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Curt Tysk, Johan Bohr, Nils Nyhlin, Anna Wickbom, Department of Medicine, Division of Gastroenterology, Örebro University Hospital and School of Health and Medical Sciences, Örebro University, SE-701 85 Örebro, Sweden Sune Eriksson, Department of Pathology, Örebro University Hospital, SE-701 85 Örebro, Sweden Author contributions: All authors contributed in writing the article. Supported by Grants 16898-2005, 18293-2006 and 21142-2008 from the Swedish Society of Medicine (Bengt Ihre Foundation), Örebro County Research Committee, and Örebro University Hospital Research Foundation Correspondence to: Curt Tysk, Professor, Department of Medicine, Division of Gastroenterology, Örebro University Hospital, SE-701 85 Örebro, Sweden. curt.tysk@orebroll.se Telephone: +46-19-6021000 Fax: +46-19-6021774 Received: October 28, 2008 Revised: December 3,2008 Accepted: December 10,2008 Published online: December 28, 2008
Abstract Microscopic colitis, comprising collagenous and lymphocytic colitis, is characterized clinically by chronic watery diarrhea, and a macroscopically normal colonic mucosa where diagnostic histopathological features are seen on microscopic examination. The annual incidence of each disorder is 4-6/100 000 inhabitants, with a peak incidence in 60-70-year-old individuals and a noticeable female predominance for collagenous colitis. The etiology is unknown. Chronic diarrhea, abdominal pain, weight loss, fatigue and fecal incontinence are common symptoms, which impair the health-related quality of life of the patient. There is an association with other autoimmune disorders such as celiac disease, diabetes mellitus, thyroid disorders and arthritis. Budesonide is the best-documented short-term treatment, but the optimal long-term strategy needs further study. The long-term prognosis is good and the risk of complications including colonic cancer is low.
© 2008 The WJG Press. All rights reserved.
Key words: Microscopic colitis; Collagenous colitis; Lymphocytic colitis; Chronic diarrhea; Budesonide
Peer reviewer: David S Rampton, Professor, Centre for Gastroenterology, Institute of Cell and Molecular Science, Queen Mary School of Medicine and Dentistry, London E1 2AD, United Kingdom
Tysk C, Bohr J, Nyhlin N, Wickbom A, Eriksson S. Diagnosis and management of microscopic colitis. World J Gastroenterol 2008; 14(48): 7280-7288 Available from: URL: http://www.wjgnet.com/1007-9327/14/7280.asp DOI: http://dx.doi.org/10.3748/wjg.14.7280
INTRODUCTION Chronic diarrhea, reported in 4%-5% of individuals in Western populations, is a common cause for consulting a physician in general practice or in internal medicine, and for referral to a gastroenterologist[1]. Microscopic colitis (MC), previously regarded as rare, and certainly overlooked, has now emerged as a common cause of chronic diarrhea especially in elderly women. The condition is characterized clinically by chronic watery diarrhea, and a macroscopically normal or almost normal colonic mucosa, where microscopic examination of mucosal biopsies reveals characteristic histopathological changes[2]. MC comprises the two entities collagenous colitis (CC) and lymphocytic colitis (LC), which have indistinguishable clinical presentations but are separated by histopathological characteristics. This review will highlight epidemiology, clinical features, diagnosis and management of MC.
Epidemiology CC and LC, first described in 1976[3] and in 1989[4], respectively, have mostly been reported from European or North American centers, but the disease is found worldwide[5-10]. Currently, epidemiological data have been reported from seven different regions (Table 1)[5,6,11-17]. Long-term epidemiological data from Sweden and US since the 1980s show a rising incidence, which seems to have levelled off during the last study periods in the Swedish study. Whether the increasing incidence figures are an artefact, reflecting an increased awareness and improved diagnosis of the condition, or in fact represents a true rise is at present unknown. MC may be diagnosed in 10%-20% of cases investigated for chronic watery diarrhea[5]. CC mainly affects middle-aged women with a peak incidence around 65 years of age, and the female:male ratio is about 7:1 (Figure 1)[6,18]. However, the disease can occur in all ages, including children[19]. In LC, the peak incidence is in the same age group as CC, but the female predominance is less pronounced with a female:male ratio of 2-3:1 (Figure 1)[20].
Clinical presentation The clinical symptoms of CC and LC are similar and the diseases cannot be differentiated on clinical grounds. Both disorders cause chronic or recurrent non-bloody, watery diarrhea, often associated with nocturnal diarrhea, diffuse abdominal pain, and weight loss, which may be substantial[18,20,21]. Although some patients may suffer from severe diarrhea, serious dehydration is rare. Fatigue, nausea and fecal incontinence are other associated symptoms and the disease may significantly impair quality of life in the affected patient[22,23]. The onset of disease can be sudden and mimic infectious diarrhea[18,20]. The clinical course is often chronic relapsing and benign. Severe complications are rare, although there are reports of colonic perforation in CC[24-26]. No increased risk of colorectal cancer has been reported in CC[27]. A few cases with concomitant lymphoproliferative disorders and CC have been presented but further studies are required to assess if there is an increased risk[28]. Some patients may have mild symptoms that may be misinterpreted as irritable bowel syndrome[29]. Morphological findings of LC have been reported even in constipated or asymptomatic patients[30]. The natural history of the condition in these patients is unknown. Patients with MC often have concomitant autoimmune diseases[18,20,21]. The most common are thyroid disorders, celiac disease, diabetes mellitus and rheumatoid arthritis. The occurrence of such associations, reported in up to 40%-50% of patients in some cases, is variable depending on the study, and differences between LC and CC with respect to associated conditions have been described[18,20,21,31]. Bile acid malabsorption can often co-exist with MC and lead to worsening of symptoms[32]. An interchange between ulcerative colitis or Crohn’s disease and MC has been reported occasionally[33,34]. Whether this merely is a chance association of two fairly common disorders occurring in the same individual, or results from a common genetic predisposition or shared immunological pathways remains unknown.
Etiology and pathogenesis of mucosal inflammation The cause of MC is multifactorial and largely unknown. CC and LC are presently considered to represent specific mucosal responses in predisposed individuals to various noxious luminal agents. As CC and LC have many clinical similarities and share histopathological features, except for the subepithelial collagen layer found in CC, it has been discussed whether LC and CC are in fact the same disease seen in different stages of development. Conversion of LC to CC or vice versa has been reported. However, conversion is seen infrequently and this fact, together with the observed difference in sex ratio, makes it more likely to consider CC and LC as two separate but related entities. Data on the mucosal inflammation in MC are limited. In the epithelium, mainly CD8+ T lymphocytes are found that carry the a/b form of the T-cell receptor, and in the lamina propria there are mainly CD4+ T lymphocytes[35]. By means of segmental colorectal perfusion, increased luminal levels of eosinophilic cationic protein (ECP), basic fibroblast growth factor (bFGF) and vascular endothelial growth factor (VEGF) have been found in CC[36-38]. By immunohistochemistry, others have verified increased mucosal levels of VEGF that are not affected following therapy with budesonide[39]. A study of cytokines in MC found a TH1 mucosal cytokine profile with interferon g, tumor necrosis factor (TNF)a and interleukin-15 as the predominantly up-regulated cytokines[40]. Using Ussing chamber technology, transcellular and paracellular mucosal permeability has been found to be increased in patients with CC[41,42]. The excess subepithelial collagen in CC may be caused by an imbalance of collagen turnover. An increased collagen synthesis is supported by the finding of an increase in the number or the activity of myofibroblasts[43]. Among degrading enzymes, matrix-metalloproteinases (MMPs) have a central role that is regulated by tissue endogenous inhibitors of metalloproteinases (TIMPs)[44]. Impaired collagen degradation in CC is supported by the finding of restricted MMP-1 RNA expression and increased TIMP expression[45].
Genetics A familial occurrence of MC has been reported, but the role of genetic factors still remains largely unknown[46-49]. Human leukocyte antigen (HLA) studies have shown an association between MC and HLA-DQ2 or DQ1/3, and recently an association has reported between MC and HLA-DR3-DQ2 haplotype and with TNF2 allele carriage, irrespective of the presence of concomitant celiac disease[50,51]. Variants of the MMP-9 gene have been reported to be associated with CC[52]. No association with NOD2/CARD15 polymorphisms and susceptibility to CC has been found[53].
Luminal factoRS The mucosal inflammation with an increased number of intraepithelial T lymphocytes has suggested that MC may be caused by an immunological response to a luminal agent in predisposed individuals. This theory is supported by the observation that diversion of the fecal stream by an ileostomy normalizes or reduces the characteristic histopathological changes in CC[54]. After closure of the ileostomy, recurrence of symptoms and histopathological changes occur.
Drug-induced MC There are several reports on drug-induced MC and a strong likelihood of association has been found with acarbose, aspirin, Cyclo3 Fort, non-steroidal anti-inflammatory drugs, lansoprazole, ranitidine, sertraline and ticlopidine[55]. Assessment of concomitant drug use in patients with MC is therefore important to identify and consider withdrawal of drugs that might cause or worsen the condition.
Infection An infectious cause has been suspected, especially in patients with a sudden onset of disease. An association with MC and Campylobacter jejuni, Yersinia enterocolitica or Clostridium difficile has been reported occasionally[56-59]. LC shares many features with “Brainerd diarrhea”, which refers to outbreaks of acute watery diarrhea with long duration, first reported among 122 residents of Brainerd, Minnesota, USA[60]. Colonic biopsies of these patients show epithelial lymphocytosis similar to LC, but no crypt distortion or epithelial destruction[61]. Investigations of several outbreaks of Brainerd diarrhea have established an incubation period of 10-30 d and median duration of illness of 16 mo[62]. Although an infectious agent is thought to be the cause of Brainerd diarrhea, no microorganism has yet been identified. Furthermore, a seasonal pattern of onset of LC[20,63] may support an infectious cause. However, in most cases of MC with a sudden onset, stool cultures remain negative.
Bile acids Bile acid malabsorption can coexist with MC, which leads to worsening of symptoms. Concurrent bile acid malabsorption was found in 27%-44% of patients with CC and in 9%-60% of patients with LC[32,64,65]. These observations are the rationale for recommendations on bile acid binding treatment in MC. The treatment is especially effective in patients with concomitant bile acid malabsorption, but improvement has also been shown in patients without bile acid malabsorption.
Autoimmunity The association with other autoimmune diseases such as thyroid disease, celiac disease, diabetes mellitus or arthritis has suggested an autoimmune process. However, no specific autoantibody or marker has been identified.
Nitric oxide (NO) Colonic NO production is greatly increased in active MC caused by upregulation of inducible nitric oxide synthase (iNOS) in the colonic epithelium[66-69]. A major transcriptional inducer of iNOS gene expression is the transcription factor nuclear factor-kB (NF-kB). In active CC, colonic mucosal NF-kB has been found to be activated in epithelial cells but not in lamina propria macrophages, in contrast to ulcerative colitis[70]. The levels of NO are correlated to clinical and histological disease activity[67]. NO has been suggested to be involved in the pathophysiology of diarrhea in CC, as infusion in the colon of NG-monomethyl-L-arginine, an inhibitor of NOS, reduced colonic net secretion by 70% and the addition of L-arginine, a precursor of NO synthesis, increased colonic net secretion by 50%[68]. Further support for NO being involved in the pathogenesis of CC comes from therapeutic studies. Treatment with budesonide, in contrast to placebo, has resulted in a significant reduction of iNOS mRNA that is correlated with clinical and histopathological improvement[71].
Secretory or osmotic diarrhea The exact mechanism of diarrhea in MC has not been clarified fully. In CC, diarrhea has been regarded as secretory and caused by reduced net absorption of Na+ and Cl- ions caused by epithelial cell lesions, and the thickened collagenous layer as a co-factor that causes a diffusion barrier, and by additional active Cl- secretion[72]. Fasting, on the other hand, seems to reduce diarrhea, which indicates an osmotic component in some patients as well[73].
Diagnosis
Diagnosis
of MC relies solely on typical microscopic changes seen in colonic
mucosal biopsies[74]. In CC, a thickening of the
subepithelial collagen layer is seen together with a chronic mononuclear
inflammation in the lamina propria, and epithelial cell damage, with an
occasionally increased number of intraepithelial lymphocytes (Figure 2).
The thickened subepithelial collagen layer in CC is
≥
10 mm in well-orientated sections, in contrast to a normal basal
membrane of The diagnostic features of LC (Figure 2) are an increased number of intraepithelial lymphocytes (≥ 20/100 surface epithelial cells), in conjunction with surface epithelial cell damage and infiltration of lymphocytes and plasma cells into the lamina propria, but the collagen layer is normal, in contrast to CC[74]. In uncertain cases, immunostaining of CD3+ T lymphocytes facilitates the assessment of intraepithelial lymphocyte count (Figure 4). Barium enema and colonoscopy are usually normal, although subtle mucosal changes can be seen such as edema, erythema and abnormal vascular pattern[18,20]. Tears of colonic mucosa have occasionally been seen during colonoscopy, which might be a sign of increased risk of colonic perforation during the procedure[26,77-79]. In the future, the use of confocal laser microscopy may enable in vivo diagnosis of MC[80-82]. Laboratory tests are non-diagnostic and only non-specific abnormalities such as moderately elevated C-reactive protein, erythrocyte sedimentation rate, or mild anemia are found. Stool tests reveal no pathological microorganisms, but fecal calprotectin can be slightly elevated[83].
Atypical MC In addition to CC and LC, other rare subtypes of MC have been described including MC with giant cells[84,85], paucicellular LC[86], cryptal LC[87], pseudomembranous CC[88], MC with granulomatous inflammation[89], and MC not otherwise specified[74]. The clinical features of these conditions are similar to those of classical MC, but histopathological appearance differs. Further studies are required to address the relationship and clinical significance of these atypical forms of MC[90].
Therapy and prognosis A careful assessment of concomitant drug use and dietary factors such as excess use of caffeine, alcohol and dairy products that might worsen the condition is important. Concomitant bile acid malabsorption or celiac disease should be considered. In the patient with mild symptoms, loperamide or cholestyramine are recommended as the first step of treatment (Figure 5). Budesonide is the best-documented treatment and significantly improves the clinical symptoms and the patient’s quality of life. Three short-term, randomized controlled trials in CC have consistently shown that budesonide 9 mg daily for 6-8 wk is superior to placebo (Table 2)[91-93]. About 80% of patients responded to budesonide and had a decrease in the number of loose stools after 2-4 wk of therapy. In a Cochrane meta-analysis, the pooled odds ratio for clinical response with budesonide compared to placebo was 12.32 (95% CI 5.53-27.46), and the number needed to treat was two patients[94]. In a placebo-controlled trial including 41 patients, budesonide treatment was effective also in LC[95]. After 6 wk treatment, 18 of 21 patients (86%; 95% CI 65%-96%) in the budesonide group achieved a clinical response compared to eight of 20 patients (40%; 95% CI 22%-61%) in the placebo group, which yielded an odds ratio of 9.00 (95% CI 1.98-40.93; P = 0.004)[96]. The number needed to treat to achieve a clinical response with budesonide was three patients.
The
relapse rate is high after cessation of successful short-term budesonide
therapy in CC and 61%-80% of treated patients will have a recurrence of
symptoms[91-93]. In clinical practice, tapering doses of
budesonide to Other oral corticosteroids, such as prednisolone, are associated with more frequent side-effects, and the efficacy seems inferior to budesonide, although no formal comparative studies are available[99]. Bismuth subsalicylate has been shown to be effective in a small placebo-controlled study including nine patients with CC and five with LC[100]. This drug is not available in a number of countries because of concerns regarding drug toxicity. Sulfasalazine or mesalazine have been extensively used in MC but not strictly evaluated in randomized placebo-controlled trials. In a recent trial, 64 patients with MC were randomized to mesalazine 2.4 g/d or mesalazine 2.4 g/d + cholestyramine 4 g/d for 6 mo. A high remission rate was seen in both treatment arms, and 85% of patients with LC and 91% of those with CC were in remission at study end. Combined therapy was superior in CC and induced an earlier clinical response in both diseases[101]. The benefit of mesalazine with or without cholestyramine needs to be confirmed in a placebo-controlled trial. Antibiotics such as metronidazole or erythromycin have been used but not in a controlled fashion. Probiotic treatment shows uncertain results and need further evaluation[102]. Boswelia serrata extract has been tried in a placebo-controlled trial showing a non-significant trend in favor of active treatment[103]. In patients with unresponsive or steroid-resistant disease, immunosuppressive therapy may be considered, although the evidence is limited. An open study with azathioprine gave partial or complete remission in eight of nine patients with MC[104]. The efficacy of methotrexate has been assessed in a retrospective study[105]. Out of 19 patients with CC, a good response, generally seen within 2-3 wk of treatment, was seen in 16 and a partial response in two patients. The dose of methotrexate ranged from 5-25 mg/wk (median 7.5-10 mg/wk). Surgical therapy may be considered for patients with severe unresponsive MC. Both split ileostomy and subtotal colectomy have been performed and reported as successful[54,106]. The indications for surgical therapy today are limited, considering the improvement of medical therapy. The long-term prognosis of MC is generally good. In a follow-up study of CC, 63% of the patients had a lasting remission after 3.5 years, and in another cohort study, all 25 patients were improved 47 mo after diagnosis, and only 29% of them required ongoing medication[107,108]. A benign course was reported in 27 cases with LC, with resolution of diarrhea and normalization of histology in > 80% of patients within 38 mo[109]. Others have reported that 63% of patients with LC had a single attack, with a median duration from onset of symptoms to remission of 6 mo[20].
CONCLUSION MC is a fairly common cause of chronic diarrhea, especially in elderly women, and may considerably impair the patient’s quality of life. The correct diagnosis depends on the awareness of the condition by the clinician (referring the patient with chronic diarrhea to colonoscopy and not to barium enema), by the endoscopist (obtaining mucosal biopsies although the colonic mucosa is endoscopically normal) and by the pathologist (recognizing the histopathological features of MC). Treatment with budesonide is effective in the short term and improves the patient’s symptoms and quality of life, but the optimal long-term therapy needs further study. The long-term prognosis is good and the risk of complications including colonic cancer is low.
REFERENCES
1
Thomas PD, Forbes A, Green J, Howdle P, Long R, Playford R,
Sheridan M, Stevens R, Valori R, Walters J, Addison GM, 2 Pardi DS. Microscopic colitis: an update. Inflamm Bowel Dis 2004; 10: 860-870 PubMed DOI 3 Lindström CG. 'Collagenous colitis' with watery diarrhoea--a new entity? Pathol Eur 1976; 11: 87-89 PubMed
4
Lazenby AJ, Yardley JH, Giardiello FM, Jessurun J, Bayless TM.
Lymphocytic ("microscopic") colitis: a comparative
5
Olesen M, Eriksson S, Bohr J, Järnerot G, Tysk C. Microscopic
colitis: a common diarrhoeal disease. An epidemiological
6
Pardi DS, Loftus EV Jr, Smyrk TC, Kammer PP, Tremaine WJ, Schleck
CD, Harmsen WS, Zinsmeister AR, Melton LJ 3rd,
7
Rubio-Tapia A, Martínez-Salgado J, García-Leiva J,
Martínez-Benítez B, Uribe M. Microscopic colitides: a single center
8
Fekih M, Ben Hriz F, Sassi A, Matri S, Filali A, Boubaker J.
[Microscopic colitis. A 20 cases series] Tunis Med 2006; 84:
9 Tagkalidis P, Bhathal P, Gibson P. Microscopic colitis. J Gastroenterol Hepatol 2002; 17: 236-248 PubMed DOI
10
Garg PK, Singh J, Dhali GK, Mathur M, Sharma MP. Microscopic
colitis is a cause of large bowel diarrhea in Northern
11
Agnarsdottir M, Gunnlaugsson O, Orvar KB, Cariglia N, Birgisson
S, Bjornsson S, Thorgeirsson T, Jonasson JG.
12
Bohr J, Tysk C, Eriksson S, Järnerot G. Collagenous colitis in
Orebro, Sweden, an epidemiological study 1984-1993. Gut
13
Fernández-Bañares F, Salas A, Forné M, Esteve M, Espinós J, Viver
JM. Incidence of collagenous and lymphocytic
14
Heron T, Walsh S, Mowat A. Microscopic colitis in Tayside:
clinical features, associations, and behaviour. Gut 2005; 54
15
Rajan J, Noble C, Anderson C, Satsangi J, Lessels A, Arnott I.
The epidemiology and clinical features of collagenous
16
Wickbom A, Nyhlin N, Eriksson S, Bohr J, Tysk C. Collagenous
colitis and lymphocytic colitis in Örebro, Sweden 1999-
17
Williams JJ, Kaplan GG, Makhija S, Urbanski SJ, Dupre M,
Panaccione R, Beck PL. Microscopic colitis-defining incidence
18 Bohr
J, Tysk C, Eriksson S, Abrahamsson H, Järnerot G. Collagenous
colitis: a retrospective study of clinical presentation
19
Benchimol EI, Kirsch R, Viero S, Griffiths AM. Collagenous
colitis and eosinophilic gastritis in a 4-year old girl: a case
20
Olesen M, Eriksson S, Bohr J, Järnerot G, Tysk C. Lymphocytic
colitis: a retrospective clinical study of 199 Swedish
21
Pardi DS, Ramnath VR, Loftus EV Jr, Tremaine WJ, Sandborn WJ.
Lymphocytic colitis: clinical features, treatment, and
22
Madisch A, Heymer P, Voss C, Wigginghaus B, Bästlein E,
Bayerdörffer E, Meier E, Schimming W, Bethke B, Stolte M,
23
Hjortswang H, Tysk C, Bohr J, Benoni C, Kilander A, Vigren L,
Larsson L, Taha Y, Ström M. Health-related quality of life
24
Allende DS, Taylor SL, Bronner MP. Colonic perforation as a
complication of collagenous colitis in a series of 12
25
Bohr J, Larsson LG, Eriksson S, Järnerot G, Tysk C. Colonic
perforation in collagenous colitis: an unusual complication.
26
Sherman A, Ackert JJ, Rajapaksa R, West AB, Oweity T. Fractured
colon: an endoscopically distinctive lesion associated
27
Chan JL, Tersmette AC, Offerhaus GJ, Gruber SB, Bayless TM,
Giardiello FM. Cancer risk in collagenous colitis. Inflamm 28 Freeman HJ. Lymphoproliferative disorders in collagenous colitis. Inflamm Bowel Dis 2005; 11: 781-782 PubMed DOI
29
Limsui D, Pardi DS, Camilleri M, Loftus EV Jr, Kammer PP,
Tremaine WJ, Sandborn WJ. Symptomatic overlap between
30
Barta Z, Mekkel G, Csípo I, Tóth L, Szakáll S, Szabó GG, Bakó G,
Szegedi G, Zeher M. Microscopic colitis: a retrospective
31
Koskela RM, Niemelä SE, Karttunen TJ, Lehtola JK. Clinical
characteristics of collagenous and lymphocytic colitis. Scand
32
Ung KA, Gillberg R, Kilander A, Abrahamsson H. Role of bile acids
and bile acid binding agents in patients with
33
Aqel B, Bishop M, Krishna M, Cangemi J. Collagenous colitis
evolving into ulcerative colitis: a case report and review of
34
Pokorny CS, Kneale KL, Henderson CJ. Progression of collagenous
colitis to ulcerative colitis. J Clin Gastroenterol 2001;
35
Mosnier JF, Larvol L, Barge J, Dubois S, De La Bigne G, Hénin D,
Cerf M. Lymphocytic and collagenous colitis: an
36
Taha Y, Carlson M, Thorn M, Loof L, Raab Y. Evidence of local
eosinophil activation and altered mucosal permeability in
37
Taha Y, Raab Y, Larsson A, Carlson M, Lööf L, Gerdin B, Thörn M.
Mucosal secretion and expression of basic fibroblast
38
Taha Y, Raab Y, Larsson A, Carlson M, Lööf L, Gerdin B, Thörn M.
Vascular endothelial growth factor (VEGF)--a possible
39
Griga T, Tromm A, Schmiegel W, Pfisterer O, Müller KM, Brasch F.
Collagenous colitis: implications for the role of
40
Tagkalidis PP, Gibson PR, Bhathal PS. Microscopic colitis
demonstrates a T helper cell type 1 mucosal cytokine profile. J
41
Münch A, Söderholm JD, Wallon C, Ost A, Olaison G, Ström M.
Dynamics of mucosal permeability and inflammation in
42
Münch A, Söderholm JD, Öst A, Ström M. Increased transmucosal
uptake of E. coli in collagenous colitis is not reversed
43
Salas A, Fernández-Bañares F, Casalots J, González C, Tarroch X,
Forcada P, González G. Subepithelial myofibroblasts
44
Medina C, Radomski MW. Role of matrix metalloproteinases in
intestinal inflammation. J Pharmacol Exp Ther 2006;
45
Günther U, Schuppan D, Bauer M, Matthes H, Stallmach A, Schmitt-Gräff
A, Riecken EO, Herbst H. Fibrogenesis and 46 Freeman HJ. Familial occurrence of lymphocytic colitis. Can J Gastroenterol 2001; 15: 757-760 PubMed
47
Järnerot G, Hertervig E, Grännö C, Thorhallsson E, Eriksson S,
Tysk C, Hansson I, Björknäs H, Bohr J, Olesen M, Willén 48 Abdo AA, Zetler PJ, Halparin LS. Familial microscopic colitis. Can J Gastroenterol 2001; 15: 341-343 PubMed
49
van Tilburg AJ, Lam HG, Seldenrijk CA, Stel HV, Blok P, Dekker W,
Meuwissen SG. Familial occurrence of collagenous
50
Fine KD, Do K, Schulte K, Ogunji F, Guerra R, Osowski L,
McCormack J. High prevalence of celiac sprue-like HLA-DQ
51
Koskela RM, Karttunen TJ, Niemelä SE, Lehtola JK, Ilonen J,
Karttunen RA. Human leucocyte antigen and TNFalpha
52
Madisch A, Miehlke S, Schreiber S, Bethke B, Stolte M, Hellmig S.
Matrix metalloproteinase-9 gene polymorphism is
53
Madisch A, Hellmig S, Schreiber S, Bethke B, Stolte M, Miehlke S.
NOD2/CARD15 gene polymorphisms are not
54
Järnerot G, Tysk C, Bohr J, Eriksson S. Collagenous colitis and
fecal stream diversion. Gastroenterology 1995; 109:
55
Beaugerie L, Pardi DS. Review article: drug-induced microscopic
colitis - proposal for a scoring system and review of
56
Erim T, Alazmi WM, O'Loughlin CJ, Barkin JS. Collagenous colitis
associated with Clostridium difficile: a cause effect? Dig
57
Perk G, Ackerman Z, Cohen P, Eliakim R. Lymphocytic colitis: a
clue to an infectious trigger. Scand J Gastroenterol 1999;
58
Bohr J, Nordfelth R, Järnerot G, Tysk C. Yersinia species in
collagenous colitis: a serologic study. Scand J Gastroenterol
59
Mäkinen M, Niemelä S, Lehtola J, Karttunen TJ. Collagenous
colitis and Yersinia enterocolitica infection. Dig Dis Sci
60
Osterholm MT, MacDonald KL, White KE, Wells JG, Spika JS, Potter
ME, Forfang JC, Sorenson RM, Milloy PT, Blake PA.
61
Bryant DA, Mintz ED, Puhr ND, Griffin PM, Petras RE. Colonic
epithelial lymphocytosis associated with an epidemic of 62 Mintz E. A riddle wrapped in a mystery inside an enigma: Brainerd diarrhoea turns 20. Lancet 2003; 362: 2037-2038
63
LaSala PR, Chodosh AB, Vecchio JA, Schned LM, Blaszyk H. Seasonal
pattern of onset in lymphocytic colitis. J Clin
64
Fernandez-Bañares F, Esteve M, Salas A, Forné TM, Espinos JC,
Martín-Comin J, Viver JM. Bile acid malabsorption in
65
Ung KA, Kilander A, Willén R, Abrahamsson H. Role of bile acids
in lymphocytic colitis. Hepatogastroenterology 2002;
66
Lundberg JO, Herulf M, Olesen M, Bohr J, Tysk C, Wiklund NP,
Morcos E, Hellström PM, Weitzberg E, Järnerot G.
67
Olesen M, Middelveld R, Bohr J, Tysk C, Lundberg JO, Eriksson S,
Alving K, Järnerot G. Luminal nitric oxide and epithelial
68
Perner A, Andresen L, Normark M, Fischer-Hansen B, Sørensen S,
Eugen-Olsen J, Rask-Madsen J. Expression of nitric
69 Perner
A, Nordgaard I, Matzen P, Rask-Madsen J. Colonic production of
nitric oxide gas in ulcerative colitis, collagenous
70
Andresen L, Jørgensen VL, Perner A, Hansen A, Eugen-Olsen J, Rask-Madsen
J. Activation of nuclear factor kappaB in
71
Bonderup OK, Hansen JB, Madsen P, Vestergaard V, Fallingborg J,
Teglbjaerg PS. Budesonide treatment and
72
Bürgel N, Bojarski C, Mankertz J, Zeitz M, Fromm M, Schulzke JD.
Mechanisms of diarrhea in collagenous colitis.
73
Bohr J, Järnerot G, Tysk C, Jones I, Eriksson S. Effect of
fasting on diarrhoea in collagenous colitis. Digestion 2002;
65:
74
Warren BF, Edwards CM, Travis SP. 'Microscopic colitis':
classification and terminology. Histopathology 2002; 40:
374-
75
Tanaka M, Mazzoleni G, Riddell RH. Distribution of collagenous
colitis: utility of flexible sigmoidoscopy. Gut 1992; 33:
76
Müller S, Neureiter D, Stolte M, Verbeke C, Heuschmann P,
Kirchner T, Aigner T. Tenascin: a sensitive and specific
77
Cruz-Correa M, Milligan F, Giardiello FM, Bayless TM, Torbenson
M, Yardley JH, Jackson FW, Wilson Jackson F.
78
Wickbom A, Lindqvist M, Bohr J, Ung KA, Bergman J, Eriksson S,
Tysk C. Colonic mucosal tears in collagenous colitis.
79
Smith RR, Ragput A. Mucosal tears on endoscopic insufflation
resulting in perforation: an interesting presentation of
80
Kiesslich R, Hoffman A, Goetz M, Biesterfeld S, Vieth M, Galle
PR, Neurath MF. In vivo diagnosis of collagenous colitis by
81
Meining A, Schwendy S, Becker V, Schmid RM, Prinz C. In vivo
histopathology of lymphocytic colitis. Gastrointest Endosc
82
Zambelli A, Villanacci V, Buscarini E, Bassotti G, Albarello L.
Collagenous colitis: a case series with confocal laser
83
Wildt S, Nordgaard-Lassen I, Bendtsen F, Rumessen JJ. Metabolic
and inflammatory faecal markers in collagenous
84
Libbrecht L, Croes R, Ectors N, Staels F, Geboes K. Microscopic
colitis with giant cells. Histopathology 2002; 40: 335-
85
Sandmeier D, Bouzourene H. Microscopic colitis with giant cells:
a rare new histopathologic subtype? Int J Surg Pathol
86
Goldstein NS, Bhanot P. Paucicellular and asymptomatic
lymphocytic colitis: expanding the clinicopathologic spectrum of
87
Rubio CA, Lindholm J. Cryptal lymphocytic coloproctitis: a new
phenotype of lymphocytic colitis? J Clin Pathol 2002; 55:
88
Yuan S, Reyes V, Bronner MP. Pseudomembranous collagenous
colitis. Am J Surg Pathol 2003; 27: 1375-1379
89
Saurine TJ, Brewer JM, Eckstein RP. Microscopic colitis with
granulomatous inflammation. Histopathology 2004; 45: 82-
90
Chang F, Deere H, Vu C. Atypical forms of microscopic colitis:
morphological features and review of the literature. Adv
91
Baert F, Schmit A, D'Haens G, Dedeurwaerdere F, Louis E, Cabooter
M, De Vos M, Fontaine F, Naegels S, Schurmans P,
92
Bonderup OK, Hansen JB, Birket-Smith L, Vestergaard V, Teglbjaerg
PS, Fallingborg J. Budesonide treatment of
93
Miehlke S, Heymer P, Bethke B, Bästlein E, Meier E, Bartram HP,
Wilhelms G, Lehn N, Dorta G, DeLarive J, Tromm A,
94
Chande N, McDonald JW, Macdonald JK. Interventions for treating
collagenous colitis. Cochrane Database Syst Rev
95
Miehlke S, Madisch A, Karimi D, Wonschik S, Beckmann R, Kuhlisch
E, Morgner A, Müller R, Greinwald R, Baretton G,
96
Chande N, McDonald JW, Macdonald JK. Interventions for treating
lymphocytic colitis. Cochrane Database Syst Rev
97
Bonderup OK, Hansen JB, Teglbjoerg PS, Christensen LA,
Fallingborg JF. Long-term budesonide treatment of
98
Miehlke S, Madisch A, Bethke B, Morgner A, Kuhlisch E, Henker C,
Vogel G, Andersen M, Meier E, Baretton G, Stolte M.
99
Munck LK, Kjeldsen J, Philipsen E, Fischer Hansen B. Incomplete
remission with short-term prednisolone treatment in
100
Fine KD, Ogunji F, Lee E, Lafon G, Tanzi M. Randomized, double
blind, placebo-controlled trial of bismuth subsalicylate
101
Calabrese C, Fabbri A, Areni A, Zahlane D, Scialpi C, Di Febo G.
Mesalazine with or without cholestyramine in the
102
Wildt S, Munck LK, Vinter-Jensen L, Hanse BF, Nordgaard-Lassen I,
Christensen S, Avnstroem S, Rasmussen SN,
103
Madisch A, Miehlke S, Eichele O, Mrwa J, Bethke B, Kuhlisch E,
Bästlein E, Wilhelms G, Morgner A, Wigginghaus B,
104
Pardi DS, Loftus EV Jr, Tremaine WJ, Sandborn WJ. Treatment of
refractory microscopic colitis with azathioprine and 6-
105
Riddell J, Hillman L, Chiragakis L, Clarke A. Collagenous colitis:
oral low-dose methotrexate for patients with difficult
106
Varghese L, Galandiuk S, Tremaine WJ, Burgart LJ. Lymphocytic
colitis treated with proctocolectomy and ileal J-pouch-
107
Goff JS, Barnett JL, Pelke T, Appelman HD. Collagenous colitis:
histopathology and clinical course. Am J Gastroenterol
108
Bonner GF, Petras RE, Cheong DM, Grewal ID, Breno S, Ruderman WB.
Short- and long-term follow-up of treatment for
109
Mullhaupt B, Güller U, Anabitarte M, Güller R, Fried M. Lymphocytic
colitis: clinical presentation and long term course.
S- Editor Tian L L- Editor Kerr C E- Editor Zheng XM
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