Association between High-Sensitive C-Reactive Protein and the Development of Liver Damage in Japanese Male Workers
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Measurements
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Kunutsor, S.K.; Apekey, T.A.; Khan, H. Liver enzymes and risk of cardiovascular disease in the general population: A meta-analysis of prospective cohort studies. Atherosclerosis 2014, 236, 7–17. [Google Scholar] [CrossRef]
- Kunutsor, S.K.; Apekey, T.A.; Walley, J. Liver Aminotransferases and Risk of Incident Type 2 Diabetes: A Systematic Review and Meta-Analysis. Am. J. Epidemiol. 2013, 178, 159–171. [Google Scholar] [CrossRef] [Green Version]
- Saito, T.; Nishise, Y.; Makino, N.; Haga, H.; Ishii, R.; Okumoto, K.; Ito, J.; Watanabe, H.; Saito, K.; Takeda, H.; et al. Impact of metabolic syndrome on elevated serum alanine aminotransferase levels in the Japanese population. Metab. Clin. Exp. 2009, 58, 1067–1075. [Google Scholar] [CrossRef]
- Chen, S.C.-C.; Tsai, S.P.; Jhao, J.-Y.; Jiang, W.-K.; Tsao, C.K.; Chang, L.-Y. Liver Fat, Hepatic Enzymes, Alkaline Phosphatase and the Risk of Incident Type 2 Diabetes: A Prospective Study of 132,377 Adults. Sci. Rep. 2017, 7, 1–9. [Google Scholar] [CrossRef]
- Aneni, E.C.; Oni, E.T.; Martin, S.S.; Blaha, M.J.; Agatston, A.S.; Feldman, T.; Veledar, E.; Conceicao, R.D.; Carvalho, J.A.M.; Santos, R.D.; et al. Blood pressure is associated with the presence and severity of nonalcoholic fatty liver disease across the spectrum of car-diometabolic risk. J. Hypertens. 2015, 33, 1207–1214. [Google Scholar] [CrossRef] [PubMed]
- Loomba, R.; Sanyal, A.J. The global NAFLD epidemic. Nat. Rev. Gastroenterol. Hepatol. 2013, 10, 686–690. [Google Scholar] [CrossRef] [PubMed]
- Devaraj, S.; Singh, U.; Jialal, I. Human C-reactive protein and the metabolic syndrome. Curr. Opin. Lipidol. 2009, 20, 182–189. [Google Scholar] [CrossRef] [Green Version]
- Ridker, P.; Silvertown, J. Inflammation, C-reactive protein, and atherothrombosis. J. Periodontol. 2008, 79, 1544–1551. [Google Scholar] [CrossRef] [Green Version]
- Hotamisligil, G.S. Inflammation and metabolic disorders. Nat. Cell Biol. 2006, 444, 860–867. [Google Scholar] [CrossRef]
- van Dijk, E.J.; Prins, N.D.; Vermeer, S.E.; Vrooman, H.A.; Hofman, A.; Koudstaal, P.J.; Breteler, M.M.B. C-reactive protein and cerebral small-vessel disease: The rotterdam scan study. Circulation 2005, 112, 900–905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Danesh, J.; Wheeler, J.G.; Hirschfield, G.M.; Eda, S.; Eiriksdottir, G.; Rumley, A.; Lowe, G.D.; Pepys, M.B.; Gudnason, V. C-Reactive Protein and Other Circulating Markers of Inflammation in the Prediction of Coronary Heart Disease. N. Engl. J. Med. 2004, 350, 1387–1397. [Google Scholar] [CrossRef]
- Pepys, M.B.; Hirschfield, G.M. C-reactive protein: A critical update. J. Clin. Investig. 2003, 111, 1805–1812. [Google Scholar] [CrossRef]
- Yeniova, A.O.; Küçükazman, M.; Ata, N.; Dal, K.; Kefeli, A.; Başyiğit, S.; Aktaş, B.; Ağladioğlu, K.; Akin, K.O.; Ertugrul, D.T.; et al. High-sensitivity C-reactive protein is a strong predictor of non-alcoholic fatty liver disease. Hepatogastroenterology 2014, 61, 422–425. [Google Scholar]
- Ndumele, C.E.; Nasir, K.; Conceiçao, R.D.; Carvalho, J.A.M.; Blumenthal, R.S.; Santos, R.D. Hepatic Steatosis, Obesity, and the Metabolic Syndrome Are Independently and Additively Associated with Increased Systemic Inflammation. Arter. Thromb. Vasc. Biol. 2011, 31, 1927–1932. [Google Scholar] [CrossRef] [Green Version]
- Yoneda, M.; Mawatari, H.; Fujita, K.; Iida, H.; Yonemitsu, K.; Kato, S.; Takahashi, H.; Kirikoshi, H.; Inamori, M.; Nozaki, Y.; et al. High-sensitivity C-reactive protein is an independent clinical feature of nonalcoholic steatohepatitis (NASH) and also of the severity of fibrosis in NASH. J. Gastroenterol. 2007, 42, 573–582. [Google Scholar] [CrossRef] [PubMed]
- Park, S.H.; Kim, B.I.; Yun, J.W.; Kim, J.W.; Park, D.I.; Cho, Y.K.; Sung, I.K.; Park, C.Y.; Sohn, C.I.; Jeon, W.K.; et al. Insulin resistance and C-reactive protein as independent risk factors for non-alcoholic fatty liver disease in non-obese Asian men. J. Gastroenterol. Hepatol. 2004, 19, 694–698. [Google Scholar] [CrossRef]
- Sunto, A.; Mochizuki, K.; Miyauchi, R.; Misaki, Y.; Shimada, M.; Kasezawa, N.; Tohyama, K.; Goda, T. Serum gamma-GTP Activity Is Closely Associated with Serum CRP Levels in Non-Overweight and Overweight Middle-Aged Japanese Men. J. Nutr. Sci. Vitaminol. 2013, 59, 108–114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leiva, E.; Mujica, V.; Palomo, I.; Orrego, R.; Guzmán, L.; Núñez, S.; Moore-Carrasco, R.; Icaza, G.; Diaz, N. High-sensitivity C-reactive protein and liver enzymes in individuals with Metabolic Syndrome in Talca, Chile. Exp. Ther. Med. 2009, 1, 175–179. [Google Scholar] [CrossRef] [PubMed]
- Browning, L.M.; Krebs, J.D.; Siervo, M.; Hall, R.M.; Finer, N.; Allison, M.E.; Jebb, S.A. Inflammation is associated with liver function markers, independent of other metabolic risk factors in overweight women. Br. J. Diabetes Vasc. Dis. 2008, 8, 73–76. [Google Scholar] [CrossRef]
- Kazumi, T.; Yoshino, G.; Kawaguchi, A.; Hirano, T. Serum Alanine Aminotransferase is Associated with Serum Adiponectin, C-reactive Protein and Apolipoprotein B in Young Healthy Men. Horm. Metab. Res. 2006, 38, 119–124. [Google Scholar] [CrossRef]
- Kerner, A.; Avizohar, O.; Sella, R.; Bartha, P.; Zinder, O.; Markiewicz, W.; Levy, Y.; Brook, G.J.; Aronson, D. Association between elevated liver enzymes and C-reactive protein: Possible hepatic contribution to systemic inflammation in the metabolic syndrome. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 193–197. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, D.; Jacobs, D.R., Jr. Association between serum gamma-glutamyltransferase and C-reactive protein. Atherosclerosis 2005, 178, 327–330. [Google Scholar] [CrossRef]
- Sattar, N.; Scherbakova, O.; Ford, I.; O’Reilly, D.S.J.; Stanley, A.; Forrest, E.; Macfarlane, P.W.; Packard, C.J.; Cobbe, S.M.; Shepherd, J. Elevated Alanine Aminotransferase Predicts New-Onset Type 2 Diabetes Independently of Classical Risk Factors, Metabolic Syndrome, and C-Reactive Protein in the West of Scotland Coronary Prevention Study. Diabetes 2004, 53, 2855–2860. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luyendyk, J.P.; Guo, G.L. Steatosis DeLIVERs High-Sensitivity C-Reactive Protein. Arter. Thromb. Vasc. Biol. 2011, 31, 1714–1715. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, J.; Yoon, K.; Ryu, S.; Chang, Y.; Kim, H.-R. High-normal levels of hs-CRP predict the development of non-alcoholic fatty liver in healthy men. PLoS ONE 2017, 12, e0172666. [Google Scholar] [CrossRef]
- Morimoto, H.; Sakata, K.; Oishi, M.; Tanaka, K.; Nakada, S.; Nogawa, K.; Suwazono, Y. Effect of high-sensitivity C-reactive protein on the development of diabetes as demonstrated by pooled logistic-regression analysis of annual health-screening information from male Japanese workers. Diabetes Metab. 2013, 39, 27–33. [Google Scholar] [CrossRef]
- Siest, G.; Schiele, F.; Galteau, M.; Panek, E.; Steinmetz, J.; Fagnani, F.; Gueguen, R. Aspartate aminotransferase and alanine ami-notransferase activities in plasma: Statistical distributions, individual variations, and reference values. Clin. Chem. 1975, 21, 1077–1087. [Google Scholar] [CrossRef]
- Pratt, D.S.; Kaplan, M.M. Evaluation of Abnormal Liver-Enzyme Results in Asymptomatic Patients. N. Engl. J. Med. 2000, 342, 1266–1271. [Google Scholar] [CrossRef]
- Rifai, N.; Tracy, R.P.; Ridker, P.M. Clinical efficacy of an automated high-sensitivity C-reactive protein assay. Clin. Chem. 1999, 45, 2136–2141. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meaney, E.; Alva, F.; Moguel, R.; Meaney, A.; Alva, J.; Webel, R. Formula and nomogram for the sphygmomanometric calculation of the mean arterial pressure. Heart 2000, 84, 64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kato, M. A Research Report Concerning Stress and Its Effects on Health in Workplace, Ministry of Health, Labor and Welfare, “Study on Prevention of Work-Related Diseases”; Preventive Medicine and Public Health Tokyo & Tokyo Medical University: Tokyo, Japan, 2000. (In Japanese) [Google Scholar]
- D’Agostino, R.B.; Lee, M.; Belanger, A.J.; Cupples, L.A.; Anderson, K.; Kannel, W.B. Relation of pooled logistic regression to time de-pendent cox regression analysis: The framingham heart study. Stat. Med. 1990, 9, 1501–1515. [Google Scholar] [CrossRef]
- Verrijken, A.; Francque, S.; Mertens, I.; Talloen, M.; Peiffer, F.; Van Gaal, L. Visceral adipose tissue and inflammation correlate with elevated liver tests in a cohort of overweight and obese patients. Int. J. Obes. 2010, 34, 899–907. [Google Scholar] [CrossRef] [Green Version]
- Clark, J.M.; Brancati, F.L.; Diehl, A.M. The prevalence and etiology of elevated aminotransferase levels in the united states. Am. J. Gastroenterol. 2003, 98, 960–967. [Google Scholar] [CrossRef] [PubMed]
- Ioannou, G.N.; Boyko, E.J.; Lee, S.P. The Prevalence and Predictors of Elevated Serum Aminotransferase Activity in the United States in 1999-2002. Am. J. Gastroenterol. 2006, 101, 76–82. [Google Scholar] [CrossRef] [PubMed]
- Daniel, S.; Ben-Menachem, T.; Vasudevan, G.; Ma, C.K.; Blumenkehl, M. Prospective evaluation of unexplained chronic liver transaminase abnormalities in asymptomatic and symptomatic patients. Am. J. Gastroenterol. 1999, 94, 3010–3014. [Google Scholar] [CrossRef] [PubMed]
- Motegi, S.; Nishizaki, Y.; Shiozawa, H.; Higashi, T.; Aoki, J.; Matsuzaki, S.; Kuwahira, I.; Kashihara, H.; Tamura, M.; Ogawa, T.; et al. Study on Causes and Ratio of the Liver Function Abnormalities in General Health Check-up. Health Eval. Promot. 2010, 37, 484–489. [Google Scholar] [CrossRef] [Green Version]
- Ogawa, W.; Kasuga, M. Cell signaling: Fat Stress and Liver Resistance. Science 2008, 322, 1483–1484. [Google Scholar] [CrossRef]
- Wieckowska, A.; Papouchado, B.G.; Li, Z.; Lopez, R.; Zein, N.N.; Feldstein, A.E. Increased Hepatic and Circulating Interleukin-6 Levels in Human Nonalcoholic Steatohepatitis. Am. J. Gastroenterol. 2008, 103, 1372–1379. [Google Scholar] [CrossRef]
- Anty, R.; Bekri, S.; Luciani, N.; Saint-Paul, M.; Dahman, M.; Iannelli, A.; Amor, I.B.; Staccini-Myx, A.; Huet, P.; Gugenheim, J.; et al. The inflammatory C-reactive protein is increased in both liver and adipose tissue in se-verely obese patients independently from metabolic syndrome, type 2 diabetes, and NASH. Am. J. Gastroenterol. 2006, 101, 1824–1833. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.; Mei, M.; Yang, S.; Li, Q. Roles of Chronic Low-Grade Inflammation in the Development of Ectopic Fat Deposition. Mediat. Inflamm. 2014, 2014, 1–7. [Google Scholar] [CrossRef]
- Eguchi, Y.; Eguchi, T.; Mizuta, T.; Ide, Y.; Yasutake, T.; Iwakiri, R.; Hisatomi, A.; Ozaki, I.; Yamamoto, K.; Kitajima, Y.; et al. Visceral fat accumulation and insulin resistance are important factors in nonalcoholic fatty liver disease. J. Gastroenterol. 2006, 41, 462–469. [Google Scholar] [CrossRef]
- Maximos, M.; Bril, F.; Sanchez, P.P.; Lomonaco, R.; Orsak, B.; Biernacki, D.; Suman, A.; Weber, M.; Cusi, K. The role of liver fat and insulin resistance as determinants of plasma aminotransferase elevation in nonalcoholic fatty liver disease. Hepatology 2015, 61, 153–160. [Google Scholar] [CrossRef] [PubMed]
- Morisco, F.; Stroffolini, T.; Mele, A.; Taliani, G.; Smedile, A.; Caronna, S.; Tosti, M.E.; Niro, G.; Levrero, M.; Fiorillo, M.T.; et al. Etiology of and risk factors for transient and persistent aminotransferase elevation in a population of virus-free blood donors: A multicentre study. Dig. Liver Dis. 2010, 42, 441–445. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, A.; Angulo, P.; Lymp, J.; St. Sauver, J.; Muto, A.; Okada, T.; Lindor, K. Chronological development of elevated aminotrans-ferases in a nonalcoholic population. Hepatology 2005, 41, 64–71. [Google Scholar] [CrossRef]
- Ruhl, C.E.; Everhart, J.E. Joint Effects of Body Weight and Alcohol on Elevated Serum Alanine Aminotransferase in the United States Population. Clin. Gastroenterol. Hepatol. 2005, 3, 1260–1268. [Google Scholar] [CrossRef]
- Becker, U.; Deis, A.; Sorensen, T.I.; Gronbaek, M.; Borch-Johnsen, K.; Muller, C.F.; Schnohr, P.; Jensen, G. Prediction of risk of liver disease by alcohol intake, sex, and age: A prospective population study. Hepatology 1996, 23, 1025–1029. [Google Scholar] [CrossRef]
- Dong, M.H.; Bettencourt, R.; Brenner, D.A.; Barrett-Connor, E.; Loomba, R. Serum levels of alanine aminotransferase decrease with age in longitudinal analysis. Clin. Gastroenterol. Hepatol. 2012, 10, 285–290.e1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tanaka, J.; Koyama, T.; Mizui, M.; Uchida, S.; Katayama, K.; Matsuo, J.; Akita, T.; Nakashima, A.; Miyakawa, Y.; Yoshizawa, H. Total Numbers of Undiagnosed Carriers of Hepatitis C and B Viruses in Japan Estimated by Age- and Area-Specific Prevalence on the National Scale. Intervirology 2011, 54, 185–195. [Google Scholar] [CrossRef]
- Kwo, P.Y.; Cohen, S.M.; Lim, J.K. ACG Clinical Guideline: Evaluation of Abnormal Liver Chemistries. Am. J. Gastroenterol. 2017, 112, 18–35. [Google Scholar] [CrossRef] [PubMed]
Variables | Mean (Standard Deviation) |
---|---|
Age (y) | 45.1 (12.0) |
Body mass index (kg/m2) | 23.8 (3.2) |
Systolic blood pressure (mmHg) | 129.8 (13.1) |
Diastolic blood pressure (mmHg) | 78.9 (8.9) |
Mean blood pressure (mmHg) | 95.9 (9.6) |
Alcohol consumption (gou */day) | 0.75 (0.85) |
Geometric mean (Geometric standard deviation) | |
C-reactive protein (mg/dL) | 0.05 (2.9) |
Aspartate aminotransferase (IU/L) | 21.1 (1.3) |
High-density lipoprotein cholesterol (mg/dL) | 52.9 (1.3) |
HbA1c (%) | 5.3 (1.1) |
Creatinine (mg/dL) | 0.8 (1.2) |
Uric acid (mg/dL) | 5.7 (1.3) |
Rate (%) | |
Job Schedule type | |
Daytime | 61.1% |
3-shiftwork | 32.1% |
2-shiftwork | 5.2% |
Others | 1.6% |
Smoking | |
Nonsmoker | 46.3% |
Smoker | 53.7% |
Habitual exercise | |
None | 37.6% |
once-twice/month | 18.9% |
once-twice/week | 26.9% |
3–4 times/week | 10.4% |
5 times/week or more | 6.2% |
Meals | |
Cooked by oneself | 6.0% |
Cooked by family | 81.0% |
Eating out or catering | 6.0% |
Eating in a dormitory | 6.2% |
Others | 0.8% |
Soft drink consumption | |
Rare | 28.0% |
Occasional | 46.3% |
Frequent | 25.6% |
In-between snacking | |
Rare | 41.2% |
Occasional | 50.7% |
Frequent | 8.0% |
Brief Job Stress Questionnaire | |
Job demand (High) | 43.7% |
Job control (Low) | 38.4% |
Interpersonal relationship (Low) | 17.6% |
Compatibility (Low) | 19.7% |
Data Items | Men |
---|---|
Number of subjects examined | 7830 |
Number of subjects who developed liver damage | 800 |
(%) | 10.2 |
Total person-years of observation | 23,215 |
Incidence rate per 1000 person years | 34.5 |
Mean observed years per person | 2.96 |
Men | ||
---|---|---|
Independent Variables | OR * (95% CI †) | p |
C-reactive protein | 1.07 (1.03, 1.10) | <0.001 |
Age (+1 y) | 0.99 (0.98, 0.99) | <0.001 |
Alcohol consumption (+1 gou/day) | 1.46 (1.35, 1.59) | <0.001 |
Body mass index (+1 kg/m2) | 1.10 (1.07, 1.13) | <0.001 |
Mean blood pressure (+10 mmHg) | 1.16 (1.06, 1.26) | 0.001 |
High-density lipoprotein cholesterol | 0.87 (0.76, 0.99) | 0.034 |
Meals (/Cooked by family ‡) | ||
Cooking by oneself | 1.39 (1.07, 1.80) | 0.014 |
Eating out or catering | 0.89 (0.65, 1.21) | 0.459 |
Eating in a dormitory | 0.86 (0.59, 1.26) | 0.436 |
Others | 1.68 (0.84, 3.36) | 0.141 |
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Kuroda, R.; Nogawa, K.; Watanabe, Y.; Morimoto, H.; Sakata, K.; Suwazono, Y. Association between High-Sensitive C-Reactive Protein and the Development of Liver Damage in Japanese Male Workers. Int. J. Environ. Res. Public Health 2021, 18, 2985. https://doi.org/10.3390/ijerph18062985
Kuroda R, Nogawa K, Watanabe Y, Morimoto H, Sakata K, Suwazono Y. Association between High-Sensitive C-Reactive Protein and the Development of Liver Damage in Japanese Male Workers. International Journal of Environmental Research and Public Health. 2021; 18(6):2985. https://doi.org/10.3390/ijerph18062985
Chicago/Turabian StyleKuroda, Reiko, Kazuhiro Nogawa, Yuuka Watanabe, Hideki Morimoto, Kouichi Sakata, and Yasushi Suwazono. 2021. "Association between High-Sensitive C-Reactive Protein and the Development of Liver Damage in Japanese Male Workers" International Journal of Environmental Research and Public Health 18, no. 6: 2985. https://doi.org/10.3390/ijerph18062985