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Published in: BMC Gastroenterology 1/2014

Open Access 01-12-2014 | Research article

NOX2-generated oxidative stress is associated with severity of ultrasound liver steatosis in patients with non-alcoholic fatty liver disease

Authors: Maria Del Ben, Licia Polimeni, Roberto Carnevale, Simona Bartimoccia, Cristina Nocella, Francesco Baratta, Lorenzo Loffredo, Pasquale Pignatelli, Francesco Violi, Francesco Angelico

Published in: BMC Gastroenterology | Issue 1/2014

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Abstract

Background

Chronic oxidative stress is one of the key mechanisms responsible for disease progression in non-alcoholic fatty liver disease. However, so far, few studies reported increased circulating levels of oxidative stress markers in patients with non-alcoholic fatty liver and no study has been performed with newer markers of systemic oxidative stress. The aim was to assess the relationship between urinary 8-iso-prostaglandin F2α and serum soluble NOX2-derived peptide and the severity of liver steatosis in subjects with non-alcoholic fatty liver.

Methods

The study was performed in 264 consecutive patients referred for suspected metabolic disease. Steatosis was defined according to Hamaguchi ultrasonographic criteria. Oxidative stress was assessed by urinary 8-iso- prostaglandin F2α and serum soluble NOX2-derived peptide levels.

Results

Patients with non-alcoholic fatty liver had higher (p < 0.001) mean values of urinary 8-iso-PGF2α and of serum soluble NOX2-derived peptide, alanine aminotransferase, Cytokeratin-18 and homeostasis model of insulin resistance and lower values of serum adiponectin as compared to those without. Prevalence of metabolic syndrome and of its clinical features was significantly higher in patients with non-alcoholic fatty liver. Same findings were also observed after the exclusion of obese subjects, or subjects with diabetes or with metabolic syndrome and in those not taking statin medication. In addition, the levels of urinary 8-iso-PGF2α were independent predictors of non-alcoholic fatty liver and a strong association of urinary 8-iso-PGF2α and of serum soluble NOX2-derived peptide with the severity of steatosis at ultrasound was also observed.

Conclusions

We demonstrated increased markers of oxidative stress in subjects with non-alcoholic fatty liver. Urinary 8-iso-PGF2α and serum soluble NOX2-derived peptide levels were independent from obesity, diabetes and metabolic syndrome and increased with the severity of liver steatosis at ultrasound.
Literature
1.
go back to reference Angulo P: Nonalcoholic fatty liver disease. N Engl J Med. 2002, 346: 1221-1231. 10.1056/NEJMra011775.CrossRefPubMed Angulo P: Nonalcoholic fatty liver disease. N Engl J Med. 2002, 346: 1221-1231. 10.1056/NEJMra011775.CrossRefPubMed
2.
go back to reference Bedogni G, Miglioli L, Masutti F, Tiribelli C, Marchesini G, Bellentani S: Prevalence of and risk factors for non-alcoholic fatty liver disease: the dionysos nutrition and liver study. Hepatology. 2005, 42: 44-52.CrossRefPubMed Bedogni G, Miglioli L, Masutti F, Tiribelli C, Marchesini G, Bellentani S: Prevalence of and risk factors for non-alcoholic fatty liver disease: the dionysos nutrition and liver study. Hepatology. 2005, 42: 44-52.CrossRefPubMed
3.
go back to reference Angelico F, Del Ben M, Conti R, Francioso S, Feole K, Maccioni D, Antonini TM, Alessandri C: Non alcoholic fatty liver disease: an hepatic consequence of common metabolic diseases. J Gastroenterol Hepatol. 2003, 18: 588-594. 10.1046/j.1440-1746.2003.02958.x.CrossRefPubMed Angelico F, Del Ben M, Conti R, Francioso S, Feole K, Maccioni D, Antonini TM, Alessandri C: Non alcoholic fatty liver disease: an hepatic consequence of common metabolic diseases. J Gastroenterol Hepatol. 2003, 18: 588-594. 10.1046/j.1440-1746.2003.02958.x.CrossRefPubMed
4.
go back to reference Kotronen A, Yki-Järvinen H: Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol. 2008, 28: 27-38.CrossRefPubMed Kotronen A, Yki-Järvinen H: Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol. 2008, 28: 27-38.CrossRefPubMed
5.
go back to reference Angelico F, Del Ben M, Conti R, Francioso S, Feole K, Fiorello S, Cavallo MG I, Zalunardo B, Lirussi F, Alessandri C, Violi F: Insulin resistance, the metabolic syndrome, and nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2005, 90: 1578-1582. 10.1210/jc.2004-1024.CrossRefPubMed Angelico F, Del Ben M, Conti R, Francioso S, Feole K, Fiorello S, Cavallo MG I, Zalunardo B, Lirussi F, Alessandri C, Violi F: Insulin resistance, the metabolic syndrome, and nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2005, 90: 1578-1582. 10.1210/jc.2004-1024.CrossRefPubMed
6.
go back to reference Targher G, Day CP, Bonora E: Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med. 2010, 363: 1341-1350. 10.1056/NEJMra0912063.CrossRefPubMed Targher G, Day CP, Bonora E: Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med. 2010, 363: 1341-1350. 10.1056/NEJMra0912063.CrossRefPubMed
7.
go back to reference Del Ben M, Baratta F, Polimeni L, Angelico F: Non-alcoholic fatty liver disease and cardiovascular disease: epidemiological, clinical and pathophysiological evidences. Intern Emerg Med. 2012, 7 (Suppl 3): S291-S296.CrossRefPubMed Del Ben M, Baratta F, Polimeni L, Angelico F: Non-alcoholic fatty liver disease and cardiovascular disease: epidemiological, clinical and pathophysiological evidences. Intern Emerg Med. 2012, 7 (Suppl 3): S291-S296.CrossRefPubMed
8.
go back to reference Videla LA, Rodrigo R, Araya J, Poniachik J: Insulin resistance and oxidative stress interdependency in non-alcoholic fatty liver disease. Trends Mol Med. 2006, 12: 555-558. 10.1016/j.molmed.2006.10.001.CrossRefPubMed Videla LA, Rodrigo R, Araya J, Poniachik J: Insulin resistance and oxidative stress interdependency in non-alcoholic fatty liver disease. Trends Mol Med. 2006, 12: 555-558. 10.1016/j.molmed.2006.10.001.CrossRefPubMed
9.
go back to reference Day CP: Pathogenesis of steatohepatitis. Best Pract Res Clin Gastroenterol. 2002, 16: 663-678. 10.1053/bega.2002.0333.CrossRefPubMed Day CP: Pathogenesis of steatohepatitis. Best Pract Res Clin Gastroenterol. 2002, 16: 663-678. 10.1053/bega.2002.0333.CrossRefPubMed
10.
go back to reference Tilg H, Moschen AR: Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology. 2010, 52: 1836-1846. 10.1002/hep.24001.CrossRefPubMed Tilg H, Moschen AR: Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology. 2010, 52: 1836-1846. 10.1002/hep.24001.CrossRefPubMed
11.
go back to reference Yilmaz Y: Review article: is non-alcoholic fatty liver disease a spectrum, or are steatosis and non-alcoholic steatohepatitis distinct conditions?. Aliment Pharmacol Ther. 2012, 36: 815-823.CrossRefPubMed Yilmaz Y: Review article: is non-alcoholic fatty liver disease a spectrum, or are steatosis and non-alcoholic steatohepatitis distinct conditions?. Aliment Pharmacol Ther. 2012, 36: 815-823.CrossRefPubMed
12.
go back to reference Sanyal AJ, Chalasani N, Kowdley KV, McCullough A, Diehl AM, Bass NM, Neuschwander-Tetri BA, Lavine JE, Tonascia J, Unalp A, Van Natta M, Clark J, Brunt EM, Kleiner DE, Hoofnagle JH, Robuck PR NASHCRN: Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. New Engl J Med. 2010, 362: 1675-1685. 10.1056/NEJMoa0907929.CrossRefPubMedPubMedCentral Sanyal AJ, Chalasani N, Kowdley KV, McCullough A, Diehl AM, Bass NM, Neuschwander-Tetri BA, Lavine JE, Tonascia J, Unalp A, Van Natta M, Clark J, Brunt EM, Kleiner DE, Hoofnagle JH, Robuck PR NASHCRN: Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. New Engl J Med. 2010, 362: 1675-1685. 10.1056/NEJMoa0907929.CrossRefPubMedPubMedCentral
13.
go back to reference Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Michael C, Arun Sanyal J: The diagnosis and management of non-alcoholic fatty liver disease: Practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012, 55: 2005-2023. 10.1002/hep.25762.CrossRefPubMed Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Michael C, Arun Sanyal J: The diagnosis and management of non-alcoholic fatty liver disease: Practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012, 55: 2005-2023. 10.1002/hep.25762.CrossRefPubMed
14.
go back to reference Chalasani N, Deeg MA, Crabb DW: Systemic levels of lipid peroxidation and its metabolic and dietary correlates in patients with nonalcoholic steatohepatitis. Am J Gastroenterol. 2004, 99: 1497-1502. 10.1111/j.1572-0241.2004.30159.x.CrossRefPubMed Chalasani N, Deeg MA, Crabb DW: Systemic levels of lipid peroxidation and its metabolic and dietary correlates in patients with nonalcoholic steatohepatitis. Am J Gastroenterol. 2004, 99: 1497-1502. 10.1111/j.1572-0241.2004.30159.x.CrossRefPubMed
15.
go back to reference Yesilova Z, Yaman H, Oktenli C, Ozcan A, Uygun A, Cakir E, Sanisoglu SY, Erdil A, Ates Y, Aslan M, Musabak U, Erbil MK, Karaeren N, Dagalp K: Systemic markers of lipid peroxidation and antioxidants in patients with nonalcoholic fatty liver disease. Am J Gastroenterol. 2005, 100: 850-855. 10.1111/j.1572-0241.2005.41500.x.CrossRefPubMed Yesilova Z, Yaman H, Oktenli C, Ozcan A, Uygun A, Cakir E, Sanisoglu SY, Erdil A, Ates Y, Aslan M, Musabak U, Erbil MK, Karaeren N, Dagalp K: Systemic markers of lipid peroxidation and antioxidants in patients with nonalcoholic fatty liver disease. Am J Gastroenterol. 2005, 100: 850-855. 10.1111/j.1572-0241.2005.41500.x.CrossRefPubMed
16.
go back to reference Narasimhan S, Gokulakrishnan K, Sampathkumar R, Farooq S, Ravikumar R, Mohan V, Balasubramanyam M: Oxidative stress is independently associated with non-alcoholic fatty liver disease (NAFLD) in subjects with and without type 2 diabetes. Clin Biochem. 2010, 43: 815-821. 10.1016/j.clinbiochem.2010.04.003.CrossRefPubMed Narasimhan S, Gokulakrishnan K, Sampathkumar R, Farooq S, Ravikumar R, Mohan V, Balasubramanyam M: Oxidative stress is independently associated with non-alcoholic fatty liver disease (NAFLD) in subjects with and without type 2 diabetes. Clin Biochem. 2010, 43: 815-821. 10.1016/j.clinbiochem.2010.04.003.CrossRefPubMed
17.
go back to reference Nobili V, Parola M, Alisi A, Marra F, Piemonte F, Mombello C, Sutti S, Povero D, Maina V, Novo E, Albano E: Oxidative stress parameters in paediatric non-alcoholic fatty liver disease. Intern J Molec Med. 2010, 26: 471-476.CrossRef Nobili V, Parola M, Alisi A, Marra F, Piemonte F, Mombello C, Sutti S, Povero D, Maina V, Novo E, Albano E: Oxidative stress parameters in paediatric non-alcoholic fatty liver disease. Intern J Molec Med. 2010, 26: 471-476.CrossRef
18.
go back to reference Irie M, Sohda T, Iwata K, Kunimoto H, Fukunaga A, Kuno S, Yotsumoto K, Sakurai K, Iwashita H, Hirano G, Ueda SI, Yokoyama K, Morihara D, Nishizawa S, Anan A, Takeyama Y, Sakamoto M, Shakado S, Sakisaka S: Levels of the oxidative stress marker g-glutamyltranspeptidase at different stages of nonalcoholic fatty liver disease. J Intern Med Res. 2012, 40: 924-933. 10.1177/147323001204000311.CrossRef Irie M, Sohda T, Iwata K, Kunimoto H, Fukunaga A, Kuno S, Yotsumoto K, Sakurai K, Iwashita H, Hirano G, Ueda SI, Yokoyama K, Morihara D, Nishizawa S, Anan A, Takeyama Y, Sakamoto M, Shakado S, Sakisaka S: Levels of the oxidative stress marker g-glutamyltranspeptidase at different stages of nonalcoholic fatty liver disease. J Intern Med Res. 2012, 40: 924-933. 10.1177/147323001204000311.CrossRef
19.
go back to reference Pirgon O, Bilgin H, Kurku H, Cekmez F, Dündar BN: Association between insulin resistance and oxidative stress parameters in obese adolescents with non-alcoholic fatty liver disease. J Clin Res Pediatr Endocrinol. 2013, 5: 33-39. 10.4274/Jcrpe.825.CrossRefPubMedPubMedCentral Pirgon O, Bilgin H, Kurku H, Cekmez F, Dündar BN: Association between insulin resistance and oxidative stress parameters in obese adolescents with non-alcoholic fatty liver disease. J Clin Res Pediatr Endocrinol. 2013, 5: 33-39. 10.4274/Jcrpe.825.CrossRefPubMedPubMedCentral
20.
go back to reference Bonnefont-Rousselot D, Ratziu V, Giral P, Charlotte F, Beucler I, Poynard T: For the lido study group: blood oxidative stress markers are unreliable markers of hepatic steatosis. Alim Pharmacol Ther. 2006, 23: 91-99. 10.1111/j.1365-2036.2006.02719.x.CrossRef Bonnefont-Rousselot D, Ratziu V, Giral P, Charlotte F, Beucler I, Poynard T: For the lido study group: blood oxidative stress markers are unreliable markers of hepatic steatosis. Alim Pharmacol Ther. 2006, 23: 91-99. 10.1111/j.1365-2036.2006.02719.x.CrossRef
21.
22.
go back to reference Montuschi P, Barnes PJ, Roberts LJ: Isoprostanes: markers and mediators of oxidative stress. FASEB J. 2004, 18: 1791-1800. 10.1096/fj.04-2330rev.CrossRefPubMed Montuschi P, Barnes PJ, Roberts LJ: Isoprostanes: markers and mediators of oxidative stress. FASEB J. 2004, 18: 1791-1800. 10.1096/fj.04-2330rev.CrossRefPubMed
23.
go back to reference Praticò D: Prostanoid and isoprostanoid pathways in atherogenesis. Atherosclerosis. 2008, 201: 8-16. 10.1016/j.atherosclerosis.2008.04.037.CrossRefPubMed Praticò D: Prostanoid and isoprostanoid pathways in atherogenesis. Atherosclerosis. 2008, 201: 8-16. 10.1016/j.atherosclerosis.2008.04.037.CrossRefPubMed
24.
go back to reference Cave AC, Brewer AC, Narayanapanicker A, Ray R, Grieve DJ, Walker S, Shah AM: NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal. 2006, 8: 691-728. 10.1089/ars.2006.8.691.CrossRefPubMed Cave AC, Brewer AC, Narayanapanicker A, Ray R, Grieve DJ, Walker S, Shah AM: NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal. 2006, 8: 691-728. 10.1089/ars.2006.8.691.CrossRefPubMed
25.
go back to reference Cangemi R, Angelico F, Loffredo L, Del Ben M, Pignatelli P, Martini A, Violi F: Oxidative stress-mediated arterial dysfunction in patients with metabolic syndrome: effect of ascorbic acid. Free Rad Biol Med. 2007, 43: 853-859. 10.1016/j.freeradbiomed.2007.06.002.CrossRefPubMed Cangemi R, Angelico F, Loffredo L, Del Ben M, Pignatelli P, Martini A, Violi F: Oxidative stress-mediated arterial dysfunction in patients with metabolic syndrome: effect of ascorbic acid. Free Rad Biol Med. 2007, 43: 853-859. 10.1016/j.freeradbiomed.2007.06.002.CrossRefPubMed
26.
go back to reference Angelico F, Loffredo L, Pignatelli P, Augelletti T, Carnevale R, Pacella A, Albanese F, Mancini I, Di Santo S, Del Ben M, Violi F: Weight loss is associated with improved endothelial dysfunction via NOX2-generated oxidative stress down-regulation in patients with the metabolic syndrome. Int Emerg Med. 2012, 7: 219-227. 10.1007/s11739-011-0591-x.CrossRef Angelico F, Loffredo L, Pignatelli P, Augelletti T, Carnevale R, Pacella A, Albanese F, Mancini I, Di Santo S, Del Ben M, Violi F: Weight loss is associated with improved endothelial dysfunction via NOX2-generated oxidative stress down-regulation in patients with the metabolic syndrome. Int Emerg Med. 2012, 7: 219-227. 10.1007/s11739-011-0591-x.CrossRef
27.
go back to reference Loffredo L, Martino F, Carnevale R, Pignatelli P, Catasca E, Perri L, Calabrese CM, Palumbo MM, Baratta F, Del Ben M, Angelico F, Violi F: Obesity and hypercholesterolemia are associated with NOX-2 generated oxidative stress and arterial dysfunction. J Pediatr. 2012, 161: 1004-1009. 10.1016/j.jpeds.2012.05.042.CrossRefPubMed Loffredo L, Martino F, Carnevale R, Pignatelli P, Catasca E, Perri L, Calabrese CM, Palumbo MM, Baratta F, Del Ben M, Angelico F, Violi F: Obesity and hypercholesterolemia are associated with NOX-2 generated oxidative stress and arterial dysfunction. J Pediatr. 2012, 161: 1004-1009. 10.1016/j.jpeds.2012.05.042.CrossRefPubMed
28.
go back to reference Del Ben M, Fabiani M, Loffredo L, Polimeni L, Carnevale R, Baratta F, Brunori M, Albanese F, Augelletti T, Violi F, Angelico F: Oxidative stress mediated arterial dysfunction in patients with obstructive sleep apnoea and the effect of continuous positive airway pressure treatment. BMC Pulm Med. 2012, 23 (12): 36-CrossRef Del Ben M, Fabiani M, Loffredo L, Polimeni L, Carnevale R, Baratta F, Brunori M, Albanese F, Augelletti T, Violi F, Angelico F: Oxidative stress mediated arterial dysfunction in patients with obstructive sleep apnoea and the effect of continuous positive airway pressure treatment. BMC Pulm Med. 2012, 23 (12): 36-CrossRef
29.
go back to reference World Health Organisation: Report of a WHO Consultation. Definition diagnosis and classification of diabetes mellitus and its complications. 1999, Geneva, Switzerland: World Health Organisation World Health Organisation: Report of a WHO Consultation. Definition diagnosis and classification of diabetes mellitus and its complications. 1999, Geneva, Switzerland: World Health Organisation
30.
go back to reference Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC, Spertus JA, Costa F, American Heart Association; National Heart, Lung, and Blood Institute: Diagnosis and management of the metabolic syndrome: an american heart association/national heart, lung, and blood institute scientific statement. Circulation. 2005, 112: 2735-2752. 10.1161/CIRCULATIONAHA.105.169404.CrossRefPubMed Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC, Spertus JA, Costa F, American Heart Association; National Heart, Lung, and Blood Institute: Diagnosis and management of the metabolic syndrome: an american heart association/national heart, lung, and blood institute scientific statement. Circulation. 2005, 112: 2735-2752. 10.1161/CIRCULATIONAHA.105.169404.CrossRefPubMed
31.
go back to reference Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC: Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985, 28: 412-419. 10.1007/BF00280883.CrossRefPubMed Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC: Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985, 28: 412-419. 10.1007/BF00280883.CrossRefPubMed
32.
go back to reference Pignatelli P, Carnevale R, Cangemi R, Loffredo L, Sanguigni V, Stefanutti C, Basili S, Violi F: Atorvastatin inhibits gp91phox circulating levels in patients with hypercholesterolemia. Arterioscler Thromb Vasc Biol. 2010, 30: 360-367. 10.1161/ATVBAHA.109.198622.CrossRefPubMed Pignatelli P, Carnevale R, Cangemi R, Loffredo L, Sanguigni V, Stefanutti C, Basili S, Violi F: Atorvastatin inhibits gp91phox circulating levels in patients with hypercholesterolemia. Arterioscler Thromb Vasc Biol. 2010, 30: 360-367. 10.1161/ATVBAHA.109.198622.CrossRefPubMed
33.
go back to reference Wang Z, Ciabattoni G, Creminon C, Lawson J, Fitzgerald GA, Patrono C, Maclouf J: Immunological characterization of urinary 8-epi-prostaglandin F2 alpha excretion in man. J Pharmacol Exper Ther. 1995, 275: 94-100. Wang Z, Ciabattoni G, Creminon C, Lawson J, Fitzgerald GA, Patrono C, Maclouf J: Immunological characterization of urinary 8-epi-prostaglandin F2 alpha excretion in man. J Pharmacol Exper Ther. 1995, 275: 94-100.
34.
go back to reference Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, Kato T, Takeda N, Okuda J, Ida K, Kawahito Y, Yoshikawa T, Okanoue T: The severity of ultrasound findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol. 2007, 102: 1-8. 10.1111/j.1572-0241.2007.01057.x.CrossRef Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, Kato T, Takeda N, Okuda J, Ida K, Kawahito Y, Yoshikawa T, Okanoue T: The severity of ultrasound findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol. 2007, 102: 1-8. 10.1111/j.1572-0241.2007.01057.x.CrossRef
35.
go back to reference Seki S, Kitata T, Yamada T, Sakaguchi H, Nakatami K, Wakasa K: In situ detection of lipid peroxidation and oxidative DNA damage in non-alcoholic fatty liver diseases. J Hepatol. 2002, 37: 56-62. 10.1016/S0168-8278(02)00073-9.CrossRefPubMed Seki S, Kitata T, Yamada T, Sakaguchi H, Nakatami K, Wakasa K: In situ detection of lipid peroxidation and oxidative DNA damage in non-alcoholic fatty liver diseases. J Hepatol. 2002, 37: 56-62. 10.1016/S0168-8278(02)00073-9.CrossRefPubMed
36.
go back to reference Roest M, Voorbij HA, Van der Schouw YT, Peeters PH, Teerlink T, Scheffer PG: High levels of urinary F2-isoprostanes predict cardiovascular mortality in postmenopausal women. J Clin Lipidol. 2008, 2: 298-303. 10.1016/j.jacl.2008.06.004.CrossRefPubMed Roest M, Voorbij HA, Van der Schouw YT, Peeters PH, Teerlink T, Scheffer PG: High levels of urinary F2-isoprostanes predict cardiovascular mortality in postmenopausal women. J Clin Lipidol. 2008, 2: 298-303. 10.1016/j.jacl.2008.06.004.CrossRefPubMed
37.
go back to reference Feldstein AE, Anna Wieckowska A, Rocio Lopez A, Yao-Chang L, Nizar Zein N, Arthur McCullough J, Rocio Lopez A, Yao-Chang L, Nizar N, Arthur J: Cytokeratin-18 fragment levels as noninvasive biomarkers for nonalcoholic steatohepatitis: a multicenter validation study. Hepatology. 2009, 50: 1072-1078. 10.1002/hep.23050.CrossRefPubMedPubMedCentral Feldstein AE, Anna Wieckowska A, Rocio Lopez A, Yao-Chang L, Nizar Zein N, Arthur McCullough J, Rocio Lopez A, Yao-Chang L, Nizar N, Arthur J: Cytokeratin-18 fragment levels as noninvasive biomarkers for nonalcoholic steatohepatitis: a multicenter validation study. Hepatology. 2009, 50: 1072-1078. 10.1002/hep.23050.CrossRefPubMedPubMedCentral
38.
go back to reference Dasarathy S, Dasarathy J, Khiyami A, Joseph R, Lopez R, McCullough AJ: Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol. 2009, 51: 1061-1067. 10.1016/j.jhep.2009.09.001.CrossRefPubMed Dasarathy S, Dasarathy J, Khiyami A, Joseph R, Lopez R, McCullough AJ: Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol. 2009, 51: 1061-1067. 10.1016/j.jhep.2009.09.001.CrossRefPubMed
Metadata
Title
NOX2-generated oxidative stress is associated with severity of ultrasound liver steatosis in patients with non-alcoholic fatty liver disease
Authors
Maria Del Ben
Licia Polimeni
Roberto Carnevale
Simona Bartimoccia
Cristina Nocella
Francesco Baratta
Lorenzo Loffredo
Pasquale Pignatelli
Francesco Violi
Francesco Angelico
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Gastroenterology / Issue 1/2014
Electronic ISSN: 1471-230X
DOI
https://doi.org/10.1186/1471-230X-14-81

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