Is a fatty pancreas a banal lesion?

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VOLUME 16 , ISSUE 66 (October 2016) > List of articles

Is a fatty pancreas a banal lesion?

Andrzej Smereczyński * / Katarzyna Kołaczyk

Keywords : pancreas, adiposis, adiposis classification, nonalcoholic fatty pancreas disease, ultrasonography

Citation Information : Journal of Ultrasonography. Volume 16, Issue 66, Pages 273-280, DOI: https://doi.org/10.15557/JoU.2016.0027

License : (CC BY-NC-ND 3.0)

Received Date : 31-March-2015 / Accepted: 04-August-2015 / Published Online: 07-September-2016

ARTICLE

ABSTRACT

So far, a fatty pancreas has been related to obesity and the ageing processes in the body. The current list of pathogenetic factors of the condition is clearly extended with genetically conditioned diseases (cystic fibrosis, Shwachman-Diamond syndrome and Johanson-Blizzard syndrome), pancreatitis, especially hereditary and obstructive, metabolic and hormonal disorders (hypertriglyceridemia, hypercholesterolemia, hyperinsulinemia and hypercortisolemia), alcohol overuse, taking some medicines (especially adrenal cortex hormones), disease of the liver and visceral adiposis. As regards lipomatosis of that organ resulting mainly from dyslipidemia and hyperglycemia, the term “nonalcoholic fatty pancreas disease” was introduced. Experimental studies on animals and histological preparations of the pancreatic fragments show that the lipotoxicity of the collected adipocytes collected ion the organ release a cascade of proinflammatory phenomena, and even induces the processes of carcinogenesis. Pancreas adiposis is best defined in Computed Tomography and Magnetic Resonance Imaging. However, a series of works proved the usefulness in the diagnostics of that pathology of transabdominal and endoscopic ultrasonography. In that method, the degree of adiposis was based on the comparison of echogenicity of the pancreas and the liver, renal parenchyma, spleen and/or retroperitoneal adipose. Recently, the evaluation was expanded by the evaluation of the degree of pancreatic adipose with the pancreas-to-liver index, utilizing to that end a special computer program. According to our experience, the simplest solution is the method utilized by us. On one crosssection of the body of the pancreas, its echogenicity is assessed in comparison to retroperitoneal adipose and the visibility of the splenic vein, pancreatic duct and the major retroperitoneal vessels. Depending on the visualization of these structures, it is possible to determine the degree of pancreas adiposis. Such a study applies to 250 people, in whom the adiposis was detected in 16.5%, which is close to other cohort US examinations results.

Dotychczas otłuszczenie trzustki wiązano głównie z otyłością i starzeniem się organizmu. Obecnie lista czynników patogenetycznych tego stanu wyraźnie się wydłużyła o choroby uwarunkowane genetycznie (mukowiscydoza, zespół Shwachmana i Diamonda oraz zespół Johansona i Blizzarda), zapalenia trzustki, zwłaszcza dziedziczne i obturacyjne, zaburzenia metaboliczne i hormonalne (hipertriglicerydemia, hipercholesterolemia, hiperinsulinemia i hiperkortyzolemia), nadużywanie alkoholu, przyjmowanie niektórych leków (zwłaszcza hormonów kory nadnercza), choroby wątroby i otłuszczenie trzewne. W odniesieniu do lipomatozy tego narządu wynikającej głównie z dyslipidemii i hiperglikemii wprowadzono określenie niealkoholowej choroby otłuszczeniowej trzustki (nonalcoholic fatty pancreas disease). W badaniach eksperymentalnych na zwierzętach oraz w preparatach histopatologicznych wyciętych fragmentów trzustki stwierdzono, że lipotoksyczność nagromadzonych w tym narządzie adipocytów wyzwala kaskadę zjawisk prozapalnych, a nawet indukuje procesy karcinogenezy. Otłuszczenie trzustki jest najlepiej definiowane za pomocą tomografii komputerowej i rezonansu magnetycznego. Jednak szereg prac udowodniło przydatność w diagnostyce tej patologii ultrasonografii przezbrzusznej i endoskopowej. W metodzie tej stopień otłuszczenia opierano na porównaniu echogeniczności trzustki z wątrobą, miąższem nerki, śledzioną i/lub tłuszczem zaotrzewnowym. Ostatnio też wprowadzono do oceny stopnia otłuszczenia trzustki wskaźnik trzustkowo-okołowątrobowy, wykorzystując do tego specjalny program komputerowy. Według naszych doświadczeń prostszym rozwiązaniem jest metoda stosowana przez nas. Na jednym przekroju poprzecznym trzonu trzustki ocenia się jego echogeniczność w odniesieniu do tłuszczu zaotrzewnowego i widoczność żyły śledzionowej, przewodu trzustkowego oraz głównych naczyń zaotrzewnowych. W zależności od wizualizacji tych struktur można określić stopień otłuszczenia trzustki. Opracowanie takie dotyczy 250 osób, u których otłuszczenie wykryto w 16,5%, co jest zbliżone do innych kohortowych wyników badań USG.

Graphical ABSTRACT

Pancreas is an organ containing some amount of fat even in healthy people. For a very long time the issue has been that the amount of the tissue usually increases pro rata with age and body mass(15). The current list of pathogenetic factors of fatty pancreas (FP) is clearly extended with genetically conditioned diseases (cystic fibrosis, Shwachman-Diamond syndrome and Johanson-Blizzard syndrome), pancreatitis, especially hereditary and obstructive, metabolic and hormonal disorders (hypertriglyceridemia, hypercholesterolemia, hyperinsulinemia and hypercortisolemia), alcohol overuse, taking some medicines (especially adrenal cortex hormones), disease of the liver and visceral adiposis(613). Moreover, recently, there has been introduced – especially as regards FP related to dyslipidemia and hyperglycemia – as in the case of non-alcoholic fatty liver disease (NAFLD) the notion of a nonalcoholic fatty pancreas disease, NAFPD, which some people want to attach to the criteria of a metabolic syndrome(5, 1418). These two pathologies are often concomitant(13, 15, 18). The research of Lee et al.(18) showed fatty liver with hyperechogenic pancreas in 67.9% of the cases. It is unclear, whether NAFPD may promote non-alcoholic fatty pancreas disease, as in the case of liver, where NAFLD may initiate non-alcoholic steatohepatitis, NASH(19). Uygun et al.(20) observed in 51.2% of the cases the presence of FP among patients with NASH. Lipotoxicity of the collected adipocytes through the activation of a proinflammation mechanism is a known fact. Such an operation of the adipose tissue is of particular importance as regards the viscera through the release of specific factors, such as: IL-6, IL-1 and TNF-alpha. Increase in the concentration of leptin at simultaneous decrease in the concentration of adiponectin will be of similar importance. Rebours et al.(21) in the exsected segments of pancreas infiltrated with adipose tissue clearly more frequently observed fibrosis and intraepithelial neoplasia foci than in the preparations without adipocytes accumulation. Similar conclusions were drawn by Tomita et al.(22) confirming the previous determination from the analysis of over 2 thousand pancreas carcinomas(23). The presented data prove that FP in some people is not a banal lesion, since it may mainly be linked with the disorders of glucose and adipose metabolism, often it is concomitant with the metabolic disorder and may initiate carcinogenesis in that organ. Therefore, the ultrasonography of the abdominal cavity should take into consideration adiposis, which should be reflected in the examination result description. At present, the diagnostics of pancreas adiposis utilizes, apart from transabdominal ultrasonography, also its endoscopic version (EUS) and Computed Tomography (CT) and Magnetic Resonance Imaging (MRI), which is considered and optimum method in this pathology(4, 610, 1320, 24). Ultrasonography is not characterized by such a specific nature as in the case of CT and MRI. In ultrasonography the crucial symptom of fat collection is the hyperechogenic image of the pancreas. However, a similar image of that organ is sometimes caused by the fibrosis or the commonly present mixed process called fibrolipomatosis. The last pathology named usually involves the enlargement of the pancreas(25). The non-selected transabdominal ultrasound examinations proved the presence of FP in the range of 12.9–16%(1517, 20). A similar result was obtained by Wong et al. (16.1%) with the utilization of MRI(24). However, Sepe et al.(14), with the use of EUS as the diagnostic tool, observed such lesions in 27.8% of the patients. The condition of the pancreas in overweight and obese people deteriorates, since the features of FP are observed in 61.4% of them(18). A similar situation was observed among patients with non-alcoholic fatty liver disease, among whom the index amounted to 51.2%(20).

So far, to identify FP, several methods were used, they were compared to the echogenicity of the liver, renal parenchyma, spleen and retroperitoneal adipose. It seems that the most fallible will be the comparison to the liver, which often is subject to adiposis(4, 10). The parenchyma of the kidney may also present various levels of echogenicity depending on the inflammatory process or the degree of failure of that organ. Moreover, the organ in healthy people presents lowest echogenicity among the organs in the epigastrium, possibly similar to the liver. It is also impossible to compare in one cross-section the echogenicity of the body of the pancreas with the echogenicity of the parenchyma of the kidney, therefore the degree of adiposis is indicated indirectly through differences in the echogenicity between the kidney and the liver as well as the liver and the kidney, and even retroperitoneal adipose(1518). Retroperitoneal adipose is often unavailable in the ultrasound imaging in obese and overweight people, yet Uygun et al.(20) took its echogenicity as a reference point to the renal parenchyma and the body of the pancreas. The spleen was used as an organ to conduct a comparative assessment in endoscopic ultrasonography(10, 14). Fig. 1 presents in two cross-sections three organs in a healthy 25-year-old woman: spleen (S), left kidney (K) and tail of the pancreas (P), which shows a slightly higher echogenicity. For comparison, Fig. 2 presents fatty tail of the pancreas. On the basis of solely that image, it is not possible to objectively determine the degree of pancreas adiposis through the reference to the echogenicity of the spleen or renal parenchyma. Recently, Jeong et al.(26) applied the quantitative assessment of the pancreas adiposis degree, using a special computer program determining the average value of pancreas brightness, at-liver adipose (supraperitoneal between the abdominal integuments and the liver) and the measurements gave the pancreas-liver index. Our so far unpublished ultrasound examinations of the abdominal cavity pertaining to 250 people with no pancreas disease showed pancreas adiposis in 42 people (16.8%). In 35 out of 42 (83%) the cause was mainly dyslipidemia, hyperglycemia or both the metabolic disorders at the same time. In the remaining seven people, FP might have been referred to increased body mass and inappropriate nutrition, also the consumption of alcohol. The assessment utilized the classification of the degree of liver adiposis proposed by Scatarige et al.(27) with the introduction of own modification. Using the grey scale imaging, after the assessment of the whole pancreas, the assessment of the degree of adiposis was performed on the cross-section of the body. Correct echogenicity of the body of the pancreas (the best visible part of that gland) is a situation when it has lower echogenicity than in the cross-section retorperitoneal adipose within the area of the superior mesenteric artery and the splenic vein and pancreatic duct were clearly separated. Such an image is presented in Fig. 3 and Fig. 4. Figure 5, on the other hand, presents on two cross-sections the pancreas with its buds distinct in terms of echogenicity. Abdominal bud is of proper echogenicity, while the dorsal bud presents adiposis – an option of echostructure which is a well-known issue(28).

Fig. 1

One cross-section, two projections covering three organs in a healthy 25-year-old woman: P – pancreas with slightly increased echogenicity than the spleen (S) and the parenchyma of the left kidney (K)

10.15557_JoU.2016.0027-g001.jpg
Fig. 2

The same projections as in Fig. 1, but in a 50-year-old woman with fatty tail of the pancreas (arrows). S – spleen, K – parenchyma of the left kidney

10.15557_JoU.2016.0027-g002.jpg
Fig. 3

Image of a normal body of the pancreas in a 35-year-old woman. Echogenicity of the pancreas visibly lower than the adipose in the area of the superior mesenteric artery. L – liver, ICV – inferior vena cava, A – aorta

10.15557_JoU.2016.0027-g003.jpg
Fig. 4

Image of a normal body of the pancreas in a 73-year-old man. Echogenicity of the pancreas visibly lower than the retroperitoneal adipose. L – liver, ICV – inferior vena cava, A – aorta

10.15557_JoU.2016.0027-g004.jpg
Fig. 5

In two cross-sections, the pancreas with a visibly more distinct echogenicity of the buds of the organ. The abdominal bud shows correct echogenicity (a), while the dorsal bud is fatty (arrows). L – liver, S – stomach, ICV – inferior vena cava, A – aorta

10.15557_JoU.2016.0027-g005.jpg

The first degree of pancreas adiposis is the condition when the body of that organ obtained similar echogenicity to the adipose tissue in the area of the superior mesenteric artery. Moreover, the gland itself showed no enlargement, its echogenicity was homogenously increased, it has a smooth abdominal outline and the splenic vein and superior mesenteric artery and pancreatic duct were well visible (Fig. 6).

Fig. 6

First degree of pancreas adiposis. Echogenicity of the body similar to the echogenicity of the retroperitoneal adipose. L – liver, GB – gallbladder, ICV – inferior vena cava, A – aorta

10.15557_JoU.2016.0027-g006.jpg

The second degree of adiposis was characterized by increased echogenicity at simultaneous darker background of the dorsal part of the gland (lowered transsonicity), blurred edges of the splenic vein and the pancreatic duct with almost invisible area of the superior mesenteric artery. In some cases, the abdominal outline of the gland became wavy and its visibility sometimes reached the upper level of standard (Fig. 7).

Fig. 7

Second degree of adiposis. The body of the pancreas with lowered dorsal transsonicity of the parenchyma and blurred outline of the splenic vein and deeper structures. L – liver, A – aorta

10.15557_JoU.2016.0027-g007.jpg

The third degree of adiposis included deteriorated propagation of ultrasound waves of the gland, so that it was possible to see only its abdominal portion, most often with a clear external waviness. In these cases, it was impossible to expose the splenic vein, the area of the superior mesenteric artery or the pancreatic duct (Fig. 8). Sometimes, the second and the third degree of adiposis may include mutual penetration of fatty hyperechogenic pancreatic lobes and the hypoechogenic adipose surrounding that gland (interference) (Fig. 9). The image should not be mistaken for the fluid surrounding the abdominal surface of the gland.

Fig. 8

Third degree of adiposis. Clearly deteriorated dorsal transsonicity of the pancreas. Invisible splenic vein and anatomical structures located deeper. F – supraperitoneal fat

10.15557_JoU.2016.0027-g008.jpg
Fig. 9

Mutual penetration of hyperechogenic lobes of the pancreas with the hypoechogenic at-pancreas adipose (arrows)

10.15557_JoU.2016.0027-g009.jpg

The described classification of FP applies only to the process, which homogenously covers the whole gland or its dorsal bud. A separate issue is single or multiple lipomatosis, lipomatous pseudohypertrophy and lipoma of the pancreas. Our observations show that there are huge obstacle in the diagnosis of this acute inflammation of the fatty gland, since usually there is no typical evolution of decrease in its echogenicity over time. Moreover, it should be noted that acute pancreatitis in the case of its lipomatosis involves huge tendency to produce necrotic lesions and multi-organ failure, which may be the cause of death even in the case of 30% of the patients(29, 30). Another observation is slow retreat of FP despite the introduction of a reasonable diet and medicines correcting the metabolic disorders (Fig. 10).

Fig. 10

A 79-year-old physician over 20 years ago lost 24 kilos, obtaining the appropriate body mass through the application of a reasonable diet and medicine lowering lipids. Despite that fact, pancreas shows the 2nd degree of adiposis, while correct echogenicity was obtained by the liver (L)

10.15557_JoU.2016.0027-g010.jpg

Summary

The presented data from literature and own determinations prove that the adiposis of the pancreas should be treated more seriously, since it is often the symptom of a multi-factor damage to that organ. The identification of these factors is supposed to induce to apply a well-thought out health promoting strategy, which with time may contribute to risk reduction, especially of cardiovascular accident and diabetes. Our manner of classification of pancreas adiposis seems simple and possible to be applied with the use of any class of ultrasound device.

Conflict of interest

Authors do not report any financial or personal connections with other persons or organizations, which might negatively affect the contents of this publication and/or claim authorship rights to this publication.

References


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  3. Bochenek A,Reicher M,Anatomia człowieka 1998 II Warszawa Wydawnictwo Lekarskie PZWL 168 180
  4. Glaser J,Stienecker K,Pancreas and aging: a study using ultrasonography Gerontology 2000 46 93 96
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  5. 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 1190
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  6. Tham RT,Heyerman HG,Falke TH,Zwinderman AH,Bloem JL,Bakker W,Cystic fibrosis: MR imaging of the pancreas Radiology 1991 179 183 186
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  7. Matsumoto S,Mori H,Miyake H,Takaki H,Maeda T,Yamada Y,Uneven fatty replacement of the pancreas: evaluation with CT Radiology 1995 194 453 458
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  9. Robberecht E,Nachtegaele P,Van Rattinghe R,Afschrift M,Kunnen M,Verhaaren R,Pancreatic lipomatosis in the Shwachman-Diamond syndrome. Identification by sonography and CT-scan Pediatr Radiol 1985 15 348 349
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FIGURES & TABLES

Fig. 1

One cross-section, two projections covering three organs in a healthy 25-year-old woman: P – pancreas with slightly increased echogenicity than the spleen (S) and the parenchyma of the left kidney (K)

Full Size   |   Slide (.pptx)

Fig. 2

The same projections as in Fig. 1, but in a 50-year-old woman with fatty tail of the pancreas (arrows). S – spleen, K – parenchyma of the left kidney

Full Size   |   Slide (.pptx)

Fig. 3

Image of a normal body of the pancreas in a 35-year-old woman. Echogenicity of the pancreas visibly lower than the adipose in the area of the superior mesenteric artery. L – liver, ICV – inferior vena cava, A – aorta

Full Size   |   Slide (.pptx)

Fig. 4

Image of a normal body of the pancreas in a 73-year-old man. Echogenicity of the pancreas visibly lower than the retroperitoneal adipose. L – liver, ICV – inferior vena cava, A – aorta

Full Size   |   Slide (.pptx)

Fig. 5

In two cross-sections, the pancreas with a visibly more distinct echogenicity of the buds of the organ. The abdominal bud shows correct echogenicity (a), while the dorsal bud is fatty (arrows). L – liver, S – stomach, ICV – inferior vena cava, A – aorta

Full Size   |   Slide (.pptx)

Fig. 6

First degree of pancreas adiposis. Echogenicity of the body similar to the echogenicity of the retroperitoneal adipose. L – liver, GB – gallbladder, ICV – inferior vena cava, A – aorta

Full Size   |   Slide (.pptx)

Fig. 7

Second degree of adiposis. The body of the pancreas with lowered dorsal transsonicity of the parenchyma and blurred outline of the splenic vein and deeper structures. L – liver, A – aorta

Full Size   |   Slide (.pptx)

Fig. 8

Third degree of adiposis. Clearly deteriorated dorsal transsonicity of the pancreas. Invisible splenic vein and anatomical structures located deeper. F – supraperitoneal fat

Full Size   |   Slide (.pptx)

Fig. 9

Mutual penetration of hyperechogenic lobes of the pancreas with the hypoechogenic at-pancreas adipose (arrows)

Full Size   |   Slide (.pptx)

Fig. 10

A 79-year-old physician over 20 years ago lost 24 kilos, obtaining the appropriate body mass through the application of a reasonable diet and medicine lowering lipids. Despite that fact, pancreas shows the 2nd degree of adiposis, while correct echogenicity was obtained by the liver (L)

Full Size   |   Slide (.pptx)

REFERENCES

  1. Ogilvie RF,The islands of Langerhaus in 19 cases of obesity J Pathol Bacteriol 1933 37 473 481
    [CROSSREF]
  2. Olsen TS,Lipomatosis of the pancreas in autopsy material and its relation to age and overweight Acta Pathol Microbiol Scand A 1978 86A 367 373
    [PUBMED]
  3. Bochenek A,Reicher M,Anatomia człowieka 1998 II Warszawa Wydawnictwo Lekarskie PZWL 168 180
  4. Glaser J,Stienecker K,Pancreas and aging: a study using ultrasonography Gerontology 2000 46 93 96
    [PUBMED] [CROSSREF]
  5. 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 1190
    [PUBMED] [CROSSREF]
  6. Tham RT,Heyerman HG,Falke TH,Zwinderman AH,Bloem JL,Bakker W,Cystic fibrosis: MR imaging of the pancreas Radiology 1991 179 183 186
    [PUBMED] [CROSSREF]
  7. Matsumoto S,Mori H,Miyake H,Takaki H,Maeda T,Yamada Y,Uneven fatty replacement of the pancreas: evaluation with CT Radiology 1995 194 453 458
    [PUBMED] [CROSSREF]
  8. Bom EP,van der Sande FM,Tjon RT,Tham A,Hillen HF,Shwachman syndrome: CT and MR diagnosis J Comput Assist Tomogr 1993 17 474 476
    [PUBMED] [CROSSREF]
  9. Robberecht E,Nachtegaele P,Van Rattinghe R,Afschrift M,Kunnen M,Verhaaren R,Pancreatic lipomatosis in the Shwachman-Diamond syndrome. Identification by sonography and CT-scan Pediatr Radiol 1985 15 348 349
    [PUBMED] [CROSSREF]
  10. Al-Haddad M,Khashab M,Zyromski N,Pungpapong S,Wallace MB,Scolapio J,Risk factors for hiperechogenic pancreas on endoscopic ultrasound: a case-control study Pancreas 2009 38 672 675
    [PUBMED] [CROSSREF]
  11. Rezaei N,Sabbaghian M,Liu Z,Zenker M,Eponym: Johanson-Blizzard syndrome Eur J Pediatr 2011 170 179 183
    [PUBMED] [CROSSREF]
  12. Ellery KM,Erdman SH,Johanson-Blizzard syndrome: expanding the phenotype of exocrine pancreatic insufficiency JOP 2014 15 388 390
    [PUBMED]
  13. Targher G,Rossi AP,Zamboni GA,Fantin F,Antonioli A,Corzato F,Pancreatic fat accumulation and its relationships with liver content and other fat depots in obese individuals J Endocrinal Invest 2012 35 748 753
  14. Sepe PS,Ohri A,Sanaka S,Berzin TM,Sekhon S,Bennett G,A prospective evaluation of fatty pancreas by using EUS Gastrointest Endosc 2011 73 987 993
    [PUBMED] [CROSSREF]
  15. Wu WC,Wang CY,Association between nonalcoholic fatty pancreatic disease (AAFPD) and the metabolic syndrome: case-control retrospective study Cardiovasc Diabetol 2013 12 77
    [PUBMED] [CROSSREF]
  16. Ou HY,Wang CY,Yang YC,Chen MF,Chang CJ,The association between nonalcoholic fatty pancreas disease and diabetes PLoS One 2013 8 e76537
    [PUBMED] [CROSSREF]
  17. Wang CY,Ou HY,Chen MF,Chang TC,Chang CJ,Enigmatic ectopic fat: prevalence of nonalcoholic pancreas disease and its association factors in a Chinese population J Am Heart Assoc 2014 3 e000297
    [PUBMED] [CROSSREF]
  18. Lee JS,Kim SH,Jun DW,Han JH,Jang EC,Park JY,Clinical implications of fatty pancreas: correlations between fatty pancreas and metabolic syndrome World J Gastroenterol 2009 15 1869 1875
    [PUBMED] [CROSSREF]
  19. Pezzilli R,Calculli L,Pancreatic steatosis: is it related to either obesity or diabetes mellitus World J Diabetes 2014 15 415 419
    [CROSSREF]
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