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Ileal interposition reduces oxidative stress via oxidant-antioxidant enzymes in rats with metabolic syndrome

Year 2022, Volume: 47 Issue: 2, 820 - 827, 30.06.2022

Abstract

Purpose: This study aims to examine the effect of ileal transposition (IT) on plasma levels of the total antioxidant status (TAS), total oxidant status (TOS), Oxidative Stress Index (OSI), Superoxide dismutase (SOD), Nicotinamide adenine dinucleotide phosphate oxidase (NOX), Catalase (CAT), Reduced Glutathione (GSH) in both rats with Metabolic syndrome (MetS) and healthy controls.
Materials and Methods: In the MetS model, newborn male Wistar albino rats were given MSG (4 g/mg) on days 0, 2, 4, 6, 8, and 10. The control group was injected only saline. In the 5th month, sham and IT animals underwent selected surgery. 2 months after surgery TOS, TAS, OSI, SOD, NOX, CAT, and GSH levels were assessed in the plasma.
Results: IT procedure significantly increased SOD and CAT levels in MetS + IT group when compared to the MetS group (SOD; MetS 1.75 ± 0.04, MetS+IT 2.1 ± 0.15, CAT; MetS 32.02 ± 1.73, MetS+IT 41.64 ± 1.18,). As expected, while GSH levels was increased in MetS+IT rats compared to MetS rats, but the difference was not significant (MetS 243.31 ± 6.36, MetS+IT 269.76 ± 9.17). The NOX activity was significantly lower in MetS+IT group than MetS and MetS+S groups (MetS 610.35 ± 26.25, MetS+IT 348.86 ± 14.12).
Conclusion: These data revealed the healing effect of IT surgery against oxidative stress associated with MetS. The available data endorses IT surgery as an effective strategy to reduce oxidative damage in rats with MetS by modulating systemic oxidant and antioxidant responses.

References

  • 1. Lee L, Arrington Sanders R. Metabolic Syndrome. Pediatr Rev. 2012;33:459-66.
  • 2. Reaven GM. Role of insulin resistance in human disease. Diabetes 1988;37:1595–607.
  • 3. Roberts CK, Sindhu KK. Oxidative stress and metabolic syndrome. Life Sci. 2001;84:705–12.
  • 4. Colak E, Pap D. The role of oxıdatıve stress ın the development of obesıty and obesıty-related metabolıc dısorders. J Med Biochem. 2021;40:1–9.
  • 5. Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insülin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb and Vasc Biol. 2004;24:816–23.
  • 6. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114:1752–61.
  • 7. Poljsak B, Šuput D, Milisav I. Achieving the balance between ros and antioxidants: when to use the synthetic antioxidants. Oxid Med Cell Longev. 2013;2013:956792.
  • 8. Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, et al. Oxidative stress: harms and benefits for human health. Oxid Med Cell Longev. 2017;2017:8416763.
  • 9. Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J. 2012;5: 9–19.
  • 10. Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y, et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med. 2016;8:67.
  • 11. Busetto L, Dicker D, Azran C, Batterham RL, Farpour-Lambert N, et al. Practical recommendations of the obesity management task force of the european association for the study of obesity for the post-bariatric surgery medical management. Obes Facts. 2017;10:597-632.
  • 12. Sjöström L, Peltonen M, Jacobson P, Ahlin S, Andersson-Assarsson J, Anveden A, et al. Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA 2014;311:2297-304.
  • 13. Al Assal K, Prifti E, Belda E, Sala P, Clément K, Dao MC, et al. Gut microbiota profile of obese diabetic women submitted to Roux-en-Y gastric bypass and its association with food intake and postoperative diabetes remission. Nutrients. 2020;12:278.
  • 14. França BK, Alves MRM, Souto FMS, Tiziane L, Boaventura RF, Guimarães A, et al. Peroxidação lipídica e obesidade: métodos para aferição do estresse oxidativo em obesos. J Port Gastrenterol. 2013;20:199-206.
  • 15. Ferraz EM, Arruda PCL, Barcelar TS, Ferraz AAB, Albuquerque AC, Leão CS. Tratamento cirúrgico da obesidade mórbida. Rev Col Bras Cir. 2003;3:98-105.
  • 16. Santry HP, Gillen DL, Lauderdale DS. Trends in bariatric surgical procedures. JAMA. 2005;294:1909-17.
  • 17. Fejfer K, Buczko P, Niczyporuk M, Ładny JR, Hady HR, Kna´s M, et al. Oxidative modification of biomolecules in the nonstimulated and stimulated saliva of patients with morbid obesity treated with bariatric surgery. Biomed Res Int. 2017;2017:4923769.
  • 18. Lushchak VI. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact. 2014;224:164–75.
  • 19. Vona R, Gambardella L, Cittadini C, Straface E, Pietraforte D. Biomarkers of oxidative stress in metabolic syndrome and associated diseases. Oxid Med Cell Longev. 2019;5:8267234.
  • 20. Tunc-Ata M, Altintas F, Senol H, Nizamoglu E, Kucukatay V. Ileal interposition improves metabolic syndrome parameters in a rat model of metabolic syndrome induced by monosodium glutamate. Life Sci. 2021;1:118846.
  • 21. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37:277-85.
  • 22. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38:1103-11.
  • 23. Miranda RA, Agostinho AR, Trevenzoli IH, Barella LF, Franco CCS, Trombini AB, et al. Insulin oversecretion in MSG-obese rats is related to alterations in cholinergic muscarinic receptor subtypes in pancreatic islets. Cell Physiol Biochem. 2014;33:1075-86.
  • 24. Rosa DD, Grze´skowiak LM, Ferreira CLLF, Fonseca ACM, Reis SA, Dias MM, et al. Kefir reduces insulin resistance and inflammatory cytokine expression in an animal model of metabolic syndrome. Food Funct. 2016;7:3390–401.
  • 25. Gbore FA, Oluseyifunmi IW, Jinadu DT, Jimoh FJ, Omojuyigbe AE. Growth and reproductive performance of female mice administered varied concentrations of monosodium glutamate. Nigerian J Anim Sci. 2019;2:63-71.
  • 26. Bousova I, Matouskova P, Bartikova H. Szotáková B, Hanušová V, Tománková V, et al. Influence of diet supplementation with green tea extract on drug-metabolizing enzymes in a mouse model of monosodium glutamate-induced obesity. Eur J Nutr 2015;55:361-71.
  • 27. Brosnan JT, Drewnowski A, Friedman MI. Is there a relationship between dietary MSG and obesity in animals or humans? Amino Acids 2014;46:2075–87.
  • 28. Shen JZ, Ma LN, Han Y, Liu JX, Yang WQ, Chen L, et al. Pentamethylquercetin generates beneficial effects in monosodium glutamate-induced obese mice and C2C12 myotubes by activating AMP-activated protein kinase. Diabetologia 2012;55:1836–46.
  • 29. Fernández-Sánchez A, Madrigal-Santillán E, Bautista M, Esquivel-Soto J, Morales-Gonzalez A, Esquivel-Chirino C, et al. Inflammation, oxidative stress, and obesity. Int J Mol Sci. 2011;12:3117–32.
  • 30. Esposito K, Ciotola M, Schisano B, Misso L, Giannetti G, Cariello A, et al. Oxidative stress in the metabolic syndrome. J Endocrinol Invest. 2006;29:791–5.
  • 31. Araki S, Dobashi K, Yamamoto Y, Asayama K, Kusuhara K. Increased plasma isoprostane is associated with visceral fat, high molecular weight adiponectin, and metabolic complications in obese children. Eur J Pediatr. 2010;169:965–70.
  • 32. Matusik P, Prokopowicz Z, Norek B, Olszanecka-Glinianowicz M, Chudek J, Malecka-Tendera E. Oxidative/antioxidative status in obese and sport trained children: a comparative study. BioMed Res Int. 2015; 2015;315747.
  • 33 Mingrone G, Panunzi S, de Gaetano A, Guidone C, Laconelli A, Leccesi L, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med. 2012;366:1577–85.
  • 34. Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Aminian A, Brethauer SA, et al. Bariatric surgery versus intensive medical therapy for diabetes - 5-year outcomes. N Engl J Med. 2017;376:641–51.
  • 35. Illán-Gómez F, Gonzálvez-Ortega M, Orea-Soler I, Alcaraz-Tafalla MS, Aragón-Alonso A, Pascual-Díaz M, et al. Obesity and inflammation: Change in adiponectin, C-reactive protein, tumour necrosis factor-alpha and interleukin-6 after bariatric surgery. Obes Surg. 2012;22:950-5.
  • 36. Sledzinski T, Goyke E, Smolenski RT, Sledzinski Z, Swierczynski J. Decrease in serum protein carbonyl groups concentration and maintained hyperhomocysteinemia in patients undergoing bariatric surgery. Obesity Surg. 2009;19:321–6.
  • 37. Gletsu-Miller N, Hansen JM, Jones DP, Go YM, Torres WE, Ziegler TR, et al. Loss of total and visceral adipose tissue mass predicts decreases in oxidative stress after weight-loss surgery. Obesity. 2009;17:439–46.
  • 38. Olusi SO. Obesity is an independent risk factor for plasma lipid peroxidation and depletion of erythrocyte cytoprotectic enzymes in humans. Int J Obes Relat Metab Disord. 2002;26:1159–64.
  • 39. Ozata M, Mergen M, Oktenli C, Aydin A, Sanisoglu SY, Bolu E, et al. Increased oxidative stress and hypozincemia in male obesity. Clin Biochem. 2002;35:627–31.
  • 40. Karra E, Yousseif A, Batterham RL. Mechanisms facilitating weight loss and resolution of type 2 diabetes following bariatric surgery. Trends Endocrinol Metab. 2010;21:337–44.
  • 41. Campos SP, Torrinhas RS, Giannella-Neto D, Linetzky Waitzberg D. Relationship between gut hormones and glucose homeostasis after bariatric surgery. Diabetol Metab Syndr. 2014;6:87.

İleal interpozisyon, metabolik sendromlu sıçanlarda oksidan-antioksidan enzimler yoluyla oksidatif stresi azaltır

Year 2022, Volume: 47 Issue: 2, 820 - 827, 30.06.2022

Abstract

Amaç: Bu çalışmanın amacı ileal transpozisyonun (IT) hem metabolik sendrom (MetS) sıçanları hem de sağlıklı kontrollerdeki toplam antioksidan durum (TAS), toplam oksidan durum (TOS), Oksidatif Stres İndeksi (OSI), Süperoksit dismutaz (SOD), Nikotinamid adenin dinükleotid fosfat oksidaz (NOX), Katalaz (CAT), İndirgenmiş Glutatyon (GSH)’un plazma seviyeleri üzerindeki etkisini incelemektir.
Gereç ve Yöntem: MetS modeline göre, yeni doğan erkek Wistar albino sıçanlara 0, 2, 4, 6, 8 ve 10. günlerde monosodyum glutamat (MSG) (4 mg/g) verildi. Kontrol grubuna sadece salin enjekte edildi. 5. ayda sham ve IT hayvanlara seçilmiş cerrahi uygulandı. Ameliyattan 2 ay sonra plazmada TOS, TAS, OSI, SOD, NOX, CAT, GSH seviyeleri değerlendirildi.
Bulgular: IT prosedürü MetS + IT grubunda MetS grubuna kıyasla SOD ve CAT düzeylerini önemli ölçüde artırdı (SOD; MetS 1.75 ± 0.04, MetS+IT 2.1 ± 0.15, CAT; MetS 32.02 ± 1.73, MetS+IT 41.64 ± 1.18). Beklendiği gibi, MetS+IT sıçanlarda MetS sıçanlara göre GSH seviyeleri artarken, aradaki fark anlamlı değildi (MetS 243.31 ± 6.36, MetS+IT 269.76 ± 9.17). NOX aktivitesi MetS+IT grubunda MetS ve MetS+S gruplarına göre anlamlı derecede düşüktü (MetS 610.35 ± 26.25, MetS+IT 348.86 ± 14.12).
Sonuç: Bu veriler, IT cerrahisinin MetS ile ilişkili oksidatif strese karşı iyileştirici etkisini ortaya koydu. Mevcut veriler, sistemik oksidan ve antioksidan yanıtları modüle ederek MetS'li sıçanlarda oksidatif hasarı azaltmak için IT cerrahisini etkili bir strateji olarak desteklemektedir.

References

  • 1. Lee L, Arrington Sanders R. Metabolic Syndrome. Pediatr Rev. 2012;33:459-66.
  • 2. Reaven GM. Role of insulin resistance in human disease. Diabetes 1988;37:1595–607.
  • 3. Roberts CK, Sindhu KK. Oxidative stress and metabolic syndrome. Life Sci. 2001;84:705–12.
  • 4. Colak E, Pap D. The role of oxıdatıve stress ın the development of obesıty and obesıty-related metabolıc dısorders. J Med Biochem. 2021;40:1–9.
  • 5. Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insülin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb and Vasc Biol. 2004;24:816–23.
  • 6. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114:1752–61.
  • 7. Poljsak B, Šuput D, Milisav I. Achieving the balance between ros and antioxidants: when to use the synthetic antioxidants. Oxid Med Cell Longev. 2013;2013:956792.
  • 8. Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, et al. Oxidative stress: harms and benefits for human health. Oxid Med Cell Longev. 2017;2017:8416763.
  • 9. Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J. 2012;5: 9–19.
  • 10. Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y, et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med. 2016;8:67.
  • 11. Busetto L, Dicker D, Azran C, Batterham RL, Farpour-Lambert N, et al. Practical recommendations of the obesity management task force of the european association for the study of obesity for the post-bariatric surgery medical management. Obes Facts. 2017;10:597-632.
  • 12. Sjöström L, Peltonen M, Jacobson P, Ahlin S, Andersson-Assarsson J, Anveden A, et al. Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA 2014;311:2297-304.
  • 13. Al Assal K, Prifti E, Belda E, Sala P, Clément K, Dao MC, et al. Gut microbiota profile of obese diabetic women submitted to Roux-en-Y gastric bypass and its association with food intake and postoperative diabetes remission. Nutrients. 2020;12:278.
  • 14. França BK, Alves MRM, Souto FMS, Tiziane L, Boaventura RF, Guimarães A, et al. Peroxidação lipídica e obesidade: métodos para aferição do estresse oxidativo em obesos. J Port Gastrenterol. 2013;20:199-206.
  • 15. Ferraz EM, Arruda PCL, Barcelar TS, Ferraz AAB, Albuquerque AC, Leão CS. Tratamento cirúrgico da obesidade mórbida. Rev Col Bras Cir. 2003;3:98-105.
  • 16. Santry HP, Gillen DL, Lauderdale DS. Trends in bariatric surgical procedures. JAMA. 2005;294:1909-17.
  • 17. Fejfer K, Buczko P, Niczyporuk M, Ładny JR, Hady HR, Kna´s M, et al. Oxidative modification of biomolecules in the nonstimulated and stimulated saliva of patients with morbid obesity treated with bariatric surgery. Biomed Res Int. 2017;2017:4923769.
  • 18. Lushchak VI. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact. 2014;224:164–75.
  • 19. Vona R, Gambardella L, Cittadini C, Straface E, Pietraforte D. Biomarkers of oxidative stress in metabolic syndrome and associated diseases. Oxid Med Cell Longev. 2019;5:8267234.
  • 20. Tunc-Ata M, Altintas F, Senol H, Nizamoglu E, Kucukatay V. Ileal interposition improves metabolic syndrome parameters in a rat model of metabolic syndrome induced by monosodium glutamate. Life Sci. 2021;1:118846.
  • 21. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37:277-85.
  • 22. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38:1103-11.
  • 23. Miranda RA, Agostinho AR, Trevenzoli IH, Barella LF, Franco CCS, Trombini AB, et al. Insulin oversecretion in MSG-obese rats is related to alterations in cholinergic muscarinic receptor subtypes in pancreatic islets. Cell Physiol Biochem. 2014;33:1075-86.
  • 24. Rosa DD, Grze´skowiak LM, Ferreira CLLF, Fonseca ACM, Reis SA, Dias MM, et al. Kefir reduces insulin resistance and inflammatory cytokine expression in an animal model of metabolic syndrome. Food Funct. 2016;7:3390–401.
  • 25. Gbore FA, Oluseyifunmi IW, Jinadu DT, Jimoh FJ, Omojuyigbe AE. Growth and reproductive performance of female mice administered varied concentrations of monosodium glutamate. Nigerian J Anim Sci. 2019;2:63-71.
  • 26. Bousova I, Matouskova P, Bartikova H. Szotáková B, Hanušová V, Tománková V, et al. Influence of diet supplementation with green tea extract on drug-metabolizing enzymes in a mouse model of monosodium glutamate-induced obesity. Eur J Nutr 2015;55:361-71.
  • 27. Brosnan JT, Drewnowski A, Friedman MI. Is there a relationship between dietary MSG and obesity in animals or humans? Amino Acids 2014;46:2075–87.
  • 28. Shen JZ, Ma LN, Han Y, Liu JX, Yang WQ, Chen L, et al. Pentamethylquercetin generates beneficial effects in monosodium glutamate-induced obese mice and C2C12 myotubes by activating AMP-activated protein kinase. Diabetologia 2012;55:1836–46.
  • 29. Fernández-Sánchez A, Madrigal-Santillán E, Bautista M, Esquivel-Soto J, Morales-Gonzalez A, Esquivel-Chirino C, et al. Inflammation, oxidative stress, and obesity. Int J Mol Sci. 2011;12:3117–32.
  • 30. Esposito K, Ciotola M, Schisano B, Misso L, Giannetti G, Cariello A, et al. Oxidative stress in the metabolic syndrome. J Endocrinol Invest. 2006;29:791–5.
  • 31. Araki S, Dobashi K, Yamamoto Y, Asayama K, Kusuhara K. Increased plasma isoprostane is associated with visceral fat, high molecular weight adiponectin, and metabolic complications in obese children. Eur J Pediatr. 2010;169:965–70.
  • 32. Matusik P, Prokopowicz Z, Norek B, Olszanecka-Glinianowicz M, Chudek J, Malecka-Tendera E. Oxidative/antioxidative status in obese and sport trained children: a comparative study. BioMed Res Int. 2015; 2015;315747.
  • 33 Mingrone G, Panunzi S, de Gaetano A, Guidone C, Laconelli A, Leccesi L, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med. 2012;366:1577–85.
  • 34. Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Aminian A, Brethauer SA, et al. Bariatric surgery versus intensive medical therapy for diabetes - 5-year outcomes. N Engl J Med. 2017;376:641–51.
  • 35. Illán-Gómez F, Gonzálvez-Ortega M, Orea-Soler I, Alcaraz-Tafalla MS, Aragón-Alonso A, Pascual-Díaz M, et al. Obesity and inflammation: Change in adiponectin, C-reactive protein, tumour necrosis factor-alpha and interleukin-6 after bariatric surgery. Obes Surg. 2012;22:950-5.
  • 36. Sledzinski T, Goyke E, Smolenski RT, Sledzinski Z, Swierczynski J. Decrease in serum protein carbonyl groups concentration and maintained hyperhomocysteinemia in patients undergoing bariatric surgery. Obesity Surg. 2009;19:321–6.
  • 37. Gletsu-Miller N, Hansen JM, Jones DP, Go YM, Torres WE, Ziegler TR, et al. Loss of total and visceral adipose tissue mass predicts decreases in oxidative stress after weight-loss surgery. Obesity. 2009;17:439–46.
  • 38. Olusi SO. Obesity is an independent risk factor for plasma lipid peroxidation and depletion of erythrocyte cytoprotectic enzymes in humans. Int J Obes Relat Metab Disord. 2002;26:1159–64.
  • 39. Ozata M, Mergen M, Oktenli C, Aydin A, Sanisoglu SY, Bolu E, et al. Increased oxidative stress and hypozincemia in male obesity. Clin Biochem. 2002;35:627–31.
  • 40. Karra E, Yousseif A, Batterham RL. Mechanisms facilitating weight loss and resolution of type 2 diabetes following bariatric surgery. Trends Endocrinol Metab. 2010;21:337–44.
  • 41. Campos SP, Torrinhas RS, Giannella-Neto D, Linetzky Waitzberg D. Relationship between gut hormones and glucose homeostasis after bariatric surgery. Diabetol Metab Syndr. 2014;6:87.
There are 41 citations in total.

Details

Primary Language English
Subjects Clinical Sciences
Journal Section Research
Authors

Melek Tunç-ata 0000-0002-0384-2356

Ayşegül Çört 0000-0001-8946-7173

Barış Özgür Dönmez 0000-0003-1066-5981

İsmail Hakkı Akbudak 0000-0002-3716-9243

Vural Küçükatay 0000-0002-6850-6281

Publication Date June 30, 2022
Acceptance Date May 24, 2022
Published in Issue Year 2022 Volume: 47 Issue: 2

Cite

MLA Tunç-ata, Melek et al. “Ileal Interposition Reduces Oxidative Stress via Oxidant-Antioxidant Enzymes in Rats With Metabolic Syndrome”. Cukurova Medical Journal, vol. 47, no. 2, 2022, pp. 820-7.