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High red and processed meat consumption is associated with non-alcoholic fatty liver disease and insulin resistance
Abstract
Background & aims High red and processed meat consumption is related to type 2 diabetes. In addition, cooking meat at high temperatures for a long duration forms heterocyclic amines (HCAs), which are related to oxidative stress. However, the association between meat consumption and non-alcoholic fatty liver disease (NAFLD) is yet to be thoroughly tested. Therefore, we aimed to test the association of meat type and cooking method with NAFLD and insulin resistance (IR).Methods This was a cross-sectional study in individuals who were 40-70 years old and underwent screening colonoscopy between 2013 and 2015 in a single center in Israel. NAFLD and IR were evaluated by ultrasonography and homeostasis model assessment. Meat type and cooking method were measured by a food frequency questionnaire (FFQ) and a detailed meat questionnaire. Unhealthy cooking methods were considered as frying and grilling to a level of well done and very well done. Dietary HCA intake was calculated.Results A total of 789 individuals had a valid FFQ and 357 had a valid meat questionnaire. High consumption of total meat (portions/day above the median) (odds ratio [OR] 1.49; 95% CI 1.05-2.13; p = 0.028; OR 1.63; 1.12-2.37; p = 0.011), red and/or processed meat (OR1.47; 95% CI 1.04-2.09; p = 0.031; OR1.55; 1.07-2.23; p = 0.020) was independently associated with higher odds of NAFLD and IR, respectively, when adjusted for: body mass index, physical activity, smoking, alcohol, energy, saturated fat and cholesterol intake. High intake of meat cooked using unhealthy methods (OR1.92; 95% CI 1.12-3.30; p = 0.018) and HCAs (OR2.22; 95% CI 1.28-3.86; p = 0.005) were independently associated with higher odds of IR.Conclusion High consumption of red and/or processed meat is associated with both NAFLD and IR. High HCA intake is associated with IR. If confirmed in prospective studies, limiting the consumption of unhealthy meat types and improving preparation methods may be considered as part of NAFLD lifestyle treatment.Lay summary High red and processed meat consumption is related to several diseases. In addition, cooking meat at high temperatures for a long duration forms heterocyclic amines, which have harmful health effects. Non-alcoholic fatty liver disease is a significant public health burden and its formation is strongly related to insulin resistance. In this study, both were found to be more frequent in people who consume relatively high quantities of red and processed meat. In addition, a high intake of heterocyclic amines was associated with insulin resistance.
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“Several observational and crosssectional studies have shown the harmful association between MASLD and high intake of red and processed meat. 302 -304”
From EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). (2024) · cites this paper as [303]
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Cites
Chalasani, N., Younossi, Z., Lavine, J. E., Charlton, M., Cusi, K., Rinella, M., Harrison, S. A., Brunt, E. M., & Sanyal, A. J. (2018) · Hepatology · doi:10.1002/hep.29367 · Cited by 7,239
EASL–EASD–EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease
(2016) · Journal of Hepatology · doi:10.1016/j.jhep.2015.11.004 · Cited by 4,836
Willett, W. C. (1998) · doi:10.1093/acprof:oso/9780195122978.001.0001 · Cited by 4,541
Advanced glycation end-products: A review
Singh, R., Barden, A., Mori, T., & Beilin, L. (2001) · Diabetologia · doi:10.1007/s001250051591 · Cited by 2,597
Estes, C., Razavi, H. A., Loomba, R. S., Younossi, Z. M., & Sanyal, A. J. (2017) · Hepatology · doi:10.1002/hep.29466 · Cited by 2,496
Mozaffarian, D. (2016) · Circulation · doi:10.1161/circulationaha.115.018585 · Cited by 2,216
Carcinogenicity of consumption of red and processed meat
Bouvard, V., LOOMIS, D. P., Guyton, K. Z., Grosse, Y., Ghissassi, F. E., Benbrahim‐Tallaa, L., Guha, N., Mattock, H., & Straíf, K. (2015) · The Lancet Oncology · doi:10.1016/s1470-2045(15)00444-1 · Cited by 1,918
Loomba, R. S., & Sanyal, A. J. (2013) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2013.171 · Cited by 1,732
Brunt, E. M., Kleiner, D. E., Wilson, L. A., Belt, P., & Neuschwander-Tetri, B. A. (2011) · Hepatology · doi:10.1002/hep.24127 · Cited by 1,251
Micha, R., Wallace, S. K., & Mozaffarian, D. (2010) · Circulation · doi:10.1161/circulationaha.109.924977 · Cited by 1,244
Vessby, B., Uusitupa, M., Hermansen, K., Riccardi, G., Rivellese, A. A., Tapsell, L. C., Nälsén, C., Berglund, L., Louheranta, A., Rasmussen, B. M., et al. (2001) · Diabetologia · doi:10.1007/s001250051620 · Cited by 1,119
Standards of Medical Care in Diabetes—2017 Abridged for Primary Care Providers
American Diabetes Association (2017) · Clinical Diabetes · doi:10.2337/cd16-0067 · Cited by 977
Ryan, M. C., Itsiopoulos, C., Thodis, T., Ward, G., Trost, N., Hofferberth, S., O’Dea, K., Desmond, P. V., Johnson, N. A., & Wilson, A. M. (2013) · Journal of Hepatology · doi:10.1016/j.jhep.2013.02.012 · Cited by 778
Nonalcoholic Fatty Liver Disease, Hepatic Insulin Resistance, and Type 2 Diabetes
Birkenfeld, A. L., & Shulman, G. I. (2013) · Hepatology · doi:10.1002/hep.26672 · Cited by 752
Cross-Talk Between Iron Metabolism and Diabetes
Fernández-Real, J. M., López-Bermejo, A., & Ricart, W. (2002) · Diabetes · doi:10.2337/diabetes.51.8.2348 · Cited by 704
Trichopoulou, A., Martínez‐González, M. Á., Tong, T. Y. N., Forouhi, N. G., Khandelwal, S., Prabhakaran, D., Mozaffarian, D., & de Lorgeril, M. (2014) · BMC Medicine · doi:10.1186/1741-7015-12-112 · Cited by 696
Francque, S., van der Graaff, D., & Kwanten, W. J. (2016) · Journal of Hepatology · doi:10.1016/j.jhep.2016.04.005 · Cited by 591
Cancer risk of heterocyclic amines in cooked foods: an analysis and implications for research
Layton, D. W., Bogen, K. T., Knize, M. G., Hatch, F. T., Johnson, V. M., & Felton, J. S. (1995) · Carcinogenesis · doi:10.1093/carcin/16.1.39 · Cited by 553
Zelber‐Sagi, S., Nitzan, D., Goldsmith, R., Webb, M., Blendis, L. M., Halpern, Z., & Oren, R. (2007) · Journal of Hepatology · doi:10.1016/j.jhep.2007.06.020 · Cited by 552
Self-citationFeskens, E. J. M., Virtanen, S. M., Räsänen, L., Tuomilehto, J. O., Stengård, J., Pekkanen, J., Nissinen, A. M., & Kromhout, D. (1995) · Diabetes Care · doi:10.2337/diacare.18.8.1104 · Cited by 504
Bjermo, H., Iggman, D., Kullberg, J., Dahlman, I., Johansson, L., Persson, L., Berglund, J., Pulkki, K., Basu, S., Uusitupa, M., et al. (2012) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.030114 · Cited by 490
Wouters, K., van Gorp, P. J., Bieghs, V., Gijbels, M. J., Duimel, H., Lütjohann, D., Kerksiek, A., van Kruchten, R., Maeda, N., Staels, B., et al. (2008) · Hepatology · doi:10.1002/hep.22363 · Cited by 482
Wang, X., Lin, X., Ouyang, Y. Y., Liu, J., Zhao, G., Pan, A., & Hu, F. B. (2016) · Public Health Nutrition · doi:10.1017/s1368980015002062 · Cited by 412
A Prospective Study of Red Meat Consumption and Type 2 Diabetes in Middle-Aged and Elderly Women
Song, Y., Manson, J. E., Buring, J. E., & Liu, S. (2004) · Diabetes Care · doi:10.2337/diacare.27.9.2108 · Cited by 368
Nutrition and physical activity in NAFLD: An overview of the epidemiological evidence
Zelber‐Sagi, S. (2011) · World Journal of Gastroenterology · doi:10.3748/wjg.v17.i29.3377 · Cited by 307
Self-citationWebb, M., Yeshua, H., Zelber‐Sagi, S., Santo, E., Brazowski, E., Halpern, Z., & Oren, R. (2009) · American Journal of Roentgenology · doi:10.2214/ajr.07.4016 · Cited by 286
Self-citationWell-Done Meat Intake, Heterocyclic Amine Exposure, and Cancer Risk
Zheng, W., & Lee, S. (2009) · Nutrition and Cancer · doi:10.1080/01635580802710741 · Cited by 268
Oddy, W. H., Herbison, C. E., Jacoby, P., Ambrosini, G. L., O’Sullivan, T. A., Ayonrinde, O. T., Olynyk, J. K., Black, L. J., Beilin, L. J., Mori, T. A., et al. (2013) · The American Journal of Gastroenterology · doi:10.1038/ajg.2013.95 · Cited by 259
Marshall, J. A., Bessesen, D. H., & Hamman, R. F. (1997) · Diabetologia · doi:10.1007/s001250050697 · Cited by 251
Birlouez‐Aragon, I., Saavedra, G., Tessier, F. J., Galinier, A., Ameur, L. A., Lacoste, F., Niamba, C.-N., Alt, N., Somoza, V., & Lecerf, J. (2010) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.28737 · Cited by 250
Paniagua, J. A., de la Sacristana, A. G., Romero, I., Vidal‐Puig, A., Latre, J. M., Sánchez, E., Pérez‐Martínez, P., López‐Miranda, J., & Pérez‐Jiménez, F. (2007) · Diabetes Care · doi:10.2337/dc06-2220 · Cited by 242
Zhao, Z., Li, S., Liu, G., Yan, F., Ma, X., Huang, Z., & Tian, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041641 · Cited by 227
Yasutake, K., Nakamuta, M., Shima, Y., Ohyama, A., Masuda, K., Haruta, N., Fujino, T., Aoyagi, Y., Fukuizumi, K., Yoshimoto, T., et al. (2008) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365520802588133 · Cited by 219
Vang, A., Singh, P. N., Lee, J. W., Haddad, E. H., & Brinegar, C. H. (2008) · Annals of Nutrition and Metabolism · doi:10.1159/000121365 · Cited by 216
Parker, D., Weiss, S. T., Troisi, R. J., Cassano, P. A., Vokonas, P., & Landsberg, L. (1993) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/58.2.129 · Cited by 212
Boada, L. D., Henríquez‐Hernández, L. A., & Luzardo, O. P. (2016) · Food and Chemical Toxicology · doi:10.1016/j.fct.2016.04.008 · Cited by 205
Acute dietary fat intake initiates alterations in energy metabolism and insulin resistance
Hernández, E. Á., KAHL, S., Seelig, A., Begovatz, P., Irmler, M., Kupriyanova, Y., Nowotny, B., Nowotny, P., Herder, C., Barosa, C., et al. (2017) · Journal of Clinical Investigation · doi:10.1172/jci89444 · Cited by 205
Mediterranean and DASH Diet Scores and Mortality in Women With Heart Failure
Levitan, E. B., Lewis, C. E., Tinker, L. F., Eaton, C. B., Ahmed, A., Manson, J. E., Snetselaar, L., Martin, L. W., Trevisan, M., Howard, B. V., et al. (2013) · Circulation Heart Failure · doi:10.1161/circheartfailure.113.000495 · Cited by 203
Hyogo, H., Yamagishi, S., Iwamoto, K., Arihiro, K., Takeuchi, M., Sato, T., Ochi, H., Nonaka, M., Nabeshima, Y., Inoue, M., et al. (2007) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2007.04943.x · Cited by 188
Kim, Y., Keogh, J., & Clifton, P. (2015) · Metabolism · doi:10.1016/j.metabol.2015.03.008 · Cited by 181
Freedman, N. D., Cross, A. J., McGlynn, K. A., Abnet, C. C., Park, Y., Hollenbeck, A. R., Schatzkin, A. G., Everhart, J., & Sinha, R. (2010) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djq301 · Cited by 169
Adherence to Mediterranean Diet and Non-Alcoholic Fatty Liver Disease: Effect on Insulin Resistance
Baratta, F., Pastori, D., Polimeni, L., Bucci, T., Ceci, F., Calabrese, C. M., Ernesti, I., Pannitteri, G., Violi, F., Angelico, F., et al. (2017) · The American Journal of Gastroenterology · doi:10.1038/ajg.2017.371 · Cited by 151
Comparison of fatty liver index with noninvasive methods for steatosis detection and quantification
Zelber‐Sagi, S. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i1.57 · Cited by 128
Self-citationIsokuortti, E., Zhou, Y., Peltonen, M., Bugianesi, E., Clement, K., Bonnefont-Rousselot, D., Lacorte, J.-M., Gastaldelli, A., Schuppan, D., Schattenberg, J. M., et al. (2017) · Diabetologia · doi:10.1007/s00125-017-4340-1 · Cited by 120
Keinan‐Boker, L., Noyman, N., Chinich, A., Green, M. S., & Nitzan, D. (2005) · PubMed · Cited by 104
Fretts, A. M., Follis, J. L., Nettleton, J. A., Lemaître, R. N., Ngwa, J. S., Wojczynski, M. K., Kalafati, I. P., Varga, T. V., Wood, A. C., Houston, D. K., et al. (2015) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.101238 · Cited by 97
Associations between dietary factors and markers of NAFLD in a general Dutch adult population
Rietman, A., Sluik, D., Feskens, E. J. M., Kok, F. J., & Mensink, M. (2017) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2017.148 · Cited by 91
Öz, F., Kaban, G., & Kaya, M. (2010) · LWT · doi:10.1016/j.lwt.2010.04.014 · Cited by 86
Dietary sodium and potassium intake in relation to non-alcoholic fatty liver disease
Choi, Y., Lee, J. E., Chang, Y., Kim, M. K., Sung, E., Shin, H., & Ryu, S. (2016) · British Journal Of Nutrition · doi:10.1017/s0007114516003391 · Cited by 84
Risk Factors Associated With Non-Alcoholic Fatty Liver Disease in Indians: A Case–Control Study
Singh, S. P., Singh, A., Misra, D., Misra, B., Pati, G. K., Panigrahi, M. K., Kar, S. K., Bhuyan, P., Pattnaik, K., Meher, C., et al. (2015) · Journal of Clinical and Experimental Hepatology · doi:10.1016/j.jceh.2015.09.001 · Cited by 83
The role of dietician follow-up in the success of bariatric surgery
Endevelt, R., Ben‐Assuli, O., Klain, E., & Zelber‐Sagi, S. (2013) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2013.01.006 · Cited by 82
Self-citationMeat consumption and risk of type 2 diabetes: the Multiethnic Cohort
Steinbrecher, A., Erber, E., Grandinetti, A., Kolonel, L., & Maskarinec, G. (2011) · Public Health Nutrition · doi:10.1017/s1368980010002004 · Cited by 81
Cocate, P. G., Natali, A. J., de Oliveira, A., Alfenas, R. D. C. G., Pelúzio, M. D. C. G., Longo, G. Z., dos Santos, E. C., Buthers, J. M., de Oliveira, L. L., & Hermsdorff, H. H. M. (2013) · European Journal of Preventive Cardiology · doi:10.1177/2047487313507684 · Cited by 75
High intake of heterocyclic amines from meat is associated with oxidative stress
de Carvalho, A. M., Miranda, A. M., dos Santos, F. A., Loureiro, A. P. D. M., Fisberg, R. M., & Marchioni, D. M. L. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515000628 · Cited by 71
Cantwell, M. M., Mittl, B., Curtin, J., Carroll, R. J., Potischman, N. A., Caporaso, N. E., & Sinha, R. R. (2004) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-270-2 · Cited by 63
Wang, Y., Hui, T., Zhang, Y. W., Liu, B., Wang, F. L., Li, J. K., Cui, B., Guo, X. Y., & Peng, Z. (2014) · Food Chemistry · doi:10.1016/j.foodchem.2014.06.109 · Cited by 61
Processed and Unprocessed Red Meat Consumption and Incident Type 2 Diabetes Among French Women
Lajous, M., Tondeur, L., Fagherazzi, G., de Lauzon‐Guillain, B., Boutron‐Ruault, M., & Clavel‐Chapelon, F. (2011) · Diabetes Care · doi:10.2337/dc11-1518 · Cited by 61
Belinova, L., Kahleová, H., Malínská, H., Topolčan, O., Vrzalová, J., Oliyarnyk, O., Kazdová, L., Hill, M., & Pelikánová, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0107561 · Cited by 50
Miele, L., Dall’Armi, V., Cefalo, C., Nedović, B., Arzani, D., Amore, R., Rapaccini, G. L., Gasbarrini, A., Ricciardi, W., Grieco, A., et al. (2014) · Genes & Nutrition · doi:10.1007/s12263-013-0383-1 · Cited by 45
Free radical generation from heterocyclic amines by cytochrome b5 reductase in the presence of NADH
Maeda, H., Sawa, T., Yubisui, T., & Akaike, T. (1999) · Cancer Letters · doi:10.1016/s0304-3835(99)00139-1 · Cited by 43
Zelber‐Sagi, S., Toker, S., Armon, G., Melamed, S., Berliner, S. A., Shapira, I., Halpern, Z., Santo, E., & Shibolet, O. (2013) · Psychological Medicine · doi:10.1017/s0033291713000500 · Cited by 31
Self-citationRogers, L. J., Basnakian, A. G., Orloff, M. S., Ning, B., Yao‐Borengasser, A., Raj, V. R., & Kadlubar, S. A. (2016) · Nutrition & Metabolism · doi:10.1186/s12986-016-0111-0 · Cited by 21
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Metadata
- Authors
- Zelber-Sagi, S., Ivancovsky-Wajcman, D., Fliss Isakov, N., Webb, M., Orenstein, D., Shibolet, O., & Kariv, R.
- Affiliations
- Tel Aviv University (IL)
- University of Haifa (IL)
- Venue
- Journal of Hepatology
- Publisher
- Elsevier BV
- Published
- 2018-06
- Volume
- 68
- Issue
- 6
- Pages
- 1239-1246
- ISSN
- 0168-8278 (ISSN-L)
- OpenAlex
- W2794354514
- Cited by
- 297
- References
- 62
- Citations by year
- 2026: 19 · 2025: 35 · 2024: 38 · 2023: 54 · 2022: 44 · 2021: 33 · 2020: 38 · 2019: 29 · 2018: 6
- FWCI
- 26.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Hepatology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diet, Metabolism, and Disease
- Keywords
- red meat consumption, processed meat consumption, non-alcoholic fatty liver disease, insulin resistance, heterocyclic amines, meat cooking methods, oxidative stress, meat consumption, type 2 diabetes risk, middle-aged and older adults, dietary exposure assessment
- MeSH terms
- Red Meat, Adult, Aged, Amines, Cooking, Cross-Sectional Studies, Eating, Female, Heterocyclic Compounds, Humans, Insulin Resistance, Israel, Male, Meat Products, Middle Aged, Surveys and Questionnaires, Risk Factors, Multivariate Analysis, Non-alcoholic Fatty Liver Disease
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