Molecular typing of Sarcocystis neurona: Current status and future trends

Veterinary Parasitology

Volumn 149, Issue 1-2, 2007, Pages 43-55

  Elsheikha, Hany M ^a   Mansfield, Linda S ^b,c  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

Epidemiology; Evolution; Genetic diversity; Genotyping; Sarcocystis neurona

Indexed keywords

MEMBRANE PROTEIN;

AGGLUTINATION TEST; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ENCEPHALOMYELITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC MARKER; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HORSE DISEASE; IMMUNOFLUORESCENCE TEST; INVERSE POLYMERASE CHAIN REACTION; MICROSATELLITE MARKER; MOLECULAR TYPING; NONHUMAN; PARASITE IDENTIFICATION; PARASITE INCIDENCE; PARASITE VIRULENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTOZOAL GENETICS; RANDOM AMPLIFIED POLYMORPHIC DNA; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVIEW; RIBOSOME; SARCOCYSTIS NEURONA; SEQUENCE ANALYSIS;

ANIMALS; ENCEPHALOMYELITIS; HORSE DISEASES; HORSES; MOLECULAR DIAGNOSTIC TECHNIQUES; SARCOCYSTIS; SARCOCYSTOSIS;

EQUIDAE; SARCOCYSTIS; SARCOCYSTIS NEURONA;

EID: 34548557527     PISSN: 03044017     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetpar.2007.06.039     Document Type: Review

References (65)

1. Arbeit R.D. Laboratory procedures for the epidemiologic analysis of microorganisms. sixth ed. (1995), ASM Press, Washington, D.C. pp. 190-208
2. Asmundsson I.M., Dubey J.P., and Rosenthal B.M. A genetically diverse but distinct North American population of Sarcocystis neurona includes an overrepresented clone described by 12 microsatellite alleles. Infect. Genet. Evol. 6 (2006) 352-360
3. Asmundsson I.M., and Rosenthal B.M. Isolation and characterization of microsatellite markers from Sarcocystis neurona, a causative agent of equine protozoal myeloencephalitis. Mol. Ecol. Notes 6 (2006) 8-10
4. Blears M.J., De Grandis S.A., Lee H., and Trevors J.T. Amplified fragment length polymorphism (AFLP): review of the procedure and its applications. J. Ind. Microbiol. Biotechnol. 21 (1999) 99-114
5. Blears M.J., Pokorny N.J., Carreno R.A., Chen S., De Grandis S.A., Lee H., and Trevors J.T. DNA fingerprinting of Cryptosporidium parvum isolates using amplified fragment length polymorphism (AFLP). J. Parasitol. 86 (2000) 838-841
6. Box E.D., Meier J.L., and Smith J.H. Description of Sarcocystis falcatula stiles, 1893. A parasite of birds and opossums. J. Protozool. 31 (1984) 521-524
7. Butcher M., Lakritz J., Halaney A., Branson K., Gupta G.D., Kreeger J., and Marsh A.E. Experimental inoculation of domestic cats (Felis domesticus) with Sarcocystis neurona or S. neurona-like merozoites. Vet. Parasitol. 107 (2002) 1-14
8. Cheadle M.A., Tanhauser S.M., Dame J.B., Sellon D.C., Hines M., Ginn P.E., MacKay R.J., and Greiner E.C. The nine-banded armadillo (Dasypus novemcinctus) is an intermediate host for Sarcocystis neurona. Int. J. Parasitol. 31 (2001) 330-335
9. Cheadle M.A., Yowell C.A., Sellon D.C., Hines M., Ginn P.E., Marsh A.E., MacKay R.J., Dame J.B., and Greiner E.C. The striped skunk (Mephitis mephitis) is an intermediate host for Sarcocystis neurona. Int. J. Parasitol. 31 (2001) 843-849
10. Daft B.M., Barr B.C., Gardner I.A., Read D., Bell W., Peyser K.G., Ardans A., Kinde H., and Morrow J.K. Sensitivity and specificity of Western blot testing of cerebrospinal fluid and serum for diagnosis of equine protozoal myeloencephalitis in horses with and without neurologic abnormalities. J. Am. Vet. Med. Assoc. 221 (2002) 1007-1013
11. Dirikolu L., Karpiesiuk W., Lehner A.F., Hughes C., Woods W.E., Harkins J.D., Boyles J., Atkinson A., Granstrom D.E., and Tobin T. New therapeutic approaches for equine protozoal myeloencephalitis: pharmacokinetics of diclazuril sodium salts in horses. Vet. Ther. 7 (2006) 52-63, 72
12. Duarte P.C., Ebel E.D., Traub-Dargatz J., Wilson W.D., Conrad P.A., and Gardner I.A. Indirect fluorescent antibody testing of cerebrospinal fluid for diagnosis of equine protozoal myeloencephalitis. Am. J. Vet. Res. 67 (2006) 869-876
13. Dubey J.P. Prevalence of sarcocystis species sporocysts in wild-caught opossums (Didelphis virginiana). J. Parasitol. 86 (2000) 705-710
14. Dubey J.P., Chapman J.L., Rosenthal B.M., Mense M., and Schueler R.L. Clinical Sarcocystis neurona, Sarcocystis canis, Toxoplasma gondii, and Neospora caninum infections in dogs. Vet. Parasitol. 137 (2006) 36-49
15. Dubey J.P., Davis S.W., Speer C.A., Bowman D.D., de Lahunta A., Granstrom D.E., Topper M.J., Hamir A.N., Cummings J.F., and Suter M.M. Sarcocystis neurona n. sp. (Protozoa: Apicomplexa), the etiologic agent of equine protozoal myeloencephalitis. J. Parasitol. 77 (1991) 212-218
16. Dubey J.P., Kerber C.E., Lindsay D.S., Kasai N., and Pena H.F. The South American opossum, Didelphis marsupialis, from Brazil as another definitive host for Sarcocystis speeri Dubey and Lindsay, 1999. Parasitology 121 Pt 6 (2000) 589-594
17. Dubey J.P., Lindsay D.S., Fritz D., and Speer C.A. Structure of Sarcocystis neurona sarcocysts. J. Parasitol. 87 (2001) 1323-1327
18. Dubey J.P., Lindsay D.S., Saville W.J., Reed S.M., Granstrom D.E., and Speer C.A. A review of Sarcocystis neurona and equine protozoal myeloencephalitis (EPM). Vet. Parasitol. 95 (2001) 89-131
19. Dubey J.P., Saville W.J., Stanek J.F., Lindsay D.S., Rosenthal B.M., Oglesbee M.J., Rosypal A.C., Njoku C.J., Stich R.W., Kwok O.C., Shen S.K., Hamir A.N., and Reed S.M. Sarcocystis neurona infections in raccoons (Procyon lotor): evidence for natural infection with sarcocysts, transmission of infection to opossums (Didelphis virginiana), and experimental induction of neurologic disease in raccoons. Vet. Parasitol. 100 (2001) 117-129
20. Dubey J.P., Zarnke R., Thomas N.J., Wong S.K., Van Bonn W., Briggs M., Davis J.W., Ewing R., Mense M., Kwok O.C., Romand S., and Thulliez P. Toxoplasma gondii, Neospora caninum, Sarcocystis neurona, and Sarcocystis canis-like infections in marine mammals. Vet. Parasitol. 116 (2003) 275-296
21. Elsheikha H.M., Lacher D.W., and Mansfield L.S. Phylogenetic relationships of Sarcocystis neurona of horses and opossums to other cyst-forming coccidia deduced from SSUrRNA gene sequences. Parasitol. Res. 97 (2005) 345-357
22. Elsheikha H.M., and Mansfield L.S. Sarcocystis neurona major surface antigen gene 1 (SAG1) shows evidence of having evolved under positive selection pressure. Parasitol. Res. 94 (2004) 452-459
23. Elsheikha H.M., Murphy A.J., and Mansfield L.S. Phylogenetic congruence of Sarcocystis neurona Dubey et al., 1991 (Apicomplexa: Sarcocystidae) in the United States based on sequence analysis and restriction fragment length polymorphism (RFLP). Syst. Parasitol. 61 (2005) 191-202
24. Elsheikha H.M., Schott II H.C., and Mansfield L.S. Genetic variation among isolates of Sarcocystis neurona the agent of protozoal myeloencephalitis, as revealed by amplified fragment length polymorphism markers. Infect. Immun. 74 (2006) 3448-3454
25. Fenger C.K., Granstrom D.E., Langemeier J.L., Gajadhar A., Cothran G., Tramontin R.R., Stamper S., and Dubey J.P. Phylogenetic relationship of Sarcocystis neurona to other members of the family Sarcocystidae based on small subunit ribosomal RNA gene sequence. J. Parasitol. 80 (1994) 966-975
26. Fenger C.K., Granstrom D.E., Langemeier J.L., Stamper S., Donahue J.M., Patterson J.S., Gajadhar A.A., Marteniuk J.V., Xiaomin Z., and Dubey J.P. Identification of opossums (Didelphis virginiana) as the putative definitive host of Sarcocystis neurona. J. Parasitol. 81 (1995) 916-919
27. Furr M., McKenzie H., Saville W.J., Dubey J.P., Reed S.M., and Davis W. Prophylactic administration of ponazuril reduces clinical signs and delays seroconversion in horses challenged with Sarcocystis neurona. J. Parasitol. 92 (2006) 637-643
28. Gaji R.Y., Zhang D., Breathnach C.C., Vaishnava S., Striepen B., and Howe D.K. Molecular genetic transfection of the coccidian parasite Sarcocystis neurona. Mol. Biochem. Parasitol. 150 (2006) 1-9
29. Gerhold R.W., Howerth E.W., and Lindsay D.S. Sarcocystis neurona-associated meningoencephalitis and description of intramuscular sarcocysts in a fisher (Martes pennanti). J. Wildl. Dis. 41 (2005) 224-230
30. Goehring L.S., and Sloet van Oldruitenborgh-Oosterbaan M.M. Equine protozoal myeloencephalitis in the Netherlands? An overview. Tijdschr Diergeneeskd 126 (2001) 346-351
31. Granstrom D.E., Dubey J.P., and Giles R.C. Equine protozoal myeloencephalitis: biology and epidemiology. Equine Infectious Diseases VII Proceedings of the Seventh International Conference (1994) 109-111
32. Granstrom D.E., MacPherson J.M., Gajadhar A.A., Dubey J.P., Tramontin R., and Stamper S. Differentiation of Sarcocystis neurona from eight related coccidia by random amplified polymorphic DNA assay. Mol. Cell Probes 8 (1994) 353-356
33. Hoane J.S., Gennari S.M., Dubey J.P., Ribeiro M.G., Borges A.S., Yai L.E., Aguiar D.M., Cavalcante G.T., Bonesi G.L., and Howe D.K. Prevalence of Sarcocystis neurona and Neospora spp. infection in horses from Brazil based on presence of serum antibodies to parasite surface antigen. Vet. Parasitol. 136 (2006) 155-159
34. Hoane J.S., Morrow J.K., Saville W.J., Dubey J.P., Granstrom D.E., and Howe D.K. Enzyme-linked immunosorbent assays for detection of equine antibodies specific to Sarcocystis neurona surface antigens. Clin. Diagn. Lab. Immunol. 12 (2005) 1050-1056
35. Howe D.K. Initiation of a Sarcocystis neurona expressed sequence tag (EST) sequencing project: a preliminary report. Vet. Parasitol. 95 (2001) 233-239
36. Howe D.K., Gaji R.Y., Mroz-Barrett M., Gubbels M.J., Striepen B., and Stamper S. Sarcocystis neurona merozoites express a family of immunogenic surface antigens that are orthologues of the Toxoplasma gondii surface antigens (SAGs) and SAG-related sequences. Infect. Immun. 73 (2005) 1023-1033
37. Hyun C., Gupta G.D., and Marsh A.E. Sequence comparison of Sarcocystis neurona surface antigen from multiple isolates. Vet. Parasitol. 112 (2003) 11-20
38. Jenkins M.C., Ellis J.T., Liddell S., Ryce C., Munday B.L., Morrison D.A., and Dubey J.P. The relationship of Hammondia hammondi and Sarcocystis mucosa to other heteroxenous cyst-forming coccidia as inferred by phylogenetic analysis of the 18S SSU ribosomal DNA sequence. Parasitology 119 Pt 2 (1999) 135-142
39. Li L., Brunk B.P., Kissinger J.C., Pape D., Tang K., Cole R.H., Martin J., Wylie T., Dante M., Fogarty S.J., Howe D.K., Liberator P., Diaz C., Anderson J., White M., Jerome M.E., Johnson E.A., Radke J.A., Stoeckert Jr. C.J., Waterston R.H., Clifton S.W., Roos D.S., and Sibley L.D. Gene discovery in the apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Res. 13 (2003) 443-454
40. Li L., Crabtree J., Fischer S., Pinney D., Stoeckert Jr. C.J., Sibley L.D., and Roos D.S. ApiEST-DB: analyzing clustered EST data of the apicomplexan parasites. Nucl. Acids Res. 32 (2004) D326-D328
41. Lindsay D.S., and Dubey J.P. Direct agglutination test for the detection of antibodies to Sarcocystis neurona in experimentally infected animals. Vet. Parasitol. 95 (2001) 179-186
42. Lindsay D.S., Dubey J.P., Horton K.M., and Bowman D.D. Development of Sarcocystis falcatula in cell cultures demonstrates that it is different from Sarcocystis neurona. Parasitology 118 Pt 3 (1999) 227-233
43. Maddison W. Phylogenetic Histories Within and Among Species (1995), Missouri Botanical Garden, St. Louis pp. 273-287
44. Mansfield L.S., Schott H.C., Murphy A.J., Rossano M.G., Tanhauser S.M., Patterson J.S., Nelson K., Ewart S.L., Marteniuk J.V., Bowman D.D., and Kaneene J.B. Comparison of Sarcocystis neurona isolates derived from horse neural tissue. Vet. Parasitol. 95 (2001) 167-178
45. Marsh A.E., Barr B.C., Madigan J., Lakritz J., and Conrad P.A. Sequence analysis and polymerase chain reaction amplification of small subunit ribosomal DNA from Sarcocystis neurona. Am. J. Vet. Res. 57 (1996) 975-981
46. Marsh A.E., Barr B.C., Tell L., Bowman D.D., Conrad P.A., Ketcherside C., and Green T. Comparison of the internal transcribed spacer, ITS-1, from Sarcocystis falcatula isolates and Sarcocystis neurona. J. Parasitol. 85 (1999) 750-757
47. Murphy J.E., Marsh A.E., Reed S.M., Meadows C., Bolten K., and Saville W.J. Development and evaluation of a Sarcocystis neurona-specific IgM capture enzyme-linked immunosorbent assay. J. Vet. Intern. Med. 20 (2006) 322-328
48. NAHMS, 2001. Equine protozoal myeloencephalitis (EPM) in the U.S. USDA:APHIS:VS, CEAH, National Animal Health Monitoring System #N312.0501.
49. Pitel P.H., Lindsay D.S., Caure S., Romand S., Pronost S., Gargala G., Mitchell S.M., Hary C., Thulliez P., Fortier G., and Ballet J.J. Reactivity against Sarcocystis neurona and Neospora by serum antibodies in healthy French horses from two farms with previous equine protozoal myeloencephalitis-like cases. Vet. Parasitol. 111 (2003) 1-7
50. Rosenthal B.M., Lindsay D.S., and Dubey J.P. Relationships among Sarcocystis species transmitted by New World opossums (Didelphis spp.). Vet. Parasitol. 95 (2001) 133-142
51. Rossano M.G., Kaneene J.B., Marteniuk J.V., Banks B.D., Schott II H.C., and Mansfield L.S. A herd-level analysis of risk factors for antibodies to Sarcocystis neurona in Michigan equids. Prev. Vet. Med. 57 (2003) 7-13
52. Rossano M.G., Mansfield L.S., Kaneene J.B., Murphy A.J., Brown C.M., Schott II H.C., and Fox J.C. Improvement of Western blot test specificity for detecting equine serum antibodies to Sarcocystis neurona. J. Vet. Diagn. Invest. 12 (2000) 28-32
53. Rossano M.G., Mansfield L.S., Kaneene J.B., Murphy A.J., Brown C.M., Schott H.C., and Fox J.C. Improvement of Western blot test specificity for detecting equine serum antibodies to Sarcocystis neurona. J. Vet. Diagn. Invest. 12 (2000) 28-32
54. Saville W.J., Dubey J.P., Oglesbee M.J., Sofaly C.D., Marsh A.E., Elitsur E., Vianna M.C., Lindsay D.S., and Reed S.M. Experimental infection of ponies with Sarcocystis fayeri and differentiation from Sarcocystis neurona infections in horses. J. Parasitol. 90 (2004) 1487-1491
55. Siemer B.L., Nielsen E.M., and On S.L. Identification and molecular epidemiology of Campylobacter coli isolates from human gastroenteritis, food, and animal sources by amplified fragment length polymorphism analysis and Penner serotyping. Appl. Environ. Microbiol. 71 (2005) 1953-1958
56. Slapeta J.R., Modry D., Votypka J., Jirku M., Koudela B., and Lukes J. Multiple origin of the dihomoxenous life cycle in sarcosporidia. Int. J. Parasitol. 31 (2001) 413-417
57. Slapeta J.R., Modry D., Votypka J., Jirku M., Lukes J., and Koudela B. Evolutionary relationships among cyst-forming coccidia Sarcocystis spp. (Alveolata: Apicomplexa: Coccidea) in endemic African tree vipers and perspective for evolution of heteroxenous life cycle. Mol. Phylogenet. Evol. 27 (2003) 464-475
58. Tanhauser S.M., Cheadle M.A., Massey E.T., Mayer B.A., Schroedter D.E., Dame J.B., Greiner E.C., and MacKay R.J. The nine-banded armadillo (Dasypus novemcinctus) is naturally infected with Sarcocystis neurona. Int. J. Parasitol. 31 (2001) 325-329
59. Tanhauser S.M., Yowell C.A., Cutler T.J., Greiner E.C., MacKay R.J., and Dame J.B. Multiple DNA markers differentiate Sarcocystis neurona and Sarcocystis falcatula. J. Parasitol. 85 (1999) 221-228
60. Tenover F.C., Arbeit R.D., and Goering R.V. How to select and interpret molecular strain typing methods for epidemiological studies of bacterial infections: a review for healthcare epidemiologists. Molecular Typing Working Group of the Society for Healthcare Epidemiology of America. Infect. Contr. Hosp. Epidemiol. 18 (1997) 426-439
61. Tibayrenc M. Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. Int. J. Parasitol. 28 (1998) 85-104
62. Vaishnava S., Morrison D.P., Gaji R.Y., Murray J.M., Entzeroth R., Howe D.K., and Striepen B. Plastid segregation and cell division in the apicomplexan parasite Sarcocystis neurona. J. Cell Sci. 118 (2005) 3397-3407
63. van Belkum A., Struelens M., de Visser A., Verbrugh H., and Tibayrenc M. Role of genomic typing in taxonomy, evolutionary genetics, and microbial epidemiology. Clin. Microbiol. Rev. 14 (2001) 547-560
64. Vos P., Hogers R., Bleeker M., Reijans M., van de Lee T., Hornes M., Frijters A., Pot J., Peleman J., Kuiper M., et al. AFLP: a new technique for DNA fingerprinting. Nucl. Acids Res. 23 (1995) 4407-4414
65. Zhang D., Gaji R.Y., and Howe D.K. Identification of a dithiol-dependent nucleoside triphosphate hydrolase in Sarcocystis neurona. Int. J. Parasitol. 36 (2006) 1197-1204