FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Parasit Vectors / Genetic characterization of Theileria equi infecting horses ...
Parasites & vectors2013; 6; 35; doi: 10.1186/1756-3305-6-35

Genetic characterization of Theileria equi infecting horses in North America: evidence for a limited source of U.S. introductions.

Abstract: Theileria equi is a tick-borne apicomplexan hemoparasite that causes equine piroplasmosis. This parasite has a worldwide distribution but the United States was considered to be free of this disease until recently. Methods: We used samples from 37 horses to determine genetic relationships among North American T. equi using the 18S rRNA gene and microsatellites. We developed a DNA fingerprinting panel of 18 microsatellite markers using the first complete genome sequence of T. equi. Results: A maximum parsimony analysis of 18S rRNA sequences grouped the samples into two major clades. The first clade (n = 36) revealed a high degree of nucleotide similarity in U.S. T. equi, with just 0-2 single nucleotide polymorphisms (SNPs) among samples. The remaining sample fell into a second clade that was genetically divergent (48 SNPs) from the other U.S. samples. This sample was collected at the Texas border, but may have originated in Mexico. We genotyped T. equi from the U.S. using microsatellite markers and found a moderate amount of genetic diversity (2-8 alleles per locus). The field samples were mostly from a 2009 Texas outbreak (n = 22) although samples from five other states were also included in this study. Using Weir and Cockerham's FST estimator (θ) we found strong population differentiation of the Texas and Georgia subpopulations (θ = 0.414), which was supported by a neighbor-joining tree created with predominant single haplotypes. Single-clone infections were found in 27 of the 37 samples (73%), allowing us to identify 15 unique genotypes. Conclusions: The placement of most T. equi into one monophyletic clade by 18S is suggestive of a limited source of introduction into the U.S. When applied to a broader cross section of worldwide samples, these molecular tools should improve source tracking of T. equi outbreaks and may help prevent the spread of this tick-borne parasite.
Get Full Text
Publication Date: 2013-02-11 PubMed ID: 23399005PubMed Central: PMC3606381DOI: 10.1186/1756-3305-6-35Google 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.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

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 researchers studied the genetic characteristics of Theileria equi, a tick-borne parasite that infects horses, in North America. The results of the study suggest that most infections in the United States may have originated from a single source.

Methods

  • Theileria equi samples were collected from 37 horses in the United States.
  • The 18S rRNA gene and microsatellites were used to determine the genetic relationships between the samples.
  • A panel of 18 microsatellite markers was developed using the first complete genome sequence of T. equi.

Results

  • A maximum parsimony analysis of the 18S rRNA sequences revealed two major clades. The first group contained 36 samples with a high degree of nucleotide similarity, while the other contained one sample that was significantly divergent.
  • The genetic diversity of the samples was determined by genotyping T. equi using the developed microsatellite markers. The field samples were predominantly from a 2009 outbreak in Texas, but samples from five other states were also included.
  • The researchers found a strong population differentiation between samples from Texas and Georgia using Weir and Cockerham’s FST estimator.
  • In 27 of the 37 samples, single-clone infections were identified, revealing 15 unique genotypes.

Conclusions

  • Most T. equi samples from the U.S. were placed into a single clade by the 18S analysis, indicating a potential single source of introduction into the country.
  • The tools and methods developed in this study can improve source tracking of T. equi outbreaks in the future when applied to a broader range of samples, which could in turn help prevent the spread of this tick-borne parasite.

Cite This Article

APA
Hall CM, Busch JD, Scoles GA, Palma-Cagle KA, Ueti MW, Kappmeyer LS, Wagner DM. (2013). Genetic characterization of Theileria equi infecting horses in North America: evidence for a limited source of U.S. introductions. Parasit Vectors, 6, 35. https://doi.org/10.1186/1756-3305-6-35

Publication

Parasites & vectors
ISSN: 1756-3305
NlmUniqueID: 101462774
Country: England
Language: English
Volume: 6
Pages: 35

Researcher Affiliations

Hall, Carina M
  • Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, AZ 86011, USA.
Busch, Joseph D
    Scoles, Glen A
      Palma-Cagle, Kristina A
        Ueti, Massaro W
          Kappmeyer, Lowell S
            Wagner, David M

              MeSH Terms

              • Animals
              • Base Sequence
              • Coinfection / veterinary
              • DNA Fingerprinting / methods
              • DNA Fingerprinting / veterinary
              • DNA, Protozoan / chemistry
              • DNA, Protozoan / genetics
              • Genetic Markers / genetics
              • Genetic Variation
              • Genetics, Population
              • Genotype
              • Georgia / epidemiology
              • Haplotypes
              • Horse Diseases / epidemiology
              • Horse Diseases / parasitology
              • Horses
              • Microsatellite Repeats / genetics
              • Molecular Sequence Data
              • Phylogeny
              • RNA, Protozoan / genetics
              • RNA, Ribosomal, 18S / genetics
              • Sequence Analysis, DNA / veterinary
              • Texas / epidemiology
              • Theileria / classification
              • Theileria / genetics
              • Theileria / isolation & purification
              • Theileriasis / epidemiology
              • Theileriasis / parasitology

              References

              This article includes 40 references
              1. Knowles DP Jr, Kappmeyer LS, Stiller D, Hennager SG, Perryman LE. Antibody to a recombinant merozoite protein epitope identifies horses infected with Babesia equi.. J Clin Microbiol 1992 Dec;30(12):3122-6.
                pmc: PMC270599pubmed: 1280648doi: 10.1128/jcm.30.12.3122-3126.1992google scholar: lookup
              2. Ueti MW, Palmer GH, Kappmeyer LS, Statdfield M, Scoles GA, Knowles DP. Ability of the vector tick Boophilus microplus to acquire and transmit Babesia equi following feeding on chronically infected horses with low-level parasitemia.. J Clin Microbiol 2005 Aug;43(8):3755-9.
                doi: 10.1128/JCM.43.8.3755-3759.2005pmc: PMC1233951pubmed: 16081906google scholar: lookup
              3. Uilenberg G. Babesia--a historical overview.. Vet Parasitol 2006 May 31;138(1-2):3-10.
                pubmed: 16513280doi: 10.1016/j.vetpar.2006.01.035google scholar: lookup
              4. Stiller D, Goff WL, Johnson LW, Knowles DP. Dermacentor variabilis and boophilus microplus (Acari: Ixodidae): experimental vectors of Babesia equi to equids.. J Med Entomol 2002 Jul;39(4):667-70.
                doi: 10.1603/0022-2585-39.4.667pubmed: 12144301google scholar: lookup
              5. Gerstenberg C, Allen WR, Phipps LP. Mechanical transmission of Babesia equi infection in a British herd of horses. Proceedings of the eight international conference of equine infectious diseases Dubai: Newmarket, R & W Publications; 1999; pp. 217–222.
              6. Short MA, Clark CK, Harvey JW, Wenzlow N, Hawkins IK, Allred DR, Knowles DP, Corn JL, Grause JF, Hennager SG, Kitchen DL, Traub-Dargatz JL. Outbreak of equine piroplasmosis in Florida.. J Am Vet Med Assoc 2012 Mar 1;240(5):588-95.
                doi: 10.2460/javma.240.5.588pubmed: 22332629google scholar: lookup
              7. 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.
                pubmed: 3530065
              8. Heim A, Passos LM, Ribeiro MF, Costa-Júnior LM, Bastos CV, Cabral DD, Hirzmann J, Pfister K. Detection and molecular characterization of Babesia caballi and Theileria equi isolates from endemic areas of Brazil.. Parasitol Res 2007 Dec;102(1):63-8.
                doi: 10.1007/s00436-007-0726-1pubmed: 17828553google scholar: lookup
              9. Ueti MW, Palmer GH, Scoles GA, Kappmeyer LS, Knowles DP. Persistently infected horses are reservoirs for intrastadial tick-borne transmission of the apicomplexan parasite Babesia equi.. Infect Immun 2008 Aug;76(8):3525-9.
                doi: 10.1128/IAI.00251-08pmc: PMC2493223pubmed: 18490466google scholar: lookup
              10. Rothschild CM, Knowles DP. Equine piroplasmosis. Equine infectious diseases St. Louis: Saunders, Elsevier; 2007; pp. 465–473.
              11. Scoles GA, Hutcheson HJ, Schlater JL, Hennager SG, Pelzel AM, Knowles DP. Equine piroplasmosis associated with Amblyomma cajennense Ticks, Texas, USA.. Emerg Infect Dis 2011 Oct;17(10):1903-5.
                doi: 10.3201/eid1710.101182pmc: PMC3310643pubmed: 22000367google scholar: lookup
              12. USDA. Equine piroplasmosis domestic pathways assessment 2011: pathways assessment for the spread of the causative agents of equine piroplasmosis from the movement of a horse from a quarantined premises within the contiguous United States. USDA:APHIS:VS:CEAH: National Center for Risk Analysis Fort Collins, CO; 2011; p. 62.
              13. American Horse Council Foundation. The Economic Impact of the Horse Industry on the United States. Washington, DC: American Horse Council; 2005.
              14. USAHA. One hundred and fourteenth annual meeting of the United States Animal Health Association: 11–17 November 2011. Minneapolis: Richardson Printing; 2011; pp. 412–413.
              15. Bashiruddin JB, Cammà C, Rebêlo E. Molecular detection of Babesia equi and Babesia caballi in horse blood by PCR amplification of part of the 16S rRNA gene.. Vet Parasitol 1999 Jul;84(1-2):75-83.
                pubmed: 10435792doi: 10.1016/s0304-4017(99)00049-7google scholar: lookup
              16. Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum.. Mol Biol Evol 2000 Oct;17(10):1467-82.
                doi: 10.1093/oxfordjournals.molbev.a026247pubmed: 11018154google scholar: lookup
              17. Colman RE, Vogler AJ, Lowell JL, Gage KL, Morway C, Reynolds PJ, Ettestad P, Keim P, Kosoy MY, Wagner DM. Fine-scale identification of the most likely source of a human plague infection.. Emerg Infect Dis 2009 Oct;15(10):1623-5.
                doi: 10.3201/eid1510.090188pmc: PMC2866393pubmed: 19861057google scholar: lookup
              18. Havryliuk T, Ferreira MU. A closer look at multiple-clone Plasmodium vivax infections: detection methods, prevalence and consequences.. Mem Inst Oswaldo Cruz 2009 Feb;104(1):67-73.
                pubmed: 19274379doi: 10.1590/s0074-02762009000100011google scholar: lookup
              19. Keim P, Price LB, Klevytska AM, Smith KL, Schupp JM, Okinaka R, Jackson PJ, Hugh-Jones ME. Multiple-locus variable-number tandem repeat analysis reveals genetic relationships within Bacillus anthracis.. J Bacteriol 2000 May;182(10):2928-36.
                doi: 10.1128/JB.182.10.2928-2936.2000pmc: PMC102004pubmed: 10781564google scholar: lookup
              20. Battsetseg B, Lucero S, Xuan X, Claveria FG, Inoue N, Alhassan A, Kanno T, Igarashi I, Nagasawa H, Mikami T, Fujisaki K. Detection of natural infection of Boophilus microplus with Babesia equi and Babesia caballi in Brazilian horses using nested polymerase chain reaction.. Vet Parasitol 2002 Aug 22;107(4):351-7.
                doi: 10.1016/S0304-4017(02)00131-0pubmed: 12163246google scholar: lookup
              21. Bhoora R, Franssen L, Oosthuizen MC, Guthrie AJ, Zweygarth E, Penzhorn BL, Jongejan F, Collins NE. Sequence heterogeneity in the 18S rRNA gene within Theileria equi and Babesia caballi from horses in South Africa.. Vet Parasitol 2009 Feb 5;159(2):112-20.
                doi: 10.1016/j.vetpar.2008.10.004pubmed: 19019541google scholar: lookup
              22. Ueti MW, Palmer GH, Kappmeyer LS, Scoles GA, Knowles DP. Expression of equi merozoite antigen 2 during development of Babesia equi in the midgut and salivary gland of the vector tick Boophilus microplus.. J Clin Microbiol 2003 Dec;41(12):5803-9.
                doi: 10.1128/JCM.41.12.5803-5809.2003pmc: PMC308990pubmed: 14662988google scholar: lookup
              23. Bell AS, de Roode JC, Sim D, Read AF. Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success.. Evolution 2006 Jul;60(7):1358-71.
                pubmed: 16929653
              24. Keim P, Van Ert MN, Pearson T, Vogler AJ, Huynh LY, Wagner DM. Anthrax molecular epidemiology and forensics: using the appropriate marker for different evolutionary scales.. Infect Genet Evol 2004 Sep;4(3):205-13.
                doi: 10.1016/j.meegid.2004.02.005pubmed: 15450200google scholar: lookup
              25. Salim B, Bakheit MA, Kamau J, Nakamura I, Sugimoto C. Nucleotide sequence heterogeneity in the small subunit ribosomal RNA gene within Theileria equi from horses in Sudan.. Parasitol Res 2010 Jan;106(2):493-8.
                doi: 10.1007/s00436-009-1691-7pubmed: 19953269google scholar: lookup
              26. Kappmeyer LS, Thiagarajan M, Herndon DR, Ramsay JD, Caler E, Djikeng A, Gillespie JJ, Lau AO, Roalson EH, Silva JC, Silva MG, Suarez CE, Ueti MW, Nene VM, Mealey RH, Knowles DP, Brayton KA. Comparative genomic analysis and phylogenetic position of Theileria equi.. BMC Genomics 2012 Nov 9;13:603.
                pmc: PMC3505731pubmed: 23137308doi: 10.1186/1471-2164-13-603google scholar: lookup
              27. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.. Mol Biol Evol 2007 Aug;24(8):1596-9.
                doi: 10.1093/molbev/msm092pubmed: 17488738google scholar: lookup
              28. Benson G. Tandem repeats finder: a program to analyze DNA sequences.. Nucleic Acids Res 1999 Jan 15;27(2):573-80.
                doi: 10.1093/nar/27.2.573pmc: PMC148217pubmed: 9862982google scholar: lookup
              29. Faircloth BC. msatcommander: detection of microsatellite repeat arrays and automated, locus-specific primer design.. Mol Ecol Resour 2008 Jan;8(1):92-4.
                doi: 10.1111/j.1471-8286.2007.01884.xpubmed: 21585724google scholar: lookup
              30. Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP. Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples.. Parasitology 1999 Aug;119 ( Pt 2):113-25.
                pubmed: 10466118doi: 10.1017/s0031182099004552google scholar: lookup
              31. Waldenström J, Bensch S, Hasselquist D, Ostman O. A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood.. J Parasitol 2004 Feb;90(1):191-4.
                doi: 10.1645/GE-3221RNpubmed: 15040694google scholar: lookup
              32. Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies.. Am J Trop Med Hyg 1999 Apr;60(4):687-92.
                pubmed: 10348249doi: 10.4269/ajtmh.1999.60.687google scholar: lookup
              33. Oura CA, Asiimwe BB, Weir W, Lubega GW, Tait A. Population genetic analysis and sub-structuring of Theileria parva in Uganda.. Mol Biochem Parasitol 2005 Apr;140(2):229-39.
                doi: 10.1016/j.molbiopara.2004.12.015pubmed: 15760662google scholar: lookup
              34. Perez-Llaneza A, Caballero M, Baravalle E, Mesplet M, Mosqueda J, Suarez CE, Echaide I, Katzer F, Pacheco GM, Florin-Christensen M, Schnittger L. Development of a tandem repeat-based multilocus typing system distinguishing Babesia bovis geographic isolates.. Vet Parasitol 2010 Feb 10;167(2-4):196-204.
                pubmed: 19833439doi: 10.1016/j.vetpar.2009.09.021google scholar: lookup
              35. Simuunza M, Bilgic H, Karagenc T, Syakalima M, Shiels B, Tait A, Weir W. Population genetic analysis and sub-structuring in Babesia bovis.. Mol Biochem Parasitol 2011 Jun;177(2):106-15.
                doi: 10.1016/j.molbiopara.2011.02.002pubmed: 21316400google scholar: lookup
              36. Park SDE. Trypanotolerance in west African cattle and the population genetic effects of selection. University of Dublin, Ireland: PhD thesis; 2001.
              37. Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research--an update.. Bioinformatics 2012 Oct 1;28(19):2537-9.
                doi: 10.1111/j.1471-8286.2005.01155.xpmc: PMC3463245pubmed: 22820204google scholar: lookup
              38. Swofford DL. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). version 4. Sunderland, MA, USA: Sinauer Associates; 1998.
              39. Bhoora R, Quan M, Matjila PT, Zweygarth E, Guthrie AJ, Collins NE. Sequence heterogeneity in the equi merozoite antigen gene (ema-1) of Theileria equi and development of an ema-1-specific TaqMan MGB assay for the detection of T. equi.. Vet Parasitol 2010 Aug 27;172(1-2):33-45.
                pubmed: 20493635doi: 10.1016/j.vetpar.2010.04.025google scholar: lookup
              40. Weir W, Karagenç T, Gharbi M, Simuunza M, Aypak S, Aysul N, Darghouth MA, Shiels B, Tait A. Population diversity and multiplicity of infection in Theileria annulata.. Int J Parasitol 2011 Feb;41(2):193-203.
                doi: 10.1016/j.ijpara.2010.08.004pmc: PMC3034872pubmed: 20833170google scholar: lookup

              Citations

              This article has been cited 11 times.
              1. Grimsley M, Hicks J, Zeineldin M, Murphy G, Sigafoose T. Complete Genome Sequence of Theileria equi NVSL354.. Microbiol Resour Announc 2023 Feb 16;12(2):e0080922.
                doi: 10.1128/mra.00809-22pubmed: 36688717google scholar: lookup
              2. Onzere CK, Fry LM, Bishop RP, Silva MG, Bastos RG, Knowles DP, Suarez CE. Theileria equi claudin like apicomplexan microneme protein contains neutralization-sensitive epitopes and interacts with components of the equine erythrocyte membrane skeleton.. Sci Rep 2021 Apr 29;11(1):9301.
                doi: 10.1038/s41598-021-88902-4pubmed: 33927329google scholar: lookup
              3. Tirosh-Levy S, Gottlieb Y, Fry LM, Knowles DP, Steinman A. Twenty Years of Equine Piroplasmosis Research: Global Distribution, Molecular Diagnosis, and Phylogeny.. Pathogens 2020 Nov 8;9(11).
                doi: 10.3390/pathogens9110926pubmed: 33171698google scholar: lookup
              4. Alvarez DO, Corona-González B, Rodríguez-Mallón A, Rodríguez Gonzalez I, Alfonso P, Noda Ramos AA, Díaz-Sánchez AA, González Navarrete M, Rodríguez Fernández R, Méndez Mellor L, Catanese HN, Peláez M, Gainza YA, Marrero-Perera R, Roblejo-Arias L, Lobo-Rivero E, Silva CB, Fonseca AH, López ER, Cabezas-Cruz A. Ticks and Tick-Borne Diseases in Cuba, Half a Century of Scientific Research.. Pathogens 2020 Jul 28;9(8).
                doi: 10.3390/pathogens9080616pubmed: 32731487google scholar: lookup
              5. 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.
                doi: 10.1007/s00436-020-06797-ypubmed: 32647992google scholar: lookup
              6. Tirosh-Levy S, Steinman A, Levy H, Katz Y, Shtilman M, Gottlieb Y. Parasite load and genotype are associated with clinical outcome of piroplasm-infected equines in Israel.. Parasit Vectors 2020 May 20;13(1):267.
                doi: 10.1186/s13071-020-04133-ypubmed: 32434550google scholar: lookup
              7. Onyiche TE, Suganuma K, Igarashi I, Yokoyama N, Xuan X, Thekisoe O. A Review on Equine Piroplasmosis: Epidemiology, Vector Ecology, Risk Factors, Host Immunity, Diagnosis and Control.. Int J Environ Res Public Health 2019 May 16;16(10).
                doi: 10.3390/ijerph16101736pubmed: 31100920google scholar: lookup
              8. Sant C, Allicock OM, d'Abadie R, Charles RA, Georges K. Phylogenetic analysis of Theileria equi and Babesia caballi sequences from thoroughbred mares and foals in Trinidad.. Parasitol Res 2019 Apr;118(4):1171-1177.
                doi: 10.1007/s00436-019-06240-xpubmed: 30761425google scholar: lookup
              9. Díaz-Sánchez AA, Pires MS, Estrada CY, Cañizares EV, Del Castillo Domínguez SL, Cabezas-Cruz A, Rivero EL, da Fonseca AH, Massard CL, Corona-González B. First molecular evidence of Babesia caballi and Theileria equi infections in horses in Cuba.. Parasitol Res 2018 Oct;117(10):3109-3118.
                doi: 10.1007/s00436-018-6005-5pubmed: 30033488google scholar: lookup
              10. Guidi E, Pradier S, Lebert I, Leblond A. Piroplasmosis in an endemic area: analysis of the risk factors and their implications in the control of Theileriosis and Babesiosis in horses.. Parasitol Res 2015 Jan;114(1):71-83.
                doi: 10.1007/s00436-014-4161-9pubmed: 25280516google scholar: lookup
              11. Scoles GA, Ueti MW. Amblyomma cajennense is an intrastadial biological vector of Theileria equi.. Parasit Vectors 2013 Oct 23;6(1):306.
                doi: 10.1186/1756-3305-6-306pubmed: 24499587google scholar: lookup
              Subscribe to our newsletter
              Join 99,359 horse owners like you who receive our email updates on horse health and nutrition.