DOI QR코드

DOI QR Code

Correlation between shift work and non-alcoholic fatty liver disease among male workers in the steel manufacturing company of Korea: a cross-sectional study

  • Kiseok Kim (Department of Occupational and Environmental Medicine, Soonchunhyang University Cheonan Hospital) ;
  • Yong-Jin Lee (Department of Occupational and Environmental Medicine, Soonchunhyang University Cheonan Hospital) ;
  • Soon-Chan Kwon (Department of Occupational and Environmental Medicine, Soonchunhyang University Cheonan Hospital) ;
  • Young-Sun Min (Department of Occupational and Environmental Medicine, Soonchunhyang University Cheonan Hospital) ;
  • Hyun Kyo Lee (Department of Occupational and Environmental Medicine, Soonchunhyang University Cheonan Hospital) ;
  • Gwangin Baek (Department of Occupational and Environmental Medicine, Soonchunhyang University Cheonan Hospital) ;
  • Sang Hyeon Kim (Department of Occupational and Environmental Medicine, Soonchunhyang University Cheonan Hospital) ;
  • Eun-Chul Jang (Department of Occupational and Environmental Medicine, Soonchunhyang University Cheonan Hospital)
  • Received : 2022.06.01
  • Accepted : 2022.10.12
  • Published : 2022.12.31

Abstract

Background: Circadian rhythm disturbance caused by shift work has adverse effects on the metabolic homeostasis of the liver. Disruption of the metabolic homeostasis of the liver causes fat accumulation in the liver. The aim of this study was to investigate the correlation between shift work and non-alcoholic fatty liver disease (NAFLD) among male workers in the steel manufacturing industry of Korea. Methods: Based on medical examination data collected in June 2020, 2,511 male subjects from one steel manufacturing company in Korea were selected in total. NAFLD was evaluated using abdominal ultrasound, which was performed by two experienced radiologists. The multinomial logistic regression analysis was performed by adjusting for age, physical activity, smoking history, alcohol consumption, body mass index, waist circumference, blood pressure, blood glucose, lipidemia, liver function test, employment duration, and hepatotoxic materials exposure status. Results: Compared to daytime workers, the odds ratio (OR) of moderate-severe NAFLD in shift workers was 1.449 (95% confidence interval [CI], 1.028-2.043). Compared to daytime workers, the ORs of moderate-severe NAFLD were significantly higher for the group that engaged in total shift work for more than 20 years (OR, 2.285; 95% CI, 1.051-4.970), the group that was not allowed to sleep during night shift work (OR, 1.463; 95% CI, 1.030-2.078), and the group that consumed food during night shift work (OR, 1.580; 95% CI, 1.093-2.284). Conclusions: There was a correlation between shift work and moderate-severe NAFLD in male steel manufacturing workers. There will be a need for more research related to the correlation of shift work with steatohepatitis and cirrhosis in the future.

Keywords

Acknowledgement

We would like to thank Harrisco (www.harrisco.net) for English language editing.

References

  1. Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, et al. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American Association for the Study of Liver Diseases. Hepatology 2018;67(1):328-57.  https://doi.org/10.1002/hep.29367
  2. Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 2016;64(1):73-84.  https://doi.org/10.1002/hep.28431
  3. Le MH, Yeo YH, Li X, Li J, Zou B, Wu Y, et al. 2019 Global NAFLD prevalence: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. Forthcoming 2021. 
  4. Li J, Zou B, Yeo YH, Feng Y, Xie X, Lee DH, et al. Prevalence, incidence, and outcome of non-alcoholic fatty liver disease in Asia, 1999-2019: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol 2019;4(5):389-98. https://doi.org/10.1016/S2468-1253(19)30039-1
  5. Im HJ, Ahn YC, Wang JH, Lee MM, Son CG. Systematic review on the prevalence of nonalcoholic fatty liver disease in South Korea. Clin Res Hepatol Gastroenterol 2021;45(4):101526. 
  6. Paik JM, Henry L, De Avila L, Younossi E, Racila A, Younossi ZM. Mortality related to nonalcoholic fatty liver disease is increasing in the United States. Hepatol Commun 2019;3(11):1459-71.  https://doi.org/10.1002/hep4.1419
  7. Ahmed A, Wong RJ, Harrison SA. Nonalcoholic fatty liver disease review: diagnosis, treatment, and outcomes. Clin Gastroenterol Hepatol 2015;13(12):2062-70.  https://doi.org/10.1016/j.cgh.2015.07.029
  8. Younossi ZM, Otgonsuren M, Henry L, Venkatesan C, Mishra A, Erario M, et al. Association of nonalcoholic fatty liver disease (NAFLD) with hepatocellular carcinoma (HCC) in the United States from 2004 to 2009. Hepatology 2015;62(6):1723-30.  https://doi.org/10.1002/hep.28123
  9. Wickwire EM, Geiger-Brown J, Scharf SM, Drake CL. Shift work and shift work sleep disorder: clinical and organizational perspectives. Chest 2017;151(5):1156-72.  https://doi.org/10.1016/j.chest.2016.12.007
  10. Manohar S, Thongprayoon C, Cheungpasitporn W, Mao MA, Herrmann SM. Associations of rotational shift work and night shift status with hypertension: a systematic review and meta-analysis. J Hypertens 2017;35(10):1929-37.  https://doi.org/10.1097/HJH.0000000000001442
  11. Gan Y, Yang C, Tong X, Sun H, Cong Y, Yin X, et al. Shift work and diabetes mellitus: a meta-analysis of observational studies. Occup Environ Med 2015;72(1):72-8.  https://doi.org/10.1136/oemed-2014-102150
  12. Dutheil F, Baker JS, Mermillod M, De Cesare M, Vidal A, Moustafa F, et al. Shift work, and particularly permanent night shifts, promote dyslipidaemia: a systematic review and meta-analysis. Atherosclerosis 2020;313:156-69.  https://doi.org/10.1016/j.atherosclerosis.2020.08.015
  13. Puttonen S, Harma M, Hublin C. Shift work and cardiovascular disease - pathways from circadian stress to morbidity. Scand J Work Environ Health 2010;36(2):96-108.  https://doi.org/10.5271/sjweh.2894
  14. Saran AR, Dave S, Zarrinpar A. Circadian rhythms in the pathogenesis and treatment of fatty liver disease. Gastroenterology 2020;158(7):1948-1966.e1.  https://doi.org/10.1053/j.gastro.2020.01.050
  15. Zhang S, Wang Y, Wang Z, Wang H, Xue C, Li Q, et al. Rotating night shift work and non-alcoholic fatty liver disease among steelworkers in China: a cross-sectional survey. Occup Environ Med 2020;77(5):333-9.  https://doi.org/10.1136/oemed-2019-106220
  16. Choi H, Oh HJ, Shin JS, Lim M, Kim SK, Kang HT, et al. Relationship between shift work and liver enzymes: a cross-sectional study based on the Korea National Health and Examination Survey (2007- 2015). Ann Occup Environ Med 2019;31(1):e15. 
  17. Kang SH, Lee HW, Yoo JJ, Cho Y, Kim SU, Lee TH, et al. KASL clinical practice guidelines: management of nonalcoholic fatty liver disease. Clin Mol Hepatol 2021;27(3):363-401.  https://doi.org/10.3350/cmh.2021.0178
  18. Bull FC, Al-Ansari SS, Biddle S, Borodulin K, Buman MP, Cardon G, et al. World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br J Sports Med 2020;54(24):1451-62.  https://doi.org/10.1136/bjsports-2020-102955
  19. Lee SY, Park HS, Kim DJ, Han JH, Kim SM, Cho GJ, et al. Appropriate waist circumference cutoff points for central obesity in Korean adults. Diabetes Res Clin Pract 2007;75(1):72-80.  https://doi.org/10.1016/j.diabres.2006.04.013
  20. Seo MH, Lee WY, Kim SS, Kang JH, Kang JH, Kim KK, et al. 2018 Korean society for the study of obesity guideline for the management of obesity in Korea. J Obes Metab Syndr 2019;28(1):40-5.  https://doi.org/10.7570/jomes.2019.28.1.40
  21. Lee HY, Shin J, Kim GH, Park S, Ihm SH, Kim HC, et al. 2018 Korean Society of Hypertension guidelines for the management of hypertension: part II-diagnosis and treatment of hypertension. Clin Hypertens 2019;25(1):20.
  22. Hur KY, Moon MK, Park JS, Kim SK, Lee SH, Yun JS, et al. 2021 clinical practice guidelines for diabetes mellitus of the Korean Diabetes Association. Diabetes Metab J 2021;45(4):461-81. https://doi.org/10.4093/dmj.2021.0156
  23. Rhee EJ, Kim HC, Kim JH, Lee EY, Kim BJ, Kim EM, et al. 2018 guidelines for the management of dyslipidemia in Korea. J Lipid Atheroscler 2019;8(2):78-131.  https://doi.org/10.12997/jla.2019.8.2.78
  24. Ministry of Employment and Labor. Enforcement Regulations of Occupational Safety and Health Act. https://www.law.go.kr/LSW//admRulBylInfoPLinkR.do?admRulSeq=2100000212249&admRulNm=%EA%B1%B4%EA%B0%95%EA%B2%80%EC%A7%84%20%EC%8B%A4%EC%8B%9C%EA%B8%B0%EC%A4%80&bylNo=0004&bylBrNo=00&bylCls=BE&bylClsCd=BE&joEfYd=&bylEfYd=. Updated 2022. Accessed July 25, 2022.
  25. Korean Association for the Study of the Liver (KASL). KASL clinical practice guidelines: management of alcoholic liver disease. Clin Mol Hepatol 2013;19(3):216-54.  https://doi.org/10.3350/cmh.2013.19.3.216
  26. Lee S, Kim JS, Jung JG, Oh MK, Chung TH, Kim J. Korean alcohol guidelines for moderate drinking based on facial flushing. Korean J Fam Med 2019;40(4):204-11.  https://doi.org/10.4082/kjfm.19.0059
  27. Ministry of Employment and Labor. Enforcement Regulations of Occupational Safety and Health Act. https://www.law.go.kr/LSW//lsBylInfoPLinkR.do?lsiSeq=212709&lsNm=%EC%82%B0%EC%97%85%EC%95%88%EC%A0%84%EB%B3%B4%EA%B1%B4%EB%B2%95+%EC%8B%9C%ED%96%89%EA%B7%9C%EC%B9%99&bylNo=0022&bylBrNo=00&bylCls=BE&bylEfYd=20200116&bylEfYdYn=Y. Updated 2021. Accessed April 5, 2022.
  28. Wahlang B, Beier JI, Clair HB, Bellis-Jones HJ, Falkner KC, McClain CJ, et al. Toxicant-associated steatohepatitis. Toxicol Pathol 2013;41(2):343-60.  https://doi.org/10.1177/0192623312468517
  29. Korean Industrial Health Association. https://kiha21.or.kr/doc_download/night_ko_2018.pdf. Updated 2018. Accessed July 25, 2022.
  30. Ferraioli G, Soares Monteiro LB. Ultrasound-based techniques for the diagnosis of liver steatosis. World J Gastroenterol 2019;25(40):6053-62.  https://doi.org/10.3748/wjg.v25.i40.6053
  31. Younossi ZM. Non-alcoholic fatty liver disease - a global public health perspective. J Hepatol 2019;70(3):531-44.  https://doi.org/10.1016/j.jhep.2018.10.033
  32. Wu KT, Kuo PL, Su SB, Chen YY, Yeh ML, Huang CI, et al. Nonalcoholic fatty liver disease severity is associated with the ratios of total cholesterol and triglycerides to high-density lipoprotein cholesterol. J Clin Lipidol 2016;10(2):420-5.e1.  https://doi.org/10.1016/j.jacl.2015.12.026
  33. Lonardo A, Bellentani S, Argo CK, Ballestri S, Byrne CD, Caldwell SH, et al. Epidemiological modifiers of non-alcoholic fatty liver disease: Focus on high-risk groups. Dig Liver Dis 2015;47(12):997-1006.  https://doi.org/10.1016/j.dld.2015.08.004
  34. Hong HC, Hwang SY, Choi HY, Yoo HJ, Seo JA, Kim SG, et al. Relationship between sarcopenia and nonalcoholic fatty liver disease: the Korean Sarcopenic Obesity Study. Hepatology 2014;59(5):1772-8.  https://doi.org/10.1002/hep.26716
  35. Chung GE, Lee Y, Yim JY, Choe EK, Kwak MS, Yang JI, et al. Genetic polymorphisms of PNPLA3 and SAMM50 are associated with nonalcoholic fatty liver disease in a Korean population. Gut Liver 2018;12(3):316-23.  https://doi.org/10.5009/gnl17306
  36. Guo Z, Li M, Han B, Qi X. Association of non-alcoholic fatty liver disease with thyroid function: a systematic review and meta-analysis. Dig Liver Dis 2018;50(11):1153-62.  https://doi.org/10.1016/j.dld.2018.08.012
  37. Adams LA, Feldstein A, Lindor KD, Angulo P. Nonalcoholic fatty liver disease among patients with hypothalamic and pituitary dysfunction. Hepatology 2004;39(4):909-14.  https://doi.org/10.1002/hep.20140
  38. Chung JH. Evaluation of thyroid hormone levels and urinary iodine concentrations in Koreans based on the data from Korea National Health and Nutrition Examination Survey VI (2013 to 2015). Endocrinol Metab (Seoul) 2018;33(2):160-3.  https://doi.org/10.3803/EnM.2018.33.2.160
  39. Kim SY. Diagnosis and treatment of hypopituitarism. Endocrinol Metab (Seoul) 2015;30(4):443-55. https://doi.org/10.3803/EnM.2015.30.4.443
  40. Zisapel N. Circadian rhythm sleep disorders: pathophysiology and potential approaches to management. CNS Drugs 2001;15(4):311-28. https://doi.org/10.2165/00023210-200115040-00005
  41. Mukherji A, Bailey SM, Staels B, Baumert TF. The circadian clock and liver function in health and disease. J Hepatol 2019;71(1):200-11.  https://doi.org/10.1016/j.jhep.2019.03.020
  42. Wei T, Li C, Heng Y, Gao X, Zhang G, Wang H, et al. Association between night-shift work and level of melatonin: systematic review and meta-analysis. Sleep Med 2020;75:502-9.  https://doi.org/10.1016/j.sleep.2020.09.018
  43. Wei Y, Rector RS, Thyfault JP, Ibdah JA. Nonalcoholic fatty liver disease and mitochondrial dysfunction. World J Gastroenterol 2008;14(2):193-9.  https://doi.org/10.3748/wjg.14.193
  44. Solis-Munoz P, Solis-Herruzo JA, Fernandez-Moreira D, Gomez-Izquierdo E, Garcia-Consuegra I, MunozYague T, et al. Melatonin improves mitochondrial respiratory chain activity and liver morphology in ob/ob mice. J Pineal Res 2011;51(1):113-23.  https://doi.org/10.1111/j.1600-079X.2011.00868.x
  45. Lee SI, Nishi T, Takahashi M, Higuchi S. Effects of 2-hour nighttime nap on melatonin concentration and alertness during 12-hour simulated night work. Ind Health 2021;59(6):393-402.  https://doi.org/10.2486/indhealth.2020-0245
  46. Lowden A, Moreno C, Holmback U, Lennernas M, Tucker P. Eating and shift work - effects on habits, metabolism and performance. Scand J Work Environ Health 2010;36(2):150-62.  https://doi.org/10.5271/sjweh.2898
  47. Hampton SM, Morgan LM, Lawrence N, Anastasiadou T, Norris F, Deacon S, et al. Postprandial hormone and metabolic responses in simulated shift work. J Endocrinol 1996;151(2):259-67.  https://doi.org/10.1677/joe.0.1510259
  48. Bugianesi E, McCullough AJ, Marchesini G. Insulin resistance: a metabolic pathway to chronic liver disease. Hepatology 2005;42(5):987-1000.  https://doi.org/10.1002/hep.20920
  49. Musso G, Gambino R, Cassader M, Pagano G. Meta-analysis: natural history of non-alcoholic fatty liver disease (NAFLD) and diagnostic accuracy of non-invasive tests for liver disease severity. Ann Med 2011;43(8):617-49.  https://doi.org/10.3109/07853890.2010.518623
  50. Angulo P, Kleiner DE, Dam-Larsen S, Adams LA, Bjornsson ES, Charatcharoenwitthaya P, et al. Liver fibrosis, but no other histologic features, is associated with long-term outcomes of patients with nonalcoholic fatty liver disease. Gastroenterology 2015;149(2):389-397.e10. https://doi.org/10.1053/j.gastro.2015.04.043