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Investigating Enteric Coccidiosis in the Endangered Black-Footed Ferret

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Investigating Enteric Coccidiosis in the Endangered Black-Footed Ferret Investigating Enteric Coccidiosis in the Black-footed (Mustela nigripes) and Domestic Ferret (Mustela putorius furo) by Adriana R. Pastor A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Veterinary Science in Zoological Medicine and Pathology Guelph, Ontario, Canada © Adriana R. Pastor, November, 2017 ABSTRACT INVESTIGATING ENTERIC COCCIDIOSIS IN THE BLACK-FOOTED (MUSTELA NIGRIPES) AND DOMESTIC FERRET (MUSTELA PUTORIUS FURO) Adriana R. Pastor Advisors: University of Guelph, 2017 Dr. D. A. Smith Dr. J. R. Barta Enteric coccidiosis is a major cause of death in both juvenile and adult black-footed ferrets (BFF, Mustela nigripes) in captive breeding programs that reduces the availability of animals for release to their former North American range. Coccidiosis is poorly understood in BFF but in vivo experimental infection in this endangered host is untenable. The goal of this research was to better characterize the etiologic agents and natural history of enteric coccidiosis in BFF and to evaluate the domestic ferret (DF, Mustela putorius furo) as a model for experimental infection. Morphometric and molecular characterization of coccidia from BFF and DF was undertaken. Only Eimeria ictidea was identified in juvenile and adult BFF from 1999-2016 at the Toronto Zoo and from BFF at the Louisville Zoo in 2016. Eimeria furonis and Isospora (=Cystoisospora) laidlawi were identified in DF fecal and necropsy samples from Canadian and European diagnostic laboratories during 2008-2017. Molecular characterization of these parasites included generation of complete mitochondrial genomes and nuclear 18S rDNA sequences for Eimeria ictidea and Eimeria furonis from BFF and DF, respectively. Partial sequences were obtained from the same genetic targets from I. (=C.) laidlawi from DF. DNA isolation from formalin fixed paraffin embedded tissues and PCR amplicon sequencing permitted identification of coccidia in BFF and DF tissues dating from 1999 to present. Retrospective and prospective analyses of medical and pathology records supplemented with parasitological evaluation of repeated fecal samples was performed to determine the natural history of coccidiosis in captive BFF. Clinical signs and histopathologic changes associated with infection in BFF were as described previously in the published literature. Average yearly coccidia associated mortality rates were 0.53% in adults and 1.95% in juveniles. Domestic ferrets were confirmed as experimental hosts of E. ictidea isolated from BFF. Seven of 10 juvenile DF inoculated with oocysts from a BFF developed patent infections and mild clinical disease was observed in six of these seven. Infection was confirmed via morphometric, molecular and histologic examination of samples from infected DF. While much is still unknown about enteric coccidiosis in BFF, domestic ferrets provide a promising model for further investigation of this disease. DEDICATION For my mother, Anna Pastor…. iv ACKNOWLEDGEMENTS It’s hard to believe that my residency and thesis have been completed, and I have a lot of people to thank for that: Dale and Graham, the two people I wanted to be when I grew up, thank you for your mentorship for many years, even before this program. I know that you weren’t convinced that this project was DVSc worthy when I first proposed it, but I’m hoping that the results have changed your mind. I am sincerely grateful to all the members of my advisory committee: Dale Smith, John Barta and Simon Hollamby, for their insight, support and interest in this project. Dale, you have been an exceptional advisor; I don’t know that I will ever get to your level, but thank you for showing me that being a great clinical zoo vet and pathologist are not mutually exclusive. John thank you for spontaneously agreeing to be my advisor when I came to you with this project proposal in my first semester, for your energy and enthusiasm and for supporting my widening interest in parasitology research. My heartfelt appreciation for the Toronto Zoo WHC veterinarians, past and present: Chris Dutton, Pauline Delnatte, Simon Hollamby and Graham Crawshaw. I have learned so much from all of you that I will take forward into my future endeavours. I appreciate the extra time you put in, including comps study sessions, after-hours tête-à-têtes, and the fact that your doors were open when I needed it. For the Toronto Zoo vet techs extraordinaire: Michelle Lovering, Cassia Devison, Dawn Mihailovic and Tasha Long – you have been indispensable during this program and there are not enough words to express my gratitude. I would especially like to thank all the Wildlife Health Center staff (2013-2016): Mark Bongelli, Charles Guthrie, Christine McKenzie, Brian Telford, Rick Vos, Gerri Mintha, Margaret Kolakowski, Andrew Lentini, Rebecca Clark, Lydia Attard, Nigel Parr, Paula Roberts, Andrea Dada, Mindy Waisglass and Julie Digiandomenico, for three very memorable years. It is all of you that make the WHC such an amazing place to be. I’m not sure I have laughed so hard or so often as I did in that lunchroom, and I hope our paths will cross again. v I don’t think that I can truly express how thankful I am to Pathobiology laboratory technicians Julie Cobean and Julia Whale. Without your assistance, patient teaching and friendship, I would probably still be screening fecal samples years from now, and scratching my head as to how our lab protocols actually work. It is people like you who make sure graduate students become successful doctorates, and I can’t imagine Pathobio without you both in it. I would also like to thank my labmates in the Barta lab — Mian Hafeez, Evelyn Rejman, Rachel Imai, Perryn Kruth, Ryan Snyder and Mosun Ogedengbe. A special thank you goes to Alex Leveille, without whom my many adventures in parasitology research, from coccidia to Babesia, would not have been as successful. To all the students who helped with ferret fecal sample processing, data compilation, and necropsies: Nathalie Ferriman, Janessa Price, Thisuri Eagalle, Sarah Brisson thank you so much for your hard work and excitement about my project… even when it was very smelly ! So many thanks to the amazing staff of Central Animal Facility - Linda Groocock, Vicky Carson, Tony Cengija and Mary Fowler for the daily care and enrichment of my experimental ferrets. Your excitement about working with our ferrets and your assistance with all parts of the process helped made this project a success. To Adriana Nielsen, who was not only my better half but the other fifty percent of my brain for several years. It is your friendship, fortitude and our endless phone conversations that got me through the never-ending Toronto-Guelph commute, and this program. To all the “scope room” pathology co-residents past and present - thank you for being wonderful friends and colleagues. It is indeed rare to find so many amazing people in one place, and I know this program and my sanity would not have been the same without you. To the anatomic pathology faculty and senior graduate students - thank you for all the time, teaching and guidance you provided during my program. While I can’t say that I have become an amazing pathologist, I can say that because of your mentorship I am a better diagnostician and the type of clinician who asks better questions, takes better samples and understands that you can’t “just make a PCR for that”. vi A special thank you to Tony van Dreumel who came out of retirement for a semester to try to teach the Adrianas zoo pathology, screening cases with you was always a pleasure. To all the lovely Histo Ladies, P.M. room staff and the other AHL staff who helped me with Toronto Zoo and HSC pathology cases along the way - I don’t think the anatomic path students could survive without you. Thank you for always smiling, assisting and accommodating me, even when I made near-impossible processing requests during my weekly Guelph visits. I would also like to acknowledge and sincerely thank all the individuals who helped with resource and sample acquisition for this project. A special mention for those who went above and beyond because of their interest in this project: Don Duszynski who was instrumental in acquiring, and then providing a translator for many of the original mustelid Eimeria descriptions; and Majda Globokar, Nikola Pantchev, and Donald Martin who supplied my domestic ferret fecal samples and historical data. A shout-out to Julie Swenson, Gary West and the Phoenix Zoo BFF team who fostered my love of this endangered species and helped develop the idea for this project. As always, I continue to go out into the world and pursue my dreams with the knowledge that I have the support of my incredible family, long-time friends, and my partner Keith Morris. I am so lucky that my residency brought me home, and that it afforded us all more time spent together. For my aunt, Veronica Lacey, who has never failed to believe in my potential and always pushed me to become an academic – you’ll never get that PhD from me but I think this is pretty close! Finally, for my mother, Anna Pastor, who never lived to see my greatest achievements but had absolute faith that I could reach any goal I worked towards…. this is for you. Finally, none of this would have been possible without the generous support of the Toronto Zoo Residency program and funding through the Barta Laboratory, University of Guelph. Adriana Pastor Toronto, August 2017 vii DECLARATION OF WORK PERFORMED I declare that all the work reported in this thesis was performed by myself, with the following exceptions: Fecal samples were collected by personnel at the Toronto Zoo, Louisville Zoo and participating diagnostic laboratories.
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