Tracie C. Quick¹ and Susan E. Little^2,3
1The University of Georgia College of Veterinary Medicine, Athens, Georgia 30602, USA; ²Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, The University of Georgia, Athens, Georgia 30602, USA; ³Department of Medical Microbiology and Parasitology, The University of Georgia, Athens, Georgia 30602, USA

ABSTRACT: A white-tailed deer (Odocoileus virginianus) fawn was collected in Missouri (USA) and submitted for diagnostic evaluation. Necropsy and histologic examination revealed severe Amblyomma americanum infestation, pronounced icterus, and marked hemosiderin deposition in the liver and spleen. Whole blood evaluation revealed a normocytic-normochromic anemia and a Theileria cervi parasitemia of approximately 70%. Although Theileria cervi parasitemias have been commonly reported in healthy white-tailed deer, the severe parasitemia in this fawn may have contributed to overt clinical disease, perhaps as part of a combined malnutrition and parasitemia syndrome.

Key Words: Amblyomma americanum, lone star tick, Odocoileus virginianus, Theileriosis, Theileria cervi, white-tailed deer.

Introduction

Theileria cervi, an intraerythrocytic hemoprotozoan parasite of white-tailed deer (Odocoileus virginianus), was first reported in North America.⁸ Subsequent work has implicated Amblyomma americanum, the lone star tick, as the principle vector for Theileria cervi.^{1,2,7,9,10,14,14} This parasite has been reported in white-tailed deer collected in Missouri,⁸ Oklahoma,^1,10 Texas,^11,14 and Alabama,^2,6 as well as Arkansas, Florida, Georgia, South Carolina, Maryland, and Virginia² but its role as a primary pathogen remains unclear.

Although mortality in fawns experimentally infested with heavy burdens of Theileria-infected lone star ticks has been reported,¹ other investigators have reported equal mortality in fawn study groups highly infested with Amblyomma americanum regardless of Theileria cervi infection.⁴ Amblyomma americanum infestation alone as a primary cause of neonatal fawn mortality due to blood loss³ or tissue destruction and secondary infection² has been proposed. However, several researchers have suggested that Theileria cervi may be pathogenic to deer when high population density and poor nutrition coincide with additional hardships such as secondary infection, other principle disease, or heavy parasitism.^1,2,11 Here we report a case of a white-tailed deer fawn with an extreme Theileria cervi parasitemia which may have contributed to overt clinical disease, perhaps as part of a combined malnutrition and parasitemia syndrome.

In June 1996, a lone white-tailed deer fawn (Odocoileus virginianus) was noted beside a refuge service road in the Peck Ranch Wildlife Management Area in Carter County, Missouri (USA; 37° 02'N , 91° 09' W). Three other fawns had been found dead or dying in the same area during the previous week. The fawn was observed in situ for 24 hours then collected and held for 48 hours before being transferred to a local veterinary clinic where it was humanely euthanized due to extreme lethargy and labored breathing. Blood and tick samples were collected and shipped with the carcass to the diagnostic laboratory of the Southeastern Cooperative Wildlife Disease Study (SCWDS, The University of Georgia, Athens, Georgia, USA) for necropsy examination.

The fawn was a 6.1 kg male estimated to be 2 months of age based on tooth eruption patterns, size, and weight. The carcass was thin and infested with numerous nymphal and adult Amblyomma americanum ticks, particularly about the head and ears. Gross examination revealed pronounced icterus, an enlarged friable liver, and edematous lungs. Sections of liver, spleen, lymph node, heart, tongue, intestine, rumen, pancreas, cerebellum, cerebrum, lung, and ear pinna were fixed in 10% neutral buffered formalin, embedded in paraffin, sectioned to a 5m m thickness, and stained with hematoxylin and eosin for histologic evaluation. Aseptically collected swabs of liver, kidney, spleen, lymph node, lung, brain, heart, urine, and conjunctiva were submitted to the Athens Diagnostic Laboratory (Athens, Georgia, USA) for aerobic bacterial culture according to standard bacteriologic techniques.⁵ Whole blood samples and sections of spleen for virus isolation as well as lung samples for adenovirus fluorescent antibody testing and kidney and liver samples for Leptospira species fluorescent antibody testing were submitted to the same laboratory. Whole blood and impression smears of the lymph nodes, spleen, and liver were stained with Diff-QuikÒ (Dade Diagnostics of P.R. Inc., Aguada, Puerto Rico, USA) and examined for parasites. Theileria cervi was identified in 70% of erythrocytes in accordance with previous descriptions.^6,8,13

A complete blood count performed on EDTA-anticoagulated blood submitted with the carcass revealed a normocytic, normochromic anemia and a leukocytosis characterized by a mature neutrophilia. Chemistry profile performed on serum submitted with the carcass and an analysis of urine collected postmortem revealed a pre-renal azotemia and alterations in electrolyte balance. Histological evaluation revealed marked hemosiderin deposition in the liver and spleen. The lymph nodes showed lymphoid depletion. Multiple focally extensive areas of subacute to chronic inflammation surrounding tick bites were present in the pinna. No lesions were noted in the heart, tongue, intestine, rumen, pancreas, cerebellum, cerebrum, or lung. Virus isolation of the spleen and whole blood was unrewarding and fluorescent antibody testing for adenovirus and Leptospira sp. was negative. Bacterial cultures did not reveal any significant organisms. Whole blood smears revealed a Theileria cervi parasitemia of approximately 70% (Figure 1) with many erythrocytes containing multiple organisms (Figure 2).

Figure 1. Theileria cervi in erythrocytes of a white-tailed deer (Odocoileus virginianus).

Figure 2. Multiple Theileria cervi organisms infecting a single erythrocyte.

Marked hemosiderin deposition in the liver and spleen, together with anemia and intense icterus, indicate a severe hemolytic anemia in this fawn. Theileria cervi parasitemias ranging from 1% to 60% have been reported in intact and splenectomized deer of variable age;^1,4,8,9,11 however, the 70% parasitemia observed here is greater than previous reports, and  may have initiated a hemolytic crisis. Although a common and often incidental finding in healthy white-tailed deer, the severe parasitemia in this fawn may have contributed to overt clinical disease, perhaps as part of a combined malnutrition and parasitemia syndrome.

Acknowledgements

The authors thank J. Beringer for submission of the clinical case and Dr. K. Heise for clinical examination and sample collection. This work was supported through sponsorship from the fish and wildlife agencies of Alabama, Arkansas, Florida, Georgia, Kansas, Kentucky, Louisiana, Maryland, Mississippi, Missouri, North Carolina, Puerto Rico, South Carolina, Tennessee, Virginia, and West Virginia. Funds were provided by the Federal Aid to Wildlife Restoration Act (50 Stat. 917) and through Grant Agreement 14-45-0009-94-906, National Biological Service, U.S. Department of the Interior.

1.  BARKER, R. W., A.L. HOCH, R. G. BUCKNER, AND J. A. HAIR. 1973. Hematological changes in white-tailed deer fawns, Odocoileus virginianus, infested with Theileria-infected lone star ticks. The Journal of Parasitology 59: 1091-1098

2.  BOLTE, J. R., J. A. HAIR, AND J. FLETCHER. 1970. White-tailed deer mortality following tissue destruction induced by lone star ticks. Journal of Wildlife Management 34: 546-552.

3.  DAVIDSON, W. R., C. B. CROW, J. M. CRUM, AND R. R. GERRISH. 1983. Observations on Theileria cervi and Trypanosoma cervi in white-tailed deer (Odocoileus virginianus from the Southeastern United States. Proceedings of the Helminthological Society of Washington 50: 165-169.

4.  EMERSON, H.R. 1969. A comparison of parasitic infections of white-tailed deer (Odocoileus virginianus) from central and east Texas. Bulletin of the Wildlife Disease Association 5: 137-139.

5.  HAIR, J. A., A. L. HOCH, R. G. BUCKNER, AND R. W. BARKER. 1992. Fawn hematology and survival following tick infestation and theileriasis. Journal of Agricultural Entomology 9: 301-319.

6.  IKRAM, M., AND E. HILL. 1991. Microbiology for veterinary technicians. American Veterinary Publications, Inc., Goleta, California, 213 pp.

7.  KINGSTON, N. 1981. Protozoan parasites. In Diseases and Parasites of White-Tailed Deer, W.R. Davidson et al. (eds.). Tall Timbers Research Station, Tallahassee, Florida, Miscellaneous Publication Number 7, pp.193-236.

8.  KOCAN, A. A., S. W. MUKOLWE, AND J. S. LAIRD. 1987. Failure to detect infection in fallow deer (Cervus dama) exposed to Theileria cervi from white-tailed deer. Journal of Wildlife Diseases 23: 674-676.

9.  KREIER, J.P., M. RISTIC, AND A. M. WATRACH. 1962. Theileria sp. in a deer in the United States. American Journal of Veterinary Research 23: 657-662.

10. KUTTLER, K. L., R. M. ROBINSON, AND R.R. BELL. 1967. Tick transmission of theileriasis in a white-tailed deer. Bulletin of the Wildlife Disease Association 3: 182-183.

11. LAIRD, J. S., A. A. KOCAN, K. M. KOCAN, S. M. PRESLEY, AND J. A. HAIR. 1988. Susceptibility of Amblyomma americanum to natural and experimental infections with Theileria cervi. Journal of Wildlife Diseases 24: 679-683.

12. ROBINSON, R. M., K. L. KUTTLER, J. W. THOMAS, AND R. G. MARBURGER. 1967. Theileriasis in Texas white-tailed deer. Journal of Wildlife Management 31: 455-459.

13. SAMUEL, W. M., AND D. O. TRAINER. 1970. Amblyomma (acarina: ixodidae) on white-tailed deer, Odocoileus virginianus (Zimmermann), from south Texas with implications for theileriasis. Journal of Medical Entomology 7: 567-574.

14. TELFORD, S.R., AND D.J. FORRESTER. 1991. Piroplasms of white-tailed deer (Odocoileus virginianus) in Florida. Florida Field Naturalist 19: 49-51.

15. WALDRUP, K. A., J. MORITZ, D. BAGGETT, S. MAGYAR, AND G. G. WAGNER. 1992. Monthly incidence of Theileria cervi and seroconversion to Babesia odocoilei in white-tailed deer (Odocoileus virginianus) in Texas. Journal of Wildlife Diseases 28: 457-459.