The protective effects of propolis and flunixin meglumine on feed intake, antioxidant status and histological parameters in liver and kidney tissues against excess copper in rats

Pınar Tatlı Seven; Burcu Gül Baykalır; Tuba Parlak Ak; İsmail Seven; Neşe Başak; Mine Yaman

doi:10.1501/Vetfak_0000002873

Research Article

Year 2018, Volume: 65 Issue: 4, 395 - 406, 09.11.2018

Pınar Tatlı Seven Burcu Gül Baykalır Tuba Parlak Ak İsmail Seven Neşe Başak Mine Yaman

https://doi.org/10.1501/Vetfak_0000002873

Cited By: 7

Abstract

References

1. Abu-Zinadah OA, Hussein HK, Elshal MF, et al. (2012): Effect of excess dietary copper on proliferation and differentiation of the proerythroblasts and erythrocytes in rats. Afr J Biotechnol, 11, 6187-6191.
2. Aebi H (1984): Catalase in vitro methods in enzymology. In: Willam BJ, editor. Methods in enzymology. New York, USA: Academic Press; 1984. pp. 121-126.
3. Ahn MR, Kumazawa S, Usui Y (2007): Antioxidant activity and constituents of propolis collected in various areas of China. Food Chem, 101, 1383-1392.
4. Apak R, Guclu K, Ozyurek M, et al. (2004): Novel total antioxidantcapacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. J Agric Food Chem, 52, 7970-7981.
5. Babaknejad N, Moshtaghie AA, Shahanipour K (2015): The toxicity of copper on serum parameters related to renal functions in male wistar rats. Zahedan J Res Med Sci, 15, 29-31.
6. Bino RJ, de Vos CHR, Lieberman M, et al. (2005): The light-hyperresponsive high pigment-2dg mutation of tomato: alterations in the fruit metabolome. New Phytol, 166, 427-438.
7. Chiou PWS, Chen KL, Yu Bi (1998): Effect of dietary organic arsenicals and cupric sulfate on copper toxicity, liver accumulation and residue in eggs and excreta of laying hens. Anim Feed Sci Tech, 73, 161-171.
8. Ciftci O, Tanyildizi S, Godekmerdan A (2010): Protective effect of curcumin on immune system and body weight gain on rats intoxicated with 2,3,7,8- Tetrachlorodibenzo-p-dioxin (TCDD). Immunopharmacol Immunotoxicol, 32, 99-104.
9. Cook NC, Samman S (1996). Flavonoids-chemistry, metabolism, cardioprotective effects, and dietary sources. J Nutr Biochem, 7, 66-76.
10. Ellman GL (1959): Tissue Sulfhydryl groups. Arch Biochem Biophys, 82, 70-77.
11. Ferenci P (2004): Pathophysiology and clinical features of wilson disease. Metab Brain Dis, 19, 229-239.
12. Fuentealba IC, Aburto EM (2003): Animal models of copper-associated liver disease. Comp Hepatol, 2, 5.
13. Gaetke LM, Chow CK (2003): Copper toxicity, oxidative stress and antioxidant nutrients. Toxicology, 189, 147-163.
14. Gul Baykalir B, Tatli Seven P, Gur S, et al. (2016): The effects of propolis on sperm quality, reproductive organs and testicular antioxidant status of male rats treated with Cyclosporine-A. Anim Reprod, Belo Horizonte, 13, 105- 111.
15. Halliwell B, Gutteridge JMC (2007): Oxygen is a toxic gas – an introduction to oxygen toxicity and reactive species. In: Halliwell B, Gutteridge JMC, editors. Free radicals in biology and medicine. New York, USA: Oxford University Press; 2007. pp. 1-29.
16. Kabak YB, Gülbahar MY (2013): Sıçanlarda deneysel bakır zehirlenmesinde karaciğer ve böbrek dokularında apoptozisin belirlenmesi. Ankara Üniv Vet Fak, 60, 39-45.
17. Kim D, Jeong SW, Lee CY (2003): Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem, 81, 321-326.
18. Kodama H, Fujisawa C (2009): Copper metabolism and inherited copper transport disorders: molecular mechanisms, screening and treatment. Metallomics, 1, 42- 52.
19. Kornegay ET, van Heugten PHG, Lindemann MD, et al. (1989): Effects of biotin and high copper levels on performance and immune response of weanling pigs. J Anim Sci, 67, 1471-1477.
20. Kumar S, Mishra A, Pandey AK (2013): Antioxidant mediated protective effect of Parthenium hysterophorus against oxidative damage using in vitro models. BMC Complement Altern Med, 13, 120.
21. Kumar S, Pandey AK (2013): Phenolic content, reducing power and membrane protective activities of Solanum xanthocarpum root extracts. Vegetos, 26, 301-307.
22. Lee S, Kim YJ, Kwon S (2009): Inhibitory effects of flavonoids on TNF-α-induced IL-8 gene expression in HEK 293 cells. BMB reports, 42, 265-270.
23. Lim H, Jin JH, Park H, et al. (2011): New synthetic antiinflammatory chrysin analog, 5,7-dihydroxy-8-(pyridine- 4yl) flavone. Eur J Pharmacol, 670, 617-622.
24. Liu JY, Yang X, Sun XD, et al. (2016): Suppressive effects of copper sulfate accumulation on the spermatogenesis of rats. Biol Trace Elem Res, 174, 356-361.
25. Lowry OH, Rosebrough NJ, Farr AL, et al. (1951): Protein measurement with the folin phenol reagent. J Biol Chem, 193, 265-275.
26. Matsuno T (1995): A new clerodane diterpenoid isolated from propolis. Z Naturforsch, 50C, 93-97.
27. Meek IL, van de Laar MAFJ, Vonkeman HE (2010): Non-steroidal anti-inflammatory drugs: an overview of cardiovascular risks. Pharmaceuticals (Basel), 3, 2146- 2162.
28. Mladenović JM, Paunović MG, Matić MM, et al. (2014): Copper-induced changes of lipid peroxidation and hematobiochemical parameters in rat blood: protective role of flavonoids. Arch Biol Sci Belgrade, 66, 1271-1279.
29. Mouithys-Mickalad AML, Zheng SX, Deby-Dupont GP, et al. (2000): In vitro study of the antioxidant properties of non steroidal anti-inflammatory drugs by chemiluminescence and electron spin resonance (ESR). Free Radic Res, 33, 607-621.
30. Ohkawa H, Ohishi N, Yagi K (1979): Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem, 95, 351-358.
31. Ozcelik D, Uzun H (2009): Copper intoxication; Antioxidant defenses and oxidative damage in rat brain. Biol Trace Elem Res, 127, 45-52.
32. Rana SVS (2008): Metals and apoptosis: Recent developments. J Trace Elem Med Bio, 22, 262-284.
33. Rice-Evans CA, Miller NJ, Bolwell PG, et al. (1995): The relative antioxidant activities of plant-derived polyphenolic flavonoids. Free Radic Res, 22, 375-383.
34. Ross MH, Reith EJ, Romrell LJ (1989): Histology: a text and atlas. 2nd ed. Williams and Wilkins: Baltimore.
35. Seven I, Gul Baykalir B, Tatli Seven P, et al. (2014): The ameliorative effects of propolis against cyclosporine A induced hepatotoxicity and nephrotoxicity in rats. Kafkas Univ Vet Fak, 20, 641-648.
36. Sun Y, Oberley LW, Li YA (1988): Simple method for clinical assay of superoxide dismutase. Clin Chem, 34, 497- 500.
37. Tapiero H, Townsend DM, Tew KD (2003): Trace elements in human physiology and pathology. Copper. Biomed Pharmacother, 57, 386-398.
38. Tatli Seven P (2008): The effects of dietary Turkish Propolis and vitamin C on performance, digestibility, egg production and egg quality in laying hens under different environmental temperatures. Asian-Aust J Anim Sci, 21, 1164-1170.
39. Tatli Seven P, Seven I, Yilmaz M, et al. (2008): The effects of Turkish Propolis on growth and carcass characteristics in broilers under heat stress. Anim Feed Sci Tech, 146, 137- 148.
40. Tatli Seven P, Yilmaz S, Seven I, et al. (2012): Effects of propolis in animals exposed oxidative stress (Chapter 13). In: Lushchak VI, editor. Oxidative stress-environmental induction and dietary antioxidants. Rijeka, Croatia: InTech; 2012. pp. 267-288.
41. Velioglu YS, Mazza G, Gao L, et al. (1998): Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. J Agric Food Chem, 46, 4113-4117.
42. Zhang SS, Noordin MM, Rahman SO (2000): Effects of copper overload on hepatic lipid peroxidation and antioxidant defense in rats. Vet Hum Toxicol, 42, 261-264.
43. Zu Y, Li C, Fu Y, et al. (2006): Simultaneous determination of catechin, rutin, quercetin kaempferol and isorhamnetin in the extract of sea buckthorn (Hippophae rhamnoides L.) leaves by RP-HPLC with DAD. J Pharma Biomed Anal, 41, 714-719.

The protective effects of propolis and flunixin meglumine on feed intake, antioxidant status and histological parameters in liver and kidney tissues against excess copper in rats

Year 2018, Volume: 65 Issue: 4, 395 - 406, 09.11.2018

Pınar Tatlı Seven Burcu Gül Baykalır Tuba Parlak Ak İsmail Seven Neşe Başak Mine Yaman

https://doi.org/10.1501/Vetfak_0000002873

Cited By: 7

Abstract

This experiment was conducted to determine the protective effects of flunixin meglumine and propolis on feed
intake, antioxidant status and histological parameters in kidney and liver tissues in rats exposed to excessive copper. In this study
individually housed thirty-six male Sprague-Dawley rats were used. Animals were randomly divided into six groups; control, copper
sulphate (500 mg/kg BW/day, gavage), flunixin meglumine (2.2 mg/kg BW/day, ip), propolis (100 mg/kg BW/day, gavage), copper
sulphate+flunixin meglumine (500 mg/kg BW/day of copper sulphate by gavage and 2.2 mg/kg BW/day of flunixin meglumine, ip)
and copper sulphate+propolis (500 mg/kg BW/day of copper sulphate and 100 mg/kg BW/day of propolis by gavage). The study
demonstrated that body weight change in the copper sulphate+propolis group significantly ameliorated in comparison with copper
group (P<0.01). Propolis and flunixin meglumine administration significantly decreased MDA levels in the kidney and liver tissues,
and serum TNF-α levels (P<0.001). Propolis supplementation to rats who were also treated with copper significantly increased the
superoxide dismutase, catalase and reduced glutathione activities (P<0.001). Flunixin meglumine and propolis treatments decreased
the copper-induced degenerative and necrotic changes with the apoptotic cells in the liver and kidney tissues. In conclusion, propolis
appeared to ameliorate the adverse effects on feed intake, liver and kidney tissues seeing in the copper treatment and, apparently caused
by the copper toxicity, by scavenging the free radicals and increasing activity of antioxidants.

Keywords

Antioxidant status, copper, flunixin meglumine, histological changes, propolis

References

1. Abu-Zinadah OA, Hussein HK, Elshal MF, et al. (2012): Effect of excess dietary copper on proliferation and differentiation of the proerythroblasts and erythrocytes in rats. Afr J Biotechnol, 11, 6187-6191.
2. Aebi H (1984): Catalase in vitro methods in enzymology. In: Willam BJ, editor. Methods in enzymology. New York, USA: Academic Press; 1984. pp. 121-126.
3. Ahn MR, Kumazawa S, Usui Y (2007): Antioxidant activity and constituents of propolis collected in various areas of China. Food Chem, 101, 1383-1392.
4. Apak R, Guclu K, Ozyurek M, et al. (2004): Novel total antioxidantcapacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. J Agric Food Chem, 52, 7970-7981.
5. Babaknejad N, Moshtaghie AA, Shahanipour K (2015): The toxicity of copper on serum parameters related to renal functions in male wistar rats. Zahedan J Res Med Sci, 15, 29-31.
6. Bino RJ, de Vos CHR, Lieberman M, et al. (2005): The light-hyperresponsive high pigment-2dg mutation of tomato: alterations in the fruit metabolome. New Phytol, 166, 427-438.
7. Chiou PWS, Chen KL, Yu Bi (1998): Effect of dietary organic arsenicals and cupric sulfate on copper toxicity, liver accumulation and residue in eggs and excreta of laying hens. Anim Feed Sci Tech, 73, 161-171.
8. Ciftci O, Tanyildizi S, Godekmerdan A (2010): Protective effect of curcumin on immune system and body weight gain on rats intoxicated with 2,3,7,8- Tetrachlorodibenzo-p-dioxin (TCDD). Immunopharmacol Immunotoxicol, 32, 99-104.
9. Cook NC, Samman S (1996). Flavonoids-chemistry, metabolism, cardioprotective effects, and dietary sources. J Nutr Biochem, 7, 66-76.
10. Ellman GL (1959): Tissue Sulfhydryl groups. Arch Biochem Biophys, 82, 70-77.
11. Ferenci P (2004): Pathophysiology and clinical features of wilson disease. Metab Brain Dis, 19, 229-239.
12. Fuentealba IC, Aburto EM (2003): Animal models of copper-associated liver disease. Comp Hepatol, 2, 5.
13. Gaetke LM, Chow CK (2003): Copper toxicity, oxidative stress and antioxidant nutrients. Toxicology, 189, 147-163.
14. Gul Baykalir B, Tatli Seven P, Gur S, et al. (2016): The effects of propolis on sperm quality, reproductive organs and testicular antioxidant status of male rats treated with Cyclosporine-A. Anim Reprod, Belo Horizonte, 13, 105- 111.
15. Halliwell B, Gutteridge JMC (2007): Oxygen is a toxic gas – an introduction to oxygen toxicity and reactive species. In: Halliwell B, Gutteridge JMC, editors. Free radicals in biology and medicine. New York, USA: Oxford University Press; 2007. pp. 1-29.
16. Kabak YB, Gülbahar MY (2013): Sıçanlarda deneysel bakır zehirlenmesinde karaciğer ve böbrek dokularında apoptozisin belirlenmesi. Ankara Üniv Vet Fak, 60, 39-45.
17. Kim D, Jeong SW, Lee CY (2003): Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem, 81, 321-326.
18. Kodama H, Fujisawa C (2009): Copper metabolism and inherited copper transport disorders: molecular mechanisms, screening and treatment. Metallomics, 1, 42- 52.
19. Kornegay ET, van Heugten PHG, Lindemann MD, et al. (1989): Effects of biotin and high copper levels on performance and immune response of weanling pigs. J Anim Sci, 67, 1471-1477.
20. Kumar S, Mishra A, Pandey AK (2013): Antioxidant mediated protective effect of Parthenium hysterophorus against oxidative damage using in vitro models. BMC Complement Altern Med, 13, 120.
21. Kumar S, Pandey AK (2013): Phenolic content, reducing power and membrane protective activities of Solanum xanthocarpum root extracts. Vegetos, 26, 301-307.
22. Lee S, Kim YJ, Kwon S (2009): Inhibitory effects of flavonoids on TNF-α-induced IL-8 gene expression in HEK 293 cells. BMB reports, 42, 265-270.
23. Lim H, Jin JH, Park H, et al. (2011): New synthetic antiinflammatory chrysin analog, 5,7-dihydroxy-8-(pyridine- 4yl) flavone. Eur J Pharmacol, 670, 617-622.
24. Liu JY, Yang X, Sun XD, et al. (2016): Suppressive effects of copper sulfate accumulation on the spermatogenesis of rats. Biol Trace Elem Res, 174, 356-361.
25. Lowry OH, Rosebrough NJ, Farr AL, et al. (1951): Protein measurement with the folin phenol reagent. J Biol Chem, 193, 265-275.
26. Matsuno T (1995): A new clerodane diterpenoid isolated from propolis. Z Naturforsch, 50C, 93-97.
27. Meek IL, van de Laar MAFJ, Vonkeman HE (2010): Non-steroidal anti-inflammatory drugs: an overview of cardiovascular risks. Pharmaceuticals (Basel), 3, 2146- 2162.
28. Mladenović JM, Paunović MG, Matić MM, et al. (2014): Copper-induced changes of lipid peroxidation and hematobiochemical parameters in rat blood: protective role of flavonoids. Arch Biol Sci Belgrade, 66, 1271-1279.
29. Mouithys-Mickalad AML, Zheng SX, Deby-Dupont GP, et al. (2000): In vitro study of the antioxidant properties of non steroidal anti-inflammatory drugs by chemiluminescence and electron spin resonance (ESR). Free Radic Res, 33, 607-621.
30. Ohkawa H, Ohishi N, Yagi K (1979): Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem, 95, 351-358.
31. Ozcelik D, Uzun H (2009): Copper intoxication; Antioxidant defenses and oxidative damage in rat brain. Biol Trace Elem Res, 127, 45-52.
32. Rana SVS (2008): Metals and apoptosis: Recent developments. J Trace Elem Med Bio, 22, 262-284.
33. Rice-Evans CA, Miller NJ, Bolwell PG, et al. (1995): The relative antioxidant activities of plant-derived polyphenolic flavonoids. Free Radic Res, 22, 375-383.
34. Ross MH, Reith EJ, Romrell LJ (1989): Histology: a text and atlas. 2nd ed. Williams and Wilkins: Baltimore.
35. Seven I, Gul Baykalir B, Tatli Seven P, et al. (2014): The ameliorative effects of propolis against cyclosporine A induced hepatotoxicity and nephrotoxicity in rats. Kafkas Univ Vet Fak, 20, 641-648.
36. Sun Y, Oberley LW, Li YA (1988): Simple method for clinical assay of superoxide dismutase. Clin Chem, 34, 497- 500.
37. Tapiero H, Townsend DM, Tew KD (2003): Trace elements in human physiology and pathology. Copper. Biomed Pharmacother, 57, 386-398.
38. Tatli Seven P (2008): The effects of dietary Turkish Propolis and vitamin C on performance, digestibility, egg production and egg quality in laying hens under different environmental temperatures. Asian-Aust J Anim Sci, 21, 1164-1170.
39. Tatli Seven P, Seven I, Yilmaz M, et al. (2008): The effects of Turkish Propolis on growth and carcass characteristics in broilers under heat stress. Anim Feed Sci Tech, 146, 137- 148.
40. Tatli Seven P, Yilmaz S, Seven I, et al. (2012): Effects of propolis in animals exposed oxidative stress (Chapter 13). In: Lushchak VI, editor. Oxidative stress-environmental induction and dietary antioxidants. Rijeka, Croatia: InTech; 2012. pp. 267-288.
41. Velioglu YS, Mazza G, Gao L, et al. (1998): Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. J Agric Food Chem, 46, 4113-4117.
42. Zhang SS, Noordin MM, Rahman SO (2000): Effects of copper overload on hepatic lipid peroxidation and antioxidant defense in rats. Vet Hum Toxicol, 42, 261-264.
43. Zu Y, Li C, Fu Y, et al. (2006): Simultaneous determination of catechin, rutin, quercetin kaempferol and isorhamnetin in the extract of sea buckthorn (Hippophae rhamnoides L.) leaves by RP-HPLC with DAD. J Pharma Biomed Anal, 41, 714-719.

There are 43 citations in total.

Details

Primary Language	English
Subjects	Veterinary Surgery
Journal Section	Research Article
Authors	Pınar Tatlı Seven Burcu Gül Baykalır Tuba Parlak Ak İsmail Seven Neşe Başak Mine Yaman
Publication Date	November 9, 2018
Published in Issue	Year 2018Volume: 65 Issue: 4

Cite

APA	Tatlı Seven, P., Gül Baykalır, B., Parlak Ak, T., Seven, İ., et al. (2018). The protective effects of propolis and flunixin meglumine on feed intake, antioxidant status and histological parameters in liver and kidney tissues against excess copper in rats. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 65(4), 395-406. https://doi.org/10.1501/Vetfak_0000002873
AMA	Tatlı Seven P, Gül Baykalır B, Parlak Ak T, Seven İ, Başak N, Yaman M. The protective effects of propolis and flunixin meglumine on feed intake, antioxidant status and histological parameters in liver and kidney tissues against excess copper in rats. Ankara Univ Vet Fak Derg. November 2018;65(4):395-406. doi:10.1501/Vetfak_0000002873
Chicago	Tatlı Seven, Pınar, Burcu Gül Baykalır, Tuba Parlak Ak, İsmail Seven, Neşe Başak, and Mine Yaman. “The Protective Effects of Propolis and Flunixin Meglumine on Feed Intake, Antioxidant Status and Histological Parameters in Liver and Kidney Tissues Against Excess Copper in Rats”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 65, no. 4 (November 2018): 395-406. https://doi.org/10.1501/Vetfak_0000002873.
EndNote	Tatlı Seven P, Gül Baykalır B, Parlak Ak T, Seven İ, Başak N, Yaman M (November 1, 2018) The protective effects of propolis and flunixin meglumine on feed intake, antioxidant status and histological parameters in liver and kidney tissues against excess copper in rats. Ankara Üniversitesi Veteriner Fakültesi Dergisi 65 4 395–406.
IEEE	P. Tatlı Seven, B. Gül Baykalır, T. Parlak Ak, İ. Seven, N. Başak, and M. Yaman, “The protective effects of propolis and flunixin meglumine on feed intake, antioxidant status and histological parameters in liver and kidney tissues against excess copper in rats”, Ankara Univ Vet Fak Derg, vol. 65, no. 4, pp. 395–406, 2018, doi: 10.1501/Vetfak_0000002873.
ISNAD	Tatlı Seven, Pınar et al. “The Protective Effects of Propolis and Flunixin Meglumine on Feed Intake, Antioxidant Status and Histological Parameters in Liver and Kidney Tissues Against Excess Copper in Rats”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 65/4 (November 2018), 395-406. https://doi.org/10.1501/Vetfak_0000002873.
JAMA	Tatlı Seven P, Gül Baykalır B, Parlak Ak T, Seven İ, Başak N, Yaman M. The protective effects of propolis and flunixin meglumine on feed intake, antioxidant status and histological parameters in liver and kidney tissues against excess copper in rats. Ankara Univ Vet Fak Derg. 2018;65:395–406.
MLA	Tatlı Seven, Pınar et al. “The Protective Effects of Propolis and Flunixin Meglumine on Feed Intake, Antioxidant Status and Histological Parameters in Liver and Kidney Tissues Against Excess Copper in Rats”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 65, no. 4, 2018, pp. 395-06, doi:10.1501/Vetfak_0000002873.
Vancouver	Tatlı Seven P, Gül Baykalır B, Parlak Ak T, Seven İ, Başak N, Yaman M. The protective effects of propolis and flunixin meglumine on feed intake, antioxidant status and histological parameters in liver and kidney tissues against excess copper in rats. Ankara Univ Vet Fak Derg. 2018;65(4):395-406.