Abstract
Background
Nonalcoholic fatty pancreas disease (NAF-P) is strongly linked with nonalcoholic fatty liver disease (NAFLD), but its relationship with advanced liver disease is unknown.
Aims
This study investigated the association between NAF-P and both advanced fibrosis and nonalcoholic steatohepatitis (NASH).
Methods
This retrospective study evaluated adults with biopsy-proven NAFLD with a sonogram within 1 year of liver biopsy. NAF-P was diagnosed by comparing the echogenicity of the pancreas to the kidney and was graded by severity. The primary outcome was the effect of NAF-P on the presence of advanced fibrosis and NASH, while secondary outcomes included the association of extensive NAF-P (grade II/III). Propensity score matching for independent risk factors of advanced fibrosis (age, gender, body mass index, and diabetes) was performed.
Results
One hundred and four patients were included in the study and 91 (87.5%) had NAF-P. After propensity score matching, NAF-P was significantly associated with advanced fibrosis (OR 10.52, p < 0.001) but not NASH (p = 0.27). Extensive NAF-P was predictive of advanced fibrosis (OR 3.35, p = 0.006) and NASH (OR 5.37, p < 0.001). NAF-P had a negative predictive value (NPV) of 93% for advanced fibrosis. When matching for the NAFLD fibrosis score in addition to the variables above, both NAF-P (OR 5.36, p = 0.001) and extensive NAF-P (OR 5.38, p = 0.002) still significantly predicted advanced fibrosis.
Conclusion
NAF-P is predictive of advanced fibrosis, even when controlling for independent predictors of advanced fibrosis and the NAFLD fibrosis score. NAF-P has an excellent NPV and is a safe, inexpensive finding that can rule out advanced fibrosis.
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References
Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology of nonalcoholic fatty liver disease. Dig Dis. 2010;28:155–161.
Browning J, Szczepaniak L, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004;116:1413–1419.
Matteoni C, Younossi Z, Gramlich T, Bopari N, Liu Y, Mccullough A. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116:1413–1419.
Dulai PS, Singh S, Patel J, et al. Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: systematic review and meta-analysis. Hepatology. 2017;65:1557–1565.
Lammert E, Cleaver O, Melton D. Role of endothelial cells in early pancreas and liver development. Mech Dev. 2003;120:59–64.
Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest. 2005;115:1343–1351.
Lee JS, Kim SH, Jun DW, et al. Clinical implications of fatty pancreas: correlations between fatty pancreas and metabolic syndrome. World J Gastroenterol. 2009;15:1869–1875.
Boyd W. Text-book of pathology: An introduction to medicine. 3rd ed. Philadelphia: Lea & Febiger; 1938.
Ou HY, Wang CY, Yang YC, Chen MF, Chang CJ. The association between nonalcoholic fatty pancreas disease and diabetes. PLoS ONE. 2013. https://doi.org/10.1371/journal.pone.0062561.
Wang CY, Ou HY, Chen MF, Chang TC, Chang CJ. Enigmatic ectopic fat: prevalence of nonalcoholic fatty pancreas disease and its associated factors in a Chinese population. J Am Heart Assoc. 2014;3:e000297.
Lesmana C, Pakasi L, Inggriani S, Aidawati M, Lesmana L. Prevalence of nonalcoholic fatty pancreas disease (NAFPD) and its risk factors among adult medical check-up patients in a private hospital: a large cross sectional study. BMC Gastroenterol. 2015;15:174.
Della Corte C, Mosca A, Majo F, et al. Nonalcoholic fatty pancreas disease and Nonalcoholic fatty liver disease: more than ectopic fat. Clin Endocrinol (Oxf). 2015;83:656–662.
Uygun A, Kadayifci A, Demirci H, et al. The effect of fatty pancreas on serum glucose parameters in patients with nonalcoholic steatohepatitis. Eur J Intern Med. 2015;26:37–41.
Khoury T, Asombang AW, Berzin TM, Cohen J, Pleskow DK, Mizrahi M. The clinical implications of fatty pancreas: a concise review. Dig Dis Sci. 2017;62:2658–2667. https://doi.org/10.1007/s10620-017-4700-1.
Hori M, Takahashi M, Hiraoka N, et al. Association of pancreatic fatty infiltration with pancreatic ductal adenocarcinoma. Clin Transl Gastroenterol. 2014;5:e53.
Lingvay I, Esser V, Legendre JL, et al. Noninvasive quantification of pancreatic fat in humans. J Clin Endocrinol Metab. 2009;94:4070–4076.
Yamazaki H, Tauchi S, Kimachi M, et al. The association between pancreatic fat and incidence of metabolic syndrome: a 5-year Japanese cohort study. J Gastroenterol Hepatol. 2018. https://doi.org/10.1111/jgh.14266.
Heni M, Machann J, Staiger H, et al. Pancreatic fat is negatively associated with insulin secretion in individuals with impaired fasting glucose and/or impaired glucose tolerance: a nuclear magnetic resonance study. Diabetes Metab Res Rev. 2010;26:200–205.
Mathur A, Marine M, Lu D, et al. Nonalcoholic fatty pancreas disease. HPB (Oxford). 2007;9:312–318.
Seeff LB, Everson GT, Morgan TR, et al. Complication rate of percutaneous liver biopsies among persons with advanced chronic liver disease in the HALT-C trial. Clin Gastroenterol Hepatol. 2010;8:877–883.
Lupşor-Platon M, Stefǎnescu H, Muresçan D, et al. Noninvasive assessment of liver steatosis using ultrasound methods. Med Ultrason. 2014;16:236–245.
Zezos P, Renner EL. Liver transplantation and nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:15532–15538.
Xiao G, Zhu S, Xiao X, et al. Comparison of laboratory tests, ultrasound, or MRE to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology. 2017;66:1486–1501.
Myers RP, Pomier-Layrargues G, Kirsch R, et al. Discordance in fibrosis staging between liver biopsy and transient elastography using the FibroScan XL probe. J Hepatol. 2012;56:564–570.
Szabo G, Petrasek J. Inflammasome activation and function in liver disease. Nat Rev Gastroenterol Hepatol. 2015;12:387–400.
Ceccarelli S, Panera N, Mina M, et al. LPS-induced TNF-α factor mediates pro-inflammatory and pro-fibrogenic pattern in nonalcoholic fatty liver disease. Oncotarget. 2015;6:41434–41452.
Oben JA, Patel T, Mouralidarane A, et al. Maternal obesity programmes offspring development of nonalcoholic fatty pancreas disease. Biochem Biophys Res Commun. 2010;394:24–28.
Patel NS, Peterson MR, Lin GY, et al. Insulin resistance increases MRI-estimated pancreatic fat in nonalcoholic fatty liver disease and normal controls. Gastroenterol Res Pract. 2013;2013:1–8.
Saadeh S, Younossi ZM, Remer EM, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology. 2002;123:745–750.
Catanzaro R, Cuffari B, Italia A, Marotta F. Exploring the metabolic syndrome: nonalcoholic fatty pancreas disease. World J Gastroenterol. 2016;22:7660–7675.
Sepe PS, Ohri A, Sanaka S, et al. A prospective evaluation of fatty pancreas by using EUS. Gastrointest Endosc. 2011;73:987–993.
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Sonal Kumar has received an advisory meeting honorarium from Gilead Sciences. The other authors have no conflicts to disclose.
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Rosenblatt, R., Mehta, A., Snell, D. et al. Ultrasonographic Nonalcoholic Fatty Pancreas Is Associated with Advanced Fibrosis in NAFLD: A Retrospective Analysis. Dig Dis Sci 64, 262–268 (2019). https://doi.org/10.1007/s10620-018-5295-x
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DOI: https://doi.org/10.1007/s10620-018-5295-x