Usutu Virus Epizootic and <i>Plasmodium</i> Coinfection in Eurasian Blackbirds (<i>Turdus merula</i>) in Flanders, Belgium

Rouffaer, Lieze; Steensels, Mieke; Verlinden, Marc; Vervaeke, Muriel; Boonyarittichaikij, Roschong; Martel, An; Lambrecht, Bénédicte

doi:10.7589/2017-07-163

Cited by 27 publications

(31 citation statements)

References 12 publications

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“…USUV is an emerging mosquito-borne flavivirus highly pathogenic to several wild bird species. After its emergence in Italy in 1996 (Weissenböck et al 2013), it has spread to several European countries, including Belgium in 2012, where it re-emerged in 2016 (Cadar et al 2016, Borm et al 2017, Garigliany et al 2017, Rouffaer et al 2018. In this study, we show that USUV infection in wild birds occurred in southern Belgium during the two subsequent years (2017)(2018).…”

Section: Discussionsupporting

confidence: 53%

“…In Belgium, USUV infection was first detected in the Meuse Valley in a captive Eurasian bullfinch (Pyrrhula pyrrhula) and in a wild great spotted woodpecker (Dendrocopos major), both with neurological signs, in 2012 (Garigliany et al 2014). Four years later, high bird mortalities linked to USUV infection were documented all over the country (Cadar et al 2016, Borm et al 2017, Garigliany et al 2017, Rouffaer et al 2018, underlining the need for vigilance facing the reemergence and rapid spread of this virus.…”

Section: Introductionmentioning

confidence: 99%

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Usutu Virus Epizootic in Belgium in 2017 and 2018: Evidence of Virus Endemization and Ongoing Introduction Events

Benzarti

Sarlet

Franssen

et al. 2020

Vector-Borne and Zoonotic Diseases

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Wildlife surveillance allowed the monitoring of the zoonotic mosquito-borne Usutu virus (USUV) in birds and bats (Pipistrellus pipistrellus) in southern Belgium in 2017 and 2018. USUV-RNA was detected in 69 birds (of 253) from 15 species, among which 7 species had not previously been reported to be susceptible to the infection. Similarly, 2 bats (of 10) were detected positive by reverse transcriptase quantitative polymerase chain reaction (RT-qPCR). USUV-associated lesions were mainly found in Eurasian Blackbirds (Turdus merula), in which USUV antigens were demonstrated by immunohistochemistry in the brain, heart, liver, kidney, intestine, and lung. Partial nonstructural protein 5 gene-based phylogenetic analysis showed several identical or closely related strains from 2016, 2017, and 2018 clustering together within Europe 3 or Africa 3 lineages. Further, one USUV strain detected in a common chaffinch (Fringilla coelebs) manifested a close genetic relationship with the European 1 strains circulating in Hungary and Austria. Our data provide evidence of USUV endemization in southern Belgium in local birds and bats, extension of the host range of the virus and ongoing virus introduction from abroad, likely by migratory birds. Our results highlight the need for vigilance in the forthcoming years toward new virus-associated outbreaks in birds and possible human infections in Belgium.

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Section: Discussionsupporting

confidence: 53%

Section: Introductionmentioning

confidence: 99%

Usutu Virus Epizootic in Belgium in 2017 and 2018: Evidence of Virus Endemization and Ongoing Introduction Events

Benzarti

Sarlet

Franssen

et al. 2020

Vector-Borne and Zoonotic Diseases

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“…In contrast to P. vaughani-infected birds, in which extensive tissue merogony was rarely detected, P. matutinum-infected birds were frequently affected by severe burdens of exo-erythrocytic stages, suggesting differences in virulence of these two lineages. Different strains of P. matutinum, which belongs to the subgenus Haemamoeba, have been reported to show variable levels of virulence in avian hosts [40], and previous studies already indicated that infection with LINN1 is associated with disease and mortalities [24][25][26]. In the present study numerous phanerozoites of P. matutinum LINN1 were particularly often detected in heart, lung, and brain of birds with high parasite burdens, similar to a previous report of fatal Plasmodium infection caused by this lineage [26].…”

Section: Discussionsupporting

confidence: 90%

“…The study showed that Eurasian blackbirds and song thrushes were frequently infected with haemosporidian parasites, particularly with Plasmodium spp., among which the lineages P. matutinum LINN1 (belonging to the subgenus Haemamoeba), and P. vaughani SYAT05 (subgenus Novyella) were predominant. High Plasmodium infection rates have been reported in these host species not only from Austria [25], but also from other localities in Europe [24,[35][36][37][38] and in thrushes introduced to New Zealand [39], suggesting that these birds are natural reservoir hosts for Plasmodium parasites. In contrast to the study by Dinhopl et al [25], which detected only single infections of Plasmodium spp., This investigation demonstrates that Eurasian blackbirds were regularly (up to 30%) affected by severe burdens of exo-erythrocytic stages of Plasmodium spp.…”

Section: Discussionmentioning

confidence: 93%

“…Birds of the family Turdidae, in particular Eurasian blackbirds, are highly susceptible to Usutu virus (USUV) infection, and epizootic USUV-associated bird mortalities have been reported from several European countries, including Austria [31,[42][43][44][45][46][47][48][49][50]. More recent studies reported high USUV and Plasmodium co-infection rates in Eurasian blackbirds, suggesting that co-infection increases the likeliness of mortalities in infected birds [24,42]. In contrast to these reports, in the current investigation, USUV and Plasmodium infections were weakly associated.…”

Section: Discussionmentioning

confidence: 99%

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

Himmel

Harl

Pfanner

et al. 2019

Preprint

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Background Passerine birds are frequently infected with diverse haemosporidian parasites. While infections are traditionally considered benign in wild birds, recent studies demonstrated mortalities of passerine species due to exo-erythrocytic development of the parasites, which can damage organs in affected hosts. However, exo-erythrocytic development remains insufficiently investigated for most haemosporidian species and thus little is known about the virulence of tissue stages in wild passerine birds. The aim of the present study was to investigate natural haemosporidian infections in deceased Eurasian blackbirds (Turdus merula) and song thrushes (T. philomelos) and to determine parasite burden and associated histological effects.Methods For molecular analysis, blood and tissue samples from 306 thrushes were screened for Plasmodium, Haemoproteus and Leucocytozoon parasites by nested PCR. For the detection of parasite stages in organ samples, tissue sections were subjected to chromogenic in situ hybridization using genus- and species-specific probes targeting the rRNAs of parasites. Exo-erythrocytic parasite load was semi-quantitatively assessed and histological lesions were evaluated in haematoxylin-eosin-stained sections.Results 179 of 277 Eurasian blackbirds and 15 of 29 song thrushes were positive for haemosporidians. Parasites of all three genera were detected, with Plasmodium matutinum LINN1 and P. vaughani SYAT05 showing the highest prevalences. CISH revealed significant differences in exo-erythrocytic parasite burden between lineages in Eurasian blackbirds, with P. matutinum LINN1 frequently causing high parasite loads in various organs that were associated with histological alterations. Song thrushes infected with P. matutinum LINN1 and birds infected with other haemosporidian lineages showed mostly low parasite burdens. Two Eurasian blackbirds infected with Leucocytozoon sp. TUMER01 showed megalomeronts in various organs that were associated with inflammatory reactions and necroses.Conclusion This study suggests that P. matutinum LINN1, a common lineage among native thrushes, regularly causes high exo-erythrocytic parasite burdens in Eurasian blackbirds, which may result in disease and mortalities, indicating its high pathogenic potential. The findings further illustrate that the same parasite lineage may show different levels of virulence in related bird species which should be considered when assessing the pathogenicity of haemosporidian parasite species. Finally, the study provides evidence of virulent Leucocytozoon sp. TUMER01 infections in two Eurasian blackbirds caused by megalomeront formation.

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Usutu Virus

Malik

Milton

Ghatak

et al. 2021

Livestock Diseases and Management

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Usutu Virus Epizootic and Plasmodium Coinfection in Eurasian Blackbirds (Turdus merula) in Flanders, Belgium

Cited by 27 publications

References 12 publications

Usutu Virus Epizootic in Belgium in 2017 and 2018: Evidence of Virus Endemization and Ongoing Introduction Events

Usutu Virus Epizootic in Belgium in 2017 and 2018: Evidence of Virus Endemization and Ongoing Introduction Events

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

Usutu Virus

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