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Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate

Yıl 2019, Cilt: 14 Sayı: 1, 1 - 7, 28.04.2019
https://doi.org/10.17094/ataunivbd.367320

Öz

The aim of this study was to assay arginase activity, gelsolin (GLS) and cystatin c (Cys c) levels and determination of potential biomarker in sheep babesiosis. The Babesia genus as pathogen blood parasites causes economic problems in livestock management. Many published studies have suggested babesiosis-induced biochemical parameters, but no one have determined those parameters alterations and clarification of sensitivity and specificity. Sheep with acute babesiosis were identified based on clinical signs and the observation of Piroplasm forms in red blood cells. After blood sampling from 25 infected and same number healthy sheep, above parameters measured in plasma. The results indicated significant increase (P<0.01) in arginase and Cys c and significant decreases (P<0.01) in the levels of GLS in different parasitemia rates compared with healthy group. In conclusion, the results suggested that sheep babesiosis causes cellular damage especially in kidney (owing to high level of Cys c) and high arginase activity can be considered as one of essential factor in Babesia ovis proliferation process. Finally, high sensitivity of Cys c and arginase in the different parasitemia rates than GLS could be clarified as potential biomarker of sheep babesiosis.

Kaynakça

  • 1. Rahbari S., Nabian S., Khaki Z., Alidadi N., Ashrafihelan J., 2008. Clinical, haematologic and pathologic aspects of experimental ovine babesiosis in Iran. Iran J Vet Res, 9, 59-64. 2. Yur F., Yazar M., Değer Y., Dede S., 2010. Na+/K+ ATPase activity in sheep with natural babesiosis. Acta Vet Brno, 79, 233-236. 3. Razmi GR., Naghibi A., Aslani MR., Dastjerdi K., Hosseini H., 2003. An epidemiological study on Babesia infection in small ruminants in Mashhad suburb, Khorasan province, Iran. Small Rumin Res, 50, 39-44. 4. Alani AJ., Herbert IV., 1988. The pathogenesis of Babesia motasi (Wales) infection in sheep. Vet Parasitol, 27, 209-220. 5. Apaydin B., Dede S., 2010. Electrophoretic profile of serum protein fractions from sheep naturally infected with Babesia ovis . Rev Med Vet, 161, 57-60. 6. Shen K., Ji Y., Chen GQ., Huang B., Zhang X., Wu S., Yu GP., Wang XC., 2011. Expression and clinical significance of the NDA repair enzyme MYH in esophageal squamous cell carcinoma. Exp Ther Med, 2, 1117 1120. 7. Cederbaum SD., Yu H., Grody WW., Kern RM., Yoo P., Iyer RK., 2004. Arginases I and II: do their functions overlap? Mol Genet Metab 81 (Suppl 1): S38 S44. 8. Jenkinson CP., Grody WW., Cederbaum SD., 1996. Comparative properties of arginase. Comp Biochem Physiol B Biochem Mol Biol, 114, 107 132. 9. Na S., Kim OS., Ryoo S., Kweon TD., Choi YS., Shim HS., Oh YJ., 2014. Cervical ganglion block attenuates the progression of pulmonary hypertension via nitric oxide and arginase pathways. Hypertension, 63, 309 315. 10. Yang J., Gonon AT., Sjöquist PO., Lundberg JO., Pernow J., 2013. Arginase regulates red blood cell nitric oxide synthase and export of cardioprotective nitric oxide bioactivity. Proc Natl Acad Sci, USA 110: 15049 15054. 11. Grohmann U., Bronte V., 2010. Control of immune response by amino acid metabolism. Immunol Rev, 236, 243–264. 12. Fairlamb AH., Cerami A., 1992. Metabolism and functions of trypanothione in the Kinetoplastida. Annu. Rev. Microbiol, 46, 695–729. 13. Durante W., Johnson FK., Johnson RA., 2007. Arginase: A critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol, 34(9), 906–911. 14. Young CL., Feierstein A., Southwick FS., 1994. Calcium regulation of actin filament capping and monomer binding by macrophage capping protein. Journal of Biological Chemistry, 269(19), 13997-14002. 15. Hui QS., Masaya Y., Marisan M., Yin HL., 1999. Gelsolin, a Multifunctional Actin Regulatory Protein. Journal of Biological Chemistry, 274, 33179-33182. 16. Hu Y., Li H., Li WH., Meng HX., Fan YZ., 2013. The value of decreased plasma gelsolin levels in patients with systemic lupus erythematosus and rheumatoid arthritis in diagnosis and disease activity evaluation. Lupus, 22(14), 1455-1461. 17. Marrocco C., Rinalducci S., Mohamadkhani A., D'Amici GM., Zolla L., 2010. Plasma gelsolin protein: a candidate biomarker for hepatitis B-associated liver cirrhosis identified by proteomic approach. Blood Transfusion, 8(3), 105-112. 18. DiNubile M., Antin J., Bressler S., Stossel T., Ferrara J., 1998. Decreased gelsolin levels are associated with interstitial pneumonia after allogeneic BMT. Blood, 92, 683a. 19. Smith DB., Janmey PA., Sherwood JA., Howard RJ., Lind SE., 1988. Decreased plasma gelsolin levels in patients with Plasmodium falciparum malaria: a consequence of hemolysis? Blood, 72(1), 214-218. 20. Villa P., Jiménez M., Soriano MC., Manzanares J., Casasnovas P., 2005. Serum cystatin C concentration as a marker of acute renal dysfunction in critically ill patients. Critical Care, 9, 139-143. 21. Filler G.., Bokenkamp A, Hofmann W., Le Bricon T., Martinez-Bru C., 2005. Cystatin C as a marker of GFR-history, indications, and future research. Clin Biochem, 38, 1–8. 22. Antognoni MT., Siepi D., Porciello F., Rueca F., Fruganti G., 2007. Serum Cystatin-C Evaluation in Dogs Affected by Different Diseases Associated or Not with Renal Insufficiency. Vet Res Commun, 31(1), 269-271. 23. Lassus J., Harjola VP., 2012. Cystatin C. a step forward in assessing kidney function and cardiovascular risk. Heart Failure Reviews, 17, 251–261. 24. Herget-Rosenthal S., Bökenkamp A., Hofmann W., 2007. How to estimate GFR-serum creatinine, serum cystatin C or equations? Clin Biochem, 40, 153–161. 25. Bostom AG., Gohh RY., Bausserman L., Hakas D., Jacques PF., 1999. Serum Cystatin C as a Determinant of Fasting Total Homocysteine Levels in Renal Transplant Recipients with a Normal Serum Creatinine. J Am Society Nephrol, 10, 164–166. 26. Jensen AL., Bomholt M., Moe L., 2001. Preliminary evaluation of a particle-enhanced turbidimetric immunoassay (PETIA) for the determination of serum cystatin C-like immunoreactivity in dogs. Vet Clin Path, 30(2), 86-90. 27. Almy FS., Christopher MM., King DP., Brown SA., 2002. Evaluation of cystatin C as an endogenous marker of glomerular filtration rate in dogs. J Vet Intern Med, 16(1), 45-51. 28. Sevinc F., Turgut K., Sevinc M., 2007. Therapeutic and prophylactic efficacy of imidocarb dipropionate on experimental Babesia ovis infection of lambs. Vet Parasitol, 149, 65-71. 29. Azimzadeh K., Nouri K., Farooghi H., Rasouli S., Zamani N., 2013. Plasma malondialdehyde, thyroid hormones and some blood profiles in ovine Babesiosis. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 19, 489–493. 30. Goddard A., Leisewitz AL., Kjelgaard-Hansen M., Kristensen AT., Schoeman JP., 2016. Excessive Pro-Inflammatory Serum Cytokine Concentrations in Virulent Canine Babesiosis. PLoS ONE, 11(3), e0150113. 31. Esmaeilnejad B., Tavassoli M., Siamak Asri-Rezaei., 2012. Investigation of hematological and biochemical parameters in small ruminants naturally infected with Babesia ovis. Vet Res Forum, 3(1), 31–36. 32. Gobert A., Daulouede S., Lepoivre M., Boucher J., Bouteille B., Buguet A., Cespuglio R., Veyret B., Vincendeau P., 2000. L-Arginine availability modulates local nitric oxide production and parasite killing in experimental trypanosomiasis. Infect Immun, 68, 4653– 4657. 33. Duleu S., Vincendeau P., Courtois P., Semballa S., Lagroye I., Daulouède S., Boucher J., 2004. Mouse strain susceptibility to trypanosome infection: an arginase-dependent effect. J Immunol 172, 6298–6303. 34. Sandalova E., Laccabue D., Boni C., Watanabe T., Tan A., Zong HZ., Ferrari C., 2012. Increased levels of arginase in patients with acute hepatitis B suppress antiviral T cells. Gastroenterology, 143, 78–87. 35. Abebe T., Hailu A., Woldeyes M., Mekonen W., Bilcha K., Cloke T., Fry L., 2012. Local increase of arginase activity in lesions of patients with cutaneous leishmaniasis in Ethiopia. PLoS Negl Trop Dis, 6, e1684. 36. De Boniface J., Mao Y., Schmidt-Mende J., Kiessling R., Poschke I., 2012. Expression patterns of the immunomodulatory enzyme arginase I in blood, lymph nodes and tumor tissue of early-stage breast cancer patients. Oncoimmunology, 1, 1305–1312. 37. Perez G., Olivares IM., Rodriguez MG., Ceballos GM., Garcia Sanchez JR., 2012. Arginase activity in patients with breast cancer: an analysis of plasma, tumors, and its relationship with the presence of the estrogen receptor. Onkologie, 35, 570 –574. 38. Mei L., Zheng S., Shengbin X., Enyun S., 2014. Predictive value of serum gelsolin in hepatitis B virus (HBV)-related chronic liver disease. African Journal of Biotechnology, 11(20), 4640-4645. 39. Zhao DQ., Wang K., Zhang HD., Li YJ., 2013. Significant reduction of plasma gelsolin levels in patients with intracerebral hemorrhage. Clinica Chimica Acta, 415, 202-206. 40. Pasa S., Bayramli G., Atasoy A., Karul A., Ertug S., Ozensoy Toz S., 2009. Evaluation of serum cystatin-C in dogs with visceral leishmaniasis. Veterinary Research Communications, 33(6), 529-534. 41. Pekmezci D., Guzel M., Yildirim A., Ciftci G., Pekmezci G.Z., Tutuncu, M., 2015a. Evaluation of serum cystatin-C concentrations in dogs infected with Dirofilaria immitis. Ankara Universitesi Veteriner Fakultesi Dergisi, 62(4), 303-306. 42. Pekmezci D., Ural K., Aysul N., Guzel M., Ciftci G., (2015b). Assessment of renal function using canine cystatin- C levels in canine babesiosis and ehrlichiosis. Acta Veterinaria-Beograd, 65(1), 56-65. 43. Azimzadeh K., Izadmehr S., 2017. Evaluation of plasma hepcidin, cystatin c and gelsolin in ovine Theileriosis (Ghezel breed) based on age and parasitemia rate. Journal of veterinary clinical pathology, 11(1), 1-11. 44. Ahi S., Meram I., Ozdemir Y., 1999. Human serum arginase activity was measured by a sensitive enzyme properties and development of the method. Erciyes Medical Journal, 21, 3-9.

Koyun Babeziozisinde Plazma Arginaz, Gelsolin ve Sistatin C Arasında Olası Potansiyel Biyobelirteç Tayini: Parazitemi Oranına Göre

Yıl 2019, Cilt: 14 Sayı: 1, 1 - 7, 28.04.2019
https://doi.org/10.17094/ataunivbd.367320

Öz

Bu çalışmanın amacı, koyun babeziosisinde arginaz aktivitesi, gelsolin (GLS) ve sistatin c (Cys c) seviyelerini ve potansiyel biyobelirteç tespitini incelemektir. Patojen kan parazitleri olan Babesia türleri, hayvancılık yönetiminde ekonomik sorunlara neden olur. Yayımlanan birçok çalışmada babeziosis kaynaklı biyokimyasal parametreler önerilmiş, ancak hiç kimse bu parametrelerdeki duyarlılık ve özgüllüğü ve değişiklikleri açıklığa kavuşturmamıştır. Akut babeziosisli koyunlar, kırmızı kan hücrelerinde Piroplazma formlarının görülmesi ve klinik bulgulara göre belirlendi. Yirmibeş adet enfekte ve aynı sayıda sağlıklı koyunlardan alınan kan örneklemesinden sonra, yukardaki parametreler plazmada ölçüldü. Sonuçlar, arginaz ve Cys c'de anlamlı bir artış (P<0.01) ve sağlıklı gruba kıyasla farklı parazitemi oranlarında GLS seviyelerinde anlamlı düşüş (P<0.01) gösterdi. Sonuç olarak, koyun babeziosis'inin özellikle böbreklerde (Cys c'nin yüksek olması nedeniyle) hücresel hasara neden olduğunu ve yüksek arginaz aktivitesinin Babesia ovis proliferasyon sürecinde önemli bir faktör olarak olarak göz önünde bulundurulabileceğini göstermiştir. Son olarak, GLS 'den farklı parazitemi oranlarında CYS c ve arginaz 'nin yüksek duyarlılığı, koyun Babeziosis 'in potansiyel biyomarkeri olarak göz önünde bulundurulabilir.

Kaynakça

  • 1. Rahbari S., Nabian S., Khaki Z., Alidadi N., Ashrafihelan J., 2008. Clinical, haematologic and pathologic aspects of experimental ovine babesiosis in Iran. Iran J Vet Res, 9, 59-64. 2. Yur F., Yazar M., Değer Y., Dede S., 2010. Na+/K+ ATPase activity in sheep with natural babesiosis. Acta Vet Brno, 79, 233-236. 3. Razmi GR., Naghibi A., Aslani MR., Dastjerdi K., Hosseini H., 2003. An epidemiological study on Babesia infection in small ruminants in Mashhad suburb, Khorasan province, Iran. Small Rumin Res, 50, 39-44. 4. Alani AJ., Herbert IV., 1988. The pathogenesis of Babesia motasi (Wales) infection in sheep. Vet Parasitol, 27, 209-220. 5. Apaydin B., Dede S., 2010. Electrophoretic profile of serum protein fractions from sheep naturally infected with Babesia ovis . Rev Med Vet, 161, 57-60. 6. Shen K., Ji Y., Chen GQ., Huang B., Zhang X., Wu S., Yu GP., Wang XC., 2011. Expression and clinical significance of the NDA repair enzyme MYH in esophageal squamous cell carcinoma. Exp Ther Med, 2, 1117 1120. 7. Cederbaum SD., Yu H., Grody WW., Kern RM., Yoo P., Iyer RK., 2004. Arginases I and II: do their functions overlap? Mol Genet Metab 81 (Suppl 1): S38 S44. 8. Jenkinson CP., Grody WW., Cederbaum SD., 1996. Comparative properties of arginase. Comp Biochem Physiol B Biochem Mol Biol, 114, 107 132. 9. Na S., Kim OS., Ryoo S., Kweon TD., Choi YS., Shim HS., Oh YJ., 2014. Cervical ganglion block attenuates the progression of pulmonary hypertension via nitric oxide and arginase pathways. Hypertension, 63, 309 315. 10. Yang J., Gonon AT., Sjöquist PO., Lundberg JO., Pernow J., 2013. Arginase regulates red blood cell nitric oxide synthase and export of cardioprotective nitric oxide bioactivity. Proc Natl Acad Sci, USA 110: 15049 15054. 11. Grohmann U., Bronte V., 2010. Control of immune response by amino acid metabolism. Immunol Rev, 236, 243–264. 12. Fairlamb AH., Cerami A., 1992. Metabolism and functions of trypanothione in the Kinetoplastida. Annu. Rev. Microbiol, 46, 695–729. 13. Durante W., Johnson FK., Johnson RA., 2007. Arginase: A critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol, 34(9), 906–911. 14. Young CL., Feierstein A., Southwick FS., 1994. Calcium regulation of actin filament capping and monomer binding by macrophage capping protein. Journal of Biological Chemistry, 269(19), 13997-14002. 15. Hui QS., Masaya Y., Marisan M., Yin HL., 1999. Gelsolin, a Multifunctional Actin Regulatory Protein. Journal of Biological Chemistry, 274, 33179-33182. 16. Hu Y., Li H., Li WH., Meng HX., Fan YZ., 2013. The value of decreased plasma gelsolin levels in patients with systemic lupus erythematosus and rheumatoid arthritis in diagnosis and disease activity evaluation. Lupus, 22(14), 1455-1461. 17. Marrocco C., Rinalducci S., Mohamadkhani A., D'Amici GM., Zolla L., 2010. Plasma gelsolin protein: a candidate biomarker for hepatitis B-associated liver cirrhosis identified by proteomic approach. Blood Transfusion, 8(3), 105-112. 18. DiNubile M., Antin J., Bressler S., Stossel T., Ferrara J., 1998. Decreased gelsolin levels are associated with interstitial pneumonia after allogeneic BMT. Blood, 92, 683a. 19. Smith DB., Janmey PA., Sherwood JA., Howard RJ., Lind SE., 1988. Decreased plasma gelsolin levels in patients with Plasmodium falciparum malaria: a consequence of hemolysis? Blood, 72(1), 214-218. 20. Villa P., Jiménez M., Soriano MC., Manzanares J., Casasnovas P., 2005. Serum cystatin C concentration as a marker of acute renal dysfunction in critically ill patients. Critical Care, 9, 139-143. 21. Filler G.., Bokenkamp A, Hofmann W., Le Bricon T., Martinez-Bru C., 2005. Cystatin C as a marker of GFR-history, indications, and future research. Clin Biochem, 38, 1–8. 22. Antognoni MT., Siepi D., Porciello F., Rueca F., Fruganti G., 2007. Serum Cystatin-C Evaluation in Dogs Affected by Different Diseases Associated or Not with Renal Insufficiency. Vet Res Commun, 31(1), 269-271. 23. Lassus J., Harjola VP., 2012. Cystatin C. a step forward in assessing kidney function and cardiovascular risk. Heart Failure Reviews, 17, 251–261. 24. Herget-Rosenthal S., Bökenkamp A., Hofmann W., 2007. How to estimate GFR-serum creatinine, serum cystatin C or equations? Clin Biochem, 40, 153–161. 25. Bostom AG., Gohh RY., Bausserman L., Hakas D., Jacques PF., 1999. Serum Cystatin C as a Determinant of Fasting Total Homocysteine Levels in Renal Transplant Recipients with a Normal Serum Creatinine. J Am Society Nephrol, 10, 164–166. 26. Jensen AL., Bomholt M., Moe L., 2001. Preliminary evaluation of a particle-enhanced turbidimetric immunoassay (PETIA) for the determination of serum cystatin C-like immunoreactivity in dogs. Vet Clin Path, 30(2), 86-90. 27. Almy FS., Christopher MM., King DP., Brown SA., 2002. Evaluation of cystatin C as an endogenous marker of glomerular filtration rate in dogs. J Vet Intern Med, 16(1), 45-51. 28. Sevinc F., Turgut K., Sevinc M., 2007. Therapeutic and prophylactic efficacy of imidocarb dipropionate on experimental Babesia ovis infection of lambs. Vet Parasitol, 149, 65-71. 29. Azimzadeh K., Nouri K., Farooghi H., Rasouli S., Zamani N., 2013. Plasma malondialdehyde, thyroid hormones and some blood profiles in ovine Babesiosis. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 19, 489–493. 30. Goddard A., Leisewitz AL., Kjelgaard-Hansen M., Kristensen AT., Schoeman JP., 2016. Excessive Pro-Inflammatory Serum Cytokine Concentrations in Virulent Canine Babesiosis. PLoS ONE, 11(3), e0150113. 31. Esmaeilnejad B., Tavassoli M., Siamak Asri-Rezaei., 2012. Investigation of hematological and biochemical parameters in small ruminants naturally infected with Babesia ovis. Vet Res Forum, 3(1), 31–36. 32. Gobert A., Daulouede S., Lepoivre M., Boucher J., Bouteille B., Buguet A., Cespuglio R., Veyret B., Vincendeau P., 2000. L-Arginine availability modulates local nitric oxide production and parasite killing in experimental trypanosomiasis. Infect Immun, 68, 4653– 4657. 33. Duleu S., Vincendeau P., Courtois P., Semballa S., Lagroye I., Daulouède S., Boucher J., 2004. Mouse strain susceptibility to trypanosome infection: an arginase-dependent effect. J Immunol 172, 6298–6303. 34. Sandalova E., Laccabue D., Boni C., Watanabe T., Tan A., Zong HZ., Ferrari C., 2012. Increased levels of arginase in patients with acute hepatitis B suppress antiviral T cells. Gastroenterology, 143, 78–87. 35. Abebe T., Hailu A., Woldeyes M., Mekonen W., Bilcha K., Cloke T., Fry L., 2012. Local increase of arginase activity in lesions of patients with cutaneous leishmaniasis in Ethiopia. PLoS Negl Trop Dis, 6, e1684. 36. De Boniface J., Mao Y., Schmidt-Mende J., Kiessling R., Poschke I., 2012. Expression patterns of the immunomodulatory enzyme arginase I in blood, lymph nodes and tumor tissue of early-stage breast cancer patients. Oncoimmunology, 1, 1305–1312. 37. Perez G., Olivares IM., Rodriguez MG., Ceballos GM., Garcia Sanchez JR., 2012. Arginase activity in patients with breast cancer: an analysis of plasma, tumors, and its relationship with the presence of the estrogen receptor. Onkologie, 35, 570 –574. 38. Mei L., Zheng S., Shengbin X., Enyun S., 2014. Predictive value of serum gelsolin in hepatitis B virus (HBV)-related chronic liver disease. African Journal of Biotechnology, 11(20), 4640-4645. 39. Zhao DQ., Wang K., Zhang HD., Li YJ., 2013. Significant reduction of plasma gelsolin levels in patients with intracerebral hemorrhage. Clinica Chimica Acta, 415, 202-206. 40. Pasa S., Bayramli G., Atasoy A., Karul A., Ertug S., Ozensoy Toz S., 2009. Evaluation of serum cystatin-C in dogs with visceral leishmaniasis. Veterinary Research Communications, 33(6), 529-534. 41. Pekmezci D., Guzel M., Yildirim A., Ciftci G., Pekmezci G.Z., Tutuncu, M., 2015a. Evaluation of serum cystatin-C concentrations in dogs infected with Dirofilaria immitis. Ankara Universitesi Veteriner Fakultesi Dergisi, 62(4), 303-306. 42. Pekmezci D., Ural K., Aysul N., Guzel M., Ciftci G., (2015b). Assessment of renal function using canine cystatin- C levels in canine babesiosis and ehrlichiosis. Acta Veterinaria-Beograd, 65(1), 56-65. 43. Azimzadeh K., Izadmehr S., 2017. Evaluation of plasma hepcidin, cystatin c and gelsolin in ovine Theileriosis (Ghezel breed) based on age and parasitemia rate. Journal of veterinary clinical pathology, 11(1), 1-11. 44. Ahi S., Meram I., Ozdemir Y., 1999. Human serum arginase activity was measured by a sensitive enzyme properties and development of the method. Erciyes Medical Journal, 21, 3-9.
Toplam 1 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Sağlık Kurumları Yönetimi
Bölüm Araştırma Makaleleri
Yazarlar

Kaveh Azimzadeh

Mortaza Mahan Bu kişi benim

Negar Zamani Hergalanı Bu kişi benim 0000-0002-4919-1704

Tohid Zahed Bu kişi benim 0000-0002-0530-2935

Yayımlanma Tarihi 28 Nisan 2019
Yayımlandığı Sayı Yıl 2019 Cilt: 14 Sayı: 1

Kaynak Göster

APA Azimzadeh, K., Mahan, M., Zamani Hergalanı, N., 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 Bilimleri Dergisi, 14(1), 1-7. https://doi.org/10.17094/ataunivbd.367320
AMA Azimzadeh K, Mahan M, Zamani Hergalanı N, Zahed T. Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. Nisan 2019;14(1):1-7. doi:10.17094/ataunivbd.367320
Chicago Azimzadeh, Kaveh, Mortaza Mahan, Negar Zamani Hergalanı, ve Tohid Zahed. “Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 14, sy. 1 (Nisan 2019): 1-7. https://doi.org/10.17094/ataunivbd.367320.
EndNote Azimzadeh K, Mahan M, Zamani Hergalanı N, Zahed T (01 Nisan 2019) Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 14 1 1–7.
IEEE K. Azimzadeh, M. Mahan, N. Zamani Hergalanı, ve T. Zahed, “Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate”, Atatürk Üniversitesi Veteriner Bilimleri Dergisi, c. 14, sy. 1, ss. 1–7, 2019, doi: 10.17094/ataunivbd.367320.
ISNAD Azimzadeh, Kaveh vd. “Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 14/1 (Nisan 2019), 1-7. https://doi.org/10.17094/ataunivbd.367320.
JAMA Azimzadeh K, Mahan M, Zamani Hergalanı N, Zahed T. Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2019;14:1–7.
MLA Azimzadeh, Kaveh vd. “Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, c. 14, sy. 1, 2019, ss. 1-7, doi:10.17094/ataunivbd.367320.
Vancouver Azimzadeh K, Mahan M, Zamani Hergalanı N, Zahed T. Determination of Possible Potential Biomarker Between Plasma Arginase, Gelsolin and Cystatin C in Sheep Babesiosis: Based on Parasitemia Rate. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2019;14(1):1-7.