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Effects of processed red meat consumption on the risk of type 2 diabetes and cardiovascular diseases among Korean adults: the Korean Genome and Epidemiology Study

  • Jakyung Son
  • Yujin Lee
  • Kyong ParkEmail author
Original Contribution
  • 255 Downloads

Abstract

Purpose

Few studies have evaluated the effects of processed red meat (PRM) consumption on chronic disease risk, especially among low average PRM consumption populations. This study examined association between PRM intake and type 2 diabetes mellitus (T2DM) and cardiovascular disease (CVD) incidences in Korea.

Methods

Participants (n = 10,030; aged 40–69 years) were recruited from the Ansan–Ansung cohort study, a subset of Korean Genome Epidemiology Study. Validated 103-item semi-quantitative food frequency questionnaire was used to assess dietary information, at baseline (2001–2002) and at second follow-up (2005–2006). T2DM and CVD incidences were identified using biennial questionnaire-based interview during a 10-year follow-up period. Cox proportional hazards regression analysis was used to calculate multivariable-adjusted hazard ratios (HRs) and 95% confidence intervals (CIs).

Results

Over the 10-year follow-up period, 668 and 493 incident cases of T2DM (62,130 person-years) and CVD (63,150 person-years), respectively, were documented. In crude models, comparing the highest and lowest levels of PRM intake, no significant association occurred with incident T2DM [HR, 95% CI (0.94, 0.76–1.17)], while significant association occurred with incident CVD (0.67, 0.51–0.88). However, in adjusted models, this association was no longer significant, showing HRs (95% CI) of PRM intake for T2DM and CVD of 1.07 (0.85–1.35) and 1.14 (0.85–1.55), respectively.

Conclusions

PRM intake did not affect T2DM and CVD incidences among Korean middle-aged adults, although extremely low average consumption of PRM may explain the finding. Therefore, limiting PRM intake may not be a top priority for the prevention of chronic diseases in Korean population.

Keywords

Processed red meat Diabetes mellitus Cardiovascular disease Cohort study Korean 

Notes

Acknowledgements

Data in this study were from the Korean Genome and Epidemiology Study (KoGES; 4851-302), National Research Institute of Health, Centers for Disease Control and Prevention, Ministry for Health and Welfare, Republic of Korea. This work was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (Grant number: NRF-2017R1A1A3A04069759). The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

Author contributions

JS contributed to the writing original draft preparation, formal analysis, visualization, and software. JS, YL and KP contributed to the investigation, data curation, and writing the review and editing. KP contributed to the conceptualization, supervision, project administration, resources, funding acquisition, and validation. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the Institutional Review Board (IRB) of the Korea Centers for Disease Control and Prevention (IRB number: KU-IRB-15-EX-256-A-1), and the research procedure for the second analysis was approved by the Yeungnam University IRB (7002016-E-2016-003).

Informed consent

Written informed consent was obtained from all participants.

Supplementary material

394_2018_1799_MOESM1_ESM.docx (482 kb)
Online Resource 1: Hazard ratios for incidence type 2 diabetes mellitus and cardiovascular diseases by potential modifiers (DOCX 481 KB)
394_2018_1799_MOESM2_ESM.docx (104 kb)
Online Resource 2: Overall disease-free survival by levels of processed red meat intake (DOCX 103 KB)

References

  1. 1.
    World Health Organization (2017) Cardiovascular diseases (CVDs). http://www.who.int/mediacentre/factsheets/fs317/en/. Accessed 8 Dec 2017
  2. 2.
    International Diabetes Federation (2015) IDF DIABETES ATLAS. http://www.diabetesatlas.org/. Accessed 13 Nov 2017
  3. 3.
    Deurenberg P, Deurenberg-Yap M, Guricci S (2002) Asians are different from Caucasians and from each other in their Body Mass Index/body fat per cent relationship. Obes Rev 3(3):141–146.  https://doi.org/10.1046/j.1467-789X.2002.00065.x CrossRefPubMedGoogle Scholar
  4. 4.
    Ram CVS, Farmer JA (2012) Metabolic syndrome in south Asians. J Clin Hypertens 14(8):561–565.  https://doi.org/10.1111/j.1751-7176.2012.00652.x CrossRefGoogle Scholar
  5. 5.
    Ministry of Health and Welfare (2015) The major results of national health nutrition survey 2014. http://www.mohw.go.kr/front_new/al/sal0301vw.jsp?PAR_MENU_ID=04&MENU_ID=0403&page=16&CONT_SEQ=326126. Accessed 27 Mar 2017
  6. 6.
    Wang D, Campos H, Baylin A (2017) Red meat intake is positively associated with non-fatal acute myocardial infarction in the Costa Rica Heart Study. Br J Nutr 118(4):303–311.  https://doi.org/10.1017/S000711451700201X CrossRefPubMedGoogle Scholar
  7. 7.
    Nagao M, Iso H, Yamagishi K, Date C, Tamakoshi A (2012) Meat consumption in relation to mortality from cardiovascular disease among Japanese men and women. Eur J Clin Nutr 66(6):687–693.  https://doi.org/10.1038/ejcn.2012.6 CrossRefPubMedGoogle Scholar
  8. 8.
    Isanejad M, LaCroix AZ, Thomson CA, Tinker L, Larson JC, Qi Q, Qi L, Cooper-DeHoff RM, Phillips LS, Prentice RL, Beasley JM (2017) Branched-chain amino acid, meat intake and risk of type 2 diabetes in the Women’s Health Initiative. Br J Nutr 117(11):1523–1530.  https://doi.org/10.1017/S0007114517001568 CrossRefPubMedGoogle Scholar
  9. 9.
    Kim K, Hyeon J, Lee SA, Kwon SO, Lee H, Keum N, Lee JK, Park SM (2017) Role of total, red, processed, and white meat consumption in stroke incidence and mortality: a systematic review and meta-analysis of prospective cohort studies. J Am Heart Assoc.  https://doi.org/10.1161/jaha.117.005983 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Wang X, Lin X, Ouyang YY, Liu J, Zhao G, Pan A, Hu FB (2016) Red and processed meat consumption and mortality: dose–response meta-analysis of prospective cohort studies. Public Health Nutr 19(5):893–905.  https://doi.org/10.1017/s1368980015002062 CrossRefPubMedGoogle Scholar
  11. 11.
    Micha R, Michas G, Mozaffarian D (2012) Unprocessed red and processed meats and risk of coronary artery disease and type 2 diabetes—an updated review of the evidence. Curr Atheroscler Rep 14(6):515–524.  https://doi.org/10.1007/s11883-012-0282-8 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Park MK, Paik HY, Lee Y (2016) Intake trends of red meat, alcohol, and fruits and vegetables as cancer-related dietary factors from 1998 to 2009. Osong Public Health Res Perspect 7(3):180–189.  https://doi.org/10.1016/j.phrp.2016.04.005 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Micha R, Penalvo JL, Cudhea F, Imamura F, Rehm CD, Mozaffarian D (2017) Association between dietary factors and mortality from heart disease, stroke, and type 2 diabetes in the United States. JAMA 317(9):912–924.  https://doi.org/10.1001/jama.2017.0947 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Bendinelli B, Palli D, Masala G, Sharp SJ, Schulze MB, Guevara M, van der AD, Sera, Amiano F, Balkau P, Barricarte B, Boeing A, Crowe H, Dahm FL, Dalmeijer CC, de Lauzon-Guillain G, Egeberg B, Fagherazzi R, Franks G, Krogh PW, Huerta V, Jakszyn JM, Khaw P, Li KT, Mattiello K, Nilsson A, Overvad PM, Ricceri K, Rolandsson F, Sanchez O, Slimani MJ, Sluijs N, Spijkerman I, Teucher AM, Tjonneland B, Tumino A, van den Berg R, Forouhi SW, Langeberg NG, Feskens C, Riboli EJ, Wareham E NJ (2013) Association between dietary meat consumption and incident type 2 diabetes: the EPIC-InterAct study. Diabetologia 56(1):47–59.  https://doi.org/10.1007/s00125-012-2718-7 CrossRefPubMedGoogle Scholar
  15. 15.
    He Y, Yang X, Xia J, Zhao L, Yang Y (2016) Consumption of meat and dairy products in China: a review. Proc Nutr Soc 75(3):385–391.  https://doi.org/10.1017/s0029665116000641 CrossRefPubMedGoogle Scholar
  16. 16.
    Rohrmann S, Overvad K, Bueno-de-Mesquita HB, Jakobsen MU, Egeberg R, Tjonneland A, Nailler L, Boutron-Ruault MC, Clavel-Chapelon F, Krogh V, Palli D, Panico S, Tumino R, Ricceri F, Bergmann MM, Boeing H, Li K, Kaaks R, Khaw KT, Wareham NJ, Crowe FL, Key TJ, Naska A, Trichopoulou A, Trichopoulos D, Leenders M, Peeters PH, Engeset D, Parr CL, Skeie G, Jakszyn P, Sanchez MJ, Huerta JM, Redondo ML, Barricarte A, Amiano P, Drake I, Sonestedt E, Hallmans G, Johansson I, Fedirko V, Romieux I, Ferrari P, Norat T, Vergnaud AC, Riboli E, Linseisen J (2013) Meat consumption and mortality—results from the European prospective investigation into cancer and nutrition. BMC Med 11:63.  https://doi.org/10.1186/1741-7015-11-63 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Ministry of Food and Drug Safety (2015) The level of red meat and processed meat intake were not worrying level for Koreans. http://www.mfds.go.kr/index.do?searchkey=title:contents&mid=675&searchword=%C0%C7%BE%E0%C7%B0&pageNo=19&seq=29262&cmd=v. Accessed 27 Mar 2017
  18. 18.
    World Health Organization (2015) IARC monographs evaluate consumption of red meat and processed meat. http://www.iarc.fr/en/media-centre/pr/2015/pdfs/pr240_E.pdf. Accessed 27 Mar 2017
  19. 19.
    U.S. Department of Health and Human Services, U.S. Department of Agriculture (2015) Dietary guidelines for Americans 2015–2020. https://health.gov/dietaryguidelines/2015/guidelines/. Accessed 27 Mar 2017
  20. 20.
    Public Health England (2014) A quick guide to the government’s healthy eating recommendations. http://elearning.ymca.co.uk/ymcafit/pluginfile.php/11442/mod_resource/content/1/A%20Quick%20Guide%20to%20Government%20Healthy%20Eating.pdf. Accessed 27 Mar 2017
  21. 21.
    National Health and Medical Research Council, Department of Health and Ageing (2013) Australian dietary guidelines. https://www.nhmrc.gov.au/guidelines-publications/n55. Accessed 27 Mar 2017
  22. 22.
    Kim Y, Han BG (2017) Cohort profile: the Korean Genome and Epidemiology Study (KoGES) Consortium. Int J Epidemiol 46(2):e20.  https://doi.org/10.1093/ije/dyv316 CrossRefPubMedGoogle Scholar
  23. 23.
    Baik I, Kim J, Abbott RD, Joo S, Jung K, Lee S, Shim J, In K, Kang K, Yoo S, Shin C (2008) Association of snoring with chronic bronchitis. Arch Intern Med 168(2):167–173.  https://doi.org/10.1001/archinternmed.2007.8 CrossRefPubMedGoogle Scholar
  24. 24.
    Willett W (2013) Nutritional epidemiology, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  25. 25.
    Ahn Y, Kwon E, Shim JE, Park MK, Joo Y, Kimm K, Park C, Kim DH (2007) Validation and reproducibility of food frequency questionnaire for Korean genome epidemiologic study. Eur J Clin Nutr 61(12):1435–1441.  https://doi.org/10.1038/sj.ejcn.1602657 CrossRefPubMedGoogle Scholar
  26. 26.
    Baik I, Lee M, Jun NR, Lee JY, Shin C (2013) A healthy dietary pattern consisting of a variety of food choices is inversely associated with the development of metabolic syndrome. Nutr Res Pract 7(3):233–241.  https://doi.org/10.4162/nrp.2013.7.3.233 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Parr CL, Hjartaker A, Scheel I, Lund E, Laake P, Veierod MB (2008) Comparing methods for handling missing values in food-frequency questionnaires and proposing k nearest neighbours imputation: effects on dietary intake in the Norwegian Women and Cancer study (NOWAC). Public Health Nutr 11(4):361–370.  https://doi.org/10.1017/s1368980007000365 CrossRefPubMedGoogle Scholar
  28. 28.
    National Rural Living Science Institute (1996) Food composition table, 5th edn. Rural Development Administration, Suwon KoreaGoogle Scholar
  29. 29.
    Pate RR, Pratt M, Blair SN, Haskell WL, Macera CA, Bouchard C, Buchner D, Ettinger W, Heath GW, King AC (1995) Physical activity and public health: a recommendation from the Centers for Disease Control and Prevention and the American College of Sports Medicine. JAMA 273(5):402–407.  https://doi.org/10.1001/jama.1995.03520290054029 CrossRefPubMedGoogle Scholar
  30. 30.
    World Health Organization (2000) The Asia–Pacific perspective: redefining obesity and its treatment. http://www.wpro.who.int/nutrition/documents/Redefining_obesity/en/. Accessed 8 Dec 2017
  31. 31.
    Chen GC, Lv DB, Pang Z, Liu QF (2013) Red and processed meat consumption and risk of stroke: a meta-analysis of prospective cohort studies. Eur J Clin Nutr 67(1):91–95.  https://doi.org/10.1038/ejcn.2012.180 CrossRefPubMedGoogle Scholar
  32. 32.
    Fretts AM, Follis JL, Nettleton JA, Lemaitre RN, Ngwa JS, Wojczynski MK, Kalafati IP, Varga TV, Frazier-Wood AC, Houston DK, Lahti J, Ericson U, van den Hooven EH, Mikkila V, Kiefte-de Jong JC, Mozaffarian D, Rice K, Renstrom F, North KE, McKeown NM, Feitosa MF, Kanoni S, Smith CE, Garcia ME, Tiainen AM, Sonestedt E, Manichaikul A, van Rooij FJ, Dimitriou M, Raitakari O, Pankow JS, Djousse L, Province MA, Hu FB, Lai CQ, Keller MF, Perala MM, Rotter JI, Hofman A, Graff M, Kahonen M, Mukamal K, Johansson I, Ordovas JM, Liu Y, Mannisto S, Uitterlinden AG, Deloukas P, Seppala I, Psaty BM, Cupples LA, Borecki IB, Franks PW, Arnett DK, Nalls MA, Eriksson JG, Orho-Melander M, Franco OH, Lehtimaki T, Dedoussis GV, Meigs JB, Siscovick DS (2015) Consumption of meat is associated with higher fasting glucose and insulin concentrations regardless of glucose and insulin genetic risk scores: a meta-analysis of 50,345 Caucasians. Am J Clin Nutr 102(5):1266–1278.  https://doi.org/10.3945/ajcn.114.101238 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Kurotani K, Nanri A, Goto A, Mizoue T, Noda M, Oba S, Kato M, Matsushita Y, Inoue M, Tsugane S (2013) Red meat consumption is associated with the risk of type 2 diabetes in men but not in women: a Japan Public Health Center-Based Prospective Study. Br J Nutr 110(10):1910–1918.  https://doi.org/10.1017/s0007114513001128 CrossRefPubMedGoogle Scholar
  34. 34.
    van Woudenbergh GJ, Kuijsten A, Tigcheler B, Sijbrands EJ, van Rooij FJ, Hofman A, Witteman JC, Feskens EJ (2012) Meat consumption and its association with C-reactive protein and incident type 2 diabetes: the Rotterdam Study. Diabetes Care 35(7):1499–1505.  https://doi.org/10.2337/dc11-1899 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Steinbrecher A, Erber E, Grandinetti A, Kolonel LN, Maskarinec G (2011) Meat consumption and risk of type 2 diabetes: the Multiethnic Cohort. Public Health Nutr 14(4):568–574.  https://doi.org/10.1017/s1368980010002004 CrossRefPubMedGoogle Scholar
  36. 36.
    Bernstein AM, Pan A, Rexrode KM, Stampfer M, Hu FB, Mozaffarian D, Willett WC (2012) Dietary protein sources and the risk of stroke in men and women. Stroke 43(3):637–644.  https://doi.org/10.1161/strokeaha.111.633404 CrossRefPubMedGoogle Scholar
  37. 37.
    Villegas R, Shu XO, Gao Y-T, Yang G, Cai H, Li H, Zheng W (2006) The association of meat intake and the risk of type 2 diabetes may be modified by body weight. Int J Med Sci 3(4):152CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Feskens EJ, Sluik D, van Woudenbergh GJ (2013) Meat consumption, diabetes, and its complications. Curr Diabetes Rep 13(2):298–306.  https://doi.org/10.1007/s11892-013-0365-0 CrossRefGoogle Scholar
  39. 39.
    Yang C, Pan L, Sun C, Xi Y, Wang L, Li D (2016) Red meat consumption and the risk of stroke: a dose–response meta-analysis of prospective cohort studies. J Stroke Cerebrovasc Dis Off J Natl Stroke Assoc 25(5):1177–1186.  https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.01.040 CrossRefGoogle Scholar
  40. 40.
    Garfinkle MA (2017) Salt and essential hypertension: pathophysiology and implications for treatment. J Am Soc Hypertens 11(6):385–391.  https://doi.org/10.1016/j.jash.2017.04.006 CrossRefPubMedGoogle Scholar
  41. 41.
    Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87(1):315–424.  https://doi.org/10.1152/physrev.00029.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Forstermann U (2008) Oxidative stress in vascular disease: causes, defense mechanisms and potential therapies. Nat Clin Pract Cardiovasc Med 5(6):338–349.  https://doi.org/10.1038/ncpcardio1211 CrossRefPubMedGoogle Scholar
  43. 43.
    Heaney RP (2014) Guidelines for optimizing design and analysis of clinical studies of nutrient effects. Nutr Rev 72(1):48–54.  https://doi.org/10.1111/nure.12090 CrossRefPubMedGoogle Scholar
  44. 44.
    Pan A, Sun Q, Bernstein AM, Schulze MB, Manson JE, Stampfer MJ, Willett WC, Hu FB (2012) Red meat consumption and mortality: results from 2 prospective cohort studies. Arch Intern Med 172(7):555–563.  https://doi.org/10.1001/archinternmed.2011.2287 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Daniel CR, Cross AJ, Koebnick C, Sinha R (2011) Trends in meat consumption in the USA. Public Health Nutr 14(4):575–583.  https://doi.org/10.1017/s1368980010002077 CrossRefPubMedGoogle Scholar
  46. 46.
    Kang M, Joung H, Lim J, Lee Y, Song Y (2011) Secular trend in dietary patterns in a Korean adult population, using the 1998, 2001, and 2005 Korean National Health and Nutrition Examination Survey. (Secular Trend in Dietary Patterns in a Korean Adult Population, Using the 1998, 2001, and 2005 Korean National Health and Nutrition Examination Survey). Korean J Nutr 44(2):152–161.  https://doi.org/10.4163/kjn.2011.44.2.152 CrossRefGoogle Scholar
  47. 47.
    Korea Rural Economic Institute (2015) Consumption trend of food processing products and consumption activation plan. Korea Rural Economic Institute. Available via Nuri media. http://www.dbpia.co.kr/Article/NODE06597572. Accessed 27 Mar 2017
  48. 48.
    Brown JE, Lechtenberg E, Splett PL (2016) Nutrition through the life cycle, 6th edn. Cengage Learning, BostonGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Food and NutritionYeungnam UniversityGyeongsanRepublic of Korea

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