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1.
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-
2.
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Hisaeda H, Stowers AW, Tsuboi T, Collins WE, Sattabongkot JS, Suwanabun N, Torii M, Kaslow DC, 2000. Antibodies to malaria vaccine candidates Pvs25 and Pvs28 completely block the ability of Plasmodium vivax to infect mosquitoes. Infect Immun 68: 6618–6623.
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Mirghani HA, Eltahir HG, A-Elgadir TM, Mirghani YA, Elbashir MI, Adam I, 2010. Cytokine profiles in children with severe Plasmodium falciparum malaria in an area of unstable malaria transmission in Central Sudan. J Trop Pediatr 57: 392–395.
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Human Host-Derived Cytokines Associated with Plasmodium vivax Transmission from Acute Malaria Patients to Anopheles darlingi Mosquitoes in the Peruvian Amazon
Shira R. Abeles
Shira R. Abeles
University of California San Diego, San Diego, California; Universidad Peruana Cayetano Heredia, Lima, Peru
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Raul Chuquiyauri
Raul Chuquiyauri
University of California San Diego, San Diego, California; Universidad Peruana Cayetano Heredia, Lima, Peru
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Carlos Tong
Carlos Tong
University of California San Diego, San Diego, California; Universidad Peruana Cayetano Heredia, Lima, Peru
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Joseph M. Vinetz
Joseph M. Vinetz
University of California San Diego, San Diego, California; Universidad Peruana Cayetano Heredia, Lima, Peru
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Infection of mosquitoes by humans is not always successful in the setting of patent gametocytemia. This study tested the hypothesis that pro- or anti-inflammatory cytokines are associated with transmission of Plasmodium vivax to Anopheles darlingi mosquitoes in experimental infection. Blood from adults with acute, non-severe P. vivax malaria was fed to laboratory-reared F1 An. darlingi mosquitoes. A panel of cytokines at the time of mosquito infection was assessed in patient sera and levels compared among subjects who did and did not infect mosquitoes. Overall, blood from 43 of 99 (43%) subjects led to mosquito infection as shown by oocyst counts. Levels of IL-10, IL-6, TNF-α, and IFN-γ were significantly elevated in vivax infection and normalized 3 weeks later. The anti-inflammatory cytokine IL-10 was significantly higher in nontransmitters compared with top transmitters but was not in TNF-α and IFN-γ. The IL-10 elevation during acute malaria was associated with P. vivax transmission blocking.
Author Notes
Financial support: This work was supported by NIH/NIAID grant 1U19AI08968, K24AI068903, and R01AI067727, NIH/Fogarty International Center grant D43TW007120, and the National Institutes of Health Office of the Director, Fogarty International Center, Office of AIDS Research, National Cancer Center, National Eye Institute, National Heart, Blood, and Lung Institute, National Institute of Dental & Craniofacial Research, National Institute On Drug Abuse, National Institute of Mental Health, National Institute of Allergy and Infectious Diseases Health, and NIH Office of Women's Health and Research through the International Clinical Research Scholars and Fellows Program at Vanderbilt University (R24 TW007988), and the American Relief and Recovery Act.
Authors' addresses: Shira R. Abeles, University of California San Diego School of Medicine, La Jolla, CA, E-mail: sabeles@ucsd.edu. Raul Chuquiyauri and Joseph M. Vinetz, University of California San Diego School of Medicine, La Jolla, CA, and Instituto de Medicina Tropical Alexander von Humboldt, Universidad Peruana Cayetano Heredia, San Martin de Porres, Lima, Peru, E-mails: rachuqui@ucsd.edu or raulharo@yahoo.com and jvinetz@ucsd.edu. Carlos Tong, Universidad Peruana Cayetano Heredia Satellite Laboratory, Iquitos, Peru, E-mail: carlostongrios@gmail.com.
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-
1.
Sattabongkot J, Maneechai N, Phunkitchar V, Eikarat N, Khuntirat B, Sirichaisinthop J, Burge R, Coleman RE, 2003. 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 69: 529–535.
-
2.
Bharti AR, Chuquiyauri R, Brouwer KC, Stancil J, Lin J, Llanos-Cuentas A, Vinetz JM, 2006. Experimental infection of the neotropical malaria vector Anopheles darlingi by human patient-derived Plasmodium vivax in the Peruvian Amazon. Am J Trop Med Hyg 75: 610–616.
-
3.
Toure YT, Doumbo O, Toure A, Bagayoko M, Diallo M, Dolo A, Vernick KD, Keister DB, Muratova O, Kaslow DC, 1998. Gametocyte infectivity by direct mosquito feeds in an area of seasonal malaria transmission: implications for Bancoumana, Mali as a transmission-blocking vaccine site. Am J Trop Med Hyg 59: 481–486.
-
4.
Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, Brabin BJ, Gibson FD, Bradley DJ, Alpers MP, 1988. Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua, New Guinea. Parasitology 96: 251–263.
-
5.
Gamage-Mendis AC, Rajakaruna J, Carter R, Mendis KN, 1992. Transmission blocking immunity to human Plasmodium vivax malaria in an endemic population in Kataragama, Sri Lanka. Parasite Immunol 14: 385–396.
-
6.
Roeffen W, Geeraedts F, Eling W, Beckers P, Wizel B, Kumar N, Lensen T, Sauerwein R, 1995. Transmission blockade of Plasmodium falciparum malaria by anti-Pfs230-specific antibodies is isotype dependent. Infect Immun 63: 467–471.
-
7.
Drakeley CJ, Bousema JT, Akim NI, Teelen K, Roeffen W, Lensen AH, Bolmer M, Eling W, Sauerwein RW, 2006. Transmission-reducing immunity is inversely related to age in Plasmodium falciparum gametocyte carriers. Parasite Immunol 28: 185–190.
-
8.
Hisaeda H, Stowers AW, Tsuboi T, Collins WE, Sattabongkot JS, Suwanabun N, Torii M, Kaslow DC, 2000. Antibodies to malaria vaccine candidates Pvs25 and Pvs28 completely block the ability of Plasmodium vivax to infect mosquitoes. Infect Immun 68: 6618–6623.
-
9.
Arevalo-Herrera M, Solarte Y, Rocha L, Alvarez D, Beier JC, Herrera S, 2011. Characterization of Plasmodium vivax transmission-blocking activity in low to moderate malaria transmission settings of the Colombian Pacific coast. Am J Trop Med Hyg 84: 71–77.
-
10.
Mendis KN, Naotunne TD, Karunaweera ND, Del Giudice G, Grau GE, Carter R, 1990. Anti-parasite effects of cytokines in malaria. Immunol Lett 25: 217–220.
-
11.
Walther M, Woodruff J, Edele F, Jeffries D, Tongren JE, King E, Andrews L, Bejon P, Gilbert SC, De Souza JB, Sinden R, Hill AV, Riley EM, 2006. Innate immune responses to human malaria: heterogeneous cytokine responses to blood-stage Plasmodium falciparum correlate with parasitological and clinical outcomes. J Immunol 177: 5736–5745.
-
12.
Zeyrek FY, Kurcer MA, Zeyrek D, Simsek Z, 2006. Parasite density and serum cytokine levels in Plasmodium vivax malaria in Turkey. Parasite Immunol 28: 201–207.
-
13.
Yeom JS, Park SH, Ryu SH, Park HK, Woo SY, Ha EH, Lee BE, Yoo K, Lee JH, Kim KH, Kim S, Kim YA, Ahn SY, Oh S, Park HJ, Min GS, Seoh JY, Park JW, 2003. Serum cytokine profiles in patients with Plasmodium vivax malaria: a comparison between those who presented with and without hepatic dysfunction. Trans R Soc Trop Med Hyg 97: 687–691.
-
14.
Park JW, Park SH, Yeom JS, Huh AJ, Cho YK, Ahn JY, Min GS, Song GY, Kim YA, Ahn SY, Woo SY, Lee BE, Ha EH, Han HS, Yoo K, Seoh JY, 2003. Serum cytokine profiles in patients with Plasmodium vivax malaria: a comparison between those who presented with and without thrombocytopenia. Ann Trop Med Parasitol 97: 339–344.
-
15.
Seoh JY, Khan M, Park SH, Park HK, Shin MH, Ha EH, Lee BE, Yoo K, Han HS, Oh S, Wi JH, Hong CK, Oh CH, Kim YA, Park JW, 2003. Serum cytokine profiles in patients with Plasmodium vivax malaria: a comparison between those who presented with and without hyperpyrexia. Am J Trop Med Hyg 68: 102–106.
-
16.
Jain V, Singh PP, Silawat N, Patel R, Saxena A, Bharti PK, Shukla M, Biswas S, Singh N, 2010. A preliminary study on pro- and anti-inflammatory cytokine profiles in Plasmodium vivax malaria patients from central zone of India. Acta Trop 113: 263–268.
-
17.
Long GH, Chan BH, Allen JE, Read AF, Graham AL, 2008. Blockade of TNF receptor 1 reduces disease severity but increases parasite transmission during Plasmodium chabaudi chabaudi infection. Int J Parasitol 38: 1073–1081.
-
18.
Luckhart S, Crampton AL, Zamora R, Lieber MJ, Dos Santos PC, Peterson TM, Emmith N, Lim J, Wink DA, Vodovotz Y, 2003. Mammalian transforming growth factor beta1 activated after ingestion by Anopheles stephensi modulates mosquito immunity. Infect Immun 71: 3000–3009.
-
19.
Luckhart S, Lieber MJ, Singh N, Zamora R, Vodovotz Y, 2008. Low levels of mammalian TGF-beta1 are protective against malaria parasite infection, a paradox clarified in the mosquito host. Exp Parasitol 118: 290–296.
-
20.
Long GH, Chan BH, Allen JE, Read AF, Graham AL, 2008. Experimental manipulation of immune-mediated disease and its fitness costs for rodent malaria parasites. BMC Evol Biol 8: 128.
-
21.
Naotunne TS, Karunaweera ND, Mendis KN, Carter R, 1993. Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology 78: 555–562.
-
22.
Lyke KE, Burges R, Cissoko Y, Sangare L, Dao M, Diarra I, Kone A, Harley R, Plowe CV, Doumbo OK, Sztein MB, 2004. Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect Immun 72: 5630–5637.
-
23.
Mirghani HA, Eltahir HG, A-Elgadir TM, Mirghani YA, Elbashir MI, Adam I, 2010. Cytokine profiles in children with severe Plasmodium falciparum malaria in an area of unstable malaria transmission in Central Sudan. J Trop Pediatr 57: 392–395.
-
24.
Andrade BB, Reis-Filho A, Souza-Neto SM, Clarencio J, Camargo LM, Barral A, Barral-Netto M, 2010. Severe Plasmodium vivax malaria exhibits marked inflammatory imbalance. Malar J 9: 13.
-
25.
Kilian AH, Metzger WG, Mutschelknauss EJ, Kabagambe G, Langi P, Korte R, von Sonnenburg F, 2000. Reliability of malaria microscopy in epidemiological studies: results of quality control. Trop Med Int Health 5: 3–8.
-
26.
Bowers KM, Bell D, Chiodini PL, Barnwell J, Incardona S, Yen S, Luchavez J, Watt H, 2009. Inter-rater reliability of malaria parasite counts and comparison of methods. Malar J 8: 267.
-
27.
O'Meara WP, McKenzie FE, Magill AJ, Forney JR, Permpanich B, Lucas C, Gasser RA Jr, Wongsrichanalai C, 2005. Sources of variability in determining malaria parasite density by microscopy. Am J Trop Med Hyg 73: 593–598.
-
28.
Peyron F, Burdin N, Ringwald P, Vuillez JP, Rousset F, Banchereau J, 1994. High levels of circulating IL-10 in human malaria. Clin Exp Immunol 95: 300–303.
-
29.
Awandare GA, Goka B, Boeuf P, Tetteh JK, Kurtzhals JA, Behr C, Akanmori BD, 2006. Increased levels of inflammatory mediators in children with severe Plasmodium falciparum malaria with respiratory distress. J Infect Dis 194: 1438–1446.
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