Gene Lyons Historic Parasitology Herds
Gene Lyons Historic Parasitology Herds
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Martin K. Nielson
DVM, PhD, DipEVPC, DipACVM

Gluck Equine Research Center, Department of Veterinary Science Lexington, KY 40546-0099

859-218-1103

martin.nielsen@uky.edu

Research Outcomes

Research Outcomes

horses on farm

Four decades of research with these herds have led to numerous publications reporting the following results:

  • Epidemiology of important equine parasites. Impact of age, seasonality and immunity.
  • Documentation of how parasites responded to typical deworming schedules by becoming multi-drug resistant.
  • Documentation of how drug resistance does not disappear once it has developed, regardless of whether the horses are dewormed or not.
  • Development of new diagnostic methods for detection of important equine parasites, including a blood test for bloodworms, and ultrasound method for ascarids, and a smartphone-based automated egg counting system.
  • Evaluation of novel deworming programs, such as various forms of combination-deworming.
  • Molecular studies of mechanisms behind drug resistance.

Complete Reference List:

  1. Lyons, E.T., Drudge, J.H., Tolliver, S.C., 1973.  On the life cycle of Strongyloides westeri in the equine.  J. Parasitol. 59, 780-787.
  2. Lyons, E. T., J. H. Drudge and S. C. Tolliver. Thelazia lacrymalis in Horses in Kentucky and Observations on the Face Fly (Musca autumnalis) as a Possible Intermediate Host.  J. Parasitol. 62(6): 877-880.
  3. Lyons, E. T., J. H. Drudge, and S. C. Tolliver. Experimental Infections of Thelazia lacrymalis: Maturation of Third-Stage Larvae from Face Flies (Musca autumnalis) in Eyes of Ponies. J. Parasitol. 66(1): 181-182.
  4. Newby, T. J., D. H. Bliss, R. A. Magonigle, T. R. Bello, J. H. Drudge, and E. T. Lyons. Field Test Evaluation of Pyrantel Pamoate Against Strongyle Infections in Horses. Equine Pract. 4(4): 26-34, April, 1982.
  5. Drudge, J. H., E. T. Lyons, S. C. Tolliver, and J. E. Kubis. Pyrantel in Horses: Clinical Trials with Emphasis on a Paste Formulation and Activity on Benzimidazole Resistant Small Strongyles. VM/SAC 77(6): 957-967, June, 1982.
  6. Lyons, E. T., S. C. Tolliver, J. H. Drudge, 1983. Critical tests in equids with fenbendazole alone or combined with piperazine: Particular reference to activity on benzimidazole resistant small strongyles. Vet. Parasitol. 12, 91-98.
  7. Drudge, J. H., E. T. Lyons, T. W. Swerczek, S. C. Tolliver, 1983. Cambendazole for strongyle control in a pony band: Selection of a drug-resistant population of small strongyles and teratologic implications. Am. J. Vet. Res. 44, 110-114.
  8. Drudge, J. H., E. T. Lyons, S. C. Tolliver, T. W. Swerczek, 1985. Use of oxibendazole for control of cambendazole-resistant small strongyles in a band of ponies: A six year study. Am. J. Vet. Res. 46, 2507-2511.
  9. Lyons, E. T., J. H. Drudge, S. C. Tolliver, 1986. Fenbendazole in equids: further controlled tests with emphasis on activity of multiple doses against naturally occurring infections of migratory large strongyles. Am. J. Vet. Res. 47, 317-321.
  10. Lyons, E .T., J. H. Drudge, and S. C. Tolliver. Natural Infection with Eimeria leuckarti: Prevalence of Oocysts in Feces of Horse Foals on Several Farms in Kentucky During 1986. Am. J. Vet. Res. 49(1):96-98, 1988.
  11. Lyons, E. T., J. H. Drudge, and S. C. Tolliver. Prevalence of Some Internal Parasites Found (1971-1989) in Horses Born on a Farm in Central Kentucky. Eq. Vet. Sci. 10(2):99-107, 1990.
  12. Lyons, Eugene T., Sharon C. Tolliver, J. Harold Drudge, David E. Granstrom, Shelby Stamper, and Sandra S. Collins. Transmission of Some Internal Parasites in Horses Born in 1989 on a Farm in Central Kentucky. J. Helm. Soc. Wash. 58(2):213-219, 1991.
  13. Lyons, Eugene T., Sharon C. Tolliver and Shelby Stamper.  Observations on the Common Horse Bot (Gasterophilus intestinalis) (Diptera: Gasterophilidae): Incomplete Molting of a Second Instar Specimen.  Trans. Ky Acad. Sci. 53(1-2): 19-25, 1992.
  14. Lyons, Eugene T., Sharon C. Tolliver, J. Harold Drudge, David E. Granstrom, and Sandra S. Collins. Natural Infections of Strongyloides westeri: Prevalence in Horse Foals on Several Farms in Central Kentucky in 1992. Vet. Parasit. 50:101-107, 1993.
  15. Lyons, E. T., J. H. Drudge, S. C. Tolliver, T. W. Swerczek, S. Stamper, and D. E. Granstrom. Control of Cambendazole-Resistant Small Strongyles (Population S) with Oxibendazole in a Pony Band: An 8 Year Field Test (1984-1992). Vet. Parasit. 52:271-277, l 994.
  16. Lyons, E. T., S. C. Tolliver, S. Stamper, J. H. Drudge, D. E. Granstrom, and S. S. Collins. Transmission of Some Species of Internal Parasites in Horses Born in 1990, 1991, and 1992 in the Same Pasture on a Farm in Central Kentucky. Vet. Parasit. 52:257-269, 1994.
  17. Lyons, Eugene T., Thomas W. Swerczek, Sharon C. Tolliver, J. Harold Drudge, Shelby Stamper, David E. Granstrom, and Robert E. Holland. A Study of Natural Infections of Encysted Small Strongyles in a Horse Herd in Kentucky. Vet. Med. 89:1146-1149; 1152-1155, 1994.
  18. Lyons, E.T., Tolliver, S.C., Drudge, J.H., Stamper, S., Swerczek, T.W., Granstrom, D.E., 1996.  Critical test evaluation (1977-1992) of drug efficacy against endoparasites featuring benzimidazole-resistant small strongyles (Population S) in Shetland ponies.  Vet. Parasitol. 66, 67-73.
  19. Lyons, E.T., Tolliver, S.C., Drudge, J.H., Stamper, S., Swerczek, T.W., and Granstrom, D.E.  A Study (1977-1992) of Population Dynamics of Endoparasites Featuring Benzimidazole-Resistant Small Strongyles (Population S) in Shetland Ponies.  Vet. Parasitol. 66: 75-86, 1996.
  20. Lyons, E.T., Tolliver, S.C., Collins, S.S., Drudge, J.H., and Granstrom, D.E.  Transmission of Some Species of Internal Parasites in Horses Born in 1993, 1994, and 1995 on the Same Pasture on a Farm in Central Kentucky.  Vet. Parasitol. 70: 225-240, 1997.
  21. Lyons, E.T., Tolliver, S.C., Drudge, J.H., Collins, S.S. and Swerczek, T.W.  Continuance of studies on Population S benzimidazole-resistant small strongyles in Shetland pony herd in Kentucky: effect of pyrantel pamoate (1992-1999).  Vet. Parasitol. 94: 247-256, 2001.
  22. Lyons, E.T., Tolliver, S.C., Collins, S.S., and Drudge, J.H.  Transmission of endoparasites in horse foals on the same pasture on a farm in central Kentucky (1996-1999).  Vet. Parasitol. 97: 113-121, 2001.
  23. Lyons, Eugene.  Population-S benzimidazole- and tetrahydropyrimidine-resistant small strongyles in a pony herd in Kentucky (1977-1999): effects of anthelmintic treatment on the parasites as determined in critical tests.  Parasitol. Res. 91:407-411, 2003.
  24. Tandon, R., Kaplan, R.M., 2004. Evaluation of a larval development assay (DrenchRite) for the detection of anthelmintic resistance in cyathostomin nematodes of horses. Vet. Parasitol. 121, 125-142
  25. Tandon, R., Lyons, E. T., Tolliver, S. C., 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: 813-819, 2005.
  26. Nielsen, M.K., Baptiste, K.E., Tolliver, S.C., Collins, S.S., Lyons, E.T.  Analysis of multiyear studies in horses in Kentucky to ascertain whether counts of eggs and larvae per gram of feces are reliable indicators of numbers of strongyles and ascarids present.  Veterinary Parasitology 174, 77-84, 2010.
  27. Kuzmina, T.A., Tolliver, S.C., Lyons, E.T.  Three recently recognized species of cyathostomes (Nematoda: Strongylidae) in equids in Kentucky.  Parasitology Research 108, 1179-1184, 2011.
  28. Lyons, E.T., Kuzmina, T.A., Tolliver, S.C., Collins, S.S.  Observations on development of natural infection and species composition of small strongyles in young equids in Kentucky.  Parasitology Research 109, 1529-1535, 2011.
  29. Kuzmina, T.A., E. T. Lyons, S. C. Tolliver, I.I. Dzeverin, V.A. Kharchenko, 2012.  Fecundity of various species of strongylids (Nematoda: Strongylidae) – parasites of domestic horses. Parasitol. Res. 111, 2265-2271.
  30. Tyden E, Morrison DA, Engstrom A., Nielsen MK, Eydal E, Hoglund J. Population genetics of Parascaris equorum based on whole genome DNA fingerprinting. Infection, Genetics and Evolution 2013, 13, 236-241.
  31. Andersen UV, Howe DK, Dangoudoubiyam S, Toft N, Reinemeyer CR, Lyons ET, Olsen SN, Monrad J, Nejsum P, Nielsen MK. rSvSXP: A Strongylus vulgaris antigen with potential for prepatent diagnosis. Parasites & Vectors 2013, 6: 84.
  32. Nielsen MK, Betancourt A, Lyons ET, Horohov DW, Jacobsen S. Characterization of the inflammatory response to anthelmintic treatment in ponies naturally infected with cyathostomin parasites. Veterinary Journal 2013, 198, 457-462.
  33. Nielsen MK, Vidyashankar AN, Gravatte HS, Bellaw J, Lyons ET, Andersen UV. Development of Strongylus vulgaris-specific serum antibodies in naturally infected foals. Veterinary Parasitology 2014, 200, 233-304.
  34. Nielsen MK, Wang J, Davis R, Bellaw JL, Lyons ET, Lear TL, Goday C. Parascaris univalens – a victim of large-scale misidentification? Parasitology Research 2014, 113, 4485-4490.
  35. Bellaw JL, Nielsen MK. Evaluation of Baermann apparatus sedimentation time on recovery of Strongylus vulgaris and S. edentatus third stage larvae from equine coprocultures. Veterinary Parasitology 2015, 211, 99-101.
  36. Tolliver SC, Lyons ET, Nielsen MK, Bellaw J. Transmission of some species of internal parasites in horse foals born in 2013 in the same pasture on a farm in Central Kentucky. Helminthologia 2015, 52 (3), 211-218.
  37. Donoghue EM, Lyons ET, Bellaw JL, Nielsen MK, 2015. Biphasic appearance of corticated and decorticated ascarid egg shedding in untreated horse foals. Veterinary Parasitology, 2015, 214, 114-117.
  38. Nielsen MK, Donoghue EM, Stephens ML, Stowe CJ, Donecker JM, Fenger CK. An ultrasonographic scoring method for transabdominal monitoring of ascarid burdens in foals. Equine Veterinary Journal 2016, 48, 380-386.
  39. Slusarewicz P, Pagano S, Mills C, Popa G, Chow M, Mendenhall M, Rodgers DW, Nielsen MK. Automated parasite fecal egg counting using fluorescence labeling, smartphone image capture and computational image analysis. International Journal for Parasitology 2016 46, 485-493.
  40. Fabiani JV, Lyons ET, Nielsen MK. Dynamics of Parascaris and Strongylus spp. parasites in untreated juvenile horses. Veterinary Parasitology 2016, 30, 62-66.
  41. Nielsen MK, Lyons ET. Encysted cyathostomin larvae in foals - progression of stages and the effect of seasonality. Veterinary Parasitology 2017, 236, 108-112.
  42. Noel ML, Scare JA, Bellaw JL, Nielsen MK. Accuracy and precision of Mini-FLOTAC and McMaster techniques for determining equine strongyle egg counts. Journal of Equine Veterinary Science 2017, 48, 182-187.
  43. Pihl T, Nielsen MK, Jacobsen S. Changes in hemostatic indices in foals naturally infected with Strongylus vulgaris. J. Equine Vet. Sci. 2017, 54, 1-7.
  44. Scare J.A., Slusarewicz P., Noel M.L., Wielgus K.M., Nielsen M.K. Evaluation of accuracy and precision of a smartphone based automated parasite egg counting system in comparison to the McMaster and Mini-FLOTAC method. Veterinary Parasitology 2017, 247, 85-92.
  45. Miller, F.L., Bellaw, J.L., Lyons, E.T., Nielsen, M.K. Strongyloides westeri worm and egg counts in naturally infected young horses. Veterinary Parasitology 2017, 15, 1-3.
  46. Wang, J., Gao, S., Mostovoy, Y., Kang, Y., Zagoskin, M., Sun, Y., Zhang,  B., White, L.K.,  Easton, A., Nutman, T.B., Kwok, P.-Y.,  Hu, S.,  Nielsen, M.K., Davis, R.E. Comparative genome analysis of programmed DNA elimination in nematodes. Genome Research 2017, 27(12), 1-14.
  47. Scare, J.A., Lyons, E.T., Wielgus, K.M., Nielsen, M.K. Combination deworming for the control of double-resistant cyathostomin parasites – short and long term consequences. Veterinary Parasitology 2018, 251, 112-118.
  48. Hu, Y., Miller, M., Zhang, B., Nguyen, T.-T., Nielsen, M.K., Aroian, R.V. In vivo and in vitro studies of Cry5B and nicotinic acetylcholine receptor agonist anthelmintics reveal a powerful and unique combination therapy against intestinal nematode parasites. PLoS Neglected Tropical Diseases 2018, 12(5), e0006506.
  49. Janečka, J., Davis, B., Ghosh, S., Paria, N., Das, P., Orlando, L., Schubert, M., Nielsen, M.K., Stout, T., Brashear, W., Li, G., Johnson, C., Metz, R., Al Zadjali, A.M., Love, C., Varner, D., Bellott, D., Murphy, W., Chowdhary, B., Raudsepp, T. Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes. Nature Communications 2018, 9, 2945.
  50. Norris, J.K., Steuer, A.E., Slusarewicz, P., Scare, J.A., Bellaw, J.L., Nielsen, M.K. Determination of the specific gravity of eggs of equine strongylids, Parascaris spp., and Anoplocephala perfoliata. Veterinary Parasitology 2018, 260, 45-48.
  51. Went, H.A., Scare, J.A., Steuer, A.E., Nielsen, M.K. Effects of homogenizing methods on accuracy and precision of equine strongylid egg counts. Veterinary Parasitology 2018, 261, 91-95.
  52. Scare, J.A., Steuer A.E., Shaffer C.L., Slusarewicz P., Mousley A., Nielsen M.K. Long live the worms: Methods for maintaining and assessing the viability of intestinal stages of Parascaris spp. in vitro. Parasitology 2019, 146, 685-693.
  53. Zynda, H., Scare, J.A., Steuer, A.E., Anderson, H.P., Nielsen, M.K. Encysted cyathostomin larval counts: Mucosal digestion revisited. Veterinary Parasitology 2019, 273, 86-89.
  54. Norris, J.K., Slusarewicz, P., Nielsen, M.K. Pixel by pixel: Real-time observation and quantification of passive flotation speeds of three common equine endoparasite egg types. International Journal for Parasitology 2019, 49, 885-892.
  55. Slusarewicz, M., Slusarewicz, P., Nielsen, M.K. The effect of counting duration on quantitative fecal egg count test performance. Veterinary Parasitology X 2019, 2, 100020.
  56. Scare, J.A., Leathwick, D.M., Sauermann, C.W., Lyons, E.T., Steuer, A.E., Jones, B.A., Clark, M., Nielsen, M.K. Dealing with double trouble: Combination deworming against double-drug resistant cyathostomins. International Journal for Parasitology: Drugs and Drug Resistance 2020, 12, 28-34.
  57. Scare, J.A., Dini, P., Norris, J.K., Steuer, A.E., Scoggin, K., Gravatte, H.S., Howe, D.K., Slusarewicz, P., Nielsen, M.K. Ascarids exposed: a method for in vitro drug exposure and gene expression analysis of anthelmintic naïve Parascaris spp. Parasitology 2020, 147, 659-666.
  58. Gerhard, A.P., Krücken, J., Heitlinger, E., Janssen, I.J.I., Basiaga, M., Kornas, S., Beier, C., Nielsen, M.K., Davis, R.E., Wang, J., Samson-Himmelstjerna, G.v. The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens. Scientific Reports 2020, 10, 13586.
  59. Cain, J.L., Slusarewicz, P., Rutledge, M.H., McVey, M.R., Wielgus, K.M., Zynda, H.M., Wehling, L.M., Scare, J.A., Steuer, A.E., Nielsen, M.K. Diagnostic performance of McMaster, Wisconsin, and automated egg counting techniques for enumeration of equine strongyle eggs in fecal samples. Veterinary Parasitology 2020, 284, 109199.
  60. Poissant, J., Gavriliuc, S., Bellaw, J., Redman, E.M., Avramenko, R.W., Robinson, D., Workentine, M.L., Shury, T.K, Jenkins, E.J., McLoughlin, P.D., Nielsen, M.K., Gilleard, J.S. A repeatable and quantitative DNA metabarcoding assay to characterize mixed strongyle infections in horses. International Journal for Parasitology 2021, 51, 183–192.
  61. Reed, K.J., Kunz, I.G.Z., Scare, J.A., Nielsen, M.K., Turk, P.J., Coleman, R.J., Coleman, S.J. The pelvic flexure separates distinct microbial communities in the equine hindgut. Scientific Reports 2021, 11, 4332.
  62. Cain, J.L., Peters, K.T., Suri, P., Roher, A., Rutledge, M.H., Nielsen, M.K. The effect of analyst training on fecal egg counting variability. Parasitology Research 2021, 120, 1363-1370.
  63. Urban, Jr., J.F., Nielsen, M.K., Gazzola, D., Xie, Y., Beshah, E., Hu, Y., Li, H., Rus, F., Flanagan, K., Draper, A., Vakalapudi, S., Li, R., Ostroff, G.R., Aroian, R.V. An inactivated bacterium (paraprobiotic) expressing Bacillus thuringiensis Cry5B as a therapeutic for Ascaris and Parascaris spp. infections in large animals. One Health 2021, 12, 100241.  
  64. Soto, E.R., Rus, F., Li, H., Garceau, C., Chicca, J., Elfawal, M., Gazzola, D., Nielsen, M.K., Urban Jr, J.F., Aroian, R.V., Ostroff, G.R. Yeast particle encapsulation of scaffolded terpene compounds for controlled terpene release. Foods 2021, 10(6), 1207.
  65. Nielsen, M.K., Facison, C., Scare, J.A., Martin, A.N., Gravatte, H.S., Steuer, A.E. Diagnosing Strongylus vulgaris in pooled fecal samples. Veterinary Parasitology 2021, 296, 109494.
  66. Nielsen, M.K., Doran, D., Slusarewicz, P. Effects of sample homogenizing on the performance of an automated strongylid egg counting system. Veterinary Parasitology 2021, 300, 109623.
  67. Steuer, A.E., Anderson, H.P., Shepherd, T., Clark, M., Scare, J.A., Gravatte, H.S., Nielsen, M.K. Parasite dynamics in untreated horses through one calendar year. Parasites & Vectors 2022, 15, 50.
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Contact Information

Martin K. Nielson
DVM, PhD, DipEVPC, DipACVM

Gluck Equine Research Center, Department of Veterinary Science Lexington, KY 40546-0099

859-218-1103

martin.nielsen@uky.edu