, Volume 16, Issue 2, pp 338–345 | Cite as

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

  • Jennifer H. YuEmail author
  • 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
Short Communication


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.


Hepatozoon Ailuropoda melanoleuca Giant panda Apicomplexa Hemoparasite Conservation management Polymerase chain reaction 



The authors would like to thank our global partner zoological institutions—Smithsonian’s National Zoological Park, the Memphis Zoo, Zoo Atlanta, the Zoological Society of London Zoo, and the Chengdu Research Base of Giant Panda Breeding—for the collection of biological material and providing access to their samples. A multitude of staff and interns—including Lauren Helgen, Gracia Syed, Melanie O’Day, Kristin Stewardson, Tabitha Viner, and Beya Hull—also provided valuable assistance with this project, for which the authors are very grateful. This project was made possible with support from David M. Rubenstein and family, Judy and John W. McCarter, Jr., and the Smithsonian Institution. Generous support was also provided by the Morris Animal Foundation and Dennis and Connie Keller through our training partnership.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.


  1. Allen KE, Johnson EM, Little SE (2011) Hepatozoon spp infections in the United States. Veterinary Clinics of North America: Small Animal Practice 41:1221–1238CrossRefGoogle Scholar
  2. 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. Scholar
  3. 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. Scholar
  4. 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):125-134Google Scholar
  5. Best A, White A, Boots M (2014) The coevolutionary implications of host tolerance. Evolution 68(5):1426-1435CrossRefGoogle Scholar
  6. Clark KA, Robinson RM, Weishuhn LL, Galvin TJ, Horvath K (1973) Hepatozoon procyonis infections in Texas. Journal of Wildlife Diseases 9:182-193CrossRefGoogle Scholar
  7. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest2: more models, new heuristics and parallel computing. Nature Methods 9(8):772.CrossRefGoogle Scholar
  8. De Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecology Letters 8:117-126CrossRefGoogle Scholar
  9. 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):45-52CrossRefGoogle Scholar
  10. 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. Scholar
  11. Guindon S, Gascuel O (2003) A simple, fast, and accurate method to estimate large phylogenies by maximum likelihood. Systematic Biology 52(5):696-704.CrossRefGoogle Scholar
  12. 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): 912-920CrossRefGoogle Scholar
  13. 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):1647-1649CrossRefGoogle Scholar
  14. 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):149-153CrossRefGoogle Scholar
  15. 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):437-439CrossRefGoogle Scholar
  16. Kubo M, Miyoshi N, Yasuda N (2006) Hepatozoonosis in two species of Japanese wild cat. The Journal of Veterinary Medical Science 68(8):833-837CrossRefGoogle Scholar
  17. 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):287-294CrossRefGoogle Scholar
  18. 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):117-134Google Scholar
  19. 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):574-576CrossRefGoogle Scholar
  20. 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):867-868CrossRefGoogle Scholar
  21. 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. Scholar
  22. 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 182:329-332CrossRefGoogle Scholar
  23. 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 186:475-479CrossRefGoogle Scholar
  24. Qiu X, Mainka SA (1993) Review of mortality of the giant panda (Ailuropoda melanoleuca). Journal of Zoo and Wildlife Medicine 24(4):425-429Google Scholar
  25. 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. Scholar
  26. 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):105-109CrossRefGoogle Scholar
  27. 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. Scholar
  28. Smith KF, Sax DF, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20(5):1349-1357CrossRefGoogle Scholar
  29. Smith TG (1996) The genus Hepatozoon (Apicomplexa: Adeleina). The Journal of Parasitology 82(4):565-585CrossRefGoogle Scholar
  30. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312-1313CrossRefGoogle Scholar
  31. Swaisgood R, Wang D, Wei F (2016) Ailuropoda melanoleuca (errata version published in 2017). The IUCN Red List of Threatened Species 2016. Available: [accessed on 26 July 2018]
  32. 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. Scholar
  33. 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. Scholar
  34. 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. Scholar
  35. Zhang J, Daszak P, Huang H, Yang G, Kilpatrick AM, Zhang S (2008) Parasite threat to panda conservation. EcoHealth 5:6-9. Scholar

Copyright information

© EcoHealth Alliance 2019

Authors and Affiliations

  1. 1.Global Health ProgramSmithsonian Conservation Biology Institute, National Zoological ParkWashingtonUSA
  2. 2.School of Life SciencesUniversity of NottinghamNottinghamUK
  3. 3.Chengdu Research Base of Giant Panda BreedingChengduPeople’s Republic of China
  4. 4.EcoHealth AllianceNew YorkUSA
  5. 5.Center for Species Survival, Smithsonian Conservation Biology Institute, National Zoological ParkWashingtonUSA
  6. 6.Department of PathologySmithsonian National Zoological ParkWashingtonUSA
  7. 7.College of Veterinary MedicineKansas State UniversityManhattanUSA
  8. 8.Washington University in St. LouisSt. LouisUSA
  9. 9.Center for Conservation Genomics, Smithsonian Conservation Biology Institute, National Zoological ParkWashingtonUSA

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