Characterization of Classical Sheep Scrapie in White-tailed Deer after Experimental Oronasal Exposure

Greenlee, Justin J.; Moore, S. Jo; Cassmann, Eric D.; Lambert, Zoe J.; Kokemuller, Robyn D.; Smith, Jodi D.; Kunkle, Robert A.; Kong, Qingzhong; Greenlee, M. Heather West

doi:10.1093/infdis/jiac443

Characterization of Classical Sheep Scrapie in White-tailed Deer after Experimental Oronasal Exposure

Journal Article · Mon Nov 07 23:00:00 EST 2022 · Journal of Infectious Diseases

DOI:https://doi.org/10.1093/infdis/jiac443· OSTI ID:2425605

; Moore, S. Jo; Cassmann, Eric D.; Lambert, Zoe J.; Kokemuller, Robyn D.; Smith, Jodi D.; Kunkle, Robert A.; Kong, Qingzhong; Greenlee, M. Heather West

Abstract Background

Classic scrapie is a prion disease of sheep and goats that is associated with accumulation of abnormal prion protein (PrPSc) in the central nervous and lymphoid tissues. Chronic wasting disease (CWD) is the prion disease of cervids. This study was conducted to determine the susceptibility of white-tailed deer (WTD) to the classic scrapie agent.

Methods

We inoculated WTD (n = 5) by means of a concurrent oral/intranasal exposure with the classic scrapie agent from sheep or oronasally with the classic scrapie agent from goats (n = 6).

Results

All deer exposed to the agent of classic scrapie from sheep accumulated PrPSc. PrPSc was detected in lymphoid tissues at preclinical time points, and necropsies in deer 28 months after inoculation showed clinical signs, spongiform lesions, and widespread PrPSc in neural and lymphoid tissues. Western blots on samples from the brainstem, cerebellum, and lymph nodes of scrapie-infected WTD have a molecular profile similar to CWD and distinct from samples from the cerebral cortex, retina, or the original classic scrapie inoculum. There was no evidence of PrPSc in any of the WTD inoculated with classic scrapie prions from goats.

Conclusions

WTD are susceptible to the agent of classic scrapie from sheep, and differentiation from CWD may be difficult.

Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: SC0014664

OSTI ID:: 2425605

Journal Information:: Journal of Infectious Diseases, Journal Name: Journal of Infectious Diseases Journal Issue: 12 Vol. 227; ISSN 0022-1899

Publisher:: Infectious Diseases Society of America

Country of Publication:: United States

Language:: English

References (46)

Evaluation of Antemortem Diagnostic Techniques in Goats Naturally Infected With Scrapie Mammadova, Najiba; West Greenlee, M. Heather; Moore, S. Jo Frontiers in Veterinary Science, Vol. 7 https://doi.org/10.3389/fvets.2020.517862	journal	November 2020
Transmission and Detection of Prions in Feces Safar, Jiri G.; Lessard, Pierre; Tamgüney, Gültekin The Journal of Infectious Diseases, Vol. 198, Issue 1 https://doi.org/10.1086/588193	journal	July 2008
Sporadic Creutzfeldt-Jakob disease: Co-occurrence of different types of PrP ^Sc in the same brain Puoti, G.; Giaccone, G.; Rossi, G. Neurology, Vol. 53, Issue 9 https://doi.org/10.1212/WNL.53.9.2173	journal	December 1999
A Comparative Study of Immunohistochemical Methods for Detecting Abnormal Prion Protein with Monoclonal and Polyclonal Antibodies Hardt, M.; Baron, T.; Groschup, Mh Journal of Comparative Pathology, Vol. 122, Issue 1 https://doi.org/10.1053/jcpa.1999.0343	journal	January 2000
Salivary prions in sheep and deer Tamgüney, Gültekin; Richt, Jürgen A.; Hamir, Amir N. Prion, Vol. 6, Issue 1 https://doi.org/10.4161/pri.6.1.16984	journal	January 2012
Structural effects of PrP polymorphisms on intra- and interspecies prion transmission Angers, Rachel; Christiansen, Jeffrey; Nalls, Amy V. Proceedings of the National Academy of Sciences, Vol. 111, Issue 30 https://doi.org/10.1073/pnas.1404739111	journal	July 2014
First case of chronic wasting disease in Europe in a Norwegian free-ranging reindeer Benestad, Sylvie L.; Mitchell, Gordon; Simmons, Marion Veterinary Research, Vol. 47, Issue 1 https://doi.org/10.1186/s13567-016-0375-4	journal	September 2016
Advances in the detection of prion protein in peripheral tissues of variant Creutzfeldt‐Jakob disease patients using paraffin‐embedded tissue blotting Ritchie, D. L.; Head, M. W.; Ironside, J. W. Neuropathology and Applied Neurobiology, Vol. 30, Issue 4 https://doi.org/10.1111/j.1365-2990.2003.00544.x	journal	February 2004
Prion protein heterogeneity in sporadic but not variant Creutzfeldt–Jakob disease: U.K. cases 1991–2002 Head, Mark W.; Bunn, Tristan J. R.; Bishop, Matthew T. Annals of Neurology, Vol. 55, Issue 6 https://doi.org/10.1002/ana.20127	journal	May 2004
Infectious Prions in the Saliva and Blood of Deer with Chronic Wasting Disease Mathiason, C. K.; Powers, J. G.; Dahmes, S. J. Science, Vol. 314, Issue 5796 https://doi.org/10.1126/science.1132661	journal	October 2006
Chronic Wasting Disease of Cervids: Current Knowledge and Future Perspectives Haley, Nicholas J.; Hoover, Edward A. Annual Review of Animal Biosciences, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-animal-022114-111001	journal	February 2015
Preclinical Diagnosis of Scrapie by Immunohistochemistry of Third Eyelid Lymphoid Tissue O'Rourke, K. I.; Baszler, T. V.; Besser, T. E. Journal of Clinical Microbiology, Vol. 38, Issue 9 https://doi.org/10.1128/JCM.38.9.3254-3259.2000	journal	January 2000
Oral transmission and early lymphoid tropism of chronic wasting disease PrPres in mule deer fawns (Odocoileus hemionus ) Sigurdson, Christina J.; Williams, Elizabeth S.; Miller, Michael W. Journal of General Virology, Vol. 80, Issue 10 https://doi.org/10.1099/0022-1317-80-10-2757	journal	October 1999
Transmission of Raccoon-Passaged Chronic Wasting Disease Agent to White-Tailed Deer Cassmann, Eric D.; Frese, Alexis J.; Moore, S. Jo Viruses, Vol. 14, Issue 7 https://doi.org/10.3390/v14071578	journal	July 2022
PrP Genotype and Agent Effects in Scrapie: Change In Allelic Interaction With Different Isolates of Agent in Sheep, a Natural Host of Scrapie Goldmann, W.; Hunter, N.; Smith, G. Journal of General Virology, Vol. 75, Issue 5 https://doi.org/10.1099/0022-1317-75-5-989	journal	May 1994
Distribution of intraneuronal immunoreactivity for the prion protein in human prion diseases Kovacs, Gabor G.; Voigtländer, Till; Hainfellner, Johannes A. Acta Neuropathologica, Vol. 104, Issue 3 https://doi.org/10.1007/s00401-002-0550-8	journal	September 2002
Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects Parchi, Piero; Giese, Armin; Capellari, Sabina Annals of Neurology, Vol. 46, Issue 2 https://doi.org/10.1002/1531-8249(199908)46:2<224::AID-ANA12>3.0.CO;2-W	journal	August 1999
Lack of Prion Accumulation in Lymphoid Tissues of PRNP ARQ/ARR Sheep Intracranially Inoculated with the Agent of Scrapie Greenlee, Justin J.; Kunkle, Robert A.; Richt, Jürgen A. PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0108029	journal	September 2014
Environmental Sources of Prion Transmission in Mule Deer Miller, Michael W.; Williams, Elizabeth S.; Hobbs, N. Thompson Emerging Infectious Diseases, Vol. 10, Issue 6 https://doi.org/10.3201/eid1006.040010	journal	June 2004
Beyond PrPres Type 1/Type 2 Dichotomy in Creutzfeldt-Jakob Disease Uro-Coste, Emmanuelle; Cassard, Hervé; Simon, Stéphanie PLoS Pathogens, Vol. 4, Issue 3 https://doi.org/10.1371/journal.ppat.1000029	journal	March 2008
Infectious Prions in Pre-Clinical Deer and Transmission of Chronic Wasting Disease Solely by Environmental Exposure Mathiason, Candace K.; Hays, Sheila A.; Powers, Jenny PLoS ONE, Vol. 4, Issue 6 https://doi.org/10.1371/journal.pone.0005916	journal	June 2009
Spongiform encephalopathies in cervidae: -EN- -FR- -ES- Williams, E. S.; Young, S. Revue Scientifique et Technique de l'OIE, Vol. 11, Issue 2 https://doi.org/10.20506/rst.11.2.611	journal	June 1992
Serial Passage of Sheep Scrapie Inoculum in Suffolk Sheep Hamir, A. N.; Kunkle, R. A.; Richt, J. A. Veterinary Pathology, Vol. 46, Issue 1 https://doi.org/10.1354/vp.46-1-39	journal	January 2009
The Host Range of Chronic Wasting Disease Is Altered on Passage in Ferrets Bartz, Jason C.; Marsh, Richard F.; McKenzie, Debbie I. Virology, Vol. 251, Issue 2 https://doi.org/10.1006/viro.1998.9427	journal	November 1998
Experimental Transmission of Sheep Scrapie by Intracerebral and Oral Routes to Genetically Susceptible Suffolk Sheep in the United States Hamir, Amir N.; Kunkle, Robert A.; Richt, Juergen A. Journal of Veterinary Diagnostic Investigation, Vol. 17, Issue 1 https://doi.org/10.1177/104063870501700103	journal	January 2005
Region-specific protein misfolding cyclic amplification reproduces brain tropism of prion strains Privat, Nicolas; Levavasseur, Etienne; Yildirim, Serfildan Journal of Biological Chemistry, Vol. 292, Issue 40 https://doi.org/10.1074/jbc.M117.793646	journal	October 2017
Molecular basis of phenotypic variability in sporadc creudeldt-jakob disease Parchi, Piero; Castellani, Rudolph; Capellari, Sabina Annals of Neurology, Vol. 39, Issue 6 https://doi.org/10.1002/ana.410390613	journal	June 1996
Second passage of chronic wasting disease of mule deer to sheep by intracranial inoculation compared to classical scrapie Cassmann, Eric D.; Frese, Rylie D.; Greenlee, Justin J. Journal of Veterinary Diagnostic Investigation, Vol. 33, Issue 4 https://doi.org/10.1177/10406387211017615	journal	May 2021
Spongiform Encephalopathy in Free-Ranging mule deer (Odocoileus Hemionus), White-Tailed deer (Odocoileus Virginianus) and Rocky Mountain elk (Cervus Elaphus Nelsoni) in Northcentral Colorado Spraker, T. R.; Miller, M. W.; Williams, E. S. Journal of Wildlife Diseases, Vol. 33, Issue 1 https://doi.org/10.7589/0090-3558-33.1.1	journal	January 1997
Sporadic and familial CJD: classification and characterisation Gambetti, Pierluigi; Kong, Qingzhong; Zou, Wenquan British Medical Bulletin, Vol. 66, Issue 1 https://doi.org/10.1093/bmb/66.1.213	journal	June 2003
Successful transmission of the chronic wasting disease (CWD) agent to white-tailed deer by intravenous blood transfusion Mammadova, Najiba; Cassmann, Eric; Greenlee, Justin J. Research in Veterinary Science, Vol. 133 https://doi.org/10.1016/j.rvsc.2020.10.009	journal	December 2020
Co-existence of scrapie prion protein types 1 and 2 in sporadic Creutzfeldt–Jakob disease: its effect on the phenotype and prion-type characteristics Cali, Ignazio; Castellani, Rudolph; Alshekhlee, Amer Brain, Vol. 132, Issue 10 https://doi.org/10.1093/brain/awp196	journal	September 2009
Preliminary Observations on the Experimental Transmission of Scrapie to Elk (Cervus elaphus nelsoni) by Intracerebral Inoculation Hamir, A. N.; Miller, J. M.; Cutlip, R. C. Veterinary Pathology, Vol. 40, Issue 1 https://doi.org/10.1354/vp.40-1-81	journal	January 2003
Additional Cases of Chronic Wasting Disease in Imported Deer in Korea Kim, Tae-Yung; Shon, Hyun-Joo; Joo, Yi-Seok Journal of Veterinary Medical Science, Vol. 67, Issue 8 https://doi.org/10.1292/jvms.67.753	journal	January 2005
Brain targeting through the autonomous nervous system: lessons from prion diseases Haïk, S. Trends in Molecular Medicine, Vol. 10, Issue 3 https://doi.org/10.1016/j.molmed.2004.01.008	journal	March 2004
Chronic Wasting Disease of Captive mule Deer: a Spongiform Encephalopathy Williams, E. S.; Young, S. Journal of Wildlife Diseases, Vol. 16, Issue 1 https://doi.org/10.7589/0090-3558-16.1.89	journal	January 1980
Rapid Antemortem Detection of CWD Prions in Deer Saliva Henderson, Davin M.; Manca, Matteo; Haley, Nicholas J. PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0074377	journal	September 2013
Incidence and spectrum of sporadic Creutzfeldt–Jakob disease variants with mixed phenotype and co-occurrence of PrPSc types: an updated classification Parchi, Piero; Strammiello, Rosaria; Notari, Silvio Acta Neuropathologica, Vol. 118, Issue 5 https://doi.org/10.1007/s00401-009-0585-1	journal	August 2009
White-tailed deer are susceptible to the agent of sheep scrapie by intracerebral inoculation Greenlee, Justin J.; Smith, Jodi D.; Kunkle, Robert A. Veterinary Research, Vol. 42, Issue 1 https://doi.org/10.1186/1297-9716-42-107	journal	January 2011
Chronic Wasting Disease of Elk: Transmissibility to Humans Examined by Transgenic Mouse Models Kong, Q. Journal of Neuroscience, Vol. 25, Issue 35 https://doi.org/10.1523/JNEUROSCI.2467-05.2005	journal	August 2005
Experimental Transmission of Chronic Wasting Disease (CWD) of Elk (Cervus elaphus nelsoni), White-tailed Deer (Odocoileus virginianus), and Mule Deer (Odocoileus hemionus hemionus) to White-tailed Deer by Intracerebral Route Hamir, A. N.; Richt, J. A.; Miller, J. M. Veterinary Pathology, Vol. 45, Issue 3 https://doi.org/10.1354/vp.45-3-297	journal	May 2008
Genotype by environment interactions for chronic wasting disease in farmed US white-tailed deer Seabury, Christopher M.; Lockwood, Mitchell A.; Nichols, Tracy A. G3 Genes\|Genomes\|Genetics, Vol. 12, Issue 7 https://doi.org/10.1093/g3journal/jkac109	journal	May 2022
Comparison of Two US Sheep Scrapie Isolates Supports Identification as Separate Strains Moore, S. J.; Smith, J. D.; Greenlee, M. H. West Veterinary Pathology, Vol. 53, Issue 6 https://doi.org/10.1177/0300985816629712	journal	July 2016
Coexistence of multiple PrPSc types in individuals with Creutzfeldt-Jakob disease Polymenidou, Magdalini; Stoeck, Katharina; Glatzel, Markus The Lancet Neurology, Vol. 4, Issue 12 https://doi.org/10.1016/S1474-4422(05)70225-8	journal	December 2005
Deer Prion Proteins Modulate the Emergence and Adaptation of Chronic Wasting Disease Strains Duque Velásquez, Camilo; Kim, Chiye; Herbst, Allen Journal of Virology, Vol. 89, Issue 24 https://doi.org/10.1128/JVI.02010-15	journal	December 2015
Transmission of Sheep Scrapie to Elk (Cervus Elaphus Nelsoni) by Intracerebral Inoculation: Final Outcome of the Experiment Hamir, Amir N.; Miller, Janice M.; Cutlip, Randall C. Journal of Veterinary Diagnostic Investigation, Vol. 16, Issue 4 https://doi.org/10.1177/104063870401600410	journal	July 2004

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