BioMed Research International / 2015 / Article / Tab 1

Review Article

Association of Nonalcoholic Fatty Liver Disease with Subclinical Cardiovascular Changes: A Systematic Review and Meta-Analysis

Table 1

(a) Studies of the association between nonalcoholic fatty liver disease and alterations in cardiac structure and function in the adult population included in the meta-analysis. (b) Studies on the association between nonalcoholic fatty liver disease and alterations in cardiac structure and function in children and adolescents included in the meta-analysis.
(a)

Author/
country/
year [reference]
Study design, population, and sample sizeDiagnosisOutcomesMain resultsCommentNOS score

Goland et al./ 
Israel/
2006 [25]
Cross-sectional.
Nondiabetic, normotensive patients with NAFLD () and age- and sex-matched healthy controls ().
NAFLD patients included those with metabolic syndrome.
Liver ultrasound and liver biopsy in a subgroup of 11 NAFLD patients.LV structure and function (M-mode echocardiography; pulsed and tissue Doppler echocardiography).Patients with NAFLD had mild changes in cardiac geometry (thickening of the interventricular septum and posterior wall and increased LV mass) as well as significant differences in parameters of diastolic function compared with the control group.All data were adjusted for BMI.
On multivariate regression analysis, including all the metabolic and echocardiographic variables, on TDI was the only independent parameter associated with NAFLD.
7

Fallo et al./
Italy/
2009 [30]
Cross-sectional.
Never-treated essential hypertensive patients with () or without () fatty liver. The 2 groups were similar as to sex, age, and blood pressure levels.
Liver ultrasound.LV structure and function (M-mode echocardiography and pulsed Doppler echocardiography).NAFLD patients had similar prevalence of LV hypertrophy compared to subjects without NAFLD, but a higher prevalence of LV diastolic dysfunction.Multivariate logistic regression analysis showed that HOMA-IR and diastolic dysfunction remained independently associated with NAFLD.7

Fotbolcu et al./
Turkey/
2010 [26]
Cross-sectional.
Nondiabetic, normotensive patients with NAFLD () and control subjects (). The 2 groups were similar as to sex and age.
Liver ultrasound.LV structure and function (M-mode echocardiography and pulsed and tissue Doppler echocardiography).Patients with NAFLD had changes in cardiac geometry (thickening of the interventricular septum and posterior wall and increased LV mass) as well as significant differences in parameters of systolic and diastolic function compared with the control group.No correlation was found between BMI and waist circumference and and on TDI.7

Bonapace et al./
Italy/
2012 [31]
Cross-sectional.
T2DM patients with () and without () fatty liver. The 2 groups were similar as to sex, age, BMI, waist circumference, and diabetes duration.
Liver ultrasound.LV structure and function (M-mode echocardiography and pulsed and tissue Doppler echocardiography).T2DM patients with fatty liver showed LV diastolic dysfunction, even if the LV morphology and systolic function were preserved.LV dysfunction remained significant after adjustment for hypertension and other cardiometabolic risk factors.8

Karabay et al./
Turkey/
2014 [32]
Cross-sectional.
NAFLD patients ( and healthy controls (; normal laboratory values and liver ultrasound).
Of the 55 NAFLD patients, 9 had simple steatosis, 24 borderline NASH, and 22 definite NASH.
Liver biopsy.LV structure and function (M-mode echocardiography, pulsed and tissue Doppler echocardiography, and speckle tracking echocardiography).Patients with NAFLD and its subgroups had changes in cardiac geometry (thickening of the interventricular septum and posterior wall and increased LV mass) as well as significant differences in parameters of diastolic function compared with the control group.Speckle tracking echocardiography showed no differences in strain between subgroup patients (simple steatosis versus borderline NASH versus definite NASH).7

Kim et al./
Korea/
2014 [33]
Population-based.
Cohort included in the Korean Genome and Epidemiology study: NAFLD patients without MetS (); NAFLD patients with MetS (); NO NAFLD without MetS (); NO NAFLD with MetS ().
Liver computed tomography.LV structure and function (M-mode echocardiography and pulsed and tissue Doppler echocardiography).Compared with subjects with neither NAFLD nor MetS, those with both disorders showed the most significant differences in structural and functional LV parameters, such as LV mass index, transmitral Doppler indices, and systolic/diastolic TDI values.In multivariate analyses, NAFLD and MetS were each significantly and independently associated with TDI velocity.7

T2DM: type 2 diabetes mellitus; BMI: body mass index; HOMA-IR: homeostasis model assessment of insulin resistance; MetS: metabolic syndrome; NAFLD: nonalcoholic fatty liver disease; LV: left ventricular; NASH: nonalcoholic steatohepatitis; NOS: Newcastle-Ottawa Scale; TDI: tissue Doppler imaging.
(b)

Authors/
country/
year [reference]
Study design, population, and sample sizeDiagnosisOutcomesMain resultsCommentsNOS score

Alp et al./
Turkey/
2013 [34]
Cross-sectional.
Obese children and adolescents with () and without () NAFLD matched for gender and age and control subjects ().
Of the 93 NAFLD children, 67 had ultrasonographic grade 1 steatosis and 26 had grade 2 steatosis.
Liver ultrasound.LV structure and function; epicardial fat (M-mode echocardiography and pulsed and tissue Doppler echocardiography).Increased end-systolic thickness of the interventricular septum and larger LV mass, as well as LV systolic and diastolic dysfunction, were found in NAFLD group. In addition, obese children with NAFLD had increased epicardial fat thickness.On logistic regression analysis including anthropometric and metabolic variables, total adipose tissue mass percentage and IVSs were the only independent parameters associated with liver steatosis.8

Sert et al./
Turkey/
2013 [35]
Cross-sectional.
Obese adolescents with () and without () NAFLD and control subjects ().
Liver ultrasound and elevated serum alanine aminotransferase.LV structure and function (M-mode echocardiography and pulsed and tissue Doppler echocardiography).Obese adolescents with NAFLD exhibited increased LV dimensions and mass, as well as LV diastolic dysfunction.7

Pacifico et al./
Italy/
2014 [29]
Cross-sectional.
Obese children and adolescents with () and without ()
NAFLD matched for age, gender, Tanner stage, and BMI-SD score and healthy control subjects () matched for gender, age, and pubertal status.
Hepatic magnetic resonance imaging and liver biopsy in a subgroup of 41 NAFLD patients (26 had definite NASH and 15 were not-NASH).LV structure and function; epicardial fat (M-mode echocardiography and pulsed and tissue Doppler echocardiography).Increased interventricular septum thickness at end-diastole and at end-systole, as well as LV systolic and diastolic dysfunction, was found in NAFLD group. Children with more severe liver histology had worse LV dysfunction than those with more mild liver changes. NAFLD group had also increased epicardial fat thickness.Patients with definite NASH had significantly lower velocity and significantly higher -to- and Tei index (, resp.) than those without NASH. In multiple logistic regression analysis, NAFLD was the only statistically significant variable associated with increased -to- ratio, whereas NAFLD and systolic blood pressure were significantly associated with increased Tei index.8

NAFLD: nonalcoholic fatty liver disease; LV: left ventricular; BMI: body mass index; NASH: nonalcoholic steatohepatitis; NOS: Newcastle-Ottawa Scale.

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