Insights into epiploic appendagitis

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Nov 23, 2010 - and appendicitis. This article reviews epiploic appendagitis and includes discussion of clinical findings, pathophysiology, diagnosis and ...

rEvIEWS Insights into epiploic appendagitis Wolfgang J. Schnedl, Robert Krause, Erwin Tafeit, Manfred Tillich, Rainer W. Lipp and Sandra J. Wallner-Liebmann abstract | Epiploic appendagitis is a rare cause of abdominal pain. Diagnosis of epiploic appendagitis, although infrequent, is easily made with CT or ultrasonography in experienced hands. As reported in the literature, most patients with primary epiploic appendagitis are treated conservatively without surgery, with or without anti‑inflammatory drugs. A small number of patients are treated with antibiotics and some patients require surgical intervention to ensure therapeutic success. Symptoms of primary epiploic appendagitis usually resolve with or without treatment within a few days. A correct diagnosis of epiploic appendagitis with imaging procedures enables conservative and successful outpatient management of the condition and avoids unnecessary surgical intervention and associated additional health‑care costs. Gastroenterologists and all medical personnel should be aware of this rare disease, which mimics many other intra‑abdominal acute and subacute conditions, such as diverticulitis, cholecystitis and appendicitis. This article reviews epiploic appendagitis and includes discussion of clinical findings, pathophysiology, diagnosis and therapeutic possibilities. Schnedl, W. J. et al. Nat. Rev. Gastroenterol. Hepatol. 8, 45–49 (2011); published online 23 November 2010; doi:10.1038/nrgastro.2010.189


epiploic appendagitis is a very rare condition that results from inflammation of an epiploic appendage. owing to a lack of pathognomonic clinical features and awareness of the disease, epiploic appendagitis is rarely diagnosed as the cause of acute and subacute abdominal complaints.1 most cases reported in the literature have been diagnosed after retrospective re-evaluation of Ct images. it has been suggested that many patients treated for mild diverticulitis may actually have epiploic appendagitis.2 Furthermore, it has been reported that up to 7% of all patients clinically suspected of having diverticulitis and 1% of patients with acute appendicitis may have epiploic appendagitis.3 this condition clearly occurs more frequently than anticipated but its true prevalence is not known.4 as epiploic appendages are not well developed in childhood, epiploic appendagitis occurs mostly in adulthood; reported ages for the diagnosis of epiploic appendagitis range from childhood5 to >80 years, with an approximate mean age at diagnosis of 40 years.6 obesity and strenuous exercise are thought to be risk factors for the development of epiploic appendagitis,2 and its incidence seems to be up to four times higher in men than in women.7–9 Pathophysiologic explanations for epiploic appendagitis include spontaneous venous thrombosis, torsion of an epiploic appendage and/or inflammation in one of these appendages. in the past, diagnosis was often made during surgery, but imaging procedures are now increasingly used for this purpose. Ct is the diagnostic modality of choice for patients with suspected epiploic appendagitis because this condition Competing interests The authors declare no competing interests.

has a characteristic appearance on Ct that is easily identifiable. recognition of epiploic appendagitis has increased over the past 10 years owing to the increasing use of abdominal ultrasonography and the introduction of cross-sectional imaging Ct scans for the primary evaluation of abdominal pain.10 improved awareness of the clinical presentation of epiploic appendagitis and its characteristics on ultrasonography has enabled conservative and successful outpatient management, thereby avoiding unnecessary surgical intervention and associated additional health-care costs.1,10–12

Anatomy and function

epiploic appendages are pouches of subserosal fat that line the entire length of the colon in adults. anatomically, they appear in two parallel rows next to the anterior (taenia libera) and the posterior (omentalis) taenia coli, and are attached to the colonic wall by a vascular stalk. most appendages are 1–2 cm thick and 2–5 cm long. approximately 50–100 epiploic appendages are present in an adult. epiploic appendagitis may occur anywhere in the colon;1,13,14 however, the surgical literature suggests that 57% of cases occur in the rectosigmoid junction, 26% in the ileocecal region, 9% in the ascending colon, 6% in the transverse colon and 2% in the descending colon.2,15–17 epiploic appendagitis in the cecum is rarely described because appendages are infrequent or may be rudimentary at this location.15 single isolated appendages may occur at the vermiform appendix or small bowel loops. the development of appendages begins in the second trimester of fetal life, and they reach their full size in

nature reviews | gastroenterology & hepatology © 2011 Macmillan Publishers Limited. All rights reserved

General Practice for General Internal Medicine, Haupstrasse 5, A‑8940 Liezen, Austria (W. J schnedl). Department of Internal Medicine, Medical University of Graz, Auenbruggerplatz 15, A‑8036 Graz, Austria (r. Krause, r. W. lipp). Institute of Physiological Chemistry, Centre of Physiological Medicine, Harrachgasse 21/II, A‑8010 Graz, Austria (e. tafeit). Diagnostikum Sued‑ West, Weblinger Guertel 25, A‑8054 Graz, Austria (M. tillich). Institute of Pathophysiology, Centre for Molecular Medicine, Heinrichstrasse 31a, A‑8010 Graz, Austria (s. J. Wallnerliebmann). Correspondence to: W. J. Schnedl [email protected] dr‑

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revIeWs Key points ■ Epiploic appendagitis is a rare cause of abdominal pain and may mimic other acute and subacute conditions ■ Diagnosis is made with CT, which reveals a characteristic lesion usually located in one of the lower abdominal quadrants, or ultrasonography, which reveals a hyperechogenic paracolic oval‑shaped mass ■ Most patients recover with conservative nonsurgical management with or without the use of anti‑inflammatory drugs ■ A correct diagnosis of epiploic appendagitis enables conservative, outpatient management thereby avoiding unnecessary surgical intervention and associated additional health‑care costs

adulthood.17,18 so far, no agreement exists as to their function. it is suggested that they may have bacteriostatic properties, as well as a role in colonic absorption and/or act as flexible cushions to protect colonic blood supply when the colon is collapsed.19 additionally, epiploic appendages may represent a site of fat storage to be accessed in prolonged periods of starvation.20


epiploic appendages were first described by vesalius21 in 1543 but it was not until 1956 that the term epiploic appendagitis was defined by Dockerty et al. 22 Primary epiploic appendagitis (Pea) is thought to be an inflammatory condition and to arise primarily from torsion of an appendage causing ischemia and infarction with aseptic fat necrosis and spontaneous venous thrombosis. this type of epiploic appendagitis is a localized sterile inflammation in and surrounding one epiploic appendage.4,23,24 a limited blood supply, their pedunculated shape, bulbous configuration and excessive mobility make appendages prone to torsion.2,25 in patients with epiploic appendagitis attributable to a torsion, the reason for torsion remains unknown, but the torsion itself can be viewed on laparoscopy.5,26 Pathological review of laparoscopically resected appendages from patients with epiploic appendagitis has revealed the presence of inflammatory cells and colonic bacteria.31 such bacteria can be responsible for localized abscess formation and generalized peritonitis, which are very rare secondary complications of epiploic appendagitis. 27 antibiotic therapy is, however, reported as successful in only a few patients who have epiploic appendagitis.28–31 Pea may be accompanied by surrounding colonic inflammation, which can trigger adhesions that can then lead to rare secondary complications, such as local abscess formation, peritonitis, bowel obstruction and intussusception.27 after an appendage becomes necrotic, the inflammatory process subsides; in the nonseptic patient, the nonviable appendage is absorbed by the body. virchow has suggested that detachment of epiploic appendages might be a source of loose intraperitoneal bodies. although very rare, these detached appendages have been described as a cause of intestinal obstruction or urine retention, depending on their size and intra-abdominal location.32,33 in fact, an inflamed appendage can calcify, appearing in the abdominal cavity as a peritoneal loose

body or ‘peritoneal mice’, which are found incidentally by laparoscopy or during a radiologic evaluation.34,35 secondary epiploic appendagitis (sea) is the involvement of a healthy epiploic appendage in another disease process such as bacterial infection of an adjacent organ (for example, diverticulitis, appendicitis or cholecystitis) or iBD. the disease process leads to inflammation of the epiploic appendage. Colonic diverticulitis is reported as the most frequent source of sea.6 Ct images of sea show the typical appearance of Pea but with neighboring inflammation. sea is not clinically relevant by itself and subsides during treatment of the underlying disease.

Clinical findings

acute and subacute, recurrent, nonmigratory, localized abdominal pain is the main clinical symptom of epiploic appendagitis. other not so frequent abdominal symptoms include local tenderness, postprandial fullness, early satiety, epigastric discomfort, vomiting, bloating, diarrhea, intermittent febrile temperature and moderate weight loss.11 anatomically, pain can be located in all abdominal regions and in sea pain may be associated with the location of an acute or subacute abdominal condition such as diverticulitis, cholecystitis or appendicitis. in general, pain is mainly described in the left abdomen (in 60–80% of patients),18,36 but it is sometimes reported in the right lower abdominal quadrant.37 most patients describe the pain as dull, constant and nonmigrating, and physical examination reveals localized tenderness. abnormal laboratory parameters may include slightly elevated serum levels of C-reactive protein and neutrophil leukocytes. 2,7,8,10,11 However, all routine laboratory parameters, such as erythrocyte sedimentation rate, liver and pancreatic enzymes, are usually within normal limits.


as mentioned earlier, owing to a lack of pathognomonic clinical features and, in part, low or absent awareness of the condition among gastroenterologists and medical personnel, diagnosis of epiploic appendagitis is difficult and rare. Diagnosis based on symptoms alone is virtually impossible; therefore, imaging procedures, specifically Ct or ultrasonography, are necessary. Gastrointestinal endoscopy is sometimes performed before Ct or ultrasonography for the evaluation of abdominal pain; however, such a procedure will not provide an explanation for the presented symptoms in patients who have epiploic appendagitis. Healthy epiploic appendages cannot be seen on Ct scans. they typically have fat attenuation and cannot be distinguished from other adipose structures, such as retroperitoneal fat, unless they are surrounded by intraperitoneal fluid or inflammation.8,38,39 Historically, diagnosis of epiploic appendagitis was made only by surgical laparoscopy. By contrast, this diagnosis can now be made with imaging procedures, mainly Ct, which is employed because it reveals an easily identifiable characteristic appearance of epiploic appendagitis.7,10,18,40–42 the use of Ct for the diagnosis of epiploic

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revIeWs appendagitis was first described by Danielson et al. in 1986.39 on Ct, epiploic appendagitis is represented by an approximately 3 cm long, oval-shaped and fat-dense paracolic lesion. the inflamed and thickened visceral peritoneum surrounding the fat-containing appendage is shown as a hyperattenuating ring (Figures 1 and 2). usually the necrotic epiploic appendage adheres to the parietal peritoneum, which is also thickened. the diameter of the colonic wall and the Gerota’s fascia (a fibrous tissue envelope that surrounds the kidney) may be thickened and pelvic fluid or mesenteric lymphadenopathy may also be present.40 However, in some patients thickening of these neighboring structures is absent. Finally, a thrombosed draining vein may be present and visualized on Ct as a central hyperattenuating dot or a linear density.34 over the past 10 years, the introduction of crosssectional imaging and the increasing use of abdominal Ct scans for the primary evaluation of abdominal pain has led to increased recognition of epiploic appendagitis.34 as even radiologists may overlook this diagnosis on Ct scans, several studies to evaluate epiploic appendagitis have been performed retrospectively. such studies have re-examined the Ct images of patients who presented with acute abdominal pain in emergency departments and have identified many previously undiagnosed cases of epiploic appendagitis.3,9,27,41 Furthermore, an increasing number of cases have been identified on cross-sectional Ct imaging of the abdomen of patients who presented with a variety of symptoms.7,42,43 Follow-up Ct examination of patients with epiploic appendagitis reveals the decreasing size of the necrotic lesion followed by its eventual disappearance, although it may persist over a period of up to 1 year.2,8 the most prominent differential diagnoses of epiploic appendagitis are appendicitis, diverticulitis, acute omental infarction, abdominal abscess, sclerosing mesenteritis, neoplasms and pancreatitis. omental infarction is described as having many pathophysiologic similarities to epiploic appendagitis. However, on Ct, an omental infarction lesion is usually larger than that of epiploic appendagitis, is cake-like, centered in the omentum, and located medial to the cecum or ascending colon.3,4,41 abdominal ultrasonography has revealed epiploic appendagitis in an increasing number of individuals.37,44–47 on ultrasonography, an epiploic appendagitis lesion is shown as a noncompressible hyperechogenic paracolic oval-shaped mass (Figure 3).2 a specific feature of epiploic appendagitis on ultrasonography is that a color Doppler signal cannot be seen in the inflamed appendage, but can be seen in the hyperechogenic altered fat surrounding the infarcted appendage owing to the inflammatory reaction. 9,45 the phenomenon of moderately increased vascularization around the avascular necrotic appendage is easily shown with contrast-enhanced ultrasonography.27 in very few patients, mri can help to establish the diagnosis of epiploic appendagitis. mri findings in patients with epiploic appendagitis include an ovalshaped inflamed edematous pericolic fat mass with a



Figure 1 | Characteristic abdominal CT findings of epiploic appendagitis in a 40‑year‑ old patient. The inflamed lesion (circled) is located below the liver adjacent to the ascending colon and is shown by an oval area of fat attenuation with a diameter of 2.5 cm surrounded by a hyperattenuating ring. a | Transverse and b | longitudinal views.

Figure 2 | A transverse view of an abdominal CT of a 78‑year‑old patient with epiploic appendagitis. The inflamed lesion (circled) is located adjacent to the descending colon and is shown by an oval area of fat attenuation of 1 cm in diameter surrounded by a hyperattenuating ring.

Figure 3 | An ultrasonography image of a 44‑year‑old patient with epiploic appendagitis. The epiploic appendagitis is shown as an hyperechogenic paracolic oval‑shaped mass (circled) with a diameter of 2.2 cm in the left lower abdominal quadrant.

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revIeWs central dot on t1-weighted and t2-weighted images; an enhancing rim is shown on postgadolinium t1-weighted fat saturated images.48


in the radiological literature, epiploic appendagitis is predominantly described as a self-limiting disorder and most patients are treated conservatively and nonsurgically either with or without nsaiDs.3,10,25,34,49,50 a few patients who have epiploic appendagitis but not sepsis have been treated with antibiotics;23–26,29,34 however, such therapy is reported as successful in only a few patients and is, therefore, not an established treatment. at our center, we have successfully treated two Pea patients with antibiotic therapy (ciprofloxacin 1,000 mg daily) and an antiphlogistic therapy (ibuprofen 600 mg paindependent up to three times daily). with conservative nonsurgical management, most patients’ symptoms are alleviated between a few days and 4 weeks.5 in the past, standard therapy for epiploic appendagitis was surgical and laparoscopic excision of the inflamed appendage.23,36 By contrast, careful physical examination and awareness of the characteristic radiologic imaging findings of epiploic appendagitis mean that surgical intervention is now only recommended if conservative medical treatment fails to improve symptoms and clinical signs of the condition. 1.

Sangha, S., Soto, J. A., Becker, J. M. & Farraye, F. A. Primary epiploic appendagitis: an underappreciated diagnosis. A case series and review of the literature. Dig. Dis. Sci. 49, 347–350 (2004). 2. rioux, M. & Langis, P. Primary epiploic appendagitis: Clinical, US, and CT findings in 14 cases. Radiology 191, 523–526 (1994). 3. Breda vriesman, A. C., Lohle, P. N. M., Coerkamp, E. G. & Puylaert, J. B. C. M. Infarction of omentum and epiploic appendage: diagnosis, epidemiology and natural history. Eur. Radiol. 9, 1886–1892 (1999). 4. Almeida, A. T. et al. Epiploic appendagitis: an entity frequently unknown to clinicians— diagnostic imaging, pitfalls, and look‑alikes. Am. J. Roentgenol. 193, 1243–1251 (2009). 5. Fraser, J. D. et al. Infarction of an epiploic appengage in a pediatric patient. J. Pediatr. Surg. 44, 1659–1661 (2009). 6. Son, H. J. et al. Clinical diagnosis of primary epiploic appendagitis: differentiation from acute diverticulitis. J. Clin. Gastroenterol. 34, 435–438 (2002). 7. Ozdemir, S. et al. Torsion of the primary epiploic appendagitis: a case series and review of literature. Am. J. Surg. (in press). 8. Sand, M. et al. Epiploic appendagitis—clinical characteristics of an uncommon surgical diagnosis. BMC Surg. 7, 11 (2007). 9. Hollerweger, A., Macheiner, P., rettenbacher, T. & Gritzmann, N. Primary epiploic appendagitis: sonographic findings with CT correlation. J. Clin. Ultrasound 30, 481–495 (2002). 10. Ozkurt, H. et al. Brief clinical review: CT findings in epiploic appendagitis. Surgery 141, 530–532 (2007). 11. Sandrasegaran, K., Maglinte, D. D., rajesh, A. & Akisik, F. M. Primary epiploic appendagitis: CT diagnosis. Emerg. Radiol. 11, 9–14 (2004).


Careful clinical examination and appropriate diagnosis of epiploic appendagitis with imaging procedures, specifically Ct or ultrasonography (in experienced hands) with follow-up examinations, enables successful conservative, outpatient treatment of patients with epiploic appendagitis owing to the sterile nature of the appendage inflammation. such an approach avoids unnecessary abdominal surgery and associated additional health-care costs. nonsurgical conservative management of epiploic appendagitis with or without the use of nsaiDs is successful in the majority of patients suggesting that this is the optimal therapy for this condition. Review criteria This review is based on a PubMed MEDLINE search, performed in January 2010, for all available original articles published with the search term “epiploic appendagitis”. Other outdated terms including “appendicitis epiploica” and solely “appendagitis” were not employed in the literature search to avoid confusion with acute appendicitis of the vermiform appendix. We identified 120 papers of which approximately 100 English‑language full‑text papers, reviews, case reports, short reports and letters to the editor were reviewed. The reference lists of identified articles were searched for further papers.

12. rao, P. M., rhea, J. T., Wittenberg, J. & Warshaw, A. L. Misdiagnosis of primary epiploic appendagitis. Am. J. Surg. 176, 81–85 (1998). 13. rao, P. M., Wittenberg, J. & Lawrason, J. N. Primary epiploic appendagitis: evolutionary changes in CT appearance. Radiology 204, 713–717 (1997). 14. Singh, A. K. et al. CT appearance of acute epiploic appendagitis. Am. J. Roentgenol. 183, 1303–1307 (2004). 15. Macari, M., Laks, S., Hajdu, C. & Babb, J. Caecal epiploic appendagitis: an unlikely occurrence. Clin. Radiol. 63, 895–900 (2008). 16. Thomas, J. H., rosatto, F. E. & Patterson, L. T. Epiploic appendagitis. Surg. Gynecol. Obstet. 138, 23–25 (1974). 17. Lester, S. C., French, C. A. & Curtis, G. in Manual of Surgical Pathology (ed. Lester, S. C.) 323–343 (Elsevier, 2006). 18. Matsunaga, H., Fuji, Y. & Taniguchi, N. Ultrasonographic findings in epiploic appendagitis. J. Med. Ultrasonics 37, 31–32 (2010). 19. Ghahremani, G. G. et al. Appendices epiploicae of the colon: radiologic and pathologic features. Radiographics 12, 59–77 (1992). 20. ross, J. A. vascular loop in the appendices epiploicae: their anatomy and surgical significance, with a review of the surgical pathology of appendices epiploicae. Br. J. Surg. 37, 464–466 (1950). 21. vesalius, A. De Humanis Corporis Fabrica Libri Septem (Ex officina Joannis Oporini, Basel, 1543). 22. Dockerty, M. B., Lynn, T. E. & Waugh, J. M. A clinicopathologic study of the epiploic appendages. Surg. Gynecol. Obstet. 103, 423–433 (1956). 23. Blinder, E., Ledbetter, S. & rybicki, F. Primary epiploic appendagitis. Emerg. Radiol. 9, 231–233 (2002).

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24. Jain, T. P., Shah, T., Juneia, S. & Tambi, r. L. Case of the season: primary epiploic appendagitis: radiological diagnosis can avoid surgery. Semin. Roentgenol. 43, 4–6 (2008). 25. Singh, A. K. et al. Acute epiploic appendagitis and its mimics. Radiographics 25, 1521–1534 (2005). 26. Silva, P. D. & ripple, J. Laparoscopic diagnosis and treatment of an infarcted epiploic appendage. J. Am. Assoc. Gynecol. Laparosc. 3, 325–327 (1996). 27. romaniuk, C. S. & Simpkins, K. C. Case report: pericolic abscess secondary to a torsion of an appendix epiploica. Clin. Radiol. 47, 216–217 (1993). 28. Görg, C., Egbring, J. & Bert, T. Contrast‑enhanced ultrasound of epiploic appendagitis. Ultraschall. in Med. 30, 163–167 (2009). 29. Talukdar, r. et al. Epiploic appendagitis: report of two cases. Surg. Today 37, 150–153 (2007). 30. Hiller, N., Berelowitz, D. & Hadas‑Halpern, I. Primary epiploic appendagitis: clinical and radiological manifestations. IMAJ 2, 896–898 (2000). 31. Schnedl, W. J., Tillich, M. & Lipp, r. W. Image of the month. Primary epiploic appendagitis. Clin. Gastroenterol. Hepatol. 8, A16 (2010). 32. Lee, P. M. Small bowel obstruction due to epiploic appendagitis. Am. J. Gastroenterol. 85, 771–772 (1990). 33. Kyaw, M. M. & Koehler, P. r. Peudotumor of colon due to adhesion. Radiology 103, 597–599 (1972). 34. Borg, S. A., Whitehouse, G. H. & Griffith, C. J. A mobile calcified amputated appendix epiploica. Am. J. Roentgenol. 127, 349–350 (1976). 35. Elliot, G. B. & Freigang, B. Aseptic necrosis, calcification, and separation of appendices epiploicae. Am. Surg. 155, 501–505 (1962). 36. Jalaguier, A. et al. Accuracy of multidetector computed tomography in differentiating primary © 2011 Macmillan Publishers Limited. All rights reserved






41. 42.

epiploic appendagitis from left acute colonic diverticulitis associated with secondary epiploic appendagitis. Emerg. Radiol. 17, 51–56 (2010). Bastidas, J. G. et al. Epiploic appendagitis in a 24‑year‑old woman. Am. J. Emerg. Med. 26, 838–839 (2008). Osada, H. et al. Multidetector computed tomography diagnosis of primary and secondary epiploic appendagitis. Radiat. Med. 26, 582–586 (2008). Danielson, K., Chernin, M. M., Amberg, J. r., Goff, S. & Durham, J. r. Epiploic appendagitis: CT characteristics. J. Comput. Assist. Tomogr. 10, 142–143 (1986). Zissin, r. et al. Acute epiploic appendagitis: CT findings in 33 cases. Emerg. Radiol. 9, 262–265 (2009). Ammar, H., Looney, S. C. & Malani, A. Epiploic appendagitis. Lancet 373, 2054 (2009). Cianci, r., Filippone, A., Basilico, r. & Storto, M. L. Idiopathic segmental infarction of






the greater omentum diagnosed by unenhanced multidetector‑row CT and treated successfully by laparoscopy. Emerg. Radiol. 15, 51–56 (2008). Kirchoff, P., viehl, C. T., Heizmann, O., Oertli, D. & Potthast, S. Image of the month. Arch. Surg. 144, 587 (2009). Chou, Y. H. et al. Epiploic appendagitis of the rectosigmoid junction: demonstration with transerectal sonography. J. Clin. Ultrasound 34, 450–453 (2006). Lee, Y. C. et al. Gray‑scale and color Doppler sonographic findings of epiploic appendagitis. J. Clin. Ultrasound 29, 197–199 (2001). Hanson, J. M. & Kam, A. W. Paracolic echogenic mass in a man with lower abdominal pain. Is epiploic appendagitis more common than previously thought? Emerg. Med. J. 23, e17 (2006). Danse, E. M. et al. Epiploic appendagitis: color Doppler sonographic findings. Eur. Radiol. 11, 183–186 (2001).

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48. Sirvanci, M., Balci, N. C., Karaman, K., Duran, C. & Karakas, E. Primary epiploic appendagitis: MrI findings. Magn. Reson. Imaging 20, 137–139 (2002). 49. Mclure, M. J., Khalli, K., Sarrazin, J. & Hanbidge, A. radiological features of epiploic appendagitis and segmental omental infarction. Clin. Radiol. 56, 819–827 (2001). 50. Lien, W. C. et al. Epiploic appendagitis mimicking acute cholecystitis. Am. J. Emerg. Med. 22, 507–508 (2004).

author contributions W. J. Schnedl, r. Krause and r. W. Lipp researched data for the article and discussed the content of the manuscript together with E. Tafeit and S. J. Wallner‑Liebmann. The article was written by W. J. Schnedl, M. Tillich and S. J. Wallner‑Liebmann. All authors contributed equally to review and/or editing of the manuscript before submission.

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