Mutant Plasmodium falciparum chloroquine resistance transporter in Hodeidah, Yemen: Association with parasitologic indices and treatment-seeking behaviors

Acta Tropica

Volumn 128, Issue 3, 2013, Pages 473-478

  Abdul Ghani, Rashad ^a,b   Farag, Hoda F ^a   Allam, Amal F ^a   Shawky, Sherine M ^a   Al Mekhlafi, Abdulsalam M ^b  

^a ALEXANDRIA UNIVERSITY   (Egypt)

^b SANA A UNIVERSITY   (Yemen)

Author keywords

Chloroquine; Drug resistance; Hodeidah; Pfcrt; Plasmodium falciparum; Treatment seeking behavior

Indexed keywords

ANTIMALARIAL AGENT; CARRIER PROTEIN; CHLOROQUINE; PLASMODIUM FALCIPARUM CHLOROQUINE RESISTANCE TRANSPORTER; UNCLASSIFIED DRUG;

DISEASE INCIDENCE; DISEASE RESISTANCE; DISEASE TREATMENT; DRUG PRESCRIBING; HEALTH GEOGRAPHY; MALARIA; MICROBIAL ACTIVITY; MUTATION; VACCINATION;

ADULT; AGE DISTRIBUTION; ANTIMALARIAL DRUG RESISTANCE; ARTICLE; CROSS-SECTIONAL STUDY; DRUG USE; FEMALE; GAMETOCYTE; GENE; GENE MUTATION; HELP SEEKING BEHAVIOR; HUMAN; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MALE; MICROBIOLOGICAL PARAMETERS; MUTANT; NONHUMAN; PARASITE DENSITY; PATIENT ATTITUDE; PFCRT GENE; PLASMODIUM FALCIPARUM; YEMEN;

AL HUDAYDAH; YEMEN;

PLASMODIUM FALCIPARUM;

CHLOROQUINE; DRUG RESISTANCE; HODEIDAH; PFCRT; PLASMODIUM FALCIPARUM; TREATMENT-SEEKING BEHAVIOR;

ADOLESCENT; ADULT; ANTIMALARIALS; CHILD; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; DRUG RESISTANCE; FEMALE; GENE FREQUENCY; HUMANS; MALARIA, FALCIPARUM; MALE; MEMBRANE TRANSPORT PROTEINS; MUTANT PROTEINS; PATIENT ACCEPTANCE OF HEALTH CARE; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; YEMEN; YOUNG ADULT;

EID: 84892518420     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2013.07.010     Document Type: Article

References (57)

1. Al-Kabsi A.M., Al-Shamahy H.A., Al-Harazy A.H., Harmal N.S. The therapeutic efficacy of sulfadoxine/pyrimethamine against Plasmodium falciparum in Yemen. Medical Principles and Practice 2009, 18:62-66.
2. Abdul-Ghani R., Farag H.F., Allam A.F. Sulfadoxine-pyrimethamine resistance in Plasmodium falciparum: a zoomed image at the molecular level within a geographic context. Acta Tropica 2013, 125:163-190.
3. Al-Maktari M.T., Bassiouny H.K. Malaria status in Al-Hodeidah Governorate, Republic of Yemen. Part II: Human factors causing the persistence of chloroquine resistant P. falciparum local strain. Journal of the Egyptian Society of Parasitology 2003, 33:829-839.
4. Al-Maktari M.T., Bassiouny H.K., Al-Hamd Z.S., Assabri A.M., El-Massry A.G., Shatat H.Z. Malaria status in Al-Hodeidah Governorate, Yemen: malariometric parasitic survey & chloroquine resistance P. falciparum local strain. Journal of the Egyptian Society of Parasitology 2003, 33:361-372.
5. Al-Mekhlafi A.M., Fong M.Y., Azazy A.A., Mahdy M.A. Study on the prevalence of malaria among patients with fever in Hodiedah Province, Yemen. 45th Annual Scientific Seminar of the Malaysian Society of Parasitology and Tropical Medicine 2009, 55.
6. Al-Mekhlafi A.M., Mahdy M.A., Al-Mekhlafi H.M., Azazy A.A., Fong M.Y. High frequency of Plasmodium falciparum chloroquine resistance marker (pfcrt T76 mutation) in Yemen: an urgent need to re-examine malaria drug policy. Parasites & Vectors 2011, 4:94.
7. Al-Shamahy H., Al-Harazy A.H., Harmal N.S., Al-Kabsi A.M. The prevalence and degree of resistance of Plasmodium falciparum to first-line antimalarial drugs: an in vitro study from a malaria endemic region in Yemen. Annals of Saudi Medicine 2007, 27:432-436.
8. Ali E., Mackinnon M.J., Abdel-Muhsin A.M., Ahmed S., Walliker D., Babiker H.A. Increased density but not prevalence of gametocytes following drug treatment of Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 2006, 100:176-183.
9. Banjara M.R., Imwong M., Petmitr S., Sirawaraporn W., Joshi A.B., Chavalitshewinkoon-Petmitr P. Factors associated with regional bias of pfcrt (Plasmodium falciparum chloroquine resistance transporter) haplotypes in Nepal. Southeast Asian Journal of Tropical Medicine and Public Health 2011, 42:1-8.
10. Bloland P.B., Kachur S.P., Williams H.A. Trends in antimalarial drug deployment in sub-Saharan Africa. Journal of Experimental Biology 2003, 206:3761-3769.
11. Bousema T., Roeffen W., Meijerink H., Mwerinde H., Mwakalinga S., van Gemert G.J., van de Vegte-Bolmer M., Mosha F., Targett G., Riley E.M., Sauerwein R., Drakeley C. The dynamics of naturally acquired immune responses to Plasmodium falciparum sexual stage antigens Pfs230 & Pfs48/45 in a low endemic area in Tanzania. PLoS ONE 2010, 5:e14114.
12. Buabeng K., Duwiejua M., Dodoo A., Matowe L., Enlund H. Self-reported use of anti-malarial drugs and health facility management of malaria in Ghana. Malaria Journal 2007, 6:85.
13. Carrara V.I., Zwang J., Ashley E.A., Price R.N., Stepniewska K., Barends M., Brockman A., Anderson T., Mcgready R., Phaiphun L., Proux S., van Vugt M., Hutagalung R., Lwin K.M., Phyo A.P., Preechapornkul P., Imwong M., Pukrittayakamee S., Singhasivanon P., White N.J., Nosten F. Changes in the treatment responses to artesunate-mefloquine on the northwestern border of Thailand during 13 years of continuous deployment. PLoS ONE 2009, 4:e4551.
14. Cheesbrough M. District Laboratory Practice in Tropical Countries: Part 1 2005, Cambridge University Press, London.
15. Cooper R.A., Hartwig C.L., Ferdig M.T. Pfcrt is more than the Plasmodium falciparum chloroquine resistance gene: a functional and evolutionary perspective. Acta Tropica 2005, 94:170-180.
16. Das Sutar S.K., Dhangadamajhi G., Kar S.K., Ranjit M. Molecular monitoring of antimalarial drug resistance among Plasmodium falciparum field isolates from Odisha, India. Acta Tropica 2013, 126:84-87.
17. Djimdé A., Doumbo O.K., Cortese J.F., Kayentao K., Doumbo S., Diourté Y., Coulibaly D., Dicko A., Su X.Z., Nomura T., Fidock D.A., Wellems T.E., Plowe C.V. A molecular marker for chloroquine-resistant falciparum malaria. New England Journal of Medicine 2001, 344:257-263.
18. Djimdé A.A., Doumbo O.K., Traore O., Guindo A.B., Kayentao K., Diourte Y., Niare-Doumbo S. Clearance of drug-resistant parasites as a model for protective immunity in Plasmodium falciparum malaria. American Journal of Tropical Medicine and Hygiene 2003, 69:558-563.
19. Dunyo S., Afari E., Koram K., Ahorlu C., Abubakar I., Nkrumah F. Health centre vs home presumptive diagnosis of malaria in southern Ghana: implications for home-based care policy. Transactions of the Royal Society of Tropical Medicine and Hygiene 2000, 94:285-288.
20. Ecker A., Lehane A.M., Clain J., Fidock D.A. PfCRT and its role in antimalarial drug resistance. Trends in Parasitology 2012, 28:504-514.
21. Ekland E., Fidock D. Advances in understanding the genetic basis of antimalarial drug resistance. Current Opinion in Microbiology 2007, 10:363-370.
22. Fidock D.A., Nomura T., Talley A.K., Cooper R.A., Dzekunov S.M., Ferdig M.T., Ursos L.M., Sidhu A.B., Naudé B., Deitsch K.W., Su X.Z., Wootton J.C., Roepe P.D., Wellems T.E. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Molecular Cell 2000, 6:861-871.
23. Frosch A., Venkatesan M., Laufer M. Patterns of chloroquine use and resistance in sub-Saharan Africa: a systematic review of household survey and molecular data. Malaria Journal 2011, 10:116.
24. Gharbi M., Flegg J., Hubert V., Kendjo E., Metcalf J., Bertaux L., Guerin P., Le Bras J. Longitudinal study assessing the return of chloroquine susceptibility of Plasmodium falciparum in isolates from travellers returning from West and Central Africa, 2000-2011. Malaria Journal 2013, 12:35. Members of the French National Reference Centre for Imported Malaria Study.
25. Greenwood B., Mutabingwa T. Malaria in 2002. Nature 2002, 415:670-672.
26. Hastings I.M., Watkins W.M., White N.J. The evolution of drug-resistant malaria: the role of drug elimination half-life. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2002, 357:505-519.
27. Hyde J.E. Drug-resistant malaria. Trends in Parasitology 2005, 21:494-498.
28. Hyde J.E. Drug-resistant malaria - an insight. FEBS Journal 2007, 274:4688-4698.
29. Johnson D.J., Fidock D.A., Mungthin M., Lakshmanan V., Sidhu A.B., Bray P.G., Ward S.A. Evidence for a central role for PfCRT in conferring Plasmodium falciparum resistance to diverse antimalarial agents. Molecular Cell 2004, 15:867-877.
30. Klein E., Smith D., Boni M., Laxminarayan R. Clinically immune hosts as a refuge for drug-sensitive malaria parasites. Malaria Journal 2008, 7:67.
31. 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. Journal of Infectious Diseases 2003, 187:1870-1875.
32. Lakshmanan V., Bray P.G., Verdier-Pinard D., Johnson D.J., Horrocks P., Muhle R.A., Alakpa G.E., Hughes R.H., Ward S.A., Krogstad D.J., Sidhu A.B., Fidock D.A. A critical role for PfCRT K76T in Plasmodium falciparum verapamil-reversible chloroquine resistance. EMBO Journal 2005, 24:2294-2305.
33. Laufer M.K., Thesing P.C., Eddington N.D., Masonga R., Dzinjalamala F.K., Takala S.L., Taylor T.E., Plowe C.V. Return of chloroquine antimalarial efficacy in Malawi. New England Journal of Medicine 2006, 355:1959-1966.
34. Mita T., Kaneko A., Lum J., Bwijo B., Takechi M., Zungu I., Tsukahara T., Tanabe K., Kobayakawa T., Bjorkman A. Recovery of chloroquine sensitivity and low prevalence of the Plasmodium falciparum chloroquine resistance transporter gene mutation K76T following the discontinuance of chloroquine use in Malawi. American Journal of Tropical Medicine and Hygiene 2003, 68:413-415.
35. Modrzynska K.K. The Genetics of Drug Resistance in Malaria - Identification of Genes conferring Chloroquine and Artemisinin Resistance in Rodent Malaria Parasite Plasmodium chabaudi 2010, University of Edinburgh, Edinburgh.
36. Mubjer R., Adeel A., Chance M., Hassan A. Molecular markers of anti-malarial drug resistance in Lahj Governorate, Yemen: baseline data and implications. Malaria Journal 2011, 10:245.
37. Mwai L., Ochong E., Abdirahman A., Kiara S., Ward S., Kokwaro G., Sasi P., Marsh K., Borrmann S., Mackinnon M., Nzila A. Chloroquine resistance before and after its withdrawal in Kenya. Malaria Journal 2009, 8:106.
38. NMCP Yemen's national malaria control and elimination strategic plan (2011-2015) 2010, Yemeni National Malaria Control Program/Ministry of Public Health and Population, Sana'a.
39. Norahmad N.A., Abdullah N.R., Yaccob N., Jelip J., Dony J.F., Ruslan K.F., Sulaiman L.H., Sidek H.M., Noedl H., Ismail Z. High prevalence of pfcrt K76T mutants among Plasmodium falciparum isolates from Sabah, Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 2011, 42:1322-1326.
40. Ord R., Alexander N., Dunyo S., Hallett R., Jawara M., Targett G., Drakeley C.J., Sutherland C.J. Seasonal carriage of pfcrt and pfmdr1 alleles in Gambian Plasmodium falciparum imply reduced fitness of chloroquine-resistant parasites. Journal of Infectious Diseases 2007, 196:1613-1619.
41. Osman M.E., Mockenhaupt F.P., Bienzle U., Elbashir M.I., Giha H.A. 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. Infection, Genetics and Evolution 2007, 7:52-59.
42. Oster N., Rohrbach P., Sanchez C.P., Andrews K.T., Kammer J., Coulibaly B., Stieglbauer G., Becher H., Lanzer M. Apparent bias for P. falciparum parasites carrying the wild-type pfcrt allele in the placenta. Parasitology Research 2010, 106:1065-1670.
43. Plowe C.V., Cortese J.F., Djimde A., Nwanyanwu O.C., Watkins W.M., Winstanley P.A., Estrada-Franco J.G., Mollinedo R.E., Avila J.C., Cespedes J.L., Carter D., Doumbo O.K. Mutations in Plasmodium falciparum dihydrofolate reductase and dihydropteroate synthase and epidemiologic patterns of pyrimethamine-sulfadoxine use and resistance. Journal of Infectious Diseases 1997, 176:1590-1596.
44. Robert V., Molez J.F., Trape J.F. Short report: gametocytes, chloroquine pressure, and the relative parasite survival advantage of resistant strains of falciparum malaria in West Africa. American Journal of Tropical Medicine and Hygiene 1996, 55:350-351.
45. Sisowath C., Petersen I., Veiga M., Martensson A., Premji Z., Bjorkman A., Fidock D., Gil J. In vivo selection of Plasmodium falciparum parasites carrying the chloroquine-susceptible pfcrt K76 allele after treatment with artemether-lumefantrine in Africa. Journal of Infectious Diseases 2009, 199:750-757.
46. Sutherland C.J., Alloueche A., Curtis J., Drakeley C.J., Ord R., Duraisingh M., Greenwood B.M. Gambian children successfully treated with chloroquine can harbor and transmit Plasmodium falciparum gametocytes carrying resistance genes. American Journal of Tropical Medicine and Hygiene 2002, 67:578-585.
47. Tagelsir N., Ibrahim Z., Medani A., Salih O., Hamad A., Giha H., El-Agib A., Khan B., Saeed N., Ibrahim M. High frequency of Plasmodium falciparum PfCRT K76T and Pfpgh N86Y in patients clearing infection after chloroquine treatment in the Sudan. Acta Tropica 2006, 97:19-25.
48. Ursing J., Kofoed P.E., Rodrigues A., Rombo L. No seasonal accumulation of resistant P. falciparum when high-dose chloroquine is used. PLoS ONE 2009, 4:e6866.
49. Ursing J., Schmidt B.A., Lebbad M., Kofoed P.E., Dias F., Gil J.P., Rombo L. Chloroquine resistant P. falciparum prevalence is low and unchanged between 1990 and 2005 in Guinea-Bissau: an effect of high chloroquine dosageα. Infection, Genetics and Evolution 2007, 7:555-561.
50. Vafa M., Troye-Blomberg M., Anchang J., Garcia A., Migot-Nabias F. Multiplicity of Plasmodium falciparum infection in asymptomatic children in Senegal: relation to transmission, age and erythrocyte variants. Malaria Journal 2008, 7:17.
51. Valderramos S.G., Fidock D.A. Transporters involved in resistance to antimalarial drugs. Trends in Pharmacological Sciences 2006, 27:594-601.
52. Wang X., Mu J., Li G., Chen P., Guo X., Fu L., Chen L., Su X., Wellems T.E. Decreased prevalence of the Plasmodium falciparum chloroquine resistance transporter 76T marker associated with cessation of chloroquine use against P. falciparum malaria in Hainan, People's Republic of China. American Journal of Tropical Medicine and Hygiene 2005, 72:410-414.
53. Watsierah C., Jura W., Raballah E., Kaseje D., Abong'o B., Ouma C. Knowledge and behaviour as determinants of anti-malarial drug use in a peri-urban population from malaria holoendemic region of western Kenya. Malaria Journal 2011, 10:99.
54. WHO World Malaria Report 2010 2012, World Health Organization, Geneva.
55. Wongsrichanalai C., Meshnick S.R. Declining artesunate-mefloquine efficacy against falciparum malaria on the Cambodia-Thailand border. Emerging Infectious Diseases 2008, 14:716-719.
56. Wongsrichanalai C., Pickard A.L., Wernsdorfer W.H., Meshnick S.R. Epidemiology of drug-resistant malaria. Lancet Infectious Diseases 2002, 2:209-218.
57. Wurtz N., Fall B., Pascual A., Diawara S., Sow K., Baret E., Diatta B., Fall K., Mbaye P., 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. Malaria Journal 2012, 11:197.