Characterising temporal trends in asymptomatic Plasmodium infections and transporter polymorphisms during transition from high to low transmission in Zanzibar, 2005-2013

Infection, Genetics and Evolution

Volumn 33, Issue , 2015, Pages 110-117

  Morris, Ulrika ^a   Xu, Weiping ^a   Msellem, Mwinyi I ^b   Schwartz, Alanna ^c   Abass, Ali ^b   Shakely, Delér ^a,d   Cook, Jackie ^a,b   Bhattarai, Achuyt ^e   Petzold, Max ^f,g   Greenhouse, Bryan ^c   Ali, Abdullah S ^b   Björkman, Anders ^a   Fröberg, Gabrielle ^a   Mårtensson, Andreas ^a,h  

^a KAROLINSKA INSTITUTE   (Sweden)

^b and Children   (Tanzania)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Kungälv Hospital   (Sweden)

^e CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^f UNIVERSITY OF GOTHENBURG   (Sweden)

^g UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^h UPPSALA UNIVERSITY   (Sweden)

Author keywords

Antimalarial drug resistance markers; Asymptomatic; Low transmission; Molecular surveillance; Plasmodium

Indexed keywords

ASPARTIC ACID; TYROSINE; CARRIER PROTEIN; PROTOZOAL PROTEIN;

ADULT; ARTICLE; ASYMPTOMATIC INFECTION; CHILD; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FEMALE; GENE FREQUENCY; GENETIC VARIABILITY; HEALTH SURVEY; HUMAN; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MALE; NONHUMAN; PARASITE PREVALENCE; PARASITE TRANSMISSION; PARASITE VECTOR; PFCRT GENE; PFMDR1 GENE; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; POPULATION DENSITY; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; SYMPTOM; TREND STUDY; YOUNG ADULT; ZOONOSIS; ADOLESCENT; CLASSIFICATION; GENETICS; GENOTYPE; INFANT; MALARIA, FALCIPARUM; MIDDLE AGED; PARASITE LOAD; PARASITOLOGY; PREVALENCE; TANZANIA;

PLASMODIUM FALCIPARUM;

ADOLESCENT; ADULT; ASYMPTOMATIC INFECTIONS; CHILD; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; FEMALE; GENOTYPE; HUMANS; INFANT; MALARIA, FALCIPARUM; MALE; MEMBRANE TRANSPORT PROTEINS; MIDDLE AGED; PARASITE LOAD; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE; PREVALENCE; PROTOZOAN PROTEINS; TANZANIA; YOUNG ADULT;

EID: 84937970915     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2015.04.018     Document Type: Article

References (54)

1. Alonso P.L., Tanner M. Public health challenges and prospects for malaria control and elimination. Nat. Med. 2013, 19:150-155.
2. Anderson T.J., Haubold B., Williams J.T., Estrada-Franco J.G., Richardson L., Mollinedo R., Bockarie M., Mokili J., Mharakurwa S., French N., Whitworth J., Velez I.D., Brockman A.H., Nosten F., Ferreira M.U., Day K.P. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol. Biol. Evol. 2000, 17:1467-1482.
3. Babiker H.A., Hastings I.M., Swedberg G. Impaired fitness of drug-resistant malaria parasites: evidence and implication on drug-deployment policies. Expert Rev. Anti Infect. Ther. 2009, 7:581-593.
4. Beer N., Ali A.S., Shakely D., Elfving K., Al-Mafazy A.W., Msellem M., Petzold M., Bjorkman A., Kallander K. High effective coverage of vector control interventions in children after achieving low malaria transmission in Zanzibar Tanzania. Malar. J. 2013, 12:38.
5. Bhattarai A., Ali A.S., Kachur S.P., Martensson A., Abbas A.K., Khatib R., Al-Mafazy A.W., Ramsan M., Rotllant G., Gerstenmaier J.F., Molteni F., Abdulla S., Montgomery S.M., Kaneko A., Bjorkman A. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 2007, 4:e309.
6. Bousema T., Okell L., Felger I., Drakeley C. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat. Rev. Microbiol. 2014.
7. Brown T., Smith L.S., Oo E.K., Shawng K., Lee T.J., Sullivan D., Beyrer C., Richards A.K. Molecular surveillance for drug-resistant Plasmodium falciparum in clinical and subclinical populations from three border regions of Burma/Myanmar: cross-sectional data and a systematic review of resistance studies. Malar. J. 2012, 11:333.
8. Cook J., Xu W., Msellem M., Vonk M., Bergstrom B., Gosling R., Al-Mafazy A.W., McElroy P., Molteni F., Abass A.K., Garimo I., Ramsan M., Ali A., Martensson A., Bjorkman A. Mass screening and treatment using a falciparum-specific rapid diagnostic test did not reduce malaria incidence in Zanzibar. J. Infect. Dis. 2014.
9. Costa D.C., Madureira A.P., Amaral L.C., Sanchez B.A., Gomes L.T., Fontes C.J., Limongi J.E., de Brito C.F., Carvalho L.H. Submicroscopic malaria parasite carriage: how reproducible are polymerase chain reaction-based methods?. Mem. Inst. Oswaldo Cruz 2014, 109:21-28.
10. Cotter C., Sturrock H.J., Hsiang M.S., Liu J., Phillips A.A., Hwang J., Gueye C.S., Fullman N., Gosling R.D., Feachem R.G. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet 2013.
11. Djimde A.A., Fofana B., Sagara I., Sidibe B., Toure S., Dembele D., Dama S., Ouologuem D., Dicko A., Doumbo O.K. Efficacy, safety, and selection of molecular markers of drug resistance by two ACTs in Mali. Am. J. Trop. Med. Hyg. 2008, 78:455-461.
12. Duraisingh M.T., Drakeley C.J., Muller O., Bailey R., Snounou G., Targett G.A., Greenwood B.M., Warhurst D.C. Evidence for selection for the tyrosine-86 allele of the pfmdr 1 gene of Plasmodium falciparum by chloroquine and amodiaquine. Parasitology 1997, 114(Pt 3):205-211.
13. Echeverry D.F., Holmgren G., Murillo C., Higuita J.C., Bjorkman A., Gil J.P., Osorio L. Short report: polymorphisms in the pfcrt and pfmdr1 genes of Plasmodium falciparum and in vitro susceptibility to amodiaquine and desethylamodiaquine. Am. J. Trop. Med. Hyg. 2007, 77:1034-1038.
14. Folarin O.A., Bustamante C., Gbotosho G.O., Sowunmi A., Zalis M.G., Oduola A.M., Happi C.T. In vitro amodiaquine resistance and its association with mutations in pfcrt and pfmdr1 genes of Plasmodium falciparum isolates from Nigeria. Acta Trop. 2011, 120:224-230.
15. Froberg G., Jornhagen L., Morris U., Shakely D., Msellem M.I., Gil J.P., Bjorkman A., Martensson A. Decreased prevalence of Plasmodium falciparum resistance markers to amodiaquine despite its wide scale use as ACT partner drug in Zanzibar. Malar. J. 2012, 11:321.
16. Froberg G., Ferreira P.E., Martensson A., Ali A., Bjorkman A., Gil J.P. Assessing the cost-benefit effect of a Plasmodium falciparum drug resistance mutation on parasite growth in vitro. Antimicrob. Agents Chemother. 2013, 57:887-892.
17. Ganguly S., Saha P., Guha S.K., Biswas A., Das S., Kundu P.K., Maji A.K. High prevalence of asymptomatic malaria in a tribal population in eastern India. J. Clin. Microbiol. 2013, 51:1439-1444.
18. Gharbi M., Flegg J.A., Hubert V., Kendjo E., Metcalf J.E., Bertaux L., Guerin P.J., Le Bras J., Members of the French National Reference Centre for Imported Malaria S., Aboubaca A., Agnamey P., Angoulvant A., Barbut P., Basset D., Belkadi G., Bellanger A.P., Bemba D., Benoit-Vica F., Berry A., Bigel M.L., Bonhomme J., Botterel F., Bouchaud O., Bougnoux M.E., Bouree P., Bourgeois N., Branger C., Bret L., Buret B., Casalino E., Chevrier S., Conquere de Monbrison F., Cuisenier B., Danis M., Darde M.L., De Gentile L., Delarbre J.M., Delaunay P., Delaval A., Desoubeaux G., Develoux M., Dunand J., Durand R., Eloy O., Fauchet N., Faugere B., Faye A., Fenneteau O., Flori P., Fontrouge M., Garabedian C., Gayandrieu F., Godineau N., Houze P., Houze S., Hurst J.P., Ichou H., Lachaud L., Lebuisson A., Lefevre M., LeGuern A.S., Le Moal G., Lusina D., Machouart M.C., Malvy D., Matheron S., Maubon D., Mechali D., Megarbane B., Menard G., Millon L., Aiach M.M., Minodier P., Morelle C., Nevez G., Parola P., Parzy D., Patey O., Patoz P., Penn P., Perignon A., Picot S., Pilo J.E., Poilane I., Pons D., Poupart M., Pradines B., Raffenot D., Rapp C., Receveur M.C., Sarfati C., Senghor Y., Simon F., Siriez J.Y., Taudon N., Thellier M., Thouvenin M., Toubas D. Longitudinal study assessing the return of chloroquine susceptibility of Plasmodium falciparum in isolates from travellers returning from West and Central Africa, 2000-2011. Malar. J. 2013, 12:35.
19. Golassa L., Enweji N., Erko B., Aseffa A., Swedberg G. Detection of a substantial number of sub-microscopic Plasmodium falciparum infections by polymerase chain reaction: a potential threat to malaria control and diagnosis in Ethiopia. Malar. J. 2013, 12:352.
20. Holmgren G., Gil J.P., Ferreira P.M., Veiga M.I., Obonyo C.O., Bjorkman A. Amodiaquine resistant Plasmodium falciparum malaria in vivo is associated with selection of pfcrt 76T and pfmdr1 86Y. Infect. Genet. Evol. 2006, 6:309-314.
21. Holmgren G., Hamrin J., Svard J., Martensson A., Gil J.P., Bjorkman A. Selection of pfmdr1 mutations after amodiaquine monotherapy and amodiaquine plus artemisinin combination therapy in East Africa. Infect. Genet. Evol. 2007, 7:562-569.
22. Humphreys G.S., Merinopoulos I., Ahmed J., Whitty C.J., Mutabingwa T.K., Sutherland C.J., Hallett R.L. Amodiaquine and artemether-lumefantrine select distinct alleles of the Plasmodium falciparum mdr1 gene in Tanzanian children treated for uncomplicated malaria. Antimicrob. Agents Chemother. 2007, 51:991-997.
23. Hwang J., Jaroensuk J., Leimanis M.L., Russell B., McGready R., Day N., Snounou G., Nosten F., Imwong M. Long-term storage limits PCR-based analyses of malaria parasites in archival dried blood spots. Malar. J. 2012, 11:339.
24. Ishengoma D.S., Lwitiho S., Madebe R.A., Nyagonde N., Persson O., Vestergaard L.S., Bygbjerg I.C., Lemnge M.M., Alifrangis M. Using rapid diagnostic tests as source of malaria parasite DNA for molecular analyses in the era of declining malaria prevalence. Malar. J. 2011, 10:6.
25. Kamau E., Tolbert L.S., Kortepeter L., Pratt M., Nyakoe N., Muringo L., Ogutu B., Waitumbi J.N., Ockenhouse C.F. Development of a highly sensitive genus-specific quantitative reverse transcriptase real-time PCR assay for detection and quantitation of plasmodium by amplifying RNA and DNA of the 18S rRNA genes. J. Clin. Microbiol. 2011, 49:2946-2953.
26. Kublin J.G., Cortese J.F., Njunju E.M., Mukadam R.A., Wirima J.J., Kazembe P.N., Djimde A.A., Kouriba B., Taylor T.E., Plowe C.V. Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J. Infect. Dis. 2003, 187:1870-1875.
27. Lin J.T., Saunders D.L., Meshnick S.R. The role of submicroscopic parasitemia in malaria transmission: what is the evidence?. Trends Parasitol. 2014, 30:183-190.
28. Manjurano A., Okell L., Lukindo T., Reyburn H., Olomi R., Roper C., Clarke T.G., Joseph S., Riley E.M., Drakeley C. Association of sub-microscopic malaria parasite carriage with transmission intensity in north-eastern Tanzania. Malar. J. 2011, 10:370.
29. Mawili-Mboumba D.P., Nikiema R., Bouyou-Akotet M.K., Bahamontes-Rosa N., Traore A., Kombila M. Sub-microscopic gametocyte carriage in febrile children living in different areas of Gabon. Malar. J. 2013, 12:375.
30. Morris U., Aydin-Schmidt B., Shakely D., Martensson A., Jornhagen L., Ali A.S., Msellem M.I., Petzold M., Gil J.P., Ferreira P., Bjorkman A. Rapid diagnostic tests for molecular surveillance of Plasmodium falciparum malaria -assessment of DNA extraction methods and field applicability. Malar. J. 2013, 12:106.
31. Msellem M.I., Martensson A., Rotllant G., Bhattarai A., Stromberg J., Kahigwa E., Garcia M., Petzold M., Olumese P., Ali A., Bjorkman A. Influence of rapid malaria diagnostic tests on treatment and health outcome in fever patients, Zanzibar: a crossover validation study. PLoS Med. 2009, 6:e1000070.
32. Mwingira F., Nkwengulila G., Schoepflin S., Sumari D., Beck H.P., Snounou G., Felger I., Olliaro P., Mugittu K. Plasmodium falciparum msp1, msp2 and glurp allele frequency and diversity in sub-Saharan Africa. Malar. J. 2011, 10:79.
33. Ndiaye M., Faye B., Tine R., Ndiaye J.L., Lo A., Abiola A., Dieng Y., Ndiaye D., Hallett R., Alifrangis M., Gaye O. Assessment of the molecular marker of Plasmodium falciparum chloroquine resistance (Pfcrt) in Senegal after several years of chloroquine withdrawal. Am. J. Trop. Med. Hyg. 2012, 87:640-645.
34. Nkhoma S., Molyneux M., Ward S. Molecular surveillance for drug-resistant Plasmodium falciparum malaria in Malawi. Acta Trop. 2007, 102:138-142.
35. Noor A.M., Kinyoki D.K., Mundia C.W., Kabaria C.W., Mutua J.W., Alegana V.A., Fall I.S., Snow R.W. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000-10: a spatial and temporal analysis of transmission intensity. Lancet 2014, 383:1739-1747.
36. Nsobya S.L., Dokomajilar C., Joloba M., Dorsey G., Rosenthal P.J. Resistance-mediating Plasmodium falciparum pfcrt and pfmdr1 alleles after treatment with artesunate-amodiaquine in Uganda. Antimicrob. Agents Chemother. 2007, 51:3023-3025.
37. Ogouyemi-Hounto A., Ndam N.T., Kinde Gazard D., d'Almeida S., Koussihoude L., Ollo E., Azagnandji C., Bello M., Chippaux J.P., Massougbodji A. Prevalence of the molecular marker of Plasmodium falciparum resistance to chloroquine and sulphadoxine/pyrimethamine in Benin seven years after the change of malaria treatment policy. Malar. J. 2013, 12:147.
38. Okell L.C., Ghani A.C., Lyons E., Drakeley C.J. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J. Infect. Dis. 2009, 200:1509-1517.
39. Okell L.C., Bousema T., Griffin J.T., Ouedraogo A.L., Ghani A.C., Drakeley C.J. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat. Commun. 2012, 3:1237.
40. Picot S., Olliaro P., de Monbrison F., Bienvenu A.L., Price R.N., Ringwald P. A systematic review and meta-analysis of evidence for correlation between molecular markers of parasite resistance and treatment outcome in falciparum malaria. Malar. J. 2009, 8:89.
41. Qiagen, 2012. QIAamp DNA mini and Blood Mini Handbook. Third ed., p. 42.
42. Roper C., Elhassan I.M., Hviid L., Giha H., Richardson W., Babiker H., Satti G.M., Theander T.G., Arnot D.E. Detection of very low level Plasmodium falciparum infections using the nested polymerase chain reaction and a reassessment of the epidemiology of unstable malaria in Sudan. Am. J. Trop. Med. Hyg. 1996, 54:325-331.
43. Rosenthal P.J. The interplay between drug resistance and fitness in malaria parasites. Mol. Microbiol. 2013, 89:1025-1038.
44. Sisya T.J., Kamn'gona R.M., Vareta J.A., Fulakeza J.M., Mukaka M.F., Seydel K.B., Laufer M.K., Taylor T.E., Nkhoma S.C. Subtle changes in Plasmodium falciparum infection complexity following enhanced intervention in Malawi. Acta Trop. 2015, 142:108-114.
45. Stresman G.H., Stevenson J.C., Ngwu N., Marube E., Owaga C., Drakeley C., Bousema T., Cox J. High levels of asymptomatic and subpatent Plasmodium falciparum parasite carriage at health facilities in an area of heterogeneous Malaria transmission intensity in the Kenyan highlands. Am. J. Trop. Med. Hyg. 2014.
46. Tietje K., Hawkins K., Clerk C., Ebels K., McGray S., Crudder C., Okell L., LaBarre P. The essential role of infection-detection technologies for malaria elimination and eradication. Trends Parasitol. 2014, 30:259-266.
47. Tukwasibwe S., Mugenyi L., Mbogo G.W., Nankoberanyi S., Maiteki-Sebuguzi C., Joloba M.L., Nsobya S.L., Staedke S.G., Rosenthal P.J. Differential prevalence of transporter polymorphisms in symptomatic and asymptomatic falciparum malaria infections in Uganda. J. Infect. Dis. 2014.
48. Tusting L.S., Bousema T., Smith D.L., Drakeley C. Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv. Parasitol. 2014, 84:151-208.
49. Venkatesan M., Gadalla N.B., Stepniewska K., Dahal P., Nsanzabana C., Moriera C., Price R.N., Martensson A., Rosenthal P.J., Dorsey G., Sutherland C.J., Guerin P., Davis T.M., Menard D., Adam I., Ademowo G., Arze C., Baliraine F.N., Berens-Riha N., Bjorkman A., Borrmann S., Checchi F., Desai M., Dhorda M., Djimde A.A., El-Sayed B.B., Eshetu T., Eyase F., Falade C., Faucher J.F., Froberg G., Grivoyannis A., Hamour S., Houze S., Johnson J., Kamugisha E., Kariuki S., Kiechel J.R., Kironde F., Kofoed P.E., LeBras J., Malmberg M., Mwai L., Ngasala B., Nosten F., Nsobya S.L., Nzila A., Oguike M., Otienoburu S.D., Ogutu B., Ouedraogo J.B., Piola P., Rombo L., Schramm B., Some A.F., Thwing J., Ursing J., Wong R.P., Zeynudin A., Zongo I., Plowe C.V., Sibley C.H., Group A.M.M.S., Wwarn A.L. Polymorphisms in Plasmodium falciparum chloroquine resistance transporter and multidrug resistance 1 genes: parasite risk factors that affect treatment outcomes for P. falciparum Malaria after artemether-lumefantrine and artesunate-amodiaquine. Am. J. Trop. Med. Hyg. 2014, 91:833-843.
50. WHO, 2010. World malaria report. Summary.
51. Wooden J., Kyes S., Sibley C.H. PCR and strain identification in Plasmodium falciparum. Parasitol. Today 1993, 9:303-305.
52. Wurtz N., Fall B., Pascual A., Diawara S., Sow K., Baret E., Diatta B., Fall K.B., Mbaye P.S., Fall F., Dieme Y., Rogier C., Bercion R., Briolant S., Wade B., Pradines B. Prevalence of molecular markers of Plasmodium falciparum drug resistance in Dakar, Senegal. Malar. J. 2012, 11:197.
53. Xu W., Morris U., Aydin-Schmidt B., Msellem M.I., Shakely D., Petzold M., Bjorkman A., Martensson A. SYBR green real-time PCR-RFLP assay targeting the Plasmodium cytochrome b gene - a highly sensitive molecular tool for malaria parasite detection and species determination. PloS one 2015, 10:e0120210.
54. Zhong D., Afrane Y., Githeko A., Yang Z., Cui L., Menge D.M., Temu E.A., Yan G. Plasmodium falciparum genetic diversity in western Kenya highlands. Am. J. Trop. Med. Hyg. 2007, 77:1043-1050.