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

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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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Acknowledgements

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.

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Authors and Affiliations

  1. Global Health Program, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, 20008, USA

    Jennifer H. Yu, Ellen P. Carlin, Marc T. Valitutto & Suzan Murray

  2. School of Life Sciences, University of Nottingham, Nottingham, UK

    Kate L. Durrant

  3. Chengdu Research Base of Giant Panda Breeding, Chengdu, Sichuan, People’s Republic of China

    Songrui Liu & Chengdong Wang

  4. EcoHealth Alliance, New York, NY, USA

    Ellen P. Carlin

  5. Center for Species Survival, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, 20008, USA

    Juan Rodriguez

  6. Department of Pathology, Smithsonian National Zoological Park, Washington, DC, USA

    Ann Bratthauer

  7. College of Veterinary Medicine, Kansas State University, Manhattan, KS, USA

    Tim Walsh

  8. Washington University in St. Louis, St. Louis, MO, USA

    Leah Fine

  9. Center for Conservation Genomics, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, 20008, USA

    Kate L. Durrant & Robert C. Fleischer

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  1. Jennifer H. Yu
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  2. Kate L. Durrant
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  3. Songrui Liu
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Correspondence to Jennifer H. Yu.

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Appendix

Appendix

List of all GenBank sequences used in comparative analysis in Figure 1.

  • HQ224959.1 Haemogregarina balli clone SAS_1 18S ribosomal RNA gene, partial sequence

  • HQ224958.1 Dactylosoma ranarum clone 1B1_6 18S ribosomal RNA gene, partial sequence

  • HQ224957.1 Dactylosoma ranarum clone 1A2_2 18S ribosomal RNA gene, partial sequence

  • EF622096.1 Hepatozoon canis isolate Pelotas 1 18S ribosomal RNA gene, partial sequence

  • AY461376.2 Hepatozoon canis isolate Curupira 1 18S ribosomal RNA gene, partial sequence

  • DQ439541.1 Hepatozoon canis isolate Spain 4 18S ribosomal RNA gene, partial sequence

  • LC331054.1 Hepatozoon canis gene for 18S ribosomal RNA, partial sequence, clone: MoM24

  • KX712128.1 Hepatozoon canis isolate 3470 18S ribosomal RNA gene, partial sequence

  • KX712124.1 Hepatozoon canis isolate 1 18S ribosomal RNA gene, partial sequence

  • KX712127.1 Hepatozoon canis isolate 2734 18S ribosomal RNA gene, partial sequence

  • KX712125.1 Hepatozoon canis isolate 2480 18S ribosomal RNA gene, partial sequence

  • KX712129.1 Hepatozoon canis isolate 3474 18S ribosomal RNA gene, partial sequence

  • AY150067.2 Hepatozoon canis isolate Spain-1 18S ribosomal RNA gene, partial sequence

  • AY461375.2 Hepatozoon canis isolate Curupira 3 18S ribosomal RNA gene, partial sequence

  • KX712123.1 Hepatozoon canis isolate 939 18S ribosomal RNA gene, partial sequence

  • LC169075.2 Hepatozoon canis gene for 18S ribosomal RNA, partial sequence, isolate: MT208

  • KX712126.1 Hepatozoon canis isolate 2733 18S ribosomal RNA gene, partial sequence

  • DQ439540.1 Hepatozoon canis isolate Venezuela 2 18S ribosomal RNA gene, partial sequence

  • LC331053.1 Hepatozoon canis gene for 18S ribosomal RNA, partial sequence, clone: LuM2

  • AY461378.2 Hepatozoon canis isolate Spain 2 18S ribosomal RNA gene, partial sequence

  • AY731062.1 Hepatozoon canis isolate Spain 3 18S ribosomal RNA gene, partial sequence

  • KC138531.2 Hepatozoon canis clone 9617 18S ribosomal RNA gene, partial sequence

  • KC138532.2 Hepatozoon canis clone 9618 18S ribosomal RNA gene, partial sequence

  • DQ111754.1 Hepatozoon canis isolate Dog-26 18S ribosomal RNA gene, partial sequence

  • LC331052.1 Hepatozoon canis gene for 18S ribosomal RNA, partial sequence, clone: ZD7

  • KU893120.1 Hepatozoon canis isolate fox 3-2 18S ribosomal RNA gene, partial sequence

  • KU893124.1 Hepatozoon canis isolate fox 9 18S ribosomal RNA gene, partial sequence

  • KU893127.1 Hepatozoon canis isolate dog 4 18S ribosomal RNA gene, partial sequence

  • KU893121.1 Hepatozoon canis isolate fox 4-2 18S ribosomal RNA gene, partial sequence

  • KU893126.1 Hepatozoon canis isolate dog 3 18S ribosomal RNA gene, partial sequence

  • KU893123.1 Hepatozoon canis isolate fox 6 18S ribosomal RNA gene, partial sequence

  • KU893119.1 Hepatozoon canis isolate fox 2-2 18S ribosomal RNA gene, partial sequence

  • KU893118.1 Hepatozoon canis isolate fox 1-2 18S ribosomal RNA gene, partial sequence

  • KU893125.1 Hepatozoon canis isolate fox 33 18S ribosomal RNA gene, partial sequence

  • KU893122.1 Hepatozoon canis isolate fox 5-2 18S ribosomal RNA gene, partial sequence

  • HQ829429.1 Hepatozoon ursi isolate LaCONES/Indian sloth bear 01 18S ribosomal RNA gene, partial sequence

  • EU041718.1 Hepatozoon ursi isolate Gifu 2 18S ribosomal RNA gene, partial sequence

  • HQ829434.1 Hepatozoon ursi isolate LaCONES/Indian sloth bear 06 18S ribosomal RNA gene, partial sequence

  • HQ829430.1 Hepatozoon ursi isolate LaCONES/Indian sloth bear 02 18S ribosomal RNA gene, partial sequence

  • EU041717.1 Hepatozoon ursi isolate Gifu 1 18S ribosomal RNA gene, partial sequence

  • AF176836.1 Hepatozoon americanum 18S ribosomal RNA gene, partial sequence

  • AY461377.2 Hepatozoon sp. - Curupira 2 18S ribosomal RNA gene, partial sequence

  • KC127679.1 Hepatozoon sp. F3 18S ribosomal RNA gene, partial sequence

  • LC169077.2 Hepatozoon sp. I35 gene for 18S ribosomal RNA, partial sequence, isolate: I35

  • LC169076.2 Hepatozoon sp. MT456 gene for 18S ribosomal RNA, partial sequence, isolate: MT456

  • EF222257.1 Hepatozoon sp. European pine marten 1 18S ribosomal RNA gene, partial sequence

  • KU198330.1 Hepatozoon sp. badger isolate 04/00284 18S ribosomal RNA gene, partial sequence

  • MG136688.1 Hepatozoon martis isolate 446/17 18S ribosomal RNA gene, partial sequence

  • MG136687.1 Hepatozoon martis isolate 197/16 18S ribosomal RNA gene, partial sequence

  • MK645858 Hepatozoon (panda) 113607 MeiXiang

  • KC138534.1 Hepatozoon felis clone 1 18S ribosomal RNA gene, partial sequence

  • KC138533.1 Hepatozoon felis clone 8533 18S ribosomal RNA gene, partial sequence

  • KX017290.1 Hepatozoon felis isolate Etawah 18S ribosomal RNA gene, partial sequence

  • HQ829445.1 Hepatozoon felis isolate LaCONES/Bengal tiger 01 18S ribosomal RNA gene, partial sequence

  • AY628681.1 Hepatozoon felis isolate Spain 2 18S ribosomal RNA gene, partial sequence

  • AY620232.1 Hepatozoon felis isolate Spain 1 18S ribosomal RNA gene, partial sequence

  • KX757032.1 Hepatozoon silvestris isolate 152/16 18S ribosomal RNA gene, partial sequence

  • HQ829439.1 Hepatozoon felis isolate LaCONES/Asiatic lion 02 18S ribosomal RNA gene, partial sequence

  • HQ829444.1 Hepatozoon felis isolate LaCONES/Indian leopard 02 18S ribosomal RNA gene, partial sequence

  • HQ829438.1 Hepatozoon felis isolate LaCONES/Asiatic lion 01 18S ribosomal RNA gene, partial sequence

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Yu, J.H., Durrant, K.L., Liu, S. et al. First Report of a Novel Hepatozoon sp. in Giant Pandas (Ailuropoda melanoleuca). EcoHealth 16, 338–345 (2019). https://doi.org/10.1007/s10393-019-01416-4

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  • DOI: https://doi.org/10.1007/s10393-019-01416-4

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