Parasitology Research

, Volume 107, Issue 5, pp 1241–1248 | Cite as

Development and laboratory evaluation of a lateral flow device (LFD) for the serodiagnosis of Theileria annulata infection

  • Jassim Abdo
  • Therese Kristersson
  • Ulrike Seitzer
  • Stefanie Renneker
  • Malik Merza
  • Jabbar Ahmed
Original Paper

Abstract

Several DNA-based and serological tests have been established for the detection of Theileria annulata infection, including polymerase chain reaction, reverse line blot and loop-mediated isothermal amplification, indirect enzyme-linked immunosorbent assay (ELISA), and competitive ELISA. In this study, we have applied knowledge from the development and application of a recombinant protein-based indirect ELISA and competitive ELISA to establish a rapid test for point-of-care diagnosis of T. annulata infection in the field to be used by the veterinarian. For the development of a lateral flow test, the recombinantly expressed T. annulata surface protein (TaSP) was applied as the test antigen and anti-TaSP antiserum as the control line. TaSP antigen conjugated to colloidal gold particles was used as the detection system for visualization at the test line for the binding of anti-TaSP antibody present in the serum of infected animals. The developed test specifically detected antibodies in the serum of animals experimentally infected with T. annulata and showed no cross-reactivity with serum from animals infected with other tested bovine pathogens (Trypanosoma brucei, Anaplasma marginale, Babesia bigemina, Babesia bovis, and Theileria parva). Testing of field samples was compared to results obtained by other serological tests, resulting in a sensitivity and specificity of 96.3% and 87.5% compared to indirect fluorescence antibody test, 98.7% and 81.8% compared to indirect ELISA, and 100% and 47.6% compared to competitive ELISA. In conclusion, a rapid test for the detection of T. annulata infection (T. annulata lateral flow device, Ta-LFD) has been developed, which is easy to perform, delivers results to be read by the naked eye within 10 min, and is suitable for the detection of infection in field samples.

Keywords

Indirect ELISA Reference Test Babesia Competitive ELISA Indirect Fluorescence Antibody Test 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This study was supported in part by the EU-funded Coordinated Action “Integrated Consortium on Ticks and Tick-Borne Diseases” (ICTTD-3), project number 510561.

References

  1. Ahmed JS, Rothert M, Steuber S, Schein E (1989) In vitro proliferative and cytotoxic responses of PBL from Theileria annulata-immune cattle. Zentralbl Veterinärmed B 36:584–592PubMedGoogle Scholar
  2. Bakheit MA, Schnittger L, Salih DA, Boguslawski K, Beyer D, Fadl M, Ahmed JS (2004) Application of the recombinant Theileria annulata surface protein in an indirect ELISA for the diagnosis of tropical theileriosis. Parasitol Res 92:299–302CrossRefPubMedGoogle Scholar
  3. Bakheit MA, Seitzer U, Ahmed JS (2006) A new recombinant protein-based ELISA for the diagnosis of malignant theileriosis of sheep and goats. Parasitol Res 98:145–149CrossRefPubMedGoogle Scholar
  4. Bishop YMM, Feinberg SE, Holland PW (1975) Discrete multivariate analysis. MIT Press, CambridgeGoogle Scholar
  5. Brüning A, Bellamy K, Talbot D, Anderson J (1999) A rapid chromatographic strip test for the pen-side diagnosis of rinderpest virus. J Virol Methods 81:143–154CrossRefPubMedGoogle Scholar
  6. Burridge MJ, Kimber CD (1973) Duration of serological response to the indirect fluorescent antibody test of cattle recovered from Theileria parva infection. Res Vet Sci 14:270–271PubMedGoogle Scholar
  7. Burridge MJ, Brown CG, Kimber CD (1974) Theileria annulata: cross-reactions between a cell culture schizont antigen and antigens of East African species in the indirect fluorescent antibody test. Exp Parasitol 35:374–380CrossRefPubMedGoogle Scholar
  8. Chan R, Chen J, York MK, Setijono N, Kaplan RL, Graham F, Tanowitz HB (2000) Evaluation of a combination rapid immunoassay for detection of Giardia and cryptosporidium antigens. J Clin Microbiol 38:393–394PubMedGoogle Scholar
  9. Darghouth ME, Bouattour A, Ben Miled L, Sassi L (1996) Diagnosis of Theileria annulata infection of cattle in Tunisia: comparison of serology and blood smears. Vet Res 27:613–621PubMedGoogle Scholar
  10. Dhar S, Gautam OP (1977) Indirect fluorescent antibody test for serodiagnosis in cattle infected with Theileria annulata. Indian J Anim Sci 47:720–723Google Scholar
  11. Dolan TT (1989) Theileriosis: a comprehensive review. Rev Sci Tech 8:11–36Google Scholar
  12. d'Oliveira C, van der Weide M, Habela MA, Jacquiet P, Jongejan F (1995) Detection of Theileria annulata in blood samples of carrier cattle by PCR. J Clin Microbiol 33:2665–2669PubMedGoogle Scholar
  13. Ferris NP, Nordengrahn A, Hutchings GH, Reid SM, King DP, Ebert K, Paton DJ, Kristersson T, Brocchi E, Grazioli S, Merza M (2009) Development and laboratory validation of a lateral flow device for the detection of foot-and-mouth disease virus in clinical samples. J Virol Methods 155:10–17CrossRefPubMedGoogle Scholar
  14. Friedhoff KT (1997) Tick-borne diseases of sheep and goats caused by Babesia, Theileria or Anaplasma spp. Parassitologia 39:99–109PubMedGoogle Scholar
  15. Gubbels JM, de Vos AP, van der Weide M, Viseras J, Schouls LM, de Vries E, Jongejan F (1999) Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. J Clin Microbiol 37:1782–1789PubMedGoogle Scholar
  16. Gubbels MJ, d'Oliveira C, Jongejan F (2000) Development of an indirect Tams1 enzyme-linked immunosorbent assay for diagnosis of Theileria annulata infection in cattle. Clin Diagn Lab Immunol 7:404–411PubMedGoogle Scholar
  17. Habibi GR, Esmaeil-Nia K, Bozorgi S, Najjar E, Hashemi-Fesharki R, Bordbar N (2007) PCR-based detection of Theileria annulata infection and molecular characterization of Tams I T. annulata vaccine strain. Arch Razi Inst 62:83–89Google Scholar
  18. Hooshmand-Rad P (1974) Blood protozoan diseases of ruminants. Bull Off Int Epizoot 81:779–792Google Scholar
  19. Houghton RL, Stevens YY, Hjerrild K, Guderian J, Okamoto M, Kabir M, Reed SG, Leiby DA, Morrow WJ, Lorca M, Raychaudhuri S (2009) Lateral flow immunoassay for diagnosis of Trypanosoma cruzi infection with high correlation to the radioimmunoprecipitation assay. Clin Vaccine Immunol 16:515–520CrossRefPubMedGoogle Scholar
  20. Huang X, Xuan X, Hirata H, Yokoyama N, Xu L, Suzuki N, Igarashi I (2004a) Rapid immunochromatographic test using recombinant SAG2 for detection of antibodies against Toxoplasma gondii in cats. J Clin Microbiol 42:351–353CrossRefPubMedGoogle Scholar
  21. Huang X, Xuan X, Xu L, Zhang S, Yokoyama N, Suzuki N, Igarashi I (2004b) Development of an immunochromatographic test with recombinant EMA-2 for the rapid detection of antibodies against Babesia equi in horses. J Clin Microbiol 42:359–361CrossRefPubMedGoogle Scholar
  22. Kim C, Alhassan A, Verdida RA, Yokoyama N, Xuan X, Fujisaki K, Kawazu S, Igarashi I (2007) Development of two immunochromatographic tests for the serodiagnosis of bovine babesiosis. Vet Parasitol 148:137–143CrossRefPubMedGoogle Scholar
  23. Kim CM, Blanco LB, Alhassan A, Iseki H, Yokoyama N, Xuan X, Igarashi I (2008) Development of a rapid immunochromatographic test for simultaneous serodiagnosis of bovine babesioses caused by Babesia bovis and Babesia bigemina. Am J Trop Med Hyg 78:117–121PubMedGoogle Scholar
  24. Kirvar E, Ilhan T, Katzer F, Hooshmand-Rad P, Zweygarth E, Gerstenberg C, Phipps P, Brown CG (2000) Detection of Theileria annulata in cattle and vector ticks by PCR using the Tams1 gene sequences. Parasitology 120:245–254CrossRefPubMedGoogle Scholar
  25. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174CrossRefPubMedGoogle Scholar
  26. Liao M, Zhang S, Xuan X, Zhang G, Huang X, Igarashi I, Fujisaki K (2005) Development of rapid immunochromatographic test with recombinant NcSAG1 for detection of antibodies to Neospora caninum in cattle. Clin Diagn Lab Immunol 12:885–887PubMedGoogle Scholar
  27. Mansfield MA (2005) The use of nitrocellulose membranes in lateral-flow assays. In: Wong RC, Tse HY (eds) Forensic science and medicine: drugs of abuse: body fluid testing. Humana, Totowa, pp 71–85Google Scholar
  28. McCosker PJ (1979) Global aspects of the management and control of ticks of veterinary importance. In: Rodriguez JG (ed) Recent advances in acarology. II. Proceedings of the Vth International Congress of Acarology, East Lansing. Academic, New York, pp 45–53Google Scholar
  29. Mills CD, Burgess DC, Taylor HJ, Kain KC (1999) Evaluation of a rapid and inexpensive dipstick assay for the diagnosis of Plasmodium falciparum malaria. Bull World Health Organ 77:553–559PubMedGoogle Scholar
  30. Minjauw B, McLeod A (2000) Epidemiology and economics of tick-borne diseases: their effects on the livelihoods of the poor in East and Southern Africa and in India. Consultancy report to the Animal Health Programme (AHP) of the Department for International Development (DFID). Nairobi, Kenya, p 94Google Scholar
  31. Mohammad Al-Saeed AT, Omer LT, Abdo J, Habibi G, Salih DA, Seitzer U, Ahmed J (2010) Epidemiological studies on tropical theileriosis (Theileria annulata infection of cattle) in Kurdistan Region, Iraq. Parasitol Res 106:403–407CrossRefPubMedGoogle Scholar
  32. Reithinger R, Quinnell RJ, Alexander B, Davies CR (2002) Rapid detection of Leishmania infantum infection in dogs: comparative study using an immunochromatographic dipstick test, enzyme-linked immunosorbent assay, and PCR. J Clin Microbiol 40:2352–2356CrossRefPubMedGoogle Scholar
  33. Renneker S, Kullmann B, Gerber S, Dobschanski J, Bakheit MA, Geysen D, Shiels B, Tait A, Ahmed JS, Seitzer U (2008) Development of a competitive ELISA for detection of Theileria annulata infection. Transbound Emerg Dis 55:249–256CrossRefPubMedGoogle Scholar
  34. Renneker S, Abdo J, Ahmed JS, Seitzer U (2009) Field validation of a competitive ELISA for detection of Theileria annulata infection. Parasitol Res 106:47–53CrossRefPubMedGoogle Scholar
  35. Salih DE, Ahmed JS, Bakheit MA, Ali EB, El Hussein AM, Hassan SM, Shariff OE, Fadl M, Jongejan F (2005) Validation of the indirect TaSP enzyme-linked immunosorbent assay for diagnosis of Theileria annulata infection in cattle. Parasitol Res 97:302–308CrossRefPubMedGoogle Scholar
  36. Salih DA, El Hussein AM, Seitzer U, Ahmed JS (2007a) Epidemiological studies on tick-borne diseases of cattle in Central Equatoria State, Southern Sudan. Parasitol Res 101:1035–1044CrossRefPubMedGoogle Scholar
  37. Salih DA, Hassan SM, El Hussein AM (2007b) Comparisons among two serological tests and microscopic examination for the detection of Theileria annulata in cattle in northern Sudan. Prev Vet Med 81:323–326CrossRefPubMedGoogle Scholar
  38. Salih DA, Liu Z, Bakheit MA, Ali AM, El Hussein AM, Unger H, Viljoen G, Seitzer U, Ahmed JS (2008) Development and evaluation of a loop-mediated isothermal amplification method for diagnosis of tropical theileriosis. Transbound Emerg Dis 55:238–243CrossRefPubMedGoogle Scholar
  39. Schnittger L, Katzer F, Biermann R, Shayan P, Boguslawski K, McKellar S, Beyer D, Shiels BR, Ahmed JS (2002) Characterization of a polymorphic Theileria annulata surface protein (TaSP) closely related to PIM of Theileria parva: implications for use in diagnostic tests and subunit vaccines. Mol Biochem Parasitol 120:247–256CrossRefPubMedGoogle Scholar
  40. Schnittger L, Yin H, Qi B, Gubbels MJ, Beyer D, Niemann S, Jongejan F, Ahmed JS (2004) Simultaneous detection and differentiation of Theileria and Babesia parasites infecting small ruminants by reverse line blotting. Parasitol Res 92:189–196CrossRefPubMedGoogle Scholar
  41. Seitzer U, Bakheit MA, Salih DE, Ali A, Haller D, Yin H, Schnittger L, Ahmed J (2007) From molecule to diagnostic tool: Theileria annulata surface protein TaSP. Parasitol Res 101(Suppl 2):S217–S223CrossRefPubMedGoogle Scholar
  42. Seitzer U, Beyer D, Kullmann B, Bakheit MA, Ahmed JS (2008) Evaluation of Theileria annulata recombinant immunodominant proteins for the development of ELISA. Transbound Emerg Dis 55:244–248CrossRefPubMedGoogle Scholar
  43. Shayan P, Biermann R, Schein E, Gerdes J, Ahmed JS (1998) Detection and differentiation of Theileria annulata and Theileria parva using macroschizont-derived DNA probes. Ann N Y Acad Sci 849:88–95CrossRefPubMedGoogle Scholar
  44. Thomas EE, Puterman ML, Kawano E, Curran M (1988) Evaluation of seven immunoassays for detection of rotavirus in pediatric stool samples. J Clin Microbiol 26:1189–1193PubMedGoogle Scholar
  45. Uilenberg G (1981) Theileria species of domestic livestock. In: Irvin AD, Cunningham MP, Young AS (eds) Advances in the control of theileriosis. Proc. Internat. Conf., 9–13 Feb. 1981, Nairobi. Martinus Nijhoff, The Hague, pp 4–37Google Scholar
  46. Zhang GP, Wang XN, Yang JF, Yang YY, Xing GX, Li QM, Zhao D, Chai SJ, Guo JQ (2006) Development of an immunochromatographic lateral flow test strip for detection of beta-adrenergic agonist clenbuterol residues. J Immunol Methods 312:27–33CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Jassim Abdo
    • 1
  • Therese Kristersson
    • 2
  • Ulrike Seitzer
    • 1
  • Stefanie Renneker
    • 1
  • Malik Merza
    • 2
  • Jabbar Ahmed
    • 1
  1. 1.Division of Veterinary Infection Biology and ImmunologyResearch Center BorstelBorstelGermany
  2. 2.Svanova Biotech ABUppsala Science Park, GluntenUppsalaSweden

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