Nonalcoholic fatty liver disease is associated with an increased risk of heart block in hospitalized patients with type 2 diabetes mellitus

PLoS ONE

Volumn 12, Issue 10, 2017, Pages

  Mantovani, Alessandro ^a   Rigolon, Riccardo ^a   Pichiri, Isabella ^a   Bonapace, Stefano ^b   Morani, Giovanni ^a   Zoppini, Giacomo ^a   Bonora, Enzo ^a   Targher, Giovanni ^a  

^a UNIVERSITY HOSPITAL OF VERONA   (Italy)

^b SACRO CUORE DON CALABRIA HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACARBOSE; DIPEPTIDYL PEPTIDASE IV INHIBITOR; GLITAZONE DERIVATIVE; GLUCAGON LIKE PEPTIDE 1 DERIVATIVE; HEMOGLOBIN A1C; INSULIN; METFORMIN; SULFONYLUREA;

ADULT; AGE; AGED; ARTICLE; COHORT ANALYSIS; COMPLETE HEART BLOCK; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; DISEASE SEVERITY ASSESSMENT; ECHOGRAPHY; ELECTROCARDIOGRAPHY; FEMALE; FIBROSIS 4 SCORE; FIRST DEGREE ATRIOVENTRICULAR BLOCK; HEART LEFT ANTERIOR BUNDLE BRANCH BLOCK; HEART LEFT BUNDLE BRANCH BLOCK; HEART LEFT POSTERIOR BUNDLE BRANCH BLOCK; HEART RIGHT BUNDLE BRANCH BLOCK; HEMOGLOBIN BLOOD LEVEL; HOSPITAL PATIENT; HUMAN; HYPERTENSION; ISCHEMIC HEART DISEASE; LIVER FIBROSIS; MAJOR CLINICAL STUDY; MALE; MICROANGIOPATHY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; PREVALENCE; RETROSPECTIVE STUDY; SECOND DEGREE ATRIOVENTRICULAR BLOCK; SEX; COMPLICATION; DIAGNOSTIC IMAGING; HEART BLOCK; HOSPITALIZATION; LIVER; MIDDLE AGED; PATHOPHYSIOLOGY; RISK FACTOR;

AGED; DIABETES MELLITUS, TYPE 2; ELECTROCARDIOGRAPHY; FEMALE; HEART BLOCK; HOSPITALIZATION; HUMANS; INPATIENTS; LIVER; MALE; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; RETROSPECTIVE STUDIES; RISK FACTORS; ULTRASONOGRAPHY;

EID: 85030723783     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0185459     Document Type: Article

References (34)

1. 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; 64:73–84. https://doi.org/10.1002/hep.28431 PMID: 26707365
2. 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; 47:997–1006. https://doi.org/10.1016/j.dld.2015.08.004 PMID: 26454786
3. Adams LA, Anstee QM, Tilg H, Targher G. Non-alcoholic fatty liver disease and its relationship with cardiovascular disease and other extra-hepatic diseases. Gut 2017; 66:1138–1153. https://doi.org/10.1136/gutjnl-2017-313884 PMID: 28314735
4. Targher G, Day CP, Bonora E. Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med 2010; 363:1341–1350. https://doi.org/10.1056/NEJMra0912063 PMID: 20879883
5. Targher G, Byrne CD, Lonardo A, Zoppini G, Barbui C. Nonalcoholic fatty liver disease and risk of incident cardiovascular disease: a meta-analysis. J Hepatol 2016; 65:589–600. https://doi.org/10.1016/j.jhep.2016.05.013 PMID: 27212244
6. EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. European Association for the Study of the Liver (EASL); European Association for the Study of Diabetes (EASD); European Association for the Study of Obesity (EASO). J Hepatol 2016; 64:1388–1402. https://doi.org/10.1016/j.jhep.2015.11.004 PMID: 27062661
7. Mantovani A, Ballestri S, Lonardo A, Targher G. Cardiovascular disease and myocardial abnormalities in nonalcoholic fatty liver disease. Dig Dis Sci 2016; 61:1246–1267. https://doi.org/10.1007/s10620-016-4040-6 PMID: 26809873
8. Targher G, Mantovani A, Pichiri I, Rigolon R, Dauriz M, Zoppini G, et al. Non-alcoholic fatty liver disease is associated with an increased prevalence of atrial fibrillation in hospitalized patients with type 2 diabetes. Clin Sci (Lond) 2013; 125:301–309.
9. Targher G, Valbusa F, Bonapace S, Bertolini L, Zenari L, Rodella S, et al. Non-alcoholic fatty liver disease is associated with an increased incidence of atrial fibrillation in patients with type 2 diabetes. PLoS One 2013; 8:e57183. https://doi.org/10.1371/journal.pone.0057183 PMID: 23451184
10. Käräjämäki A, Pätsi OP, Savolainen M, Kesäniemi YA, Huikuri HV, Ukkola O. Non-alcoholic fatty liver disease as a predictor of atrial fibrillation in middle-aged population (OPERA study). PLoS One 2015; 10:e0142937. https://doi.org/10.1371/journal.pone.0142937 PMID: 26571029
11. Targher G, Valbusa F, Bonapace S, Bertolini L, Zenari L, Pichiri I, et al. Association of nonalcoholic fatty liver disease with QTc interval in patients with type 2 diabetes. Nutr Metab Cardiovasc Dis 2014; 24:663–669. https://doi.org/10.1016/j.numecd.2014.01.005 PMID: 24594085
12. Hung CS, Tseng PH, Tu CH, Chen CC, Liao WC, Lee YC, et al. Nonalcoholic fatty liver disease is associated with QT prolongation in the general population. J Am Heart Assoc 2015; 4:e001820. https://doi.org/10.1161/JAHA.115.001820 PMID: 26199227
13. Mantovani A, Rigamonti A, Bonapace S, Bolzan B, Pernigo M, Morani G, et al. Non-alcoholic fatty liver disease is associated with ventricular arrhythmias in patients with type 2 diabetes referred for clinically indicated 24-hour Holter monitoring. Diabetes Care 2016; 39:1416–1423. https://doi.org/10.2337/dc16-0091 PMID: 27222503
14. Mangi MA, Minhas AM, Rehman H, Pathan F, Liang H, Beidas S. Association of non-alcoholic fatty liver disease with conduction defects on electrocardiogram. Cureus. 2017; 9:e1107. https://doi.org/10.7759/cureus.1107 PMID: 28439482
15. Pokorney SD, Radder C, Schulte PJ, Al-Khatib SM, Tricocci P, Van de Werf F, et al. High-degree atrio-ventricular block, asystole, and electro-mechanical dissociation complicating non-ST-segment elevation myocardial infarction. Am Heart J 2016; 171:25–32. https://doi.org/10.1016/j.ahj.2015.09.004PMID: 26699597
16. Coumbe AG, Naksuk N, Newell MC, Somasundaram PE, Benditt DG, Adabag S. Long-term follow-up of older patients with Mobitz type I second degree atrio-ventricular block. Heart 2013; 99:334–338. https://doi.org/10.1136/heartjnl-2012-302770 PMID: 23086974
17. Bussink BE, Holst AG, Jespersen L, Deckers JW, Jensen GB, Prescott E. Right bundle branch block: prevalence, risk factors, and outcome in the general population: results from the Copenhagen City Heart Study. Eur Heart J 2013; 34:138–146. https://doi.org/10.1093/eurheartj/ehs291 PMID: 22947613
18. Cheng S, Keyes MJ, Larson MG, McCabe EL, Newton-Cheh C, Levy D, et al. Long-term outcomes in individuals with prolonged PR interval or first-degree atrio-ventricular block. JAMA 2009; 301:2571–2577. https://doi.org/10.1001/jama.2009.888 PMID: 19549974
19. Kwok CS, Rashid M, Beynon R, Barker D, Patwala A, Morley-Davies A, et al. Prolonged PR interval, first-degree heart block and adverse cardiovascular outcomes: a systematic review and meta-analysis. Heart 2016; 102:672–680. https://doi.org/10.1136/heartjnl-2015-308956 PMID: 26879241
20. Castera L, Vilgrain V, Angulo P. Noninvasive evaluation of NAFLD. Nat Rev Gastroenterol Hepatol 2013; 10:666–675. https://doi.org/10.1038/nrgastro.2013.175 PMID: 24061203
21. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, et al; CKD-EPI (Chronic Kidney Disease Epidemiology Collaboration). A new equation to estimate glomerular filtration rate. Ann Intern Med 2009; 150:604–612. PMID: 19414839
22. Targher G, Zoppini G, Mantovani W, Chonchol M, Negri C, Stoico V, et al. Comparison of two creatinine-based estimating equations in predicting all-cause and cardiovascular mortality in patients with type 2 diabetes. Diabetes Care 2012; 35:2347–2353. https://doi.org/10.2337/dc12-0259 PMID: 22837367
23. McPherson S, Hardy T, Dufour JF, Petta S, Romero-Gomez M, Allison M, et al. Age as a confounding factor for the accurate non-invasive diagnosis of advanced NAFLD fibrosis. Am J Gastroenterol 2017; 112:740–751. https://doi.org/10.1038/ajg.2016.453 PMID: 27725647
24. The Minnesota code manual of electrocardiographic findings: standards and procedures for ECG measurement in epidemiologic and clinical trials. Prineas RJ, Crow RS, Zhang ZM, Eds. 2nd Edition. London: Springer-Verlag, 2010.
25. Hernaez R, Lazo M, Bonekamp S, Kamel I, Brancati FL, Guallar E, et al. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis. Hepatology 2011; 54:1082–1090. https://doi.org/10.1002/hep.24452 PMID: 21618575
26. Lonardo A, Sookoian A, Pirola CJ, Targher G. Non-alcoholic fatty liver disease and risk of cardiovascular disease. Metabolism 2016; 65:1136–1150. https://doi.org/10.1016/j.metabol.2015.09.017 PMID: 26477269
27. Bonapace S, Perseghin G, Molon G, Canali G, Bertolini L, Zoppini G, et al. Nonalcoholic fatty liver disease is associated with left ventricular diastolic dysfunction in patients with type 2 diabetes. Diabetes Care 2012; 35:389–395. https://doi.org/10.2337/dc11-1820 PMID: 22210573
28. Hallsworth K, Hollingsworth KG, Thoma C, Jakovljevic D, MacGowan GA, Anstee QM, et al. Cardiac structure and function are altered in adults with non-alcoholic fatty liver disease. J Hepatol 2013; 58:757–762. https://doi.org/10.1016/j.jhep.2012.11.015 PMID: 23178979
29. VanWagner LB, Wilcox JE, Colangelo LA, Lloyd-Jones DM, Carr JJ, Lima JA, et al. Association of nonalcoholic fatty liver dis- ease with subclinical myocardial remodeling and dysfunction: a population-based study. Hepatology 2015; 62:773–783. https://doi.org/10.1002/hep.27869 PMID: 25914296
30. Mantovani A, Pernigo M, Bergamini C, Bonapace S, Lipari P, Valbusa F, et al. Heart valve calcification in patients with type 2 diabetes and nonalcoholic fatty liver disease. Metabolism 2015; 64:879–887. https://doi.org/10.1016/j.metabol.2015.04.003 PMID: 25957758
31. Liu YC, Hung CS, Wu YW, Lee YC, Lin YH, Lin C, et al. Influence of non-alcoholic fatty liver disease on autonomic changes evaluated by the time domain, frequency domain, and symbolic dynamics of heart rate variability. PLoS One 2013; 8:e61803. https://doi.org/10.1371/journal.pone.0061803 PMID: 23626730
32. Kuehl M, Stevens MJ. Cardiovascular autonomic neuropathies as complications of diabetes mellitus. Nat Rev Endocrinol 2012; 8:405–416. https://doi.org/10.1038/nrendo.2012.21 PMID: 22371159
33. Byrne CD, Targher G. Time to replace assessment of liver histology with MR-based imaging tests to assess efficacy of interventions for nonalcoholic fatty liver disease. Gastroenterology 2016; 150:7–10. https://doi.org/10.1053/j.gastro.2015.11.016 PMID: 26602219
34. Park CC, Nguyen P, Hernandez C, Bettencourt R, Ramirez K, Fortney L, et al. Magnetic resonance elastography vs. transient elastography in detection of fibrosis and noninvasive measurement of steatosis in patients with biopsy-proven nonalcoholic fatty liver disease. Gastroenterology 2017; 152:598–607. https://doi.org/10.1053/j.gastro.2016.10.026 PMID: 27911262