Skip to main content
Top
Published in: Obesity Surgery 9/2016

01-09-2016 | Original Contributions

The Correlation Between Obesity-Related Diseases and Non-alcoholic Fatty Liver Disease in Women in the Pre-operative Evaluation for Bariatric Surgery Assessed by Transient Hepatic Elastography

Authors: Fernando de Barros, Sérgio Setúbal, José Manoel Martinho, Nathalie Carvalho Leite, Thais Guaraná, Ana Beatriz Soares Monteiro, Cristiane A Villela-Nogueira

Published in: Obesity Surgery | Issue 9/2016

Login to get access

Abstract

Background

Non-alcoholic fatty liver disease (NAFLD) is a common, severe disease in obese patients. However, NAFLD is usually underestimated by ultrasonography. Liver biopsy is not routinely done in bariatric surgery or during the follow-up. This study therefore examined the correlation between metabolic syndrome and NAFLD in morbidly obese patients based on an assessment using transient hepatic elastography (THE).

Material and Methods

This study involved 50 female patients in the pre-operative phase for bariatric surgery. Before surgery, we collected clinical, laboratory, and anthropometric variables. THE measurements were obtained using a FibroScan® device (Echosens, Paris, France), and steatosis was quantified using Controlled Attenuation Parameter software (CAP). Statistical analyses were done using linear correlation and the Kruskal-Wallis test.

Results

The mean of THE and CAP values were 7.56 ± 4.78 kPa and 279.94 ± 45.69 dB/m, respectively, and there was a significant linear correlation between the two measurements (r = 0.651; p < 0.001). The numbers of metabolic syndrome parameters did not influence the THE (p = 0.436) or CAP (p = 0.422) values. HbA1c and HOMA-IR showed a strong linear correlation with CAP (r = 0.643, p = 0.013 and r = 0.668, p = 0.009, respectively) and a tendency to some linear correlation with THE (r = 0.500, p = 0.05 and r = 0.500, p = 0.002, respectively).

Conclusion

Morbidly obese women submitted to FibroScan® presented a high prevalence of severe steatosis and advanced fibrosis in our sample. Insulin resistance parameters were correlated with steatosis, but less with fibrosis.
Literature
2.
go back to reference Adams LA, Lymp JF, St Sauver J, et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology. 2005;129(1):113–21.CrossRefPubMed Adams LA, Lymp JF, St Sauver J, et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology. 2005;129(1):113–21.CrossRefPubMed
3.
go back to reference Chalasani N, Younossi Z, Lavine JE, et al. American Gastroenterological Association; American Association for the Study of Liver Disease; American College of Gastroenterology. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, the American Gastroenterological Association. Gastroentelogy. 2012;142(7):1592–609.CrossRef Chalasani N, Younossi Z, Lavine JE, et al. American Gastroenterological Association; American Association for the Study of Liver Disease; American College of Gastroenterology. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, the American Gastroenterological Association. Gastroentelogy. 2012;142(7):1592–609.CrossRef
4.
go back to reference Caldwell SH, Oelsner DH, Iezzoni JC, et al. Cryptogenic cirrhosis: clinical characterization and risk factors for underlying disease. Hepatology. 1999;29(3):664–9.CrossRefPubMed Caldwell SH, Oelsner DH, Iezzoni JC, et al. Cryptogenic cirrhosis: clinical characterization and risk factors for underlying disease. Hepatology. 1999;29(3):664–9.CrossRefPubMed
5.
go back to reference El-Serag HB, Tran T, Everhart JE. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology. 2004;126:460–8.CrossRefPubMed El-Serag HB, Tran T, Everhart JE. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology. 2004;126:460–8.CrossRefPubMed
6.
go back to reference Youssef W, McCullough AJ. Diabetes mellitus, obesity, and hepatic steatosis. Semin Gastrointes Dis. 2002;13(1):17–30. Review. Youssef W, McCullough AJ. Diabetes mellitus, obesity, and hepatic steatosis. Semin Gastrointes Dis. 2002;13(1):17–30. Review.
7.
go back to reference Kimura Y, Hyogo H, Yamaqishi S, et al. Atorvastatin decreases serum levels of advanced glycation endproducts (AGEs) in nonalcoholic steatohepatitis (NASH) patients with dyslipidemia: clinical usefulness of AGEs as a biomarker for the attenuation of NASH. J Gastroenterol. 2010;45(7):750–7.CrossRefPubMed Kimura Y, Hyogo H, Yamaqishi S, et al. Atorvastatin decreases serum levels of advanced glycation endproducts (AGEs) in nonalcoholic steatohepatitis (NASH) patients with dyslipidemia: clinical usefulness of AGEs as a biomarker for the attenuation of NASH. J Gastroenterol. 2010;45(7):750–7.CrossRefPubMed
8.
go back to reference Yokohama S, Yoneda M, Haneda M, et al. Therapeutic efficacy of an angiotensin II receptor antagonist in patients with nonalcoholic steatohepatitis. Hepatology. 2004;40(5):1222–5.CrossRefPubMed Yokohama S, Yoneda M, Haneda M, et al. Therapeutic efficacy of an angiotensin II receptor antagonist in patients with nonalcoholic steatohepatitis. Hepatology. 2004;40(5):1222–5.CrossRefPubMed
9.
go back to reference Cazzo E, de Felice GF, Pareja JC, et al. Nonalcoholic fatty liver disease in morbidly obese subjects: correlation among histopatologic findings, biochemical features, and ultrasound evaluation. Obes Surg. 2014;24(4):666–8.CrossRefPubMed Cazzo E, de Felice GF, Pareja JC, et al. Nonalcoholic fatty liver disease in morbidly obese subjects: correlation among histopatologic findings, biochemical features, and ultrasound evaluation. Obes Surg. 2014;24(4):666–8.CrossRefPubMed
10.
go back to reference Saadeh S, Younossi ZM, Remer EM, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology. 2002;123(3):745–50.CrossRefPubMed Saadeh S, Younossi ZM, Remer EM, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology. 2002;123(3):745–50.CrossRefPubMed
11.
go back to reference Kleiner DE, Brunt EM, Van Natta M, et al. Nonalcoholic Steatohepatitis Clinical Research Network. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41(6):1313–21.CrossRefPubMed Kleiner DE, Brunt EM, Van Natta M, et al. Nonalcoholic Steatohepatitis Clinical Research Network. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41(6):1313–21.CrossRefPubMed
12.
go back to reference Ratziu V, Charlotte F, Heurtier A, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128(7):1898–906.CrossRefPubMed Ratziu V, Charlotte F, Heurtier A, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128(7):1898–906.CrossRefPubMed
13.
go back to reference 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(2):454–62.CrossRefPubMed 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(2):454–62.CrossRefPubMed
14.
go back to reference Myers RP, Pomier-Layrargues G, Kirsch R, et al. Feasibility and diagnostic performance of the FibroScan XL probe for liver stiffness measurement in overweight and obese patients. Hepatology. 2012;55(1):199–208.CrossRefPubMed Myers RP, Pomier-Layrargues G, Kirsch R, et al. Feasibility and diagnostic performance of the FibroScan XL probe for liver stiffness measurement in overweight and obese patients. Hepatology. 2012;55(1):199–208.CrossRefPubMed
15.
go back to reference Naveau S, Lamouri K, Pourcher G, et al. The diagnostic accuracy of transient elastography for the diagnosis of liver fibrosis in bariatric surgery candidates with suspected NAFLD. Obes Surg. 2014;24(10):1693–701.CrossRefPubMed Naveau S, Lamouri K, Pourcher G, et al. The diagnostic accuracy of transient elastography for the diagnosis of liver fibrosis in bariatric surgery candidates with suspected NAFLD. Obes Surg. 2014;24(10):1693–701.CrossRefPubMed
16.
go back to reference Sasso M, Beaugrand M, de Ledinghen V, et al. Controlled attenuation parameter (CAP): a novel VCTE guided ultrasonic attenuation measurement for the evaluation of hepatic steatosis: preliminary study and validation in a cohort of patients with chronic liver disease from various causes. Ultrasound Med Biol. 2010;36:1825–35.CrossRefPubMed Sasso M, Beaugrand M, de Ledinghen V, et al. Controlled attenuation parameter (CAP): a novel VCTE guided ultrasonic attenuation measurement for the evaluation of hepatic steatosis: preliminary study and validation in a cohort of patients with chronic liver disease from various causes. Ultrasound Med Biol. 2010;36:1825–35.CrossRefPubMed
17.
go back to reference de Lédinghen V, Vergniol J, Capdepont M, et al. Controlled attenuation parameter (CAP) for the diagnosis of steatosis: a prospective study of 5323 examinations. J Hepatol. 2014;60(5):1026–31.CrossRefPubMed de Lédinghen V, Vergniol J, Capdepont M, et al. Controlled attenuation parameter (CAP) for the diagnosis of steatosis: a prospective study of 5323 examinations. J Hepatol. 2014;60(5):1026–31.CrossRefPubMed
18.
go back to reference Sandrin L, Fourquet B, Hasquenoph JM, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29(12):1705–13.CrossRefPubMed Sandrin L, Fourquet B, Hasquenoph JM, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29(12):1705–13.CrossRefPubMed
19.
go back to reference Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.CrossRefPubMed Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.CrossRefPubMed
20.
go back to reference Bedogni G, Bellentani S, Miglioli L, et al. The Fatty Liver Index: simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol. 2006;2(6):33.CrossRef Bedogni G, Bellentani S, Miglioli L, et al. The Fatty Liver Index: simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol. 2006;2(6):33.CrossRef
21.
go back to reference Alberti KG, Alberti KG, Eckel RH, 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(16):1640–5.CrossRefPubMed Alberti KG, Alberti KG, Eckel RH, 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(16):1640–5.CrossRefPubMed
22.
go back to reference Genuth S, Alberti KG, Bennett P, et al. Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care. 2003;26(11):3160–7.CrossRefPubMed Genuth S, Alberti KG, Bennett P, et al. Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care. 2003;26(11):3160–7.CrossRefPubMed
23.
go back to reference de Lédinghen V, Vergniol J, Foucher J, et al. Non-invasive diagnosis of liver steatosis using Controlled Attenuation Parameter (CAP) and transient elastography. Liver Int. 2012;32(6):911–8.CrossRefPubMed de Lédinghen V, Vergniol J, Foucher J, et al. Non-invasive diagnosis of liver steatosis using Controlled Attenuation Parameter (CAP) and transient elastography. Liver Int. 2012;32(6):911–8.CrossRefPubMed
24.
go back to reference Lazo M, Clark JM. The epidemiology of nonalcoholic fatty liver disease: a global perspective. Semin Liver Dis. 2008;28(4):339–50.CrossRefPubMed Lazo M, Clark JM. The epidemiology of nonalcoholic fatty liver disease: a global perspective. Semin Liver Dis. 2008;28(4):339–50.CrossRefPubMed
25.
go back to reference Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther. 2011;34(3):274–85.CrossRefPubMed Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther. 2011;34(3):274–85.CrossRefPubMed
26.
27.
go back to reference Vanni E, Mezzabotta L, Bugianesi E. NAFLD and hepatocellular carcinoma: how big a problem is this really? Curr Hepatology Rep. 2014;13(2):113–8.CrossRef Vanni E, Mezzabotta L, Bugianesi E. NAFLD and hepatocellular carcinoma: how big a problem is this really? Curr Hepatology Rep. 2014;13(2):113–8.CrossRef
28.
go back to reference Verna EC. Liver biopsy at the time of bariatric surgery: a benefit for patients and the medical community. Semin Liver Dis. 2014;34(1):1–6.CrossRefPubMed Verna EC. Liver biopsy at the time of bariatric surgery: a benefit for patients and the medical community. Semin Liver Dis. 2014;34(1):1–6.CrossRefPubMed
29.
go back to reference Foucher J, Castera L, Bernard PH, et al. Prevalence and factors associated with failure of liver stiffness measurement using FibroScan in a prospective study of 2114 examinations. Eur J Gastroenterol Hepatol. 2006;18:411–2.CrossRefPubMed Foucher J, Castera L, Bernard PH, et al. Prevalence and factors associated with failure of liver stiffness measurement using FibroScan in a prospective study of 2114 examinations. Eur J Gastroenterol Hepatol. 2006;18:411–2.CrossRefPubMed
30.
go back to reference Petta S, Maida M, Macaluso FS, et al. The severity of steatosis influences liver stiffness measurement in patients with nonalcoholic fatty liver disease. Hepatology. 2015;62(4):1101–10.CrossRefPubMed Petta S, Maida M, Macaluso FS, et al. The severity of steatosis influences liver stiffness measurement in patients with nonalcoholic fatty liver disease. Hepatology. 2015;62(4):1101–10.CrossRefPubMed
31.
32.
go back to reference De Ledinghen V, Vergniol J, Foucher J, et al. Feasibility of liver transient elastography with FibroScan using a new probe for obese patients. Liver Int. 2010;30:1043–8.CrossRefPubMed De Ledinghen V, Vergniol J, Foucher J, et al. Feasibility of liver transient elastography with FibroScan using a new probe for obese patients. Liver Int. 2010;30:1043–8.CrossRefPubMed
33.
go back to reference Leite NC, Villela-Nogueira CA, Pannain VL, et al. Histopathological stages of nonalcoholic fatty liver disease in type 2 diabetes: prevalences and correlated factors. Liver Int. 2011;31(5):700–6.CrossRefPubMed Leite NC, Villela-Nogueira CA, Pannain VL, et al. Histopathological stages of nonalcoholic fatty liver disease in type 2 diabetes: prevalences and correlated factors. Liver Int. 2011;31(5):700–6.CrossRefPubMed
34.
go back to reference Kalra S, Vithalani M, Gulati G, et al. Study of prevalence of nonalcoholic fatty liver disease (NAFLD) in type 2 diabetes patients in India (SPRINT). J Assoc Physicians India. 2013;61(7):448–53.PubMed Kalra S, Vithalani M, Gulati G, et al. Study of prevalence of nonalcoholic fatty liver disease (NAFLD) in type 2 diabetes patients in India (SPRINT). J Assoc Physicians India. 2013;61(7):448–53.PubMed
35.
go back to reference Ratziu V, Marchesini G, Romero-Gomez M, et al. The HOMA index is a useful tool for risk stratification of advanced fibrotic disease in a large cohort of European NAFLD patients. J Hepatol. 2013;58(1):S548–9. Ratziu V, Marchesini G, Romero-Gomez M, et al. The HOMA index is a useful tool for risk stratification of advanced fibrotic disease in a large cohort of European NAFLD patients. J Hepatol. 2013;58(1):S548–9.
36.
go back to reference Dixon JB, Bhathal PS, O'Brien PE. Non alcoholic fatty liver disease: predictors of non alcoholic steatohepatitis and liver fibrosis in the severely obese. Gastroenterology. 2001;121(1):91–100.CrossRefPubMed Dixon JB, Bhathal PS, O'Brien PE. Non alcoholic fatty liver disease: predictors of non alcoholic steatohepatitis and liver fibrosis in the severely obese. Gastroenterology. 2001;121(1):91–100.CrossRefPubMed
37.
go back to reference Bae JC, Cho YK, Lee WY, et al. Impact of nonalcoholic fatty liver disease on insulin resistance in relation to HbA1c levels in nondiabetic subjects. Am J Gastroenterol. 2010;105(11):2389–95.CrossRefPubMed Bae JC, Cho YK, Lee WY, et al. Impact of nonalcoholic fatty liver disease on insulin resistance in relation to HbA1c levels in nondiabetic subjects. Am J Gastroenterol. 2010;105(11):2389–95.CrossRefPubMed
38.
go back to reference Ma H, Xu C, Xu L, et al. Independent association of HbA1c and nonalcoholic fatty liver disease in an elderly Chinese population. BMC Gastroenterol. 2013;13:3.CrossRefPubMedPubMedCentral Ma H, Xu C, Xu L, et al. Independent association of HbA1c and nonalcoholic fatty liver disease in an elderly Chinese population. BMC Gastroenterol. 2013;13:3.CrossRefPubMedPubMedCentral
39.
go back to reference Souza MR, Diniz Mde F, Medeiros-Filho JE, et al. Metabolic syndrome and risk factors for non-alcoholic fatty liver disease. Arq Gastroenterol. 2012;49(1):89–96.CrossRefPubMed Souza MR, Diniz Mde F, Medeiros-Filho JE, et al. Metabolic syndrome and risk factors for non-alcoholic fatty liver disease. Arq Gastroenterol. 2012;49(1):89–96.CrossRefPubMed
40.
go back to reference Sung KC, Wild SH, Kwag HJ, et al. Fatty liver, insulin resistance, and features of metabolic syndrome: relationships with coronary artery calcium in 10,153 people. Diabetes Care. 2012;35(11):2359–64.CrossRefPubMedPubMedCentral Sung KC, Wild SH, Kwag HJ, et al. Fatty liver, insulin resistance, and features of metabolic syndrome: relationships with coronary artery calcium in 10,153 people. Diabetes Care. 2012;35(11):2359–64.CrossRefPubMedPubMedCentral
41.
go back to reference Miyake T, Kumagi T, Hirooka M, et al. Body mass index is the most useful predictive factor for the onset of nonalcoholic fatty liver disease: a community-based retrospective longitudinal cohort study. J Gastroenterol. 2013;48(3):413–22.CrossRefPubMed Miyake T, Kumagi T, Hirooka M, et al. Body mass index is the most useful predictive factor for the onset of nonalcoholic fatty liver disease: a community-based retrospective longitudinal cohort study. J Gastroenterol. 2013;48(3):413–22.CrossRefPubMed
42.
go back to reference Hyogo H, Yamagishi SI, Maeda S, et al. sRAGE is associated with low waist circumference and Hb levels in NAFLD. Cent Eur J Med. 2013;8(6):830–4. Hyogo H, Yamagishi SI, Maeda S, et al. sRAGE is associated with low waist circumference and Hb levels in NAFLD. Cent Eur J Med. 2013;8(6):830–4.
43.
go back to reference Hyogo H, Yamagishi S. Advanced glycation end products (AGEs) and their involvement in liver disease. Curr Pharm Des. 2008;14(10):969–72.CrossRefPubMed Hyogo H, Yamagishi S. Advanced glycation end products (AGEs) and their involvement in liver disease. Curr Pharm Des. 2008;14(10):969–72.CrossRefPubMed
Metadata
Title
The Correlation Between Obesity-Related Diseases and Non-alcoholic Fatty Liver Disease in Women in the Pre-operative Evaluation for Bariatric Surgery Assessed by Transient Hepatic Elastography
Authors
Fernando de Barros
Sérgio Setúbal
José Manoel Martinho
Nathalie Carvalho Leite
Thais Guaraná
Ana Beatriz Soares Monteiro
Cristiane A Villela-Nogueira
Publication date
01-09-2016
Publisher
Springer US
Published in
Obesity Surgery / Issue 9/2016
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-016-2054-y

Other articles of this Issue 9/2016

Obesity Surgery 9/2016 Go to the issue