Plasmodium brasilianum ist Plasmodium malariae: Malaria-quartana-Parasiten im venezolanischen Amazonas

ZUSAMMENFASSUNG

Wir untersuchten Malariaproben aus weit entlegenen Yanomamidörfern des venezolanischen Amazonas und sequenzierten Teile der kleinen ribosomalen Untereinheit (18S) und des Circumsporozoitenantigens (CSP). Zwölf Patienten waren Träger von Malaria-quartana-Plasmodien, deren 18S-Sequenz zu 100 % identisch war mit P. brasilianum des Roten Brüllaffen (Alouatta seniculus). Auch das CSP-Antigen zeigte identische Repeatregionen. Zum ersten Mal wurden als P. brasilianum bezeichnete Plasmodien in einer natürlich erworbenen Infektion des Menschen nachgewiesen. Wir stellen die Hypothese auf, dass Malaria-quartana-Parasiten zwischen Affe und Mensch leicht hin und her wechseln und keine Spezifizität für Säugerwirte zeigen. Quartane Malaria sollte als echte Anthropozoonose betrachtet werden. Da der Name P. brasilianum eine eigenständige Spezies suggeriert, schlagen wir eine nomenklatorische Revision vor. Das große Wirtsreservoir unterscheidet quartane Malaria von anderen Malariaarten und erfordert spezifische Forschungsansätze und Kontrollstrategien im Sinne des One-Health-Konzepts.

Abstract

We investigated malaria cases from remote Yanomami indigenous communities of the Venezuelan Amazon and analyzed the genes coding for the circumsporozoite protein (CSP) and the small subunit of ribosomes (18S) by species-specific PCR and capillary based-DNA sequencing. Based on 18S rRNA gene sequencing, we identified 12 patients harboring malaria parasites which were 100 % identical with P. brasilianum isolated from the monkey, Alouatta seniculus. Translated amino acid sequences of the CS protein gene showed identical immunodominant repeat units between quartan malaria parasites isolated from both humans and monkeys. This study reports, for the first time, naturally acquired infections in humans with parasites termed as P. brasilianum. We conclude that quartan malaria parasites are easily exchanged between humans and monkeys in Latin America. We hypothesize a lack of host specificity in mammalian hosts and consider quartan malaria to be a true anthropozoonosis. Since the name P. brasilianum suggests a malaria species distinct from P. malariae, we propose that P. brasilianum should have a nomenclatorial revision in case further research confirms our findings. The expansive reservoir of mammalian hosts discriminates quartan malaria from other Plasmodium spp. and requires particular research efforts and control measures in the sense of the One Health concept.

Key words

P. brasilianum - P. malariae - quartan malaria parasites - nomenclatorial revision

• 1 Ramasamy R. Zoonotic malaria – global overview and research and policy needs.. Front Public Health 2014; 2: 123
• 2 Gonder R, von Berenberg-Gossler H. Untersuchungen über Malaria-plasmodien der, Affen.. Malar Int Arch Leipzig 1908; 1: 47-50
• 3 Coatney GR, Collins WE, Warren M. et al. The primate malarias. CD-ROM. 2003
• 4 Geiman QM, Siddiqui WA. Susceptibility of a New World monkey to Plasmodium malariae from aman.. Am J Trop Med Hyg 1969; 18: 351-354
• 5 Cochrane AH, Barnwell JW, Collins WE. et al. Monoclonal antibodies produced against sporozoites of the human parasite Plasmodium malariae abolish infectivity of sporozoites of the simian parasite Plasmodium brasilianum.. Infect Immun 1985; 50: 58-61
• 6 Lal AA, de la Cruz VF, Collins WE. et al. Circumsporozoite protein gene from Plasmodium brasilianum. Animal reservoirs for human malaria parasites?. J Biol Chem 1988; 263: 5495-5498
• 7 Snounou G, Viriyakosol S, Zhu XP. et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction.. Mol Biochem Parasitol 1993; 61: 315-320
• 8 Fandeur T, Volney B, Peneau C. et al. Monkeys of the rainforest in French Guiana are natural reservoirs for P. brasilianum/P. malariae malaria.. Parasitology 2000; 120: 11-21
• 9 Guimarães LO, Bajay MM, Wunderlich G. et al. The genetic diversity of Plasmodium malariae and Plasmodium brasilianum from human, simian and mosquito hosts in Brazil.. Acta Trop 2012; 124: 27-32
• 10 Tanomsing N, Imwong M, Pukrittayakamee S. et al. Genetic analysis of the dihydrofolate reductase-thymidylate synthase gene from geographically diverse isolates of Plasmodium malariae.. Antimicrob Agents Chemother 2007; 51: 3523-3530
• 11 Volney B, Pouliquen JF, De Thoisy B. et al. A sero-epidemiological study of malaria in human and monkey populations in French Guiana.. Acta Trop 2002; 82: 11-23
• 12 Baird JK. Malaria zoonoses.. Travel Med Infect Dis 2009; 7: 269-277
• 13 Metzger WG, Vivas-Martínez S, Rodriguez I. et al. Malaria diagnosis under field conditions in the Venezuelan Amazon.. Trans R Soc Trop Med Hyg 2008; 102: 20-24
• 14 von Humboldt A. Über die Verbindung zwischen dem Orinoko und dem Amazonenfluss.. Monatliche Correspondenz zur Beförderung der Erd- und Himmels-Kunde 1812; 26: 230-235
• 15 Metzger WG, Vivas-Martínez S, Giron A. et al. Assessment of routine malaria diagnosis in the Venezuelan Amazon.. Trans R Soc Trop Med Hyg 2011; 105: 262-268
• 16 Rodulfo H, De Donato M, Mora R. et al. Comparison of the diagnosis of malaria by microscopy, immunochromatography and PCR in endemic areas of Venezuela.. Braz J Med Biol Res 2007; 40: 535-543
• 17 Metzger WG, Giron AM, Vivas-Martínez S. et al. A rapid malaria appraisal in the Venezuelan Amazon.. Malar J 2009; 8: 291
• 18 Lalremruata A, Magris M, Vivas-Martínez S. et al. Natural infection of Plasmodium brasilianum in humans: Man and monkey share quartan malaria parasites in the Venezuelan Amazon.. EBioMedicine 2015; 2: 1186-1192
• 19 Tazi L, Ayala FJ. Unresolved direction of host transfer of Plasmodium vivax v. P. simium and P. malariae v. P.-brasilianum.. Infect Genet Evol 2011; 11: 209-221
• 20 Coatney GR. The simian malarias: zoonoses, anthroponoses, or both?. Am J Trop Med Hyg 1971; 20: 795-803
• 21 Escalante AA, Barrio E, Ayala FJ. Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene.. Mol Biol Evol 1995; 12: 616-626
• 22 Collins WE, Jeffery GM. Plasmodium malariae: parasite and disease.. Clin Microbiol Rev 2007; 20: 579-592
• 23 Mueller I, Zimmerman PA, Reeder JC. Plasmodium malariae and Plasmodium ovale – the “bashful” malaria parasites.. Trends Parasitol 2007; 23: 278-283
• 24 Hayakawa T, Arisue N, Udono T. et al. Identification of Plasmodium malariae, a human malaria parasite, in imported chimpanzees.. PLoS One 2009; 4: e7412
• 25 Ehrich JH, Eke FU. Malaria-induced renal damage: facts and myths.. Pediatr Nephrol 2007; 22: 626-637
• 26 McKenzie FE, Jeffery GM, Collins WE. Plasmodium malariae blood-stage dynamics.. J Parasitol 2001; 87: 626-637
• 27 Oliveira-Ferreira J, Lacerda MV, Brasil P. et al. Malaria in Brazil: an overview.. Malar J 2010; 9: 115
• 28 Autino B, Noris A, Russo R. et al. Epidemiology of malaria in endemic areas.. Mediterr J Hematol Infect Dis 2012; 4: e2012060
• 29 Doderer-Lang C, Atchade PS, Meckert L. et al. The ears of the African elephant: unexpected high seroprevalence of Plasmodium ovale and Plasmodium malariae in healthy populations in Western Africa.. Malar J 2014; 13: 240
• 30 Bharti PK, Chand SK, Singh MP. et al. Emergence of a new focus of Plasmodium malariae in forest villages of district Balaghat, Central India: implications for the diagnosis of malaria and its control.. Trop Med Int Health 2013; 18: 12-17
• 31 Greenwood BM, Bradley AK, Greenwood AM. et al. Mortality and morbidity from malaria among children in a rural area of The Gambia, West Africa.. Trans R Soc Trop Med Hyg 1987; 81: 478-486
• 32 Sutherland CJ, Tanomsing N, Nolder D. et al. Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally.. J Infect Dis 2010; 201: 1544-1550
• 33 de Pina-Costa A, Brasil P, Di Santi SM. et al. Malaria in Brazil: what happens outside the Amazonian endemic region.. Mem Inst Oswaldo Cruz 2014; 109: 618-633
• 34 Fuehrer HP, Swoboda P, Harl J. et al. High prevalence and genetic diversity of Plasmodium malariae and no evidence of Plasmodium knowlesi in Bangladesh.. Parasitol Res 2014; 113: 1537-1543
• 35 Bruce-Chwatt LJ. Malaria zoonosis in relation to malaria eradication. Trop Geogr Med 1968; Mar 20: 50-87