THE THERAPEUTIC AND NEUROPROTECTIVE EFFECTS OF GREEN TEA IN A RAT MODEL OF TERLIPRESSIN-INDUCED CHRONIC HYPONATREMIA
Keywords:
Green tea, Terlipressin, Hyponatremia, Hyponatremic encephalopathy, iNOS, RatAbstract
Objective: Hyponatremia (HN) is associated with mortality and morbidity risks due to the development of hyponatremic encephalopathy. Its rapid correction also carries a high risk of development of the serious cerebral disorder. This study investigated the possible therapeutic and neuroprotective effects of the green tea (GT) extract against HN and its complications in rats and compared those effects with the outcome of the rapid correction of chronic HN using hypertonic saline (HtNaCl).
Methods: Chronic HN was induced using terlipressin (TP; 0.2 mg/kg, s. c) and 2.5% d-glucose solution (equivalent to 5% initial bw/day, i. p) for 3 d. A stabilizing dose of TP (0.1 mg/kg) was used for the following 3 d, along with administration of either saline, GT (600 mg/kg/day, p. o), or HtNaCl (15 ml/kg/day, i. p). Serum sodium level, locomotor activity, pain reflex, and brain contents of iNOS and NO were assessed, together with a histopathological examination of brain tissues.
Results: TP-induced profound chronic HN that was corrected with administration of GT and HtNaCl. In a GT-treated group, correction of HN was coupled with improvement of TP-induced alteration of locomotor activity and brain histopathological picture. Elevation of brain iNOS and NO contents, along with detection of focal cellular necrosis and gliovascular proliferation changes in the HtNaCl-treated group indicated neuro pathological complications are accompanying the correction of HN with HtNaCl; a result that was not found in the GT-treated group.
Conclusion: Our findings revealed that GT corrected HN induced by TP in rats, and protected against the neuropathological features that characterized hyponatremic encephalopathy and accompanied with its rapid correction.
Keywords: Green tea, Terlipressin, Hyponatremia, Hyponatremic encephalopathy, iNOS, RatÂ
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Adrogue HJ, Madias NE. Hyponatremia. N Engl J Med 2000;342:1581-9.
Upadhyay A, Jaber BL, Madias NE. Incidence and prevalence of hyponatremia. Am J Med 2006;119:S30-5.
Verbalis JG, Goldsmith SR, Greenberg A, Schrier RW, Sterns RH. Hyponatremia treatment guidelines: expert panel recommendations. Am J Med 2007;120:S1-21.
Liamis G, Milionis H, Elisaf M. A review of drug-induced hyponatremia. Am J Kidney Dis 2008;52:144-53.
Gandelman MS. Review of carbamazepine-induced hyponatremia. Prog Neuropsychopharmacol Biol Psychiatry 1994;18:211-33.
Schrier RW, Bansal S. Diagnosis and management of hyponatremia in acute illness. Curr Opin Crit Care 2008;14:627-34.
Rosner MH, Kirven J. Exercise-associated hyponatremia. Clin J Am Soc Nephrol 2007;2:151-61.
Ghatol A, Kazory A. Ecstasy-associated acute severe hyponatremia and cerebral edema: a role for osmotic diuresis? J Emerg Med 2009;42:e137-40.
Sterns RH. Postoperative hyponatremia in menstruant women. Ann Intern Med 1993;118:984-5.
Moritz ML, Ayus JC. The pathophysiology and treatment of hyponatraemic encephalopathy: an update. Nephrol Dial Transplant 2003;18:2486-91.
Adrogue HJ, Madias NE. Hyponatremia. N Engl J Med 2000;342:1581-9.
Sjoblom E, Hojer J, Ludwigs U, Pirskanen R. Fatal hyponatraemic brain oedema due to common gastroenteritis with accidental water intoxication. Intensive Care Med 1997;23:348-50.
Sterns RH. Severe symptomatic hyponatremia: treatment and outcome. A study of 64 cases. Ann Intern Med 1987;107:656-64.
Kozniewska E, Podlecka A, Rafalowska J. Hyponatremic encephalopathy: some experimental and clinical findings. Folia Neuropathol 2003;41:41-5.
Sterns RH, Cappuccio JD, Silver SM, Cohen EP. Neurologic sequelae after treatment of severe hyponatremia: a multicenter perspective. J Am Soc Nephrol 1994;4:1522-30.
Lien YH. Role of organic osmolytes in myelinolysis. A topographic study in rats after rapid correction of hyponatremia. J Clin Invest 1995;95:1579-86.
Sterns RH, Silver SM. Brain volume regulation in response to hypo-osmolality and its correction. Am J Med 2006;119:S12-6.
Decaux G, Mols P, Cauchi P, Delwiche F. Use of urea for the treatment of water retention in hyponatraemic cirrhosis with ascites resistant to diuretics. Br Med J 1985;290:1782-3.
Verbalis JG. AVP receptor antagonists as aquaretics: review and assessment of clinical data. Cleve Clin J Med 2006;73 Suppl 3:S24-33.
Schrier RW. The sea within us: disorders of body water homeostasis. Curr Opin Invest Drugs 2007;8:304-11.
McKay DL, Blumberg JB. The role of tea in human health: an update. J Am Coll Nutr 2002;21:1-13.
Cabrera C, Artacho R, Gimenez R. Beneficial effects of green tea--a review. J Am Coll Nutr 2006;25:79-99.
Chacko SM, Thambi PT, Kuttan R, Nishigaki I. Beneficial effects of green tea: a literature review. Chin Med 2010;5:13.
Afzal M, Safer AM, Menon M. Green tea polyphenols and their potential role in health and disease. Inflammopharmacology 2015;23:151-61.
Fenton RA, Poulsen SB, de la Mora Chavez S, Soleimani M, Busslinger M, Dominguez Rieg JA, et al. Caffeine-induced diuresis and natriuresis is independent of renal tubular NHE3. Am J Physiol Renal Physiol 2015;308:F1409-20.
Ming Z, Lautt WW. Caffeine-induced natriuresis and diuresis via blockade of hepatic adenosine-mediated sensory nerves and a hepatorenal reflex. Can J Physiol Pharmacol 2010;88:1115-21.
Wu CD, Wei GX. Tea as a functional food for oral health. Nutrition 2002;18:443-4.
Zhang Y, Coca A, Casa DJ, Antonio J, Green JM, Bishop PA. Caffeine and diuresis during rest and exercise: a meta-analysis. J Sci Med Sport 2015;18:569-74.
Dona M, Dell'Aica I, Calabrese F, Benelli R, Morini M, Albini A, et al. Neutrophil restraint by green tea: inhibition of inflammation, associated angiogenesis, and pulmonary fibrosis. J Immunol 2003;170:4335-41.
Haqqi TM, Anthony DD, Gupta S, Ahmad N, Lee MS, Kumar GK, et al. Prevention of collagen-induced arthritis in mice by a polyphenolic fraction from green tea. Proc Natl Acad Sci USA 1999;96:4524-9.
Sudano Roccaro A, Blanco AR, Giuliano F, Rusciano D, Enea V. Epigallocatechin-gallate enhances the activity of tetracycline in staphylococci by inhibiting its efflux from bacterial cells. Antimicrob Agents Chemother 2004;48:1968-73.
Weber JM, Ruzindana-Umunyana A, Imbeault L, Sircar S. Inhibition of adenovirus infection and adenain by green tea catechins. Antiviral Res 2003;58:167-73.
Sartippour MR, Shao ZM, Heber D, Beatty P, Zhang L, Liu C, et al. Green tea inhibits vascular endothelial growth factor (VEGF) induction in human breast cancer cells. J Nutr 2002;132:2307-11.
Osada K, Takahashi M, Hoshina S, Nakamura M, Nakamura S, Sugano M. Tea catechins inhibit cholesterol oxidation accompanying oxidation of low-density lipoprotein in vitro. Comp Biochem Physiol Part C: Toxicol Pharmacol 2001; 128:153-64.
Salama A, Elsayeh B, Ismaiel I, El-Shenawy S. Comparative evaluation of protective effects of green tea and lycopene in potassium dichromate-induced acute renal failure in rats. J Chem Pharm Res 2014;6:168-77.
Weinreb O, Mandel S, Amit T, Youdim MB. Neurological mechanisms of green tea polyphenols in Alzheimer's and Parkinson's diseases. J Nutr Biochem 2004;15:506-16.
Assuncao M, Andrade JP. Protective action of green tea catechins in neuronal mitochondria during aging. Front Biosci 2015;20:247-62.
Raederstorff DG, Schlachter MF, Elste V, Weber P. Effect of EGCG on lipid absorption and plasma lipid levels in rats. J Nutr Biochem 2003;14:326-32.
Kapoor S. Green tea: beneficial effects on cholesterol and lipid metabolism besides endothelial function. Eur J Cardiovascular Prevention Rehabilitation 2008;15:497.
Ahmad RS, Butt MS, Sultan MT, Mushtaq Z, Ahmad S, Dewanjee S, et al. Preventive role of green tea catechins from obesity and related disorders especially hypercholesterolemia and hyperglycemia. J Transl Med 2015;13:79.
Bajerska J, Mildner-Szkudlarz S, Walkowiak J. Effects of rye bread enriched with green tea extract on weight maintenance and the characteristics of metabolic syndrome following weight loss: a pilot study. J Med Food 2015;18:698-705.
Kavanagh KT, Hafer LJ, Kim DW, Mann KK, Sherr DH, Rogers AE, et al. Green tea extracts decrease carcinogen-induced mammary tumor burden in rats and rate of breast cancer cell proliferation in culture. J Cell Biochem 2001;82:387-98.
Cerezo-Guisado MI, Zur R, Lorenzo MJ, Risco A, Martin-Serrano MA, Alvarez-Barrientos A, et al. Implication of Akt, ERK1/2 and alternative p38MAPK signaling pathways in human colon cancer cell apoptosis induced by green tea EGCG. Food Chem Toxicol 2015;84:125-32.
Sueoka N, Suganuma M, Sueoka E, Okabe S, Matsuyama S, Imai K, et al. A new function of green tea: prevention of lifestyle-related diseases. Ann N Y Acad Sci 2001;928:274-80.
Vinson JA. Black and green tea and heart disease: a review. Biofactors 2000;13:127-32.
Keske MA, Ng HL, Premilovac D, Rattigan S, Kim JA, Munir K, et al. Vascular and metabolic actions of the green tea polyphenol epigallocatechin gallate. Curr Med Chem 2015;22:59-69.
Osswald H, Schnermann J. Methylxanthines and the kidney. Handb Exp Pharmacol 2011:391-412.
Schnermann J, Osswald H, Hermle M. Inhibitory effect of methylxanthines on feedback control of glomerular filtration rate in the rat kidney. Pflügers Archiv 1977;369:39-48.
Hegazy R, Zaki H, Ismail I, Sharaf O, Kenawy S. Effects of strawberry leaves and celery seeds extracts in terlipressin-induced chronic hyponatremia in rats. Toxicol Lett 2011;205:95.
Kauppila T, Tanila H, Carlson S, Taira T. Effects of atipamezole, a novel alpha 2-adrenoceptor antagonist, in open-field, plus-maze, two compartment exploratory and forced swimming tests in the rat. Eur J Pharmacol 1991;205:177-82.
Kelly MA, Rubinstein M, Phillips TJ, Lessov CN, Burkhart-Kasch S, Zhang G, et al. Locomotor activity in D2 dopamine receptor-deficient mice is determined by gene dosage, genetic background, and developmental adaptations. J Neurosci 1998;18:3470-9.
Laviola G, Alleva E. Ontogeny of muscimol effects on locomotor activity, habituation, and pain reactivity in mice. Psychopharmacology 1990;102:41-8.
Jones M, Onslow M, Packman A, Gebski V. Guidelines for statistical analysis of the percentage of syllables stuttered data. J Speech Hear Res 2006;49:867-78.
Gowrishankar M, Chen CB, Cheema-Dhadli S, Steele A, Halperin ML. Hyponatremia in the rat in the absence of positive water balance. J Am Soc Nephrol 1997;8:524-9.
Leaf A, Bartter FC, Santos RF, Wrong O. Evidence in man that electrolyte urinary loss induced by pitressin is a function of water retention. J Clin Invest 1953;32:868-78.
Kleeman CR, Rubini ME, Lamdin E, Epstein FH. Studies on alcohol diuresis. II. The evaluation of ethyl alcohol as an inhibitor of the neurohypophysis. J Clin Invest 1955;34:448-55.
Forsling ML, Aziz LA, Miller M, Davies R, Donovan B. Conversion of tri glycyl vasopressin to lysine-vasopressin in man. J Endocrinol 1980;85:237-44.
Bernadich C, Bandi JC, Melin P, Bosch J. Effects of F-180, a new selective vasoconstrictor peptide, compared with terlipressin and vasopressin on systemic and splanchnic hemodynamics in a rat model of portal hypertension. Hepatology 1998;27:351-6.
Krag A, Bendtsen F, Pedersen EB, Holstein-Rathlou NH, Moller S. Effects of terlipressin on the aquaretic system: evidence of antidiuretic effects. Am J Physiol Renal Physiol 2008;295: F1295-300.
Soupart A, Penninckx R, Stenuit A, Perier O, Decaux G. Treatment of chronic hyponatremia in rats by intravenous saline: comparison of rate versus the magnitude of correction. Kidney Int 1992;41:1662-7.
Wada K, Matsukawa U, Fujimori A, Arai Y, Sudoh K, Sasamata M, et al. A novel vasopressin dual V1A/V2 receptor antagonist, conivaptan hydrochloride, improves hyponatremia in rats with the syndrome of inappropriate secretion of antidiuretic hormone (SIADH). Biol Pharm Bull 2007;30:91-5.
Delmas A, Leone M, Rousseau S, Albanese J, Martin C. Clinical review: vasopressin and terlipressin in septic shock patients. Crit Care 2005;9:212-22.
Coenraad MJ, Bolk JH, Frolich M, Meinders AE. Plasma arginine vasopressin and atrial natriuretic peptide concentration in patients with hyponatremia at diagnosis and the following treatment. Eur J Intern Med 2007;18:221-9.
Moritz ML, Ayus JC. New aspects in the pathogenesis, prevention, and treatment of hyponatremic encephalopathy in children. Pediatr Nephrol 2010;25:1225-38.
Szatalowicz VL, Miller PD, Lacher JW, Gordon JA, Schrier RW. Comparative effect of diuretics on renal water excretion in hyponatraemic oedematous disorders. Clin Sci 1982;62:235-8.
Goh KP. Management of hyponatremia. Am Fam Physician 2004;69:2387-94.
Michna L, Lu YP, Lou YR, Wagner GC, Conney AH. The stimulatory effect of oral administration of green tea and caffeine on locomotor activity in SKH-1 mice. Life Sci 2003;73:1383-92.
Eshghpour M, Mortazavi H, Mohammadzadeh Rezaei N, Nejat A. Effectiveness of green tea mouthwash in postoperative pain control following surgical removal of impacted third molars: double-blind, randomized clinical trial. Daru 2013;21:59.
Renno WM, Saleh F, Klepacek I, Al-Khaledi G, Ismael H, Asfar S. Green tea pain modulating effect in sciatic nerve chronic constriction injury rat model. Nutr Neurosci 2006;9:41-7.
Norenberg MD, Leslie KO, Robertson AS. Association between the rise in serum sodium and central pontine myelinolysis. Ann Neurol 1982;11:128-35.
Ke QH, Chen JH, Zheng SS, Yu J, Liang TB. Prevention of central pontine myelinolytic in rats by early treatment with dexamethasone. Zhejiang Daxue Xuebao Yixueban 2006;35:424-9.
Ke QH, Liang TB, Yu J, Zheng SS. A study of the pathogenesis and prevention of central pontine myelinolysis in a rat model. J Int Med Res 2006;34:264-71.
Takefuji S, Murase T, Sugimura Y, Takagishi Y, Hayasaka S, Oiso Y, et al. Role of microglia in the pathogenesis of osmotic-induced demyelination. Exp Neurol 2007;204:88-94.
Xie QW, Kashiwabara Y, Nathan C. Role of transcription factor NF-kappa B/Rel in the induction of nitric oxide synthase. J Biol Chem 1994;269:4705-8.
Nakagawa T, Yokozawa T. Direct scavenging of nitric oxide and superoxide by green tea. Food Chem Toxicol 2002;40:1745-50.
Srivastava RC, Husain MM, Hasan SK, Athar M. Green tea polyphenols and tannic acid act as potent inhibitors of phorbol ester-induced nitric oxide generation in rat hepatocytes independent of their antioxidant properties. Cancer Lett 2000;153:1-5.
Peristiowati Y, Indasah I, Ratnawati R. The effects of catechin isolated from green tea GMB-4 on NADPH and nitric oxide levels in endothelial cells exposed to high glucose. J Intercult Ethnopharmacol 2015;4:114-7.
Faria AM, Papadimitriou A, Silva KC, Lopes de Faria JM, Lopes de Faria JB. Uncoupling endothelial nitric oxide synthase is ameliorated by green tea in experimental diabetes by re-establishing tetrahydrobiopterin levels. Diabetes 2012;61: 1838-47.
Agnetti G, Bordoni A, Angeloni C, Leoncini E, Guarnieri C, Caldarera CM, et al. Green tea modulation of inducible nitric oxide synthase in hypoxic/reoxygenated cardiomyocytes. Biochimie 2005;87:457-60.
Chan MM, Fong D, Ho CT, Huang HI. Inhibition of inducible nitric oxide synthase gene expression and enzyme activity by epigallocatechin gallate, a natural product from green tea. Biochem Pharmacol 1997;54:1281-6.
Kim JS, Kim JM, O JJ, Jeon BS. Inhibition of inducible nitric oxide synthase expression and cell death by (-)-epigallocatechin-3-gallate, a green tea catechin, in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease. J Clin Neurosci 2010;17:1165-8.