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Published in: EcoHealth 2/2019

01-06-2019 | Polymerase Chain Reaction | Short Communication

First Report of a Novel Hepatozoon sp. in Giant Pandas (Ailuropoda melanoleuca)

Authors: Jennifer H. Yu, Kate L. Durrant, Songrui Liu, Ellen P. Carlin, Chengdong Wang, Juan Rodriguez, Ann Bratthauer, Tim Walsh, Marc T. Valitutto, Leah Fine, Suzan Murray, Robert C. Fleischer

Published in: EcoHealth | Issue 2/2019

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Abstract

The first report of giant pandas (Ailuropoda melanoleuca) infected with a novel Hepatozoon species is presented. An intraleukocytic parasite was detected via routine blood smear from a zoo-housed giant panda at the National Zoological Park. Ribosomal DNA sequences indicated a previously undescribed Hepatozoon species. Phylogenetic and distance analyses of the sequences placed it within its own branch, clustered with Old World species with carnivore (primarily ursid and mustelid) hosts. Retrospective and opportunistic testing of other individuals produced additional positive detections (17/23, 73.9%), demonstrating 100% prevalence (14/14) across five institutions. All animals were asymptomatic at time of sampling, and health implications for giant pandas remain unknown.
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Literature
go back to reference Allen KE, Johnson EM, Little SE (2011) Hepatozoon spp infections in the United States. Veterinary Clinics of North America: Small Animal Practice 41:1221–1238CrossRef Allen KE, Johnson EM, Little SE (2011) Hepatozoon spp infections in the United States. Veterinary Clinics of North America: Small Animal Practice 41:1221–1238CrossRef
go back to reference André MR, Adania CH, Teixeira RHF, Vargas GH, Falcade M, Sousa L, Salles AR, Allegretti SM, Felippe PAN, Machado RZ (2010) Molecular detection of Hepatozoon spp. in Brazilian and exotic wild carnivores. Veterinary Parasitology 173:134–138. https://doi.org/10.1016/j.vetpar.2010.06.014CrossRefPubMed André MR, Adania CH, Teixeira RHF, Vargas GH, Falcade M, Sousa L, Salles AR, Allegretti SM, Felippe PAN, Machado RZ (2010) Molecular detection of Hepatozoon spp. in Brazilian and exotic wild carnivores. Veterinary Parasitology 173:134–138. https://​doi.​org/​10.​1016/​j.​vetpar.​2010.​06.​014CrossRefPubMed
go back to reference Baneth G, Mathew JS, Macintire DK, Barta JR, Ewing SA (2003) Canine hepatozoonosis: two disease syndromes caused by separate Hepatozoon spp. Trends in Parasitology 19(1): 27-31. https://doi.org/10.1016/s1471-4922(02)00016-8CrossRefPubMed Baneth G, Mathew JS, Macintire DK, Barta JR, Ewing SA (2003) Canine hepatozoonosis: two disease syndromes caused by separate Hepatozoon spp. Trends in Parasitology 19(1): 27-31. https://​doi.​org/​10.​1016/​s1471-4922(02)00016-8CrossRefPubMed
go back to reference Barton CL, Russo EA, Craig TM, Green RW (1985) Canine hepatozoonosis: A retrospective study of 15 naturally occurring cases. Journal of the American Animal Hospital Association 21(1):125-134 Barton CL, Russo EA, Craig TM, Green RW (1985) Canine hepatozoonosis: A retrospective study of 15 naturally occurring cases. Journal of the American Animal Hospital Association 21(1):125-134
go back to reference Best A, White A, Boots M (2014) The coevolutionary implications of host tolerance. Evolution 68(5):1426-1435CrossRefPubMed Best A, White A, Boots M (2014) The coevolutionary implications of host tolerance. Evolution 68(5):1426-1435CrossRefPubMed
go back to reference Clark KA, Robinson RM, Weishuhn LL, Galvin TJ, Horvath K (1973) Hepatozoon procyonis infections in Texas. Journal of Wildlife Diseases 9:182-193CrossRefPubMed Clark KA, Robinson RM, Weishuhn LL, Galvin TJ, Horvath K (1973) Hepatozoon procyonis infections in Texas. Journal of Wildlife Diseases 9:182-193CrossRefPubMed
go back to reference De Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecology Letters 8:117-126CrossRef De Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecology Letters 8:117-126CrossRef
go back to reference East ML, Wibbelt G, Lieckfeldt D, Ludwig A, Goller K, Wilhelm K, Schares G, Thierer D, Hofer H (2008) A Hepatozoon species genetically distinct from H canis infecting spotted hyenas in the Serengeti ecosystem, Tanzania. Journal of Wildlife Diseases 44(1):45-52CrossRefPubMed East ML, Wibbelt G, Lieckfeldt D, Ludwig A, Goller K, Wilhelm K, Schares G, Thierer D, Hofer H (2008) A Hepatozoon species genetically distinct from H canis infecting spotted hyenas in the Serengeti ecosystem, Tanzania. Journal of Wildlife Diseases 44(1):45-52CrossRefPubMed
go back to reference Feng N, Yu Y, Wang T, Wilker P, Wang J, Li Y, Sun Z, Gao Y, Xia X (2015) Fatal canine distemper virus infection of giant pandas in China. Scientific Reports 6:27518. https://doi.org/10.1038/srep27518CrossRef Feng N, Yu Y, Wang T, Wilker P, Wang J, Li Y, Sun Z, Gao Y, Xia X (2015) Fatal canine distemper virus infection of giant pandas in China. Scientific Reports 6:27518. https://​doi.​org/​10.​1038/​srep27518CrossRef
go back to reference Guindon S, Gascuel O (2003) A simple, fast, and accurate method to estimate large phylogenies by maximum likelihood. Systematic Biology 52(5):696-704.CrossRefPubMed Guindon S, Gascuel O (2003) A simple, fast, and accurate method to estimate large phylogenies by maximum likelihood. Systematic Biology 52(5):696-704.CrossRefPubMed
go back to reference Hodžića A, Alić A, Beck R, Beck A, Huber D, Otranto D, Baneth G, Duschera G (2018) Hepatozoon martis n sp (Adeleorina: Hepatozoidae): Morphological and pathological features of a Hepatozoon species infecting martens (family Mustelidae). Ticks and Tick-borne Diseases 9(4): 912-920CrossRef Hodžića A, Alić A, Beck R, Beck A, Huber D, Otranto D, Baneth G, Duschera G (2018) Hepatozoon martis n sp (Adeleorina: Hepatozoidae): Morphological and pathological features of a Hepatozoon species infecting martens (family Mustelidae). Ticks and Tick-borne Diseases 9(4): 912-920CrossRef
go back to reference Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647-1649CrossRefPubMedPubMedCentral Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647-1649CrossRefPubMedPubMedCentral
go back to reference Kocan AA, Cummings CA, Panciera RJ, Mathew JS, Ewing SA, Barker RW (2000) Naturally occurring and experimentally transmitted Hepatozoon americanum in coyotes from Oklahoma. Journal of Wildlife Diseases 36(1):149-153CrossRefPubMed Kocan AA, Cummings CA, Panciera RJ, Mathew JS, Ewing SA, Barker RW (2000) Naturally occurring and experimentally transmitted Hepatozoon americanum in coyotes from Oklahoma. Journal of Wildlife Diseases 36(1):149-153CrossRefPubMed
go back to reference Kubo M, Jeong A, Kim S, Kim Y, Lee H, Kimura J, Yanai T (2010) The first report of Hepatozoon species infection in leopard cats (Prionailurus bengalensis) in Korea. The Journal of Parasitology 96(2):437-439CrossRefPubMed Kubo M, Jeong A, Kim S, Kim Y, Lee H, Kimura J, Yanai T (2010) The first report of Hepatozoon species infection in leopard cats (Prionailurus bengalensis) in Korea. The Journal of Parasitology 96(2):437-439CrossRefPubMed
go back to reference Kubo M, Miyoshi N, Yasuda N (2006) Hepatozoonosis in two species of Japanese wild cat. The Journal of Veterinary Medical Science 68(8):833-837CrossRefPubMed Kubo M, Miyoshi N, Yasuda N (2006) Hepatozoonosis in two species of Japanese wild cat. The Journal of Veterinary Medical Science 68(8):833-837CrossRefPubMed
go back to reference Kubo M, Uni S, Agatsuma T, Nagataki M, Panciera RJ, Tsubota T, Nakamura S, Sakai H, Masegi T, Yanai T (2008) Hepatozoon ursi n sp (Apicomplexa: Hepatozoidae) in Japanese black bear (Ursus thibetanus japonicas). Parasitology International 57(3):287-294CrossRefPubMed Kubo M, Uni S, Agatsuma T, Nagataki M, Panciera RJ, Tsubota T, Nakamura S, Sakai H, Masegi T, Yanai T (2008) Hepatozoon ursi n sp (Apicomplexa: Hepatozoidae) in Japanese black bear (Ursus thibetanus japonicas). Parasitology International 57(3):287-294CrossRefPubMed
go back to reference McCully RM, Basson PA, Bigalke RD, De Vos V, Young E (1975) Observations on naturally acquired hepatozoonosis of wild carnivores and dogs in the Republic of South Africa. Onderstepoort Journal of Veterinary Research 42(4):117-134 McCully RM, Basson PA, Bigalke RD, De Vos V, Young E (1975) Observations on naturally acquired hepatozoonosis of wild carnivores and dogs in the Republic of South Africa. Onderstepoort Journal of Veterinary Research 42(4):117-134
go back to reference Mercer SH, Jones LP, Rappole JH, Twedt D, Laack LL, Craig TM (1988) Hepatozoon sp in wild carnivores in Texas. Journal of Wildlife Diseases 24(3):574-576CrossRefPubMed Mercer SH, Jones LP, Rappole JH, Twedt D, Laack LL, Craig TM (1988) Hepatozoon sp in wild carnivores in Texas. Journal of Wildlife Diseases 24(3):574-576CrossRefPubMed
go back to reference Murata T, Inoue M, Tateyama S, Taura Y, Nakama S (1993) Vertical transmission of Hepatozoon canis in dogs. Journal of Veterinary Medical Science 55(5):867-868CrossRef Murata T, Inoue M, Tateyama S, Taura Y, Nakama S (1993) Vertical transmission of Hepatozoon canis in dogs. Journal of Veterinary Medical Science 55(5):867-868CrossRef
go back to reference Otranto D, Dantas-Torres F, Weigl S, Latrofa, MS, Stanneck D, Decaprariis D, Capelli G, Baneth G (2011) Diagnosis of Hepatozoon canis in young dogs by cytology and PCR. Parasits and Vectors 4:55. https://doi.org/10.1186/1756-3305-4-55CrossRef Otranto D, Dantas-Torres F, Weigl S, Latrofa, MS, Stanneck D, Decaprariis D, Capelli G, Baneth G (2011) Diagnosis of Hepatozoon canis in young dogs by cytology and PCR. Parasits and Vectors 4:55. https://​doi.​org/​10.​1186/​1756-3305-4-55CrossRef
go back to reference Pawar RM, Poornachandar A, Arun AS, Manikandan S, Shivaji S (2011) Molecular prevalence and characterization of Hepatozoon ursi infection in Indian sloth bears (Melursus ursinus). Veterinary Parasitology 182:329-332CrossRefPubMed Pawar RM, Poornachandar A, Arun AS, Manikandan S, Shivaji S (2011) Molecular prevalence and characterization of Hepatozoon ursi infection in Indian sloth bears (Melursus ursinus). Veterinary Parasitology 182:329-332CrossRefPubMed
go back to reference Pawar RM, Poornachandar A, Srinivas P, Rao KR, Lakshmikantan U, Shivaji S (2012) Molecular characterization of Hepatozoon spp infection in endangered Indian wild felids and canids. Veterinary Parasitology 186:475-479CrossRefPubMed Pawar RM, Poornachandar A, Srinivas P, Rao KR, Lakshmikantan U, Shivaji S (2012) Molecular characterization of Hepatozoon spp infection in endangered Indian wild felids and canids. Veterinary Parasitology 186:475-479CrossRefPubMed
go back to reference Qiu X, Mainka SA (1993) Review of mortality of the giant panda (Ailuropoda melanoleuca). Journal of Zoo and Wildlife Medicine 24(4):425-429 Qiu X, Mainka SA (1993) Review of mortality of the giant panda (Ailuropoda melanoleuca). Journal of Zoo and Wildlife Medicine 24(4):425-429
go back to reference Scopel KKG, Fontes CJF, Nunes AC, De Fátima Horta M, Braga EM (2004) Low sensitivity of nested PCR using Plasmodium DNA extracted from stained thick blood smears: an epidemiological retrospective study among subjects with low parasitemia in an endemic area of the Brazilian Amazon region. Malaria Journal 3:8. https://doi.org/10.1186/1475-2875-3-8CrossRefPubMedPubMedCentral Scopel KKG, Fontes CJF, Nunes AC, De Fátima Horta M, Braga EM (2004) Low sensitivity of nested PCR using Plasmodium DNA extracted from stained thick blood smears: an epidemiological retrospective study among subjects with low parasitemia in an endemic area of the Brazilian Amazon region. Malaria Journal 3:8. https://​doi.​org/​10.​1186/​1475-2875-3-8CrossRefPubMedPubMedCentral
go back to reference Shavey CA, Morado JF (2012) DNA extraction from archived Giemsa-stained blood smears using polymerase chain reaction to detect host and parasitic DNA. Journal of Histotechnology 35(30):105-109CrossRef Shavey CA, Morado JF (2012) DNA extraction from archived Giemsa-stained blood smears using polymerase chain reaction to detect host and parasitic DNA. Journal of Histotechnology 35(30):105-109CrossRef
go back to reference Simposon VR, Hargreaves J, Butler HM, Davison NJ, Everest DJ (2013) Causes of mortality and pathological lesions observed post-mortem in red squirrels (Sciurus vulgaris) in Great Britain. BioMed Central Veterinary Research 9:229. https://doi.org/10.1186/1746-6148-9-229CrossRef Simposon VR, Hargreaves J, Butler HM, Davison NJ, Everest DJ (2013) Causes of mortality and pathological lesions observed post-mortem in red squirrels (Sciurus vulgaris) in Great Britain. BioMed Central Veterinary Research 9:229. https://​doi.​org/​10.​1186/​1746-6148-9-229CrossRef
go back to reference Smith KF, Sax DF, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20(5):1349-1357CrossRefPubMed Smith KF, Sax DF, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20(5):1349-1357CrossRefPubMed
go back to reference Smith TG (1996) The genus Hepatozoon (Apicomplexa: Adeleina). The Journal of Parasitology 82(4):565-585CrossRefPubMed Smith TG (1996) The genus Hepatozoon (Apicomplexa: Adeleina). The Journal of Parasitology 82(4):565-585CrossRefPubMed
go back to reference Wei F, Song M, Liu H, Wang B, Wang S, Wang Z, Ma H, Li Z, Zeng Z, Qian J, Liu Q (2016) Molecular detection and characterization of zoonotic and veterinary pathogens in ticks from northeastern China. Frontiers in Microbiology 7:1913. https://doi.org/10.3389/fmicb.2016.01913CrossRefPubMedPubMedCentral Wei F, Song M, Liu H, Wang B, Wang S, Wang Z, Ma H, Li Z, Zeng Z, Qian J, Liu Q (2016) Molecular detection and characterization of zoonotic and veterinary pathogens in ticks from northeastern China. Frontiers in Microbiology 7:1913. https://​doi.​org/​10.​3389/​fmicb.​2016.​01913CrossRefPubMedPubMedCentral
go back to reference Williams CL, Dill-McFarland KA, Vandewege MW, Sparks DL, Willard ST, Kouba AJ, Suen G, Brown AE (2016) Dietary shifts may trigger dysbiosis and mucous stools in giant pandas (Ailuropoda melanoleuca). Frontiers in Microbiology 7:661. https://doi.org/10.3389/fmicb.2016.00661CrossRefPubMedPubMedCentral Williams CL, Dill-McFarland KA, Vandewege MW, Sparks DL, Willard ST, Kouba AJ, Suen G, Brown AE (2016) Dietary shifts may trigger dysbiosis and mucous stools in giant pandas (Ailuropoda melanoleuca). Frontiers in Microbiology 7:661. https://​doi.​org/​10.​3389/​fmicb.​2016.​00661CrossRefPubMedPubMedCentral
go back to reference Xu D, Zhang J, Shi Z, Song C, Zheng X, Zhang Y, Hao Y, Dong H, Wei L, El-Mahallawy HS, Kelly P, Xiong W, Wang H, Li J, Zhang X, Gu J, Wang C (2015) Molecular detection of vector-borne agents in dogs from ten provinces of China. Parasites and Vectors 8:501. https://doi.org/10.1186/213071-015-1120-yCrossRefPubMedPubMedCentral Xu D, Zhang J, Shi Z, Song C, Zheng X, Zhang Y, Hao Y, Dong H, Wei L, El-Mahallawy HS, Kelly P, Xiong W, Wang H, Li J, Zhang X, Gu J, Wang C (2015) Molecular detection of vector-borne agents in dogs from ten provinces of China. Parasites and Vectors 8:501. https://​doi.​org/​10.​1186/​213071-015-1120-yCrossRefPubMedPubMedCentral
go back to reference Zhang J, Daszak P, Huang H, Yang G, Kilpatrick AM, Zhang S (2008) Parasite threat to panda conservation. EcoHealth 5:6-9. https://doi.org/10.1007/s10393-007-0139-8CrossRefPubMed Zhang J, Daszak P, Huang H, Yang G, Kilpatrick AM, Zhang S (2008) Parasite threat to panda conservation. EcoHealth 5:6-9. https://​doi.​org/​10.​1007/​s10393-007-0139-8CrossRefPubMed
Metadata
Title
First Report of a Novel Hepatozoon sp. in Giant Pandas (Ailuropoda melanoleuca)
Authors
Jennifer H. Yu
Kate L. Durrant
Songrui Liu
Ellen P. Carlin
Chengdong Wang
Juan Rodriguez
Ann Bratthauer
Tim Walsh
Marc T. Valitutto
Leah Fine
Suzan Murray
Robert C. Fleischer
Publication date
01-06-2019
Publisher
Springer US
Published in
EcoHealth / Issue 2/2019
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-019-01416-4

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