In Situ Hybridization and Sequence Analysis Reveal an Association of Plasmodium Spp. with Mortalities in Wild Passerine Birds in Austria

Overview

Journal Parasitol Res

Specialty Parasitology

Date 2015 Feb 1

PMID 25636246

Citations 42

Authors

Nora Dinhopl

Nora Nedorost

Meike M Mostegl

Christiane Weissenbacher-Lang

Herbert Weissenbock

Affiliations

Soon will be listed here.

Abstract

Native European passerine birds are frequently clinically inapparent carriers of haemosporidian parasites of the genus Plasmodium. Clinical disease and death are only exceptionally reported. In the present study, tissue samples of 233 wild passerine birds found dead in Eastern Austria were examined by in situ hybridization (ISH) and partial cytochrome B gene sequence analysis for the presence, abundance and taxonomic assignment of Plasmodium spp. In 34 cases (14.6%), ISH yielded a positive result with large numbers of developmental stages in different cell types of the spleen, liver, brain and lung. The abundance of the tissue stages, which was comparable to fatal cases of avian malaria in penguins, suggested a major contribution to the cause of death. Genetic analysis revealed infections with representatives of three different valid species of Plasmodium, Plasmodium elongatum, Plasmodium lutzi and Plasmodium vaughani. Genetically identical parasite lineages had been found in a previous study in penguins kept in the Vienna zoo, providing evidence for the role of wild birds as reservoir hosts. Further, this study provides evidence that several species of Plasmodium are able to abundantly proliferate in endemic wild birds ultimately resulting in mortalities.

Citing Articles

Weak association of Usutu virus and haemosporidian infection in birds collected in Germany.

Hattendorf C, Cadar D, Bosch S, Becker N, Lachmann L, Schmidt-Chanasit J One Health. 2024; 19:100868.

PMID: 39247760 PMC: 11378720. DOI: 10.1016/j.onehlt.2024.100868.

RNAscope in situ hybridization reveals microvascular sequestration of Plasmodium relictum pSGS1 blood stages but absence of exo-erythrocytic dormant stages during latent infection of Serinus canaria.

Himmel T, Harl J, Matt J, Nedorost N, Iezhova T, Ilgunas M Malar J. 2024; 23(1):70.

PMID: 38459560 PMC: 10924391. DOI: 10.1186/s12936-024-04899-x.

Natural Vector of Avian Parasite and Factors Altering the Spread of Infection.

Ziegyte R, Palinauskas V, Bernotiene R Insects. 2023; 14(12).

PMID: 38132599 PMC: 10743420. DOI: 10.3390/insects14120926.

A non-invasive feather-based methodology for the detection of blood parasites (Haemosporida).

Gonzalez-Olvera M, Hernandez-Colina A, Chantrey J, Allen S, Lopez J, Baylis M Sci Rep. 2023; 13(1):16712.

PMID: 37794079 PMC: 10550939. DOI: 10.1038/s41598-023-43932-y.

Molecular investigation of Haemoproteus and Plasmodium species of some raptors in Hatay province: new CytB lineages for raptors of Accipitriformes in Turkey.

Zerek A, Ceylan O, Erdem I, Simsek F, Yaman M, Isler C Parasitol Res. 2023; 122(10):2423-2432.

PMID: 37615737 DOI: 10.1007/s00436-023-07948-7.

References

Sturrock H, Tompkins D . Avian malaria (Plasmodium spp) in yellow-eyed penguins: investigating the cause of high seroprevalence but low observed infection. N Z Vet J. 2007; 55(4):158-60. DOI: 10.1080/00480169.2007.36761. View

FLEISCHMAN R, SQUIRE R, SLADEN W, MELBY Jr E . Malaria (Plasmodium elongatum) in captive African penguins (Spheniscus demersus). J Am Vet Med Assoc. 1968; 153(7):928-35. View

Mantilla J, Matta N, Pacheco M, Escalante A, Gonzalez A, Moncada L . Identification of Plasmodium (Haemamoeba) lutzi (Lucena, 1939) from Turdus fuscater (Great Thrush) in Colombia. J Parasitol. 2013; 99(4):662-8. DOI: 10.1645/12-138.1. View

Chvala S, Bakonyi T, Bukovsky C, Meister T, Brugger K, Rubel F . Monitoring of Usutu virus activity and spread by using dead bird surveillance in Austria, 2003-2005. Vet Microbiol. 2007; 122(3-4):237-45. DOI: 10.1016/j.vetmic.2007.01.029. View

Atkinson C, Dusek R, Lease J . Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii amakihi. J Wildl Dis. 2001; 37(1):20-7. DOI: 10.7589/0090-3558-37.1.20. View

Christiana Grim K, van der Merwe E, Sullivan M, Parsons N, McCutchan T, Cranfield M . Plasmodium Juxtanucleare associated with mortality in black-footed penguins (Spheniscus demersus) admitted to a rehabilitation center. J Zoo Wildl Med. 2003; 34(3):250-5. DOI: 10.1638/02-070. View

Atkinson C, LaPointe D . Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. J Avian Med Surg. 2009; 23(1):53-63. DOI: 10.1647/2008-059.1. View

Perez-Tris J, Bensch S . Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology. 2005; 131(Pt 1):15-23. DOI: 10.1017/s003118200500733x. View

Scheuerlein A, Ricklefs R . Prevalence of blood parasites in European passeriform birds. Proc Biol Sci. 2004; 271(1546):1363-70. PMC: 1691737. DOI: 10.1098/rspb.2004.2726. View

10.

Dinhopl N, Mostegl M, Richter B, Nedorost N, Maderner A, Fragner K . Application of in-situ hybridization for the detection and identification of avian malaria parasites in paraffin wax-embedded tissues from captive penguins. Avian Pathol. 2011; 40(3):315-20. PMC: 3145101. DOI: 10.1080/03079457.2011.569533. View

11.

Fix A, Waterhouse C, Greiner E, Stoskopf M . Plasmodium relictum as a cause of avian malaria in wild-caught magellanic penguins (Spheniscus magellanicus). J Wildl Dis. 1988; 24(4):610-9. DOI: 10.7589/0090-3558-24.4.610. View

12.

Seidel B, Silbermayr K, Kolodziejek J, Indra A, Nowotny N, Allerberger F . Detection of Plasmodium sp.-infested Anopheles hyrcanus (Pallas 1771) (Diptera: Culicidae) in Austria, 2012. Wien Klin Wochenschr. 2013; 125(5-6):139-43. DOI: 10.1007/s00508-013-0331-5. View

13.

Martinez J, Martinez-de la Puente J, Herrero J, Del Cerro S, Lobato E, Rivero-de Aguilar J . A restriction site to differentiate Plasmodium and Haemoproteus infections in birds: on the inefficiency of general primers for detection of mixed infections. Parasitology. 2009; 136(7):713-22. DOI: 10.1017/S0031182009006118. View

14.

Graczyk T, Cranfield M, McCutchan T, Bicknese E . Characteristics of naturally acquired avian malaria infections in naive juvenile African black-footed penguins (Spheniscus demersus). Parasitol Res. 1994; 80(8):634-7. DOI: 10.1007/BF00932944. View

15.

Valkiunas G, Zehtindjiev P, Dimitrov D, Krizanauskiene A, Iezhova T, Bensch S . Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitol Res. 2008; 102(6):1185-93. DOI: 10.1007/s00436-008-0892-9. View

16.

Blanco G, Merino S, Tella J, Fargallo J, Gajon A . Hematozoa in two populations of the threatened red-billed chough in Spain. J Wildl Dis. 1997; 33(3):642-5. DOI: 10.7589/0090-3558-33.3.642. View

17.

Bentz S, Rigaud T, Barroca M, Martin-Laurent F, Bru D, Moreau J . Sensitive measure of prevalence and parasitaemia of haemosporidia from European blackbird (Turdus merula) populations: value of PCR-RFLP and quantitative PCR. Parasitology. 2006; 133(Pt 6):685-92. DOI: 10.1017/S0031182006001090. View

18.

Schoener E, Banda M, Howe L, Castro I, Alley M . Avian malaria in New Zealand. N Z Vet J. 2013; 62(4):189-98. DOI: 10.1080/00480169.2013.871195. View

19.

Howe L, Castro I, Schoener E, Hunter S, Barraclough R, Alley M . Malaria parasites (Plasmodium spp.) infecting introduced, native and endemic New Zealand birds. Parasitol Res. 2011; 110(2):913-23. PMC: 3264853. DOI: 10.1007/s00436-011-2577-z. View

20.

Bensch S, Hellgren O, Perez-Tris J . MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour. 2011; 9(5):1353-8. DOI: 10.1111/j.1755-0998.2009.02692.x. View