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Cryptogenic Multifocal Ulcerous Stenosing Enteritis: A Review of the Literature
Cryptogenic multifocal ulcerous stenosing enteritis (CMUSE) is an extremely rare illness characterised by chronic or relapsing subileus status resulting from multiple small intestinal fibrous strictures and multiple shallow ulcers of the small bowel. The etiology is unknown and pathogenesis is not fully understood. Therapy with systemic glucocorticosteroids is the treatment of choice. However, most patients develop corticosteroid dependence. Deep enteroscopy enables precise diagnostic work, possible endoscopic treatment of stenoses; may obviate the need for surgery and prevent excessive small bowel resections.
Cryptogenic multifocal ulcerous stenosing enteritis (CMUSE) is a rare illness characterised by chronic or relapsing subileus or ileus status resulting from multiple small intestinal fibrous strictures, multiple shallow ulcers of the small bowel, and favourable therapeutic effect of systemic glucocorticosteroids [1–3].
The first descriptions of this rare condition probably came from the late 50s and early 60s [4–9], followed by further case reports or small series [10–17]. Matsumoto et al.  informed that Okabe and Sakimura reported first cases of CMUSE in Japan in 1968. Japanese gastroenterologists call this illness chronic nonspecific multiple ulcers (CNSU) of the small intestine .
However, all these early reports are difficult to evaluate nowadays, as diagnostic potential was limited at that time. Nowadays, owing to deep enteroscopy, it is possible to investigate the entire small intestine [18–21], take numerous biopsy specimens, and utilise other advanced diagnostic methods like flow cytometry and/or immunohistochemistry. That is why several distinct entities can be newly recognised .
CMUSE is an extremely rare illness. Only about sixty cases of CMUSE have been published so far [1–17, 22–24], but this entity has probably been considerably underdiagnosed or misdiagnosed, mostly with Crohn’s disease and nonsteroidal anti-inflammatory drugs- (NSAIDs)-induced enteropathy . Perlemuter et al.  reported 12 cases of CMUSE hospitalised in France between 1965 and 1993. This was a retrospective analysis of medical records based on queries sent to 220 French gastroenterology departments. Matsumoto et al.  published 15 cases from Japan (1964–2006) and provided thorough review of the literature. Our group reported three cases of CMUSE (diagnosed between 1994 and 2009 in a single tertiary centre) . Chang et al.  collected 2 cases of CMUSE diagnosed by means of double balloon enteroscopy in 48 patients (a series from 6 university hospitals in Korea).
4. Etiology and Pathogenesis
Immunological pathogenesis of CMUSE is supported by the favourable therapeutical effect of systemic glucocorticosteroids . Most of these patients become corticodependent [1–3, 24, 25]. The key to the solution of etiology and understanding pathogenesis might be overstimulated production of fibrous tissue . This is a principal sign of CMUSE, responsible for chronic or relapsing subileus episodes. Fibroblast proliferation can be augmented by proinflammatory cytokines (IL-6, IL-8, and TNF-alpha), fibroblast growth factors (FGS II), granulocyte/macrophage colony-stimulating factor (GM-CSF), transforming growth factor beta (TGF-beta), platelet-derived growth factor (PDGF) , and endotoxin (lipopolysaccharide) . Other growth factors, such as the connective tissue growth factor (CTGF), which is secreted by fibroblasts and endothelial cells, also promote formation of fibrous tissue . Collagen is degraded by a family of matrix metalloproteinases that include the collagenases. Matrix cells, neutrophils, and macrophages all secrete these proteinases. In healthy people, the degradation of collagen can be very rapid and begins immediately after collagen is produced . We have hypothesized, that multifocal small intestinal disturbance of collagen degradation in CMUSE might play a crucial role in pathogenesis . In CMUSE, fibrous tissue formation can be associated with low or even absent systemic inflammatory response .
Perlemuter et al. [1, 30] proposed that CMUSE could be termed as a type of “atypical vasculitis.” However, any type of vasculitis of any cause, if found, should be assigned simply as “vasculitis” not CMUSE . Small intestinal involvement can be found in Churg-Strauss syndrome [31–34], systemic lupus erythematosus , Buerger’s disease , Wegener’s granulomatosis , Weber-Christian disease , and systemic sclerosis . Vasculitis could be associated with multiple small intestinal ulcers and their complications (including perforation), but quite rarely with multifocal stenoses of the small bowel. Furthermore, vasculitis mostly represents a systemic involvement (kidneys, skin, joints, lungs, etc.). None of our three patients revealed any extraintestinal involvement, and small intestinal histology found no signs of vasculitis . Matsumoto et al.  did not reveal any arteritis in his series as well. Perlemuter et al.  suggested the association of CMUSE with C2 complement deficiency; however, this was not confirmed by other authors . Fraile et al.  reported an association of CMUSE with X-linked recessive reticulate pigmentary disorder. CMUSE was also reported in association with homozygous deletion mutations in cytosolic phospholipase A2-α . Hussey et al.  published a case of CMUSE as a manifestation of enterocolic venopathy.
5. Clinical Features
Chronic or relapsing subileus episodes resulting from multiple small intestinal strictures are a leading clinical symptom [1–3]. Chronic iron-deficiency anaemia due to small intestinal occult blood loss is frequently found [2, 43]. Patients may present with fatigue, edema, and growth retardation, and they usually have repeated episodes of treatment for anaemia. However, these subjects rarely manifest with diarrhoea, malabsorption, hematochezia or fever. Anaemia may precede the diagnosis of CMUSE for several years .
Patients with CMUSE were often referred for surgery because of symptomatic small intestinal strictures, and several resections of the small bowel had to be performed .
Clinicopathological features of CMUSE have been summarised as (1) unexplained small intestinal strictures found in adolescent and middle-aged subjects, (2) superficial ulceration of the mucosa and submucosa, (3) chronic or relapsing clinical course (even after surgery), (4) no biological signs of systemic inflammatory reaction, and (5) beneficial effect of systemic glucocorticosteroids [1, 2].
Perlemuter et al.  reported 12 cases of CMUSE hospitalised between 1965 and 1993. Despite surgery, symptoms reoccurred in seven of ten patients, and recurrence of strictures was reported in four. Inflammatory infiltrate was made of neutrophils and eosinophils. Glucocorticosteroid therapy was effective, but caused steroid dependence . Chang et al.  collected 2 cases of CMUSE diagnosed by means of double balloon enteroscopy in 48 patients (a series from 6 university hospitals in Korea). Both individuals suffered from chronic recurrent abdominal pain. One patient was presented with recurrent melaena (for 41 months), the other one was referred for surgery because of retention of a capsule endoscope in the stenotic site. Mesenteric arteriography did not demonstrate any evidence of arteritis .
In CMUSE, there are small intestinal stenoses, shallow ulcers, and mixed inflammatory infiltrate at histology (plasma cells, monocytes, neutrophils, and eosinophils), see Figures 1, 2, 3, 4, 5, and 6.
6. Diagnostics and Differential Diagnosis
The small intestinal ulcers in CMUSE/CNSU occur predominantly in the ileum; the terminal ileum is usually spared. The ulcers are usually multiple (more than 20). The small intestinal lesions never progress to cobble-stone appearance, fissure or fistula formation. The ulcers are restricted to the mucosa or submucosa; they never extend to the proper muscular layer. The mucosal lesions are characterised by infiltration of plasma cells, lymphocytes, and eosinophils .
There are no specific laboratory tests for the diagnosis of CMUSE. The faeces are positive for occult blood. Peripheral blood test reveals iron-deficiency microcytic anaemia. Some patients may manifest with hypoproteinemia and hypoalbuminemia. C-reactive protein and other acute inflammatory reactants are usually within their normal ranges or slightly increased .
|Adopted from Matsumoto et al. .|
*Depicted as symmetric and eccentric rigidity under small-bowel radiography, and concentric or non-concentric stricture under enteroscopy.
Wireless capsule endoscopy was complicated by retention of the capsule in one of our cases of CMUSE  and was also reported by others . Spontaneous disintegration of a retained video capsule was reported by our group previously .
In differential diagnosis of CMUSE, first of all, Crohn’s disease must be excluded [2, 3, 18, 29, 45–47], see Table 2. Crohn’s disease may occur in the jejunum without active disease elsewhere, but this seems to be uncommon, and jejunal involvement is usually associated with other clinical and pathological features of Crohn’s disease . CMUSE is characterized by mixed inflammatory infiltrate at histology (mostly plasma cells) [18, 44].
According to Freeman .|
In further differential diagnosis of CMUSE, other small intestinal diseases must be excluded, too, especially NSAIDs-induced enteropathy [2, 3, 18, 46–50], tuberculosis and other chronic infections of the small bowel [18, 33, 51], Behçet disease [52–54], drug-induced small intestinal injury (thiazides, potassium chloride) , and malignancies . It is a well-known fact, that the majority of extranodal malignant lymphoma involves the gastrointestinal tract. Not only polypoid and diffuse types of this disease, but also the ulcerative ones can be detected in the small bowel . Usually either diffuse large B-cell lymphoma or mucosa-associated lymphoid tissue (MALT) lymphoma is confirmed by histology . Multiple nonspecific ulcers in the small and large intestines occurred during tocilizumab therapy for rheumatoid arthritis .
It is also obligatory to distinguish CMUSE from other nonfrequent pathological conditions. We are convinced, that CMUSE is distinct from chronic ulcerative jejunitis [58, 59], collagen sprue , and autoimmune or eosinophilic enteritis [18, 61]. Similarly, nonspecific small intestinal ulcers [18, 62–64] should not be considered to be CMUSE if multiple stenoses of the small bowel are absent .
No causal treatment is available so far. Therapy with systemic glucocorticosteroids is the treatment of choice [1–3]. Dose of corticosteroids differs interindividually; some patients need systemic glucocorticosteroids (20 mg prednisone per day) and some do profit from topic steroids (budesonide 9 mg per day) . However, most patients develop corticosteroid dependence [1–3, 25]. Enteral or parenteral nutrition together with iron supplementation are transiently effective. Treatment with oral 5-aminosalicylic acid and azathioprine was ineffective. This therapy failed to induce mucosal healing or to prevent small intestinal strictures .
Multiple small intestinal fibrous strictures were previously resected surgically [1, 2, 24]; nowadays, they can be treated endoscopically by means of deep enteroscopy [3, 45]. Balloon dilatation of small intestinal non-ulcerated stenoses, if combined with corticosteroids, leads to disappearance of colicky abdominal pain and stenoses (verified on deep enteroscopy) [1, 45]. With the intention to avoid short bowel syndrome, surgery is the last choice of treatment in contemporary medicine with the availability of deep enteroscopy (when severe ileus episode occurs and cannot be managed by the pharmacology means of treatment, that is, intravenously administrated glucocorticosteroids) .
Recently, de Schepper et al.  reported that they had induced remission in CMUSE by anti-TNF-alpha therapy (using infliximab).
Prognosis of CMUSE remains uncertain. Patients were previously referred to surgery because of symptomatic small intestinal strictures. However, the postoperative recurrence rate was high . Matsumoto et al.  reported a single case of CMUSE followed up for 40 years since 1963. This patient was operated seven times because of recurrence of tight stenoses and several resections of the small bowel had to be performed .
In conclusion, CMUSE, although a rare condition affecting the small bowel, should always be considered when chronic or relapsing subileus episodes result from multiple small intestinal strictures, and multiple shallow ulcers of the small bowel are found (in the absence of Crohn’s disease, NSAID use, or chronic small intestinal infection). Deep enteroscopy enables precise diagnostic work; possible endoscopic treatment of stenoses may obviate the need for surgery and prevent excessive small bowel resections.
Conflict of Interests
The authors disclose no conflict of interests.
The study was supported by Research Project PRVOUK P37-08 (from Charles University in Praha, Faculty of Medicine at Hradec Králové, Czech Republic). We give thanks to Věra Tyčová, MD, who provided histological and immunohistochemical materials and to Zdeněk Vacek, MD, for the pictures from enteroclysis.
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