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Variation of Copper and Zinc Levels in Sheep Flocks Infected with Toxoplasma gondii according to Sex

Year 2025, Volume: 36 Issue: 2, 121 - 125, 27.07.2025
https://doi.org/10.36483/vanvetj.1657671

Abstract

Toxoplasmosis is a common and insidious zoonotic disease. It is one of the main causes of reproductive losses in farmed animals such as sheep, goats and cattle and constitutes a serious problem. The aim of this study was to investigate the variation of copper and zinc levels according to sex in a sheep flock infected with Toxoplasma gondii. Copper and zinc levels in the blood sera of a total of 36 sheep (18 seropositive +18 seronegative), 20 females and 16 males from the same flock were measured. When compared with the reference values, both the average copper (65.90 μg/dL) and zinc (64.70 μg/dL) levels were found to be quite low. When the comparison was made according to gender, the p value for zinc was significant (p<0.001), but not for copper (p=0.615). The p values for copper (p=0.859) and zinc (p=0.681) were not significant when compared according to positivity and negativity. According to the values obtained, no correlation was found between copper and zinc.

References

  • Abd El-Hack ME, Alagawany M, Arif M et al. (2017). Organic or inorganic zinc in poultry nutrition: A review. World’s Poul Sci Jour, 73 (4), 904–915.
  • Adem IM, Alshafei NK, Saeed IH, Khaier MAM (2024). Impact of Toxoplasma gondii on Serum Protein Levels and Mineral Content in Sheep and Goats at a Small Dairy Farm in White Nile State, Sudan Int J of Path Res, 13 (5) 54-60.
  • Al-Masoudi HK, Khadhm A, AL-Karaawy FH (2020). The Impact of Toxoplasma gondii Infection on The Serum Zinc, Vitamin D and Malondialdehyde Levels among Recurrent Miscarriage Women in Babylon Province-Iraq. Sys Rev Pharm. 11 (7), 443-449.
  • Altıntaş A, Fidancı UR (1993). Evcil hayvanlarda ve insanda kanın biyokimyasal normal değerleri. Ankara Univ Vet Fak Derg, 40 (2), 173–186.
  • De Carvalho LP, de Melo EJT (2018). Further aspects of Toxoplasma gondii elimination in the presence of metals. Par research, 117 (4), 1245–1256.
  • Doguer C, Ha JH, Collins JF (2018). Intersection of iron and copper metabolism in the mammalian intestine and liver. Compr Physiol, 8 (4), 1433–1461.
  • Ferra B, Holec-Gąsior L, Grąźlewska W (2020). Toxoplasma gondii recombinant antigens in the serodiagnosis of toxoplasmosis in domestic and farm animals. Animals, 10 (8), 1245.
  • Giadinis ND, Terpsidis K, Diakou et al. (2011). Massive Toxoplasma abortions in a dairy sheep flock and therapeutic approach with different doses of sulfadimidine. Turk J Vet Anim Sci., 35 (3), 207–211.
  • Hagmeyer S, Haderspeck JC, Grabrucker AM (2015). Behavioral impairments in animal models for zinc deficiency. Front. Behav Neurosci, 8, 443.
  • Hill GM, Shannon MC (2019). Copper and zinc nutritional issues for agricultural animal production. Biol. Trace Elem Res, 188 (1), 148–159.
  • Hussain S, Khan M, Sheikh TMM et al. (2022). Zinc essentiality, toxicity, and its bacterial bioremediation: A comprehensive insight. Front. Microbiol., 13, 900740.
  • Jin X, Meng L, Zhang R, et al. (2023). Effects of essential mineral elements deficiency and supplementation on serum mineral elements concentration and biochemical parameters in grazing Mongolian sheep. Front in vet sci. 10, 1214346.
  • Johnston H, Beasley L, MacPherson N (2014). Copper toxicity in a New Zealand dairy herd. Ir Vet J, 67, 20.
  • Lei XJ, Liu ZZ, Park JH, Kim IH (2022). Novel zinc sources as antimicrobial growth promoters for monogastric animals: A review. J Anim Sci Technol, 64, 187–196.
  • Lim A, Kumar V, Hari Dass SA, Vyas A (2013). Toxoplasma gondii infection enhances testicular steroidogenesis in rats. Mol ecology, 22 (1), 102–110.
  • López-Ureña NM, Calero-Bernal R, Vázquez-Calvo Á, et al. (2023). A comparative study of serological tests used in the diagnosis of Toxoplasma gondii infection in small ruminants evidenced the importance of cross-reactions for harmonizing diagnostic performance. Research in veterinary science. 165, 105052.
  • Mitra S, Paul S, Roy S et al. (2022). Exploring the immune-boosting functions of vitamins and minerals as nutritional food bioactive compounds: A comprehensive review. Molecules, 27 (2), 555.
  • Mumtaz T, Awan UA, Mushtaq A et al. (2022). Prevalence of toxoplasmosis in sheep and goats in Pakistan: A systematic review and meta-analysis. Pathogens, 11 (11), 1331.
  • Osredkar J, Sustar N (2011). Copper and zinc, biological role and significance of copper/zinc imbalance. J Clinic Toxicol, S3.
  • Paștiu AI, Mircean V, Mercier A et al. (2023). Toxoplasma gondii infection in sheep from Romania. Paras & Vect, 16, 24.
  • Pereira AM, Maia MRG, Fonseca AJM, Cabrita ARJ (2021). Zinc in dog nutrition, health and disease: A review. Animals, 11 (4), 978.
  • Portes JA, Motta CS, Azeredo NF et al. (2017). In vitro treatment of Toxoplasma gondii with copper(II) complexes induces apoptosis-like and cellular division alterations. Vet parasitol, 245, 141–152.
  • Reis LSLS, Pardo PE, Camargos AS, Oba E (2010). Mineral element and heavy metal poisoning in animals. J Med Med Sci, 1 (12), 560–579.
  • Robert-Gangneux F, Dardé ML (2012). Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev, 25 (2), 264–296.
  • Roberts CW, Walker W, Alexander J (2001). Sex-associated hormones and immunity to protozoan parasites. Clinical microbiology reviews, 14 (3), 476–488.
  • Seyrek K, Paşa S, Kıral F et al. (2004). Levels of zinc, copper and magnesium in sheep with toxoplasmosis. Uludag Univ J Fac Vet Med, 23 (1-3), 39–42.
  • Stelzer S, Basso W, Benavides Silván J et al. (2019). Toxoplasma gondii infection and toxoplasmosis in farm animals: Risk factors and economic impact. Food Waterborne Parasitol, 15, e00037.
  • Tabatabaie F, Jalalizadegan B, Ghaffarifar F et al. (2018). Evaluation the effects of vitamins (C and E) and minerals (selenium and calcium) on proliferation of Toxoplasma gondii tachyzoites. Int Jour of Inf Dis, 73, 325.
  • Takahashi A (2022). Role of Zinc and Copper in Erythropoiesis in Patients on Hemodialysis. Jour of Ren Nutr, 2022, 1-8.
  • Tan S, Tong WH, Vyas A (2022). Impact of Plant-Based Foods and Nutraceuticals on Toxoplasma gondii Cysts: Nutritional Therapy as a Viable Approach for Managing Chronic Brain Toxoplasmosis. Front Nutr, 9, 827286.
  • Tapiero H, Townsend DM, Tew KD (2003). Trace elements in human physiology and pathology. Copper. Biomed Pharmacother, 57 (9), 386-398.
  • Tasci S, Sengil AZ, Altindis M, Arisoy K (1995). The effect of zinc supplementation in experimentally induced Toxoplasma gondii infection. Jour of the Egyptian Soc of Paras, 25 (3), 745–751.
  • Thaprawat P, Wang F, Chalasani S et al. (2025). Toxoplasma gondii PROP1 is critical for autophagy and parasite viability during chronic infection. mSphere, 10 (3), e0082924.
  • Trigunaite A, Dimo J, Jørgensen TN (2015). Suppressive effects of androgens on the immune system. Cell Immunol, 294 (2) 294, 87-94.
  • Wysocka K, Cacak-Pietrzak G, Sosulski T (2025). Mineral Concentration in Spring Wheat Grain Under Organic, Integrated, and Conventional Farming Systems and Their Alterations During Processing. Plants, 14 (7), 1003.
  • Yıldız Öz G, Ormancı N (2022). Marmara Bölgesindeki Koyunlarda Serum Bakır (Cu) ve Çinko (Zn) Değerleri. Turk Vet J, 3 (2), 34-37.
  • Zhang X, Zhang H, Fu Y et al. (2018). Effects of Estradiol and Progesterone-Induced Intracellular Calcium Fluxes on Toxoplasma gondii Gliding, Microneme Secretion, and Egress. Front in microbiol, 9, 1266.

Toxoplasma gondii ile Enfekte Koyun Sürüsünde Bakır ve Çinko Düzeylerinin Cinsiyete Göre Değişimi

Year 2025, Volume: 36 Issue: 2, 121 - 125, 27.07.2025
https://doi.org/10.36483/vanvetj.1657671

Abstract

Tokzoplazmozis, yaygın olarak görülen ve sinsi seyreden zoonoz bir hastalıktır. Çiftliklerde yetiştirilen koyun, keçi, sığır gibi hayvanlarda üreme kayıplarının ana nedenlerinden biri olarak görülür ve ciddi bir sorun teşkil eder. Bu çalışmada Toxoplasma gondii ile enfekte bir koyun sürüsünde bakır ve çinko düzeylerinin cinsiyete göre değişiminin incelenmesi amaçlandı. Çalışmada aynı sürüden 20 dişi 16 erkek olmak üzere toplam 36 (18 seropozitif +18 seronegatif) koyunun kan serumlarındaki bakır ve çinko düzeyleri ölçüldü. Referans değerlerle kıyaslandığında gerek bakır ortalaması (65.90 μg/dL) gerekse çinko ortalamasının (64.70 μg/dL) oldukça düşük kaldığı görüldü. Cinsiyete göre karşılaştırma yapıldığında, çinko için p değeri anlamlı (p<0.001), bakır için ise anlamlı bulunmadı (p=0.615). Pozitif ve negatifliğe göre karşılaştırılma yapıldığında bakır (p=0.859) ve çinko (p=0.681) için p değeri anlamlı bulunmadı. Elde edilen değerlere göre bakır ve çinko arasında korelasyon bulunmadı.

Ethical Statement

Çalışmaya Samsun Veteriner Kontrol Enstitüsü Hayvan Deneyleri Yerel Etik Kurulunun 02.12.2022 tarih ve 2022-8 no’lu etik kurul kararına ihtiyaç olmadığı yazısı alınarak başlandı. Yazarlar çıkar çatışması olmadığını beyan ederler.

References

  • Abd El-Hack ME, Alagawany M, Arif M et al. (2017). Organic or inorganic zinc in poultry nutrition: A review. World’s Poul Sci Jour, 73 (4), 904–915.
  • Adem IM, Alshafei NK, Saeed IH, Khaier MAM (2024). Impact of Toxoplasma gondii on Serum Protein Levels and Mineral Content in Sheep and Goats at a Small Dairy Farm in White Nile State, Sudan Int J of Path Res, 13 (5) 54-60.
  • Al-Masoudi HK, Khadhm A, AL-Karaawy FH (2020). The Impact of Toxoplasma gondii Infection on The Serum Zinc, Vitamin D and Malondialdehyde Levels among Recurrent Miscarriage Women in Babylon Province-Iraq. Sys Rev Pharm. 11 (7), 443-449.
  • Altıntaş A, Fidancı UR (1993). Evcil hayvanlarda ve insanda kanın biyokimyasal normal değerleri. Ankara Univ Vet Fak Derg, 40 (2), 173–186.
  • De Carvalho LP, de Melo EJT (2018). Further aspects of Toxoplasma gondii elimination in the presence of metals. Par research, 117 (4), 1245–1256.
  • Doguer C, Ha JH, Collins JF (2018). Intersection of iron and copper metabolism in the mammalian intestine and liver. Compr Physiol, 8 (4), 1433–1461.
  • Ferra B, Holec-Gąsior L, Grąźlewska W (2020). Toxoplasma gondii recombinant antigens in the serodiagnosis of toxoplasmosis in domestic and farm animals. Animals, 10 (8), 1245.
  • Giadinis ND, Terpsidis K, Diakou et al. (2011). Massive Toxoplasma abortions in a dairy sheep flock and therapeutic approach with different doses of sulfadimidine. Turk J Vet Anim Sci., 35 (3), 207–211.
  • Hagmeyer S, Haderspeck JC, Grabrucker AM (2015). Behavioral impairments in animal models for zinc deficiency. Front. Behav Neurosci, 8, 443.
  • Hill GM, Shannon MC (2019). Copper and zinc nutritional issues for agricultural animal production. Biol. Trace Elem Res, 188 (1), 148–159.
  • Hussain S, Khan M, Sheikh TMM et al. (2022). Zinc essentiality, toxicity, and its bacterial bioremediation: A comprehensive insight. Front. Microbiol., 13, 900740.
  • Jin X, Meng L, Zhang R, et al. (2023). Effects of essential mineral elements deficiency and supplementation on serum mineral elements concentration and biochemical parameters in grazing Mongolian sheep. Front in vet sci. 10, 1214346.
  • Johnston H, Beasley L, MacPherson N (2014). Copper toxicity in a New Zealand dairy herd. Ir Vet J, 67, 20.
  • Lei XJ, Liu ZZ, Park JH, Kim IH (2022). Novel zinc sources as antimicrobial growth promoters for monogastric animals: A review. J Anim Sci Technol, 64, 187–196.
  • Lim A, Kumar V, Hari Dass SA, Vyas A (2013). Toxoplasma gondii infection enhances testicular steroidogenesis in rats. Mol ecology, 22 (1), 102–110.
  • López-Ureña NM, Calero-Bernal R, Vázquez-Calvo Á, et al. (2023). A comparative study of serological tests used in the diagnosis of Toxoplasma gondii infection in small ruminants evidenced the importance of cross-reactions for harmonizing diagnostic performance. Research in veterinary science. 165, 105052.
  • Mitra S, Paul S, Roy S et al. (2022). Exploring the immune-boosting functions of vitamins and minerals as nutritional food bioactive compounds: A comprehensive review. Molecules, 27 (2), 555.
  • Mumtaz T, Awan UA, Mushtaq A et al. (2022). Prevalence of toxoplasmosis in sheep and goats in Pakistan: A systematic review and meta-analysis. Pathogens, 11 (11), 1331.
  • Osredkar J, Sustar N (2011). Copper and zinc, biological role and significance of copper/zinc imbalance. J Clinic Toxicol, S3.
  • Paștiu AI, Mircean V, Mercier A et al. (2023). Toxoplasma gondii infection in sheep from Romania. Paras & Vect, 16, 24.
  • Pereira AM, Maia MRG, Fonseca AJM, Cabrita ARJ (2021). Zinc in dog nutrition, health and disease: A review. Animals, 11 (4), 978.
  • Portes JA, Motta CS, Azeredo NF et al. (2017). In vitro treatment of Toxoplasma gondii with copper(II) complexes induces apoptosis-like and cellular division alterations. Vet parasitol, 245, 141–152.
  • Reis LSLS, Pardo PE, Camargos AS, Oba E (2010). Mineral element and heavy metal poisoning in animals. J Med Med Sci, 1 (12), 560–579.
  • Robert-Gangneux F, Dardé ML (2012). Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev, 25 (2), 264–296.
  • Roberts CW, Walker W, Alexander J (2001). Sex-associated hormones and immunity to protozoan parasites. Clinical microbiology reviews, 14 (3), 476–488.
  • Seyrek K, Paşa S, Kıral F et al. (2004). Levels of zinc, copper and magnesium in sheep with toxoplasmosis. Uludag Univ J Fac Vet Med, 23 (1-3), 39–42.
  • Stelzer S, Basso W, Benavides Silván J et al. (2019). Toxoplasma gondii infection and toxoplasmosis in farm animals: Risk factors and economic impact. Food Waterborne Parasitol, 15, e00037.
  • Tabatabaie F, Jalalizadegan B, Ghaffarifar F et al. (2018). Evaluation the effects of vitamins (C and E) and minerals (selenium and calcium) on proliferation of Toxoplasma gondii tachyzoites. Int Jour of Inf Dis, 73, 325.
  • Takahashi A (2022). Role of Zinc and Copper in Erythropoiesis in Patients on Hemodialysis. Jour of Ren Nutr, 2022, 1-8.
  • Tan S, Tong WH, Vyas A (2022). Impact of Plant-Based Foods and Nutraceuticals on Toxoplasma gondii Cysts: Nutritional Therapy as a Viable Approach for Managing Chronic Brain Toxoplasmosis. Front Nutr, 9, 827286.
  • Tapiero H, Townsend DM, Tew KD (2003). Trace elements in human physiology and pathology. Copper. Biomed Pharmacother, 57 (9), 386-398.
  • Tasci S, Sengil AZ, Altindis M, Arisoy K (1995). The effect of zinc supplementation in experimentally induced Toxoplasma gondii infection. Jour of the Egyptian Soc of Paras, 25 (3), 745–751.
  • Thaprawat P, Wang F, Chalasani S et al. (2025). Toxoplasma gondii PROP1 is critical for autophagy and parasite viability during chronic infection. mSphere, 10 (3), e0082924.
  • Trigunaite A, Dimo J, Jørgensen TN (2015). Suppressive effects of androgens on the immune system. Cell Immunol, 294 (2) 294, 87-94.
  • Wysocka K, Cacak-Pietrzak G, Sosulski T (2025). Mineral Concentration in Spring Wheat Grain Under Organic, Integrated, and Conventional Farming Systems and Their Alterations During Processing. Plants, 14 (7), 1003.
  • Yıldız Öz G, Ormancı N (2022). Marmara Bölgesindeki Koyunlarda Serum Bakır (Cu) ve Çinko (Zn) Değerleri. Turk Vet J, 3 (2), 34-37.
  • Zhang X, Zhang H, Fu Y et al. (2018). Effects of Estradiol and Progesterone-Induced Intracellular Calcium Fluxes on Toxoplasma gondii Gliding, Microneme Secretion, and Egress. Front in microbiol, 9, 1266.
There are 37 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Biochemistry
Journal Section Araştırma Makaleleri
Authors

Neslihan Ormancı 0000-0001-7645-3792

Rıfat Pak 0009-0005-0904-8144

Selma Kaya 0000-0002-8934-3418

Publication Date July 27, 2025
Submission Date March 14, 2025
Acceptance Date July 11, 2025
Published in Issue Year 2025 Volume: 36 Issue: 2

Cite

APA Ormancı, N., Pak, R., & Kaya, S. (2025). Toxoplasma gondii ile Enfekte Koyun Sürüsünde Bakır ve Çinko Düzeylerinin Cinsiyete Göre Değişimi. Van Veterinary Journal, 36(2), 121-125. https://doi.org/10.36483/vanvetj.1657671
AMA Ormancı N, Pak R, Kaya S. Toxoplasma gondii ile Enfekte Koyun Sürüsünde Bakır ve Çinko Düzeylerinin Cinsiyete Göre Değişimi. Van Vet J. July 2025;36(2):121-125. doi:10.36483/vanvetj.1657671
Chicago Ormancı, Neslihan, Rıfat Pak, and Selma Kaya. “Toxoplasma Gondii Ile Enfekte Koyun Sürüsünde Bakır Ve Çinko Düzeylerinin Cinsiyete Göre Değişimi”. Van Veterinary Journal 36, no. 2 (July 2025): 121-25. https://doi.org/10.36483/vanvetj.1657671.
EndNote Ormancı N, Pak R, Kaya S (July 1, 2025) Toxoplasma gondii ile Enfekte Koyun Sürüsünde Bakır ve Çinko Düzeylerinin Cinsiyete Göre Değişimi. Van Veterinary Journal 36 2 121–125.
IEEE N. Ormancı, R. Pak, and S. Kaya, “Toxoplasma gondii ile Enfekte Koyun Sürüsünde Bakır ve Çinko Düzeylerinin Cinsiyete Göre Değişimi”, Van Vet J, vol. 36, no. 2, pp. 121–125, 2025, doi: 10.36483/vanvetj.1657671.
ISNAD Ormancı, Neslihan et al. “Toxoplasma Gondii Ile Enfekte Koyun Sürüsünde Bakır Ve Çinko Düzeylerinin Cinsiyete Göre Değişimi”. Van Veterinary Journal 36/2 (July2025), 121-125. https://doi.org/10.36483/vanvetj.1657671.
JAMA Ormancı N, Pak R, Kaya S. Toxoplasma gondii ile Enfekte Koyun Sürüsünde Bakır ve Çinko Düzeylerinin Cinsiyete Göre Değişimi. Van Vet J. 2025;36:121–125.
MLA Ormancı, Neslihan et al. “Toxoplasma Gondii Ile Enfekte Koyun Sürüsünde Bakır Ve Çinko Düzeylerinin Cinsiyete Göre Değişimi”. Van Veterinary Journal, vol. 36, no. 2, 2025, pp. 121-5, doi:10.36483/vanvetj.1657671.
Vancouver Ormancı N, Pak R, Kaya S. Toxoplasma gondii ile Enfekte Koyun Sürüsünde Bakır ve Çinko Düzeylerinin Cinsiyete Göre Değişimi. Van Vet J. 2025;36(2):121-5.

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