Chloroquine efficacy studies confirm drug susceptibility of Plasmodium vivax in Chennai, India

Malaria Journal

Volumn 13, Issue 1, 2014, Pages

  Shalini, Sneh ^a   Chaudhuri, Saumyadripta ^a   Sutton, Patrick L ^b   Mishra, Neelima ^a   Srivastava, Nalini ^c   David, Joseph K ^a   Ravindran, K John ^d   Carlton, Jane M ^b   Eapen, Alex ^d  

^a INDIAN COUNCIL OF MEDICAL RESEARCH   (India)

^b NEW YORK UNIVERSITY   (United States)

^c JIWAJI UNIVERSITY   (India)

^d NATIONAL INSTITUTE OF MALARIA RESEARCH   (India)

Author keywords

Chennai; Chloroquine; Genetic diversity; In vitro; In vivo; Plasmodium vivax

Indexed keywords

CHLOROQUINE; DNA;

ADOLESCENT; ADULT; AGED; ALLELE; ANTIMALARIAL DRUG SUSCEPTIBILITY; ARTICLE; BASE PAIRING; CHROMOSOME; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; GENE LOCUS; GENE SEQUENCE; GENOTYPE; HAPLOTYPE; HUMAN; IC 50; IN VITRO STUDY; IN VIVO STUDY; INDIA; MAJOR CLINICAL STUDY; MALE; MICROBIAL DIVERSITY; MICROBIAL GENOME; NONHUMAN; PLASMODIUM VIVAX; RECURRENT INFECTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; ADULT; AGED; ANTIMALARIALS; CHILD; CHLOROQUINE; DRUG RESISTANCE; FEMALE; HUMANS; INDIA; MALARIA, VIVAX; MALE; MIDDLE AGED; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PARASITIC SENSITIVITY TESTS; PLASMODIUM VIVAX; POLYMORPHISM, GENETIC; PROTOZOAN PROTEINS; YOUNG ADULT;

EID: 84898478446     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-13-129     Document Type: Article

References (66)

1. Malaria in India: challenges and opportunities. Dash AP, Valecha N, Anvikar AR, Kumar A, J Biosci 2008 33 583 592 10.1007/s12038-008-0076-x 19208983
2. Resistance to chloroquine by Plasmodium vivax in Irian Jaya, Indonesia. Baird JK, Basri H, Purnomo, Bangs MJ, Subianto B, Patchen LC, Hoffman SL, Am J Trop Med Hyg 1991 44 547 552 1676566
3. Chloroquine-resistant Plasmodium vivax from Indonesia. Schwartz IK, Lackritz EM, Patchen LC, N Engl J Med 1991 324 927
4. Plasmodium vivax resistance to chloroquine? Rieckmann KH, Davis DR, Hutton DC, Lancet 1989 2 1183 1184 2572903 (Pubitemid 19275451)
5. Plasmodium vivax resistance to chloroquine (R2) and mefloquine (R3) in Brazilian Amazon region. Alecrim MG, Alecrim W, Macedo V, Rev Soc Bras Med Trop 1999 32 67 68 9927829 (Pubitemid 29006271)
6. Failure of combined chloroquine and high-dose primaquine therapy for Plasmodium vivax malaria acquired in Guyana, South America. Phillips EJ, Keystone JS, Kain KC, Clin Infect Dis 1996 23 1171 1173 10.1093/clinids/23.5. 1171 8922821 (Pubitemid 126782788)
7. Plasmodium vivax clinically resistant to chloroquine in Colombia. Soto J, Toledo J, Gutierrez P, Luzz M, Llinas N, Cedeno N, Dunne M, Berman J, Am J Trop Med Hyg 2001 65 90 93 11508397 (Pubitemid 32744210)
8. Comparison of chloroquine, sulfadoxine/pyrimethamine, mefloquine and mefloquine-artesunate for the treatment of falciparum malaria in Kachin State, North Myanmar. Smithuis F, Shahmanesh M, Kyaw MK, Savran O, Lwin S, White NJ, Trop Med Int Health 2004 9 1184 1190 10.1111/j.1365-3156.2004.01323.x 15548314 (Pubitemid 39573990)
9. Chloroquine resistant Plasmodium vivax malaria in India. Dua VK, Kar PK, Sharma VP, Trop Med Int Health 1996 1 816 819 8980595 (Pubitemid 27010563)
10. Vivax malaria resistant to chloroquine: case reports from Bombay. Garg M, Gopinathan N, Bodhe P, Kshirsagar NA, Trans R Soc Trop Med Hyg 1995 89 656 657 10.1016/0035-9203(95)90432-8 8594687 (Pubitemid 26016354)
11. An unusual case of multidrug-resistant Plasmodium vivax malaria in Mumbai (Bombay), India. Kshirsagar NA, Gogtay NJ, Rajgor D, Dalvi SS, Wakde M, Ann Trop Med Parasitol 2000 94 189 190 10.1080/00034980057536 10827874 (Pubitemid 30209445)
12. Monitoring the chloroquine sensitivity of Plasmodium vivax from Calcutta and Orissa, India. Nandy A, Addy M, Maji AK, Bandyopadhyay AK, Ann Trop Med Parasitol 2003 97 215 220 10.1179/000349803235001868 12803853 (Pubitemid 36606354)
13. Emergence of chloroquine-resistant vivax malaria in south Bihar (India). Singh RK, Trans R Soc Trop Med Hyg 2000 94 327 10.1016/S0035-9203(00)90344-4 10975013 (Pubitemid 30406572)
14. Pfcrt haplotypes and the evolutionary history of chloroquine-resistant Plasmodium falciparum. Awasthi G, Satya Prasad GB, Das A, Mem Inst Oswaldo Cruz 2012 107 129 134 10.1590/S0074-02762012000100018 22310546
15. Battling the malaria iceberg with chloroquine in India. Sharma VP, Malar J 2007 6 105 10.1186/1475-2875-6-105 17683630 (Pubitemid 47507061)
16. Resistance to chloroquine in falciparum malaria in Assam state, India. Sehgal PN SM, Sharma SL, Gogai S, J Commun Dis 1973 5 175 180
17. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Fidock DA, Nomura T, Talley AK, Cooper RA, Dzekunov SM, Ferdig MT, Ursos LM, Sidhu AB, Naude B, Deitsch KW, Su XZ, Wootton JC, Roepe PD, Wellems TE, Mol Cell 2000 6 861 871 10.1016/S1097-2765(05)00077-8 11090624
18. Amplification of the multidrug resistance gene in some chloroquine-resistant isolates of P. falciparum. Foote SJ, Thompson JK, Cowman AF, Kemp DJ, Cell 1989 57 921 930 10.1016/0092-8674(89)90330-9 2701941 (Pubitemid 19168372)
19. High-level chloroquine resistance in Sudanese isolates of Plasmodium falciparum is associated with mutations in the chloroquine resistance transporter gene pfcrt and the multidrug resistance gene pfmdr1. Babiker HA, Pringle SJ, Abdel-Muhsin A, Mackinnon M, Hunt P, Walliker D, J Infect Dis 2001 183 1535 1538 10.1086/320195 11319692 (Pubitemid 32417707)
20. Sequence polymorphisms in pfcrt are strongly associated with chloroquine resistance in Plasmodium falciparum. Chen N, Russell B, Staley J, Kotecka B, Nasveld P, Cheng Q, J Infect Dis 2001 183 1543 1545 11319698 (Pubitemid 32417711)
21. A molecular marker for chloroquine-resistant falciparum malaria. Djimde A, Doumbo OK, Cortese JF, Kayentao K, Doumbo S, Diourte Y, Coulibaly D, Dicko A, Su XZ, Nomura T, Fidock DA, Wellems TE, Plowe CV, N Engl J Med 2001 344 257 263 10.1056/NEJM200101253440403 11172152 (Pubitemid 32108530)
22. Polymorphisms in the Plasmodium falciparum pfcrt and pfmdr-1 genes and clinical response to chloroquine in Kampala, Uganda. Dorsey G, Kamya MR, Singh A, Rosenthal PJ, J Infect Dis 2001 183 1417 1420 10.1086/319865 11294677 (Pubitemid 32337128)
23. Prevalence of the K76T mutation in the putative Plasmodium falciparum chloroquine resistance transporter (pfcrt) gene and its relation to chloroquine resistance in Mozambique. Mayor AG, Gomez-Olive X, Aponte JJ, Casimiro S, Mabunda S, Dgedge M, Barreto A, Alonso PL, J Infect Dis 2001 183 1413 1416 10.1086/319856 11294676 (Pubitemid 32337127)
24. Evidence for different mechanisms of chloroquine resistance in 2 plasmodium species that cause human malaria. Nomura T, Carlton JM, Baird JK, del Portillo HA, Fryauff DJ, Rathore D, Fidock DA, Su X, Collins WE, McCutchan TF, Wootton JC, Wellems TE, J Infect Dis 2001 183 1653 1661 10.1086/320707 11343215 (Pubitemid 32466704)
25. Real-time PCR for dihydrofolate reductase gene single-nucleotide polymorphisms in Plasmodium vivax isolates. Brega S, de Monbrison F, Severini C, Udomsangpetch R, Sutanto I, Ruckert P, Peyron F, Picot S, Antimicrob Agents Chemother 2004 48 2581 2587 10.1128/AAC.48.7.2581-2587.2004 15215112 (Pubitemid 38823428)
26. Plasmodium vivax resistance to chloroquine in Madagascar: clinical efficacy and polymorphisms in pvmdr1 and pvcrt-o genes. Barnadas C, Ratsimbasoa A, Tichit M, Bouchier C, Jahevitra M, Picot S, Menard D, Antimicrob Agents Chemother 2008 52 4233 4240 10.1128/AAC.00578-08 18809933
27. Identification of the Plasmodium vivax mdr-like gene (pvmdr1) and analysis of single-nucleotide polymorphisms among isolates from different areas of endemicity. Brega S, Meslin B, de Monbrison F, Severini C, Gradoni L, Udomsangpetch R, Sutanto I, Peyron F, Picot S, J Infect Dis 2005 191 272 277 10.1086/426830 15609238 (Pubitemid 40096386)
28. Characterisation of pvmdr1 and pvdhfr genes associated with chemoresistance in Brazilian Plasmodium vivax isolates. Gama BE, Oliveira NK, Souza JM, Daniel-Ribeiro CT, Ferreira-da-Cruz Mde F, Mem Inst Oswaldo Cruz 2009 104 1009 1011 20027469
29. In vivo therapeutic efficacy of chloroquine alone or in combination with primaquine in vivax malaria in Kolkata, West Bengal, India and polymorphism in pvmdr1 and pvcrt-0 genes. Ganguly S, Saha P, Guha SK, Das S, Bera DK, Biswas A, Kundu PK, Saha B, Ray K, Maji AK, Antimicrob Agents Chemother 2012 57 1246 1251 23262997
30. In vitro anti-malarial drug susceptibility of temperate Plasmodium vivax from central China. Lu F, Gao Q, Chotivanich K, Xia H, Cao J, Udomsangpetch R, Cui L, Sattabongkot J, Am J Trop Med Hyg 2011 85 197 201 10.4269/ajtmh.2011.10- 0070 21813834
31. Genetic analysis of Plasmodium falciparum infections on the north-western border of Thailand. Paul RE, Brockman A, Price RN, Luxemburger C, White NJ, Looareesuwan S, Nosten F, Day KP, Trans R Soc Trop Med Hyg 1999 93 587 593 10.1016/S0035-9203(99)90057-3 10717738 (Pubitemid 30015777)
32. Molecular surveillance of drug-resistant Plasmodium vivax using pvdhfr, pvdhps and pvmdr1 markers in Nouakchott, Mauritania. Mint Lekweiry K, Ould Mohamed Salem Boukhary A, Gaillard T, Wurtz N, Bogreau H, Hafid JE, Trape JF, Bouchiba H, Ould Ahmedou Salem MS, Pradines B, Rogier C, Basco LK, Briolant S, J Antimicrob Chemother 2012 67 367 374 10.1093/jac/dkr464 22086859
33. In vitro activity of pyronaridine against multidrug-resistant Plasmodium falciparum and Plasmodium vivax. Price RN, Marfurt J, Chalfein F, Kenangalem E, Piera KA, Tjitra E, Anstey NM, Russell B, Antimicrob Agents Chemother 2010 54 5146 5150 10.1128/AAC.00801-10 20876370
34. Amplification of pvmdr1 associated with multidrug-resistant Plasmodium vivax. Suwanarusk R, Chavchich M, Russell B, Jaidee A, Chalfein F, Barends M, Prasetyorini B, Kenangalem E, Piera KA, Lek-Uthai U, Anstey NM, Tjitra E, Nosten F, Cheng Q, Price RN, J Infect Dis 2008 198 1558 1564 10.1086/592451 18808339
35. Chloroquine resistant Plasmodium vivax: in vitro characterisation and association with molecular polymorphisms. Suwanarusk R, Russell B, Chavchich M, Chalfein F, Kenangalem E, Kosaisavee V, Prasetyorini B, Piera KA, Barends M, Brockman A, Lek-Uthai U, Anstey NM, Tjitra E, Nosten F, Cheng Q, Price RN, PLoS One 2007 2 1089 10.1371/journal.pone.0001089 17971853 (Pubitemid 351566688)
36. In vitro chloroquine resistance for Plasmodium vivax isolates from the Western Brazilian Amazon. Chehuan YF, Costa MR, Costa JS, Alecrim MG, Nogueira F, Silveira H, Brasil LW, Melo GC, Monteiro WM, Lacerda MV, Malar J 2013 12 226 10.1186/1475-2875-12-226 23819884
37. Genetic polymorphism in pvmdr1 and pvcrt-o genes in relation to in vitro drug susceptibility of Plasmodium vivax isolates from malaria-endemic countries. Lu F, Lim CS, Nam DH, Kim K, Lin K, Kim TS, Lee HW, Chen JH, Wang Y, Sattabongkot J, Han ET, Acta Trop 2011 117 69 75 10.1016/j.actatropica.2010.08. 011 20933490
38. Mutant pfcrt "SVMNT" haplotype and wild type pfmdr1 "N86" are endemic in Plasmodium vivax dominated areas of India under high chloroquine exposure. Mallick PK, Joshi H, Valecha N, Sharma SK, Eapen A, Bhatt RM, Srivastava HC, Sutton PL, Dash AP, Bhasin VK, Malar J 2012 11 16 10.1186/1475-2875-11-16 22236376
39. Genetic hitchhiking under heterogeneous spatial selection pressures. Schneider KA, Kim Y, PLoS One 2013 8 61742 10.1371/journal.pone.0061742 23637897
40. Approximations for the hitchhiking effect caused by the evolution of antimalarial-drug resistance. Schneider KA, Kim Y, J Math Biol 2011 62 789 832 10.1007/s00285-010-0353-9 20623287
41. An analytical model for genetic hitchhiking in the evolution of antimalarial drug resistance. Schneider KA, Kim Y, Theor Popul Biol 2010 78 93 108 10.1016/j.tpb.2010.06.005 20600206
42. Plasmodium vivax: paroxysm-associated lipids mediate leukocyte aggregation. Karunaweera N, Wanasekara D, Chandrasekharan V, Mendis K, Carter R, Malar J 2007 6 62 10.1186/1475-2875-6-62 17517147 (Pubitemid 46917331)
43. Effective and cheap removal of leukocytes and platelets from Plasmodium vivax infected blood. Sriprawat K, Kaewpongsri S, Suwanarusk R, Leimanis ML, Lek-Uthai U, Phyo AP, Snounou G, Russell B, Renia L, Nosten F, Malar J 2009 8 115 10.1186/1475-2875-8-115 19490618
44. Determinants of in vitro drug susceptibility testing of Plasmodium vivax. Russell B, Chalfein F, Prasetyorini B, Kenangalem E, Piera K, Suwanarusk R, Brockman A, Prayoga P, Sugiarto P, Cheng Q, Tjitra E, Anstey NM, Price RN, Antimicrob Agents Chemother 2008 52 1040 1045 10.1128/AAC.01334-07 18180357 (Pubitemid 351358386)
45. Simple in vitro assay for determining the sensitivity of Plasmodium vivax isolates from fresh human blood to antimalarials in areas where P. vivax is endemic. Russell BM, Udomsangpetch R, Rieckmann KH, Kotecka BM, Coleman RE, Sattabongkot J, Antimicrob Agents Chemother 2003 47 170 173 10.1128/AAC.47.1. 170-173.2003 12499187 (Pubitemid 36070360)
46. Alternative polymerase chain reaction method to identify Plasmodium species in human blood samples: the semi-nested multiplex malaria PCR (SnM-PCR). Rubio JM, Post RJ, van Leeuwen WM, Henry MC, Lindergard G, Hommel M, Trans R Soc Trop Med Hyg 2002 96 Suppl 1 199 204 12055839
47. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Gouy M, Guindon S, Gascuel O, Mol Biol Evol 2010 27 221 224 10.1093/molbev/msp259 19854763
48. A call to arms: on refining Plasmodium vivax microsatellite marker panels for comparing global diversity. Sutton PL, Malar J 2013 12 447 10.1186/1475-2875-12-447 24330329
49. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP, Mol Biol Evol 2000 17 1467 1482 10.1093/oxfordjournals.molbev.a026247 11018154
50. Maximum-likelihood estimation of molecular haplotype frequencies in a diploid population. Excoffier L, Slatkin M, Mol Biol Evol 1995 12 921 927 7476138
51. Rice JA, Mathematical statistics and data analysis Belmont, CA: Duxburry Press 2 1995
52. Primaquine therapy for malaria. Baird JK, Hoffman SL, Clin Infect Dis 2004 39 1336 1345 10.1086/424663 15494911 (Pubitemid 39458520)
53. Kitchen SF, Malariology London: W B Saunders 1939
54. Studies on the Plasmodium vivax relapse pattern in Delhi, India. Adak T, Sharma VP, Orlov VS, Am J Trop Med Hyg 1998 59 175 179 9684649 (Pubitemid 28304818)
55. Plasmodium vivax polymorphism in a clinical drug trial. Adak T, Valecha N, Sharma VP, Clin Diagn Lab Immunol 2001 8 891 894 11527798 (Pubitemid 32868302)
56. Relapse pattern of Plasmodium vivax in Mumbai: a study of 283 cases of vivax malaria. Gogtay NJ, Desai S, Kadam VS, Kamtekar KD, Dalvi SS, Kshirsagar NA, J Assoc Physicians India 2000 48 1085 1086 11310387
57. Efficacy of a 14-day primaquine regimen in preventing relapses in patients with Plasmodium vivax malaria in Mumbai, India. Rajgor DD, Gogtay NJ, Kadam VS, Kamtekar KD, Dalvi SS, Chogle AR, Aigal U, Bichile LS, Kain KC, Kshirsagar NA, Trans R Soc Trop Med Hyg 2003 97 438 440 10.1016/S0035-9203(03) 90082-4 15259476 (Pubitemid 39186028)
58. Determinants of relapse periodicity in Plasmodium vivax malaria. White NJ, Malar J 2011 10 297 10.1186/1475-2875-10-297 21989376
59. WHO, World malaria report 2011 Geneva: World Health Organization http://www.who.int/malaria/world-malaria-report-2011/9789241564403-eng.pdf
60. Malaria in India: the center for the study of complex malaria in India. Das A, Anvikar AR, Cator LJ, Dhiman RC, Eapen A, Mishra N, Nagpal BN, Nanda N, Raghavendra K, Read AF, Sharma SK, Singh OP, Singh V, Sinnis P, Srivastava HC, Sullivan SA, Sutton PL, Thomas MB, Carlton JM, Valecha N, Acta Trop 2012 121 267 273 10.1016/j.actatropica.2011.11.008 22142788
61. Improved assessment of Plasmodium vivax response to antimalarial drugs by a colorimetric double-site plasmodium lactate dehydrogenase antigen capture enzyme-linked immunosorbent assay. Druilhe P, Brasseur P, Blanc C, Makler M, Antimicrob Agents Chemother 2007 51 2112 2116 10.1128/AAC.01385-06 17387158 (Pubitemid 46903102)
62. Gene amplification of the multidrug resistance 1 gene of Plasmodium vivax isolates from Thailand, Laos, and Myanmar. Imwong M, Pukrittayakamee S, Pongtavornpinyo W, Nakeesathit S, Nair S, Newton P, Nosten F, Anderson TJ, Dondorp A, Day NP, White NJ, Antimicrob Agents Chemother 2008 52 2657 2659 10.1128/AAC.01459-07 18443118 (Pubitemid 351915703)
63. Prevalence of molecular markers of anti-malarial drug resistance in Plasmodium vivax and Plasmodium falciparum in two districts of Nepal. Ranjitkar S, Schousboe ML, Thomsen TT, Adhikari M, Kapel CM, Bygbjerg IC, Alifrangis M, Malar J 2011 10 75 10.1186/1475-2875-10-75 21457533
64. Analysis of single-nucleotide polymorphisms in the crt-o and mdr1 genes of Plasmodium vivax among chloroquine-resistant isolates from the Brazilian Amazon region. Orjuela-Sanchez P, de Santana Filho FS, Machado-Lima A, Chehuan YF, Costa MR, Alecrim M, del Portillo HA, Antimicrob Agents Chemother 2009 53 3561 3564 10.1128/AAC.00004-09 19451296
65. Absence of nucleotide polymorphism in a Plasmodium vivax multidrug resistance gene after failure of mefloquine prophylaxis in French Guyana. Picot S, Brega S, Gerome P, Velut G, de Monbrison F, Cheminel V, Peyron F, Trans R Soc Trop Med Hyg 2005 99 234 237 10.1016/j.trstmh.2004.09.007 15653127 (Pubitemid 40104024)
66. Plasmodium vivax: allele variants of the mdr1 gene do not associate with chloroquine resistance among isolates from Brazil, Papua, and monkey-adapted strains. Sa JM, Nomura T, Neves J, Baird JK, Wellems TE, del Portillo HA, Exp Parasitol 2005 109 256 259 10.1016/j.exppara.2004.12.005 15755424 (Pubitemid 40332326)