Seroprevalence of antibodies against Anaplasma phagocytophilum and Borrelia burgdorferi in horses (Equus caballus) from northern Algeria

Laamari, Abdelouahab; Azzag, Naouelle; Tennah, Safia; Derdour, Salima-Yamina; China, Bernard; Bouabdallah, Ryhan; Ghalmi, Farida

doi:10.2478/jvetres-2020-0045

Abstract

Introduction

Horses (Equus caballus) are susceptible to tick-borne diseases. Two of them, Lyme borreliosis due to Borrelia burgdorferi and granulocytic anaplasmosis due to Anaplasma phagocytophilum were investigated in Algerian horses. The diseases have been less extensively studied in horses and results pertinent to Algeria have not been published.

Material and Methods

Blood samples were obtained from 128 horses. IgG antibodies directed against Anaplasma phagocytophilum and Borrelia burgdorferi were detected by an indirect immunofluorescence antibody test (IFAT) and ELISA. The potential effects of age, gender, breed, and health status on seropositivity were also evaluated.

Results

Using IFAT, 28 (21.8%) and 25 (19.5%) animals were positive for B. burgdorferi and A. phagocytophilum, respectively. Using ELISA, 19 (14.8%) and 33 (25.9%) animals were positive for these bacteria.

Conclusion

The study shows that horses in Algeria are exposed or co-exposed to tick-transmitted zoonotic bacterial species.

References

Amusategui I., Sainz A., Tesouro M.A.: Serological evaluation of Anaplasma phagocytophilum infection in livestock in northwestern Spain. Ann N Y Acad Sci 2006, 1078, 487–490.
Search in Google Scholar Back to article
Azzag N., Petit E., Gandoin C., Bouillin C., Ghalmi F., Haddad N., Boulouis H.J.: Prevalence of select vector-borne pathogens in stray and client-owned dogs from Algiers. Comp Immunol Microbiol Infect Dis 2015, 38, 1–7.
Search in Google Scholar Back to article
Bensaid M., Belkahia H., Sayahi L., Aloui M., Jemli M.H., Hadj Mohamed B., Sassi L., Darghouth M.A., Djaïem A.A., Bayoudh M., Messadi L.: Première étude sérologique de la prévalence d’Anaplasma phagocytophilum chez le dromadaire Camelus dromedarius en Tunisie. Bull Soc Pathol Exot 2014, 107, 1–6.
Search in Google Scholar Back to article
Bermann F., Davoust B., Fournier P.E., Brisou-Lapointe A.V., Brouqui P.: Ehrlichia equi Anaplasma phagocytophila infection in an adult horse in France. Vet Rec 2002, 150, 787–788.
Search in Google Scholar Back to article
Bhide M., Yilmaz Z., Golcu E., Torun S., Mikula I.: Seroprevalence of anti-Borrelia burgdorferi antibodies in dogs and horses in Turkey. Ann Agric Environ Med 2008, 15, 85–90.
Search in Google Scholar Back to article
Burgess B.: British Columbia. Lyme disease in horses. Can Vet J 1988, 29, 393–394.
Search in Google Scholar Back to article
Büscher G., Gandras R., Apel G., Friedhoff K.T.: The 1st case of ehrlichiosis in a horse in Germany. Dtsch Tierarztl Wochenschr 1984, 91, 408–409.
Search in Google Scholar Back to article
Devilbiss B., Mohammed H.O., Divers T.J.: Perception of equine practitioners regarding the occurrence of selected equine neurologic diseases in the Northeast over a 10-year period. J Equine Vet Sci 2009, 29, 237–246.
Search in Google Scholar Back to article
Durrani A.Z., Goyal S.M., Kamal N.: Retrospective study on seroprevalence of Borrelia burgdorferi antibodies in horses in Minnesota. T Equine Vet Sci 2011, 31, 427–429.
Search in Google Scholar Back to article
Dzierzecka M., Kita J.: The use of chosen serological diagnostic methods in Lyme disease in horses. Part I. Indirect immunofluorescence and enzyme-linked immunosorbent assay (ELISA). Pol J Vet Sci 2002, 5, 71–77.
Search in Google Scholar Back to article
Ebani V.V., Bertelloni F., Pinzauti P., Cerri D.: Seroprevalence of Leptospira spp. and Borrelia burgdorferi sensu lato in Italian horses. Ann Agric Environ Med 2012, 19, 237–240.
Search in Google Scholar Back to article
Ebani V.V.: Serological evidence of Anaplasma phagocytophilum and spotted fever group Rickettsia spp. exposure in horses from central Italy. Pathogens 2019, 8, 88.
Search in Google Scholar Back to article
Egenvall A., Franzén P., Gunnarsson A., Engvall E.O., Vågsholm I., Wikström U.B., Artursson K.: Cross-sectional study of the seroprevalence to Borrelia burgdorferi sensu lato and granulocytic Ehrlichia spp and demographic, clinical and tick-exposure factors in Swedish horses. Prev Vet Med 2001, 49, 191–208.
Search in Google Scholar Back to article
Elelu N.: Tick-borne relapsing fever as a potential veterinary medical problem.Vet Med Sci 2018, 4, 271–279.
Search in Google Scholar Back to article
Hermann M.: Colitis X in the horse: 9 cases. Schweiz Arch Tierheilkd 1985, 127, 385–396.
Search in Google Scholar Back to article
Imai D.M., Barr B.C., Daft B., Bertone J.J., Feng S., Hodzic E., Johnston J.M., Olsen K.J., Barthold S.W.: Lyme neuroborreliosis in 2 horses. Vet Pathol 2011, 48, 1151–1157.
Search in Google Scholar Back to article
Johnson A.L., Divers T.J., Chang Y.F.: Validation of an in-clinic enzyme-linked immunosorbent assay kit for diagnosis of Borrelia burgdorferi infection in horses. J Vet Diagn Invest 2008, 20, 321–324.
Search in Google Scholar Back to article
Kiss T., Cadar D., Krupaci A.F., Bordeanu A., Brudaşcă G.F., Mihalca A.D., Mircean V., Gliga L., Dumitrache M.O., Spînu M.: Serological reactivity to Borrelia burgdorferi sensu lato in dogs and horses from distinct areas in Romania. Vector Borne Zoonotic Dis 2011, 11, 1259–1262.
Search in Google Scholar Back to article
Korbutiak E., Schneiders D.: Equine granulocytic ehrlichiosis in the UK. Vet Rec 1994, 135, 387–388.
Search in Google Scholar Back to article
Laus F., Veronesi F., Passamonti F., Paggi E., Cerquetella M., Hyatt D., Tesei B., Fioretti D.P.: Prevalence of tick borne pathogens in horses from Italy. J Vet Med Sci 2013, 75, 715–720.
Search in Google Scholar Back to article
Leblond A., Pradier S., Pitel P.H., Fortier G., Boireau P., Chadoeuf J., Sabatier P.: Enquête épidémiologique sur l’anaplasmose équine Anaplasma phagocytophilum dans le Sud de la France. Rev Sci Tech 2005, 24, 899–908.
Search in Google Scholar Back to article
Lee S.H., Yun S.H., Choi E., Park Y.S., Lee S.E., Cho G.J., Kwon O.D., Kwak D.: Serological detection of Borrelia burgdorferi among horses in Korea. Korean J Parasitol 2016, 54, 97–101.
Search in Google Scholar Back to article
Madigan J.E., Gribble D.: Equine ehrlichiosis in northern California: 49 cases (1968–1981). J Am Vet Med Assoc 1987, 190, 445–448.
Search in Google Scholar Back to article
Maloney E.M., Lindenmayer J.L.: Seroprevalence and clinical signs of Lyme disease in Cape Cod horses. Eq Pract 1992, 14, 15–19.
Search in Google Scholar Back to article
Maurizi L., Marié J.L., Aoun O., Courtin C., Gorsane S., Chal D., Davoust B.: Seroprevalence survey of equine Lyme borreliosis in France and in sub-Saharan Africa. Vector Borne Zoonotic Dis 2010, 10, 535–537.
Search in Google Scholar Back to article
Passamonti F., Veronesi F., Cappelli K., Capomaccio S., Reginato A., Miglio A., Vardi D.M., Stefanetti V., Coletti M., Bazzica C., Pepe M.: Polysynovitis in a horse due to Borrelia burgdorferi sensu lato infection – Case study. Ann Agric Environ Med 2015, 22, 247–250.
Search in Google Scholar Back to article
Petrie A., Watson P.: Statistics for Veterinary and Animal Science, Wiley Blackwell, Chichester, 2013.
Search in Google Scholar Back to article
Pusterla N., Madigan J.E.: Initial clinical impressions of the U.C. Davis large animal lift and its use in recumbent equine patients. Schweiz Arch Tierheilkd 2006, 148, 161–166.
Search in Google Scholar Back to article
Saleem S., Ijaz M., Farooqi S.H., Ghaffar A., Ali A., Iqbal K., Mehmood K., Zhang H.: Equine granulocytic anaplasmosis 28 years later. Microb Pathog 2018, 119, 1–8.
Search in Google Scholar Back to article
Saleem S., Ijaz M., Farooqi S.H., Rashid M.I., Khan A., Masud A., Aqib A.I., Hussain K., Mehmood K., Zhang H.: First molecular evidence of equine granulocytic anaplasmosis in Pakistan. Acta Trop 2018, 180, 18–25.
Search in Google Scholar Back to article
Salinas-Mélendez J.A., Galván de la Garza S., Riojas-Valdés V.M., Wong González A., Avalos-Ramírez R.: Antibody detection against Borrelia burgdorferi in horses located in the suburban areas of Monterrey, Nuevo León. Rev Latinoam Microbiol 2001, 43, 161–164.
Search in Google Scholar Back to article
Scarpulla M., Caristo M.E., Macri G., Lillini E.: Equine ehrlichiosis in Italy. Ann N Y Acad Sci 2003, 990, 259–263.
Search in Google Scholar Back to article
Schvartz G., Epp T., Burgess H.J., Chilton N.B., Lohmann K.L.: Comparison between available serologic tests for detecting antibodies against Anaplasma phagocytophilum and Borrelia burgdorferi in horses in Canada. J Vet Diagn Invest 2015, 27, 540–546.
Search in Google Scholar Back to article
Socoloski S.N.G., de Castro B.G., Cordeiro M.D., da Fonseca A.H., Cepeda M.B., Nicolino R.R., Lopes L.B.: Epidemiological investigation of Borrelia burgdorferi in horses in the municipality of Sinop-MT, Brazil. Trop Anim Health Prod 2018, 50, 831–836.
Search in Google Scholar Back to article
Stefanciková A., Adaszek L., Pet'ko B., Winiarczyk S., Dudinák V.: Serological evidence of Borrelia burgdorferi sensu lato in horses and cattle from Poland and diagnostic problems of Lyme borreliosis. Ann Agric Environ Med 2008, 15, 37–43.
Search in Google Scholar Back to article
Thrusfield M., Ortega C., De Blas I., Noordhuizen J.P., Frankena K.: Win Episcope 2.0: improved epidemiological software for veterinary medicine. Vet Rec 2001, 148, 567–572
Search in Google Scholar Back to article
Tsachev I., Pantchev N., Marutsov P., Petrov V., Gundasheva D., Baymakova M.: Serological evidence of Borrelia burgdorferi Anaplasma phagocytophilum and Ehrlichia spp. infections in horses from Southeastern Bulgaria. Vector Borne Zoonotic Dis 2018, 18, 588–594.
Search in Google Scholar Back to article
Veronesi F., Laus F., Passamonti F., Tesei B., Piergili Fioretti D., Genchi C.: Occurrence of Borrelia lusitaniae infection in horses. Vet Microbiol 2012, 160, 535–538.
Search in Google Scholar Back to article
von Fricken M.E., Sukhbaatar L., Boldbaatar B., Nymadawa P., Weppelmann T.A., Baigalmaa B.O., Anderson B.D., Reller M.E., Lantos P.M., Gray G.C.: Estimated seroprevalence of Anaplasma spp. and spotted fever group Rickettsia exposure among herders and livestock in Mongolia. Acta Trop 2018, 177, 179–185.
Search in Google Scholar Back to article
Wagner B., Erb H.N.: Dogs and horses with antibodies to outer-surface protein C as on-time sentinels for ticks infected with Borrelia burgdorferi in New York State in 2011. Prev Vet Med 2012, 107, 275–279.
Search in Google Scholar Back to article