IJGII Inernational Journal of Gastrointestinal Intervention

pISSN 2636-0004 eISSN 2636-0012
ESCI
scopus

Article

home All Articles View

Review Article

Int J Gastrointest Interv 2023; 12(1): 29-36

Published online January 31, 2023 https://doi.org/10.18528/ijgii220003

Copyright © International Journal of Gastrointestinal Intervention.

Radiologic images of complications of Crohn’s disease

Sungjin Yoon , So Hyun Park* , and Jun Seong Kim

Department of Radiology, Gil Medical Center, Gachon University College of Medicine, Incheon, Korea

Correspondence to:*Department of Radiology, Gil Medical Center, Gachon University College of Medicine, 21 Namdong-daero 774beon-gil, Namdong-gu, Incheon 21565, Korea.
E-mail address: nnoleeter@gilhospital.com (S.H. Park).

Received: February 3, 2022; Revised: March 6, 2022; Accepted: March 6, 2022

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/bync/4.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Crohn’s disease is a chronic inflammatory disease that may occur in the alimentary tract and has various clinical courses. It is characterized by several complications, including bowel strictures, bowel obstruction, fistulas, abscesses, and hydronephroureterosis. Each complication is related to adjacent bowel involvement in Crohn’s disease, and other complications can require surgical or interventional treatment. Patients with Crohn’s disease who develop intra-abdominal abscess tend to suffer from recurrent intra-abdominal abscess during the follow-up period. Intra-abdominal abscess can often develop at the fistula site. Bowel stricture due to Crohn’s disease leads to bowel obstruction. Radiologic examinations, such as computed tomography and magnetic resonance imaging, play an essential role in evaluating disease severity and complications in patients with Crohn’s disease.

Keywords: Crohn disease, Magnetic resonance imaging, Tomography, spiral computed

Patients with Crohn’s disease (CD) develop several complications, including penetrating disease during the long-term follow-up period. Chronic intestinal inflammation that occurs in CD can lead to the development of intestinal complications including strictures, fistulas, and abscesses.1 Each complication is associated with other complications; perilesional abscess can often develop at the fistula site during the course of CD. Patients with CD who develop intra-abdominal abscess (IAA) tend to suffer from recurrent IAA during the follow-up period. The American College of Gastroenterology (ACG) recommends that objective assessment using endoscopic or cross-sectional imaging be performed periodically to minimize errors of under- or over-treatment because the symptoms of CD do not correlate properly with the presence of active inflammation.1 Computed tomography (CT) and magnetic resonance imaging (MRI), which are representative cross-sectional imaging modalities, play a key role in the evaluation of disease severity and complications, such as IAA, bowel perforation, stricture, fistula, and hydronephroureterosis,13 whereas ileocolonoscopy is a crucial examination method for the diagnosis and follow-up evaluation of CD. Pelvic MRI has a main role in the investigation of perianal fistulas and abscesses.4,5 Thus, we reviewed the various CD-associated complications that can be revealed by radiologic examinations.

IAAs may result from the perforation of a hollow viscus into the peritoneum and from gastrointestinal fistulas. IAA is a common complication in patients with CD, occurring in up to 10% of these patients.6,7 The American College of Radiology suggests that if an IAA is suspected, cross-sectional imaging (i.e., CT) of the abdomen and pelvis should be performed.1 In CT images, IAAs show a rim-enhancing mass with perilesional infiltration adjacent to CD-associated active inflammation (Fig. 14). Asymmetric mural hyperenhancement, especially on the mesenteric side of the small bowel, is a specific CT finding of active inflammation in CD.2 An IAA is sometimes mistaken for a normal small bowel and thus can be missed in the radiologist’s reading of contrast-enhanced CT images. IAAs tend to occur adjacent to the CD-associated severely active inflammatory small bowel or other CD lesions, such as fistulizing lesions. The most common site of IAA is the right side of the abdomen, especially around the terminal ileum.8 It was found that 26% to 46% of patients who had previous IAAs developed recurrent abscesses during the course of CD.911 Thus, radiologists need to carefully to evaluate a patient who has fistulizing CD or had previous abscess, regardless of the presence of abscess in CT images. Radiologists must also take note of abscess-muscle fistulas or enterocutaneous fistulas in CT images, which can delay healing of the abscess or recurrent abscess (Fig. 5, 6). Patients who develop IAAs can be treated medically with antibiotics only, with antibiotics plus percutaneous drainage, or with antibiotics plus surgery.1 Currently, the first-line treatment of IAAs is antibiotic therapy with or without percutaneous drainage.12 The European Crohn’s and Colitis Organisation (ECCO) and the European Society of Colo-Proctology (ESCP) consensus recommend that IAAs smaller than 5 cm in size be treated with antibiotics only and that large abscesses (> 5 cm) be treated by percutaneous drainage with antibiotic therapy and follow-up by imaging.12 Percutaneous drainage may avoid surgery, be less invasive, and preserve bowel length to minimize the risk of short bowel syndrome.13,14

Figure 1. A 3-cm intra-abdominal abscess in a 38-year-old male patient with Crohn’s disease. Postcontrast-enhanced axial (A) and coronal (B) computed tomography images show fluid and air collection with rim enhancement in the right lower quadrant mesentery, consistent with an intra-abdominal abscess (white arrows). Multifocal segmental mural hyperenhancement (white arrowheads) and increased mesenteric vascularity (“comb sign”) with enlarged mesenteric lymph nodes (black arrow) are noted in the involved segment of the distal and terminal ileum. These findings are suggestive of active Crohn’s disease.
Figure 2. Several intra-abdominal abscesses in a 45-year-old male patient with Crohn’s disease. Postcontrast-enhanced axial (A) and coronal (B) computed tomography images show an intra-abdominal abscess (white arrows) in the right lower quadrant mesentery. There is another small abscess (black arrow) with peripheral enhancement on the right side of the larger abscess. Note that segmental mural hyperenhancement of the inner layer of the involved distal and terminal ileum (white arrowheads). These findings are suggestive of intra-abdominal abscess and adjacent active inflammatory Crohn’s disease.
Figure 3. A 3.6-cm intra-abdominal abscess in a 29-year-old male patient with Crohn’s disease. Postcontrast-enhanced axial (A) and coronal (B) computed tomography images show an air-containing abscess (white arrows) in the right lower mesentery. The coronal image exhibits severe wall thickening of the right proximal colon and deformity of the ileocecal valve (black arrow). A small amount of fluid (white arrowhead) is noted in the right paracolic gutter, consistent with localized peritonitis due to active Crohn’s disease with penetrating disease.
Figure 4. A 5-cm intra-abdominal abscess in a 22-year-old male patient with Crohn’s disease. Postcontrast-enhanced axial (A) and coronal (B) computed tomography images show fluid and air-containing abscesses (arrows) with rim enhancement in the adjacent pelvic loop of ileum. Coronal image demonstrates mild wall thickening and asymmetric mural hyperenhancement (arrowhead) along the mesenteric border of the pelvic ileal loop, consistent with active inflammatory Crohn’s disease.
Figure 5. Intra-abdominal abscess-muscle fistula and musculocutaneous fistula in a 21-year-old male patient with Crohn’s disease. (A) Postcontrast-enhanced axial computed tomography image shows a fistula between the intra-abdominal abscess and right iliopsoas muscle (white arrow). The patient underwent percutaneous drainage treatment. (B, C) Axial T2-weighted magnetic resonance images with fat saturation after 2 months. The residual abscess is noted in the right lower abdomen (white arrowhead). A tram track-like structure crossing from the peritoneal cavity to the anterior abdominal wall (subcutaneous fat layer and transversus abdominis) can be seen, consistent with musculocutaneous fistula (black arrows).
Figure 6. Enterocutaneous fistula in a 22-year-old male patient with Crohn’s disease, (A, B) Postcontrast-enhanced axial and coronal computed tomography images show a percutaneous drain catheter (arrows) inserted for the treatment of an intra-abdominal abscess. The catheter is inserted through the right rectus abdominis muscle. (C, D) Postcontrast-enhanced axial and coronal computed tomography images after 3 months of percutaneous drainage treatment. An enterocutaneous fistula (arrowheads) developed at the previous drain catheter insertion site.

Fistulas occur in approximately 30% of patients with CD, with the perianal area as the most common location. Enteroenteric, enterocolic, enterovesical, and rectovaginal fistulas can also develop in patients with CD.

Perianal fistulas occur in up to one-fourth of patients with CD.1 These fistulas are categorized as either simple (mainly in the anal sphincter area with a single tract, located distal to the dentate line) or complex (transsphincteric, suprasphincteric, or intersphincteric; may have multiple fistula tracts).1 Patients with symptomatic perianal fistulas usually undergo rectal MRI, which reveals the extent and complications of the fistula. In previous studies, endoscopic ultrasound and MRI examinations showed comparable accuracy for the diagnosis of perianal fistulas.15,16 When a patient undergoes an MRI examination, it is important to cover the full range of the perianal fistula. Because the external opening of the perianal fistula is often seen at the upper thigh level, the scan range of the pelvic MRI should include the upper thigh level and extend more caudally than usual rectal MRI to avoid incomplete coverage of the lesion. The radiologist can sometimes encounter an invisible external opening of the perianal fistula in MRIs due to incomplete scan range coverage. In such cases, the patient may undergo repetitive MRI to evaluate the end of the fistula tract. Fat suppression T2-weighted and contrast-enhanced fat suppression T1-weighted images (WIs) are especially useful for evaluating the extent of the fistula tract. Contrast-enhanced MRI and T2WI can be helpful in differentiating perianal fistulas with active inflammation from perianal fistulas with fibrotic change.17,18 Perianal fistulas with active inflammation generally appear as hyperintense tracts on T2WI (Fig. 7, 8), whereas fistula with fibrosis can be seen as a dark signal intensity on T2WI.19 Although inactive, healing fistulas may appear as loss of gadolinium enhancement with a linear tract on contrast-enhanced T1WI,19 and lesions with fibrosis can demonstrate progressive enhancement of variable degrees depending on the amount of fibrosis.18 Rectovaginal fistulas occur in approximately 9% of female with CD with anal involvement.20 Perianal fistulas are considered complex when the lesion has a tract along the perineum and external opening at the vagina (Fig. 7, 8). When radiologists review perianal fistulas in pelvic MRIs, they may describe the number of fistulas and all internal and external openings with complexity.

Figure 7. Complex-type intersphincteric perianal fistula in a 21-year-old female patient with perianal Crohn’s disease. (A, B) Axial T2-weighted fat-suppressed magnetic resonance images show an intersphincteric perianal fistula in the left posterior aspect of the anus (white arrows). (C, D) The white arrowhead indicates the superior aspect of the fistula where the internal opening connects to the left aspect (3’o clock, white arrowhead) of the rectum, and the black arrow indicates the inferior aspect of the fistula where the external opening connects to the posterior aspect (6’o clock) of the perineum.
Figure 8. Complex-type intersphincteric perianal fistulas in a 24-year-old female patient with perianal Crohn’s disease. (A) Axial T2-weighted magnetic resonance image (MRI) without fat saturation shows internal openings of two intersphincteric fistulas in the 11 o’clock and 2 o’clock directions (white arrows). (B) Coronal T2-weighted MRI without fat saturation shows the inferior extension of fistulas into the level of the lower rectum (white arrowheads). (C) Axial T2-weighted MRI without fat saturation shows the external opening of the left-sided fistula connected to the perineum (black arrow). (D) Axial diffusion-weighted image and (E) apparent diffusion coefficient map also show two fistulous tracts on both sides (black arrowheads).

Enteroenteric and enterocolic fistulas, which are one of internal fistulas, especially those connected between bowel segments, rarely require therapy and are often asymptomatic. CT examination is helpful in evaluating the presence and extent of internal fistulas (Fig. 9). The aggravation of asymmetric inflammation at the mesenteric side with sacculations along the antimesenteric side may result in enteroenteric and enterocolic fistulas. However, patients with internal fistulas often develop IAAs that affect treatment options, such as anti-tumor necrosis factor (anti-TNF) agents.9 Because the anti-TNF agentthat is used to treat severely active CD leads to apoptosis of macrophages, natural killer cells, and T-lymphocytes and reduces chronic pathologic inflammation, it may increase the risk of infections.21 As a result, anti-TNF agents can induce delayed healing when the patient has an abscess or other infections. IAA can sometimes be underestimated in contrast-enhanced CT images because the lesion can be mistaken for the adjacent bowel segment, which has a similar enhancement, thus inducing a delayed diagnosis of the abscess. Therefore, when enteroenteric or enterocolic fistulas present in CD, it is important to assess for adjacent bowel segments, which is commonly related to active inflammatory changes or other complications, such as abscess.

Figure 9. Enteroenteric fistulas in a 31-year-old male patient with Crohn’s disease. Postcontrast-enhanced axial (A) and coronal (B) computed tomography images show mural hyperenhancement of the distal ileal loop and right colon. These bowel loops are tethered and angulated to form asterisk-shaped ileocolic and ileoileal fistula complexes (arrows).

An enterovesical fistula can demonstrate recurrent urinary frequency and recurrent cystitis regardless of proper treatment (Fig. 10). It develops in 2%–8% of patients with CD.22,23 The right bladder dome is the predominant site of CD-related enterovesical fistulas, which is the site of the bladder closest to the terminal ileum.24 Superior elongation of the bladder with connection to the ileum is a common imaging finding of enterovesical fistula-associated CD. Sagittal and coronal CT images are more useful than axial CT scans for detecting enterovesical fistulas. Because the uterus and vagina protect the bladder from inflammation extension, enterovesical fistulas occur three times more frequently in male than in female.

Figure 10. Internal fistulas in a 33-year-old male patient with Crohn’s disease. (A) Postcontrast-enhanced coronal computed tomography image shows tethered distal ileal loop with mural hyperenhancement, forming an enterocolic fistula (white arrows). (B) There are tiny air bubbles in the urinary bladder (black arrow) and fistulous tract between the distal ileum and urinary bladder, consistent with an enterovesical fistula (white arrowheads).

The most common indication for surgical resection of the bowel in CD is intestinal obstruction due to a fibrostenotic stricture.1 The most common area of de novo strictures is the ileum and ileocolonic region, probably due to the ileum having a diameter smaller than that of the colon.25,26 In one patient, CT imaging revealed long segmental bowel dilatation with abrupt luminal narrowing manifesting as a transitional zone showing severe active CD involvement; the patient also had bowel obstruction symptoms (Fig. 11, 12). The National Cooperative CD Study in the USA described at least one small bowel stricture in 25% and at least single colonic stricture in 10% of patients with CD.27 The postoperative recurrence of CD at the anastomosis site commonly occurs after intestinal resection for the complication of a stricture, particularly in patients with ileocolonic anastomosis.28,29

Figure 11. Small bowel obstruction due to inflammatory stricture in a 21-year-old male patient with Crohn’s disease. (A) Postcontrast-enhanced coronal computed tomography image shows dilated small bowel loop with small bowel feces sign (white arrow). (B) The mesenteric border of the pelvic ileal loop is mildly thickened and shows asymmetrical mural hyperenhancement (white arrowheads). (C) Upstream small bowel loops are markedly distended (black arrow). (A–C) These findings suggest small bowel obstruction at the pelvic ileal loop owing to stricture associated with active inflammatory Crohn’s disease.
Figure 12. Active inflammation with stricturing Crohn’s disease and small bowel obstruction in a 17-year-old male patient. Postcontrast-enhanced coronal computed tomography image shows segmental bowel wall thickening and mural enhancement in the proximal jejunum (white arrow) (A), distal jejunum (black arrow) (B), and ileum (black arrowhead) (C), findings consistent with active inflammatory Crohn’s disease. The upstream proximal jejunum is markedly dilated (white arrowheads), consistent with small bowel obstruction due to stricturing Crohn’s disease.

Ureteral stricture with obstructive uropathy can develop after inflammation and fibrosis in the retroperitoneum. A common site for the development of ureteral strictures in patients with CD is the ureteropelvic junction at the sacroiliac joint level, which may necessitate urological intervention.30 Stent placement (usually as a transient double-J catheter30) and transient percutaneous nephrostomy31 are helpful in patients until proper surgical or medical treatment can be performed.32 Percutaneous nephrostomy can prevent renal damage before surgery, and double-J catheter placement can restore regular ureteral flow and minimize the risk of ureteral damage during the surgery.30,31 The associated inflammatory penetrating behavior of terminal ileal involvement, regardless of urolithiasis, predominantly occurs on the right side.33 The incidence rate of ureteral stricture-related hydronephrosis is approximately 6% in those with CD.24 The radiologist may consider inflammation of CD extension into the right ureter when the patient present with right hydronephroureterosis without urolithiasis and adjacent bowel inflammation in CT images (Fig. 13, 14).

Figure 13. Hydronephroureterosis in a 24-year-old male patient with Crohn’s disease. (A, B) Postcontrast-enhanced coronal computed tomography images show intra-abdominal abscess (black arrows; A), distal ileal wall thickening with symmetric bowel wall hyperenhancement (black arrows; B), and extended inflammation in the right ureter (white arrowheads; B) abdomen due to Crohn’s disease. This small bowel inflammation caused intra-abdominal abscess and ureteral obstruction in the right middle ureter (white arrowheads) and right hydronephrosis (white arrows).
Figure 14. Hydronephroureterosis in a 35-year-old male patient with Crohn’s disease. (A, B) Postcontrast-enhanced coronal computed tomography images show segmental wall thickening at pelvic ileal loop and terminal ileum with slightly asymmetric bowel wall hyperenhancement and pelvic inflammation (black arrows), causing right ureteral stenosis, upstream right ureteral dilatation (white arrowheads), and right hydroneprhosis (white arrows), findings consistent with active inflammatory Crohn’s disease with hydronephroureterosis. (C) The patient underwent percutaneous nephrostomy and ureteral stent insertion for the stricture.

Appendiceal CD is sometimes misdiagnosed as primary acute appendicitis in radiologic CT reports. A patient with active CD involving the appendix presents with clinical symptoms of acute appendicitis or periappendiceal abscess.3436 However, CT images of appendiceal CD (i.e., CD involving the appendix) show wall thickening of the appendix with periappendiceal inflammation combined with mural hyperenhancement of the adjacent other bowel and most of the cecum showing severe ileocolonic inflammation.35 Mural hyperenhancement of the cecum is different from secondary changes of the cecum due to primary acute appendicitis in CT images, which reveals mainly submucosal edema in the cecum. Therefore, these image features can be useful in distinguishing CD with appendiceal involvement from primary acute appendicitis. In particular, when a less experienced radiologist is likely to misdiagnose acute appendicitis or periappendiceal abscess in CT images in patients with appendiceal CD, patients who have not been diagnosed with CD (i.e. without prior history of CD) are clinically suspected of having acute appendicitis. When radiologists suspect acute appendicitis, they may determine whether the lesion is primary appendicitis or due to other disease involvement (Fig. 15). Because CT interpretation may affect the surgical plan (e.g., laparoscopic appendectomy, ileocecectomy, or delayed operation with percutaneous catheter drainage insertion), appropriate interpretation is needed for accurate patient diagnosis and treatment.

Figure 15. Intra-abdominal abscess around appendix mimicking perforated appendicitis in a 28-year-old male patient with Crohn’s disease. (A, B) Postcontrast-enhanced coronal computed tomography images show intra-abdominal abscess (white arrows) and segmental mural hyperenhancement of the right colon (white arrowhead) and distal ileum (black arrowhead), suggesting severe active inflammation of Crohn’s disease and penetrating disease. During the initial presentation, the patient was misdiagnosed with acute appendicitis and periappendiceal abscess with secondary bowel change. However, the patient had persistent abdominal pain and anemia after the appendectomy. After the computed tomography image was reviewed again, the patient was diagnosed with active Crohn’s disease involvement with penetrating disease. (C) The patient underwent percutaneous drainage due to recurred abscess. Tubography shows fistula formation (black arrows) between the complicated fluid collection and terminal ileum.
  1. Lichtenstein GR, Loftus EV, Isaacs KL, Regueiro MD, Gerson LB, Sands BE. ACG clinical guideline: management of Crohn’s disease in adults. Am J Gastroenterol. 2018;113:481-517. Erratum in: Am J Gastroenterol. 2018;113:1101.
    Pubmed CrossRef
  2. Guglielmo FF, Anupindi SA, Fletcher JG, Al-Hawary MM, Dillman JR, Grand DJ, et al. Small bowel Crohn disease at CT and MR enterography: imaging atlas and glossary of terms. Radiographics. 2020;40:354-75.
    Pubmed CrossRef
  3. Furukawa A, Saotome T, Yamasaki M, Maeda K, Nitta N, Takahashi M, et al. Cross-sectional imaging in Crohn disease. Radiographics. 2004;24:689-702.
    Pubmed CrossRef
  4. Gee MS, Harisinghani MG. MRI in patients with inflammatory bowel disease. J Magn Reson Imaging. 2011;33:527-34.
    Pubmed KoreaMed CrossRef
  5. Amitai MM, Ben-Horin S, Eliakim R, Kopylov U. Magnetic resonance enterography in Crohn’s disease: a guide to common imaging manifestations for the IBD physician. J Crohns Colitis. 2013;7:603-15.
    Pubmed CrossRef
  6. Greenstein AJ, Sachar DB, Greenstein RJ, Janowitz HD, Aufses AH Jr. Intraabdominal abscess in Crohn’s (ileo) colitis. Am J Surg. 1982;143:727-30.
    Pubmed CrossRef
  7. Keighley MR, Eastwood D, Ambrose NS, Allan RN, Burdon DW. Incidence and microbiology of abdominal and pelvic abscess in Crohn’s disease. Gastroenterology. 1982;83:1271-5.
    Pubmed CrossRef
  8. Yamaguchi A, Matsui T, Sakurai T, Ueki T, Nakabayashi S, Yao T, et al. The clinical characteristics and outcome of intraabdominal abscess in Crohn’s disease. J Gastroenterol. 2004;39:441-8.
    Pubmed CrossRef
  9. Nguyen DL, Sandborn WJ, Loftus EV Jr, Larson DW, Fletcher JG, Becker B, et al. Similar outcomes of surgical and medical treatment of intra-abdominal abscesses in patients with Crohn’s disease. Clin Gastroenterol Hepatol. 2012;10:400-4.
    Pubmed CrossRef
  10. Graham E, Rao K, Cinti S. Medical versus interventional treatment of intra-abdominal abscess in patients with Crohn disease. Infect Dis (Auckl). 2017;10: 1179916117701736.
    Pubmed KoreaMed CrossRef
  11. Garcia JC, Persky SE, Bonis PA, Topazian M. Abscesses in Crohn’s disease: outcome of medical versus surgical treatment. J Clin Gastroenterol. 2001;32:409-12.
    Pubmed CrossRef
  12. Bemelman WA, Warusavitarne J, Sampietro GM, Serclova Z, Zmora O, Luglio G, et al. ECCO-ESCP consensus on surgery for Crohn’s disease. J Crohns Colitis. 2018; 12:1-16.
    Pubmed CrossRef
  13. Clancy C, Boland T, Deasy J, McNamara D, Burke JP. A meta-analysis of percutaneous drainage versus surgery as the initial treatment of Crohn’s disease-related intra-abdominal abscess. J Crohns Colitis. 2016;10:202-8.
    Pubmed CrossRef
  14. Feagins LA, Holubar SD, Kane SV, Spechler SJ. Current strategies in the management of intra-abdominal abscesses in Crohn’s disease. Clin Gastroenterol Hepatol. 2011;9:842-50.
    Pubmed CrossRef
  15. Wise PE, Schwartz DA. The evaluation and treatment of Crohn perianal fistulae: EUA, EUS, MRI, and other imaging modalities. Gastroenterol Clin North Am. 2012;41:379-91.
    Pubmed CrossRef
  16. Villa C, Pompili G, Franceschelli G, Munari A, Radaelli G, Maconi G, et al. Role of magnetic resonance imaging in evaluation of the activity of perianal Crohn’s disease. Eur J Radiol. 2012;81:616-22.
    Pubmed CrossRef
  17. Van Assche G, Vanbeckevoort D, Bielen D, Coremans G, Aerden I, Noman M, et al. Magnetic resonance imaging of the effects of infliximab on perianal fistulizing Crohn’s disease. Am J Gastroenterol. 2003;98:332-9.
    Pubmed CrossRef
  18. Santillan CS, Huang C, Eisenstein S, Al-Hawary MM. MRI of perianal Crohn disease: technique and interpretation. Top Magn Reson Imaging. 2021;30:63-76.
    Pubmed CrossRef
  19. Sheedy SP, Bruining DH, Dozois EJ, Faubion WA, Fletcher JG. MR imaging of perianal Crohn disease. Radiology. 2017;282:628-45.
    Pubmed CrossRef
  20. Hyman NH, Fazio VW, Tuckson WB, Lavery IC. Consequences of ileal pouch-anal anastomosis for Crohn’s colitis. Dis Colon Rectum. 1991;34:653-7.
    Pubmed CrossRef
  21. Ali T, Kaitha S, Mahmood S, Ftesi A, Stone J, Bronze MS. Clinical use of anti-TNF therapy and increased risk of infections. Drug Healthc Patient Saf. 2013;5:79-99.
    Pubmed KoreaMed CrossRef
  22. Greenstein AJ, Sachar DB, Tzakis A, Sher L, Heimann T, Aufses AH Jr. Course of enterovesical fistulas in Crohn’s disease. Am J Surg. 1984;147:788-92.
    Pubmed CrossRef
  23. Schwartz DA, Loftus EV Jr, Tremaine WJ, Panaccione R, Harmsen WS, Zinsmeister AR, et al. The natural history of fistulizing Crohn’s disease in Olmsted County, Minnesota. Gastroenterology. 2002;122:875-80.
    Pubmed CrossRef
  24. Ben-Ami H, Ginesin Y, Behar DM, Fischer D, Edoute Y, Lavy A. Diagnosis and treatment of urinary tract complications in Crohn’s disease: an experience over 15 years. Can J Gastroenterol. 2002;16:225-9.
    Pubmed CrossRef
  25. Gasche C, Scholmerich J, Brynskov J, D’Haens G, Hanauer SB, Irvine EJ, et al. A simple classification of Crohn’s disease: report of the Working Party for the World Congresses of Gastroenterology, Vienna 1998. Inflamm Bowel Dis. 2000;6:8-15.
    Pubmed CrossRef
  26. Fukumoto A, Tanaka S, Yamamoto H, Yao T, Matsui T, Iida M, et al. Diagnosis and treatment of small-bowel stricture by double balloon endoscopy. Gastrointest Endosc. 2007;66(3 Suppl):S108-12.
    Pubmed CrossRef
  27. Summers RW, Switz DM, Sessions JT Jr, Becktel JM, Best WR, Kern F Jr, et al. National cooperative Crohn’s disease study: results of drug treatment. Gastroenterology. 1979;77(4 Pt 2):847-69.
    Pubmed CrossRef
  28. Peyrin-Biroulet L, Loftus EV Jr, Colombel JF, Sandborn WJ. The natural history of adult Crohn’s disease in population-based cohorts. Am J Gastroenterol. 2010;105: 289-97.
    Pubmed CrossRef
  29. Rutgeerts P, Geboes K, Vantrappen G, Kerremans R, Coenegrachts JL, Coremans G. Natural history of recurrent Crohn’s disease at the ileocolonic anastomosis after curative surgery. Gut. 1984;25:665-72.
    Pubmed KoreaMed CrossRef
  30. Angelberger S, Fink KG, Schima W, Szlauer R, Vogelsang H, Reinisch W, et al. Complications in Crohn’s disease: right-sided ureteric stenosis and hydronephrosis. Inflamm Bowel Dis. 2007;13:1056-7.
    Pubmed CrossRef
  31. Ruffolo C, Angriman I, Scarpa M, Polese L, Barollo M, Bertin M, et al. Minimally invasive management of Crohn’s disease complicated by ureteral stenosis. Surg Laparosc Endosc Percutan Tech. 2004;14:292-4.
    Pubmed CrossRef
  32. Kane S. Urogenital complications of Crohn’s disease. Am J Gastroenterol. 2006; 101(12 Suppl):S640-3.
    CrossRef
  33. Sigel A, Botticher R, Wilhelm E. Urological complications in chronic inflammatory diseases of the bowel. Eur Urol. 1977;3:7-10.
    Pubmed CrossRef
  34. Han H, Kim H, Rehman A, Jang SM, Paik SS. Appendiceal Crohn’s disease clinically presenting as acute appendicitis. World J Clin Cases. 2014;2:888-92.
    Pubmed KoreaMed CrossRef
  35. Mostyka M, Fulmer CG, Hissong EM, Yantiss RK. Crohn disease infrequently affects the appendix and rarely causes granulomatous appendicitis. Am J Surg Pathol. 2021;45:1703-6.
    Pubmed CrossRef
  36. Bronner MP. Granulomatous appendicitis and the appendix in idiopathic inflam­matory bowel disease. Semin Diagn Pathol. 2004;21:98-107.
    Pubmed CrossRef