MESTRADO INTEGRADO EM MEDICINA
MR ASSESSMENT OF LIVER AND
PANCREAS STEATOSIS IN CHRONIC
LIVER DISEASES
João Pedro Ferreira Silva Vieira
ARTIGO ORIGINAL
MESTRADO INTEGRADO EM MEDICINA
INSTITUTO DE CIÊNCIAS BIOMÉDICAS ABEL SALAZAR, UNIVERSIDADE DO PORTO
MAIO 2019
MR Assessment of Liver and Pancreas Steatosis in
Chronic Liver Diseases
João Pedro Ferreira Silva Vieira
1Orientador: Prof. Doutora Maria Manuela França Oliveira
2Coorientador: Dr. João Filipe Pinheiro de Amorim
31 Estudante do 6º ano do mestrado integrado em Medicina, Instituto de Ciências Biomédicas
Abel Salazar, Universidade do Porto Email: joaopfsvieira@gmail.com
2 Diretora do Serviço de Radiologia, Centro Hospitalar Universitário do Porto; Professora
Catedrática, Convidada - Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto.
3 Médico Interno de Formação Específica de Radiologia no Serviço de Radiologia, Centro
O autor,
João Pedro Ferreira Silva Vieira
A Orientadora,
Professora Dra. Maria Manuela França Oliveira
O Coorientador,
Dr. João Filipe Pinheiro de Amorim
Agradecimentos
É com orgulho que findo esta etapa que foram 6 anos da minha vida, gostaria de deixar o meu agradecimento a todos os que me acompanharam de alguma forma neste caminho e que o tornaram possível.
Em primeiro lugar, quero agradecer à Professora Dra. Manuela França, por me ter recebido no Departamento de Radiologia e ter ajudado em todo o processo de elaboração deste trabalho. Foi uma honra e um prazer a colaboração neste último ano, tendo feito a diferença na minha formação académica.
Agradeço também ao Dr. João Amorim, pela ajuda e acompanhamento.
Aos meus pais e irmã, agradeço todo o apoio e inspiração que me deram ao longo destes anos, por serem um exemplo de trabalho e dedicação.
À Ana Isabel Ferreira, obrigado pelo carinho, paciência, apoio incondicional e incentivo. Por fim, agradeço a todos os meus amigos que fui encontrando ao longo da minha jornada 2013-2019, com quem partilhei alegrias, conhecimentos e ideias.
Financiamento
Este trabalho foi parcialmente financiado por uma bolsa de investigação do departamento de ensino e investigação do Centro Hospitalar do Porto (DEFI:309/12(213-DEFI/251-CES)). O financiador não entreviu no desenho do estudo, na recolha de dados ou na sua análise.
Resumo Objetivo
Comparar a esteatose pancreática e hepática mediante a determinação da proton density fat
fraction (PDFF) por ressonância magnética (RM), em pacientes com doença hepática crónica.
Material e métodos
Estudo transversal de 46 pacientes adultos com biopsia hepática por hepatite viral crónica (n=19) ou por outras doenças hepáticas crónicas de etiologia não-alcoólica (n=27). A biopsia hepática foi utilizada como referência para a gradação da esteatose hepática. Todos os doentes foram submetidos a uma avaliação clínica e estudo por RM com uma sequência multi-eco de gradiente chemical shift-encoded, para a quantificação da PDFF no fígado e pâncreas. Utilizou-se o coeficiente de correlação de Spearman para calcular a correlação entre a PDFF hepática e os graus histológicos de esteatose hepática, e entre a PDFF pancreática e a esteatose hepática, tanto com os graus histológicos de esteatose como com a PDFF hepática. O T-test foi realizado para comparar variáveis contínuas / ordinais nos grupos de hepatite viral crónica e no grupo das outras doenças hepáticas crónicas de etiologia não-alcoólica. As variáveis categóricas foram avaliadas mediante a prova de chi-quadrado.
Resultados
Observou-se uma correlação significativa entre a PDFF hepática e os graus de esteatose (RS=0,875, p<0,001). Também se evidenciou uma correlação positiva entre a PDFF pancreática e
tanto os graus de esteatose hepática (RS=0.573, p<0.001), como a PDFF hepática (RS=0.536,
p<0.001). No subgrupo de doentes com doenças hepáticas crónica de etiologia não alcoólica, foi mantida uma correlação positiva significativa entre a PDFF pancreática e hepática (RS=0.632,
p<0.001) e com a esteatose hepática (RS=0.608, p<0.001). Estas correlações não se verificaram,
contudo, no subgrupo de doentes com hepatite viral crónica.
Conclusão
A deposição pancreática de gordura correlaciona-se com a esteatose hepática em doentes com doenças hepáticas crónica de etiologia não alcoólica, mas não doentes com hepatite viral crónica.
Palavras chave: Adulto; Pâncreas; Fígado; Esteatose; Hepatite crónica; Doenças hepáticas;
Abstract Aim
To compare pancreatic and hepatic steatosis by means of magnetic resonance (MR) determined proton density fat fraction (PDFF) in patients with chronic liver disease.
Material and Methods
This cross-sectional study included 46 adult patients submitted to liver biopsy during their investigation of chronic viral hepatitis (n=19) or other chronic non-alcoholic liver diseases (NALD) (n=27). Liver biopsy was used as the gold standard for hepatic steatosis diagnosing and grading. All patients underwent clinical evaluation and MR imaging with a multi-echo chemical shift-encoded (MECSE) gradient echo sequence for liver and pancreas PDFF quantification. The Spearman correlation coefficient was used to calculate the degree of association between hepatic PDFF and steatosis grades, and between pancreatic PDFF and both steatosis grades and hepatic PDFF measurements. The T–test was performed to compare continuous/ordinal variables across the chronic viral hepatitis and the NALD group. Categorical variables were evaluated by the chi-squared test.
Results
There was a significant correlation between hepatic PDFF and steatosis grades (RS =0.875,
p<0.001). Also, there was a positive correlation between pancreatic PDFF and both hepatic steatosis grades (RS=0.573, p<0.001) and hepatic PDFF measurements (RS=0.536, p<0.001). In
the subgroup of patients with chronic NALD, the significant positive correlation between pancreatic PDFF and both hepatic PDFF (RS=0.632, p<0.001) and liver steatosis (RS=0.608,
p<0.001) was maintained, but not in the subgroup of patients with viral hepatitis.
Conclusion
Pancreatic fat deposition is correlated with hepatic steatosis in patients with chronic NALD but not in those with chronic viral hepatitis.
Keywords: Adult; Pancreas; Liver; Steatosis; Chronic Hepatitis; Liver Diseases; Magnetic
Abbreviations
BMI - Body Mass Index CSE - Chemical Shift-Encoded CT - Computed Tomography ET - Echo Time
MR - Magnetic Resonance
MRS - Magnetic Resonance Spectroscopy MECSE - Multi-Echo Chemical Shift Encoded NALD - Non-Alcoholic Liver Diseases
NAFLD - Non-Alcoholic Fatty Liver Disease NASH - Non-Alcoholic Steatohepatitis PDFF - Proton Density Fat Fraction ROI - Region of Interest
Índice
Introduction ... 1
Materials and Methods ... 2
Results ... 4
Discussion ... 6
Lista de Tabelas
Table I - Data are expressed as mean with standard deviation in parentheses unless otherwise noted. ... 11
Lista de Figuras
Figure 1 - Number of patients by liver histologic steatosis grade ... 12
Figure 2 - Correlation of the Liver PDFF with Liver histologic steatosis grade ... 13
Figure 3 - Correlation of Pancreatic PDFF with Liver histologic steatosis grade ... 14
Figure 4 - Correlation of Pancreatic PDFF with Liver PDFF ... 15
Figure 5 - Correlation of Pancreatic PDFF with Liver PDFF in each subgroup: Non-alcoholic Liver Disease and Chronic Viral Hepatitis ... 16
Introduction
Pancreatic steatosis is a common yet neglected pathological condition. According to Smits et al, the term pancreatic steatosis describes not only the accumulation of fat in the islet cells or in acinar cells, but also the fat accumulation in pancreatic adipocytes. [1] Pancreatic steatosis is linked to chronic pancreatitis and pancreatic adenocarcinoma induction. [2]
During pancreatic transplant procedures, a direct inspection of the organ can classify pancreatic steatosis as mild or massive, [3] while in the histological examinations, the increased number of pancreatic fat is recognized in the pancreatic tissue. [4] Biopsy and histological evaluation are considered gold standards to evaluate the presence of hepatic and pancreatic steatosis, but there are several limitations with this technique. Liver biopsy is invasive and associated with morbidity and even mortality, being operator dependent and subject to high variability [5]. Biopsy of the pancreatic parenchyma for quantifying steatosis is, therefore, avoided for ethical reasons. Imaging techniques, such as ultrasonography, computed tomography (CT), and magnetic resonance (MR) imaging, can be used to diagnose pancreatic steatosis. [1, 6, 7] Transabdominal ultrasonography has some disadvantages: the full pancreas is not always visible (especially in obese patients), it is not possible to distinguish pancreatic fibrosis from steatosis, and it is necessary to compare the pancreas echogenicity with other reference organ, usually the kidney or the liver. [1, 6]
On non-enhanced CT images, the steatotic pancreas shows low attenuation of the parenchyma. [1] The quantification of pancreatic steatosis on non-contrast CT can be done by comparing the pancreatic attenuation to the splenic attenuation. [8] However, there are no defined cut-off values for pancreatic steatosis, being not feasible to distinguish it from the fatty replacement of pancreatic parenchyma that is often seen with aging. [6]
Abdominal MR imaging is considered the best imaging technique to evaluate liver and pancreatic steatosis as it can quantify pancreatic fat with high accuracy. [6, 9-14] Several methods have been proposed to measure parenchymal fat, including 2-point Dixon, 3-point Dixon, advanced complex-based chemical shift-encoded (CSE) methods and magnetic resonance spectroscopy (MRS). [9] Advanced multi-echo CSE (MECSE) gradient-echo curve-fitting and computational modeling methods have been used to assess the proton density fat fraction (PDFF) from MR as a biomarker of pancreatic steatosis. [10]
MECSE quantification of liver PDFF was already accepted as the best imaging biomarker of hepatic steatosis. [11-14] Hepatic steatosis is the hallmark of non-alcoholic fatty liver disease
(NAFLD), being frequently associated with metabolic syndrome. This syndrome includes central obesity, glucose intolerance or diabetes, hypertension and dyslipidemia. [15, 16] In this sense, hepatic steatosis is not considered a clinical diagnosis but a common manifestation present in many diffuse liver disorders, such as alcoholic liver disease and viral hepatitis, being a common histological feature in both chronic hepatitis C and chronic hepatitis B. [17-19]
The effects of pancreatic fatty infiltration have been less well studied, but it has been strongly associated with metabolic syndrome, [20] both pancreatic and hepatic steatosis being directly associated with general obesity. [21] A recent study suggested a positive correlation between hepatic and pancreatic steatosis in patients with NAFLD, using MR imaging PDFF quantification. [22] Even though hepatitis viral infection has also been reported as a cause of pancreatic steatosis, little is still known about the possible causes of pancreatic fat deposition in this specific clinical scenario. [1, 6, 7]
The aim of this study was to assess liver and pancreas PDFF by using a MECSE MR sequence, comparing the relationship between organs and the influence of the underlying chronic liver disease (viral infection versus other non-alcoholic liver diseases).
Materials and Methods
Study Design and Patient Population:
This is a cross-section analysis of a prospective single-institution cohort study, with 99 consecutive adult patients with chronic viral hepatitis, [14] NAFLD or under investigation for elevated liver enzyme levels, having a clinical indication for liver biopsy. All patients were recruited for an abdominal MR examination. Patients’ clinical and physical examination data were collected from the hospital files. The histological and MR imaging examination were consecutively performed in the same institution, over a period of 11 months.
The study was approved by the Institution Ethics Committee, and written informed consent was obtained from all the patients.
Exclusion Criteria:
Exclusion criteria considered were severe claustrophobia; pacing devices or other incompatible medical devices and refusal to perform an MR imaging examination. Moreover, patients with liver transplant (n=26); history of alcoholic liver disease (n=10), toxic hepatitis (n=4) or hemochromatosis (n=8); or patients with any known history or imaging findings concerning for hepatic or pancreatic malignancy were also excluded (n=5).
Clinical evaluation:
The Body Mass Index (BMI) and the diabetic status assessment were recorded. Histopathological liver analysis:
All 46 finally included patients underwent liver biopsies. Only one biopsy was performed per patient. Biopsies were scored by two experienced liver pathologists, blinded to the MR imaging results, evaluating the liver biopsy samples in consensus. All cases were diagnosed as chronic liver disease. The grade of hepatic steatosis was based on the proportion of hepatocytes containing fat vesicles, being expressed semi-quantitatively on a scale of 0-3 (grade 0, <5%-no steatosis; grade 1, 5-33%-mild steatosis; grade 2, 33%-66%-moderate steatosis; grade 3, >66%-severe steatosis). [23]
MR Imaging Protocol:
The hepatic and pancreatic PDFF were determined by using a 3 Tesla (Achieva TX, Philips Healthcare, The Netherlands) MECSE gradient-echo MR imaging sequence obtained in a single breath hold 2D multi-slice acquisition. [14]
The MECSE sequence was constructed with a Repetition Time (RT) = 10 ms, and multiple Echo Times (ET) = 0.99, 1.69, 2.39, 3.09, 3.79, 4.49, 5.19, 5.89, 6.59, 7.29, 7.99, 8.69 ms. The flip angle was 10° to minimize the T1 bias. The in-plane voxel dimensions were of 3x3mm, with a slice thickness of 7 mm and 0.3 mm gap between slices. The total acquisition time was of 12s, allowing for expiratory phase breath hold acquisition, and imaging the whole liver and the pancreas during a single breath-hold acquisition.
Image Analysis:
Images were exported as raw data in magnitude and phase to pixel-wise quantify PDFF using QLiver® software (QUIBIM, Valencia, Spain), based on non-linear least squares analysis by
Levenberg–Marquardt algorithm. The pixel PDFF was the ratio between the normalized fat proton density and the total (fat and water) proton density. [24]
One radiologist (MF, 10 years of experience on abdominal imaging), blinded to clinical and histological data, reviewed the images and performed quantification of the hepatic and pancreatic PDFF, by placing regions of interest (ROI) within the biopsied liver segment (ROI of 8mm) and within the head of the pancreas (ROI of 6mm). Prior MR imaging studies already describe no significant difference regarding fat fractions among the 3 regions of pancreas (head, body and tail).[22, 25] The ROIs were placed on homogeneous areas avoiding any artifact, vessel, and adjacent visceral fat.
Statistical Analysis:
Groups’ data are presented as mean (±standard deviation) or median and interquartile range. The Spearman correlation coefficient was used to calculate the degree of association between continuous and/or ordinal variables. The T–test was performed to compare continuous/ordinal variables and the categorical variables were evaluated by the chi-squared test. Differences of PDFF values between histological groups of hepatic steatoses were assessed with one-way analysis of variance.
All statistical analyses were performed using SPSS software package (version 24; SPSS, IBM, Chicago, Ill). For all tests, a two-tailed p value of less than 0.05 was considered as statistically significant.
Results
The study population included 46 patients (22 men and 24 women), with age ranged from 19 to 77 years (mean age was 44 years). (Table I). Regarding the clinical and histological diagnosis, 19 patients had chronic viral hepatitis (hepatitis C virus (n=14) and hepatitis B virus (n=5)) and 27 have chronic Non-Alcoholic Liver Diseases (NALD), including non-alcoholic steatohepatitis (NASH) (n=8), autoimmune hepatitis (n=8) and a group of patients under investigation for permanent elevated liver enzyme levels without a specific diagnosis of liver disease (n=11).
The mean (±standard deviation) MR imaging-determined liver fat content was 9.6±4%. The median and interquartile range were: 8.6 (4.0-23.6)%.
Using the Spearman (RS) correlation analysis, there was a positive correlation between BMI and both hepatic PDFF (RS=0.405, p<0.004) and pancreas PDFF (RS=0.408, p<0.002) whereas there was no correlation between age and both hepatic PDFF (RS=0.162, p<0.141) and pancreas PDFF (RS=0.103, p<0.241).
In the general study population, the liver PDFF increased significantly with increasing the histological-determined hepatic steatosis grade (p<0.001). An excellent positive correlation was demonstrated between the liver PDFF and the histological steatosis grade (RS=0.875, p<0.001). (Fig. 2)
The mean MR imaging-determined pancreatic fat content was 11.5±6.3%. The median and interquartile range were: 9.8 (9.6-13.4)%.
The pancreatic PDFF measurements were significantly different between patients with no liver steatosis (grade 0) and patients with liver steatosis (histologic grade 1 or greater) (p<0.001). (Fig. 3)
Pancreatic PDFF values also demonstrated a positive correlation with hepatic histologic steatosis grades (RS=0.536, p<0.001) and with hepatic PDFF measurements (RS=0.573, p<0.001). (Fig. 4) Subgroup analysis:
In the subgroup of patients with chronic NALD, pancreatic PDFF values were significantly different between different histological grades of liver steatosis (p<0.05). Furthermore, a significant positive correlation was found between pancreatic PDFF and both hepatic PDFF (RS=0.632, p<0.001) and histologic liver steatosis (RS=0.608, p<0.001).
On the other hand, in the subgroup of patients with chronic viral hepatitis, no significant correlation was found between pancreatic and hepatic PDFF nor grades of histological liver steatosis. The values of pancreatic PDFF were not significantly different between the different grades of histological liver steatosis (p>0.05). (Fig. 5)
There was no statistically significant difference across NALD group and chronic viral hepatitis group for gender (P=0.08), BMI (P=0.09), age (P=0.10) nor diabetes status (P=0.63).
Discussion
In this study, MECSE MR-derived PDFF measurements allowed a non-invasive quantification of the pancreatic and hepatic fat content in a cohort of patients with diffuse liver diseases of different etiologies. As expected, a positive strong correlation between hepatic PDFF values and histologic steatosis grades was found, in concordance with the results from previous studies that have confirmed liver PDFF measurements as a reliable tool to assess hepatic steatosis. [11-14] The positive correlation between liver PDFF and BMI is also in agreement with a previous study and is comprehensible as hepatic steatosis is frequently related with metabolic syndrome and obesity. [15, 16] A positive correlation between pancreas PDFF and BMI also exists. The effect of metabolic syndrome on the pancreas is not so well characterized, but there is increasing evidence describing the association of obesity and pancreatic steatosis. [20, 21]
We could not find any significant correlation between aging and pancreas PDFF, which is not in line with prior studies. [26] This might be explained because previous studies only focused on healthy patients without known liver disease, and therefore without a predisposing factor for pancreatic steatosis. Moreover, in the previous studies, imaging evaluation was performed by ultrasonography whereas we used MR imaging, which is considered the best imaging technique to evaluate pancreatic steatosis. A prior study involving only NAFLD patients was in accordance with our conclusion. [22]
In this study population, a positive correlation was also found between pancreatic PDFF and hepatic steatosis, suggesting a relationship between hepatic and pancreatic steatosis. However, when the population is split in viral and non-viral subgroups, the positive correlation between pancreatic PDFF and both hepatic PDFF and histologic liver steatosis is only found in the subgroup of NALD, but not in patients with chronic viral hepatitis.
Hepatic diseases, especially chronic viral hepatitis, have been suggested to be a cause of pancreatic steatosis by several recent review articles. [1, 6, 7] Nevertheless, there is a general lack of information about this topic with only a case report of a patient with chronic hepatitis B and pancreatic steatosis supporting the hypothesis that chronic viral hepatitis is linked with pancreatic steatosis. [27] Our results suggest no relationship between viral infection and
involved in the liver and pancreas fat accumulation. NAFLD is associated with metabolic syndrome and similar risk factors have also been linked with pancreas steatosis. [16, 20-22] In a previous study, the prevalence rate for hepatic steatosis in Autoimmune Hepatitis is within the expected rate for the general population. [28] The influence of autoimmune hepatitis in pancreatic steatosis is not defined yet.
There were no significant differences across NALD group and chronic viral hepatitis group for gender, BMI, age nor diabetes status. As the two subgroups were not significantly different in these characteristics, they seem not to have any role in the differences found in the two subsets of patients.
The clinical associations of pancreatic fat deposition have been studied and are already supported by an increasing evidence of the role of pancreatic fat in the development of β-cell dysfunction, [29] carotid atherosclerosis, [30] severe acute pancreatitis, [1] pancreatic cancer [31] and even an increased risk of post-operative fistula in patients undergoing pancreatic surgery. [32] So, pancreatic steatosis may have a role in the patient outcome, although little information is available to guide any clinical management of these patients.
There are some limitations in our study. Histologic confirmation of pancreatic steatosis was absent for ethical reasons. The study involved a small number of patients in each subgroup of liver disease, and only few patients had high liver steatosis grades. The subgroup of patients with chronic NALD had a significant number of patients with elevation of transaminases but no specific diagnosis of liver disease. In liver studies, the MECSE analysis by considering different fat spectral peaks has been increasingly used due to major consistency of results. [11-14] However, a future study would be needed to demonstrate the benefit of this type of analysis in pancreas, if several types of fat are also deposited this organ.
Further investigation regarding pancreatic MR-estimated PDFF quantification could bring insights about the physiologic pathways of visceral fat deposition and its clinical implications. Possible risk factors and other possible causes for the development and natural history of pancreatic steatosis should be also addressed in future studies.
In conclusion, pancreatic steatosis can be easily evaluated by means of MECSE MR imaging, at the same time as hepatic steatosis. There is a positive correlation between both findings in patients with chronic non-viral non-alcoholic liver diseases, but not with chronic viral hepatitis.
References
[1] Smits MM, van Geenen EJ. The clinical significance of pancreatic steatosis. Nat Rev Gastroenterol Hepatol. 2011;8:169-77.
[2] Feakins RM. Obesity and metabolic syndrome: pathological effects on the gastrointestinal tract. Histopathology. 2016;68:630-40.
[3] Verma AR, Papalois V. Evaluating steatosis in pancreatic transplant. Exp Clin Transplant. 2011;9:159-64.
[4] Pinnick KE, Collins SC, Londos C, Gauguier D, Clark A, Fielding BA. Pancreatic ectopic fat is characterized by adipocyte infiltration and altered lipid composition. Obesity (Silver Spring). 2008;16:522-30.
[5] Ratziu V, Charlotte F, Heurtier A, Gombert S, Giral P, Bruckert E, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128:1898-906.
[6] Tariq H, Nayudu S, Akella S, Glandt M, Chilimuri S. Non-Alcoholic Fatty Pancreatic Disease: A Review of Literature. Gastroenterology Res. 2016;9:87-91.
[7] 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;62:2658-67.
[8] Kim SY, Kim H, Cho JY, Lim S, Cha K, Lee KH, et al. Quantitative Assessment of Pancreatic Fat by Using Unenhanced CT: Pathologic Correlation and Clinical Implications. Radiology. 2014;271:104-12.
[9] Hong CW, Fazeli Dehkordy S, Hooker JC, Hamilton G, Sirlin CB. Fat Quantification in the Abdomen. Top Magn Reson Imaging. 2017;26:221-7.
[10] Idilman IS, Tuzun A, Savas B, Elhan AH, Celik A, Idilman R, et al. Quantification of liver, pancreas, kidney, and vertebral body MRI-PDFF in non-alcoholic fatty liver disease. Abdom Imaging. 2015;40:1512-9.
[11] Permutt Z, Le TA, Peterson MR, Seki E, Brenner DA, Sirlin C, et al. Correlation between liver histology and novel magnetic resonance imaging in adult patients with non-alcoholic fatty liver disease - MRI accurately quantifies hepatic steatosis in NAFLD. Alimentary pharmacology & therapeutics. 2012;36:22-9.
[12] Tang A, Tan J, Sun M, Hamilton G, Bydder M, Wolfson T, et al. Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology. 2013;267:422-31.
[13] Idilman IS, Aniktar H, Idilman R, Kabacam G, Savas B, Elhan A, et al. Hepatic steatosis: quantification by proton density fat fraction with MR imaging versus liver biopsy. Radiology. 2013;267:767-75.
[16] Yki-Jarvinen H. Non-alcoholic fatty liver disease as a cause and a consequence of metabolic syndrome. Lancet Diabetes Endocrinol. 2014;2:901-10.
[17] Lim CT, Kumar R. Hepatitis B and concomitant hepatic steatosis. Ann Transl Med. 2017;5:38. [18] Yoon EJ, Hu KQ. Hepatitis C virus (HCV) infection and hepatic steatosis. Int J Med Sci. 2006;3:53-6.
[19] Reeder SB, Sirlin CB. Quantification of liver fat with magnetic resonance imaging. Magn Reson Imaging Clin N Am. 2010;18:337-57, ix.
[20] Wu WC, Wang CY. Association between non-alcoholic fatty pancreatic disease (NAFPD) and the metabolic syndrome: case-control retrospective study. Cardiovascular diabetology. 2013;12:77.
[21] van Geenen EJ, Smits MM, Schreuder TC, van der Peet DL, Bloemena E, Mulder CJ. Nonalcoholic fatty liver disease is related to nonalcoholic fatty pancreas disease. Pancreas. 2010;39:1185-90.
[22] Patel NS, Peterson MR, Brenner DA, Heba E, Sirlin C, Loomba R. Association between novel MRI-estimated pancreatic fat and liver histology-determined steatosis and fibrosis in non-alcoholic fatty liver disease. Alimentary Pharmacology & Therapeutics. 2013;37:630-9.
[23] Brunt EM, Kleiner DE, Wilson LA, Belt P, Neuschwander-Tetri BA, Network NCR. Nonalcoholic fatty liver disease (NAFLD) activity score and the histopathologic diagnosis in NAFLD: distinct clinicopathologic meanings. Hepatology. 2011;53:810-20.
[24] Marti-Bonmati L, Alberich-Bayarri A, Sanchez-Gonzalez J. Overload hepatitides: quanti-qualitative analysis. Abdom Imaging. 2012;37:180-7.
[25] Li J, Xie Y, Yuan F, Song B, Tang C. Noninvasive quantification of pancreatic fat in healthy male population using chemical shift magnetic resonance imaging: effect of aging on pancreatic fat content. Pancreas. 2011;40:295-9.
[26] Glaser J, Stienecker K. Pancreas and aging: a study using ultrasonography. Gerontology. 2000;46:93-6.
[27] Sasaki M, Nakanuma Y, Ando H. Lipomatous pseudohypertrophy of the pancreas in a patient with cirrhosis due to chronic hepatitis B. Pathol Int. 1998;48:566-8.
[28] De Luca-Johnson J, Wangensteen KJ, Hanson J, Krawitt E, Wilcox R. Natural History of Patients Presenting with Autoimmune Hepatitis and Coincident Nonalcoholic Fatty Liver Disease. Dig Dis Sci. 2016;61:2710-20.
[29] Szczepaniak LS, Victor RG, Mathur R, Nelson MD, Szczepaniak EW, Tyer N, et al. Pancreatic steatosis and its relationship to beta-cell dysfunction in humans: racial and ethnic variations. Diabetes Care. 2012;35:2377-83.
[30] Kim MK, Chun HJ, Park JH, Yeo DM, Baek K-H, Song K-H, et al. The association between ectopic fat in the pancreas and subclinical atherosclerosis in type 2 diabetes. Diabetes Research and Clinical Practice. 2014;106:590-6.
[31] Hori M, Takahashi M, Hiraoka N, Yamaji T, Mutoh M, Ishigamori R, et al. Association of pancreatic Fatty infiltration with pancreatic ductal adenocarcinoma. Clin Transl Gastroenterol. 2014;5:e53.
[32] Mathur A, Pitt HA, Marine M, Saxena R, Schmidt CM, Howard TJ, et al. Fatty pancreas: a factor in postoperative pancreatic fistula. Ann Surg. 2007;246:1058-64.
Table I
Table I - Data are expressed as mean with standard deviation in parentheses unless otherwise noted.
NALD (n=27) Chronic Viral Hepatitis
(n=19) P value Demographics: Gender (%male) 37.04 63.16 0.08 Age 45.74 (15.68) 41.79 (9.72) 0.10 BMI 25.68 (5.03) 24.33 (3.28) 0.09 Diabetes status (%) 7.41 5.26 0.63 MR Imaging: MR Imaging-PDFF Liver (%) 10.15 (4.62) 8.75 (2.95) 0.10 MR Imaging-PDFF Pancreas (%) 12.95 (7.02) 9.53 (4.56) 0.02
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 5 - Correlation of Pancreatic PDFF with Liver PDFF in each subgroup: Non-alcoholic Liver Disease and Chronic Viral Hepatitis
