Three-dimensional analysis of pancreatic fat by fat-water magnetic resonance imaging provides detailed characterization of pancreatic steatosis with improved reproducibility

Autoři: Shingo Kato aff001;  Akito Iwasaki aff001;  Yusuke Kurita aff001;  Jun Arimoto aff001;  Toh Yamamoto aff003;  Sho Hasegawa aff001;  Takamitsu Sato aff001;  Kento Imajo aff001;  Kunihiro Hosono aff001;  Noritoshi Kobayashi aff002;  Masato Yoneda aff001;  Takuma Higurashi aff001;  Kensuke Kubota aff001;  Daisuke Utsunomiya aff003;  Atsushi Nakajima aff001
Působiště autorů: Department of Gastroenterology and Hepatology, Yokohama City University School of Medicine, Yokohama, Japan aff001;  Department of Oncology, Yokohama City University Hospital, Yokohama, Japan aff002;  Diagnostic Radiology, Yokohama City University Graduate School of Medicine, Yokohama, Japan aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article



Since pancreatic steatosis is reported as a possible risk factor for pancreatic cancer, the development of a non-invasive method to quantify pancreatic steatosis is needed. Proton density fat fraction (PDFF) measurement is a magnetic resonance imaging (MRI) based method for quantitatively assessing the steatosis of a region of interest (ROI). Although it is commonly used for quantification of hepatic steatosis, pancreatic PDFF can greatly vary depending on the ROI’s location because of the patchy nature of pancreatic fat accumulation. In this study, we attempted to quantify pancreatic steatosis by fat-water MRI with improved reproducibility.


Using the MRI images of 159 patients with nonalcoholic fatty liver disease, we attempted to calculate the average PDFF of whole pancreas. We set ROIs covering the entire area of the pancreas appearing in every slice and calculated the average PDFF from all the voxels included in the pancreas. We named this average value as whole-pancreatic PDFF and evaluated the reproducibility of the measured values. In addition to whole-pancreatic PDFF, we measured the average PDFF of the pancreatic head (head-PDFF) and that of the pancreatic body plus tail separately and analyzed their correlation with the clinical characteristics of the patients.


The mean inter-examiner coefficient of variation of the whole-pancreatic PDFF was 11.39%. The whole-pancreatic PDFF was correlated with age (p = 0.039), body mass index (p = 0.0093) and presence/absence of diabetes (p = 0.0055). The serum level of low-density lipoprotein cholesterol was inversely correlated with the head-PDFF.


We developed a new measurement method of the pancreatic PDFF with greater reproducibility. Using this method, we characterized pancreatic steatosis in detail. This novel measurement method allows accurate estimation of the severity of pancreatic steatosis and is therefore useful for the detailed characterization of pancreatic steatosis.

Klíčová slova:

Fats – Fatty liver – Histology – Magnetic resonance imaging – Steatosis


1. Takahashi M, Hori M, Ishigamori R, Mutoh M, Imai T, Nakagama H. Fatty pancreas: A possible risk factor for pancreatic cancer in animals and humans. Cancer Sci. 2018;109(10):3013–23. doi: 10.1111/cas.13766 30099827; PubMed Central PMCID: PMC6172058.

2. Hori M, Takahashi M, Hiraoka N, Yamaji T, Mutoh M, Ishigamori R, et al. Association of pancreatic Fatty infiltration with pancreatic ductal adenocarcinoma. Clinical and translational gastroenterology. 2014;5:e53. doi: 10.1038/ctg.2014.5 24622469; PubMed Central PMCID: PMC3972693.

3. Olsen TS. Lipomatosis of the pancreas in autopsy material and its relation to age and overweight. Acta Pathol Microbiol Scand A. 1978;86A(5):367–73. doi: 10.1111/j.1699-0463.1978.tb02058.x 716899.

4. Stamm BH. Incidence and diagnostic significance of minor pathologic changes in the adult pancreas at autopsy: a systematic study of 112 autopsies in patients without known pancreatic disease. Human pathology. 1984;15(7):677–83. doi: 10.1016/s0046-8177(84)80294-4 6745910.

5. Hu HH, Kim HW, Nayak KS, Goran MI. Comparison of fat-water MRI and single-voxel MRS in the assessment of hepatic and pancreatic fat fractions in humans. Obesity. 2010;18(4):841–7. doi: 10.1038/oby.2009.352 19834463; PubMed Central PMCID: PMC2847037.

6. Imajo K, Kessoku T, Honda Y, Tomeno W, Ogawa Y, Mawatari H, et al. Magnetic Resonance Imaging More Accurately Classifies Steatosis and Fibrosis in Patients With Nonalcoholic Fatty Liver Disease Than Transient Elastography. Gastroenterology. 2016;150(3):626–37 e7. doi: 10.1053/j.gastro.2015.11.048 26677985.

7. Kuhn JP, Berthold F, Mayerle J, Volzke H, Reeder SB, Rathmann W, et al. Pancreatic Steatosis Demonstrated at MR Imaging in the General Population: Clinical Relevance. Radiology. 2015;276(1):129–36. doi: 10.1148/radiol.15140446 25658037; PubMed Central PMCID: PMC4554208.

8. Wong VW, Wong GL, Yeung DK, Abrigo JM, Kong AP, Chan RS, et al. Fatty pancreas, insulin resistance, and beta-cell function: a population study using fat-water magnetic resonance imaging. The American journal of gastroenterology. 2014;109(4):589–97. doi: 10.1038/ajg.2014.1 24492753.

9. 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(6):630–9. doi: 10.1111/apt.12237 23383649; PubMed Central PMCID: PMC4136524.

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. Abdominal imaging. 2015;40(6):1512–9. doi: 10.1007/s00261-015-0385-0 25715922.

11. Yoon JH, Lee JM, Lee KB, Kim SW, Kang MJ, Jang JY, et al. Pancreatic Steatosis and Fibrosis: Quantitative Assessment with Preoperative Multiparametric MR Imaging. Radiology. 2016;279(1):140–50. doi: 10.1148/radiol.2015142254 26566228.

12. Matsumoto S, Mori H, Miyake H, Takaki H, Maeda T, Yamada Y, et al. Uneven fatty replacement of the pancreas: evaluation with CT. Radiology. 1995;194(2):453–8. doi: 10.1148/radiology.194.2.7824726 7824726.

13. Yu H, Shimakawa A, Hines CD, McKenzie CA, Hamilton G, Sirlin CB, et al. Combination of complex-based and magnitude-based multiecho water-fat separation for accurate quantification of fat-fraction. Magn Reson Med. 2011;66(1):199–206. doi: 10.1002/mrm.22840 21695724; PubMed Central PMCID: PMC3130743.

14. Jennings RE, Berry AA, Strutt JP, Gerrard DT, Hanley NA. Human pancreas development. Development. 2015;142(18):3126–37. doi: 10.1242/dev.120063 26395141.

15. Marz W, Scharnagl H, Gouni-Berthold I, Silbernagel G, Dressel A, Grammer TB, et al. LDL-Cholesterol: Standards of Treatment 2016: A German Perspective. Am J Cardiovasc Drugs. 2016;16(5):323–36. doi: 10.1007/s40256-016-0179-y 27430233.

16. Biswas N, Sangma MA. Serum LDL (Low Density Lipoprotein) As a Risk Factor for Ischemic Stroke. Mymensingh Med J. 2016;25(3):425–32. 27612886.

17. Sun DQ, Liu WY, Wu SJ, Zhu GQ, Braddock M, Zhang DC, et al. Increased levels of low-density lipoprotein cholesterol within the normal range as a risk factor for nonalcoholic fatty liver disease. Oncotarget. 2016;7(5):5728–37. doi: 10.18632/oncotarget.6799 26735337; PubMed Central PMCID: PMC4868717.

18. 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(8):1185–90. doi: 10.1097/MPA.0b013e3181f6fce2 20871475.

19. Ou HY, Wang CY, Yang YC, Chen MF, Chang CJ. The association between nonalcoholic fatty pancreas disease and diabetes. PLoS One. 2013;8(5):e62561. doi: 10.1371/journal.pone.0062561 23671610; PubMed Central PMCID: PMC3643962.

20. Harrison SA, Torgerson S, Hayashi PH. The natural history of nonalcoholic fatty liver disease: a clinical histopathological study. The American journal of gastroenterology. 2003;98(9):2042–7. doi: 10.1111/j.1572-0241.2003.07659.x 14499785.

21. Smits MM, van Geenen EJ. The clinical significance of pancreatic steatosis. Nat Rev Gastroenterol Hepatol. 2011;8(3):169–77. doi: 10.1038/nrgastro.2011.4 21304475.

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2019 Číslo 12
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