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Association between dietary total antioxidant capacity and hepatocellular ballooning in nonalcoholic steatohepatitis: a cross-sectional study

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Abstract

Purpose

Nonalcoholic steatohepatitis (NASH) is characterized by steatosis, lobular inflammation, ballooning, and in some cases, fibrosis, which can progress to cirrhosis and carcinoma. The progression of NASH is closely related to oxidative stress. Dietary intake of antioxidants has been suggested in protection against oxidative damage and related clinical complications. Thus, we evaluated the potential association of dietary total antioxidant capacity (TAC) with disease severity in NASH patients, as well as with anthropometric and body composition markers and biochemical parameters.

Methods

Thirty-three outpatients with a mean age of 48.4 ± 1.9 years were evaluated. Dietary TAC was estimated from a quantitative food frequency questionnaire. NASH severity, determined by liver biopsy, lifestyle characteristics, occurrence of comorbidities, anthropometry, body composition, and biochemical parameters were assessed.

Results

NASH patients who had a higher dietary TAC had fewer ballooned hepatocytes compared to those with a lower TAC (p = 0.024). The patients with the highest dietary TAC had a reduction of approximately 20% in the risk of having many ballooned hepatocytes (OR 0.791; 95% CI 0.643–0.974; p = 0.027). There was no association of steatosis, lobular inflammation, and fibrosis with dietary TAC. The same occurred for lifestyle characteristics, occurrence of comorbidities, anthropometry, body composition, and biochemical parameters.

Conclusion

Dietary TAC is higher in patients with lower hepatic injury (ballooning), suggesting a possible role of food intake naturally high in its antioxidant capacity in reducing free radical production and, consequently, oxidative stress.

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References

  1. Bellentani S, Scaglioni F, Marino M, Bedogni G (2010) Epidemiology of non-alcoholic fatty liver disease. Dig Dis 28:155–161

    Article  CAS  PubMed  Google Scholar 

  2. Magee N, Zou A, Zhang Y (2016) Pathogenesis of nonalcoholic steatohepatitis: interactions between liver parenchymal and nonparenchymal cells. Biomed Res Int. https://doi.org/10.1155/2016/5170402

    Article  PubMed  PubMed Central  Google Scholar 

  3. Mosca A, Nobili V, De Vito R, Crudele A, Scorletti E, Villani A, Alisi A, Byrne CD (2017) Serum uric acid concentrations and fructose consumption are independently associated with NASH in children and adolescents. J Hepatol 66:1031–10236

    Article  CAS  PubMed  Google Scholar 

  4. Softic S, Cohen DE, Kahn CR (2016) Role of dietary fructose and hepatic de novo lipogenesis in fatty liver disease. Dig Dis Sci 61:1282–1293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Basaranoglu M, Basaranoglu G, Bugianesi E (2015) Carbohydrate intake and nonalcoholic fatty liver disease: fructose as a weapon of mass destruction. Hepatobiliary Surg Nutr 4:109–116

    PubMed  PubMed Central  Google Scholar 

  6. Keating SE, Hackett DA, George J, Johnson NA (2012) Exercise, and non-alcoholic fatty liver disease: a systematic review and meta-analysis. J Hepatol 57:157–166

    Article  CAS  PubMed  Google Scholar 

  7. Law K, Brunt EM (2010) Nonalcoholic fatty liver disease. Clin Liver Dis 14:591–604

    Article  PubMed  Google Scholar 

  8. Younossi ZM (2008) Review article: current management of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis. Aliment Pharmacol Ther 28:2–12

    Article  CAS  PubMed  Google Scholar 

  9. Losekann A, Weston AC, Mattos AA, Tovo CV, Carli LA, Espindola MB, Pioner SR, Coral GP (2015) Non-alcoholic steatohepatitis (NASH): risk factors in morbidly obese patients. Int J Mol Sci 16:25552–25559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Williams CD, Stengel J, Asike MI, Torres DM, Shaw J, Contreras M, Landt CL, Harrison SA (2011) Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology 140:124–131

    Article  PubMed  Google Scholar 

  11. Zhan YT, An W (2010) Roles of liver innate immune cells in nonalcoholic fatty liver disease. World J Gastroenterol 16:4652–4660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Day CP, James OFW (1998) Steatohepatitis: a tale of two ‘Hits’? Gastroenterology 114:842–845

    Article  CAS  PubMed  Google Scholar 

  13. Friedman SL (2013) Liver fibrosis in 2012: convergent pathways that cause hepatic fibrosis in NASH. Nat Rev Gastroenterol Hepatol 10:71–72

    Article  CAS  PubMed  Google Scholar 

  14. Ghetti FF, Oliveira DG, Oliveira JM, Ferreira LEVVC, Cesar DE, Moreira APB (2017) Influence of gut microbiota on the development and progression of nonalcoholic steatohepatitis. Eur J Nutr. https://doi.org/10.1007/s00394-017-1524-x

    Article  Google Scholar 

  15. Tilg H, Moschen AR (2010) Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 52:1836–1846

    Article  CAS  PubMed  Google Scholar 

  16. Koek GH, Liedorp PR, Bast A (2011) The role of oxidative stress in non-alcoholic steatohepatitis. Clin Chim Acta 412:1297–1305

    Article  CAS  PubMed  Google Scholar 

  17. Kim K, Vance TM, Chen MH, Chun OK (2017) Dietary total antioxidant capacity is inversely associated with all-cause and cardiovascular disease death of US adults. Eur J Nutr. https://doi.org/10.1007/s00394-017-1519-7

    Article  PubMed  Google Scholar 

  18. Torres T, Farah A (2017) Coffee, maté, açaí and beans are the main contributors to the antioxidant capacity of Brazilian’s diet. Eur J nutr 56:1523–1533

    Article  CAS  PubMed  Google Scholar 

  19. Valtueña S, Pellegrini N, Franzini L, Bianchi MA, Ardigo D, Del Rio D, Piatti P, Scazzina F, Zavaroni I, Brighenti F (2008) Food selection based on total antioxidant capacity can modify antioxidant intake, systemic inflammation, and liver function without altering markers of oxidative stress. Am J Clin Nutr 87:1290–1297

    Article  PubMed  Google Scholar 

  20. Finelli C, Tarantino G (2012) Is there any consensus as to what diet or lifestyle approach is the right one for NAFLD patients? J Gastrointestin Liver Dis 21:293–302

    PubMed  Google Scholar 

  21. De Wit NJ, Afman LA, Mensink M, Muller M (2012) Phenotyping the effect of diet on non-alcoholic fatty liver disease. J Hepatol 57:1370–1373

    Article  CAS  PubMed  Google Scholar 

  22. American Gastroenterological Association (2002) American Gastroenterological Association medical position statement: nonalcoholic fatty liver disease. Gastroenterology 123:1702–1704

    Article  Google Scholar 

  23. Pardini R, Matsudo SMM, Araújo T, Matsudo V, Andrade E, Braggion C, Andrade D, Oliveira L, Figueira Júnior A, Raso V (2001) Validação do questionário internacional de nível de atividade física (IPAQ—versão 6): estudo piloto em adultos jovens brasileiros. Rev Bras Ciên Mov 9:45–51

    Google Scholar 

  24. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr et al (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120:1640–1645

    Article  CAS  PubMed  Google Scholar 

  25. Cotrim HP, Parise ER, Oliveira CP, Leite N, Martinelli A, Galizzi J, Silva E, de C, Mattos, Pereira A, Amorim L, Ivantes W, Souza C, Costa F, Maia M, Pessoa L, Oliveira M F (2011) Nonalcoholic fatty liver disease in Brazil. Clinical and histological profile. Ann Hepatol 10:33–37

    Article  PubMed  Google Scholar 

  26. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu YC, Torbenson MS, Unalp-Arida A, Yeh M, McCullough AJ, Sanyal AL et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313–1321

    Article  PubMed  Google Scholar 

  27. Friedewald WT, Levi RI, Fredrickson DS (1972) Estimation of the concentration of low density lipoproteins cholesterol in plasma without use of the ultracentrifuge. Clin Chem 18:499–502

    CAS  PubMed  Google Scholar 

  28. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419

    Article  CAS  PubMed  Google Scholar 

  29. Ribeiro AC, Oliveira KESD, Rodrigues MDLCF, Costa THM, Schmitz BAS (2006) Validation of a food frequency questionnaire for the adult population. Rev Nutr 19:553–562

    Article  Google Scholar 

  30. Carlsen MH, Halvorsen BL, Holte K, Bøhn SK, Dragland S, Sampson L, Willey C, Senoo H, Umezono Y, Sanada C, Barikmo I, Berhe N, Willett WC, Phillips KM, Jacobs DR, Blomhoff R (2010) The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr J 9:3

    Article  PubMed  PubMed Central  Google Scholar 

  31. Payne AC, Mazzer A, Clarkson GJ, Taylor G (2013) Antioxidant assays - consistent findings from FRAP and ORAC reveal a negative impact of organic cultivation on antioxidant potential in spinach but not watercress or rocket leaves. Food Sci Nutr 1:439–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Tiveron AP, Melo OS, Bergamaschi KB, Vieira TM, Regitano-d’Arce MA, Alencar SM (2012) Antioxidant activity of Brazilian vegetables and its relation with phenolic composition. Int J Mol Sci 13:8943–8957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Halvorsen BL, Blomhoff R (2011) Validation of a quantitative assay for the total content of lipophilic and hydrophilic antioxidants in foods. Food Chem 127:761–768

    Article  CAS  PubMed  Google Scholar 

  34. Paśko P, Bartoń H, Fołta M, Gwizdz J (2007) Evaluation of antioxidant activity of amaranth (Amaranthus cruentus) grain and by-products (flour, popping, cereal). Rocz Panstw Zakl Hig 58:35–40

    PubMed  Google Scholar 

  35. Halvorsen BL, Carlsen MH, Phillips KM, Bøhn SK, Holte K, Jacobs DR Jr, Blomhoff R (2006) Content of redox-active compounds (ie, antioxidants) in foods consumed in the United States. Am J Clin Nutr 84:95–135

    Article  CAS  PubMed  Google Scholar 

  36. Llorach R, Tomás-Barberán FA, Ferreres F (2004) Lettuce and chicory byproducts as a source of antioxidant phenolic extracts. J Agric Food Chem 52:5109–5116

    Article  CAS  PubMed  Google Scholar 

  37. Pellegrini N, Serafini M, Colombi B, Del Rio D, Salvatore S, Bianchi M, Brighenti F (2003) Total antioxidant capacity of plant foods, beverages and oils consumed in Italy assessed by three different in vitro assays. J Nutr 133:2812–2819

    Article  CAS  PubMed  Google Scholar 

  38. Halvorsen BL, Holte K, Myhrstad MC, Barikmo I, Hvattum E, Remberg SF, Wold AB, Haffner K, Baugerod H, Andersen LF, Moskaug O, Jacobs DR Jr, Blomhoff R (2002) A systematic screening of total antioxidants in dietary plants. J Nutr 132:461–471

    Article  CAS  PubMed  Google Scholar 

  39. Hermsdorff HHM, Barbosa KBF, Volp ACP, Puchau B, Bressan J, Zulet MA, Martínez JA (2012) Vitamin C and fibre consumption from fruits and vegetables improves oxidative stress markers in healthy young adults. Br J Nutr 107:1119–1127

    Article  CAS  PubMed  Google Scholar 

  40. Hermsdorff HHM, Puchau B, Volp ACP, Barbosa KBF, Bressan J, Zulet MA, Martínez JA (2011) Dietary total antioxidant capacity is inversely related to central adiposity as well as to metabolic and oxidative stress markers in healthy young adults. Nutr Metab (Lond) 8:59

    Article  CAS  Google Scholar 

  41. Puchau B, Zulet MA, De Echávarri AG, Hermsdorff HHM, Martínez JA (2010) Dietary total antioxidant capacity is negatively associated with some metabolic syndrome features in healthy young adults. Nutrition 26:534–541

    Article  CAS  PubMed  Google Scholar 

  42. Caldwell S, Ikura Y, Dias D, Isomoto K, Yabu A, Moskaluk C, Pramoonjago P, Simmons W, Scruggs H, Rosenbaum N, Wilkinson T, Toms P, Argo CK, Al-Osaimi AM, Redick JA (2010) Hepatocellular ballooning in NASH. J Hepatol 53:719–723

    Article  PubMed  PubMed Central  Google Scholar 

  43. Li XH, Mcgrath KCY, Nammi S, Heather AK, Roufogalis BD (2012) Attenuation of liver pro-inflammatory responses by zingiber ofcinale via inhibition of NF-kappa B activation in high-fat diet-fed rats. Basic Clin Pharmacol Toxicol 110:238–244

    Article  CAS  PubMed  Google Scholar 

  44. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, long JM, Wynshaw-Boris A, Poli G, Olefsky J, Karin M (2005) IKK-β links inflammation to obesity-induced insulin resistance. Nat Med 11:191–198

    Article  CAS  PubMed  Google Scholar 

  45. Machado MV, Ravasco P, Jesus L, Marques-Vidal P, Oliveira CR, Proença T, Baldeiras I, Camilo ME, Cortez-Pinto H (2008) Blood oxidative stress markers in non-alcoholic steatohepatitis and how it correlates with diet. Scand J Gastroenterol 43:95–102

    Article  CAS  PubMed  Google Scholar 

  46. Erhardt A, Stahl W, Sies H, Lirussi F, Donner A, Haussinger D (2011) Plasma levels of vitamin E and carotenoids are decreased in patients with Nonalcoholic Steatohepatitis (NASH). Eur J Med Res 16:76–78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Singal AK, Jampana SC, Weinman SA (2011) Antioxidants as therapeutic agents for liver disease. Liver Int 31:1432–1448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Musso G, Gambino R, De Michieli F, Cassader M, Rizzeto M, Durazzo M, Fagà E, Silli B, Pagano G (2003) Dietary habits and their relations to insulin resistance and postprandial lipidemia in nonalcoholic steatohepatitis. Hepatology 37:909–915

    Article  CAS  PubMed  Google Scholar 

  49. Georgoulis M, Fragopoulou E, Kontogianni MD, Margariti MD, Boulamatsi O, Detopoulou P, Tiniakos D, Zafiropoulou R, Papatheodoridis G (2015) Blood redox status is associated with the likelihood of nonalcoholic fatty liver disease irrespectively of diet’s total antioxidant capacity. Nutr Res 35:41–48

    Article  CAS  PubMed  Google Scholar 

  50. Mann JP, Tang GY, Nobili V, Armstrong MJ (2018) Evaluations of lifestyle, dietary, and pharmacologic treatments for pediatric non-alcoholic fatty liver disease—a systematic review. Clin Gastroenterol Hepatol S1542-3565:30555-X

    Google Scholar 

  51. Lisboa QC, Silvia Marinho Ferolla Costa SMF, Couto CA (2016) Current management of non-alcoholic fatty liver disease. Rev Assoc Med Bras 62:872–887

    Article  PubMed  Google Scholar 

  52. Lavine JE, Schwimmer JB, Van Natta ML, Molleston JP, Murray KF, Rosenthal P, Abrams SH, Scheimann AO, Sanyal AJ, Chalasani N, Tonascia J, Unalp A, Clark JM, Brunt EM, Kleiner DE, Hoofnagle JH, Robuck PR et al (2011) Effect of vitamin E or metformin for treatment of nonalcoholic fatty liver disease in children and adolescents: the TONIC randomized controlled trial. JAMA 305:1659–1668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 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, NASH CRN (2010) Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med 362:1675–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Kawanaka M, Nishino K, Nakamura J, Suehiro M, Goto D, Urata N, Oka T, Kawamoto H, Nakamura H, Yodoi J, Hino K, Yamada G (2013) Treatment of nonalcoholic steatohepatitis with vitamins E and C: a pilot study. Hepat Med 5:11–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Rolo AP, Teodoro JS, Palmeira CM (2012) Role of oxidative stress in the pathogenesis of nonalcoholic steatohepatitis. Free Radic Biol Med 52:59–69

    Article  CAS  PubMed  Google Scholar 

  56. Romero-Gómez M, Zelber-Sagi S, Trenell M (2017) Treatment of NAFLD with diet, physical activity and exercise. J Hepatol 67:829–846

    Article  PubMed  Google Scholar 

  57. Micek A, Grosso G, Polak M, Kozakiewicz K, Tykarski A, Puch Walczak A, Drygas W, Kwasniewska M, Pajak A (2018) Association between tea and coffee consumption and prevalence of metabolic syndrome in Poland - results from the WOBASZ II study (2013–2014). Int J Food Sci Nutr 69:358–368

    Article  CAS  PubMed  Google Scholar 

  58. Agudo A, Cabrera L, Amiano P, Ardanaz E, Barricarte A, Berenguer T, Chirlaque MD, Dorronsoro M, Jakszyn P, Larranaga N, Martinez C, Navarro C, Quirós JR, Sanchez MJ, Tormo MJ, Gonzalez CA (2007) Fruit and vegetable intakes, dietary antioxidant nutrients, and total mortality in Spanish adults: findings from theSpanish cohort of the European Prospective Investigation into Cancer and Nutrition (EPIC-Spain). Am J Clin Nutr 85:1634–1642

    Article  CAS  PubMed  Google Scholar 

  59. Pellegrini N, Serafini M, Colombi B, Del Rio D, Salvatore S, Bianchi M, Brighenti F (2003) Total antioxidant capacity of plant foods, beveragesand oils consumed in Italy assessed by three different in vitro assays. J Nutr 133:2812–2819

    Article  CAS  PubMed  Google Scholar 

  60. Sumida Y, Nakajima A, Itoh Y (2014) Limitations of liver biopsy and non-invasive diagnostic tests for the diagnosis of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. World J Gastroenterol 20:475–485

    Article  PubMed  PubMed Central  Google Scholar 

  61. Stinton LM, Loomba R (2014) Recommendations for liver biopsy evaluation in non-alcoholic fatty liver disease. Minerva Gastroenterol Dietol 60:5–13

    CAS  PubMed  Google Scholar 

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Acknowledgements

The study was supported by Brazilian Government Organization (Fundação de Amparo à Pesquisa do Estado de Minas Gerais/FAPEMIG; APQ 01522-15). D. G. O. is the recipient of a CAPES grant. D. G. O., F. F. G., and (A) P. (B) M. participated in the design and protocol of the study. D. G. O., F. F. G., and J. M. O. carried out the study. D. G. O. and H. H. M. F. participated in the evaluation of the dietary total antioxidant capacity. D. G. O., (A) P. (B) M., and L. E. V. V. (C) F. were involved with editing the manuscript and all authors read and approved the final manuscript.

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Authors and Affiliations

  1. Departamento de Nutrição, Universitary Hospital, School of Medicine, Federal University of Juiz de Fora, Bairro Martelos, s/n, CEP 36036-330, Juiz de Fora, Minas Gerais, Brazil

    Daiane Gonçalves de Oliveira, Fabiana de Faria Ghetti, Juliano Machado de Oliveira & Lincoln Eduardo Villela Vieira de Castro Ferreira

  2. Nutrition Department, Federal University of Juiz de Fora, Juiz de Fora, Minas Gerais, Brazil

    Daiane Gonçalves de Oliveira & Ana Paula Boroni Moreira

  3. Nutrition and Health Department, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil

    Helen Hermana Miranda Hermsdorff

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  1. Daiane Gonçalves de Oliveira
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  2. Fabiana de Faria Ghetti
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Correspondence to Daiane Gonçalves de Oliveira.

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de Oliveira, D.G., de Faria Ghetti, F., Moreira, A.P.B. et al. Association between dietary total antioxidant capacity and hepatocellular ballooning in nonalcoholic steatohepatitis: a cross-sectional study. Eur J Nutr 58, 2263–2270 (2019). https://doi.org/10.1007/s00394-018-1776-0

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