LIVER, PANCREAS, AND BILIARY TRACT
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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2013;11: LIVER, PANCREAS, AND BILIARY TRACT Association Between Anthropometric Parameters and Measurements of Liver Stiffness by Transient Elastography GRACE LAI HUNG WONG,*, HENRY LIK YUEN CHAN,*, PAUL CHEUNG LUNG CHOI, ANTHONY WING HUNG CHAN, ANGELINE OI SHAN LO,*, ANGEL MEI LING CHIM,*, and VINCENT WAI SUN WONG*, *Institute of Digestive Disease, Department of Medicine and Therapeutics, and Department of Anatomical and Cellular Pathology, Chinese University of Hong Kong, Hong Kong, China BACKGROUND & AIMS: METHODS: RESULTS: CONCLUSIONS: We investigated the association between anthropometric parameters and results of liver stiffness measurements (LSMs) by transient elastography in healthy subjects and patients with nonalcoholic fatty liver disease (NAFLD). We analyzed anthropometric and LSM data from 658 healthy subjects (37% male; mean age, years; body mass index [BMI], kg/m 2 ; LSM, kpa) and 247 patients with biopsy-proven NAFLD (50% male; mean age, years; BMI, kg/m 2 ; LSM, kpa). Healthy subjects were defined as individuals without viral hepatitis, alcoholic liver disease, or NAFLD. We investigated associations between anthropometric parameters, including BMI and waist circumference, and LSM. LSMs were slightly higher among healthy subjects with BMIs <18.5 kg/m 2 (n 84, kpa) and BMIs of kg/m 2 (n 76, kpa) than those with BMIs of kg/m 2 (n 492, kpa; P.16 by analysis of variance). Among patients with NAFLD of Brunt fibrosis stage 0 or 1, LSMs were lowest among those with BMIs of kg/m 2 (stage 0: n 34, kpa; stage 1: n 18, kpa). LSMs were higher among those with BMIs of kg/m 2 (stage 0: n 41, kpa; stage 1: n 26, kpa) and highest for those with BMIs >30 kg/m 2 (stage 0: n 13, kpa; stage 1: n 22, kpa) (P <.001 and P.002, respectively, by analysis of variance). High BMI was independently associated with high LSM, in addition to fibrosis stage, among patients with NAFLD. Patients with different waist circumferences had comparable LSMs. BMI >30 kg/m 2 is associated with higher LSMs in patients with NAFLD, after adjusting for fibrosis stage. Keywords: Liver Fibrosis; Cirrhosis; Biopsy; Nonalcoholic Fatty Liver Disease; Body Mass Index; Waist Circumference. See editorial on page 309. Liver stiffness measurement (LSM) by transient elastography has been a widely validated and increasingly popular noninvasive assessment for liver fibrosis. 1 It has been found to be an accurate and reproducible method to predict advanced liver fibrosis and cirrhosis in various chronic liver diseases. 2 4 This tool provides important information on liver fibrosis, which is important in the decision process of treatment in chronic viral hepatitis and/or predicting disease prognosis. 5 7 One major advantage of LSM is its noninvasiveness, such that it can be applied in a population-based study. 8 Despite a high success rate, it has been noted that unreliable and failed LSMs occur in around 3% and 11.6% 18.4% of all examinations, respectively, and they are independently associated with body mass index (BMI) 30 kg/m 2 in both white and Chinese patients. 9,10 The success rate of LSM with M probe could be as low as 75% in nonalcoholic fatty liver disease (NAFLD) patients with BMI 30 kg/m 2. 4 A BMI 28 kg/m 2 has been found to be an independent risk factor for LSM failure. 11 On the other hand, patients with extreme BMI were found to have higher LSMs in a recent Indian population study. 12 Therefore, the performance of transient elastography Abbreviations used in this paper: ALT, alanine aminotransferase; ANOVA, analysis of variance; BMI, body mass index; 1 H-MRS, protonmagnetic resonance spectroscopy; IHTG, intrahepatic triglyceride content; IQR, interquartile range; kpa, kilopascal; LSM, liver stiffness measurement; NAFLD, nonalcoholic fatty liver disease by the AGA Institute /$
2 296 WONG ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 3 may be compromised in lean and obese subjects. It is particularly true for obese subjects because they are more commonly encountered worldwide in the last few decades, 13 and they are at substantial risk of NAFLD and liver fibrosis. 8 In the Indian population study, 12 the healthy subjects might actually include those with undiagnosed NAFLD, such that the genuine relationship between anthropometric parameters and LSM could not be demonstrated. On one hand, it is technically demanding to identify a cohort of truly healthy subjects because of reasons mentioned above. It is even more challenging to identify an optimal histologic cohort to illustrate the effect of anthropometric parameters on LSM. Serum alanine aminotransferase (ALT) level is a very important confounding factor of LSM in chronic viral hepatitis patients, which makes this group of patients inappropriate. This confounding effect of ALT is not seen among NAFLD patients, among whom elevated ALT might just reflect fatty change rather than necroinflammation. 4 Most NAFLD patients have only modestly elevated ALT levels, and intrahepatic steatosis grading will not significantly affect the LSM results. 4 Therefore, we aimed to investigate the effect of anthropometric parameters on the results and quality of LSM by transient elastography in a cohort of truly healthy subjects selected from the general population with chronic liver diseases including NAFLD stringently excluded, as well as a biopsyproven NAFLD cohort to study the effect of anthropometric parameters on LSM adjusted for liver fibrosis stage. Methods Study Design and Subjects Healthy subject cohort. Adult subjects from the general population were randomly selected from the census database of the Hong Kong government and were invited by mail and phone calls from May 2008 to September Subjects with active malignancy, metallic implants, or other contraindications to magnetic resonance imaging, positive hepatitis B surface antigen or antibody against hepatitis C virus, and decompensated liver disease (defined as bilirubin 50 mol/l, albumin 35 g/l, platelet count /L, international normalized ratio 1.3, or the presence of ascites or varices) were excluded. Proton-magnetic resonance spectroscopy ( 1 H-MRS) was performed to measure intrahepatic triglyceride content (IHTG) within 8 weeks from the baseline visit in the population cohorts. Whole-body 3.0T scanner with a single voxel pointresolved spectroscopy sequence was performed, and the details of the procedure have been previously described. 20 Patients who had an IHTG of 5% or greater were diagnosed to have fatty liver, 21 so they were excluded from the analysis. Nonalcoholic fatty liver disease cohort. Consecutive adult patients with NAFLD who were clinically indicated for liver biopsy examination in the Prince of Wales Hospital, Hong Kong were prospectively recruited from July 2006 to June The indications of liver biopsy were to assess the severity of liver fibrosis and necroinflammatory activity. We excluded patients who were chronic drinkers (with regular consumption of at least 20 g of alcohol weekly) and who had decompensated liver disease as stated above, complications of liver cirrhosis, or previous liver surgery or liver transplantation. NAFLD was diagnosed by histology after exclusion of other possible etiologies of fatty liver. 22 The study protocol was approved by the Clinical Research Ethics Committee of the Chinese University of Hong Kong. All subjects provided informed written consent. Clinical Evaluation and Laboratory Tests All patients received comprehensive clinical assessment at the time of transient elastography. Comorbid illness was recorded with a standard questionnaire. Anthropometric tests included body weight, body height, and waist circumference measurements. BMI was calculated as weight (kg) divided by height (m) squared. Patients were classified into different BMI categories (underweight, 18.5 kg/m 2 ; normal weight, kg/m 2 ; moderate obesity, kg/m 2 ; and severe obesity, 30 kg/m 2 ) according to the World Health Organization. 23 Waist circumference was measured at a level midway between the lower rib margin and iliac crest, with the tape all around the body in the horizontal position. A venous blood sample was taken for albumin, bilirubin, and ALT. Metabolic syndrome was defined according to the ethnic-specific criteria by the International Diabetes Federation, which was modified from the National Cholesterol Education Program, Adult Treatment Panel III Guidelines. 24 Liver Stiffness Measurement With Transient Elastography All consecutive patients underwent LSM with standard M probe by using transient elastography (Fibroscan; Echosens, Paris, France) according to the instructions and training provided by the manufacturer, and the details of operation were described previously. 25 Measurements were performed on the right lobe of the liver through intercostal spaces, with the patient lying in dorsal decubitus position with the right arm in maximal abduction. Ten successful acquisitions were performed on each patient. The median value represented the liver elastic modulus. The liver stiffness was expressed in kilopascals (kpas). Reliable measurements were defined as those with 10 successful acquisitions, an interquartile range (IQR)/LSM 0.30, and success rate of 60% or above. Histologic Assessment Percutaneous liver biopsy was performed by using the 16-gauge Temno (Cardinal Health, Dublin, OH) needle. Liver histology was assessed by pathologists who specialized in liver diseases (P.C.-L.C., A.W.-H.C.) and were without knowledge of the clinical data. A liver sample was considered adequate if it was longer than 15 mm and contained 6 portal tracts or more. The histologic grading and staging of NAFLD followed the criteria of Brunt et al. 26 Statistical Analysis Statistical tests were performed by using the Statistical Package for Social Sciences (SPSS Inc, Chicago, IL) version Continuous variables were expressed as mean standard deviation or median (range) and compared by using unpaired Student t test and Mann Whitney U test as appropriate. Categorical variables were compared by using 2 test or Fisher exact test as appropriate. The Pearson correlation coefficient was used to test the correlations between BMI and LSM. One-way analysis of variance (ANOVA) was used to compare the LSM values in different BMI categories. Clinical characteristics and quality of transient elastography of patients in different BMI categories
3 March 2013 FIBROSCAN AND BMI 297 Figure 1. Method of subject selection of healthy subjects and NAFLD cohorts. were compared. We conducted simple linear regression analyses to determine clinical parameters associated with LSM values in different patient groups. The multiple linear regression model was then performed among covariates that were associated with LSM values on simple linear regression (P.10) to determine independent factors. Significance was taken as P.05, except that P.0083 was considered significant in the one-way ANOVA with Bonferroni correction because there was a total of 6 comparisons among 4 categories of BMI. Results Patients Healthy subject cohort. Invitation letters were sent to 3000 randomly selected Hong Kong residents from the census database, and 1069 subjects responded, with a response rate of 35.6%. Nine hundred twenty-two patients had valid 1 H-MRS results without concurrent viral hepatitis. Two hundred forty-six subjects were excluded because they had NAFLD as a result of an IHTG 5% or above; hence, 658 were defined as healthy subjects (Figure 1). The mean age of the healthy subject was years; most of them were female (63%). The mean BMI was kg/m 2, and 13% of subjects had BMI 18.5 kg/m 2, 74% had BMI kg/m 2, 12% had BMI kg/m 2, and 1% had BMI 30 kg/m 2. Most of them had normal liver biochemistry (Table 1). Nonalcoholic fatty liver disease cohort. Two hundred seventy-nine NAFLD patients underwent liver biopsy within the study period; 27 and 5 patients were excluded because they did not have LSM and/or adequate liver biopsy samples, respectively. Therefore, 247 biopsy-proven NAFLD patients were included for the analysis (Figure 1). Their mean age was years; half of them were male. The mean BMI was kg/m 2. Only 1% of NAFLD patients had BMI 18.5 kg/m 2, whereas 27% had BMI kg/m 2, 44% had BMI kg/m 2, and 28% had BMI 30 kg/m 2. Most of them had compensated liver function and mildly elevated ALT (mean serum ALT, IU/L). With healthy subjects as the reference group, NAFLD patients were more likely to be male and had higher BMI and higher serum ALT levels. Body Mass Index, Waist Circumference, and Liver Stiffness Measurement Healthy subject cohort. The mean LSM was kpa, whereas the median (IQR), 5th, and 95th percentile values of LSM were 4.1 ( ), 2.8, and 7.4 kpa, respectively. Hence the normal values of LSM ranged between 2.8 and 7.4 kpa. None of the clinical parameters (age, sex, BMI, waist circumference, or serum ALT) were found associated with LSM values in healthy subjects. Overall, there was no significant correlation between LSM values and BMI (r 0.002, P.95; Supplementary Figure 1A). If BMI was divided into the 4 categories, LSM values were higher among healthy subjects with BMI 18.5 kg/m 2 ( kpa) compared with healthy subjects with BMI kg/m 2 ( kpa), but the mean difference was only kpa. There was a trend that LSM values were higher among healthy subjects with BMI kg/m 2 ( kpa) compared with those with BMI kg/m 2. There were only 6 healthy subjects with BMI 30 kg/m 2, and their mean LSM was kpa (Supplementary Figure 2A). In view of the small numbers of patients with extreme BMI, no statistically significant difference was demonstrated from ANOVA (P.16; Table 2).
4 298 WONG ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 3 Table 1. Clinical Characteristics of the Patients Healthy subject cohort NAFLD cohort P value Number of patients Male sex (%) a 246 (37) 124 (50).001 Age, mean (SD), y b Body weight, mean (SD), kg b Body height, mean (SD), cm b BMI, mean (SD), kg/m 2b (%) c 84 (13) 2 (1) (%) a 76 (12) 108 (44) 30 (%) c 6 (1) 70 (28) Waist circumference, mean (SD), cm b Hip circumference, mean (SD), cm b Waist-to-hip ratio (SD) b Systolic blood pressure, mean (SD), mm Hg b Diastolic blood pressure, mean (SD), mm Hg b Metabolic syndrome (%) a 62 (9) 166 (67).001 Central obesity (%) a 187 (28) 170 (69).001 Raised triglycerides (%) a 89 (14) 122 (49).001 Reduced high-density lipoprotein cholesterol (%) a 81 (12) 115 (47).001 Hypertension (%) a 62 (9) 177 (72).001 Diabetes mellitus (%) c 19 (3) 160 (65).001 Biochemical Albumin, mean (SD), g/l b Bilirubin, mean (SD), mol/l b Alkaline phosphatase, mean (SD), IU/L d ALT, mean (SD), IU/L d Gamma-glutamyl transpeptidase (SD), IU/L d Liver histology Biopsy length, mean (SD), mm 20 5 No. of portal tracts, mean (SD) 9 4 Brunt fibrosis stage (%) (42) 1 73 (30) 2 22 (9) 3 25 (10) 4 23 (9) Steatosis, mean (SD), % Steatosis grade 0 19 (8) 1 74 (30) 2 85 (34) 3 69 (28) LSM, kpa b Reliable LSM (%) c 542 (82) 212 (86).27 IQR/LSM ratio d Success rate of acquisition, mean (SD), % b NOTE. Normal ranges of biochemical parameters: albumin, g/l; bilirubin, 17 mol/l; alkaline phosphatase, IU/L; ALT, 55 IU/L; gamma-glutamyl transpeptidase, 45 IU/L. SD, standard deviation. a Chi-square test was used. b Student t test was used. c Fisher exact test was used. d Mann Whitney U test was used. The rate of valid and reliable LSM by transient elastography decreased with increasing BMI. The majority of the unreliable LSMs were related to success rate of acquisition below 60% and/or IQR/LSM ratio above The probabilities of success rate below 60% increased dramatically with BMI categories (0% in BMI 18.5 kg/m 2,9%inBMI kg/m 2, 24% in BMI kg/m 2, and 50% in BMI 30 kg/m 2, respectively; P.001). On the other hand, the IQR/LSM ratios were similar among healthy subjects in different BMI categories (Supplementary Figure 2B). Healthy subjects of small body build (waist circumference less than 70 cm) had higher LSM compared with those with waist circumference of cm ( kpa vs kpa, P.001), but the difference was small ( kpa). Healthy subjects with higher waist circumference had comparable LSM; the IQR/LSM ratios were similar among healthy
5 March 2013 FIBROSCAN AND BMI 299 Table 2. LSM Values in Different BMI Categories World Health Organization BMI categories Underweight (BMI 18.5 kg/m 2 ) Normal weight (BMI kg/m 2 ) Moderate obesity (BMI kg/m 2 ) Severe obesity (BMI 30 kg/m 2 ) P value a Healthy subjects (N 658) No. of patients LSM, kpa ( ) 4.0 ( ) 4.3 ( ) 4.3 ( ) NAFLD patients with Brunt fibrosis stage 0 or 1 (N 177) Stage 0 (N 104) No. of patients LSM, kpa ( ) 5.8 ( ) 7.9 ( ) Stage 1 (N 73) No. of patients LSM, kpa NA ( ) 7.2 ( ) 10.3 ( ) NOTE. Values are presented as mean standard deviation and median (IQR). a Significance was taken as P.0083 was considered significant in one-way ANOVA with Bonferroni correction. subjects in different waist circumference categories (Supplementary Figure 2C and D). Nonalcoholic fatty liver disease cohort. The mean LSM was kpa, whereas the median (IQR) LSM was 8.7 ( ) kpa. By simple linear regression, BMI, waist circumference, systolic blood pressure, serum ALT level, and fibrosis stage were associated with high LSM. By multiple linear regression analysis, BMI (B 0.41; 95% confidence interval, ; P.001) was an independent factor in addition to Brunt fibrosis stage associated with LSM values (Table 3). There were significant correlations between LSM values and BMI in patients of Brunt fibrosis stage 0 (r 0.432, P.001) and stage 1 (r 0.406, P.001) (Supplementary Figure 1B and C). LSM values were significantly higher among NAFLD patients with BMI 30 kg/m 2 ( kpa for Brunt fibrosis stage 0; kpa for Brunt fibrosis stage 1) compared with those with BMI kg/m 2 ( kpa for Brunt fibrosis stage 0, kpa for Brunt fibrosis stage 1; P.001 for both comparisons) (Table 2). LSM values were also higher among NAFLD patients with BMI kg/m 2 ( kpa for Brunt fibrosis stage 0, kpa for Brunt fibrosis stage 1) compared with those with BMI kg/m 2, but the difference was significant only in Brunt fibrosis stage 0 (P.02) (Figure 2). There was statistically significant difference demonstrated from ANOVA in Brunt fibrosis stages 0and1(P.001 and P.002, respectively; Table 2). The rate of valid and reliable LSM by transient elastography also decreased with increasing BMI. The probabilities of success rate below 60% increased dramatically when BMI 30 kg/m 2 (38%). Sixteen patients (34%) with BMI 30 kg/m 2 had 10 valid acquisitions, compared with none of the patients in other BMI categories (P.001, Supplementary Table 1). Factors Associated With Falsely High Liver Stiffness Measurement Among Healthy Subjects Because the 95th percentile value of LSM in the healthy subject cohort was 7.4 kpa, it was defined as the upper limit of normal for healthy subjects. Forty-one healthy subjects had LSM above 7.4 kpa. Most of them were male (30 subjects, 73%); 5 (12%) had BMI 18.5 kg/m 2, 3 (7%) had BMI kg/m 2, and none had BMI 30 kg/m 2. These 41 subjects did not have significant differences in all clinical characteristics compared with the rest of the same cohort. In Table 3. Simple and Multiple Linear Regression Analyses of Clinical Parameters Associated With LSM Values Among NAFLD Patients Simple linear regression Multiple linear regression Coefficient (B) 95% CI P value Coefficient (B) 95% CI P value Male sex to Age (y) to BMI, kg/m Waist circumference (cm) to Systolic blood pressure (mm Hg) to ALT (IU/L) to Presence of metabolic syndrome to Brunt fibrosis stage Hepatic steatosis grade to CI, confidence interval.
6 300 WONG ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 3 multiple linear regression analysis, LSM/IQR 0.3 was the single independent factor associated with the falsely high LSM among healthy subjects. Factors Associated With Falsely High Liver Stiffness Measurement Among Nonalcoholic Fatty Liver Disease Patients From a previous validation study, a cutoff at 9.0 kpa had high specificity to exclude Brunt fibrosis stage 2 or above fibrosis. 4 Thirty-three NAFLD patients of Brunt fibrosis 0 to 1 had LSM of 9.0 kpa or above; hence, they were defined to have falsely high LSM. They were predominantly female (55%) and had higher BMI ( kg/m 2 ) compared with the rest of the cohort ( kg/m 2 ). In multiple linear regression analysis, high BMI was the single independent factor associated with the falsely high LSM among NAFLD patients. Figure 2. Box plot showing LSM in different categories of BMI in different cohorts: (A) healthy subject cohort, (B) NAFLD patients of Brunt fibrosis stage 0, and (C) NAFLD patients of Brunt fibrosis stage 1. Discussion This study reported the largest series of healthy subjects and biopsy-proven NAFLD patients that was investigating the effect of anthropometric parameters on the results and quality of LSM with transient elastography. We found that LSM was higher in NAFLD patients with BMI 30 kg/m 2, adjusting for the liver fibrosis stage. There was a similar trend observed in healthy subject cohort, but the subjects with BMI 30 kg/m 2 were underrepresented such that no significant difference was demonstrated. On the other hand, LSM was slightly higher in underweight healthy subjects, but the absolute difference was small, so it would not affect the accuracy of the measurements. LSM by transient elastography has been increasingly used as a diagnostic as well as a monitoring tool of liver fibrosis in patients with chronic liver disease. 27,28 It has also been recently studied as a screening tool of cirrhosis in apparently healthy subjects from the general population. 29 The accuracy of this widely adopted noninvasive tool has been challenged. 30 LSM was found to be affected by sex, BMI, and presence of metabolic syndrome among apparently healthy subjects. 31 Whether these factors affected LSM independent of the presence of NAFLD was not known from previous studies. In the current study, we stringently identified and excluded NAFLD with 1 H-MRS in the population cohort, together with other common chronic liver diseases. Therefore, the healthy subjects were not just apparently healthy but had most common chronic liver diseases confidently ruled out. The normal range of LSM derived from our group of healthy subjects was kpa, which was comparable to the range ( kpa) proposed by a recent population-based study from India. 12 More importantly, we did not identify any of the clinical parameters (age, sex, BMI, waist circumference, or serum ALT) associated with LSM values among our healthy subjects. When patients were categorized into 4 BMI groups, LSM values were slightly increased in subjects with BMI 18.5 kg/m 2, whereas there was a trend that healthy subjects with BMI 25 kg/m 2 also had higher LSM values when compared with those with BMI kg/m 2. However, much higher LSM values at extreme BMI categories (ie, U-shaped distribution) were noted in the Indian study. 12 On one hand, this study echoed our observation that underweight healthy subjects had mean LSM approximately 0.3 kpa higher than normal-weight subjects; on the other hand, a much higher LSM in healthy subjects with BMI 25 kg/m 2 was not observed here. One of the explanations was that
7 March 2013 FIBROSCAN AND BMI 301 NAFLD was not stringently excluded in the Indian cohort; instead, it was diagnosed by transabdominal ultrasonography, which is known to be insensitive to mild hepatic steatosis. 32 Hence, the seemingly much higher LSM values among obese subjects might be partly increased by the presence of some undiagnosed NAFLD subjects in their cohorts. Using 1 H-MRS, a highly sensitive tool for steatosis, avoided this problem. Another important observation of this study was that NAFLD patients with BMI 30 kg/m 2 had increased LSM values, and this relationship was adjusting for the severity of liver fibrosis. The mechanism of higher LSM values among NAFLD patients of higher BMI has not been well defined. Previous study demonstrated that obesity, together with other metabolic risk factors, was well associated with liver fibrosis in NAFLD as well as chronic hepatitis B patients. 25,33 However, the findings of the current study supported that there was an association between BMI and LSM, in addition to the increased risk of liver fibrosis. More interestingly, the higher LSM in obese subjects seemingly was not related to the larger body build and thicker subcutaneous fat, because higher LSM was not observed in patients with higher waist circumference. This relationship between BMI and LSM probably implied that LSM by the conventional M probe may overestimate LSM in patients with BMI 30 kg/m 2, such that the XL probe should be considered as the probe of choice for these patients. 34 The factors associated with the falsely high LSM among healthy subjects and NAFLD patients somehow appeared different. In fact, the probability of LSM/IQR 0.3 increased with BMI among healthy subjects. However, probably because subjects with BMI kg/m 2 were underrepresented ( 1%), LSM/ IQR 0.3 instead of BMI was able to stand out as an independent factor of falsely high LSM among healthy subjects. Because obese patients were more adequately represented in NAFLD patients, the independent association of high BMI and falsely high LSM was hence highlighted. Therefore, these results echoed our key message that high BMI was associated with high LSM values. Our study had the strength of large sample sizes in different patient groups. The healthy subjects were representative because we recruited asymptomatic individuals from the general population by using the government census database. The use of well-validated noninvasive tests including 1 H-MRS and transient elastography allowed accurate assessment of hepatic steatosis and fibrosis in a large number of subjects in the community, in which liver biopsy may not be feasible. We included a large number of NAFLD patients with liver biopsy. The numbers of NAFLD patients with no or mild fibrosis in different BMI categories were respectable, such that the comparisons were meaningful. On the other hand, our study was limited by only including ethnic Chinese subjects, such that the findings might not be extrapolated to other ethnicities. Nonetheless, our results echoed those from another population-based study from India. 12 We believe these observations on how anthropometric parameters influence LSM are likely applicable in different ethnic groups. Another limitation was there was still a small probability that some uncommonly seen chronic liver diseases, namely subclinical autoimmune liver diseases, might have been missed, whereas primary hemochromatosis and alpha 1 -antitrypsin deficiency are exceedingly rare in Hong Kong. In conclusion, LSM was increased in NAFLD patients with BMI 30 kg/m 2, adjusting for liver fibrosis stage. On the basis of these observations, LSM should be interpreted with caution in patients with BMI 30 kg/m 2, and LSM by XL probe should be considered for these patients. Supplementary Material Note: To access the supplementary material accompanying this article, visit the online version of Clinical Gastroenterology and Hepatology at and at doi.org/ /j.cgh References 1. Wong VW, Chan HL. Transient elastography. J Gastroenterol Hepatol 2010;25: Chan HL, Wong GL, Choi PC, et al. Alanine aminotransferasebased algorithms of liver stiffness measurement by transient elastography (Fibroscan) for liver fibrosis in chronic hepatitis B. J Viral Hepat 2009;16: Castéra L, Vergniol J, Foucher J, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 2005;128: Wong VW, Vergniol J, Wong GL, et al. Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease. Hepatology 2010;51: Liaw YF, Leung N, Kao JH, et al. Asian-Pacific consensus statement on the management of chronic hepatitis B: a 2008 update. Hepatol Int 2008;2: Lok AS, McMahon BJ. Chronic hepatitis B: update Hepatology 2009;50: Wong VW, Wong GL, Choi PC, et al. Disease progression of non-alcoholic fatty liver disease: a prospective study with paired liver biopsies at 3 years. Gut 2010;59: Wong VW, Chu WC, Wong GL, et al. Prevalence of non-alcoholic fatty liver disease and advanced fibrosis in Hong Kong Chinese: a population study using proton-magnetic resonance spectroscopy and transient elastography. Gut 2012;61: Castéra L, Foucher J, Bernard PH, et al. Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology 2010;51: Wong GL, Wong VW, Chim AM, et al. Factors associated with unreliable liver stiffness measurement and its failure with transient elastography in the Chinese population. J Gastroenterol Hepatol 2011;26: Abenavoli L, Beaugrand M. Transient elastography in non-alcoholic fatty liver disease. Ann Hepatol 2012;11: Das K, Sarkar R, Ahmed SM, et al. Normal liver stiffness measure (LSM) values are higher in both lean and obese individuals: a population-based study from a developing country. Hepatology 2012;55: Finucane MM, Stevens GA, Cowan MJ, et al. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet 2011;377: Wong GL, Wong VW, Choi PC, et al. Evaluation of alanine transaminase and hepatitis B virus DNA to predict liver cirrhosis in hepatitis B e antigen-negative chronic hepatitis B using transient elastography. Am J Gastroenterol 2008;103: Wong GL, Wong VW, Choi PC, et al. Increased liver stiffness measurement by transient elastography in severe acute exacerbation of chronic hepatitis B. J Gastroenterol Hepatol 2009;24: Gaia S, Carenzi S, Barilli AL, et al. Reliability of transient elastography for the detection of fibrosis in non-alcoholic fatty liver disease and chronic viral hepatitis. J Hepatol 2011;54:64 71.
8 302 WONG ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No Lupsor M, Badea R, Stefanescu H, et al. Performance of unidimensional transient elastography in staging non-alcoholic steatohepatitis. J Gastrointest Liver Dis 2010;19: Nobili V, Vizzutti F, Arena U, et al. Accuracy and reproducibility of transient elastography for the diagnosis of fibrosis in pediatric nonalcoholic steatohepatitis. Hepatology 2008;48: Yoneda M, Yoneda M, Mawatari H, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with nonalcoholic fatty liver disease (NAFLD). Dig Liver Dis 2008;40: Wong VW, Wong GL, Tsang SW, et al. High prevalence of colorectal neoplasm in patients with non-alcoholic steatohepatitis. Gut 2011;60: Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004;40: Chan HL, de Silva HJ, Leung NW, et al. How should we manage patients with non-alcoholic fatty liver disease in 2007? J Gastroenterol Hepatol 2007;22: WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 2004;363: Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009;120: Wong GL, Wong VW, Choi PC, et al. Metabolic syndrome increases the risk of liver cirrhosis in chronic hepatitis B. Gut 2009;58: Brunt EM, Janney CG, Di Bisceglie AM, et al. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol 1999;94: Wong GL, Wong VW, Choi PC, et al. Clinical factors associated with liver stiffness in hepatitis B e antigen-positive chronic hepatitis B patients. Clin Gastroenterol Hepatol 2009;7: Wong GL, Wong VW, Choi PC, et al. On-treatment monitoring of liver fibrosis with transient elastography in chronic hepatitis B patients. Antivir Ther 2011;16: Roulot D, Costes JL, Buyck JF, et al. Transient elastography as a screening tool for liver fibrosis and cirrhosis in a communitybased population aged over 45 years. Gut 2011;60: Wong GL, Wong VW, Chan HL. Is transient elastography inaccurate in chronic hepatitis B and non-alcoholic fatty liver disease? J Hepatol 2011;55:497, author reply Roulot D, Czernichow S, Le Clésiau H, et al. Liver stiffness values in apparently healthy subjects: influence of gender and metabolic syndrome. J Hepatol 2008;48: Saadeh S, Younossi ZM, Remer EM, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology 2002;123: Wong VW, Wong GL, Chu WC, et al. Hepatitis B virus infection and fatty liver in the general population. J Hepatol 2012;56: de Lédinghen V, Wong VW, Vergniol J, et al. Diagnosis of liver fibrosis and cirrhosis using liver stiffness measurement: comparison between M and XL probe of FibroScan(R). J Hepatol 2012; 56: Reprint requests Address requests for reprints to: Vincent W. S. Wong, MD, Department of Medicine and Therapeutics, 9/F Prince of Wales Hospital, Ngan Shing Street, Shatin, Hong Kong. wongv@cuhk. edu.hk; fax: Acknowledgments The authors acknowledge the statistical support of Mr Yee-Kit Tse, statistician of Institute of Digestive Disease, Chinese University of Hong Kong, in proofreading the statistical analysis and statements of this manuscript. Conflicts of interest These authors disclose the following: Grace Wong has served as an advisory committee member for Otsuka and a speaker for Echosens. Henry Chan is a consultant for Abbott, Bristol-Myers Squibb, Gilead, Merck, Novartis, and Roche; has received honorarium for lectures for Abbott, Bristol-Myers Squibb, FuRui, Gilead, Glaxo-Smith-Kline, Merck, Novartis, and Roche; and has received an unrestricted grant from Roche for hepatitis B research. Vincent Wong has served as an advisory committee member for Roche, Novartis, Gilead, and Otsuka. He has also served as a speaker for Bristol-Myers Squibb, Roche, Novartis, Abbott Diagnostics, and Echosens. The remaining authors disclose no conflicts.
9 302.e1 WONG ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 3 Supplementary Table 1. Clinical Characteristics and Quality of Transient Elastography Among Healthy Subjects and Patients Without Liver Fibrosis, According to Different BMI Categories Underweight (BMI 18.5 kg/m 2 ) World Health Organization BMI categories Normal weight (BMI kg/m 2 ) Moderate obesity (BMI kg/m 2 ) Severe obesity (BMI 30 kg/m 2 ) P value a Healthy subjects (N 658) No. of patients Central obesity (%) 2 (2) 187 (28) 65 (86) 4 (67).001 LSM, kpa Reliable LSM (%) 73 (87) 415 (84) 51 (67) 3 (50).008 Success rate 60% (%) 0 (0) 43 (9) 18 (24) 3 (50).001 IQR/LSM ratio 0.30 (%) 11 (13) 70 (14) 13 (17) 2 (33).53 Fewer than 10 valid acquisitions (%) 0 (0) 2 (0.4) 0 (0) 0 (0).88 NAFLD with Brunt fibrosis stage 0 or 1(N 177) No. of patients Central obesity (%) 0 (0) 20 (34) 57 (81) 37 (79).001 LSM, kpa Reliable LSM (%) 1 (100) 51 (86) 66 (94) 29 (61).12 Success rate 60% (%) 0 (0) 1 (2) 1 (1) 18 (38).001 IQR/LSM ratio 0.30 (%) 0 (0) 5 (10) 3 (4) 3 (6).16 Fewer than 10 valid acquisitions (%) 0 (0) 0 (0) 0 (0) 16 (34).001 a P values from the Bonferroni correction for multiple testing were reported.
10 March 2013 FIBROSCAN AND BMI 302.e2 Supplementary Figure 1. Scatterplots of relationship between LSMs and BMI in different cohorts: (A) healthy subject cohort, (B) NAFLD patients with Brunt fibrosis stage 0, and (C) NAFLD patients with Brunt fibrosis stage 1.
11 302.e3 WONG ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 3 Supplementary Figure 2. Box plot showing (A) LSM values and (B) IQR over LSM ratios in different categories of BMI and (C) LSM values and (D) IQR/LSM ratio in different categories of waist circumference among healthy subjects.
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