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Patterns of Plasmodium Homocircumflexum Virulence in Experimentally Infected Passerine Birds

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Patterns of Plasmodium Homocircumflexum Virulence in Experimentally Infected Passerine Birds Ilgūnas et al. Malar J (2019) 18:174 https://doi.org/10.1186/s12936-019-2810-2 Malaria Journal RESEARCH Open Access Patterns of Plasmodium homocircumfexum virulence in experimentally infected passerine birds Mikas Ilgūnas1* , Dovilė Bukauskaitė1, Vaidas Palinauskas1, Tatjana Iezhova1, Karin Fragner2, Elena Platonova1, Herbert Weissenböck2 and Gediminas Valkiūnas1 Abstract Background: Avian malaria parasites (genus Plasmodium) are cosmopolitan and some species cause severe patholo- gies or even mortality in birds, yet their virulence remains fragmentally investigated. Understanding mechanisms and patterns of virulence during avian Plasmodium infections is crucial as these pathogens can severely afect bird popula- tions in the wild and cause mortality in captive individuals. The goal of this study was to investigate the pathologies caused by the recently discovered malaria parasite Plasmodium homocircumfexum (lineage pCOLL4) in four species of European passeriform birds. Methods: One cryopreserved P. homocircumfexum strain was multiplied and used for experimental infections. House sparrows (Passer domesticus), common chafnches (Fringilla coelebs), common crossbills (Loxia curvirostra) and com- mon starlings (Sturnus vulgaris) were exposed by subinoculation of infected blood. Experimental and control groups (8 individuals in each) were observed for over 1 month. Parasitaemia, haematocrit value and body mass were moni- tored. At the end of the experiment, samples of internal organs were collected and examined using histological and chromogenic in situ hybridization methods. Results: All exposed birds were susceptible, with similar average prepatent period and maximum parasitaemia, yet virulence was diferent in diferent bird species. Mortality due to malaria was reported in chafnches, house sparrows and crossbills (7, 5 and 3 individuals died respectively), but not in starlings. Exoerythrocytic meronts (phanerozoites) were observed in the brain of all dead experimental birds. Blockage of blood vessels in the brain led to cerebral ischaemia, invariably causing brain damage, which is likely the main reason of mortality. Phanerozoites were observed in parenchymal organs, heart and muscles of all infected individuals, except starlings. Conclusion: This study shows that P. homocircumfexum is generalist and the same lineage caused similar parasitae- mia-related pathologies in diferent host species. Additionally, the mode of exo-erythrocytic development is diferent in diferent birds, resulting in diferent mortality rates. This should be taken into consideration in studies addressing pathology during avian malaria infections. Keywords: Avian malaria, Plasmodium, Birds, Phanerozoites, Pathology *Correspondence: [email protected] 1 Nature Research Centre, Akademijos 2, 08412 Vilnius, Lithuania Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ilgūnas et al. Malar J (2019) 18:174 Page 2 of 14 Background Phanerozoite stage is difcult to access in wild-caught With the exception of Antarctica, agents of avian malaria naturally infected avian hosts, in which the longevity of (Plasmodiidae, Haemosporida) have been reported all malaria infection usually is unknown. Additionally, the over the world [1, 2]. In all, 55 species of these pathogens exo-erythrocytic meronts also are sometimes difcult to have been recognized [3], and many new agents of avian visualize using the traditional histological approaches, malaria were discovered recently [4–9]. Species of Plas- particularly during light malaria infections. Molecu- modium have complex life cycles, which remain incom- lar diagnostic tools have been developed and might aid pletely investigated for the majority of these pathogens with the detection and identifcation of phanerozoites [10]. Tese parasites can cause severe health disorders in [26, 27]. Several recent studies reported detection of exo- domestic, wild and captive birds, sometimes even leading erythrocytic stages of avian malaria parasites, but these to lethal malaria [10–14]. were mainly case reports [19, 28–30]. Patterns of the Tere are two main causes of pathology during avian exo-erythrocytic development of avian Plasmodium spe- malaria infections: blood pathology [12, 15] and organ cies are still insufciently understood. Experimental work damage due to phanerozoites—tissue meronts develop- would be helpful to develop this knowledge, which is cru- ing during secondary exo-erythrocytic merogony [11, 12, cial to answer questions related to bird health, treatment, 16, 17]. During avian malaria, merozoites from erythro- ecology and possible threats to biodiversity. cytic meronts can induce exo-erythrocytic merogony Malaria parasite Plasmodium homocircumfexum (lin- (development of phanerozoites), and that is not the case eage pCOLL4) was recently discovered and described in during malaria in mammals. If blood pathology caused Europe [8, 31]. A pilot study was conducted with the aim by erythrocytic stages of avian malaria parasites has been to investigate the efects of this infection on three indi- relatively well studied [1, 12], the damage caused by tis- vidual birds belonging to three species [17]. Te obtained sue stages and patterns of their occurrence remain insuf- data suggested that Eurasian siskins (Carduelis spinus), fciently understood. Because phanerozoites develop in common crossbills (Loxia curvirostra) and common various non-specialized reticuloendothelial cells (mac- starlings (Sturnus vulgaris) were readily susceptible to P. rophages, endothelial cells of capillaries), they can occur homocircumfexum infections. Moreover, this parasite and cause damage of various organs in susceptible ver- developed phanerozoites in these birds and was lethal in tebrate hosts [10–12, 18, 19]. Due to the secondary exo- all tested bird individuals. Tis called for more a detailed erythrocytic merogony, avian malaria may be a more investigation of pathology caused by P. homocircum- virulent disease than human malaria. Additionally, the fexum in avian hosts. cause of virulence in avian malaria is more difcult to Te goal of this study was to experimentally investigate predict than during malaria in mammals due to unclear (1) the dynamics of parasitaemia and the parasitaemia patterns of phanerozoite occurrence. related health parameters (haematocrit value and body Recently, the issue of virulence of avian malaria patho- mass) during P. homocircumfexum (lineage pCOLL4) gens has attracted much attention. However, majority of infection in four common European bird species (com- the investigations focused mainly on parasitaemia during mon crossbill, common starling, house sparrow Passer Plasmodium infections [20–25]. Tese studies provided domesticus and common chafnch Fringilla coelebs) and valuable information about blood-related pathological (2) the development of secondary exo-erythrocytic mer- changes but are limited to truly evaluate mechanisms onts and pathologies caused in these birds. Parasitaemia, of the virulence during avian malaria due to the lack of haematocrit level and bird body mass were monitored at information about pathology caused in organs. Knowl- consistent time intervals, and birds were screened using edge about patterns of exo-erythrocytic development histological and chromogenic in situ hybridization meth- of malaria and other haemosporidian parasites remains ods for detection of the exo-erythrocytic stages. insufcient. Most studies dealing with exo-erythrocytic development were carried out between 1930s and 1960s Methods [10]—before molecular diagnostic techniques were intro- Study site duced in avian malaria research. Application of molecular Tis study was carried out at the Biological Station of the diagnostic methods showed that the diversity of parasites Zoological Institute of the Russian Academy of Sciences (both inter- and intra-species) is far greater than previ- on the Curonian Spit in the Baltic Sea (55°05′ N, 20°44′ ously believed. Tus, it becomes even more difcult E) during the months of May–August, 2015 and 2016. to address exo-erythrocytic development of particular Juvenile wild birds (< 7 months old) were used. Tey parasites and their lineages, calling for the application were caught using funnel traps and mists nets and iden- of modern diagnostic tools and experimental research in tifed to species and age according to [32]. Prior to the avian malaria studies. experiments, all birds were screened for haemosporidian Ilgūnas et al. MalarJ(2019)18:174 et al. Table 1 Susceptibility of passerine birds to Plasmodium homocircumfexum (lineage pCOLL4) infection after experimental exposure Bird species, group No. exposed No. died Prepatent Maximum parasitemiaa Minimum Maximum weight, ga No. of individuals with phanerozoites located in and infection dose (no. infected) period hematocrit (days) valuea Brain Heart Liver Lung Spleen Kidney Muscle Loxia curvirostra Experimental (3 106)b 8 (8) 7 4–8 3.3–23.3
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