Advertisement

Fatty liver index is associated to pulse wave velocity in healthy subjects: Data from the Brisighella Heart Study

  • Author Footnotes
    1 These authors equally contributed to the manuscript.
    Arrigo F.G. Cicero
    Correspondence
    Corresponding author at: Atherosclerosis Research Unit, Medical and Surgical Sciences Department, Sant'Orsola-Malpighi Hospital - University of Bologna, Via Albertoni, 15, 40138 Bologna, Italy.
    Footnotes
    1 These authors equally contributed to the manuscript.
    Affiliations
    Atherosclerosis Research Unit, Department of Medical and Surgical Sciences, University of Bologna and Azienda Ospedaliero-Universitaria di Bologna, Policlinico Sant'Orsola Malpighi, Bologna, Italy
    Search for articles by this author
  • Author Footnotes
    1 These authors equally contributed to the manuscript.
    Stefano Gitto
    Footnotes
    1 These authors equally contributed to the manuscript.
    Affiliations
    ITEC Unit, Department of Medical and Surgical Sciences, University of Bologna and Azienda Ospedaliero-Universitaria di Bologna, Policlinico Sant'Orsola Malpighi, Bologna, Italy

    Research Center for the Study of Hepatitis, Department of Medical and Surgical Sciences, University of Bologna, Italy
    Search for articles by this author
  • Federica Fogacci
    Affiliations
    Atherosclerosis Research Unit, Department of Medical and Surgical Sciences, University of Bologna and Azienda Ospedaliero-Universitaria di Bologna, Policlinico Sant'Orsola Malpighi, Bologna, Italy
    Search for articles by this author
  • Martina Rosticci
    Affiliations
    Atherosclerosis Research Unit, Department of Medical and Surgical Sciences, University of Bologna and Azienda Ospedaliero-Universitaria di Bologna, Policlinico Sant'Orsola Malpighi, Bologna, Italy
    Search for articles by this author
  • Marina Giovannini
    Affiliations
    Atherosclerosis Research Unit, Department of Medical and Surgical Sciences, University of Bologna and Azienda Ospedaliero-Universitaria di Bologna, Policlinico Sant'Orsola Malpighi, Bologna, Italy
    Search for articles by this author
  • Sergio D'Addato
    Affiliations
    Atherosclerosis Research Unit, Department of Medical and Surgical Sciences, University of Bologna and Azienda Ospedaliero-Universitaria di Bologna, Policlinico Sant'Orsola Malpighi, Bologna, Italy
    Search for articles by this author
  • Pietro Andreone
    Affiliations
    ITEC Unit, Department of Medical and Surgical Sciences, University of Bologna and Azienda Ospedaliero-Universitaria di Bologna, Policlinico Sant'Orsola Malpighi, Bologna, Italy

    Research Center for the Study of Hepatitis, Department of Medical and Surgical Sciences, University of Bologna, Italy
    Search for articles by this author
  • Claudio Borghi
    Affiliations
    Atherosclerosis Research Unit, Department of Medical and Surgical Sciences, University of Bologna and Azienda Ospedaliero-Universitaria di Bologna, Policlinico Sant'Orsola Malpighi, Bologna, Italy
    Search for articles by this author
  • for the Brisighella Heart Study Group Medical and Surgical Sciences Dept., University of Bologna
    Author Footnotes
    2 Arrigo F.G. Cicero, Martina Rosticci, Federica Fogacci, Enrico Bertagnin, Elisa Grandi, Sergio D’Addato, Silvia Palmesano, Ilaria Ricci Iamino, Fulvio Ventura, Federico Verardi, Marina Giovannini, Elisabetta Rizzoli, Giuseppe Derosa, Stefano Bacchelli, Claudio Borghi.
  • Author Footnotes
    1 These authors equally contributed to the manuscript.
    2 Arrigo F.G. Cicero, Martina Rosticci, Federica Fogacci, Enrico Bertagnin, Elisa Grandi, Sergio D’Addato, Silvia Palmesano, Ilaria Ricci Iamino, Fulvio Ventura, Federico Verardi, Marina Giovannini, Elisabetta Rizzoli, Giuseppe Derosa, Stefano Bacchelli, Claudio Borghi.
Published:March 24, 2018DOI:https://doi.org/10.1016/j.ejim.2018.03.010

      Highlights

      • Fatty liver has to be considered the expression of a metabolic systemic disease.
      • HSI, FLI, LAP and Serum Uric Acid might be predictors of AS in healthy subjects.
      • Indirect indexes of fatty liver can be useful tools for cardiovascular assessment.

      Abstract

      Background

      Non-Alcoholic Fatty Liver Disease (NAFLD) is associated to increased risk of cardiovascular disease. Our aim was to evaluate association of indexes of fatty liver with arterial stiffness (AS).

      Methods

      We analyzed data of adult volunteers visited during the last Brisighella survey. We evaluated the Pulse Wave Velocity (PWV) and the following non-invasive indexes of liver steatosis: Fatty Liver Index (FLI), Lipid Accumulation Product (LAP), Hepatic Steatosis Index (HSI). We compared patients according to the risk of Non-Alcoholic Steatohepatitis (NASH): low-risk (BMI < 28 and no diabetes), intermediate-risk (BMI ≥ 28 or diabetes), high-risk (BMI ≥ 28 and diabetes). Multiple Linear Regression analysis was assessed for predictors of AS.

      Results

      We studied 1731 volunteers. In subjects with low metabolic risk, HSI (RR = 0.138, 95%CI 0.105–0.170, p < 0.001), FLI (RR = 0.024, 95%CI 0.016–0.032, p < 0.001), LAP (RR = 0.014, 95%CI 0.008–0.020, p < 0.001) and Serum Uric Acid (RR = 0.150, 95%CI 0.024–0.275, p = 0.019) were significant predictors of AS. HSI and FLI emerged as predictors of PWV in intermediate risk group (RR = 0.116, 95%CI 0.071–0.160, p < 0.001; RR = 0.010, 95%CI 0.001–0.020, p = 0.041). In volunteers with high risk, FLI and Uric Acid were related to PWV (RR = 0.049, 95%CI 0.011–0.087, p = 0.013; RR = 0.632, 95% CI 0.222–1.041, p = 0.003).

      Conclusion

      Fatty liver indirect indexes were associated to AS in subjects with different metabolic risk profiles.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to European Journal of Internal Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Vernon G.
        • Baranova A.
        • Younossi Z.M.
        Systematic review: The epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults.
        Aliment Pharmacol Ther. 2011; 34: 274-285
        • 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)
        EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease.
        J Hepatol. 2016; 64: 1388-1402https://doi.org/10.1016/j.jhep.2015.11.004
        • Younossi Z.M.
        • Stepanova M.
        • Negro F.
        • Hallaji S.
        • Younossi Y.
        • Lam B.
        • et al.
        Nonalcoholic fatty liver disease in lean individuals in the United States.
        Medicine. 2012; 91: 319-327
        • Ratziu V.
        • Bellentani S.
        • Cortez-Pinto H.
        • Day C.
        • Marchesini G.
        A position statement on NAFLD/NASH based on the EASL 2009 special conference.
        J Hepatol. 2010; 53: 372-384
        • Kim J.A.
        • Montagnani M.
        • Koh K.K.
        • Quon M.J.
        Reciprocal relationships between insulin resistance and endothelial dysfunction: Molecular and pathophysiological mechanisms.
        Circulation. 2006; 113: 1888-1904
        • Bedogni G.
        • Bellentani S.
        • Miglioli L.
        • Masutti F.
        • Passalacqua M.
        • Castiglione A.
        • et al.
        The fatty liver index: A simple and accurate predictor of hepatic steatosis in the general population.
        BMC Gastroenterol. 2006; 6: 33
        • Koehler E.M.
        • Schouten J.N.
        • Hansen B.E.
        • Hofman A.
        • Stricker B.H.
        • Janssen H.L.
        External validation of the fatty liver index for identifying nonalcoholic fatty liver disease in a population-based study.
        Clin Gastroenterol Hepatol. 2013; 11: 1201-1204https://doi.org/10.1016/j.cgh.2012.12.031
        • Cuthbertson D.J.
        • Weickert M.O.
        • Lythgoe D.
        • Sprung V.S.
        • Dobson R.
        • Shoajee-Moradie F.
        • et al.
        External validation of the fatty liver index and lipid accumulation product indices, using 1H-magnetic resonance spectroscopy, to identify hepatic steatosis in healthy controls and obese, insulin-resistant individuals.
        Eur J Endocrinol. 2014; 171: 561-569https://doi.org/10.1530/EJE-14-0112
        • Bedogni G.
        • Kahn H.S.
        • Bellentani S.
        • Tiribelli C.
        A simple index of lipid overaccumulation is a good marker of liver steatosis.
        BMC Gastroenterol. 2010; 1098https://doi.org/10.1186/1471-230X-10-98
        • Kahn H.S.
        The “lipid accumulation product” performs better than the body mass index for recognizing cardiovascular risk: A population-based comparison.
        BMC Cardiovasc Disord. 2005; 5: 26
        • Fedchuk L.
        • Nascimbeni F.
        • Pais R.
        • Charlotte F.
        • Housset C.
        • Ratziu V.
        • et al.
        Performance and limitations of steatosis biomarkers in patients with nonalcoholic fatty liver disease.
        Aliment Pharmacol Ther. 2014; 40: 1209-1222
        • Lee J.H.
        • Kim D.
        • Kim H.J.
        • Lee C.H.
        • Yang J.I.
        • Kim W.
        • et al.
        Hepatic steatosis index: A simple screening tool reflecting nonalcoholic fatty liver disease.
        Dig Liver Dis. 2010; 42: 503-508https://doi.org/10.1016/j.dld.2009.08.002
        • Li N.
        • Zhang G.W.
        • Zhang J.R.
        • Jin D.
        • Li Y.
        • Liu T.
        • et al.
        Nonalcoholic fatty liver disease is associated with progression of arterial stiffness.
        Nutr Metab Cardiovasc Dis. 2015; 25: 218-223
        • Vlachopoulos C.
        • Aznaouridis K.
        • Stefanadis C.
        Prediction of cardiovascular events and all-cause mortality with arterial stiffness: A systematic review and meta-analysis.
        J Am Coll Cardiol. 2010; 55: 1318-1327
        • Sunbul M.
        • Agirbasli M.
        • Durmus E.
        • Kivrak T.
        • Akin H.
        • Aydin Y.
        • et al.
        Arterial stiffness in patients with non-alcoholic fatty liver disease is related to fibrosis stage and epicardial adipose tissue thickness.
        Atherosclerosis. 2014; 237: 490-493
        • Boutari C.
        • Lefkos P.
        • Athyros V.G.
        • Karagiannis A.
        • Tziomalos K.
        Nonalcoholic fatty liver disease vs. nonalcoholic steatohepatitis: Pathological and clinical implications.
        Curr Vasc Pharmacol. 2017 Jun 20; https://doi.org/10.2174/1570161115666170621075157
        • Targher G.
        • Day C.P.
        • Bonora E.
        Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease.
        N Engl J Med. 2010; 363: 1341-1350
        • Dam-Larsen S.
        • Franzmann M.
        • Andersen I.B.
        • Christoffersen P.
        • Jensen L.B.
        • Sørensen T.I.
        • et al.
        Long term prognosis of fatty liver: Risk of chronic liver disease and death.
        Gut. 2004; 53: 750
        • Yu X.Y.
        • Zhao Y.
        • Song X.X.
        • Song Z.Y.
        Association between non-alcoholic fatty liver disease and arterial stiffness in the nonobese, non-hypertensive, and non-diabetic young and middleaged Chinese population.
        J Zhejiang Univ Sci B. 2014; 15: 879-887
        • Cicero A.F.
        • Rosticci M.
        • Bove M.
        • Fogacci F.
        • Giovannini M.
        • Urso R.
        • et al.
        Serum uric acid change and modification of blood pressure and fasting plasma glucose in an overall healthy population sample: Data from the Brisighella Heart Study.
        Ann Med. 2017; 49: 275-282https://doi.org/10.1080/07853890.2016.1222451
        • Cicero A.F.
        • Morbini M.
        • Urso R.
        • Rosticci M.
        • Parini A.
        • Grandi E.
        • et al.
        Association between self-reported snoring and arterial stiffness: Data from the Brisighella Heart Study.
        Intern Emerg Med. 2016; 11: 77-83https://doi.org/10.1007/s11739-015-1310-9
        • Ruscica M.
        • Ferri N.
        • Fogacci F.
        • Rosticci M.
        • Botta M.
        • Marchiano S.
        • et al.
        Circulating levels of proprotein convertase subtilisin/kexin type 9 and arterial stiffness in a large population sample: Data from the Brisighella Heart Study.
        J Am Heart Assoc. 2017; 6 (pii: e005764)https://doi.org/10.1161/JAHA.117.005764
        • Cicero A.F.
        • Rosticci M.
        • Fogacci F.
        • Grandi E.
        • D'Addato S.
        • Borghi C.
        • et al.
        High serum uric acid is associated to poorly controlled blood pressure and higher arterial stiffness in hypertensive subjects.
        Eur J Intern Med. 2017; 37: 38-42https://doi.org/10.1016/j.ejim.2016.07.026
        • Harrison S.A.
        • Oliver D.
        • Arnold H.L.
        • Gogia S.
        • Neuschwander-Tetri B.A.
        Development and validation of a simple NAFLD clinical scoring system for identifying patients without advanced disease.
        Gut. 2008; 57: 1441-1447
        • Van Bortel L.M.
        • Laurent S.
        • Boutouyrie P.
        • Chowienczyk P.
        • Cruickshank J.K.
        • DeBacker T.
        • et al.
        Expert consensus document on the measurement of aortic stiffness in daily practice using carotid-femoral pulse wave velocity.
        J Hypertens. 2012; 30: 445-448
        • Marque V.
        • Van Essen H.
        • Struijker-Boudier H.A.
        • Atkinson J.
        • Lartaud-Idjouadiene I.
        Determination of aortic elastic modulus by pulse wave velocity and wall tracking in a rat model of aortic stiffness.
        J Vasc Res. 2001; 38: 546-550
        • Hirata K.
        • Kawakami M.
        • O'Rourke M.F.
        Pulse wave analysis and pulse wave velocity: A review of blood pressure interpretation 100 years after Korotkov.
        Circ J. 2006; 70: 1231-1239
        • Hickson S.S.
        • Butlin M.
        • Broad J.
        • Avolio A.P.
        • Wilkinson I.B.
        • McEniery C.M.
        Validity and repeatability of the Vicorder apparatus: A comparison with the SphygmoCor device.
        Hypertens Res. 2009; 32: 1079-1085
        • Pucci G.
        • Cheriyan J.
        • Hubsch A.
        • Hickson S.S.
        • Gajendragadkar P.R.
        • Watson T.
        • et al.
        Evaluation of the Vicorder, a novel cuff-based device for the noninvasive estimation of central blood pressure.
        J Hypertens. 2013; 31: 77-85
        • Bots M.L.
        • Dijk J.M.
        • Oren A.
        • Grobbee D.E.
        Carotid intima-media thickness, arterial stiffness and risk of cardiovascular disease: Current evidence.
        J Hypertens. 2002; 20: 2317-2325
        • Cheng Y.L.
        • Wang Y.J.
        • Lan K.H.
        • Huo T.I.
        • Huang Y.H.
        • Su C.W.
        • et al.
        Fatty liver index and lipid accumulation product can predict metabolic syndrome in subjects without fatty liver disease.
        Gastroenterol Res Pract. 2017; 20179279836
        • Cicero A.F.
        • D'Addato S.
        • Reggi A.
        • Marchesini G.
        • Borghi C.
        • Brisighella Heart Study
        Gender difference in hepatic steatosis index and lipid accumulation product ability to predict incident metabolic syndrome in the historical cohort of the Brisighella Heart Study.
        Metab Syndr Relat Disord. 2013; 11: 412https://doi.org/10.1089/met.2012.0147
        • Huh J.H.
        • Ahn S.V.
        • Koh S.B.
        • Choi E.
        • Kim J.Y.
        • Sung K.C.
        • et al.
        A prospective study of fatty liver index and incident hypertension: The KoGES-ARIRANG study.
        PLoS One. 2015; 10e0143560
        • Cheung C.-L.
        • Lam K.S.L.
        • Wong I.C.K.
        • Cheung B.M.Y.
        Non-invasive score identifies ultrasonography-diagnosed non-alcoholic fatty liver disease and predicts mortality in the USA.
        BMC Med. 2014; 12: 154
        • Calori G.
        • Lattuada G.
        • Ragogna F.
        • Garancini M.P.
        • Crosignani P.
        • Villa M.
        • et al.
        Fatty liver index and mortality: The Cremona study in the 15th year of follow-up.
        Hepatology. 2011; 54: 145-152
        • Chen J.Y.
        • Chou C.H.
        • Tsai W.C.
        • Wang M.C.
        • Ho C.S.
        • Li Y.H.
        • et al.
        Effects of increased systemic inflammation and central obesity on arterial stiffness in patients with nonalcoholic fatty liver disease.
        J Am Soc Hypertens. 2012; 6: 253-260
        • Han E.N.
        • Cheong E.S.
        • Lee J.I.
        • Kim M.C.
        • Byrne C.D.
        • Sung K.
        Change in fatty liver status and 5-year risk of incident metabolic syndrome: A retrospective cohort study.
        Clin Hypertens. 2015; 21
        • Angelico F.
        • Del Ben M.
        • Conti R.
        • Francioso S.
        • Feole K.
        • Fiorello S.
        • et al.
        Insulin resistance, the metabolic syndrome, and nonalcoholic fatty liver disease.
        J Clin Endocrinol Metabol. 2005; 90: 1578-1582
        • Arrigo Ciceroa F.G.
        • Kuwabarab Masanari
        • Johnson Richard
        • Bovea Marilisa
        • Fogaccia Federica
        • Rosticcia Martina
        • Giovanninia Marina
        • D'Addatoa Sergio
        • Borghia Claudio
        LDL-oxidation, serum uric acid, kidney function and pulse-wave velocity: Data from the Brisighella Heart Study cohort.
        Int J Cardiol. 2018; (Available online 17 March 2018)https://doi.org/10.1016/j.ijcard.2018.03.077
        • Wijarnpreecha K.
        • Panjawatanan P.
        • Lekuthai N.
        • Thongprayoon C.
        • Cheungpasitporn W.
        • Ungprasert P.
        Hyperuricaemia and risk of nonalcoholic fatty liver disease: A meta-analysis.
        Liver Int. 2017; 37: 906-918https://doi.org/10.1111/liv.13329
        • Jaruvongvanich V.
        • Ahuja W.
        • Wirunsawanya K.
        • Wijarnpreecha K.
        • Ungprasert P.
        Hyperuricemia is associated with nonalcoholic fatty liver disease activity score in patients with nonalcoholic fatty liver disease: A systematic review and meta-analysis.
        Eur J Gastroenterol Hepatol. 2017 Jun 21; https://doi.org/10.1097/MEG.0000000000000931