Patterns of Plasmodium homocircumflexum virulence in experimentally infected passerine birds

Abstract

Background Avian malaria parasites (genus Plasmodium ) are cosmopolitan and some species cause severe pathologies 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 affect bird populations 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 homocircumflexum (lineage pCOLL4) in four species of European passeriform birds. Methods One cryopreserved P. homocircumflexum strain was multiplied and used for experimental infections. House sparrows ( Passer domesticus ), common chaffinches ( Fringilla coelebs ), common crossbills ( Loxia curvirostra ) and common 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 monitored. 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 different in different bird species. Mortality due to malaria was reported in chaffinches, 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. homocircumflexum is generalist and the same lineage caused similar parasitaemia-related pathologies in different host species. Additionally, the mode of exo-erythrocytic development is different in different birds, resulting in different mortality rates. This should be taken into consideration in studies addressing pathology during avian malaria infections.

Plasmodium asexual growth and sexual development in the haematopoietic niche of the host

“…also show erythrocytic schizogony. merozoites from erythrocytic and exo-erythrocytic schizonts can initiate secondary exo-erythrocytic schizogony, forming phanerozoites, which often develop in endothelial cells lining the capillaries 110,119,120 . massive infestation of bone marrow cells by phanerozoites often occurs during infection of birds with Plasmodium elongatum and some other species 110,111,121 .…”

“…P. elongatum can cause dyserythropoiesis and anaemia due to damage of bone marrow cells 111,122 . The ability of erythrocytic and exo-erythrocytic merozoites to initiate secondary exo-erythrocytic schizogony in avian and reptile parasites opens opportunities for experiments on the tissue stages by inoculation of infected blood, avoiding the use of vectors 119 . Blood schizogony is only reported for Plasmodium spp.…”

Geographic and host distribution of haemosporidian parasite lineages from birds of the family Turdidae

“…Additional experimental infections of canaries with pLINN1 could help confirm differences between P. giovannolai and P. matutinum pLINN1 regarding the location of tissue stage formation. It is worth mentioning that the same Plasmodium strain might be markedly different in the ability to produce phanerozoites in the brain of different avian host species [87], so this feature should be used carefully in taxonomic research.…”

Haemosporidioses in wild Eurasian blackbirds (Turdus merula) and song thrushes (T. philomelos): an in situ hybridization study with emphasis on exo-erythrocytic parasite burden

“…In contrast, infection of immunologically naïve host species regularly results in severe morbidity and has caused mortalities in several non-passerine bird species [10][11][12][13][14][15][16][17][18]. However, several experimental infection studies demonstrated also high susceptibility of passerine bird species to certain haemosporidian parasites and markedly different pathogenicity depending both on infected host species and parasite strain [19][20][21][22][23]. Moreover, few reports showed lethal infections with Plasmodium spp.…”