RESEARCH IN THE CLASSICAL PARASITOLOGY SECTION OF THE DEPARTMENT OF VETERINARY SCIENCE, UNIVERSITY OF KENTUCKY, LEXINGTON, KENTUCKY, USA

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1 RESEARCH IN THE CLASSICAL PARASITOLOGY SECTION OF THE DEPARTMENT OF VETERINARY SCIENCE, UNIVERSITY OF KENTUCKY, LEXINGTON, KENTUCKY, USA E.T. LYONS 1, SHARON C. TOLLIVER 1, SANDRA S. COLLINS 1, S. MORARIU 2 1 Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky ; 2 Faculty of Veterinary Medicine, Calea Aradului 119, Timisoara , Romania Summary This paper describes the research activities of the classical Parasitology section of the Department of Veterinary Science, University of Kentucky, Gluck Equine Research Center, Lexington, Kentucky, USA, over a more than 50 year period. Pioneer research has been conducted on resistance phenomenon against equine small strongyles, sheep stomach worms and equine ascarids. New targets are determining which cyathostomin species are the most resistant to the newest anthelmintic drugs, and what the course of the therapy is. But the paper also describes the wide and important research on endoparasites in otariid pinnipeds conducted by Professor Eugene Lyons and his colleagues in Alaska and California. This paper also presents some of the important publications of the Parasitology section. The Maxwell H. Gluck Center from University of Kentucky, Lexington, has received international recognition for its research dedicated to improving the health and welfare of horses. It is the most important research center on horse problems from all over the world, located in Lexington who s known as The capital of horses. The Maxwell H. Gluck Equine Research Center is only one of the divisions comprising the Department of Veterinary Science. The others are the Livestock Disease Diagnostic Center and the Equine Parentage Testing and Research Laboratory (Figure 1). Fig.1. The Maxwell H. Gluck Center from University of Kentucky, Lexington 473

2 The Department of Veterinary Science offers the Master of Science and the Doctor of Philosophy degrees in Veterinary Science with specialization in pathology, virology, microbiology, parasitology, immunology, immunogenetics, reproductive physiology, and pharmacology with emphasis on the horse. There are important correlations on the entire departments of the Research Centers all over the USA concerning horse health (Figure 2). Fig.2. Network diagram offering a new state-wide horse health information all over the USA, and, also, worldwide Important viral (equine arteritis, equine influenza, equine infectious anemia, equine herpes including the abortion, paralytic and respiratory forms), bacterial (such as the causative agent of strangles) and parasitic (strongyles, tapeworms, and the protozoan responsible for neurological condition equine protozoal myeloencephalitis) microorganisms are being investigated by the Infectious Diseases group. In addition to laboratory-based studies, the incidence of infectious diseases in horses throughout the country is closely monitored and studies are 474

3 conducted to assist horse owners (also from abroad) and veterinarians manage severe outbreaks including those caused by bioterrorism. Here are the most important researchers from the Infectious Diseases group: George P. Allen, Sergey C. Artiushin, Udeni B. R. Balasuriya, Thomas M. Chambers, R. Frank Cook, Roberta M. Dwyer, Daniel K. Howe, Charles J. Issel, Eugene T. Lyons, David G. Powell, John F. Timoney and Peter J. Timoney, respectively. These investigations are complimented by the Immunology group who are characterizing immune responses of the horse at the molecular level. Scientists in Reproductive Physiology study environmental and biochemical factors affecting pregnancy in mares. Arthritis and related joint injuries that frequently limit athletic performance in horses is being studied by the musculoskeletal group. Medications, toxic compounds, and problems associated with detection of performance enhancing drugs are the focus of the Pharmacology, Therapeutics, and Toxicology group. Scientists in the Immunogenetics and Genomics group investigate the organization of genes on equine chromosomes and work to identify genetic determinants of important inherited traits in horses. Members of this group are also active participants in the international collaborative effort to sequence the entire horse genome. After this introduction, research is presented for the Classical Parasitology section of the Department of Veterinary Science, University of Kentucky, Gluck Equine Research Center, Lexington, Kentucky, USA, which continues in the direction started over 50 years ago. That is, to do research on the control and transmission of internal parasites of domestic animals, especially horses. Prominent personalities dedicate their entire life to the progress of Parasitologic sciences, such as Prof. H.J. Drudge (deceased) (Figure 3 left), Prof. E.T. Lyons or Sharon C. Tolliver (Figure 3 right). Figure 3. Prof. H.J. Drudge (left) and Prof. E.T. Lyons with Sharon C. Tolliver in the lab (right). 475

4 Virtually all drugs on the market for removing nematodes, tapeworms and bots (insects) were tested here as independent evaluators of the efficacy of these compounds on internal parasites of horses. This research usually was done before the compounds were marketed. Results were sent to drug companies which submitted the data to the Food and Drug administration for either verification of activity or lack of activity against specific parasite species. Then these data were published in scientific journals and in bulletins to provide scientists and animal owners with information about the effectiveness of the various compounds on internal parasites. Pioneer research has been on drug resistant parasites in horses and sheep and orientated towards multi-year study for instance on equine small strongyles which are resistant to most of the commercially available parasiticides. The first discovery of drug resistant nematodes was at the University of Kentucky and that was finding resistance of the sheep stomach worm, Haemonchus contortus, to phenothiazine. Recent research here was in the termination of a 40- year study of a population (B) of drug-resistant small strongyles in horses. Initially they were resistant to phenothiazine, then to thiabendazole, and finally to piperazine and pyrantel pamoate. It was found that even though horses with this population of small strongyles were not treated with any compound for about 22 years, the resistance to thiabendazole was still evident. In other words, after the several years of no treatment, the parasites did not revert back to susceptibility to thiabendazole. Research in the last few years has focused on determining, in field tests, the status of drug resistance of small strongyles and ascarids (Parascaris equorum) in horses on commercial farms to compounds on the market. This research verified that of others showing that small strongyle eggs per gram of feces (EPG counts) are returning much quicker after macrocyclic lactone (ivermectin) treatment than occurred when this class of compounds first was marketed. Also it was found that ivermectin is inactive on ascarids, a finding by researchers in many parts of the world. In ranking of activity of compounds with label claims against ascarids, oxibendazole and fenbendazole were the most efficacious, and pyrantel pamoate and ivermectin the least effective. Transmission of equine parasites also is an important aspect of research. The purposes of these studies are to follow the changes of prevalence due to use of parasiticides, to determine the treatment regimen necessary to control parasites and to determine whether the compounds are as efficacious as they were when they first came on the market. Visits of parasitologist teachers/scientists to the University of Kentucky have resulted in mutual benefits for them and their host colleagues in sharing of knowledge, interactive research, and friendship. Some recent visitors were drs. Jane Hodgkinson from England, Martin Nielsen from Denmark, and three from Romania: Mariana IoniŃa, Gabriela Predescu and Sorin Morariu. 476

5 Besides research on endoparasites of domestic animals, there have been extensive studies on parasites, especially hookworms, in otariid pinnipeds. The hosts include northern fur seals, California sea lions, and Steller sea lions. There is a cross over of value of studies on parasites in one host to another host. For instance it was found that there is transmammary transmission of hookworms from northern fur seal cows to their pups. This was the first proven transmission of nematode larvae through the milk of the mother and maturation in her offspring. From this research, it was found that this manner of transmission of parasites occurs in many animals including the tiny nematode, Strongyloides westeri, in horses. Following this presentation are references demonstrating some of the research: References 1. Lyons, E.T., Tolliver, S.C., Drudge, J.H. - Historical perspective of cyathostomes: prevalence, treatment and control programs. Vet. Parasitol., 85: , Tolliver, S.C. (Photographs by E.T. Lyons) - A Practical Method of Identification of North American Cyathostomes (Small Strongyles) in Equids in Kentucky. Univ. Ky. Ag. Exp. Sta. Bull. No. SR , Monograph, 37 pp., Lyons, E.T., Spraker, T.R., Olson, K.D., Tolliver, S.C. Bair, H.D. - Prevalence of hookworms (Uncinaria lucasi Stiles) in northern fur seal (Callorhinus ursinus Linnaeus) pups on St. Paul Island, Alaska, U.S.A.: Comp. Parasitol., 67: , Bair, H.D., Lyons, E.T., Swerczek, T.W., Tolliver, S.C. - Atypical specimens of helminth parasites (Anoplocephala perfoliata and Thelazia lacrymalis) of horses in Kentucky, U.S.A. Comp. Parasitol., 67: , Lyons, E.T., Swerczek, T.W., Tolliver, S.C., Bair, H.D., Drudge, J.H., Ennis, L.E. -Prevalence of selected species of internal parasites in equids at necropsy in central Kentucky ( ). Vet. Parasitol., 92: 51-62, Nadler, S.A., Adams, B.J., Lyons, E.T., Delong, R.L., Melin, S.R. - Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions and northern fur seals: Hypothesis testing supplants verification. J. Parasitol., 86: , Lyons, E.T., Delong, R.L., Gulland, F.M., Melin, S.R., Tolliver, S.C., Spraker, T.R. - Comparative biology of Uncinaria spp. in the California sea lion (Zalophus californianus) and the northern fur seal (Callorhinus ursinus) in California. J. Parasitol. 86: , Lyons, E.T., Drudge, J.H. Tolliver, S.C. - Larval Cyathostomiasis. Vet. Clin. N. Amer.: Equine Pract. 16: ,

6 9. Lyons, E.T., Tolliver, S.C., Drudge, J.H., Collins, S.S., Swerczek, T.W. - Continuance of studies on Population S benzimidazole-resistant small strongyles in Shetland pony herd in Kentucky: effect of pyrantel pamoate ( ). Vet. Parasitol., 94: , Lyons, E.T., Tolliver, S.C., Collins, S.S., Drudge, J.H. - Transmission of endoparasites in horse foals on the same pasture on a farm in central Kentucky ( ). Vet. Parasitol., 97: , Lyons, E.T., Melin, S.R., Delong, R.L., Orr, A.J., Gulland, F.M., Tolliver, S.C. -Current prevalence of adult Uncinaria spp. in northern fur seal (Callorhinus ursinus) and California sea lion (Zalophus californianus) pups on San Miguel Island, California, with notes on the biology of these hookworms. Vet. Parasitol. 97: , Lyons, E.T. - Habronemiasis of horse. In Service, M. W. (ed): Encyclopedia of Arthropod-transmitted Infections of Man and Domestic Animals, CABI Publishing, New York, pp , Duncan, J.L., Abbott, E.M., Arundel, J.H., Eysker, M., Klei, T.R., Krecek, R.C., Lyons, E.T., Reinemeyer, C., Slocombe, J.O.D. - World Association for the Advancement of Veterinary Parasitology (WAAVP): Second edition of guidelines for evaluating the efficacy of equine anthelmintics. Vet. Parasitol., 103:1-18, Lyons, E.T., Swerczek, T.W., Tolliver, S.C. - Parasitologic examination of the eyes, esophagus, lungs, rumen, and feces of cattle and small intestine of horses at necropsy in central Kentucky in 2000 and Compar. Parasitol., 70:55-59, Lyons, E.T., DeLong, R.L., Spraker, T.R., Melin, S.R., Tolliver, S.C. - Observations in 2001 on hookworms (Uncinaria spp.) in otariid pinnipeds. Parasitol. Res., 89: , Spraker, T.R., Lyons, E.T., Tolliver, S.C. - Ascaridoid nematodes and associated lesions in stomachs of subadult male northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska: ( ). J. Vet. Diagn. Invest. 15: , Lyons, E.T., Tolliver, S.C. - Field test data on small strongyles in evaluation of activity of fenbendazole given once a day for 5 consecutive days to thoroughbred yearlings on two farms in Kentucky in 2002 and Parasitol. Res., 91: , Lyons, Eugene - Population-S benzimidazole- and tetrahydropyrimidineresistant small strongyles in a pony herd in Kentucky ( ): effects of anthelminitc treatment on the parasites as determined in critical tests. Parasitol. Res., 91: , Lyons, E.T., AND Tolliver, S.C. - Prevalence of parasite eggs (Strongyloides westeri, Parascaris equorum, and strongyles) and oocysts (Eimeria leuckarti) in the feces of Thoroughbred foals on 14 farms in central Kentucky in Parasitol. Res., 92: ,

7 20. Spraker, T.R., Lyon, E.T., Delong, R.L., AND Zink, R.R. - Penetration of the small intestine of a California sea lion (Zalophus californianus) pup by adult hookworms (Uncinaria spp). Parasitol. Res., 92: , Kaplan, Ray M., Klei, Tom R., Lyons, Eugene T., Lester, Guy, Courtney, Charles H., French, Dennis D., Tolliver, Sharon C., Vidyashankar, Anand, N., AND Zhao, Ying. -Prevalence of Anthelmintic resistant cyathostomes on horse farms. JAVMA, 225: , Lyons, E.T., AND Delong, R.L. - Photomicrographic images of some features of Uncinaria spp (Nematoda: Ancylostomatidae) from otariid pinnipeds. Parasitol. Res., 95: , Lyons, E.T. - Historic importance of some aspects of research by O. Wilford Olsen on hookworms (Uncinaria lucasi) in northern fur seals (Callorhinus ursinus) and Steller sea lions (Eumatopias jubatus) in 1951 on St. Paul Island, Alaska. Parasitol. Res., 95: , Tandon, R., Lyons, E.T., Tolliver, S.C., AND Kaplan, R.M. - Effect of moxidectin selection on the genetic variation within Cylicocyclus nassatus based on amplified fragment length polymorphism (AFLP). Int. J. Parasitol., 35: , Lyons, E.T., Delong, R.L., Spraker, T.R., Melin, S.R., Laake, J.L., AND Tolliver, S.C. - Seasonal prevalence and intensity of hookworms (Uncinaria spp.) in California sea lion (Zalophus californinus) pups born in 2002 on San Miguel Island, California. Parasitol. Res., 96: , Acevedo-Whitehouse, K, SPRAKER, T.R., LYONS, E.T., Melin, S.R., Gulland, F., Delong, R.L., AND Amos, W. - Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Molecular Ecology, 15: , Castinel, A., Duignan, P.J., Pomroy, W.E., Lyons, E.T., Nadler, S.A., Dailey, M.D., Wilkinson, L.S., AND Chilvers, B.L. - First report and characterization of adult Uncinaria spp. in New Zealand sea lion (Phocarctos hookeri) pups from the Auckland Islands, New Zealand. Parasitol. Res., 98: , Lyons, E.T., Tolliver, S.C., AND Collins, S.S. - Field studies on endoparasites of Thoroughbred foals on seven farms in central Kentucky in Parasitol. Res., 98: , Lyons, E.T., Tolliver, S.C., Collins, S.S. - Prevalence of large endoparasites at necropsy in horses infected with Population B small strongyles in a herd established in Kentucky in Parasitol. Res., 99: , Bryant, U.K., Lyons, E.T., Bain, F.T., Hong, C.B. - Halicephalobus gingivalis-associated meningoencephalitis in a Thoroughbred foal. J. Vet. Diag. Invest., 18: , Lyons, E.T., TOLLIVER. S.C., RATHGEBER, R.A., COLLINS, S.S. - Parasite field study in central Kentucky on Thoroughbred foals (born in 2004) 479

8 treated with pyrantel tartrate daily and other parasiticides periodically. Parasitol. Res., 100: , Castinel, A., Duignan, P.J., Lyons, E.T., Pomroy, W.E., Lopez- Villalobos, N., Wilkinson, L.S., Chilvers, B.L., Gibbs, N. - Epidemiology of hookworm (Uncinaria spp) infection n New Zealand (Hooker s) Sea Lions (Phocarctos hookeri) pups on Enderby Island, Auckland Islands (New Zealand) during the breeding seasons from 1999/2000 to 2004/2005. Parasitol. Res., 101: 53-62, Spraker, T.R., Delong, R.L., Melin, S.R., Lyons, E.T. - Hookworm enteritis with bacteremia in California sea lion pups on San Miguel Island. J. Wildlife Dis., 43: , Lyons, E.T., Tolliver, S.C., Collins, S.S. - Study (1991 to 2001) of drugresistant Population B small strongyles in critical tests in horses in Kentucky at the termination of a 40-year investigation. Parasitol. Res., 101: ,