Abstract
Five psittacine birds, one eastern rosella (Platycercus eximius), one rose-ringed parakeet (Psittacula krameri), two eclectus parrot (Eclectus roratus), and one princess parrot (Polytelis alexandrae), all housed in a commercial aviary from La Plata, Buenos Aires, Argentina, suddenly died after a short period of dyspnea. The most significant histopathological findings for all specimens were interstitial exudative pneumonia, with marked congestion and hemorrhage, septa thickening, and massive perivascular lymphoplasmacytic infiltration. Structures compatible with protozoal schizonts were observed in the capillary lumen. No bacterial development was obtained and the real-time PCR for Chlamydia spp. and several psittacine viruses were negative. All the samples resulted negative on the specific PCR for T. gondii. Sarcocystis spp. PCR was positive in the lung and/or liver samples from all birds. The samples showed a restriction pattern of S. neurona and of S. falcatula-like by PCR–RFLP using JNB25-JD396 and JNB33-JNB54 primers, respectively. Sequences obtained from Sarcocystis sp. 18S rRNA and COI gene from 4 birds showed a high identity among them. The 18S rRNA fragment and complete gene sequences obtained showed the highest similarity with S. falcatula and S. speeri sequences but also with S. neurona SN5 isolate sequence. Likewise, COI sequences have 99.89–100% similarity with S. falcatula and S. speeri sequences. Based on all biological and molecular information recorded, we conclude that the etiological agent was S. falcatula-like, close related with the species shed by opossums in South America.
References
Acosta ICL, Soares RM, Mayorga LFSP, Alves BF, Soares HS, Gennari SM (2018) Occurrence of tissue cyst forming coccidia in Magellanic penguins (Spheniscus magellanicus) rescued on the coast of Brazil. PLoS ONE 13(12):e0209007. https://doi.org/10.1371/journal.pone.0209007
Cesar MO, Matushima ER, Zwarg T, de Oliveira AS, Sanches TC, Joppert AM, Keid LB, Oliveira TMFS, Ferreira HL, Llano HAB, Konradt G, Bianchi MV, Gregori F, Gondim LFP, Soares RM (2018) Multilocus characterization of Sarcocystis falcatula-related organisms isolated in Brazil supports genetic admixture of high diverse SAG alleles among the isolates. Exp Parasitol 188:42–49. https://doi.org/10.1016/j.exppara.2018.03.004
Clubb SL, Frenkel JK (1992) Sarcocystis falcatula of opossums: transmission by cockroaches with fatal pulmonary disease in psittacine birds. J Parasitol 78(1):116–124
Dubey JP, Venturini L, Venturini C, Basso W, Unzaga J (1999) Isolation of Sarcocystis falcatula from the South American opossum (Didelphis albiventris) from Argentina. Vet Parasitol 86(4):239–244. https://doi.org/10.1016/S0304-4017(99)00145-4
Dubey JP, Venturini L, Venturini MC, Speer CA (2000) Isolation of Sarcocystis speeri Dubey and Lindsay, 1999 from the South American opossum (Didelphis albiventris) from Argentina. J Parasitol 86(1):160–163. https://doi.org/10.1645/0022-3395(2000)086[0160:IOSSDA]2.0.CO;2
Dubey JP, Verma SK, Dunams D, Calero-Bernal R, Rosenthal BM (2015) Molecular characterization and development of Sarcocystis speeri sarcocysts in gamma interferon gene knockout mice. Parasitology 142(13):1555–1562. https://doi.org/10.1017/S0031182015001109
Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer R (2016) Sarcocystosis of animals and humans. CRC Press, Boca Raton, p 510
Ecco R, Luppi MM, Malta MC, Araújo MR, Guedes RM, Shivaprasad HL (2008) An outbreak of sarcocystosis in psittacines and a pigeon in a zoological collection in Brazil. Avian Dis 52(4):706–710. https://doi.org/10.1637/8303-040408-Case.1
Ehricht R, Slickers P, Goellner S, Hotzel H, Sachse K (2006) Optimized DNA microarray assay allows detection and genotyping of single PCR-amplifiable target copies. Mol Cell Probes 20(1):60–63. https://doi.org/10.1016/j.mcp.2005.09.003
Gallo SSM, Lindsay DS, Ederli NB, Matteoli FP, Venancio TM, de Oliveira FCR (2018) Identification of opossums Didelphis aurita (Wied-Neuweid, 1826) as a definitive host of Sarcocystis falcatula-like sporocysts. Parasitol Res 117(1):213–223. https://doi.org/10.1007/s00436-017-5695-4
Gjerde B (2014) Molecular characterisation of Sarcocystis rileyi from a common eider (Somateria mollissima) in Norway. Parasitol Res 113(9):3501–3509. https://doi.org/10.1007/s00436-014-4062-y
Godoy SN, De Paula CD, Cubas ZS, Matushima ER, Catão-Dias JL (2009) Occurrence of Sarcocystis falcatula in captive psittacine birds in Brazil. J Avian Med Surg 23(1):18–24. https://doi.org/10.1647/2008-006R.1
Gondim LSQ, Jesus RF, Ribeiro-Andrade M, Silva JCR, Siqueira DB, Marvulo MFV, Aléssio FM, Mauffrey JF, Julião FS, Savani ESMM, Soares RM, Gondim LFP (2017) Sarcocystis neurona and Neospora caninum in Brazilian opossums (Didelphis spp.): molecular investigation and in vitro isolation of Sarcocystis spp. Vet Parasitol 243:192–198. https://doi.org/10.1016/j.vetpar.2017.07.002
Gondim LFP, Soares RM, Tavares AS, Borges-Silva W, de Jesus RF, Llano HAB, Gondim LQ (2019) Sarcocystis falcatula-like derived from opossum in Northeastern Brazil: in vitro propagation in avian cells, molecular characterization and bioassay in birds. Int J Parasitol Parasites Wildl 10:132–137. https://doi.org/10.1016/j.ijppaw.2019.08.008
Gondim LFP, Soares RM, Moré G, Jesus RF, Llano HAB (2021) Sarcocystis neurona and related Sarcocystis spp. shed by opossums (Didelphis spp.) in South America. Rev Bras Parasitol Vet 30(3):e006521. https://doi.org/10.1590/S1984-29612021059
Hillyer EV, Anderson MP, Greiner EC, Atkinson CT, Frenkel JK (1991) An outbreak of Sarcocystis in a collection of psittacines. J Zoo Wildl Med 22(4):434–445
Katoh H, Ohya K, Fukushi H (2008) Development of novel real-time PCR assays for detecting DNA virus infections in psittaciform birds. J Virol Methods 154(1–2):92–98. https://doi.org/10.1016/j.jviromet.2008.08.015
Máca O, González-Solís D (2021) Sarcocystis cristata sp. nov. (Apicomplexa, Sarcocystidae) in the imported great blue turaco Corythaeola cristata (Aves, Musophagidae). Parasit Vectors 14:56. https://doi.org/10.1186/s13071-020-04553-w
Moré G, Pardini L, Basso W, Machuca M, Bacigalupe D, Villanueva MC, Schares G, Venturini MC, Venturini L (2010) Toxoplasmosis and genotyping of Toxoplasma gondii in Macropus rufus and Macropus giganteus in Argentina. Vet Parasitol 169(1-2):57–61. https://doi.org/10.1016/j.vetpar.2009.12.004
Moré G, Schares S, Maksimov A, Conraths FJ, Venturini MC, Schares G (2013) Development of a multiplex real time PCR to differentiate Sarcocystis spp. affecting cattle. Vet Parasitol 197(1–2):85–94. https://doi.org/10.1016/j.vetpar.2013.04.024
Prakas P, Kutkienè L, Butkauskas D, Sruoga A, Žalakevičius M (2013) Molecular and morphological investigations of Sarcocystis corvusi sp. nov. from the jackdaw (Corvus monedula). Parasitol Res 112(3):1163–1167. https://doi.org/10.1007/s00436-012-3247-5
Rimoldi G, Speer B, Wellehan JF Jr, Bradway DS, Wright L, Reavill D, Barr BC, Childress A, Shivaprasad HL, Chin RP (2013) An outbreak of Sarcocystis calchasi encephalitis in multiple psittacine species within an enclosed zoological aviary. J Vet Diagn Invest 25(6):775–781. https://doi.org/10.1177/1040638713502981
Siegal-Willott JL, Pollock CG, Carpenter JW, Nietfeld J (2005) Encephalitis caused by Sarcocystis falcatula-like organisms in a white cockatoo (Cacatua alba). J Avian Med Surg 19(1):19–24
Tanhauser SM, Yowell CA, Cutler TJ, Greiner EC, Mackay RJ, Dame JB (1999) Multiple DNA markers differentiate Sarcocystis neurona and Sarcocystis falcatula. J Parasitol 85(2):221–228
Valadas SY, da Silva JI, Lopes EG, Keid LB, Zwarg T, de Oliveira AS, Sanches TC, Joppert AM, Pena HF, Oliveira TM, Ferreira HL, Soares RM (2016) Diversity of Sarcocystis spp. shed by opossums in Brazil inferred with phylogenetic analysis of DNA coding ITS1, cytochrome B, and surface antigens. Exp Parasitol 164:71–78. https://doi.org/10.1016/j.exppara.2016.02.008
Verma SK, Trupkiewicz JG, Georoff T, Dubey JP (2018) Molecularly confirmed acute, fatal Sarcocystis falcatula infection in the Rainbow Lorikeets (Trichoglossus moluccanus) at the philadelphia zoo. J Parasitol 104(6):710–712. https://doi.org/10.1645/18-78
Villar D, Kramer M, Howard L, Hammond E, Cray C, Latimer K (2008) Clinical presentation and pathology of sarcocystosis in psittaciform birds: 11 cases. Avian Dis 52(1):187–194. https://doi.org/10.1637/8104-090207-Case
Acknowledgements
We would like to thank Erika Badura for carrying out histo-technical work and Dra Maria Alejandra Quiroga for his valuable revision of the histopathological description.
Funding
This work was partially funded through grant PICT2016-3117 from Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), Argentina, and by the research founding grant code 11/V198 from Universidad Nacional de La Plata (UNLP).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Daniel K Howe
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Origlia, J., Unzaga, F., Piscopo, M. et al. Fatal sarcocystosis in psittacine birds from Argentina. Parasitol Res 121, 491–497 (2022). https://doi.org/10.1007/s00436-021-07375-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07375-6