Study of changes in thyroid function tests (anti-thyroglobulin, anti – thyroid peroxidase, thyroglobulin, triiodothyronine, tetraiodothyronine) cystatin C and sphingosine 1 phosphate in the serum of dogs with Babesiosis and determination of relevant potential diagnostic biomarkers
Subject Areas :
Veterinary Clinical Pathology
Laya
Nasirzadeh
1
(D.V.M. Graduate, Faculty of Veterinary Medicine, Islamic Azad University of Urmia, Urmia , Iran.)
Kaveh
Azimzadeh
2
(Professor, Department of Clinical Pathology, Faculty of Veterinary Medicine, Islamic Azad University of Urmia, Urmia, Iran.)
Received: 2023-06-26
Accepted : 2023-11-21
Published : 2023-10-23
Keywords:
Dog,
Cystatin C,
Thyroid function,
Sphingosine 1 phosphate,
babesiosis,
Abstract :
Babesiosis is classified as blood parasitic disease that is caused by genus Babesia. This parasite is transmitted by hard ticks and blood transfusion and causes fever, anemia, hemoglobinuria and jaundice. Study on babesiosis is important in terms of its public health concerns. This study was performed to evaluate serum changes of thyroid function indices [Anti-Thyroglobulin (a-Tg), Anti–Thyroid Peroxidase (a-Tpo), Thyroglobulin (Tg), Triiodothyronine (T3), Tetraiodothyronine (T4)], Cystatin C and sphingosine 1-phosphate in dogs with babesiosis. For this purpose, 5 ml of blood were taken from the cephalic vein of 35 dogs with babesiosis in several small animal clinics (in Tehran, Tabriz and Mashhad) which were diagnosed based on clinical signs and laboratory tests and the same number of healthy dogs (35) with consent of their owners and after serum preparation, thyroid function parameters (a-Tg, a-Tpo, Tg, T3, T4) Cystatin C and sphingosine 1 phosphate were measured by specific ELISA kits and evaluated statistically with SPSS version 17. The results indicated significant increase (p≤0.01) in all of the measured parameters in comparison with the healthy group (control group). Based on the ROC statistical test, the obtained results indicate that due to the high sensitivity of the method used in measuring the indicators of thyroid function (except tetraiodo-thyronine) and cystatin C, it is possible to use the serum values of the mentioned indicators (Tg, T3, a-Tg, a-Tpo) and cystatin C as possible potential biomarkers for the diagnosis of canine babesiosis.
References:
Alencar Filho, A.C., Lacerda, M.V., Okoshi, K. and Okoshi, M.P. (2014). Malaria and vascular endothelium. Arquivos Brasileiros de Cardiologia, 103(2): 9-
Almy, F.S., Christopher, M.M., King, D.P. and Brown, S.A. (2002). Evaluation of cystatin C as an endogenous marker of glomerular filtration rate in dogs. Journal of Veterinary Internal Medicine, 16(1): 45-51.
Antognoni, M.T., Siepi, D., Porciello, F. and Fruganti, G. (2005). Use of serum cystatin C determination as a marker of renal function in the dog. Veterinary Research Communication, 29: 265-267.
Antognoni, M.T., Siepi, D., Porciello, F., Rueca, F. and Fruganti, G. (2007). Serum cystatin C evaluation in dogs affected by different diseases associated or not with renal insufficiency. Veterinary Research Communications, 31(1): 269-271.
Ashrafi, Helan, J., Haddadzadeh, H.R., Shirani, D., Khazraiinia, P. and Mostofi, S. (2001). Histopathologic, hematologic and clinical study on canine Babesiosis. Iranian Journal of Veterinary Medicine. 56(3): 93-96. [In Persian]
Autino, B., Corbett, Y., Castelli, F. and Taramelli, D. (2012). Pathogenesis of malaria in tissues and blood. Mediterranian Journal of Hematology Infectious Diseases, 4(1).
Azimzadeh, K., Nouri, K. and Farooghi, H. (2013). Plasma Malondialdehyde, Thyroid Hormones and Some Blood Profiles in Ovine Babesiosis. Kafkas Universitesi Veteriner Fakultesi Dergisi, 19(3): 489-493.
Azimzadeh, K., Mahan, M., Zamani, N. and Zahed, T. (2019). Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate. Atatürk Üniversitesi Veteriner Bilim Dergisi, 14(1): 1-7.
Blaho, V.A. and Hla, T. (2014). An update on the biology of sphingosine 1-phosphate receptors. Journal of Lipid Research, 55(8): 608-
Boozer, A.L. and Macintire, D.K. (2003). Canine babesiosis. Veterinary Clinics: Small Animal Practice, 33(4): 885-904.
Bostom, A.G., Gohh, R.Y., Bausserman, L., Hakas, D. and Jacques, P.F. (1999). Serum cystatin C as a determinant of fasting total homocysteine levels in renal transplant recipients with a normal serum creatinine. Journal of American Society Nephrology, 10(2): 164-166.
Cerutti, A. and Rescigno, M. (2008). The biology of intestinal immunoglobulin A responses. Immunity, 28(4): 740-
Clark, I.A. and Jacobson, L.S. (1998). Do babesiosis and malaria share a common disease process? Annals of Tropical Medicine & Parasitology, 92(4): 483-488.
Collett, M.G. (2000). Survey of canine babesiosis in South Africa. Journal of the South African Veterinary Association, 71(3): 180-186.
Filler, G., Bokenkamp, A., Hofmann, W., Le Bricon, T., Martinez-Bru, C. and Grubb, A. (2005). Cystatin C as a marker of GFR-history, indications, and future research. Clinical Biochemistry, 38(6): 1-8.
Garg, S.K., Volpe, E., Palmieri, G., Mattei, M., Galati, D., Martino, A., et al. (2004). Sphingosine 1-phosphate induces antimicrobial activity both in vitro and in vivo. The Journal of Infectious Diseases, 189(11): 2129-2138.
Gika, H., Lämmerhofer, M., Papadoyannis, I. and Lindner, W. (2004). Direct separation and quantitative analysis of thyroxine and triiodothyronine enantiomers in pharmaceuticals by highperformance liquid chromatography. Journal of Chromatography B Analytic Technology Biomedical Life Science, 800(12): 193-201.
Gillrie, M.R., Lee, K., Gowda, D.C., Davis, S.P., Monestier, M., Cui, L., et al. (2012). Plasmodium falciparum histones induce endothelial proinflammatory response and barrier dysfunction. American Journal of Pathology, 180(3): 39-
Graham, P.A., Nachreiner, R.F., Refsal, K.R. and Provencher-Bolliger, A.L. (2001). Lymphocytic thyroiditis. Veterinary Clinical North American Small Animal Practice, 31(5): 915-933.
Herget-Rosenthal, S., Bökenkamp, A. and Hofmann, W. (2007). How to estimate GFR-serum creatinine, serum cystatin C or equations? Clinical Biochemistry, 40(3): 153-161.
Irwin, P.J. and Hutchinson, G.W. (1991). Clinical and pathological findings of Babesia infection in dogs. Australian Veterinary Journal, 68(6): 204-209.
Jacobson, L.S. and Clark, I.A. (1994). The pathophysiology of canine babesiosis: new approaches to an old puzzle. Journal of the South African Veterinary Association, 65(3): 134-145.
Jensen, A.L., Bomholt, M. and Moe, L. (2001). Preliminary evaluation of a particle-enhanced turbidimetric immunoassay (PETIA) for the determination of serum cystatin C-like immunereactivity in dogs. Veterinary Clinical Pathology, 30(2): 86-90.
Lassus, J. and Harjola, V.P. (2012). Cystatin C: a step forward in assessing kidney function and cardiovascular risk. Heart Failure Reviews, 17(3): 251-261.
Mathe, A., Voros, K., Papp, L. ansd Reiczigel, J. (2006). Clinical manifestations of canine Babesiosis in Hungary (63 cases). Acta Veterinaria Hungarica, 54: 367-385.
Miyagawa, Y., Takemura, N. and Hirose, H. (2009). Evaluation of the measurement of serum cystatin C by an enzyme-linked immunosorbent assay for humans as a marker of the glomerular filtration rate in dogs. Journal of Veterinary Medicine Science, 71.
Ono, Y., Kurano, M., Ohkawa, R., Yokota, H., Igarashi, K., Aoki, J., et al. (2013). Sphingosine 1-phosphate release from platelets during clot formation: close correlation between platelet count and serum sphingosine 1- phosphate concentration. Lipids Health Diseases, 8(1): 12-20.
Pasa, S., Bayramli, G., Atasoy, A., Karul, A., Ertug, S. and Ozensoy Toz, S. (2009). Evaluation of serum cystatin-C in dogs with visceral leishmaniasis. Veterinary Research Communications, 33(6): 529-534.
Pekmezci, D., Güzel, M., Yildirim, A., Çiftci, G., Pekmezci, G.Z., Tütüncü, M. and Abdullah, I.N.C.I. (2015). Evaluation of serum cystatinC concentrations in dogs infected with Dirofilaria immitis. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 62(4): 303-306.
Punsawad, C. and Viriyavejakul, P. (2017). Reduction in serum sphingosine 1-phosphate concentration in malaria. PLOS ONE, 12(6): e0180631.
Randers, E. and Erlandsen, E.J. (1999). Serum cystatin C as an endogenous marker of the renal function – A Review. Clinical Chemistry Laboratory Medicine, 37(8): 389-395.
Schoeman, J.P. (2009). Canine babesiosis: tick-borne diseases. Onderstepoort Journal of Veterinary Research, 76(1): 59-66.
Shakespeare, A.S. (1995). The incidence of canine babesiosis amongst sick dogs presented to the Onderstepoort Veterinary Academic Hospital. Journal of the South African Veterinary Association, 66(4): 247-250.
Soulsby, E.J.L. (1982). Babesia of Horses in Helminths.Arthropods and Protozoa of Domesticated Animals, Lea and Febiger Inc, pp: 719-723.
Vito, C.D., Hadi, L.A., Navone, S.E., Marfia, G., Campanella, R., Mancuso, M.E., et al. (2016). Platelet-derived sphingosine-1-phosphate and inflammation: from basic mechanisms to clinical implications. Platelets, 27(5): 393-401.
Villa, P., Jiménez, M., Soriano, M.C., Manzanares, J. and Casasnovas, P. (2005). Serum cystatin C concentration as a marker of acute renal dysfunction in critically ill patients. Critical Care, 9(1): 139-143.
Welzl, C., Leisewitz, A.L., Jacobson, L.S., Vaughan-Scott, T. and Myburgh, E. (2001). Systemic inflammatory response syndrome and multiple-organ damage/dysfunction in complicated canine babesiosis. Journal of the South African Veterinary Association, 72(3): 158-162.
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Alencar Filho, A.C., Lacerda, M.V., Okoshi, K. and Okoshi, M.P. (2014). Malaria and vascular endothelium. Arquivos Brasileiros de Cardiologia, 103(2): 9-
Almy, F.S., Christopher, M.M., King, D.P. and Brown, S.A. (2002). Evaluation of cystatin C as an endogenous marker of glomerular filtration rate in dogs. Journal of Veterinary Internal Medicine, 16(1): 45-51.
Antognoni, M.T., Siepi, D., Porciello, F. and Fruganti, G. (2005). Use of serum cystatin C determination as a marker of renal function in the dog. Veterinary Research Communication, 29: 265-267.
Antognoni, M.T., Siepi, D., Porciello, F., Rueca, F. and Fruganti, G. (2007). Serum cystatin C evaluation in dogs affected by different diseases associated or not with renal insufficiency. Veterinary Research Communications, 31(1): 269-271.
Ashrafi, Helan, J., Haddadzadeh, H.R., Shirani, D., Khazraiinia, P. and Mostofi, S. (2001). Histopathologic, hematologic and clinical study on canine Babesiosis. Iranian Journal of Veterinary Medicine. 56(3): 93-96. [In Persian]
Autino, B., Corbett, Y., Castelli, F. and Taramelli, D. (2012). Pathogenesis of malaria in tissues and blood. Mediterranian Journal of Hematology Infectious Diseases, 4(1).
Azimzadeh, K., Nouri, K. and Farooghi, H. (2013). Plasma Malondialdehyde, Thyroid Hormones and Some Blood Profiles in Ovine Babesiosis. Kafkas Universitesi Veteriner Fakultesi Dergisi, 19(3): 489-493.
Azimzadeh, K., Mahan, M., Zamani, N. and Zahed, T. (2019). Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate. Atatürk Üniversitesi Veteriner Bilim Dergisi, 14(1): 1-7.
Blaho, V.A. and Hla, T. (2014). An update on the biology of sphingosine 1-phosphate receptors. Journal of Lipid Research, 55(8): 608-
Boozer, A.L. and Macintire, D.K. (2003). Canine babesiosis. Veterinary Clinics: Small Animal Practice, 33(4): 885-904.
Bostom, A.G., Gohh, R.Y., Bausserman, L., Hakas, D. and Jacques, P.F. (1999). Serum cystatin C as a determinant of fasting total homocysteine levels in renal transplant recipients with a normal serum creatinine. Journal of American Society Nephrology, 10(2): 164-166.
Cerutti, A. and Rescigno, M. (2008). The biology of intestinal immunoglobulin A responses. Immunity, 28(4): 740-
Clark, I.A. and Jacobson, L.S. (1998). Do babesiosis and malaria share a common disease process? Annals of Tropical Medicine & Parasitology, 92(4): 483-488.
Collett, M.G. (2000). Survey of canine babesiosis in South Africa. Journal of the South African Veterinary Association, 71(3): 180-186.
Filler, G., Bokenkamp, A., Hofmann, W., Le Bricon, T., Martinez-Bru, C. and Grubb, A. (2005). Cystatin C as a marker of GFR-history, indications, and future research. Clinical Biochemistry, 38(6): 1-8.
Garg, S.K., Volpe, E., Palmieri, G., Mattei, M., Galati, D., Martino, A., et al. (2004). Sphingosine 1-phosphate induces antimicrobial activity both in vitro and in vivo. The Journal of Infectious Diseases, 189(11): 2129-2138.
Gika, H., Lämmerhofer, M., Papadoyannis, I. and Lindner, W. (2004). Direct separation and quantitative analysis of thyroxine and triiodothyronine enantiomers in pharmaceuticals by highperformance liquid chromatography. Journal of Chromatography B Analytic Technology Biomedical Life Science, 800(12): 193-201.
Gillrie, M.R., Lee, K., Gowda, D.C., Davis, S.P., Monestier, M., Cui, L., et al. (2012). Plasmodium falciparum histones induce endothelial proinflammatory response and barrier dysfunction. American Journal of Pathology, 180(3): 39-
Graham, P.A., Nachreiner, R.F., Refsal, K.R. and Provencher-Bolliger, A.L. (2001). Lymphocytic thyroiditis. Veterinary Clinical North American Small Animal Practice, 31(5): 915-933.
Herget-Rosenthal, S., Bökenkamp, A. and Hofmann, W. (2007). How to estimate GFR-serum creatinine, serum cystatin C or equations? Clinical Biochemistry, 40(3): 153-161.
Irwin, P.J. and Hutchinson, G.W. (1991). Clinical and pathological findings of Babesia infection in dogs. Australian Veterinary Journal, 68(6): 204-209.
Jacobson, L.S. and Clark, I.A. (1994). The pathophysiology of canine babesiosis: new approaches to an old puzzle. Journal of the South African Veterinary Association, 65(3): 134-145.
Jensen, A.L., Bomholt, M. and Moe, L. (2001). Preliminary evaluation of a particle-enhanced turbidimetric immunoassay (PETIA) for the determination of serum cystatin C-like immunereactivity in dogs. Veterinary Clinical Pathology, 30(2): 86-90.
Lassus, J. and Harjola, V.P. (2012). Cystatin C: a step forward in assessing kidney function and cardiovascular risk. Heart Failure Reviews, 17(3): 251-261.
Mathe, A., Voros, K., Papp, L. ansd Reiczigel, J. (2006). Clinical manifestations of canine Babesiosis in Hungary (63 cases). Acta Veterinaria Hungarica, 54: 367-385.
Miyagawa, Y., Takemura, N. and Hirose, H. (2009). Evaluation of the measurement of serum cystatin C by an enzyme-linked immunosorbent assay for humans as a marker of the glomerular filtration rate in dogs. Journal of Veterinary Medicine Science, 71.
Ono, Y., Kurano, M., Ohkawa, R., Yokota, H., Igarashi, K., Aoki, J., et al. (2013). Sphingosine 1-phosphate release from platelets during clot formation: close correlation between platelet count and serum sphingosine 1- phosphate concentration. Lipids Health Diseases, 8(1): 12-20.
Pasa, S., Bayramli, G., Atasoy, A., Karul, A., Ertug, S. and Ozensoy Toz, S. (2009). Evaluation of serum cystatin-C in dogs with visceral leishmaniasis. Veterinary Research Communications, 33(6): 529-534.
Pekmezci, D., Güzel, M., Yildirim, A., Çiftci, G., Pekmezci, G.Z., Tütüncü, M. and Abdullah, I.N.C.I. (2015). Evaluation of serum cystatinC concentrations in dogs infected with Dirofilaria immitis. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 62(4): 303-306.
Punsawad, C. and Viriyavejakul, P. (2017). Reduction in serum sphingosine 1-phosphate concentration in malaria. PLOS ONE, 12(6): e0180631.
Randers, E. and Erlandsen, E.J. (1999). Serum cystatin C as an endogenous marker of the renal function – A Review. Clinical Chemistry Laboratory Medicine, 37(8): 389-395.
Schoeman, J.P. (2009). Canine babesiosis: tick-borne diseases. Onderstepoort Journal of Veterinary Research, 76(1): 59-66.
Shakespeare, A.S. (1995). The incidence of canine babesiosis amongst sick dogs presented to the Onderstepoort Veterinary Academic Hospital. Journal of the South African Veterinary Association, 66(4): 247-250.
Soulsby, E.J.L. (1982). Babesia of Horses in Helminths.Arthropods and Protozoa of Domesticated Animals, Lea and Febiger Inc, pp: 719-723.
Vito, C.D., Hadi, L.A., Navone, S.E., Marfia, G., Campanella, R., Mancuso, M.E., et al. (2016). Platelet-derived sphingosine-1-phosphate and inflammation: from basic mechanisms to clinical implications. Platelets, 27(5): 393-401.
Villa, P., Jiménez, M., Soriano, M.C., Manzanares, J. and Casasnovas, P. (2005). Serum cystatin C concentration as a marker of acute renal dysfunction in critically ill patients. Critical Care, 9(1): 139-143.
Welzl, C., Leisewitz, A.L., Jacobson, L.S., Vaughan-Scott, T. and Myburgh, E. (2001). Systemic inflammatory response syndrome and multiple-organ damage/dysfunction in complicated canine babesiosis. Journal of the South African Veterinary Association, 72(3): 158-162.
