Research Article
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Investigation of the neuroprotective effect of kefir in experimental spinal cord injury

Year 2023, , 9 - 19, 30.12.2022
https://doi.org/10.33988/auvfd.872947

Abstract

In this study, the antioxidant, anti-inflammatory, and neuroprotective effects of kefir were investigated in spinal cord injury that was experimentally created on rats with a compression trauma model. A total of 56 Wistar-Albino male rats were used in the study. Daily freshly prepared 18 ml/kg/day of kefir was given by oral gavage to animals 7 days before and during the trauma and during the trauma. Spinal cord injury was created according to the weight drop method. On the 1st and 7th days before euthanasia, intracardiac blood was collected for analysis, and then they were sacrificed. The damaged spinal cord segments were examined biochemically, immunohistochemically, and histopathologically. When compared to the sham groups, kefir had a positive effect in the preconditioning and treatment groups by decreasing spinal cord bleeding, edema, myelin sheath damage, liquefactive necrosis, neuronal necrosis, selectivity of canalis centralis, and gitter cell levels significantly. When compared to the sham groups, kefir was found to have a positive effect in the treatment groups by decreasing the neuron specific enolase (NSE), ionized calcium binding adapter molecule 1 (IBA-1), inducible nitric oxide synthase (INOS), cyclooxygenase 2 (COX-2) and myelin basic protein (MBP) levels significantly on the 1st and 7th days, and by increasing the glial fibrillary acidic protein (GFAP) level significantly. As a result, it was demonstrated that kefir had a protective and therapeutic effect on spinal cord injury. 

Supporting Institution

The Coordinatorship of Scientific Research Projects of Hatay Mustafa Kemal University

Project Number

18.M.021

Thanks

The authors would like to thank Assoc. Prof. Dr. Pınar PEKER AKALIN for their contribution in the evaluation phase of biochemistry parameters. X. National and I. International Veterinary Pathology Congress (online) is presented as an oral presentation (27-37 October 2020, Burdur-Türkiye).

References

  • Banji OJ, Banji D, Ch K (2014): Curcumin and hesperidin improve cognition by suppressing mitochondrial dysfunction and apoptosis induced by D-galactose in rat brain. Food Chem Toxicol, 74, 51-59.
  • Bathina S, Das UN (2015): Brain-derived neurotrophic factor and its clinical implications. Arch Med Sci, 11, 1164.
  • Binder DK, Scharfman HE (2004): Brain-derived neurotrophic factor. Growth Factors, 22, 123.
  • Delen E, Durmaz R, Oglakci A, et al (2015): Efficacy of kefir on the release of lysosomal proteases after expremintal spinal cord trauma. J Clin Anal Med, 6, 21-25.
  • Duitschaever C, Kemp N, Emmons D (1987): Pure culture formulation and procedure for the production of kefir. Milchwiss, 42, 80-82.
  • Eddleston M, Mucke L (1993): Molecular profile of reactive astrocytes—implications for their role in neurologic disease. Neurosci, 54, 15-36.
  • Eng LF, Ghirnikar RS (1994): GFAP and astrogliosis. Brain Pathol, 4, 229-237.
  • Erdem H, Oktay M, Yildirim U, et al (2013): Expression of AEG-1 and p53 and their clinicopathological significance in malignant lesions of renal cell carcinomas: a microarray study. Pol J Pathol, 64, 28-32.
  • Font-Nieves M, Sans-Fons MG, Gorina R, et al (2012): Induction of COX-2 enzyme and down-regulation of COX-1 expression by lipopolysaccharide (LPS) control prostaglandin E2 production in astrocytes. J Biol Chem, 287, 6454-6468.
  • Friques AG, Santos FD, Angeli DB, et al (2020): Bisphenol A contamination in infant rats: molecular, structural, and physiological cardiovascular changes and the protective role of kefir. J Nutr Biochem, 75, 108254.
  • Furukawa N, Matsuoka A, Yamanaka Y (1990): Effects of orally administered yogurt and kefir on tumor growth in mice. J Jpn Soc Nutr Food Sci, 43, 450-453.
  • Gale K, Kerasidis H, Wrathall JR (1985): Spinal cord contusion in the rat: behavioral analysis of functional neurologic impairment. Exp Neurol, 88, 123-134.
  • Gao J, Ding G, Li Q, et al (2019): Tibet kefir milk decreases fat deposition by regulating the gut microbiota and gene expression of Lpl and Angptl4 in high fat diet-fed rats. Food Res Int, 121, 278-287.
  • Gopez JJ, Yue H, Vasudevan R, et al (2005): Cyclooxygenase-2-specific inhibitor improves functional outcomes, provides neuroprotection, and reduces inflammation in a rat model of traumatic brain injury. Neurosurg, 56, 590-604.
  • Guo R, Overman M, Chatterjee D, et al (2014): Aberrant expression of p53, p21, cyclin D1, and Bcl2 and their clinicopathological correlation in ampullary adenocarcinoma. Hum Pathol, 45, 1015-1023.
  • Gurcan O, Gurcay AG, Kazanci A, et al (2017): Effect of asiatic acid on the treatment of spinal cord injury: An Experimental study in rats. Turk Neurosurg, 27, 259-264.
  • Guven M, Akman T, Yener AU, et al (2015): The neuroprotective effect of kefir on spinal cord ischemia/reperfusion injury in rats. J Korean Neurosurg Soc, 57, 335.
  • Hanci V, Kerimoğlu A, Koca K, et al (2010): The biochemical effectiveness of N-acetylcysteine in experimental spinal cord injury in rats. Turk J Trauma Emerg Surg, 16, 15-21.
  • Haque A, Ray SK, Cox A, et al (2016): Neuron specific enolase: a promising therapeutic target in acute spinal cord injury. Metab Brain Dis, 31, 487-495.
  • Hewett SJ, Bell SC, Hewett JA (2006): Contributions of cyclooxygenase-2 to neuroplasticity and neuropathology of the central nervous system. Pharmacol Ther, 112, 335-357.
  • Huang EJ, Reichardt LF (2001): Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci, 24, 677-736.
  • Imai Y, Kohsaka S (2002): Intracellular signaling in M‐CSF‐induced microglia activation: role of Iba1. Glia, 40, 164-174.
  • Jia Y, Lu T, Yao S, et al (2019): The effects of interferon-β on neuronal apoptosis and the expressions of BDNF and TrkB in rats with spinal cord injuries. Int J Clin Exp Med, 12,12693-12701.
  • Kato K (2012): Stem cells in human normal endometrium and endometrial cancer cells: characterization of side population cells. Kaohsiung J Med Sci, 28, 63-71.
  • Kavakli HS, Koca C, Alici O (2011): Antioxidant effects of curcumin in spinal cord injury in rats. Turk J Trauma Emerg Surg, 17, 14-18.
  • Kubo M, Odani T, Nakamura S, et al (1992): Pharmacological study on kefir--a fermented milk product in Caucasus. I. On antitumor activity (1). Yakugaku Zasshi, 112, 489-495.
  • Matsuu M, Shichijo K, Okaichi K, et al (2003): The protective effect of fermented milk kefir on radiation-induced apoptosis in colonic crypt cells of rats. J Radiat Res, 44, 111-115.
  • Miller AD, Westmoreland SV, Evangelous NR, et al (2012): Acute traumatic spinal cord injury induces glial activation in the cynomolgus macaque (Macaca fascicularis). J Med Primatol, 41, 202-209.
  • Mumford A (2007): An Investigation into the spatial organization of kefir grains. Microb Divers, 1-11.
  • Özsoy S (2016): The Protective Effect of Kefir on Carbon Tetrachloride-induced Histopathological Changes in the Livers of Rats. Kafkas Univ Vet Fak Derg, 22, 403-408.
  • Resnick DK, Graham SH, Dixon CE, et al (1998): Role of cyclooxygenase 2 in acute spinal cord injury. J Neurotrauma, 15, 1005-1013.
  • Rollason V, Flora Samer C, Daali Y, et al (2014): Prediction by pharmacogenetics of safety and efficacy of non-steroidal anti-inflammatory drugs: a review. Curr Drug Metab, 15, 326-343.
  • Serarslan Y, Yönden Z, Özgiray E, et al (2010): Protective effects of tadalafil on experimental spinal cord injury in rats. J Clin Neurosci, 17, 349-352.
  • Siebels á, Rohrmann K, Oberneder R, et al (2011): A clinical phase I/II trial with the monoclonal antibody cG250 (RENCAREX®) and interferon-alpha-2a in metastatic renal cell carcinoma patients. World J Urol, 29, 121-126.
  • Sirin Y, Keles H, Besalti O, et al (2012): Comparison of ATP-MgCl2 and methylprednisolone in experimentally induced spinal cord trauma. J Clin Anal Med, 3, 442-447.
  • St-Onge M-P, Farnworth ER, Jones PJ (2000): Consumption of fermented and nonfermented dairy products: effects on cholesterol concentrations and metabolism. Am J Clin Nutr, 71, 674-681.
  • Toklu HZ, Hakan T, Celik H, et al (2010): Neuroprotective effects of alpha-lipoic acid in experimental spinal cord injury in rats. J Spinal Cord Med, 33, 401-409.
  • Yu S, Yao S, Wen Y, et al (2016): Angiogenic microspheres promote neural regeneration and motor function recovery after spinal cord injury in rats. Sci Rep, 6, 1-13.
  • Zhang D, Ma G, Hou M, et al (2016): The neuroprotective effect of puerarin in acute spinal cord injury rats. Cell Physiol Biochem, 39, 1152-1164.
  • Zhang Z, Krebs CJ, Guth L (1997): Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp Neurol, 143, 141-152.
Year 2023, , 9 - 19, 30.12.2022
https://doi.org/10.33988/auvfd.872947

Abstract

Project Number

18.M.021

References

  • Banji OJ, Banji D, Ch K (2014): Curcumin and hesperidin improve cognition by suppressing mitochondrial dysfunction and apoptosis induced by D-galactose in rat brain. Food Chem Toxicol, 74, 51-59.
  • Bathina S, Das UN (2015): Brain-derived neurotrophic factor and its clinical implications. Arch Med Sci, 11, 1164.
  • Binder DK, Scharfman HE (2004): Brain-derived neurotrophic factor. Growth Factors, 22, 123.
  • Delen E, Durmaz R, Oglakci A, et al (2015): Efficacy of kefir on the release of lysosomal proteases after expremintal spinal cord trauma. J Clin Anal Med, 6, 21-25.
  • Duitschaever C, Kemp N, Emmons D (1987): Pure culture formulation and procedure for the production of kefir. Milchwiss, 42, 80-82.
  • Eddleston M, Mucke L (1993): Molecular profile of reactive astrocytes—implications for their role in neurologic disease. Neurosci, 54, 15-36.
  • Eng LF, Ghirnikar RS (1994): GFAP and astrogliosis. Brain Pathol, 4, 229-237.
  • Erdem H, Oktay M, Yildirim U, et al (2013): Expression of AEG-1 and p53 and their clinicopathological significance in malignant lesions of renal cell carcinomas: a microarray study. Pol J Pathol, 64, 28-32.
  • Font-Nieves M, Sans-Fons MG, Gorina R, et al (2012): Induction of COX-2 enzyme and down-regulation of COX-1 expression by lipopolysaccharide (LPS) control prostaglandin E2 production in astrocytes. J Biol Chem, 287, 6454-6468.
  • Friques AG, Santos FD, Angeli DB, et al (2020): Bisphenol A contamination in infant rats: molecular, structural, and physiological cardiovascular changes and the protective role of kefir. J Nutr Biochem, 75, 108254.
  • Furukawa N, Matsuoka A, Yamanaka Y (1990): Effects of orally administered yogurt and kefir on tumor growth in mice. J Jpn Soc Nutr Food Sci, 43, 450-453.
  • Gale K, Kerasidis H, Wrathall JR (1985): Spinal cord contusion in the rat: behavioral analysis of functional neurologic impairment. Exp Neurol, 88, 123-134.
  • Gao J, Ding G, Li Q, et al (2019): Tibet kefir milk decreases fat deposition by regulating the gut microbiota and gene expression of Lpl and Angptl4 in high fat diet-fed rats. Food Res Int, 121, 278-287.
  • Gopez JJ, Yue H, Vasudevan R, et al (2005): Cyclooxygenase-2-specific inhibitor improves functional outcomes, provides neuroprotection, and reduces inflammation in a rat model of traumatic brain injury. Neurosurg, 56, 590-604.
  • Guo R, Overman M, Chatterjee D, et al (2014): Aberrant expression of p53, p21, cyclin D1, and Bcl2 and their clinicopathological correlation in ampullary adenocarcinoma. Hum Pathol, 45, 1015-1023.
  • Gurcan O, Gurcay AG, Kazanci A, et al (2017): Effect of asiatic acid on the treatment of spinal cord injury: An Experimental study in rats. Turk Neurosurg, 27, 259-264.
  • Guven M, Akman T, Yener AU, et al (2015): The neuroprotective effect of kefir on spinal cord ischemia/reperfusion injury in rats. J Korean Neurosurg Soc, 57, 335.
  • Hanci V, Kerimoğlu A, Koca K, et al (2010): The biochemical effectiveness of N-acetylcysteine in experimental spinal cord injury in rats. Turk J Trauma Emerg Surg, 16, 15-21.
  • Haque A, Ray SK, Cox A, et al (2016): Neuron specific enolase: a promising therapeutic target in acute spinal cord injury. Metab Brain Dis, 31, 487-495.
  • Hewett SJ, Bell SC, Hewett JA (2006): Contributions of cyclooxygenase-2 to neuroplasticity and neuropathology of the central nervous system. Pharmacol Ther, 112, 335-357.
  • Huang EJ, Reichardt LF (2001): Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci, 24, 677-736.
  • Imai Y, Kohsaka S (2002): Intracellular signaling in M‐CSF‐induced microglia activation: role of Iba1. Glia, 40, 164-174.
  • Jia Y, Lu T, Yao S, et al (2019): The effects of interferon-β on neuronal apoptosis and the expressions of BDNF and TrkB in rats with spinal cord injuries. Int J Clin Exp Med, 12,12693-12701.
  • Kato K (2012): Stem cells in human normal endometrium and endometrial cancer cells: characterization of side population cells. Kaohsiung J Med Sci, 28, 63-71.
  • Kavakli HS, Koca C, Alici O (2011): Antioxidant effects of curcumin in spinal cord injury in rats. Turk J Trauma Emerg Surg, 17, 14-18.
  • Kubo M, Odani T, Nakamura S, et al (1992): Pharmacological study on kefir--a fermented milk product in Caucasus. I. On antitumor activity (1). Yakugaku Zasshi, 112, 489-495.
  • Matsuu M, Shichijo K, Okaichi K, et al (2003): The protective effect of fermented milk kefir on radiation-induced apoptosis in colonic crypt cells of rats. J Radiat Res, 44, 111-115.
  • Miller AD, Westmoreland SV, Evangelous NR, et al (2012): Acute traumatic spinal cord injury induces glial activation in the cynomolgus macaque (Macaca fascicularis). J Med Primatol, 41, 202-209.
  • Mumford A (2007): An Investigation into the spatial organization of kefir grains. Microb Divers, 1-11.
  • Özsoy S (2016): The Protective Effect of Kefir on Carbon Tetrachloride-induced Histopathological Changes in the Livers of Rats. Kafkas Univ Vet Fak Derg, 22, 403-408.
  • Resnick DK, Graham SH, Dixon CE, et al (1998): Role of cyclooxygenase 2 in acute spinal cord injury. J Neurotrauma, 15, 1005-1013.
  • Rollason V, Flora Samer C, Daali Y, et al (2014): Prediction by pharmacogenetics of safety and efficacy of non-steroidal anti-inflammatory drugs: a review. Curr Drug Metab, 15, 326-343.
  • Serarslan Y, Yönden Z, Özgiray E, et al (2010): Protective effects of tadalafil on experimental spinal cord injury in rats. J Clin Neurosci, 17, 349-352.
  • Siebels á, Rohrmann K, Oberneder R, et al (2011): A clinical phase I/II trial with the monoclonal antibody cG250 (RENCAREX®) and interferon-alpha-2a in metastatic renal cell carcinoma patients. World J Urol, 29, 121-126.
  • Sirin Y, Keles H, Besalti O, et al (2012): Comparison of ATP-MgCl2 and methylprednisolone in experimentally induced spinal cord trauma. J Clin Anal Med, 3, 442-447.
  • St-Onge M-P, Farnworth ER, Jones PJ (2000): Consumption of fermented and nonfermented dairy products: effects on cholesterol concentrations and metabolism. Am J Clin Nutr, 71, 674-681.
  • Toklu HZ, Hakan T, Celik H, et al (2010): Neuroprotective effects of alpha-lipoic acid in experimental spinal cord injury in rats. J Spinal Cord Med, 33, 401-409.
  • Yu S, Yao S, Wen Y, et al (2016): Angiogenic microspheres promote neural regeneration and motor function recovery after spinal cord injury in rats. Sci Rep, 6, 1-13.
  • Zhang D, Ma G, Hou M, et al (2016): The neuroprotective effect of puerarin in acute spinal cord injury rats. Cell Physiol Biochem, 39, 1152-1164.
  • Zhang Z, Krebs CJ, Guth L (1997): Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp Neurol, 143, 141-152.
There are 40 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section Research Article
Authors

Ziya Yurtal 0000-0001-6080-1860

Tuncer Kutlu 0000-0002-8771-1256

Muhammed Altuğ 0000-0003-3896-9944

Bülent Özsoy 0000-0003-0045-3790

Halil Alakuş 0000-0001-9265-2310

Şule Yurdagül Özsoy 0000-0002-0743-2063

Project Number 18.M.021
Publication Date December 30, 2022
Published in Issue Year 2023

Cite

APA Yurtal, Z., Kutlu, T., Altuğ, M., Özsoy, B., et al. (2022). Investigation of the neuroprotective effect of kefir in experimental spinal cord injury. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 70(1), 9-19. https://doi.org/10.33988/auvfd.872947
AMA Yurtal Z, Kutlu T, Altuğ M, Özsoy B, Alakuş H, Özsoy ŞY. Investigation of the neuroprotective effect of kefir in experimental spinal cord injury. Ankara Univ Vet Fak Derg. December 2022;70(1):9-19. doi:10.33988/auvfd.872947
Chicago Yurtal, Ziya, Tuncer Kutlu, Muhammed Altuğ, Bülent Özsoy, Halil Alakuş, and Şule Yurdagül Özsoy. “Investigation of the Neuroprotective Effect of Kefir in Experimental Spinal Cord Injury”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 70, no. 1 (December 2022): 9-19. https://doi.org/10.33988/auvfd.872947.
EndNote Yurtal Z, Kutlu T, Altuğ M, Özsoy B, Alakuş H, Özsoy ŞY (December 1, 2022) Investigation of the neuroprotective effect of kefir in experimental spinal cord injury. Ankara Üniversitesi Veteriner Fakültesi Dergisi 70 1 9–19.
IEEE Z. Yurtal, T. Kutlu, M. Altuğ, B. Özsoy, H. Alakuş, and Ş. Y. Özsoy, “Investigation of the neuroprotective effect of kefir in experimental spinal cord injury”, Ankara Univ Vet Fak Derg, vol. 70, no. 1, pp. 9–19, 2022, doi: 10.33988/auvfd.872947.
ISNAD Yurtal, Ziya et al. “Investigation of the Neuroprotective Effect of Kefir in Experimental Spinal Cord Injury”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 70/1 (December 2022), 9-19. https://doi.org/10.33988/auvfd.872947.
JAMA Yurtal Z, Kutlu T, Altuğ M, Özsoy B, Alakuş H, Özsoy ŞY. Investigation of the neuroprotective effect of kefir in experimental spinal cord injury. Ankara Univ Vet Fak Derg. 2022;70:9–19.
MLA Yurtal, Ziya et al. “Investigation of the Neuroprotective Effect of Kefir in Experimental Spinal Cord Injury”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 70, no. 1, 2022, pp. 9-19, doi:10.33988/auvfd.872947.
Vancouver Yurtal Z, Kutlu T, Altuğ M, Özsoy B, Alakuş H, Özsoy ŞY. Investigation of the neuroprotective effect of kefir in experimental spinal cord injury. Ankara Univ Vet Fak Derg. 2022;70(1):9-19.