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Comparative Assessment and External Validation of Hepatic Steatosis Formulae in a Community-Based Setting

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Comparative Assessment and External Validation of Hepatic Steatosis Formulae in a Community-Based Setting Journal of Clinical Medicine Article Comparative Assessment and External Validation of Hepatic Steatosis Formulae in a Community-Based Setting 1, 2, 2 2, Tae Yang Jung y, Myung Sub Kim y , Hyun Pyo Hong , Kyung A Kang * and Dae Won Jun 1,* 1 Department of Internal Medicine, Hanyang University College of Medicine, Seoul 04763, Korea; [email protected] 2 Department of Radiology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul 03181, Korea; [email protected] (M.S.K.); [email protected] (H.P.H.) * Correspondence: [email protected] (K.A.K.); [email protected] (D.W.J.) These authors are co-first authors and contributed equally to this work. y Received: 14 July 2020; Accepted: 1 September 2020; Published: 3 September 2020 Abstract: Several hepatic steatosis formulae have been validated in various cohorts using ultrasonography. However, none of these studies has been validated in a community-based setting using the gold standard method. Thus, the aim of this study was to externally validate hepatic steatosis formulae in community-based settings using magnetic resonance imaging (MRI). A total of 1301 community-based health checkup subjects who underwent liver fat quantification with MRI were enrolled in this study. Diagnostic performance was assessed using the area under the receiver operating characteristic curve (AUROC). Non-alcoholic fatty liver disease (NAFLD) liver fat score showed the highest diagnostic performance with an AUROC of 0.72, followed by Framingham steatosis index (0.70), hepatic steatosis index (HSI, 0.69), ZJU index (0.69), and fatty liver index (FLI, 0.68). There were considerable gray zones in three fatty liver prediction models using two cutoffs (FLI, 28.9%; HSI, 48.9%; and ZJU index, 53.6%). The diagnostic performance of NAFLD liver fat score for detecting steatosis was comparable to that of ultrasonography. The diagnostic agreement was 72.7% between NAFLD liver fat score and 70.9% between ultrasound and MRI. In conclusion, the NAFLD liver fat score showed the best diagnostic performance for detecting hepatic steatosis. Its diagnostic performance was comparable to that of ultrasonography in a community-based setting. Keywords: non-alcoholic fatty liver disease; fatty liver; validation study; population groups; magnetic resonance imaging 1. Introduction Non-alcoholic fatty liver disease (NAFLD) is the most common cause of chronic liver disease. The prevalence of NAFLD has increased along with that of diabetes, obesity, and metabolic syndrome [1]. Recognizing fatty liver is the first step in the screening for those with a high risk of steatohepatitis in the general population. Although hepatic fibrosis is a more serious and clinically significant disorder that may progress to cirrhosis, early detection of simple steatosis is also an important and promising field from a public health system view. Various prediction models have been developed for hepatic steatosis using routine biochemical test results and anthropometric parameters as simple screening tools. Some prediction models for hepatic steatosis have persistently demonstrated acceptable diagnostic performances in several cohorts. However, most studies were performed using ultrasonography (USG) [2–8]. Although USG is widely used as a screening tool for detecting the presence of fatty liver in the general population, the quality J. Clin. Med. 2020, 9, 2851; doi:10.3390/jcm9092851 www.mdpi.com/journal/jcm J. Clin. Med. 2020, 9, 2851 2 of 11 J. Clin. Med. 2020, 9, x FOR PEER REVIEW 2 of 11 of the USG is highly operator dependent because it is based on a subjective assessment of liver echogenicityliver echogenicity [9]. Liver [9]. biopsy Liver isbiopsy the “gold is the standard” “gold standard” method method to assess to hepatic assess steatosis.hepatic steatosis However,. it isHowever impossible, it tois performimpossible it onto ap largeerform scale it on for a the large general scale population. for the general Magnetic population. resonance Magnetic imaging resonance imaging (MRI) can provide a reliable estimation of fatty liver. It is now considered as “the (MRI) can provide a reliable estimation of fatty liver. It is now considered as “the next best method” next best method” as compared with liver biopsy [10]. To date, only five studies have validated as compared with liver biopsy [10]. To date, only five studies have validated prediction models of prediction models of hepatic steatosis using gold standard [11–15]. One study used liver biopsy [11] hepatic steatosis using gold standard [11–15]. One study used liver biopsy [11] and the other four used and the other four used proton magnetic resonance spectroscopy (1H-MRS) [12–15]. However, all five 1 protonstudies magnetic were performed resonance on spectroscopy selected populations ( H-MRS) wi [th12 small–15]. However,sample sizes all. five studies were performed on selectedThe populationsdiagnostic performance, with small especially sample sizes. positive predictive value (PPV) and negative predictive valueThe (NPV), diagnostic critically performance, depends on especially the prevalence positive of predictivethe disease value[16]. Therefore (PPV) and, external negative validation predictive valuestudies (NPV), for critically“average- dependsrisk group” on theusing prevalence gold standard of the diseasemethod [are16]. needed. Therefore, To externalthe best validationof our studiesknowledge, for “average-risk there is no group”appropriate using external gold standard validation method study for are existing needed. fatty To the liver best prediction of our knowledge, models thereusing is no MRI appropriate in the general external population. validation Thus, study the foraim existingof this study fatty liverwas to prediction comparatively models assess using and MRI in theexternally general validate population. existing Thus, hepatic the steatosis aim of formulae this study in wasa community to comparatively-based setting. assess and externally validate existing hepatic steatosis formulae in a community-based setting. 2. Materials and Methods 2. Materials and Methods 2.1. Study Population 2.1. Study Population A retrospective analysis was performed using health examination data collected by a medical examinationA retrospective center. analysis The populat was performedion of thisusing study health was composed examination of data2149 collectedKorean adults by a medicalwho examinationunderwent center. a medical The examination population ofand this an study MRI in was Kangbuk composed Samsung of 2149 Hospital Korean Healthcare adults who Screening underwent a medicalCenter (Seoul examination and Suwon and an, Korea) MRI inbetween Kangbuk January Samsung 2015 Hospital and May Healthcare 2018. According Screening to Centerthe (SeoulOccupational and Suwon, Safety Korea) and betweenHealth Act, January it is mandatory 2015 and Mayfor companies 2018. According with more to thethan Occupational 40 employees Safety to andprovide Health empolyee Act, it is mandatorybenefits for annual for companies or biannual with medical more than examinations 40 employees in Korea to provide. MRI scans empolyee are benefitsvoluntary for annual chosen orby biannual employees medical and the examinations charge is paid in by Korea. their MRIemployer. scans Over are voluntary 90% of the chosen study by population were employees and their family members. This study was approved by the Kangbuk employees and the charge is paid by their employer. Over 90% of the study population were employees Samsung Hospital Institutional Review Board (IRB No. KBSMC 2019-12-002). The clinical protocol and their family members. This study was approved by the Kangbuk Samsung Hospital Institutional was registered with the Korean Clinical Research Information Service with a registration number of Review Board (IRB No. KBSMC 2019-12-002). The clinical protocol was registered with the Korean KCT0004645. Clinical Research Information Service with a registration number of KCT0004645. 2.2. Inclusion and Exclusion Criteria 2.2. Inclusion and Exclusion Criteria The study population included 2149 subjects aged 18 years or older who visited Kangbuk SamsungThe study Hospital’s population Health included Screening 2149 Center subjects with aged their 18 yearsliver orfat oldercontent who measured visited Kangbuk using MRI. Samsung We Hospital’sexcluded Health subjects Screening with viral Center hepatitis with B ( theirn = 167) liver or fatC ( contentn = 12), subjects measured with using chronic MRI. liver We disease excluded subjectscaused with by significant viral hepatitis alcohol B (consumptionn = 167) or C (>20 (n =g/day,12), subjectsn = 642) [17,18] with chronic, and subjects liver disease with suspected caused by significantchronic liver alcohol disease consumption or liver cirrhosis (>20 g/ day,on USnG= (642)n = 27) [17 in,18 order], and to subjects exclude withchronic suspected liver disease chronic with liver diseaseunknown or liver etiology cirrhosis such onas USGautoimmune (n = 27) hepatitis, in order primary to exclude biliary chronic cirrhosis, liver and disease hemochromatosis with unknown etiology(Figure such 1). as autoimmune hepatitis, primary biliary cirrhosis, and hemochromatosis (Figure1). FigureFigure 1. Flow1. Flow chart chart showing showing enrollment enrollment ofof participantsparticipants for for this this study. study. * *NAFLD NAFLD = Non= Non-alcoholic-alcoholic fatty fatty liverliver disease. disease Fatty. Fatty liver liver was was defined defined as as hepatichepatic fat fraction ≥5%5% on on
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