Tierarztl Prax Ausg K Kleintiere Heimtiere 2015; 43(02): 94-100
DOI: 10.15654/TPK-140409
Original Article
Schattauer GmbH

Changes in selected subpopulations of lymphocytes in dogs infected with Babesia canis treated with imidocarb

Veränderungen ausgewählter Lymphozyten-Subpopulationen bei mit Babesia canis infizierten Hunden nach Behandlung mit Imidocarb
Ł. Adaszek
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
,
Ł. Jarosz
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
,
M. Kalinowski
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
,
M. Staniec
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
,
Z. Grądzki
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
,
B. Salmons
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
2   SG Austria (Austrianova), Centros, Singapore
,
S. Winiarczyk
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
1   Department of Epizootiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
› Author Affiliations
Further Information

Publication History

Received: 08 May 2014

Accepted after revision: 10 March 2014

Publication Date:
08 January 2018 (online)

Summary

Objective: The purpose of this study was to track changes in selected subpopulations of lymphocytes in the blood of dogs infected with Babesia (B.) canis and treated with imidocarb. Material and methods: The study included 16 dogs divided into two groups. The first group (n = 6) consisted of healthy control animals. Dogs of the second group (n = 10) were infected with B. canis and after establishment of the diagnosis each animal received a single dose of imidocarb (5 mg/kg). Flow cytometry was used to enumerate several immune cell phenotypes. Results: It was concluded that the invasion of B. canis contributes to the decreased percentage of CD3+, CD4+, CD8+, CD21+ lymphocytes in the blood of infected animals. The decreased level of tested subpopulations of lymphocytes in group 2 persisted for the entire 12-day period of the test. After the administration of imidocarb, each tested lymphocyte fraction in the blood of the dogs with babesiosis increased, but did not reach physiological values. Conclusion: The presented results indicate that the resolution of clinical signs associated with babesiosis may be related to the stimulation and intensity of cellular immunity, dependent on the CD4+ T cells profile. After administration of imidocarb, the parasitemia is cleared which allows the recovery of the lymphocyte populations.

Zusammenfassung

Ziel: Ziel der Studie war herauszufinden, welche Veränderungen ausgewählter Subpopulationen von Blutlymphozyten bei Hunden auftreten, die mit Protozoen des Typs Babesia (B.) canis infiziert sind und mit Imidocarb behandelt wurden. Material und Methoden: Zur Untersuchungen dienten 16 Hunde, aufgeteilt in zwei Gruppen: Die erste Gruppe (n = 6) umfasste gesunde Kontrolltiere, die zweite Gruppe mit B. canis infizierte Hunde (n = 10), die nach Diagnose der Krankheit einmalig Imidocarb in einer Dosis von 5 mg/kg erhielten. Mittels Durchflusszytometrie wurden verschiedene Phänotypen von Immunzellen bestimmt. Ergebnisse: Die Invasion der B.-canis-Protozoen führt zur Reduzierung des prozentualen Anteils an Lymphozyten des Typs CD3+, CD4+, CD8+ und CD21+ im Blut der kranken Tiere im Vergleich zu gesunden Individuen. Das gesunkene Niveau der untersuchten Subpopulationen von Lymphozyten in Gruppe 2 blieb im gesamten 12-tägigen Untersuchungszeitraum konstant. Nach der Verabreichung von Imidocarb stieg der Anteil jeder der untersuchten Lymphozyten-Subpopulationen im Blut der Hunde mit diagnostizierter Babesiose an, wobei keine physiologischen Werte erreicht wurden. Schlussfolgerung: Die Ergebnisse zeigen, dass Ausmaß und Dauer des Rückgangs der Krankheitssymptome bei Babesiose mit der Stimulation und Intensität der Widerstandsfähigkeit der CD4-positiven T-Zellen zusammenhängen können. Der Einsatz von Imidocarb beseitigt die Parasitämie und ermöglicht die Erholung der Zellzahl.

 
  • References

  • 1 Abdalla HS, Hussein HS, Kreier JP. Babesia rodhaini: passive protection of mice with immune serum. Tropenmed Parasitol 1978; 29: 295-306.
  • 2 Adachi K, Tateishi M, Horii Y, Nagatomo H, Shimizu T, Makimura S. Elevated erythrocyte-bound IgG value in dogs with clinical Babesia gibsoni infection. J Vet Med Sci 1994; 56: 757-759.
  • 3 Adachi K, Ueno C, Makimura S. Immunosuppression in dogs naturally infected with Babesia gibsoni . J Vet Med Sci 1993; 55: 503-505.
  • 4 Adaszek Ł, Górna M, Klimiuk P, Kalinowski M, Winiarczyk S. A presumptive case of cerebral babesiosis in a dog in Poland caused by a virulent Babesia canis strain. Tierärztl Prax 2012; 40 (K): 367-371.
  • 5 Adaszek Ł, Martinez AC, Winiarczyk S. Factors affecting the distribution of babesiosis in dogs in Poland. Vet Parasitol 2011; 181: 160-165.
  • 6 Adaszek Ł, Winiarczyk S, Łukaszewska J. A first case of ehrlichiosis in a horse in Poland. Dtsch Tierarztl Wochenschr 2009; 116: 330-334.
  • 7 Adaszek Ł, Winiarczyk S. Molecular characterization of Babesia canis canis isolates from naturally infected dogs in Poland. Vet Parasitol 2008; 152: 235-241.
  • 8 Aquilar-Delfin I, Homer MJ, Wettstein PJ, Persing DH. Innate resistance to Babesia infection is influenced by genetic background and gender. Infect Immun 2001; 69: 7955-7958.
  • 9 Brown WC, Norimine J, Knowles DP, Goff WL. Immune control of Babesia bovis infection. Vet Parasitol 2006; 138: 75-87.
  • 10 Brown WC, Ruef BJ, Norimine J, Kegerreis KA, Suarez CE, Conley PG, Stich RW, Carson KH, Rice-Ficht AC. A novel 20-kilodalton protein conserved in Babesia bovis and B . bigemina stimulates memory CD4+ T lymphocyte responses in B. bovis-immune cattle. Mol Biochem Parasitol 2001; 118: 97-109.
  • 11 Butler CM, Nijhof AM, Van der Kolk JH, De Haseth OB, Taoufik A, Jongejan F, Houwers DJ. Repeated high dose imidocarb dipropionate treatment did not eliminate Babesia caballi from naturally infected horses as determined by PCR-reverse line blot hybridization. Vet Parasitol 2008; 151: 320-322.
  • 12 Cardoso L, Costa A, Tuna J, Vieira L, Eyal O, Yisaschar-Mekuzas Y, Baneth G. Babesia canis canis and Babesia canis vogeli infections in dogs from northern Portugal. Vet Parasitol 2008; 156: 199-204.
  • 13 Carret C, Walas F, Carcy B, Grande N, Précigout É, Moubri K, Schetters T, Gorenflot A. Babesia canis canis, Babesia canis vogeli, Babesia canis rossi: Differentiation of three subspecies by restriction fragment length polymorphism analysis on amplified small subunit ribosomal RNA genes. J Eukaryot Microbiol 1999; 46: 298-303.
  • 14 Chapman WE, Ward PA. Babesia rodhaini: requirement of complement for penetration of human erythrocytes. Science 1977; 196: 67-70.
  • 15 Chen D, Copeman DB, Burnell J, Hutchinson GW. Helper T cell and antibody responses to infection of CBA mice with Babesia microti . Parasite Immunol 2000; 22: 81-88.
  • 16 Chen D, Copeman DB, Hutchinson GW, Burnell J. Inhibition of growth of cultured Babesia microti by serum and macrophages in the presence or absence of T cells. Parsasitol Int 2000; 48: 223-231.
  • 17 Christensson DA. Inverse age resistance to experimental Babesia divergens infection in cattle. Acta Vet Scand 1989; 30: 453-464.
  • 18 Clawson ML, Paciorkowski N, Rajan TV, La Vake C, Pope C, La Vake M, Wikel SK, Krause PJ, Radolf JD. Cellular immunity, but not gamma interferon, is essential for resolution of Babesia microti infection in BALB/c mice. Infect Immun 2002; 70: 5304-5306.
  • 19 Echaide IE, Hines SA, McElwain TF, Suarez CE, McGuire TC, Palmer GH. In vivo binding of immunoglobulin M to the surfaces of Babesia bigeminainfected erythrocytes. Infect Immun 1998; 66: 2922-2927.
  • 20 Goff WL, Johnson WC, Parish SM, Barrington GM, Tuo W, Valdez RA. Age-related immunity in cattle to Babesia bovis infection involves the rapid induction of interleukin-12, interferon-γ, and inducible nitric oxide synthase mRNA expression in the spleen. Parasite Immunol 2001; 23: 463-471.
  • 21 Gothe R, Wegerdt S. Die Babesiosen des Hundes in Deutschland: epidemiologische Fallanalysen. Tierärztl Prax 1991; 19: 170-173.
  • 22 Hemmer RM, Ferrick DA, Conrad PA. Role of T cells and cytokines in fatal and resolving experimental babesiosis: protection in TNFRp55-/mice infected with the human Babesia WA1 parasite. J Parasitol 2000; 86: 736-742.
  • 23 Homer MJ, Aguilar-Delfin I, Telford 3rd SR, Krause PJ, Persing DH. Babesiosis. Clin Microbiol Rev 2000; 13: 451-469.
  • 24 Kubelová M, Tkadlec E, Bednář M, Roubalová E, Siroký P. West-to-east differences of Babesia canis canis prevalence in Dermacentor reticulatus ticks in Slovakia. Vet Parasitol 2011; 180: 191-196.
  • 25 Langhorne J, Meding SJ, Eichmann K, Gillard SS. The response of CD4+ T cells to Plasmodium chabaudi chabaudi . Immunol Rev 1989; 112: 71-94.
  • 26 Matijatko V, Torti M, Schetters TP. Canine babesiosis in Europe: how many diseases?. Trends Parasitol 2012; 28: 99-105.
  • 27 Milczak A, Riha T, Abramowicz B, Madej E. Hemostatic disorders during the course of canine babesiosis. Med Weter 2004; 60: 1067-1070.
  • 28 Mosqueda J, Olvera-Ramírez A, Aguilar-Tipacamú G, Cantó GJ. Current advances in detection and treatment of babesiosis. Curr Med Chem 2012; 19: 1504-1518.
  • 29 Mota MM, Brown KN, Holder AA, Jarra W. Acute Plasmodium chabaudi chabaudi malaria infection induces antibodies which bind to the surfaces of parasitized erythrocytes and promote their phagocytosis by macrophages in vitro. Infect Immun 1998; 66: 4080-4086.
  • 30 Preston PM, Jongejan F. Protective immune mechanisms to ticks and tickborne diseases of ruminants. Parasitol Today 1999; 15: 255-258.
  • 31 Reggeti F, Bienzle D. Flow cytometry in veterinary oncology. Vet Pathol 2011; 48: 223-235.
  • 32 Rosenberg YJ, Evans CB. Resistance of mice suppressed for IgM production to Babesia microti infection. Nature 1979; 281: 302-304.
  • 33 Simpson CF, Neal FC. Ultrastructure of Babesia equi in ponies treated with imidocarb. Am J Vet Res 1980; 41: 267-271.
  • 34 Solano-Gallego L, Trotta M, Carli E, Carcy B, Caldin M, Furlanello T. Babesia canis canis and Babesia canis vogeli clinicopathological findings and DNA detection by means of PCR-RFLP in blood from Italian dogs suspected of tick-borne disease. Vet Parasitol 2008; 157: 211-221.
  • 35 Tamura K, Nagashima N, Oda H, Kunimi M, Itoi T, Yasukawa M, Miyata T, Terakado K, Takemitsu H. Investigations into the lymphocyte phenotypes and the presence of rheumatoid factor and antinuclear antibody in the peripheral blood of 515 dogs. Vet Med 2012; 57: 529-535.
  • 36 Taylor-Robinson AW, Phillips RS, Severn A, Moncada S, Liew FY. The role of TH1 and TH2 cells in a rodent malaria infection. Science 1993; 260: 1931-1934.
  • 37 Terkawi MA, Kawai S, Aboulaila M, Nayel M, Mousa A, Zaghawa A, Yokoyama N, Igarashi I. Specific antibody to a conserved region of Babesia apical membrane antigen-1 inhibited the invasion of B . bovis into the erythrocyte. Exp Parasitol 2013; 135: 623-628.
  • 38 Vial HJ, Gorenflot A. Chemotherapy against babesiosis. Vet Parasitol 2006; 31: 147-160.
  • 39 Wang HH, Lin CY, Huang TP. Patterns of CD4/CD8 T-cell ratio in dialysis effluents predict the long-term outcome of peritonitis in patients undergoing peritoneal dialysis. Nephrol Dial Transplant 2003; 18: 1181-1189.
  • 40 Wulansari R, Wijaya A, Ano H, Horii Y, Makimura S. Lymphocyte subsets and specific IgG antibody levels in clindamycin-treated and untreated dogs experimentally infected with Babesia gibsoni . J Vet Med Sci 2003; 65: 579-584.
  • 41 Zahler M, Schein E, Rinder H, Gothe R. Characteristic genotypes discriminate between Babesia canis isolates of differing vector specificity and pathogenicity in dogs. Parasitol Res 1998; 84: 544-548.
  • 42 Zivkovic D, Seinen W, Kuil H, Albers-van Bemmel CM, Speksnijder JE. Immunity to Babesia in mice. I. Adoptive transfer of immunity to Babesia rodhaini with immune spleen cells and the effect of irradiation on the protection of immune mice. Vet Immunol Immunopathol 1984; 05: 343-357.
  • 43 Zygner W, Rapacka G, Gójska-Zygner O, Długosz E, Wedrychowicz H. Biochemical abnormalities observed in serum of dogs infected with large Babesia in Warsaw (Poland). Pol J Vet Sci 2007; 10: 245-253.