Safety and Reproducibility of a Clinical Trial System Using Induced Blood Stage Plasmodium vivax Infection and Its Potential as a Model to Evaluate Malaria Transmission

PLoS Neglected Tropical Diseases

Volumn 10, Issue 12, 2016, Pages

  Griffin, Paul ^a,b,c,d   Pasay, Cielo ^a   Elliott, Suzanne ^b   Sekuloski, Silvana ^a   Sikulu, Maggy ^a   Hugo, Leon ^a   Khoury, David ^e   Cromer, Deborah ^e   Davenport, Miles ^e   Sattabongkot, Jetsumon ^f   Ivinson, Karen ^g   Ockenhouse, Christian ^g   McCarthy, James ^a,d  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b Q Pharm Pty Ltd   (Australia)

^c MATER MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

^f MAHIDOL UNIVERSITY   (Thailand)

^g Malaria Vaccine Initiative ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALUMINUM HYDROXIDE; ASPARTATE AMINOTRANSFERASE; CREATINE KINASE; INFUSION FLUID; LACTATE DEHYDROGENASE; MAGNESIUM HYDROXIDE; MESSENGER RNA; METOCLOPRAMIDE; ONDANSETRON; PARACETAMOL; RANITIDINE; SIMETHICONE;

ADULT; ANIMAL EXPERIMENT; ANOPHELES STEPHENSI; ARTICLE; CLINICAL OUTCOME; CONTROLLED STUDY; DISEASE MODEL; FEMALE; FEVER; HEADACHE; HEARTBURN; HISTOLOGY; HUMAN; HUMAN EXPERIMENT; INDUCED BLOOD STAGE MALARIA; INOCULATION; LIVER FUNCTION TEST; MALE; NAUSEA; NONHUMAN; NORMAL HUMAN; PARASITE MULTIPLICATION; PARASITE PHENOMENA AND FUNCTIONS; PARASITE TRANSMISSION; PHASE 1 CLINICAL TRIAL; PLASMODIUM VIVAX MALARIA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK ASSESSMENT; SINGLE DRUG DOSE; ANIMAL; ANOPHELES; CLINICAL TRIAL; ERYTHROCYTE; MALARIA, VIVAX; MOSQUITO VECTOR; OOCYST; PARASITEMIA; PARASITOLOGY; PHYSIOLOGY; REPRODUCIBILITY; TRANSMISSION;

ANIMALS; ANOPHELES; DISEASE MODELS, ANIMAL; ERYTHROCYTES; HEALTHY VOLUNTEERS; HUMAN EXPERIMENTATION; HUMANS; MALARIA, VIVAX; MOSQUITO VECTORS; OOCYSTS; PARASITEMIA; REPRODUCIBILITY OF RESULTS;

EID: 85008625475     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0005139     Document Type: Article

References (66)

1. Burrows JN, Burlot E, Campo B, Cherbuin S, Jeanneret S, Leroy D, et al. Antimalarial drug discovery—the path towards eradication. Parasitology. 2014; 141: 128–139. doi: 10.1017/S003118201300082623863111
2. Held J, Kreidenweiss A, Mordmuller B, Novel approaches in antimalarial drug discovery. Expert Opin Drug Discov. 2013; 8: 1325–1337. doi: 10.1517/17460441.2013.84352224090219
3. Abdul-Ghani R, Beier JC, Strategic use of antimalarial drugs that block falciparum malaria parasite transmission to mosquitoes to achieve local malaria elimination. Parasitol Res. 2014; 113: 3535–3546. doi: 10.1007/s00436-014-4091-625185662
4. Chulay JD, Schneider I, Cosgriff TM, Hoffman SL, Ballou WR, Quakyi IA, et al. Malaria transmitted to humans by mosquitoes infected from cultured Plasmodium falciparum. Am J Trop Med Hyg. 1986; 35: 66–68. 3511753
5. Church LW, Le TP, Bryan JP, Gordon DM, Edelman R, Fries L, et al. Clinical manifestations of Plasmodium falciparum malaria experimentally induced by mosquito challenge. J Infect Dis. 1997; 175: 915–920. 9086149
6. Epstein JE, Rao S, Williams F, Freilich D, Luke T, Sedegah M, et al. Safety and clinical outcome of experimental challenge of human volunteers with Plasmodium falciparum-infected mosquitoes: an update. J Infect Dis. 2007; 196: 145–154. doi: 10.1086/51851017538895
7. Lyke KE, Laurens M, Adams M, Billingsley PF, Richman A, Loyevsky M, et al. Plasmodium falciparum malaria challenge by the bite of aseptic Anopheles stephensi mosquitoes: results of a randomized infectivity trial. PLoS One. 2010; 5: e13490. doi: 10.1371/journal.pone.001349021042404
8. Laurens MB, Billingsley P, Richman A, Eappen AG, Adams M, Li T, et al. Successful human infection with P. falciparum using three aseptic Anopheles stephensi mosquitoes: a new model for controlled human malaria infection. PLoS One. 2013; 8: e68969. doi: 10.1371/journal.pone.006896923874828
9. Shekalaghe S, Rutaihwa M, Billingsley PF, Chemba M, Daubenberger CA, James ER, et al. Controlled human malaria infection of Tanzanians by intradermal injection of aseptic, purified, cryopreserved Plasmodium falciparum sporozoites. Am J Trop Med Hyg. 2014; 91: 471–480. doi: 10.4269/ajtmh.14-011925070995
10. Roestenberg M, Bijker EM, Sim BK, Billingsley PF, James ER, Bastiaens GJ, et al. Controlled human malaria infections by intradermal injection of cryopreserved Plasmodium falciparum sporozoites. Am J Trop Med Hyg. 2013; 88: 5–13. doi: 10.4269/ajtmh.2012.12-061323149582
11. Sheehy SH, Spencer AJ, Douglas AD, Sim BK, Longley RJ, Edwards NJ, et al. Optimising controlled human malaria infection studies using cryopreserved P. falciparum parasites administered by needle and syringe. PLoS One. 2013; 8: e65960. doi: 10.1371/journal.pone.006596023823332
12. Cheng Q, Lawrence G, Reed C, Stowers A, Ranford-Cartwright L, Creasey A, et al. Measurement of Plasmodium falciparum growth rates in vivo: a test of malaria vaccines. Am J Trop Med Hyg. 1997; 57: 495–500. 9347970
13. McCarthy JS, Sekuloski S, Griffin PM, Elliott S, Douglas N, Peatey C, et al. A pilot randomised trial of induced blood-stage Plasmodium falciparum infections in healthy volunteers for testing efficacy of new antimalarial drugs. PLoS One. 2011; 6: e21914. doi: 10.1371/journal.pone.002191421887214
14. Engwerda CR, Minigo G, Amante FH, McCarthy JS, Experimentally induced blood stage malaria infection as a tool for clinical research. Trends Parasitol. 2012; 28: 515–521. doi: 10.1016/j.pt.2012.09.00123041118
15. Herrera S, Fernandez O, Manzano MR, Murrain B, Vergara J, Blanco P, et al. Successful sporozoite challenge model in human volunteers with Plasmodium vivax strain derived from human donors. Am J Trop Med Hyg. 2009; 81: 740–746. doi: 10.4269/ajtmh.2009.09-019419861603
16. Herrera S, Solarte Y, Jordan-Villegas A, Echavarria JF, Rocha L, Palacios R, et al. Consistent safety and infectivity in sporozoite challenge model of Plasmodium vivax in malaria-naive human volunteers. Am J Trop Med Hyg. 2011; 84: 4–11. doi: 10.4269/ajtmh.2011.09-049821292872
17. Bennett JW, Yadava A, Tosh D, Sattabongkot J, Komisar J, Ware LA, et al. Phase 1/2a Trial of Plasmodium vivax malaria vaccine candidate VMP001/AS01B in malaria-naive adults: safety, immunogenicity, and efficacy. PLoS Negl Trop Dis. 2016; 10: e0004423. doi: 10.1371/journal.pntd.000442326919472
18. Bennett JW, Pybus BS, Yadava A, Tosh D, Sousa JC, McCarthy WF, et al. Primaquine failure and cytochrome P-450 2D6 in Plasmodium vivax malaria. N Engl J Med. 2013; 369: 1381–1382. doi: 10.1056/NEJMc130193624088113
19. McCarthy JS, Griffin PM, Sekuloski S, Bright AT, Rockett R, Looke D, et al. Experimentally induced blood-stage Plasmodium vivax infection in healthy volunteers. J Infect Dis. 2013; 208: 1688–1694. doi: 10.1093/infdis/jit39423908484
20. Bruce-Chwatt LJ, Bruce-Chwatt's essential malariology; 3rd ed.London, UK: Taylor & Francis Ltd.1993.
21. International Conference of Harmonisation (ICH). ICH Harmonised Tripartite Guideline. Clinical safety data management: definitions and standards for expedited reporting E2A. 1994.
22. Ouédraogo AE, Guelbéogo WM, Cohuet A, Morlais I, King JG, Gonçalves BP, et al. A protocol for membrane feeding assays to determine the infectiousness of P. falciparum naturally infected individuals to Anopheles gambiae. MalariaWorld Journal. 2013; 4: 1–4.
23. Knowles R BB, Laboratory studies on the infectivity of Anopheles stephensi. J Mal Inst India. 1943; 5: 1–29.
24. Peters W, Ramkaran AE, The chemotherapy of rodent malaria, XXXII. The influence of p-aminobenzoic acid on the transmission of Plasmodium yoelii and P. berghei by Anopheles stephensi. Ann Trop Med Parasitol. 1980; 74: 275–282. 6994664
25. Collins FH, Mendez MA, Rasmussen MO, Mehaffey PC, Besansky NJ, Finnerty V, A ribosomal RNA gene probe differentiates member species of the Anopheles gambiae complex. Am J Trop Med Hyg. 1987; 37: 37–41. 2886070
26. Lobo ML, Silveira H, Ramos S, Xiao L, Matos O, Characterization of a pathogen related to Vavraia culicis detected in a laboratory colony of Anopheles stephensi. J Eukaryot Microbiol. 2006; 53Suppl 1: S65–67.
27. Moura H, Da Silva JL, Sodre FC, Brasil P, Wallmo K, Wahlquist S, et al. Gram-chromotrope: a new technique that enhances detection of microsporidial spores in clinical samples. J Eukaryot Microbiol. 1996; 43: 94s–95s. 8822884
28. Snounou G, Perignon JL, Malariotherapy—insanity at the service of malariology. Adv Parasitol. 2013; 81: 223–255. doi: 10.1016/B978-0-12-407826-0.00006-023384625
29. Sattabongkot J, Maneechai N, Rosenberg R, Plasmodium vivax: gametocyte infectivity of naturally infected Thai adults. Parasitology. 1991; 102 Pt 1: 27–31.
30. Collins WE, Sullivan JS, Galland GG, Barnwell JW, Nace D, Williams A, et al. Rio Meta strain of Plasmodium vivax in New World monkeys and anopheline mosquitoes. J Parasitol. 2004; 90: 685–688. doi: 10.1645/GE-336115357053
31. Temple R, Hy's law: predicting serious hepatotoxicity. Pharmacoepidemiol Drug Saf. 2006; 15: 241–243. doi: 10.1002/pds.121116552790
32. Reuben A, Hy's law. Hepatology. 2004; 39: 574–578. doi: 10.1002/hep.2008114768020
33. Duncan CJ, Draper SJ, Controlled human blood stage malaria infection: current status and potential applications. Am J Trop Med Hyg. 2012; 86: 561–565. doi: 10.4269/ajtmh.2012.11-050422492136
34. Tangpukdee N, Thanachartwet V, Krudsood S, Luplertlop N, Pornpininworakij K, Chalermrut K, et al. Minor liver profile dysfunctions in Plasmodium vivax, P. malaria and P. ovale patients and normalization after treatment. Korean J Parasitol. 2006; 44: 295–302. doi: 10.3347/kjp.2006.44.4.29517170571
35. Fredricks MG, Hoffbauer FW, A study of hepatic function in therapeutic malaria. Journal of the American Medical Association. 1945; 128: 495–499.
36. Guttman SA, Potter HR, Hanger FM, Moore DB, Pierson PS, Moore DH, Significance of cephalin-cholesterol flocculation test in malarial fever. J Clin Invest. 1945; 24: 296–300. doi: 10.1172/JCI10160616695216
37. Kopp I, Solomon HC, 1943; 205: 90–97.
38. McMahon AEJ, Kelsey JE, Derauf DE, Hepatitis of malarial origin: clinical and pathologic study of fifty-four Korean veterans. AMA Arch Intern Med. 1954; 93: 379–386. 13123562
39. Anand AC, Puri P, Jaundice in malaria. J Gastroenterol Hepatol. 2005; 20: 1322–1332. doi: 10.1111/j.1440-1746.2005.03884.x16105116
40. Jain A, Kaushik R, Kaushik RM, Malarial hepatopathy: Clinical profile and association with other malarial complications. Acta Trop. 2016; 159: 95–105. doi: 10.1016/j.actatropica.2016.03.03127019056
41. Jaiprakash H, Narayana S, Mohanraj J, Drug-induced hepatotoxicity in a tertiary care hospital in rural South India. N Am J Med Sci. 2012; 4: 90–93. doi: 10.4103/1947-2714.9338522408755
42. Kochar DK, Kaswan K, Kochar SK, Sirohi P, Pal M, Kochar A, et al. A comparative study of regression of jaundice in patients of malaria and acute viral hepatitis. J Vector Borne Dis. 2006; 43: 123–129. 17024861
43. Patwari A, Aneja S, Berry AM, Ghosh S, Hepatic dysfunction in childhood malaria. Arch Dis Child. 1979; 54: 139–141. 373643
44. Saya RP, Debabrata G, Saya GK, Malarial hepatopathy and its outcome in India. N Am J Med Sci. 2012; 4: 449–452. doi: 10.4103/1947-2714.10198123112964
45. Whitten R, Milner DA, Jr.Yeh MM, Kamiza S, Molyneux ME, Taylor TE, Liver pathology in Malawian children with fatal encephalopathy. Hum Pathol. 2011; 42: 1230–1239. doi: 10.1016/j.humpath.2010.11.01921396681
46. Deroost K, Lays N, Pham TT, Baci D, Van den Eynde K, Komuta M, et al. Hemozoin induces hepatic inflammation in mice and is differentially associated with liver pathology depending on the Plasmodium strain. PLoS One. 2014; 9: e113519. doi: 10.1371/journal.pone.011351925419977
47. Dey S, Guha M, Alam A, Goyal M, Bindu S, Pal C, et al. Malarial infection develops mitochondrial pathology and mitochondrial oxidative stress to promote hepatocyte apoptosis. Free Radic Biol Med. 2009; 46: 271–281. doi: 10.1016/j.freeradbiomed.2008.10.03219015023
48. Watkins PB, Kaplowitz N, Slattery JT, Colonese CR, Colucci SV, Stewart PW, et al. Aminotransferase elevations in healthy adults receiving 4 grams of acetaminophen daily: a randomized controlled trial. Jama. 2006; 296: 87–93. doi: 10.1001/jama.296.1.8716820551
49. Krishna S, Pukrittayakamee S, Supanaranond W, ter Kuile F, Ruprah M, Sura T, et al. Fever in uncomplicated Plasmodium falciparum malaria: randomized double-'blind' comparison of ibuprofen and paracetamol treatment. Trans R Soc Trop Med Hyg. 1995; 89: 507–509. 8560525
50. Vanderberg JP, Gwadz RW, Kreier JP, The transmisison by mosquitoes of plasmodia in the laboratory. In: Pathology, Vector Studies, and Culture: Academic Press; 1980. pp. 153–234.
51. Collins WE, Jeffery GM, Roberts JM, A retrospective examination of the effect of fever and microgametocyte count on mosquito infection on humans infected with Plasmodium vivax. Am J Trop Med Hyg. 2004; 70: 638–641. 15211005
52. Sattabongkot J, Maneechai N, Phunkitchar V, Eikarat N, Khuntirat B, Sirichaisinthop J, et al. Comparison of artificial membrane feeding with direct skin feeding to estimate the infectiousness of Plasmodium vivax gametocyte carriers to mosquitoes. Am J Trop Med Hyg. 2003; 69: 529–535. 14695091
53. Bousema T, Dinglasan RR, Morlais I, Gouagna LC, van Warmerdam T, Awono-Ambene PH, et al. Mosquito feeding assays to determine the infectiousness of naturally infected Plasmodium falciparum gametocyte carriers. PLoS One. 2012; 7: e42821. doi: 10.1371/journal.pone.004282122936993
54. Diallo M, Toure AM, Traore SF, Niare O, Kassambara L, Konare A, et al. Evaluation and optimization of membrane feeding compared to direct feeding as an assay for infectivity. Malar J. 2008; 7: 248. doi: 10.1186/1475-2875-7-24819055715
55. Mohan BN, Comparative experimental infections in Anopheles fluviatilis and Anopheles stephensi (type) with Plasmodium falciparum welch, 1897. Indian J Malariol. 1955; 9: 81–84. 13262833
56. McCarthy VC, Clyde DF, Comparative efficiency of Anopheles stephensi and Anopheles gambiae as vectors of drug-resistant Plasmodium falciparum from Thailand. Am J Trop Med Hyg. 1974; 23: 313. 4594077
57. Adak T, Singh OP, Das MK, Wattal S, Nanda N, Comparative susceptibility of three important malaria vectors Anopheles stephensi, Anopheles fluviatilis, and Anopheles sundaicus to Plasmodium vivax. J Parasitol. 2005; 91: 79–82. doi: 10.1645/GE-351415856876
58. Graves PM, Studies on the use of a membrane feeding technique for infecting Anopheles gambiae with Plasmodium falciparum. Trans R Soc Trop Med Hyg. 1980; 74: 738–742. 7010696
59. Boudin C, Olivier M, Molez JF, Chiron JP, Ambroise-Thomas P, High human malarial infectivity to laboratory-bred Anopheles gambiae in a village in Burkina Faso. Am J Trop Med Hyg. 1993; 48: 700–706. 8517489
60. Coleman RE, Kumpitak C, Ponlawat A, Maneechai N, Phunkitchar V, Rachapaew N, et al. Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in western Thailand. J Med Entomol. 2004; 41: 201–208. 15061279
61. Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007; 76: 470–474. 17360869
62. Vallejo AF, Garcia J, Amado-Garavito AB, Arevalo-Herrera M, Herrera S, Plasmodium vivax gametocyte infectivity in sub-microscopic infections. Malar J. 2016; 15: 48. doi: 10.1186/s12936-016-1104-126822406
63. Schneider P, Reece SE, van Schaijk BC, Bousema T, Lanke KH, Meaden CS, et al. Quantification of female and male Plasmodium falciparum gametocytes by reverse transcriptase quantitative PCR. Mol Biochem Parasitol. 2015; 199: 29–33. doi: 10.1016/j.molbiopara.2015.03.00625827756
64. Bounkeua V, Li F, Chuquiyauri R, Abeles SR, McClean CM, Neyra V, et al. Lack of molecular correlates of Plasmodium vivax ookinete development. Am J Trop Med Hyg. 2011; 85: 207–213. doi: 10.4269/ajtmh.2011.10-072921813836
65. Chansamut N, Buates S, Takhampunya R, Udomsangpetch R, Bantuchai S, Sattabongkot J, Correlation of Pfg377 ortholog gene expression of Plasmodium vivax and mosquito infection. Trop Med Int Health. 2012; 17: 414–422. doi: 10.1111/j.1365-3156.2011.02940.x22296040
66. Tachibana M, Suwanabun N, Kaneko O, Iriko H, Otsuki H, Sattabongkot J, et al. Plasmodium vivax gametocyte proteins, Pvs48/45 and Pvs47, induce transmission-reducing antibodies by DNA immunization. Vaccine. 2015; 33: 1901–1908. doi: 10.1016/j.vaccine.2015.03.00825765968