadoxine–pyrimethamine (IPTp-SP). Geneva: World Health Organization; 2013.
12.
go back to reference WHO. A Strategic framework for malaria prevention and control during pregnancy in the African Region. Brazzaville: World Health Organization Regional Office for Africa; 2004. WHO. A Strategic framework for malaria prevention and control during pregnancy in the African Region. Brazzaville: World Health Organization Regional Office for Africa; 2004.
13.
go back to reference Karunajeewa HA, Salman S, Mueller I, Baiwog F, Gomorrai S, Law I, et al. Pharmacokinetic properties of sulfadoxine–pyrimethamine in pregnant women. Antimicrob Agents Chemother. 2009;53:4368–76.CrossRefPubMedPubMedCentral Karunajeewa HA, Salman S, Mueller I, Baiwog F, Gomorrai S, Law I, et al. Pharmacokinetic properties of sulfadoxine–pyrimethamine in pregnant women. Antimicrob Agents Chemother. 2009;53:4368–76.CrossRefPubMedPubMedCentral
14.
15.
go back to reference Geiger C, Compaore G, Coulibaly B, Sie A, Dittmer M, Sanchez C, et al. Substantial increase in mutations in the genes pfdhfr and pfdhps puts sulphadoxine-pyrimethamine-based intermittent preventive treatment for malaria at risk in Burkina Faso. Trop Med Int Health. 2014;19:690–7.CrossRefPubMed Geiger C, Compaore G, Coulibaly B, Sie A, Dittmer M, Sanchez C, et al. Substantial increase in mutations in the genes pfdhfr and pfdhps puts sulphadoxine-pyrimethamine-based intermittent preventive treatment for malaria at risk in Burkina Faso. Trop Med Int Health. 2014;19:690–7.CrossRefPubMed
16.
go back to reference Harrington WE, Mutabingwa TK, Muehlenbachs A, Sorensen B, Bolla MC, Fried M, et al. Competitive facilitation of drug-resistant Plasmodium falciparum malaria parasites in pregnant women who receive preventive treatment. Proc Natl Acad Sci USA. 2009;106:9027–32.CrossRefPubMedPubMedCentral Harrington WE, Mutabingwa TK, Muehlenbachs A, Sorensen B, Bolla MC, Fried M, et al. Competitive facilitation of drug-resistant Plasmodium falciparum malaria parasites in pregnant women who receive preventive treatment. Proc Natl Acad Sci USA. 2009;106:9027–32.CrossRefPubMedPubMedCentral
17.
go back to reference Harrington WE, Morrison R, Fried M, Duffy PE. Intermittent preventive treatment in pregnant women is associated with increased risk of severe malaria in their offspring. PLoS ONE. 2013;8:e56183.CrossRefPubMedPubMedCentral Harrington WE, Morrison R, Fried M, Duffy PE. Intermittent preventive treatment in pregnant women is associated with increased risk of severe malaria in their offspring. PLoS ONE. 2013;8:e56183.CrossRefPubMedPubMedCentral
18.
go back to reference Desai M, Gutman J, Taylor SM, Wiegand RE, Khairallah C, Kayentao K, et al. Impact of sulfadoxine–pyrimethamine resistance on effectiveness of intermittent preventive therapy for malaria in pregnancy at clearing infections and preventing low birth weight. Clin Infect Dis. 2016;62:323–33.CrossRefPubMed Desai M, Gutman J, Taylor SM, Wiegand RE, Khairallah C, Kayentao K, et al. Impact of sulfadoxine–pyrimethamine resistance on effectiveness of intermittent preventive therapy for malaria in pregnancy at clearing infections and preventing low birth weight. Clin Infect Dis. 2016;62:323–33.CrossRefPubMed
19.
go back to reference Happi CT, Gbotosho GO, Folarin OA, Akinboye DO, Yusuf BO, Ebong OO, et al. Polymorphisms in Plasmodium falciparum dhfr and dhps genes and age related in vivo sulfadoxine–pyrimethamine resistance in malaria-infected patients from Nigeria. Acta Trop. 2005;95:183–93.CrossRefPubMed Happi CT, Gbotosho GO, Folarin OA, Akinboye DO, Yusuf BO, Ebong OO, et al. Polymorphisms in Plasmodium falciparum dhfr and dhps genes and age related in vivo sulfadoxine–pyrimethamine resistance in malaria-infected patients from Nigeria. Acta Trop. 2005;95:183–93.CrossRefPubMed
20.
go back to reference Gansané A, Nébié I, Soulama I, Tiono A, Diarra A, Konaté AT, et al. Les raison d’un changement de médicaments de première intention pour le traitement du paludisme simple au Burkina Faso en 2005. Bull Soc Path Exot. 2009;102:31–5.CrossRef Gansané A, Nébié I, Soulama I, Tiono A, Diarra A, Konaté AT, et al. Les raison d’un changement de médicaments de première intention pour le traitement du paludisme simple au Burkina Faso en 2005. Bull Soc Path Exot. 2009;102:31–5.CrossRef
21.
go back to reference Bertin G, Briand V, Bonaventure D, Carrieu A, Massougbodji A, Cot M, et al. Molecular markers of resistance to sulphadoxine-pyrimethamine during intermittent preventive treatment of pregnant women in Benin. Malar J. 2011;10:196.CrossRefPubMedPubMedCentral Bertin G, Briand V, Bonaventure D, Carrieu A, Massougbodji A, Cot M, et al. Molecular markers of resistance to sulphadoxine-pyrimethamine during intermittent preventive treatment of pregnant women in Benin. Malar J. 2011;10:196.CrossRefPubMedPubMedCentral
22.
go back to reference Coulibaly SO, Kayentao K, Taylor S, Guirou EA, Khairallah C, Guindo N, et al. Parasite clearance following treatment with sulphadoxine-pyrimethamine for intermittent preventive treatment in Burkina-Faso and Mali: 42-day in vivo follow-up study. Malar J. 2014;13:41.CrossRefPubMedPubMedCentral Coulibaly SO, Kayentao K, Taylor S, Guirou EA, Khairallah C, Guindo N, et al. Parasite clearance following treatment with sulphadoxine-pyrimethamine for intermittent preventive treatment in Burkina-Faso and Mali: 42-day in vivo follow-up study. Malar J. 2014;13:41.CrossRefPubMedPubMedCentral
23.
go back to reference Tahita MC, Tinto H, Erhart A, Kazienga A, Fitzhenry R, VanOvermeir C, et al. Prevalence of the dhfr and dhps Mutations among pregnant women in rural Burkina Faso five years after the introduction of intermittent preventive treatment with sulfadoxine–pyrimethamine. PLoS ONE. 2015;10:e0137440.CrossRefPubMedPubMedCentral Tahita MC, Tinto H, Erhart A, Kazienga A, Fitzhenry R, VanOvermeir C, et al. Prevalence of the dhfr and dhps Mutations among pregnant women in rural Burkina Faso five years after the introduction of intermittent preventive treatment with sulfadoxine–pyrimethamine. PLoS ONE. 2015;10:e0137440.CrossRefPubMedPubMedCentral
24.
go back to reference Scott S, Mens PF, Tinto H, Nahum A, Ruizendaal E, Pagnoni F, et al. Community-based scheduled screening and treatment of malaria in pregnancy for improved maternal and infant health in The Gambia, Burkina Faso and Benin: study protocol for a randomized controlled trial. Trials. 2014;15:340.CrossRefPubMedPubMedCentral Scott S, Mens PF, Tinto H, Nahum A, Ruizendaal E, Pagnoni F, et al. Community-based scheduled screening and treatment of malaria in pregnancy for improved maternal and infant health in The Gambia, Burkina Faso and Benin: study protocol for a randomized controlled trial. Trials. 2014;15:340.CrossRefPubMedPubMedCentral
25.
go back to reference Kattenberg JH, Tahita CM, Versteeg IJ, Tinto H, Traoré-Coulibaly M, Schallig HDFH, et al. Antigen persistence of rapid diagnostic tests in pregnant women in Nanoro, Burkina Faso, and the implications for the diagnosis of malaria in pregnancy. Trop Med Int Health. 2012;17:550–7.CrossRefPubMed Kattenberg JH, Tahita CM, Versteeg IJ, Tinto H, Traoré-Coulibaly M, Schallig HDFH, et al. Antigen persistence of rapid diagnostic tests in pregnant women in Nanoro, Burkina Faso, and the implications for the diagnosis of malaria in pregnancy. Trop Med Int Health. 2012;17:550–7.CrossRefPubMed
26.
go back to reference Hermsen CC, Telgt DS, Linders EH, van de Locht LA, Eling WM, Mensink EJ, et al. Detection of Plasmodium falciparum malaria parasites in vivo by real-time quantitative PCR. Mol Biochem Parasitol. 2001;118:247–51.CrossRefPubMed Hermsen CC, Telgt DS, Linders EH, van de Locht LA, Eling WM, Mensink EJ, et al. Detection of Plasmodium falciparum malaria parasites in vivo by real-time quantitative PCR. Mol Biochem Parasitol. 2001;118:247–51.CrossRefPubMed
27.
go back to reference Wang CW, Hermsen CC, Sauerwein RW, Arnot DE, Theander TG, Lavstsen T. The Plasmodium falciparum var gene transcription strategy at the onset of blood stage infection in a human volunteer. Parasitol Int. 2009;58:478–80.CrossRefPubMed Wang CW, Hermsen CC, Sauerwein RW, Arnot DE, Theander TG, Lavstsen T. The Plasmodium falciparum var gene transcription strategy at the onset of blood stage infection in a human volunteer. Parasitol Int. 2009;58:478–80.CrossRefPubMed
28.
go back to reference Duraisingh MT, Curtis J, Warhurst DC. Plasmodium falciparum: detection of polymorphisms in the dihydrofolate reductase and dihydropteroate synthetase genes by PCR and restriction digestion. Exp Parasitol. 1998;89:1–8.CrossRefPubMed Duraisingh MT, Curtis J, Warhurst DC. Plasmodium falciparum: detection of polymorphisms in the dihydrofolate reductase and dihydropteroate synthetase genes by PCR and restriction digestion. Exp Parasitol. 1998;89:1–8.CrossRefPubMed
29.
go back to reference Diallo DA, Sutherland C, Nebié I, Konaté AT, Ord R, Pota H, et al. Sustained use of insecticide-treated curtains is not associated with greater circulation of drug-resistant malaria parasites, or with higher risk of treatment failure among children with uncomplicated malaria in Burkina Faso. Am J Trop Med Hyg. 2007;76:237–44.PubMed Diallo DA, Sutherland C, Nebié I, Konaté AT, Ord R, Pota H, et al. Sustained use of insecticide-treated curtains is not associated with greater circulation of drug-resistant malaria parasites, or with higher risk of treatment failure among children with uncomplicated malaria in Burkina Faso. Am J Trop Med Hyg. 2007;76:237–44.PubMed
30.
go back to reference Bouyou-Akotet MK, Mawili-Mboumba DP, Tchantchou T, Kombila M. High prevalence of sulfadoxine/pyrimethamine-resistant alleles of Plasmodium falciparum isolates in pregnant women at the time of introduction of intermittent preventive treatment with sulfadoxine/pyrimethamine in Gabon. J Antimicrob Chemother. 2010;65:438–41.CrossRefPubMed Bouyou-Akotet MK, Mawili-Mboumba DP, Tchantchou T, Kombila M. High prevalence of sulfadoxine/pyrimethamine-resistant alleles of Plasmodium falciparum isolates in pregnant women at the time of introduction of intermittent preventive treatment with sulfadoxine/pyrimethamine in Gabon. J Antimicrob Chemother. 2010;65:438–41.CrossRefPubMed
31.
go back to reference Mockenhaupt FP, Bedu-Addo G, Eggelte TA, Hommerich L, Holmberg V, von Oertzen C, et al. Rapid increase in the prevalence of sulfadoxine–pyrimethamine resistance among Plasmodium falciparum isolated from pregnant women in Ghana. J Infect Dis. 2008;198:1545–9.CrossRefPubMed Mockenhaupt FP, Bedu-Addo G, Eggelte TA, Hommerich L, Holmberg V, von Oertzen C, et al. Rapid increase in the prevalence of sulfadoxine–pyrimethamine resistance among Plasmodium falciparum isolated from pregnant women in Ghana. J Infect Dis. 2008;198:1545–9.CrossRefPubMed
32.
go back to reference Moussiliou A, De Tove YS-S, Doritchamou J, Luty AJF, Massougbodji A, Alifrangis M, et al. High rates of parasite recrudescence following intermittent preventive treatment with sulphadoxine–pyrimethamine during pregnancy in Benin. Malar J. 2013;12:195.CrossRefPubMedPubMedCentral Moussiliou A, De Tove YS-S, Doritchamou J, Luty AJF, Massougbodji A, Alifrangis M, et al. High rates of parasite recrudescence following intermittent preventive treatment with sulphadoxine–pyrimethamine during pregnancy in Benin. Malar J. 2013;12:195.CrossRefPubMedPubMedCentral
33.
go back to reference Chauvin P, Menard S, Iriart X, Nsango SE, Tchioffo MT, Abate L, et al. Prevalence of Plasmodium falciparum parasites resistant to sulfadoxine/pyrimethamine in pregnant women in Yaounde, Cameroon: emergence of highly resistant pfdhfr/pfdhps alleles. J Antimicrob Chemother. 2015;70:2566–71.CrossRefPubMed Chauvin P, Menard S, Iriart X, Nsango SE, Tchioffo MT, Abate L, et al. Prevalence of Plasmodium falciparum parasites resistant to sulfadoxine/pyrimethamine in pregnant women in Yaounde, Cameroon: emergence of highly resistant pfdhfr/pfdhps alleles. J Antimicrob Chemother. 2015;70:2566–71.CrossRefPubMed
34.
go back to reference Menéndez C, Serra-Casas E, Scahill MD, Sanz S, Nhabomba A, Bardají A, et al. HIV and placental infection modulate the appearance of drug-resistant Plasmodium falciparum in pregnant women who receive intermittent preventive treatment. Clin Infect Dis. 2011;52:41–8.CrossRefPubMed Menéndez C, Serra-Casas E, Scahill MD, Sanz S, Nhabomba A, Bardají A, et al. HIV and placental infection modulate the appearance of drug-resistant Plasmodium falciparum in pregnant women who receive intermittent preventive treatment. Clin Infect Dis. 2011;52:41–8.CrossRefPubMed
35.
go back to reference Asih PBS, Rogers WO, Susanti AI, Rahmat A, Rozi IE, Kusumaningtyas MA, et al. Seasonal distribution of anti-malarial drug resistance alleles on the island of Sumba, Indonesia. Malar J. 2009;8:222.CrossRefPubMedPubMedCentral Asih PBS, Rogers WO, Susanti AI, Rahmat A, Rozi IE, Kusumaningtyas MA, et al. Seasonal distribution of anti-malarial drug resistance alleles on the island of Sumba, Indonesia. Malar J. 2009;8:222.CrossRefPubMedPubMedCentral
36.
go back to reference Bushman M, Morton L, Duah N, Quashie N, Abuaku B, Koram KA, et al. Within-host competition and drug resistance in the human malaria parasite Plasmodium falciparum. Proc R Soc Lond B. 2016;283:20183038.CrossRef Bushman M, Morton L, Duah N, Quashie N, Abuaku B, Koram KA, et al. Within-host competition and drug resistance in the human malaria parasite Plasmodium falciparum. Proc R Soc Lond B. 2016;283:20183038.CrossRef
37.
go back to reference Wargo AR, Huijben S, de Roode JC, Shepherd J, Read AF. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc Natl Acad Sci USA. 2007;104:19914–9.CrossRefPubMedPubMedCentral Wargo AR, Huijben S, de Roode JC, Shepherd J, Read AF. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc Natl Acad Sci USA. 2007;104:19914–9.CrossRefPubMedPubMedCentral
38.
go back to reference Råberg L, de Roode JC, Bell AS, Stamou P, Gray D, Read AF. The role of immune-mediated apparent competition in genetically diverse malaria infections. Am Nat. 2006;168:41–53.PubMed Råberg L, de Roode JC, Bell AS, Stamou P, Gray D, Read AF. The role of immune-mediated apparent competition in genetically diverse malaria infections. Am Nat. 2006;168:41–53.PubMed
39.
go back to reference Agomo CO, Oyibo WA, Sutherland C, Hallet R, Oguike M. Assessment of markers of antimalarial drug resistance in Plasmodium falciparum isolates from pregnant women in Lagos, Nigeria. PLoS ONE. 2016;11:e0146908.CrossRefPubMedPubMedCentral Agomo CO, Oyibo WA, Sutherland C, Hallet R, Oguike M. Assessment of markers of antimalarial drug resistance in Plasmodium falciparum isolates from pregnant women in Lagos, Nigeria. PLoS ONE. 2016;11:e0146908.CrossRefPubMedPubMedCentral
40.
go back to reference Iwalokun BA, Iwalokun SO, Adebodun V, Balogun M. Carriage of mutant dihydrofolate reductase and dihydropteroate synthase genes among Plasmodium falciparum isolates recovered from pregnant women with asymptomatic infection in Lagos, Nigeria. Med Princ Pract. 2015;24:436–43.CrossRefPubMed Iwalokun BA, Iwalokun SO, Adebodun V, Balogun M. Carriage of mutant dihydrofolate reductase and dihydropteroate synthase genes among Plasmodium falciparum isolates recovered from pregnant women with asymptomatic infection in Lagos, Nigeria. Med Princ Pract. 2015;24:436–43.CrossRefPubMed
41.
go back to reference Khalil IF, Rønn AM, Alifrangis M, Gabar HA, Jelinek T, Satti GMH, et al. Response of Plasmodium falciparum to cotrimoxazole therapy: relationship with plasma drug concentrations and dihydrofolate reductase and dihydropteroate synthase genotypes. Am J Trop Med Hyg. 2005;73:174–7.PubMed Khalil IF, Rønn AM, Alifrangis M, Gabar HA, Jelinek T, Satti GMH, et al. Response of Plasmodium falciparum to cotrimoxazole therapy: relationship with plasma drug concentrations and dihydrofolate reductase and dihydropteroate synthase genotypes. Am J Trop Med Hyg. 2005;73:174–7.PubMed
42.
go back to reference Mockenhaupt FP, May J, Eggelte TA, Thies FL, Ademowo OG, Bienzle U, et al. Short report: high prevalence and imbalanced age distribution of the Plasmodium falciparum dihydrofolate reductase gene Asn108 mutation in an area of low pyrimethamine usage in Nigeria. Am J Trop Med Hyg. 1999;61:375–7.PubMed Mockenhaupt FP, May J, Eggelte TA, Thies FL, Ademowo OG, Bienzle U, et al. Short report: high prevalence and imbalanced age distribution of the Plasmodium falciparum dihydrofolate reductase gene Asn108 mutation in an area of low pyrimethamine usage in Nigeria. Am J Trop Med Hyg. 1999;61:375–7.PubMed
43.
go back to reference Raman J, Little F, Roper C, Kleinschmidt I, Cassam Y, Maharaj R, et al. 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. 2010;82:788–94.CrossRefPubMedPubMedCentral Raman J, Little F, Roper C, Kleinschmidt I, Cassam Y, Maharaj R, et al. 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. 2010;82:788–94.CrossRefPubMedPubMedCentral
44.
go back to reference McCollum AM, Schneider KA, Griffing SM, Zhou Z, Kariuki S, Ter-Kuile F, et al. Differences in selective pressure on dhps and dhfr drug resistant mutations in western Kenya. Malar J. 2012;11:77.CrossRefPubMedPubMedCentral McCollum AM, Schneider KA, Griffing SM, Zhou Z, Kariuki S, Ter-Kuile F, et al. Differences in selective pressure on dhps and dhfr drug resistant mutations in western Kenya. Malar J. 2012;11:77.CrossRefPubMedPubMedCentral
45.
go back to reference Minja DTR, Schmiegelow C, Mmbando B, Boström S, Oesterholt M, Magistrado P, et al. Plasmodium falciparum mutant haplotype infection during pregnancy associated with reduced birthweight, Tanzania. Emerg Infect Dis. 2013;19:1446–54.CrossRefPubMedCentral Minja DTR, Schmiegelow C, Mmbando B, Boström S, Oesterholt M, Magistrado P, et al. Plasmodium falciparum mutant haplotype infection during pregnancy associated with reduced birthweight, Tanzania. Emerg Infect Dis. 2013;19:1446–54.CrossRefPubMedCentral
46.
go back to reference Gutman J, Kalilani L, Taylor S, Zhou Z, Wiegand RE, Thwai KL, et al. The A581G mutation in the gene encoding Plasmodium falciparum dihydropteroate synthetase reduces the effectiveness of sulfadoxine–pyrimethamine preventive therapy in Malawian pregnant women. J Infect Dis. 2015;211:1997–2005.CrossRefPubMedPubMedCentral Gutman J, Kalilani L, Taylor S, Zhou Z, Wiegand RE, Thwai KL, et al. The A581G mutation in the gene encoding Plasmodium falciparum dihydropteroate synthetase reduces the effectiveness of sulfadoxine–pyrimethamine preventive therapy in Malawian pregnant women. J Infect Dis. 2015;211:1997–2005.CrossRefPubMedPubMedCentral
47.
go back to reference Chico RM, Cano J, Ariti C, Collier TJ, Chandramohan D, Roper C, et al. Influence of malaria transmission intensity and the 581G mutation on the efficacy of intermittent preventive treatment in pregnancy: systematic review and meta-analysis. Trop Med Int Health. 2015;20:1621–33.CrossRefPubMed Chico RM, Cano J, Ariti C, Collier TJ, Chandramohan D, Roper C, et al. Influence of malaria transmission intensity and the 581G mutation on the efficacy of intermittent preventive treatment in pregnancy: systematic review and meta-analysis. Trop Med Int Health. 2015;20:1621–33.CrossRefPubMed
Metadata
Title
Increase in the prevalence of mutations associated with sulfadoxine–pyrimethamine resistance in Plasmodium falciparum isolates collected from early to late pregnancy in Nanoro, Burkina Faso
Authors
Esmée Ruizendaal
Marc C. Tahita
Ronald B. Geskus
Inge Versteeg
Susana Scott
Umberto d’Alessandro
Palpouguini Lompo
Karim Derra
Maminata Traore-Coulibaly
Menno D. de Jong
Henk D. F. H. Schallig
Halidou Tinto
Petra F. Mens
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-1831-y

Other articles of this Issue 1/2017

Malaria Journal 1/2017 Go to the issue