Clinical Progression of Theileria haneyi in Splenectomized Horses Reveals Decreased Virulence Compared to Theileria equi.
Abstract: The global importance of the hemoparasite to equine health was recently shown by its resistance to imidocarb dipropionate (ID) and its interference with clearance by ID in some co-infected horses. Genetic characterization of revealed marked genomic reduction compared to , and initial experiments demonstrated reduced clinical severity in spleen-intact horses. Furthermore, in early experiments, splenectomized horses survived infection and progressed to an asymptomatic carrier state, in stark contrast to the high fatality rate of in splenectomized horses. Thus, we hypothesized that is less virulent than . To objectively assess virulence, clinical data from nine splenectomized, -infected horses were evaluated and compared to published data on -infected, splenectomized horses. Seven of eight splenectomized, -infected horses survived. Further, in six horses co-infected with and , only horses cleared of by ID survived splenectomy and became asymptomatic carriers. The reduced virulence of in splenectomized horses instructs why was, until recently, undetected. This naturally occurring comparative reduction in virulence in a natural host provides a foundation for defining virulence mechanisms of theileriosis and Apicomplexa in general.
Publication Date: 2022-02-16 PubMed ID: 35215197PubMed Central: PMC8879895DOI: 10.3390/pathogens11020254Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Asymptomatic Carriers
- Clinical Findings
- Comparative Study
- Diagnosis
- Disease Diagnosis
- Disease Etiology
- Disease Management
- Disease Surveillance
- Disease Treatment
- Equine Diseases
- Equine Health
- Genetics
- Horses
- Imidocarb Dipropionate
- Infectious Disease
- Parasites
- Pathogenicity
- Spleen
- Theileria equi
- Veterinary Medicine
- Virulence
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research paper examines the relative virulence of Theileria haneyi (Th) compared to Theileria equi (Te) in splenectomized horses, with the authors concluding that Th is less virulent. This conclusion is based on studies showing a higher survival rate of horses infected with Th versus those infected with Te after spleen removal.
Introduction and Theoretical Basis
- The research is grounded on recent findings proving the significance of the hemoparasite Theileria to equine health. One of these findings is the resistance of certain strains to the drug imidocarb dipropionate (ID) and interference with its efficacy in some co-infected horses.
- The scientists also took note of the marked genomic reduction of Theileria haneyi compared to Theileria equi, indicating different biological characteristics between these two parasites.
- The initial experiments conducted by the research team showed less harmful effects of Th on horses with an intact spleen compared to those infected with Te.
- Earlier results also revealed that splenectomized horses – horses having their spleen removed – survived Th infection and did not exhibit any clinical symptoms, unlike their counterparts infected with Te, which faced a high mortality rate.
Research Methodology
- To test their hypothesis of Th being less severe than Te, the scientists examined clinical data from nine splenectomized horses infected with Th and compared these to existing data on Te-infected, splenectomized horses.
- In addition, they observed cases of horses co-infected with both Te and Th. The survival rates of these horses after their spleen was removed and they were subsequently treated with ID were analyzed.
Findings and Conclusions
- Most of the splenectomized horses infected with Th (seven out of eight) survived, supporting the hypothesis of Th’s reduced virulence.
- In the case of the six co-infected horses, only those who received ID treatment to eliminate Th survived spleen removal and no longer displayed any disease symptoms.
- This observed decreased virulence of Th in splenectomized horses is the reason why its presence was difficult to detect until recently.
- These results offer valuable insight into understanding the mechanisms that define the virulence of diseases like theileriosis (caused by Theileria) and other diseases within the Apicomplexa phylum.
Cite This Article
APA
Sears KP, Knowles DP, Fry LM.
(2022).
Clinical Progression of Theileria haneyi in Splenectomized Horses Reveals Decreased Virulence Compared to Theileria equi.
Pathogens, 11(2), 254.
https://doi.org/10.3390/pathogens11020254 Publication
Researcher Affiliations
- Department of Clinical Science, Carlson College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331-4801, USA.
- Department of Veterinary Microbiology and Pathology, Washington State University, College of Veterinary Medicine, Pullman, WA 99164-6630, USA.
- Department of Veterinary Microbiology and Pathology, Washington State University, College of Veterinary Medicine, Pullman, WA 99164-6630, USA.
- Department of Veterinary Microbiology and Pathology, Washington State University, College of Veterinary Medicine, Pullman, WA 99164-6630, USA.
- USDA-ARS, Animal Disease Research Unit, Pullman, WA 99164-6630, USA.
Grant Funding
- CRIS# #2090-320000-034-00D / USDA-ARS
Conflict of Interest Statement
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
References
This article includes 52 references
- Knowles DP, Kappmeyer LS, Haney D, Herndon DR, Fry LM, Munro JB, Sears K, Ueti MW, Wise LN, Silva M, Schneider DA, Grause J, White SN, Tretina K, Bishop RP, Odongo DO, Pelzel-McCluskey AM, Scoles GA, Mealey RH, Silva JC. Discovery of a novel species, Theileria haneyi n. sp., infective to equids, highlights exceptional genomic diversity within the genus Theileria: implications for apicomplexan parasite surveillance.. Int J Parasitol 2018 Aug;48(9-10):679-690.
- Wise LN, Kappmeyer LS, Mealey RH, Knowles DP. Review of equine piroplasmosis.. J Vet Intern Med 2013 Nov-Dec;27(6):1334-46.
- Mshelia PW, Kappmeyer L, Johnson WC, Kudi CA, Oluyinka OO, Balogun EO, Richard EE, Onoja E, Sears KP, Ueti MW. Molecular detection of Theileria species and Babesia caballi from horses in Nigeria.. Parasitol Res 2020 Sep;119(9):2955-2963.
- Coultous RM, McDonald M, Raftery AG, Shiels BR, Sutton DGM, Weir W. Analysis of Theileria equi diversity in The Gambia using a novel genotyping method.. Transbound Emerg Dis 2020 May;67(3):1213-1221.
- Bhoora RV, Collins NE, Schnittger L, Troskie C, Marumo R, Labuschagne K, Smith RM, Dalton DL, Mbizeni S. Molecular genotyping and epidemiology of equine piroplasmids in South Africa.. Ticks Tick Borne Dis 2020 Mar;11(2):101358.
- Zobba R, Ardu M, Niccolini S, Chessa B, Manna L, Cocco R, Pinna Parpaglia ML. Clinical and Laboratory Findings in Equine Piroplasmosis. J. Equine Vet. Sci. 2008;28:301–308.
- Hailat NQ, Lafi SQ, al-Darraji AM, al-Ani FK. Equine babesiosis associated with strenuous exercise: clinical and pathological studies in Jordan.. Vet Parasitol 1997 Apr;69(1-2):1-8.
- Sears KP, Kappmeyer LS, Wise LN, Silva M, Ueti MW, White S, Reif KE, Knowles DP. Infection dynamics of Theileria equi and Theileria haneyi, a newly discovered apicomplexan of the horse.. Vet Parasitol 2019 Jul;271:68-75.
- Wise LN, Kappmeyer LS, Silva MG, White SN, Grause JF, Knowles DP. Verification of post-chemotherapeutic clearance of Theileria equi through concordance of nested PCR and immunoblot.. Ticks Tick Borne Dis 2018 Feb;9(2):135-140.
- Sears K, Knowles D, Dinkel K, Mshelia PW, Onzere C, Silva M, Fry L. Imidocarb Dipropionate Lacks Efficacy against Theileria haneyi and Fails to Consistently Clear Theileria equi in Horses Co-Infected with T. haneyi.. Pathogens 2020 Dec 10;9(12).
- Ogier JC, Pagès S, Bisch G, Chiapello H, Médigue C, Rouy Z, Teyssier C, Vincent S, Tailliez P, Givaudan A, Gaudriault S. Attenuated virulence and genomic reductive evolution in the entomopathogenic bacterial symbiont species, Xenorhabdus poinarii.. Genome Biol Evol 2014 Jun 5;6(6):1495-513.
- Diop A, Raoult D, Fournier PE. Rickettsial genomics and the paradigm of genome reduction associated with increased virulence.. Microbes Infect 2018 Aug-Sep;20(7-8):401-409.
- Casadevall A. The Pathogenic Potential of a Microbe.. mSphere 2017 Jan-Feb;2(1).
- Lover AA, Coker RJ. Do mixed infections matter? Assessing virulence of mixed-clone infections in experimental human and murine malaria.. Infect Genet Evol 2015 Dec;36:82-91.
- Mackinnon MJ, Read AF. Virulence in malaria: an evolutionary viewpoint.. Philos Trans R Soc Lond B Biol Sci 2004 Jun 29;359(1446):965-86.
- Schmidt LH, Fradkin R, Sesler C, Squires W, Zeyen P. Attenuation of the virulence of the M strain of Plasmodium cynomolgi during prolonged multiplication in splenectomized rhesus monkeys.. Am J Trop Med Hyg 1987 Nov;37(3):460-90.
- Ueti MW, Mealey RH, Kappmeyer LS, White SN, Kumpula-McWhirter N, Pelzel AM, Grause JF, Bunn TO, Schwartz A, Traub-Dargatz JL, Hendrickson A, Espy B, Guthrie AJ, Fowler WK, Knowles DP. Re-emergence of the apicomplexan Theileria equi in the United States: elimination of persistent infection and transmission risk.. PLoS One 2012;7(9):e44713.
- Kuttler KL, Zaugg JL, Gipson CA. Imidocarb and parvaquone in the treatment of piroplasmosis (Babesia equi) in equids.. Am J Vet Res 1987 Nov;48(11):1613-6.
- Zaugg JL, Lane VM. Evaluations of buparvaquone as a treatment for equine babesiosis (Babesia equi).. Am J Vet Res 1989 May;50(5):782-5.
- Bach O, Baier M, Pullwitt A, Fosiko N, Chagaluka G, Kalima M, Pfister W, Straube E, Molyneux M. Falciparum malaria after splenectomy: a prospective controlled study of 33 previously splenectomized Malawian adults.. Trans R Soc Trop Med Hyg 2005 Nov;99(11):861-7.
- Buffet PA, Safeukui I, Deplaine G, Brousse V, Prendki V, Thellier M, Turner GD, Mercereau-Puijalon O. The pathogenesis of Plasmodium falciparum malaria in humans: insights from splenic physiology.. Blood 2011 Jan 13;117(2):381-92.
- Ambawat HK, Malhotra DV, Kumar S, Dhar S. Erythrocyte associated haemato-biochemical changes in Babesia equi infection experimentally produced in donkeys.. Vet Parasitol 1999 Sep 1;85(4):319-24.
- Guimarães AM, Lima JD, Tafuri WL, Ribeiro MFB, Sciavicco CJS, Botelho ACC. Clinical and histopathological aspects of splenectomized foals infected by Babesia equi. J. Equine Vet. Sci. 1997;17:211–216.
- Singh B, Banerjee DP, Gautam OP, Gupta RKP. Clinicopathological changes in splenectomised donkeys infected with Babesia equi. Indian J. Parasitol. 1980;4:77–80.
- Knowles DP Jr, Kappmeyer LS, Perryman LE. Specific immune responses are required to control parasitemia in Babesia equi infection.. Infect Immun 1994 May;62(5):1909-13.
- White NJ. Malaria parasite clearance.. Malar J 2017 Feb 23;16(1):88.
- Kuttler KL, Gipson CA, Goff WL, Johnson LW. Experimental Babesia equi infection in mature horses.. Am J Vet Res 1986 Aug;47(8):1668-70.
- Cunha CW, McGuire TC, Kappmeyer LS, Hines SA, Lopez AM, Dellagostin OA, Knowles DP. Development of specific immunoglobulin Ga (IgGa) and IgGb antibodies correlates with control of parasitemia in Babesia equi Infection.. Clin Vaccine Immunol 2006 Feb;13(2):297-300.
- Teuscher F, Gatton ML, Chen N, Peters J, Kyle DE, Cheng Q. Artemisinin‐induced dormancy in plasmodium falciparum: duration, recovery rates, and implications in treatment failure.. J Infect Dis 2010 Nov 1;202(9):1362-8.
- Bediako Y, Ngoi JM, Nyangweso G, Wambua J, Opiyo M, Nduati EW, Bejon P, Marsh K, Ndungu FM. The effect of declining exposure on T cell-mediated immunity to Plasmodium falciparum - an epidemiological "natural experiment".. BMC Med 2016 Sep 22;14(1):143.
- Nahrendorf W, Ivens A, Spence PJ. Inducible mechanisms of disease tolerance provide an alternative strategy of acquired immunity to malaria.. Elife 2021 Mar 23;10.
- Fry LM, Schneider DA, Frevert CW, Nelson DD, Morrison WI, Knowles DP. East Coast Fever Caused by Theileria parva Is Characterized by Macrophage Activation Associated with Vasculitis and Respiratory Failure.. PLoS One 2016;11(5):e0156004.
- Kho S, Barber BE, Johar E, Andries B, Poespoprodjo JR, Kenangalem E, Piera KA, Ehmann A, Price RN, William T, Woodberry T, Foote S, Minigo G, Yeo TW, Grigg MJ, Anstey NM, McMorran BJ. Platelets kill circulating parasites of all major Plasmodium species in human malaria.. Blood 2018 Sep 20;132(12):1332-1344.
- Nafie TH, El-Allawy T, Mottelib AA, EL-Amrousi S. Effect of induced equine piroplasmosis on some blood constituents. Assiut Vet. Med. J. 1982;9:123–128.
- Rudolph W, Correa J, Zurita L, Manley W. Equine piroplasmosis: leukocytic response to Babesia equi (Laveran, 1901) infection in Chile.. Br Vet J 1975 Sep-Oct;131(5):601-9.
- Hviid L, Kemp K. What is the cause of lymphopenia in malaria?. Infect Immun 2000 Oct;68(10):6087-9.
- Aitken EH, Alemu A, Rogerson SJ. Neutrophils and Malaria.. Front Immunol 2018;9:3005.
- Juneja S, Januszewicz E, Wolf M, Cooper I. Post-splenectomy lymphocytosis.. Clin Lab Haematol 1995 Dec;17(4):335-7.
- Dürig M, Landmann RM, Harder F. Lymphocyte subsets in human peripheral blood after splenectomy and autotransplantation of splenic tissue.. J Lab Clin Med 1984 Jul;104(1):110-5.
- Sponaas AM, Freitas do Rosario AP, Voisine C, Mastelic B, Thompson J, Koernig S, Jarra W, Renia L, Mauduit M, Potocnik AJ, Langhorne J. Migrating monocytes recruited to the spleen play an important role in control of blood stage malaria.. Blood 2009 Dec 24;114(27):5522-31.
- Court RA, Jackson LA, Lee RP. Elevated anti-parasitic activity in peripheral blood monocytes and neutrophils of cattle infected with Babesia bovis.. Int J Parasitol 2001 Jan;31(1):29-37.
- Klei TR, Meinderts SM, van den Berg TK, van Bruggen R. From the Cradle to the Grave: The Role of Macrophages in Erythropoiesis and Erythrophagocytosis.. Front Immunol 2017;8:73.
- Duez J, Holleran JP, Ndour PA, Pionneau C, Diakité S, Roussel C, Dussiot M, Amireault P, Avery VM, Buffet PA. Mechanical clearance of red blood cells by the human spleen: Potential therapeutic applications of a biomimetic RBC filtration method.. Transfus Clin Biol 2015 Aug;22(3):151-7.
- Kim CC, Nelson CS, Wilson EB, Hou B, DeFranco AL, DeRisi JL. Splenic red pulp macrophages produce type I interferons as early sentinels of malaria infection but are dispensable for control.. PLoS One 2012;7(10):e48126.
- Stijlemans B, Cnops J, Naniima P, Vaast A, Bockstal V, De Baetselier P, Magez S. Development of a pHrodo-based assay for the assessment of in vitro and in vivo erythrophagocytosis during experimental trypanosomosis.. PLoS Negl Trop Dis 2015 Mar;9(3):e0003561.
- Erhart LM, Yingyuen K, Chuanak N, Buathong N, Laoboonchai A, Miller RS, Meshnick SR, Gasser RA Jr, Wongsrichanalai C. Hematologic and clinical indices of malaria in a semi-immune population of western Thailand.. Am J Trop Med Hyg 2004 Jan;70(1):8-14.
- Gérardin P, Rogier C, Ka AS, Jouvencel P, Brousse V, Imbert P. Prognostic value of thrombocytopenia in African children with falciparum malaria.. Am J Trop Med Hyg 2002 Jun;66(6):686-91.
- Nwaneri D, Oladipo O, Ifebi E, Oviawe O, Asemota O, Ogboghodo B, Israel-Aina Y, Sadoh A. Haematological Parameters and Spleen Rate of Asymptomatic and Malaria Negative Children in Edo South District, Nigeria.. Ann Glob Health 2020 Jun 17;86(1):62.
- Kini RG, Chandrashekhar J. Parasite and the Circulating Pool- Characterisation of Leukocyte Number and Morphology in Malaria.. J Clin Diagn Res 2016 May;10(5):EC44-8.
- Dobbs KR, Embury P, Vulule J, Odada PS, Rosa BA, Mitreva M, Kazura JW, Dent AE. Monocyte dysregulation and systemic inflammation during pediatric falciparum malaria.. JCI Insight 2017 Sep 21;2(18).
- Ortega-Pajares A, Rogerson SJ. The Rough Guide to Monocytes in Malaria Infection.. Front Immunol 2018;9:2888.
- Bastos RG, Sears K, Dinkel KD, Knowles DP, Fry LM. Changes in the Molecular and Functional Phenotype of Bovine Monocytes during Theileria parva Infection.. Infect Immun 2019 Dec;87(12).
Citations
This article has been cited 3 times.- Onzere CK, Hulbert M, Sears KP, Williams LBA, Fry LM. Tulathromycin and Diclazuril Lack Efficacy against Theileria haneyi, but Tulathromycin Is Not Associated with Adverse Clinical Effects in Six Treated Adult Horses.. Pathogens 2023 Mar 14;12(3).
- Ozubek S, Ulucesme MC, Aktas M. Discovery of a Novel Species Infecting Goats: Morphological and Molecular Characterization of Babesia aktasi n. sp.. Pathogens 2023 Jan 10;12(1).
- Elchaninov A, Vishnyakova P, Sukhikh G, Fatkhudinov T. Spleen: Reparative Regeneration and Influence on Liver.. Life (Basel) 2022 Apr 22;12(5).
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists