Erythrocyte Antioxidants and Hexokinase Activity Alterations in CCl4-Induced Cirrhotic Rats Through Naltrexone Treatment
-
Fatemeh Sarhadi kholari
,
Mitra Nourbakhsh
,
Golsa Shekarkhar
,
Ahmad Reza Dehpour
,
Abolfazl Golestani
Abstract
Cirrhosis is the consequence of chronic liver injury Considering the crucial role of oxidative stress in the progression of liver cirrhosis, we aimed to investigate the ameliorative effect of NTX against oxidative stress in carbon tetrachloride (CCl4)-induced cirrhotic rats. Eighty-four male Wistar rats were randomly assigned into 4 groups (21 rats /group I) receiving CCl4; (II) NTX+CCl4; (III) mineral oil (M) (as the control); (IV) NTX+M. The animals in each group were sacrificed in 3 different time-points 2 weeks, 6 weeks (early cirrhosis) and 8 weeks (advanced cirrhosis). Liver function tests, NO metabolites, GSH level, as well as the activity of antioxidant enzymes including superoxide dismutase (SOD), catalase (CAT), glutathione peroxides (GPX), and hexokinase (HK) were assessed. NTX was able to ameliorate liver injury, revealed by attenuation of ALT activity, which was significantly enhanced due to cirrhosis induction, as well as pathological evaluation. HK was also increased significantly after treatment with CCl₄ while NTX moderated this increase. Although CCl4 treatment did not have a significant effect on GSH levels, NTX was able to considerably increase GSH in blood. The activity of CAT and SOD as well as NO levels were all augmented by NTX in CCl4-treated rats. Naltrexone demonstrates antioxidative effects in liver cirrhosis and may confer a protective effect against hepatic cirrhosis through modulation of oxidative stress.
1. Williams R. Global challenges in liver disease. Hepatology. 2006;44(3):521-6.
2. Li Y, Shi Y, Sun Y, Liu L, Bai X, Wang D, et al. Restorative effects of hydroxysafflor yellow A on hepatic function in an experimental regression model of hepatic fibrosis induced by carbon tetrachloride. Molecular medicine reports. 2017;15(1):47-56.
3. Hernandez–Gea V, Toffanin S, Friedman SL, Llovet JM. Role of the microenvironment in the pathogenesis and treatment of hepatocellular carcinoma. Gastroenterology. 2013;144(3):512-27.
4. Shiraha H, Yamamoto K, Namba M. Human hepatocyte carcinogenesis (Review). International journal of oncology. 2013;42(4):1133-8.
5. Marcellin P, Kutala BK. Liver diseases: A major, neglected global public health problem requiring urgent actions and large‐scale screening. Liver International. 2018;38:2-6.
6. Patel K, Gordon SC, Jacobson I, Hézode C, Oh E, Smith KM, et al. Evaluation of a panel of non-invasive serum markers to differentiate mild from moderate-to-advanced liver fibrosis in chronic hepatitis C patients. Journal of hepatology. 2004;41(6):935-42.
7. Marcellin P, Ziol M, Bedossa P, Douvin C, Poupon R, De Lédinghen V, et al. Non‐invasive assessment of liver fibrosis by stiffness measurement in patients with chronic hepatitis B. Liver International. 2009;29(2):242-7.
8. Geetha A, Lakshmi Priya M, Jeyachristy SA, Surendran R. Level of oxidative stress in the red blood cells of patients with liver cirrhosis. Indian Journal of Medical Research. 2007;126(3):204.
9. Rosa DPd, Bona S, Simonetto D, Zettler C, Marroni CA, Marroni NP. Melatonin protects the liver and erythrocytes against oxidative stress in cirrhotic rats. Arquivos de gastroenterologia. 2010;47(1):72-8.
10. Violi F, Leo R, Vezza E, Basili S, Cordova C, Balsano F. Bleeding time in patients with cirrhosis: relation with degree of liver failure and clotting abnormalities. Journal of hepatology. 1994;20(4):531-6.
11. Llessuy S. Introducción y especies activas de oxígeno in estresse oxidativo e antioxidantes. Canoas: ULBRA. 2002:21-31.
12. Ha BJ, Lee JY. The effect of chondroitin sulfate against CCl4-induced hepatotoxicity. Biological and Pharmaceutical Bulletin. 2003;26(5):622-6.
13. Lee JY, Lee SH, Kim HJ, Ha J-M, Lee S-H, Lee J-H, et al. The preventive inhibition of chondroitin sulfate against the CCI 4-lnduced oxidative stress of subcellular level. Archives of pharmacal research. 2004;27(3):340-5.
14. Geetha A, Priya ML, Jeyachristy SA, Surendran R. Level of oxidative stress in the red blood cells of patients with liver cirrhosis. Indian Journal of Medical Research. 2007;126(3):204.
15. Tien Y-C, Liao J-C, Chiu C-S, Huang T-H, Huang C-Y, Chang W-T, et al. Esculetin ameliorates carbon tetrachloride-mediated hepatic apoptosis in rats. International journal of molecular sciences. 2011;12(6):4053-67.
16. Korpi ER, Linden Am, Hytönen HR, Paasikoski N, Vashchinkina E, Dudek M, et al. Continuous delivery of naltrexone and nalmefene leads to tolerance in reducing alcohol drinking and to supersensitivity of brain opioid receptors. Addiction biology. 2017;22(4):1022-35.
17. Javadi-Paydar M, Ghiassy B, Ebadian S, Rahimi N, Norouzi A, Dehpour AR. Nitric oxide mediates the beneficial effect of chronic naltrexone on cholestasis-induced memory impairment in male rats. Behavioural pharmacology. 2013;24(3):195-206.
18. Kiani S, Ebrahimkhani MR, Shariftabrizi A, Doratotaj B, Payabvash S, Riazi K, et al. Opioid system blockade decreases collagenase activity and improves liver injury in a rat model of cholestasis. Journal of gastroenterology and hepatology. 2007;22(3):406-13.
19. De Minicis S, Candelaresi C, Marzioni M, Saccomano S, Roskams T, Casini A, et al. Role of endogenous opioids in modulating HSC activity in vitro and liver fibrosis in vivo. Gut. 2008;57(3):352-64.
20. Marzioni M, Alpini G, Saccomanno S, De Minicis S, Glaser S, Francis H, et al. Endogenous opioids modulate the growth of the biliary tree in the course of cholestasis. Gastroenterology. 2006;130(6):1831-47.
21. Payabvash S, Kiumehr S, Nezami BG, Zandieh A, Anvari P, Tavangar SM, et al. Endogenous opioids modulate hepatocyte apoptosis in a rat model of chronic cholestasis: the role of oxidative stress. Liver International. 2007;27(4):538-47.
22. Lin S-L, Lee Y-M, Chang H-Y, Cheng Y-W, Yen M-H. Effects of naltrexone on lipopolysaccharide-induced sepsis in rats. Journal of biomedical science. 2005;12(2):431-40.
23. Almansa I, Barcia JM, López-Pedrajas R, Muriach M, Miranda M, Romero FJ. Naltrexone reverses ethanol-induced rat hippocampal and serum oxidative damage. Oxidative medicine and cellular longevity. 2013;2013.
24. Kholari FS, Dehpour AR, Nourbakhsh M, Doustimotlagh AH, Bagherieh M, Golestani A. Erythrocytes membrane alterations reflecting liver damage in CCl₄-induced cirrhotic rats: the ameliorative effect of naltrexone. Acta Medica Iranica. 2016;54(10):631-9.
25. Ghasemi A, Hedayati M, Biabani H. Protein precipitation methods evaluated for determination of serum nitric oxide end products by the Griess assay. Journal of Medical Sciences Research. 2007;2(0):29-32.
26. Drabkin D, Austin J. Spectrophotometric studies: Spectrophotometric constants for common hemoglobin derivatives in human, dog and rabbit blood. J Biol Chem. 1932;98(719):33.
27. Brewer KL, Troendle MM, Pekman L, Meggs WJ. Naltrexone prevents delayed encephalopathy in rats poisoned with the sarin analogue diisopropylflurophosphate. The American journal of emergency medicine. 2013;31(4):676-9.
28. Thomas CP, Wallack SS, Lee S, McCarty D, Swift R. Research to practice: adoption of naltrexone in alcoholism treatment. Journal of Substance Abuse Treatment. 2003;24(1):1-11.
29. Li S, Tan H-Y, Wang N, Zhang Z-J, Lao L, Wong C-W, et al. The role of oxidative stress and antioxidants in liver diseases. International journal of molecular sciences. 2015;16(11):26087-124.
30. Wang C-C, Cheng P-Y, Peng Y-J, Wu ES, Wei H-P, Yen M-H. Naltrexone Protects Against Lipopolysaccharide/D-Galactosamine–Induced Hepatitis in Mice. Journal of pharmacological sciences. 2008;108(3):239-47.
31. de Andrade Belo MA, Soares VE, de Souza LM, da Rosa Sobreira MF, Cassol DMS, Toma SB. Hepatoprotective treatment attenuates oxidative damages induced by carbon tetrachloride in rats. Experimental and Toxicologic Pathology. 2012;64(3):155-65.
32. Shah V, Toruner M, Haddad F, Cadelina G, Papapetropoulos A, Choo K, et al. Impaired endothelial nitric oxide synthase activity associated with enhanced caveolin binding in experimental cirrhosis in the rat. Gastroenterology. 1999;117(5):1222-8.
33. Doustimotlagh AH, Dehpour AR, Golestani A. Involvement of nitrergic and opioidergic systems in the oxidative stress induced by BDL rats. Journal of Advances in Medicine and Medical Research. 2016:1-10.
34. El-Sherif AM, Abou-Shady MA, Al-Bahrawy AM, Bakr RM, Hosny A-MM. Nitric oxide levels in chronic liver disease patients with and without oesophageal varices. Hepatology international. 2008;2(3):341.
35. Wiest R, Groszmann RJ. The paradox of nitric oxide in cirrhosis and portal hypertension: too much, not enough. Hepatology. 2002;35(2):478-91.
36. Yang X, Greenhaw J, Shi Q, Roberts DW, Hinson JA, Muskhelishvili L, et al. Mouse liver protein sulfhydryl depletion after acetaminophen exposure. Journal of Pharmacology and Experimental Therapeutics. 2013;344(1):286-94.
37. Kennedy AB, Chen Q, Kirby JT, Dalrymple RA. Boussinesq modeling of wave transformation, breaking, and runup. I: 1D. Journal of waterway, port, coastal, and ocean engineering. 2000;126(1):39-47.
38. Ebrahimkhani MR, Kiani S, Oakley F, Kendall T, Shariftabrizi A, Tavangar SM, et al. Naltrexone, an opioid receptor antagonist, attenuates liver fibrosis in bile duct ligated rats. Gut. 2006;55(11):1606-16.
39. Magnani M, Serafini G, Stocchi V, Bossù M, Dachà M. Solubilization, purification, and properties of rabbit brain hexokinase. Archives of biochemistry and biophysics. 1982;216(2):449-54.
40. Szuster-Ciesielska A, Daniluk J, Kandefer-Szerszen M. Alcohol-related cirrhosis with pancreatitis. The role of oxidative stress in the progression of the disease. ARCHIVUM IMMUNOLOGIAE ET THERAPIAE EXPERIMENTALIS-ENGLISH EDITION-. 2001;49(2):139-46.
41. Federico A, Conti V, Russomanno G, Dallio M, Masarone M, Stiuso P, et al. A Long-term Treatment with Silybin in Patients with Non-alcoholic Steatohepatitis Stimulates Catalase Activity in Human Endothelial Cells. in vivo. 2017;31(4):609-18.
42. Goth L, Meszaros I, Nemeth H. Serum catalase enzyme activity in liver diseases. Acta Biologica Hungarica. 1987;38(2):287-90.
43. Glorieux C, Zamocky M, Sandoval JM, Verrax J, Calderon PB. Regulation of catalase expression in healthy and cancerous cells. Free Radical Biology and Medicine. 2015;87:84-97.
44. Salarian A, Kadkhodaee M, Zahmatkesh M, Seifi B, Bakhshi E, Akhondzadeh S, et al. Opioid Use Disorder Induces Oxidative Stress and Inflammation: The Attenuating Effect of Methadone Maintenance Treatment. Iranian journal of psychiatry. 2018;13(1):46.
45. Safarinejad MR, Asgari SA, Farshi A, Ghaedi G, Kolahi AA, Iravani S, et al. The effects of opiate consumption on serum reproductive hormone levels, sperm parameters, seminal plasma antioxidant capacity and sperm DNA integrity. Reproductive Toxicology. 2013;36:18-23.
46. Borges JP, Verdoorn KS, Daliry A, Powers SK, Ortenzi VH, Fortunato RS, et al. Delta opioid receptors: the link between exercise and cardioprotection. PLoS One. 2014;9(11):e113541.
47. Liu D-w, Chen Z-w, Xu H-z. Effects of leucine-enkephalin on catalase activity and hydrogen peroxide levels in the haemolymph of the Pacific Oyster (Crassostrea gigas). Molecules. 2008;13(4):864-70.
48. Chen Y-L, Chen L-J, Bair M-J, Yao M-L, Peng H-C, Yang S-S, et al. Antioxidative status of patients with alcoholic liver disease in southeastern Taiwan. World Journal of Gastroenterology. 2011;17(8):1063-70.
49. Guemouri L, Lecomte E, Herbeth B, Pirollet P, Paille F, Siest G, et al. Blood activities of antioxidant enzymes in alcoholics before and after withdrawal. Journal of studies on alcohol. 1993;54(5):626-9.
50. Ozenirler S, Tuncer C, Ongun O, Altan N, Kandilci U. Activities of superoxide dismutase in erythrocyte of nonalcoholic chronic liver diseases. General pharmacology. 1994;25(7):1349-51.
51. Togashi H, Shinzawa H, Wakabayashi H, Nakamura T, Yamada N, Takahashi T, et al. Activities of free oxygen radical scavenger enzymes in human liver. Journal of hepatology. 1990;11(2):200-5.
52. Clemente C, Elba S, Buongiorno G, Guerra V, D'attoma B, Orlando A, et al. Manganese superoxide dismutase activity and incidence of hepatocellular carcinoma in patients with Child–Pugh class A liver cirrhosis: a 7‐year follow‐up study. Liver International. 2007;27(6):791-7.
53. Koruk M, Aksoy H, Akçay F, Onuk MD. Antioxidant capacity and nitric oxide in patients with hepatic cirrhosis. Annals of Clinical & Laboratory Science. 2002;32(3):252-6.
54. Hadi MY, Kacmaz M, Serda HO, Durak I. Antioxidant status of erythrocytes from patients with cirrhosis. Hepato-gastroenterology. 1999;46(28):2460-3.
2. Li Y, Shi Y, Sun Y, Liu L, Bai X, Wang D, et al. Restorative effects of hydroxysafflor yellow A on hepatic function in an experimental regression model of hepatic fibrosis induced by carbon tetrachloride. Molecular medicine reports. 2017;15(1):47-56.
3. Hernandez–Gea V, Toffanin S, Friedman SL, Llovet JM. Role of the microenvironment in the pathogenesis and treatment of hepatocellular carcinoma. Gastroenterology. 2013;144(3):512-27.
4. Shiraha H, Yamamoto K, Namba M. Human hepatocyte carcinogenesis (Review). International journal of oncology. 2013;42(4):1133-8.
5. Marcellin P, Kutala BK. Liver diseases: A major, neglected global public health problem requiring urgent actions and large‐scale screening. Liver International. 2018;38:2-6.
6. Patel K, Gordon SC, Jacobson I, Hézode C, Oh E, Smith KM, et al. Evaluation of a panel of non-invasive serum markers to differentiate mild from moderate-to-advanced liver fibrosis in chronic hepatitis C patients. Journal of hepatology. 2004;41(6):935-42.
7. Marcellin P, Ziol M, Bedossa P, Douvin C, Poupon R, De Lédinghen V, et al. Non‐invasive assessment of liver fibrosis by stiffness measurement in patients with chronic hepatitis B. Liver International. 2009;29(2):242-7.
8. Geetha A, Lakshmi Priya M, Jeyachristy SA, Surendran R. Level of oxidative stress in the red blood cells of patients with liver cirrhosis. Indian Journal of Medical Research. 2007;126(3):204.
9. Rosa DPd, Bona S, Simonetto D, Zettler C, Marroni CA, Marroni NP. Melatonin protects the liver and erythrocytes against oxidative stress in cirrhotic rats. Arquivos de gastroenterologia. 2010;47(1):72-8.
10. Violi F, Leo R, Vezza E, Basili S, Cordova C, Balsano F. Bleeding time in patients with cirrhosis: relation with degree of liver failure and clotting abnormalities. Journal of hepatology. 1994;20(4):531-6.
11. Llessuy S. Introducción y especies activas de oxígeno in estresse oxidativo e antioxidantes. Canoas: ULBRA. 2002:21-31.
12. Ha BJ, Lee JY. The effect of chondroitin sulfate against CCl4-induced hepatotoxicity. Biological and Pharmaceutical Bulletin. 2003;26(5):622-6.
13. Lee JY, Lee SH, Kim HJ, Ha J-M, Lee S-H, Lee J-H, et al. The preventive inhibition of chondroitin sulfate against the CCI 4-lnduced oxidative stress of subcellular level. Archives of pharmacal research. 2004;27(3):340-5.
14. Geetha A, Priya ML, Jeyachristy SA, Surendran R. Level of oxidative stress in the red blood cells of patients with liver cirrhosis. Indian Journal of Medical Research. 2007;126(3):204.
15. Tien Y-C, Liao J-C, Chiu C-S, Huang T-H, Huang C-Y, Chang W-T, et al. Esculetin ameliorates carbon tetrachloride-mediated hepatic apoptosis in rats. International journal of molecular sciences. 2011;12(6):4053-67.
16. Korpi ER, Linden Am, Hytönen HR, Paasikoski N, Vashchinkina E, Dudek M, et al. Continuous delivery of naltrexone and nalmefene leads to tolerance in reducing alcohol drinking and to supersensitivity of brain opioid receptors. Addiction biology. 2017;22(4):1022-35.
17. Javadi-Paydar M, Ghiassy B, Ebadian S, Rahimi N, Norouzi A, Dehpour AR. Nitric oxide mediates the beneficial effect of chronic naltrexone on cholestasis-induced memory impairment in male rats. Behavioural pharmacology. 2013;24(3):195-206.
18. Kiani S, Ebrahimkhani MR, Shariftabrizi A, Doratotaj B, Payabvash S, Riazi K, et al. Opioid system blockade decreases collagenase activity and improves liver injury in a rat model of cholestasis. Journal of gastroenterology and hepatology. 2007;22(3):406-13.
19. De Minicis S, Candelaresi C, Marzioni M, Saccomano S, Roskams T, Casini A, et al. Role of endogenous opioids in modulating HSC activity in vitro and liver fibrosis in vivo. Gut. 2008;57(3):352-64.
20. Marzioni M, Alpini G, Saccomanno S, De Minicis S, Glaser S, Francis H, et al. Endogenous opioids modulate the growth of the biliary tree in the course of cholestasis. Gastroenterology. 2006;130(6):1831-47.
21. Payabvash S, Kiumehr S, Nezami BG, Zandieh A, Anvari P, Tavangar SM, et al. Endogenous opioids modulate hepatocyte apoptosis in a rat model of chronic cholestasis: the role of oxidative stress. Liver International. 2007;27(4):538-47.
22. Lin S-L, Lee Y-M, Chang H-Y, Cheng Y-W, Yen M-H. Effects of naltrexone on lipopolysaccharide-induced sepsis in rats. Journal of biomedical science. 2005;12(2):431-40.
23. Almansa I, Barcia JM, López-Pedrajas R, Muriach M, Miranda M, Romero FJ. Naltrexone reverses ethanol-induced rat hippocampal and serum oxidative damage. Oxidative medicine and cellular longevity. 2013;2013.
24. Kholari FS, Dehpour AR, Nourbakhsh M, Doustimotlagh AH, Bagherieh M, Golestani A. Erythrocytes membrane alterations reflecting liver damage in CCl₄-induced cirrhotic rats: the ameliorative effect of naltrexone. Acta Medica Iranica. 2016;54(10):631-9.
25. Ghasemi A, Hedayati M, Biabani H. Protein precipitation methods evaluated for determination of serum nitric oxide end products by the Griess assay. Journal of Medical Sciences Research. 2007;2(0):29-32.
26. Drabkin D, Austin J. Spectrophotometric studies: Spectrophotometric constants for common hemoglobin derivatives in human, dog and rabbit blood. J Biol Chem. 1932;98(719):33.
27. Brewer KL, Troendle MM, Pekman L, Meggs WJ. Naltrexone prevents delayed encephalopathy in rats poisoned with the sarin analogue diisopropylflurophosphate. The American journal of emergency medicine. 2013;31(4):676-9.
28. Thomas CP, Wallack SS, Lee S, McCarty D, Swift R. Research to practice: adoption of naltrexone in alcoholism treatment. Journal of Substance Abuse Treatment. 2003;24(1):1-11.
29. Li S, Tan H-Y, Wang N, Zhang Z-J, Lao L, Wong C-W, et al. The role of oxidative stress and antioxidants in liver diseases. International journal of molecular sciences. 2015;16(11):26087-124.
30. Wang C-C, Cheng P-Y, Peng Y-J, Wu ES, Wei H-P, Yen M-H. Naltrexone Protects Against Lipopolysaccharide/D-Galactosamine–Induced Hepatitis in Mice. Journal of pharmacological sciences. 2008;108(3):239-47.
31. de Andrade Belo MA, Soares VE, de Souza LM, da Rosa Sobreira MF, Cassol DMS, Toma SB. Hepatoprotective treatment attenuates oxidative damages induced by carbon tetrachloride in rats. Experimental and Toxicologic Pathology. 2012;64(3):155-65.
32. Shah V, Toruner M, Haddad F, Cadelina G, Papapetropoulos A, Choo K, et al. Impaired endothelial nitric oxide synthase activity associated with enhanced caveolin binding in experimental cirrhosis in the rat. Gastroenterology. 1999;117(5):1222-8.
33. Doustimotlagh AH, Dehpour AR, Golestani A. Involvement of nitrergic and opioidergic systems in the oxidative stress induced by BDL rats. Journal of Advances in Medicine and Medical Research. 2016:1-10.
34. El-Sherif AM, Abou-Shady MA, Al-Bahrawy AM, Bakr RM, Hosny A-MM. Nitric oxide levels in chronic liver disease patients with and without oesophageal varices. Hepatology international. 2008;2(3):341.
35. Wiest R, Groszmann RJ. The paradox of nitric oxide in cirrhosis and portal hypertension: too much, not enough. Hepatology. 2002;35(2):478-91.
36. Yang X, Greenhaw J, Shi Q, Roberts DW, Hinson JA, Muskhelishvili L, et al. Mouse liver protein sulfhydryl depletion after acetaminophen exposure. Journal of Pharmacology and Experimental Therapeutics. 2013;344(1):286-94.
37. Kennedy AB, Chen Q, Kirby JT, Dalrymple RA. Boussinesq modeling of wave transformation, breaking, and runup. I: 1D. Journal of waterway, port, coastal, and ocean engineering. 2000;126(1):39-47.
38. Ebrahimkhani MR, Kiani S, Oakley F, Kendall T, Shariftabrizi A, Tavangar SM, et al. Naltrexone, an opioid receptor antagonist, attenuates liver fibrosis in bile duct ligated rats. Gut. 2006;55(11):1606-16.
39. Magnani M, Serafini G, Stocchi V, Bossù M, Dachà M. Solubilization, purification, and properties of rabbit brain hexokinase. Archives of biochemistry and biophysics. 1982;216(2):449-54.
40. Szuster-Ciesielska A, Daniluk J, Kandefer-Szerszen M. Alcohol-related cirrhosis with pancreatitis. The role of oxidative stress in the progression of the disease. ARCHIVUM IMMUNOLOGIAE ET THERAPIAE EXPERIMENTALIS-ENGLISH EDITION-. 2001;49(2):139-46.
41. Federico A, Conti V, Russomanno G, Dallio M, Masarone M, Stiuso P, et al. A Long-term Treatment with Silybin in Patients with Non-alcoholic Steatohepatitis Stimulates Catalase Activity in Human Endothelial Cells. in vivo. 2017;31(4):609-18.
42. Goth L, Meszaros I, Nemeth H. Serum catalase enzyme activity in liver diseases. Acta Biologica Hungarica. 1987;38(2):287-90.
43. Glorieux C, Zamocky M, Sandoval JM, Verrax J, Calderon PB. Regulation of catalase expression in healthy and cancerous cells. Free Radical Biology and Medicine. 2015;87:84-97.
44. Salarian A, Kadkhodaee M, Zahmatkesh M, Seifi B, Bakhshi E, Akhondzadeh S, et al. Opioid Use Disorder Induces Oxidative Stress and Inflammation: The Attenuating Effect of Methadone Maintenance Treatment. Iranian journal of psychiatry. 2018;13(1):46.
45. Safarinejad MR, Asgari SA, Farshi A, Ghaedi G, Kolahi AA, Iravani S, et al. The effects of opiate consumption on serum reproductive hormone levels, sperm parameters, seminal plasma antioxidant capacity and sperm DNA integrity. Reproductive Toxicology. 2013;36:18-23.
46. Borges JP, Verdoorn KS, Daliry A, Powers SK, Ortenzi VH, Fortunato RS, et al. Delta opioid receptors: the link between exercise and cardioprotection. PLoS One. 2014;9(11):e113541.
47. Liu D-w, Chen Z-w, Xu H-z. Effects of leucine-enkephalin on catalase activity and hydrogen peroxide levels in the haemolymph of the Pacific Oyster (Crassostrea gigas). Molecules. 2008;13(4):864-70.
48. Chen Y-L, Chen L-J, Bair M-J, Yao M-L, Peng H-C, Yang S-S, et al. Antioxidative status of patients with alcoholic liver disease in southeastern Taiwan. World Journal of Gastroenterology. 2011;17(8):1063-70.
49. Guemouri L, Lecomte E, Herbeth B, Pirollet P, Paille F, Siest G, et al. Blood activities of antioxidant enzymes in alcoholics before and after withdrawal. Journal of studies on alcohol. 1993;54(5):626-9.
50. Ozenirler S, Tuncer C, Ongun O, Altan N, Kandilci U. Activities of superoxide dismutase in erythrocyte of nonalcoholic chronic liver diseases. General pharmacology. 1994;25(7):1349-51.
51. Togashi H, Shinzawa H, Wakabayashi H, Nakamura T, Yamada N, Takahashi T, et al. Activities of free oxygen radical scavenger enzymes in human liver. Journal of hepatology. 1990;11(2):200-5.
52. Clemente C, Elba S, Buongiorno G, Guerra V, D'attoma B, Orlando A, et al. Manganese superoxide dismutase activity and incidence of hepatocellular carcinoma in patients with Child–Pugh class A liver cirrhosis: a 7‐year follow‐up study. Liver International. 2007;27(6):791-7.
53. Koruk M, Aksoy H, Akçay F, Onuk MD. Antioxidant capacity and nitric oxide in patients with hepatic cirrhosis. Annals of Clinical & Laboratory Science. 2002;32(3):252-6.
54. Hadi MY, Kacmaz M, Serda HO, Durak I. Antioxidant status of erythrocytes from patients with cirrhosis. Hepato-gastroenterology. 1999;46(28):2460-3.
| Files | ||
| Issue | Vol 61 No 11 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/acta.v61i11.16078 | |
| Keywords | ||
| Liver cirrhosis Naltrexone Antioxidant Oxidative stress Carbon tetrachloride | ||
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How to Cite
1.
Sarhadi kholari F, Nourbakhsh M, Shekarkhar G, Dehpour AR, Golestani A. Erythrocyte Antioxidants and Hexokinase Activity Alterations in CCl4-Induced Cirrhotic Rats Through Naltrexone Treatment. Acta Med Iran. 2024;61(11):667-676.
