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Liver stiffness measurement identifies subclinical myocardial dysfunction in non-advanced non-alcoholic fatty liver disease patients without overt heart disease

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Abstract

Patients with non-advanced non-alcoholic fatty liver disease (NAFLD) have an increased cardiovascular risk. The present study was designed to evaluate the relationship between liver stiffness measurement (LSM) by transient elastography (TE) and myocardial deformation indices of all cardiac chambers in NAFLD patients without overt heart disease. All consecutive NAFLD patients diagnosed with LSM < 12.5 kPa on TE between September 2021 and December 2021 entered the study. All participants underwent blood tests, TE and two-dimensional (2D) transthoracic echocardiography (TTE) implemented with speckle-tracking echocardiography (STE) analysis of left ventricular (LV) global longitudinal strain (GLS), global circumferential strain (GCS) and global radial strain (GRS), right ventricular (RV) GLS, left atrial (LA) total global strain (TGSA) and right atrial (RA) TGSA. Main independent predictors of impaired LV-GLS (defined as absolute value less negative than − 20%) were evaluated. A total of 92 NAFLD patients (54.0 ± 11.1 years, 50% males) were prospectively analyzed. Mean LSM was 6.2 ± 2.4 kPa. Fibroscan results revealed that 76.1% of patients had F0-F1, 5.4% F2 and 18.5% F3 liver fibrosis. Despite normal biventricular systolic function on 2D-TTE, LV-GLS, LV-GCS and LV-GRS, RV-GLS, LA-TGSA and RA-TGSA were reduced in 64.1%, 38.0%, 38.0%, 31.5%, 39.1% and 41.3% of patients, respectively. Body mass index (BMI) (OR 1.76, 95% CI 1.18–2.64), neutrophil-to-lymphocyte ratio (NLR) (OR 4.93, 95% CI 1.15–31.8) and LSM (OR 9.26, 95% CI 2.24–38.3) were independently associated to impaired LV-GLS. BMI ≥ 29.3 kg/m2, NLR ≥ 1.8 and LSM ≥ 5.5 kPa were the best cut-off values for detecting outcome. LSM ≥ 5.5 kPa identifies NAFLD patients with subclinical myocardial dysfunction.

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Abbreviations

2D:

Two-dimensional

ALP:

Alkaline phosphatase

ALT:

Alanine aminotransferase

AST:

Aspartate aminotransferase

BMI:

Body mass index

CAP:

Controlled attenuation parameter

CI:

Confidence interval

CO:

Cardiac output

DBP:

Diastolic blood pressure

EaI:

Arterial elastance index

EAT:

Epicardial adipose tissue

EesI:

End-systolic elastance index

eGFR:

Estimated glomerular filtration rate

ESP:

End-systolic pressure

GCS:

Global circumferential strain

GGT:

Gamma-glutamyl transferase

GLS:

Global longitudinal strain

GRS:

Global radial strain

GSA + :

Positive global atrial strain

GSA-:

Negative global atrial strain

HDL:

High-density lipoprotein

HFpEF:

Heart failure with preserved ejection fraction

ICC:

Intraclass correlation coefficient

INR:

International normalized ratio

IQR:

Interquartile range

IVC:

Inferior vena cava

LA:

Left atrial

LAVi:

Left atrial volume index

LDL:

Low-density lipoprotein

LV:

Left ventricular

LVFP:

Left ventricular fillimng pressure

LSM:

Liver stiffness measurement

LVEDVi:

Left ventricular end-diastolic volume index

LVESVi:

Left ventricular end-systolic volume index

LVEF:

Left ventricular ejection fraction

LVMi:

Left ventricular mass index

LVOT:

Left ventricular outflow tract

MACE:

Major adverse cardiovascular events

MAP:

Mean arterial pressure

MAPSE:

Mitral annular plane systolic excursion

NAFLD:

Non-alcoholic fatty liver disease

NLR:

Neutrophil-to-lymphocyte ratio

NPV:

Negative predictive value

OR:

Odds ratio

PPV:

Positive predictive value

RA:

Right atrial

RDW:

Red cell distribution width

ROC:

Receiver operating characteristics

RV:

Right ventricular

RWT:

Relative wall thickness

SBP:

Systolic blood pressure

SPAP:

Systolic pulmonary artery pressure

STE:

Speckle-tracking echocardiography

SVi:

Stroke volume index

TAPSE:

Tricuspid annular plane systolic excursion

TE:

Transient elastography

TGSA:

Total global atrial strain

TPRi:

Total peripheral resistance index

TTE:

Transthoracic echocardiography

VAC:

Ventricular arterial coupling

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Funding

This work has been supported by Italian Ministry of Health Ricerca Corrente—IRCCS MultiMedica.

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Authors and Affiliations

  1. Division of Cardiology, Ospedale San Giuseppe MultiMedica IRCCS, Via San Vittore 12, 20123, Milan, Italy

    Andrea Sonaglioni, Elisabetta Rigamonti & Michele Lombardo

  2. Division of Hepatology, Ospedale San Giuseppe MultiMedica IRCCS, Via San Vittore 12, 20123, Milan, Italy

    Federica Cerini, Antonio Cerrone, Lorenzo Argiento, Maria Grazia Rumi & Mauro Viganò

  3. University of Milan, Milan, Italy

    Federica Cerini, Antonio Cerrone, Lorenzo Argiento, Maria Grazia Rumi & Mauro Viganò

  4. Division of Cardiology, Policlinico San Giorgio, Pordenone, Italy

    Gian Luigi Nicolosi

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  1. Andrea Sonaglioni
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  2. Federica Cerini
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  3. Antonio Cerrone
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  4. Lorenzo Argiento
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Contributions

AS: conceptualization; data curation; investigation; methodology; software; visualization; writing—original draft. FC, AC, LA, ER: conceptualization; data curation; methodology. GLN, ML, MGR, MV: conceptualization; supervision; validation; writing—review and editing.

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Correspondence to Andrea Sonaglioni.

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We wish to confirm that there are no conflicts of interest associated with this publication. Andrea Sonaglioni declares that he has no conflict of interest. Federica Cerini declares that she has no conflict of interest. Antonio Cerrone declares that he has no conflict of interest. Lorenzo Argiento declares that he has no conflict of interest. Gian Luigi Nicolosi declares that he has no conflict of interest. Elisabetta Rigamonti declares that she has no conflict of interest. Michele Lombardo declares that he has no conflict of interest. Maria Grazia Rumi declares that she has no conflict of interest. Mauro Viganò declares that he has no conflict of interest.

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Sonaglioni, A., Cerini, F., Cerrone, A. et al. Liver stiffness measurement identifies subclinical myocardial dysfunction in non-advanced non-alcoholic fatty liver disease patients without overt heart disease. Intern Emerg Med 17, 1425–1438 (2022). https://doi.org/10.1007/s11739-022-02966-2

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