A Prospective Study of the Oral Manifestations of Crohn s Disease
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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2005;3: A Prospective Study of the Oral Manifestations of Crohn s Disease SINEAD HARTY,* PADRAIG FLEMING, MARION ROWLAND,* ELLEN CRUSHELL,* MICHAEL MCDERMOTT,* BRENDAN DRUMM,* and BILLY BOURKE* *Children s Research Centre, Our Lady s Hospital for Sick Children, Department of Paediatrics, Conway Institute for Biomolecular and Biomedical Research and Dublin Molecular Medicine Center, University College Dublin, Dublin; and Dublin Dental Hospital, Trinity College Dublin, Dublin, Ireland Background & Aims: Recent studies suggest that the mouth may be involved frequently in patients with Crohn s disease (CD). The aim of this study was to document prospectively the proportion of children with oral lesions at diagnosis of CD, to describe the type of lesions found, and to examine the ability of gastroenterologists to identify correctly oral Crohn s manifestations. Methods: In a prospective 3-year study, systematic dental examinations were performed on all children with suspected inflammatory bowel disease. Each child underwent upper endoscopy, colonoscopy, and barium follow-through radiography. Results: Forty-eight of 49 children with CD were examined by the dentist. Oral CD was found in 20 patients (41.7%). Oral findings included mucogingivitis (12 patients), mucosal tags (4 patients), deep ulceration (4 patients), cobblestoning (3 patients), lip swelling (3 patients), and pyostomatitis vegetans (1 patient). Noncaseating granulomas were found in all 8 oral biopsy specimens from oral CD lesions (100%). Two patients with granulomas in oral biopsy specimens had no granulomas found in any other biopsy specimens. The presence of oral manifestations was associated with perianal disease. In only 9 patients (45%) with oral CD was the mouth found to be abnormal by the consultant gastroenterologists. Only nonspecific oral changes were seen in children with ulcerative colitis and indeterminate colitis. Conclusions: More than one third of all children presenting with CD had involvement of the mouth. The ability of physicians to recognize oral lesions was poor. Expert dental evaluation may be useful during the investigation of patients with suspected inflammatory bowel disease. Although it is recognized widely that Crohn s disease (CD) can affect any site in the gastrointestinal tract from the mouth to the anus, the recognition of oral lesions in patients with CD and their potential clinical relevance has evolved only recently. 1,2 Patients with CD often suffer from aphthous ulceration of the oral cavity. However, because these ulcers also occur commonly in patients with ulcerative colitis and in the general population, they are not specific for CD. 3 In contrast, a number of characteristic oral lesions have been described in patients with CD. These include swelling of the lips, buccal mucosal swelling or cobblestoning, deep linear ulceration, mucosal tags, and mucogingivitis The prevalence of oral lesions in CD has varied widely in previous studies. 8,13,14 In a recent retrospective study performed at our centre 8 we found a particularly high prevalence of disease-specific oral lesions in children with CD. In that study of 25 children who had been examined by a pediatric dental surgeon at the time of initial presentation, 48% had disease-specific oral lesions. In addition, granulomas were found in 75% of 8 oral biopsy specimens in that study, suggesting that the mouth may provide an important site for obtaining diagnostic tissue in children with symptoms of inflammatory bowel disease (IBD). 8 Therefore, the aim of the present study was to document prospectively the proportion of children with evidence of oral CD at initial evaluation for suspected IBD and to describe the spectrum of lesions found. We also explored whether the presence of oral lesions correlated with markers of disease severity at diagnosis, and if oral CD was associated with a particular distribution of disease elsewhere in the gastrointestinal tract. In addition, we compared the results of oral examination by consultant gastroenterologists in the clinic setting with formal oral examination by a pediatric dental surgeon. Methods Over a 3-year period between January 1999 and December 2001 we prospectively recorded the oral manifestations in children presenting with suspected CD to the gastroenterology department of Our Lady s Hospital for Sick Children. Abbreviations used in this paper: CD, Crohn s disease; CI, confidence interval; IBD, inflammatory bowel disease by the American Gastroenterological Association /05/$30.00 PII: /S (05)
2 September 2005 ORAL MANIFESTATIONS OF CD 887 More than 75% of Irish children and adolescents with pediatric IBD undergo diagnostic evaluation at our institution (Irish Paediatric Surveillance unit data , unpublished data). Information was recorded prospectively on each patient before endoscopy including age, sex, presenting symptoms, oral symptoms, family history, and medications. Clinical examination was performed on each patient and findings including weight and height were recorded. Perianal findings were noted. Blood samples were taken for full blood count and liver function including albumin and C-reactive protein levels. Small-bowel contrast studies were performed routinely after the initial assessment. The oral cavity was inspected thoroughly by 1 of the 2 consultant gastroenterologists performing the endoscopy before examination by the dentist and the findings were documented. For this study, all oral examinations were performed by the same pediatric dental surgeon (P.F.). Dental examinations were performed in a dental chair with the use of standard lighting. Systematic assessment of the submandibular lymph nodes, lips, labial mucosa and sulci, commissures, buccal mucosa and sulci, gingiva, tongue, floor of mouth, and hard and soft palate were performed and findings were recorded. Oral biopsy specimens were taken only when clinically indicated. For example, when a diagnosis of CD was clear from other findings (eg, perianal disease), an oral biopsy examination was not performed. All children underwent upper gastrointestinal endoscopy as well as colonoscopy. Biopsy specimens were taken from grossly affected tissue and from unaffected gastric and colonic mucosa. All biopsy specimens were formalin fixed and paraffin embedded. Serial H&E-stained 4- m sections were examined in each case. This typically represented 18 to 20 sections per biopsy specimen. When granulomas were found, periodic acid-schiff, Grocott, and Ziehl Neelsen stains were performed on the specimens to rule out fungal and mycobacterial disease. Data were analyzed using Epi Info (CDC, Atlanta, GA). Comparison between groups was made using odds ratios and 95% confidence intervals (CIs) for categoric variables and t tests for continuous variables. Statistical significance was set at the 5% level. Results Over the 3-year period, 80 patients were diagnosed with IBD. Final diagnoses were CD in 49 (61.3%) patients, ulcerative colitis in 22 (27.5%) patients, and indeterminate colitis in 9 (11.3%) patients. Occurrence of Oral Crohn s Disease Forty-eight of the 49 patients with CD were examined by the dentist. Findings typical of oral CD were found in 20 patients (41.7%). Nonspecific gingivitis (ie, gingival inflammation related to the presence of dental plaque) was found in 8 (16.7%) patients, and 20 (41.7%) patients had a normal oral examination. Of the 20 patients with oral CD changes, 12 were boys and 8 were girls (1.5:1) compared with 13 boys and 15 girls in children not found to have oral CD (.86:1; P not significant). The mean age for all children with CD was years (SD, 2.7 y; range, y). The mean age of children with oral CD was 11.4 years (SD, 2.5 y) and without oral CD was 12.3 years (SD, 2.8 y; P not significant). No patient was being treated specifically for oral lesions. Patients with oral CD were significantly more likely to complain of oral symptoms (odds ratio, 4.9; 95% CI, ; P.01) and most complained of more than 1 symptom (mouth ulcers in 11 patients, angular stomatitis in 5 patients, and cheek/lip swelling in 8 patients). However, there was no difference in the duration of oral symptoms between the groups (mean difference, 2.9 mo; 95% CI, 4.7 to 10.5). The duration of oral symptoms ranged from 1 to 56 months (mean, 4.9 mo; SD, 12.7 mo). Oral symptoms did not precede systemic symptoms in any of the patients with oral CD. Manifestations of Oral Crohn s Disease More than half the patients (n 11) had more than 1 type of oral lesion (Figure 1). The most common oral finding was mucogingivitis (n 12), followed by mucosal tags (n 4), deep ulceration (n 4), cobblestoning (n 3), and lip swelling (n 3). One patient had pyostomatitis vegetans. Oral biopsy examinations were performed on 8 patients with oral CD. Noncaseating granulomas were found in biopsy material from all 8 patients (100%) undergoing oral biopsy examination. Five patients had biopsy specimens taken from areas of mucogingivitis, 1 patient from a tag, 1 patient from an area of cobblestoning, and 1 patient from an ulcer. Most of the oral biopsy specimens were taken from the buccal mucosa. Two patients with granulomas in oral biopsy specimens did not have granulomas present in multiple biopsy specimens taken from the upper and lower gastrointestinal tract. Clinical and Laboratory Features Associated With Oral Crohn s Disease There was no difference in the frequency of intestinal and systemic symptoms (Table 1) or the severity of laboratory markers (Table 2) between the 2 groups. The site of intestinal CD was compared in those with and without oral CD. Five children were infected with Helicobacter pylori. The presence or absence of Crohn s gastritis, as opposed to H pylori gastritis, could not be
3 888 HARTY ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 3, No. 9 Figure 1. (A) Lip swelling with fissures. (B) Cobblestone appearance of the buccal mucosa. (C) Linear ulceration deep in the mandibular vestibule. (D) Mucosal tag on the buccal aspect of the gingiva. (E) Mucogingivitis in relation to the maxillary permanent incisors. distinguished reliably in these patients and, therefore, they were excluded from this analysis. Among the remaining 43 children, those with oral CD were significantly more likely to have perianal disease than those without oral CD (10 of 20 [50%] compared with 4 of 23 [14%]; P.023, based on univariate analysis). However, other sites of disease were affected similarly in both groups (Table 3). Ability of Physicians to Recognize Oral Crohn s Disease Forty-six children with CD had oral findings recorded by both the pediatric gastroenterologist and the dentist. Agreement between the dentist and gastroenterologist was poor (,.22; 95% CI,.06 to.50). In 8 children without oral CD the gastroenter-
4 September 2005 ORAL MANIFESTATIONS OF CD 889 Table 1. Comparison of Intestinal and Systemic Manifestations Among Patients With and Without Oral CD Oral CD (total 20) Nonoral CD (total 28) Symptoms n % n % Odds ratio 95% CI P Loss of appetite NS Oral symptoms Mouth ulcers NS Angular stomatitis NS Cheek swelling a Vomiting NS Epigastric pain 0 0 a 1 4 Abdominal pain NS Tenesmus NS Blood per rectum NS Constipation NS Malena 0 0 a 0 0 Perirectal disease NS Arthritis 0 0 a 2 7 Clubbing NS Erythema nodosum NS Uveitis 0 0 a 0 0 NS, not significant. a No calculations were performed for cells with zero values. ologist classified the mouth as abnormal, and in 11 (55%) children with oral CD the gastroenterologist failed to identify the oral CD lesions correctly. The presence of mucogingivitis appeared to be particularly difficult for the nonoral expert to appreciate with only 4 of 12 cases correctly identified. Oral Findings in Children With Ulcerative Colitis and Indeterminate Colitis Although this study aimed to document the occurrence of oral findings in CD, a substantial proportion of children ultimately diagnosed with ulcerative colitis or indeterminate colitis also were examined. Of 22 patients diagnosed with ulcerative colitis during the study period, a dental examination was performed in 15 (68.2%). Only 2 patients had abnormal oral findings, comprising nonspecific gingivitis related to periodontal disease in both. Of these children 1 underwent oral biopsy examination that revealed the presence of acute and chronic inflammation without granulomas. Similarly, 7 of 9 patients with indeterminate colitis were examined by the dentist. Two patients were found to have nonspecific gingivitis; 1 patient underwent oral biopsy examination that revealed the presence of acute and chronic inflammation without granulomas. Discussion In this prospective study we confirmed that children with CD commonly harbor disease-specific oral Table 2. Comparison of Clinical and Laboratory Data for Patients With and Without Oral CD Laboratory value Oral CD, N 20 (SD) Nonoral CD, N 28 Mean difference 95% CI of mean difference Hemoglobin 99.9 (34.6) (15.6) to 6.1 Hematocrit 30.6 (11.5) 32.3 (7.8) to 3.9 MCH 21.1 (8.1) 24.3 (2.8) to.17 MCV 69.9 (17.4) 75.3 (6.4) to 1.8 Albumin 32.6 (5.3) 34.4 (6.4) to 1.8 ESR 37.1 (20.9) n (18.4) n to 16.5 CRP 39.2 (35.1) n (25.5) n to 29.8 Platelets (233.8) (136.5) to Duration of symptoms 12.7 (17.7) 9.7 (8.1) to Duration of oral symptoms 4.2 (12.6) 1.1 (5.1) to 8.44 NOTE. The use of ESR was replaced by CRP at our institution. MCH, mean cell hemoglobin; MCV, mean cell volume; ESR, erythrocyte sedimentation rate; CRP, C-reactive protein.
5 890 HARTY ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 3, No. 9 Table 3. Disease Location: Comparison of Site of Disease in Children With and Without Oral Lesions Using Single Group Comparisons Site of disease Oral CD (total 20) Nonoral CD (total 23) n % n % Odds ratio 95% CI P Stomach NS Small bowel NS Ileum NS Colon NS Perianal NS, not significant. manifestations at the time of diagnosis. At more than 40% the occurrence of oral CD correlates well with the findings of a previous retrospective study at our institution. 8 In that study, 48% of 25 children had oral involvement at the time of diagnosis of CD. The slightly lower proportion of children with oral CD in the present cohort likely is accounted for by selection bias inherent in the retrospective design of our previous investigation. However, taken together, these studies clearly indicate that the oral cavity is a useful source of diagnostic material in children presenting with IBD. Previously 8 we have speculated as to the reasons underlying the relatively higher prevalence of oral CD in our population compared with other studies. 4,5,13,14 Factors such as possible increased involvement of the proximal gastrointestinal tract in younger patients 15 and examination at the time of diagnosis, before the institution of drug therapy, may have increased the relative numbers of children with oral CD in our population. However, routine examination of the oral cavity by an experienced dental surgeon was perhaps the major factor underlying the high prevalence of oral CD findings in the present study. Although our pediatric gastroenterology group have an established interest in oral CD, the ability of the physicians in this study to identify and classify accurately the oral CD findings was poor (,.22; 95% CI,.06 to.50). Clearly, to be useful, oral examination in patients with IBD requires involvement of an experienced dentist or oral physician. The potential usefulness of oral CD findings as a source of diagnostic material in patients with CD is underscored by the frequency with which granulomas are identified in these lesions. In the present study we could not justify on ethical grounds a routine oral biopsy examination, especially in children in whom the diagnosis of CD was in little doubt (eg, those with perianal disease at presentation). However, when oral biopsy examination was performed granulomas were identified in all 8 lesions pre-identified as those of oral CD. In contrast, the 2 biopsy specimens from patients with ulcerative and indeterminate colitis harbored nonspecific inflammatory changes without the presence of granulomas. The type of mouth lesions identified in the present study covered the spectrum of oral CD manifestations In our previous study 8 mucosal tags and labial swelling were the most common oral CD findings. However, in the present study mucogingivitis (Figure 1E) was the single most common manifestation. This lesion is particularly difficult for physicians without oral expertise to identify accurately. When a biopsy examination was performed we found areas of mucogingivitis to harbor granulomas commonly, findings that simultaneously support the contention that these particular lesions are genuine disease-specific manifestations of CD and also emphasize their potential contribution toward establishing a diagnosis of CD in an individual patient. Previous studies have pointed to an apparent association between ileocolonic disease and oral CD, 2 4 and in our original retrospective cohort 8 we found that inflammation of the proximal gastrointestinal tract was more common in children with oral CD. However, in the present study, apart from an increased prevalence of oral CD in those with perianal disease, we could not show that those with oral manifestations differed phenotypically from children without oral CD. It is noteworthy that in the present study histologic evidence of inflammation was found very commonly in the stomachs of children with CD, regardless of the presence or absence of oral changes (Table 3). This finding is in keeping with data from a previous retrospective study we published that showed a very high prevalence of inflammation in the gastric mucosa of children with IBD. 16 It has been suggested that oral CD is a Celtic disease 17 and it is possible that the apparent variation in prevalence of oral CD reflects ethnic differences in susceptibility to this extraintestinal manifestation of IBD. In this respect a recent genetic study of Irish and Scottish patients with CD suggests that NOD2/CARD 15 muta-
6 September 2005 ORAL MANIFESTATIONS OF CD 891 tions may be less prevalent than in other Caucasian populations. 18 It would be of interest to characterize NOD2/CARD 15 mutations in patients with oral CD to ascertain if they differ genotypically from those without oral involvement. In summary, we have found that oral manifestations of CD are common in children presenting with IBD and are difficult to discern by gastroenterologists in a conventional clinical setting. These lesions commonly contain granulomas and are accessible easily for diagnostic biopsy examination. Oral examination by an experienced dental surgeon or oral physician can be an important adjunct to the investigation of patients with suspected IBD. References 1. Dudeney TP, Todd IP. Crohn s disease of the mouth. Proc R Soc Med 1969;62: Basu MK, Asquith P. Oral manifestations of inflammatory bowel disease. Clin Gastroenterol 1980;9: Greenstein AJ, Janowitz HD, Sachar DB. The extra-intestinal complications of Crohn s disease and ulcerative colitis: a study of 700 patients. Medicine (Baltimore) 1976;55: Basu M, Asquith P, Thompson RA, et al. Oral manifestations of Crohn s disease. Gut 1975;16: Halme LMJ, Laine P, VonSmitten K. Oral findings in patients with active or inactive Crohn s disease. Oral Surg Oral Med Oral Pathol 1993;76: Boraz RA. Oral manifestations of Crohn disease: update of the literature and report of case. J Dent Child 1988;55: Scully C, Cochran KM, Russell RI, et al. Crohn s disease of the mouth: an indicator of intestinal involvement. Gut 1982;23: Pittock S, Drumm B, Fleming P, et al. The oral cavity in Crohn s disease. J Pediatr 2001;138: Field AE. Oral lesions in IBD. Inflamm Bowel Dis 2001;2: Stricker T, Braegger CP. Oral manifestations of Crohn s disease. N Engl J Med 2000;342: Plauth M, Jenss H, Meyle J. Oral manifestations of Crohn s disease. An analysis of 79 cases. J Clin Gastroenterol 1991;13: Dupuy A, Cosnes J, Revuz J, et al. Oral Crohn disease: clinical characteristics and long-term follow-up of 9 cases. Arch Dermatol 1999;135: Hyams JS. Extraintestinal manifestations of inflammatory bowel disease in children. J Pediatr Gastroenterol Nutr 1994;19: Cosnes A, Dupuy A, Revuz J, et al. Longterm evolution of oral localisation of Crohn s disease. Gastroenterology 1998;114:A Wagtmans MJ, Verspaget HW, Lamers CB, et al. Clinical aspects of Crohn s disease of the upper gastrointestinal tract: a comparison with distal Crohn s disease. Am J Gastroenterol 1997;92: Sharif F, McDermott M, Dillon M, et al. Focally enhanced gastritis in children with Crohn s disease and ulcerative colitis. Am J Gastroenterol 2002;97: Challacombe SJ. Oro-facial granulomatosis and oral Crohns disease: are they specific diseases and do they predict systemic Crohns disease? Oral Dis 1997;3: Bairead E, Harmon DL, Curtis AM, et al. Association of NOD2 with Crohn s disease in a homogenous Irish population. Eur J Hum Genet 2003;11: Address requests for reprints to: Billy Bourke, MD, Children s Research Centre, Our Lady s Hospital for Sick Children, Crumlin, Dublin 12, Ireland. Billy.Bourke@UCD.ie; fax: (353)
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