Serum trace element levels in dogs with canine visceral leishmaniasis

Canine visceral leishmaniasis has been denoted as neglected despite being a very well-known disease. Trace element alteration has been recognized in humans with visceral and cutaneous leishmaniasis, together with canine visceral leishmaniasis. The trace elements occupy a vital position in the immunological system, and host immune responses mitigate defense against leishmaniasis. We aimed to select trace elements in a total of 45 dogs of several breeds; those at the age of 11 months to 6 and from both sexes (26 male and 19 female) were enrolled in the study. The dogs included in the study were divided into leishmaniasis-infected and noninfected groups. All cases in this study were included according to written owner consent. The trace element analysis of serum samples was carried out by using an inductively coupled plasma-optical emission spectrometry. The results of our study revealed that between the canine visceral leishmaniasis infected group and the uninfected group, Leishmania-positive dogs had significantly lower levels of Se (p < 0.001) and Zn (p < 0.001) compared to the negative ones. These results should be carefully elucidated in an attempt to analyze immune responses in dogs with canine visceral leishmaniasis.

Anahtar Kelime: Immune response selenium vector borne disease zinc

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık

1. Ertabaklar H, Ertuğ S, Çalışkan SÖ, Bozdoğan B. Determination of Leishmania species by PCR-RFLP in the smear samples taken from the lesions of cutaneous leishmaniasis cases. Mikrobiyoloji Bülteni 2016; 50 (2): 300-306. https://doi. org/10.5578/mb.22070.
2. Miró G, López-Vélez R. Clinical management of canine leishmaniosis versus human leishmaniasis due to Leishmania infantum: putting “One Health” principles into practice. Veterinary Parasitology 2018; 254: 151-159. https://doi. org/10.1016/j.vetpar.2018.03.002.
3. Ribeiro RR, Michalick MSM, da Silva ME, dos Santos CCP, Frézard FJG et al. Canine leishmaniasis: an overview of the current status and strategies for control. BioMed Research International 2018. https://doi.org/10.1155/2018/3296893
4. Karakuş M, Arserim SK, Kasap ÖE, Pekağırbaş M, Aküzüm D et al. Vector and reservoir surveillance study in a canine and human leishmaniasis endemic area in most western part of Turkey, Karaburun. Acta Tropica 2019; 190: 177-182. https:// doi.org/10.1016/j.actatropica.2018.11.020.
5. Koenhemsi L, Fabrizio V, Mariella P, Antonella M, Or E. Seroprevalence of Leishmaniosis Among Healthy Dogs in Istanbul. Israel Journal of Veterinary Medicine 2020; 75 (1): 31-34.
6. Arslan S, Öncel T, Yenİlmez K, Turan N. Detection of Leishmania infantum seropositivity in dogs by ELISA technique in Thrace region of Turkey. Eurasian Journal of Veterinary Sciences 2019; 35 (3): 165-169.
7. Buckingham-Jeffery E, Hill EM, Datta S, Dilger E, Courtenay O. Spatio-temporal modelling of Leishmania infantum infection among domestic dogs: a simulation study and sensitivity analysis applied to rural Brazil. Parasites & Vectors, 2019; 12 (1): 1-13. https://doi.org/10.1186/s13071-019-3430-y.
8. Alvar J, Canavate C, Molina R, Moreno J, Nieto J. Canine leishmaniasis. Advances in Parasitology 2004; 57 (3): 1-88.
9. Melo FA, Moura EP, Ribeiro RR, Alves CF, Caliari MV et al. Hepatic extracellular matrix alterations in dogs naturally infected with Leishmania (Leishmania) chagasi. International Journal of Experimental Pathology 2009; 90 (5): 538-548. https://doi.org/10.1111/j.1365-2613.2009.00681.x.
10. Souza CC, de O Barreto T, da Silva SM, Pinto AW, Figueiredo MM et al. A potential link among antioxidant enzymes, histopathology and trace elements in canine visceral leishmaniasis. International Journal of Experimental Pathology 2014; 95 (4): 260-270. https://doi.org/10.1111/iep.12080.
11. Silva LC, Castro RS, Figueiredo MM, Michalick MS, Tafuri WL et al. Canine visceral leishmaniasis as a systemic fibrotic disease. International Journal of Experimental Pathology 2013; 94 (2): 133-143. https://doi.org/10.1111/iep.12010.
12. Reis AB, Martins-Filho OA, Teixeira-Carvalho A, Giunchetti RC, Carneiro CM et al. Systemic and compartmentalized immune response in canine visceral leishmaniasis. Veterinary Immunology and Immunopathology 2009; 128: 87-95. https:// doi.org/10.1016/j.vetimm.2008.10.307.
13. Ayele A, Seyoum Z. Review on canine leishmaniasis, etiology, clinical sign, pathogenesis, treatment and control methods. Global Veterinaria 2016; 17 (4): 343-352. https://doi. org/10.5829/idosi.gv.2016.17.04.104151.
14. Matte C, Olivier M. Leishmania-induced cellular recruitment during the early inflammatory response: modulation of proinflammatory mediators. The Journal of Infectious Diseases 2002; 185 (5): 673-681. https://doi.org/10.1086/339260.
15. Scot, P, Novais FO. Cutaneous leishmaniasis: immune responses in protection and pathogenesis. Nature Reviews Immunology 2016; 16 (9): 581-592. https://doi.org/10.1038/nri.2016.72.
16. Chaudhuri S, Varshney JP, Patra RC. Erythrocytic antioxidant defense, lipid peroxides level and blood iron, zinc and copper concentrations in dogs naturally infected with Babesia gibsoni. Research in Veterinary Science, 2008; 85 (1): 120-124. https://doi.org/10.1016/j.rvsc.2007.09.001.
17. Klotz LO, Kroncke KD, Buchczyk DP, Sies H. Role of copper, zinc, selenium and tellurium in the cellular defense against oxidative and nitrosative stress. The Journal of Nutrition 2003; 133: 1448-1451. https://doi.org/10.1093/jn/133.5.1448S.
18. Prashanth L, Kattapagari KK, Chitturi RT, Baddam VRR, Prasad LK. A review on role of essential trace elements in health and disease. Journal of dr. ntr University of Health Sciences 2015; 4 (2): 75.
19. Wołonciej M, Milewska E, Roszkowska-Jakimiec W. Trace elements as an activator of antioxidant enzymes. Postepy Higieny i Medycyny Doswiadczalnej 2016; 70: 1483-1498. https://doi.org/10.5604/17322693.1229074.
20. Chvapil M. New aspects in the biological role of zinc: a stabilizer of macromolecules and biological membranes. Life Sciences 1973; 13 (8): 1041-1049. https://doi.org/10.1016/0024- 3205(73)90372-X.
21. Britti D, Sconza S, Morittu VM, Santori D, Boari A. Superoxide dismutase and Glutathione peroxidase in the blood of dogs with Leishmaniasis. Veterinary Research Communications 2008; 32: 251–254. https://doi.org/10.1007/s11259-008-9121-3.
22. Heidarpour M, Soltani S, Mohri M, Khoshnegah J. Canine visceral leishmaniasis: relationships between oxidative stress, liver and kidney variables, trace elements, and clinical status. Parasitology Research 2012; 111 (4): 1491–1496. https://doi. org/10.1007/s00436-012-2985-8.
23. Pasa S, Kargin F, Bildik A, Seyrek K, Ozbel Y et al. Serum and hair levels of zinc and other elements in dogs with visceral leishmaniasis. Biological Trace Element Research 2003; 94 (2): 141–147. https://doi.org/10.1385/BTER:94:2:141.
24. Souza CC, Fabrino JHF, Beinner MA, Neto WB, Cangussu SD et al. Development and validation of methods for the determination of copper and iron in serum of dogs with canine visceral Leishmaniasis using multivariate optimization and GF AAS. Analytical Methods 2013; 5 (12): 3129-3135.
25. Lombardi P, Palatucci AT, Giovazzino A, Mastellone V, Ruggiero G et al. Clinical and Immunological Response in Dogs Naturally Infected by L. infantum Treated with a Nutritional Supplement. Animals 2019; 9 (8): 501. https://doi.org/10.3390/ani9080501.
26. Özbel Y, Turgay N, Özensoy S, Özbilgin A, Alkan MZ et al. Epidemiology, diagnosis and control of leishmaniasis in the Mediterranean region. Annals of Tropical Medicine & Parasitology 1995; 89 (1): 89-93. https://doi.org/10.1080/0003 4983.1995.11813018.
27. Underwood EJ. Trace elements in human and animal nutrition. 4th ed. London, UK: Academic Press; 1977.
28. Chandra RK, Dayton DH. Trace element regulation of immunity and infection. Nutrition Research 1982; 2 (6): 721- 733. https://doi.org/10.1016/S0271-5317(82)80116-4.
29. Kodama H. Essential trace elements and immunity. Japanese Journal of Clinical Medicine 1966; 54 (1): 46-51.
30. Maspi N, Abdoli A, Ghaffarifar F. Pro-and anti-inflammatory cytokines in cutaneous leishmaniasis: a review. Pathogens and Global Health 2016; 110 (6): 247–260. https://doi.org/10.1080/ 20477724.2016.1232042.
31. Rodrigues V, Cordeiro-da-Silva A, Laforge M, Silvestre R, Estaquier J. Regulation of immunity during visceral Leishmania infection. Parasites & Vectors 2016; 9 (1): 118. https://doi. org/10.1186/s13071-016-1412-x.
32. Abdoli A, Maspi N, Ghaffarifar F. Wound healing in cutaneous leishmaniasis: a double edged sword of IL-10 and TGF-β. omparative Immunology, Microbiology and Infectious Diseases, 2017; 51: 15–26. https://doi.org/10.1016/j.cimid.2017.02.001.
33. Kaye PM, Svensson M, Ato M, Maroof A, Polley R et al. The immunopathology of experimental visceral leishmaniasis. Immunological Reviews 2004; 201 (1): 239-253. https://doi. org/10.1111/j.0105-2896.2004.00188.x.
34. Cunningham AC. Parasitic adaptive mechanisms in infection by Leishmania. Experimental and Molecular Pathology 2002; 72: 132–141. https://doi.org/10.1006/exmp.2002.2418
35. Paltrinieri S, Ravicini S, Rossi G, Roura X. Serum concentrations of the derivatives of reactive oxygen metabolites(d-ROMs) in dogs with leishmaniosis. The Veterinary Journal 2010; 186: 393–395. https://doi.org/10.1016/j.tvjl.2009.08.019.
36. Karl L, Chvapil M, Zukoski CF. Effect of zinc on the viability and phagocytic capacity of peritoneal macrophages. Proceedings of the Society for Experimental Biology and Medicine 1973; 142 (4): 1123-1127. https://doi.org/10.3181/00379727-142-37190.
37. Kreindler TG, Weston WL, Hambidge KM, Dustin R. Effect of zinc-deficiency on neutrophil and monocyte function in rats. Journal of Investigative Dermatology 1977; 68 (4): 240-241.
38. Svenson KL, Halloren R, Johansson E, Lindh U. Reduced zinc in peripheral blood cells from patients with inflammatory connective tissue diseases. Inflammation 1985; 9 (2): 189-199. https://doi.org/10.1007/BF00917591.
39. Wagner HM, Beuscher HU, Röllinghoff M, Solbach W. Interferon-γ inhibits the efficacy of interleukin 1 to generate a Th2-cell biased immune response induced by Leishmania major. Immunobiology 1991; 182 (3-4): 292-306. https://doi. org/10.1016/S0171-2985(11)80664-9.
40. Wirth JJ, Fraker PJ, Kierszenbaum F. Zinc requirement for macrophage function: effect of zinc deficiency on uptake and killing of a protozoan parasite. Immunology 1989; 68 (1): 114.
41. Fraker PJ, Caruso R, Kierszenbaum F. Alteration of the immune and nutritional status of mice by synergy between zinc deficiency and infection with Trypanosoma cruzi. The Journal of Nutrition 1982; 112: 1224-1229. https://doi.org/10.1093/ jn/112.6.1224.
42. Shi HN, Scott ME, Stevenson MM, Koski KG. Zinc deficiency impairs T-cell function in mice with primary infection of Heligmosomoidespolygyrus(Nematoda).ParasiteImmunology 1994; 16: 339-350. https://doi.org/10.1111/j.1365-3024.1994. tb00359.x.
43. Scott ME, Koski KG. Zinc deficiency impairs immune responses against parasitic nematode infections at intestinal and systemic sites. The Journal of Nutrition 2000; 130: 1412–1420. https:// doi.org/10.1093/jn/130.5.1412S
44. Teodorowski O, Winiarczyk S, Tarhan D, Dokuzeylül B, Ercan AM et al. Antioxidant status, and blood zinc and copper concentrations in dogs with uncomplicated babesiosis due to infections. Journal of Veterinary Research 2021; 65 (2): 169- 174. https://doi.org/10.2478/jvetres-2021-0031.
45. Mishra J, Carpenter S, Singh S. Low serum zinc levels in an endemic area of visceral leishmaniasis in Bihar, India. Indian Journal of Medical Research 2010; 131: 793-798.
46. Pourfallah F, Javadian S, Zamani Z, Saghiri R, Sadeghi S, et al. Evaluation of serum levels of zinc, copper, iron, and zinc/ copper ratio in cutaneous leishmaniasis. Iranian Journal of Arthropod-Borne Diseases 2009; 3 (2): 7-11.
47. Zafra R, Jaber JR, Pérez-Ecija RA, Barragán A, Martínez- Moreno A et al. High iNOS expression in macrophages in canine leishmaniasis is associated with low intracellular parasite burden. Veterinary Immunology and Immunopathology 2008; 123 (3-4): 353-359. https://doi.org/10.1016/j. vetimm.2008.02.022.
48. Farzin L, Moassesi ME. A comparison of serum selenium, zinc and copper level in visceral and cutaneous leishmaniasis. The Official Journal of Isfahan University of Medical Sciences 2014; 19 (4): 355-357.
49. Koçyiğit A, Erel Ö, Gürel MS, Seyrek A, Aktepe N et al. Decreasing selenium levels and glutathione peroxidase activity in patients with cutaneous leishmaniasis. Turkish Journal of Medical Sciences 1999; 29 (3): 291-296.

APA	GAZYAGCI A, Bilgiç B, BAYSAL BAKAY B, Tarhan D, ERCAN A, erdoğan s, ERDOĞAN H, or e, Ural K (2023). Serum trace element levels in dogs with canine visceral leishmaniasis. , 155 - 159. 10.55730/1300-0128.4280
Chicago	GAZYAGCI AYCAN NURIYE,Bilgiç Bengü,BAYSAL BAKAY BERNA,Tarhan Duygu,ERCAN ALEV MELTEM,erdoğan songül,ERDOĞAN HASAN,or erman,Ural Kerem Serum trace element levels in dogs with canine visceral leishmaniasis. (2023): 155 - 159. 10.55730/1300-0128.4280
MLA	GAZYAGCI AYCAN NURIYE,Bilgiç Bengü,BAYSAL BAKAY BERNA,Tarhan Duygu,ERCAN ALEV MELTEM,erdoğan songül,ERDOĞAN HASAN,or erman,Ural Kerem Serum trace element levels in dogs with canine visceral leishmaniasis. , 2023, ss.155 - 159. 10.55730/1300-0128.4280
AMA	GAZYAGCI A,Bilgiç B,BAYSAL BAKAY B,Tarhan D,ERCAN A,erdoğan s,ERDOĞAN H,or e,Ural K Serum trace element levels in dogs with canine visceral leishmaniasis. . 2023; 155 - 159. 10.55730/1300-0128.4280
Vancouver	GAZYAGCI A,Bilgiç B,BAYSAL BAKAY B,Tarhan D,ERCAN A,erdoğan s,ERDOĞAN H,or e,Ural K Serum trace element levels in dogs with canine visceral leishmaniasis. . 2023; 155 - 159. 10.55730/1300-0128.4280
IEEE	GAZYAGCI A,Bilgiç B,BAYSAL BAKAY B,Tarhan D,ERCAN A,erdoğan s,ERDOĞAN H,or e,Ural K "Serum trace element levels in dogs with canine visceral leishmaniasis." , ss.155 - 159, 2023. 10.55730/1300-0128.4280
ISNAD	GAZYAGCI, AYCAN NURIYE vd. "Serum trace element levels in dogs with canine visceral leishmaniasis". (2023), 155-159. https://doi.org/10.55730/1300-0128.4280

APA	GAZYAGCI A, Bilgiç B, BAYSAL BAKAY B, Tarhan D, ERCAN A, erdoğan s, ERDOĞAN H, or e, Ural K (2023). Serum trace element levels in dogs with canine visceral leishmaniasis. Turkish Journal of Veterinary and Animal Sciences, 47(2), 155 - 159. 10.55730/1300-0128.4280
Chicago	GAZYAGCI AYCAN NURIYE,Bilgiç Bengü,BAYSAL BAKAY BERNA,Tarhan Duygu,ERCAN ALEV MELTEM,erdoğan songül,ERDOĞAN HASAN,or erman,Ural Kerem Serum trace element levels in dogs with canine visceral leishmaniasis. Turkish Journal of Veterinary and Animal Sciences 47, no.2 (2023): 155 - 159. 10.55730/1300-0128.4280
MLA	GAZYAGCI AYCAN NURIYE,Bilgiç Bengü,BAYSAL BAKAY BERNA,Tarhan Duygu,ERCAN ALEV MELTEM,erdoğan songül,ERDOĞAN HASAN,or erman,Ural Kerem Serum trace element levels in dogs with canine visceral leishmaniasis. Turkish Journal of Veterinary and Animal Sciences, vol.47, no.2, 2023, ss.155 - 159. 10.55730/1300-0128.4280
AMA	GAZYAGCI A,Bilgiç B,BAYSAL BAKAY B,Tarhan D,ERCAN A,erdoğan s,ERDOĞAN H,or e,Ural K Serum trace element levels in dogs with canine visceral leishmaniasis. Turkish Journal of Veterinary and Animal Sciences. 2023; 47(2): 155 - 159. 10.55730/1300-0128.4280
Vancouver	GAZYAGCI A,Bilgiç B,BAYSAL BAKAY B,Tarhan D,ERCAN A,erdoğan s,ERDOĞAN H,or e,Ural K Serum trace element levels in dogs with canine visceral leishmaniasis. Turkish Journal of Veterinary and Animal Sciences. 2023; 47(2): 155 - 159. 10.55730/1300-0128.4280
IEEE	GAZYAGCI A,Bilgiç B,BAYSAL BAKAY B,Tarhan D,ERCAN A,erdoğan s,ERDOĞAN H,or e,Ural K "Serum trace element levels in dogs with canine visceral leishmaniasis." Turkish Journal of Veterinary and Animal Sciences, 47, ss.155 - 159, 2023. 10.55730/1300-0128.4280
ISNAD	GAZYAGCI, AYCAN NURIYE vd. "Serum trace element levels in dogs with canine visceral leishmaniasis". Turkish Journal of Veterinary and Animal Sciences 47/2 (2023), 155-159. https://doi.org/10.55730/1300-0128.4280