The Natural History of Fistulizing Crohn s Disease in Olmsted County, Minnesota
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1 GASTROENTEROLOGY 2002;122: CLINICAL RESEARCH The Natural History of Fistulizing Crohn s Disease in Olmsted County, Minnesota DAVID A. SCHWARTZ,* EDWARD V. LOFTUS, JR.,* WILLIAM J. TREMAINE,* REMO PANACCIONE, W. SCOTT HARMSEN, ALAN R. ZINSMEISTER, and WILLIAM J. SANDBORN* *Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, Minnesota; University of Calgary, Calgary, Alberta, Canada; and Section of Biostatistics, Mayo Clinic, Rochester, Minnesota Background & Aims: Little is known about the cumulative incidence and natural history of fistulas in Crohn s disease in the community. Methods: The medical records of all Olmsted County, Minnesota residents who were diagnosed with Crohn s disease from 1970 to 1993 and who developed a fistula were abstracted for clinical features and outcomes. Six patients denied research authorization. The cumulative incidence of fistula from time of diagnosis was estimated by using the Kaplan Meier product-limit method. Results: At least 1 fistula occurred in 59 patients (35%), including 33 patients (20%) who developed perianal fistulas. Twenty-six (46%) developed a fistula before or at the time of formal diagnosis. Assuming that the 9 patients with fistula before Crohn s disease diagnosis were instead simultaneous diagnoses, the cumulative risk of any fistula was 33% after 10 years and was 50% after 20 years (perianal, 21% after 10 years and 26% after 20 years). At least 1 recurrent fistula occurred in 20 patients (34%). Most fistulizing episodes (83%) required operations, most of which were minor. However, 11 perianal fistulizing episodes (23%) resulted in bowel resection. Conclusions: Fistulas in Crohn s disease were common in the community. In contrast to referral-based studies, only 34% of patients developed recurrent fistulas. Surgical treatment was frequently required. There is considerable variation in the disease pattern and severity of Crohn s disease. Subgroups of patients with Crohn s disease may have predominantly perforating (fistulizing), fibrostenotic (stricturing), or nonperforating and nonstricturing (inflammatory) disease. 1 3 The presence of fistulas in patients with Crohn s disease may result in distressing symptoms, such as rectal pain; persistent drainage from the perianal region, vagina, or abdominal wall; or recurrent urinary tract infections. Because of the morbidity associated with fistulizing Crohn s disease, patients and physicians fear this clinical presentation. Despite the obvious importance of this condition, little is known about the incidence and natural history of fistulizing Crohn s disease. The lifetime risk for developing a fistula in patients with Crohn s disease is reported 4 6 to be between 20% and 40%, and the natural history is reported to be one of exacerbation and long episodes of actively draining fistulas. 7,8 These cumulative incidence figures and natural history studies, which come from referral-center cohorts, may not accurately reflect the clinical course of the typical Crohn s disease patient with fistulas in the community. The only population-based study 7 of fistulizing Crohn s disease examined the natural history of Crohn s disease perianal fistulas among residents of Stockholm County, Sweden, during the years of The cumulative incidence of anal fistulas was reported to be 23% in this population. Fistulas at other sites were not reported, and information on the natural history of the fistula episodes was limited. We sought to determine the natural history of fistulizing Crohn s disease in a population by examining the clinical course of those patients who developed fistulizing disease in a previously identified Crohn s disease inception cohort. 8 Materials and Methods Setting Olmsted County is located in southeastern Minnesota and was composed of approximately 106,000 residents in Rochester, the county s urban center, had a population of approximately 71,000 in The remainder of the county is rural. In 1990, 96% of the population of Olmsted County was white. Although 25% of the county residents are employed in health care services (vs. 8% nationwide) and the level Abbreviation used in this paper: CI, confidence interval by the American Gastroenterological Association /02/$35.00 doi: /gast
2 876 SCHWARTZ ET AL. GASTROENTEROLOGY Vol. 122, No. 4 of education is higher (30% have completed college vs. 21% nationwide), the residents of Olmsted County are socioeconomically similar to the white population in the United States. 9 Rochester Epidemiology Project The Rochester Epidemiology Project is a unique medical records linkage system that exploits the unique health care delivery system in Olmsted County. Virtually all the health care of the county residents is provided by 2 organizations: the Mayo Medical Center, consisting of the Mayo Clinic and its 2 affiliated hospitals, and Olmsted Medical Center, consisting of a multispecialty group and its affiliated hospital. 9,10 In any 3-year period, more than 90% of the county residents are examined at 1 of the 2 organizations. 9 Diagnoses generated from all outpatient visits, emergency room visits, hospitalizations, nursing home visits, surgical procedures, autopsy examinations, and death certificates are recorded in a central diagnostic index. Therefore, it is possible to identify all cases of a disease for which patients sought medical attention. 9,10 This unique resource has resulted in more than a thousand publications describing the epidemiology and natural history of many different diseases. 11 Case Ascertainment The institutional review boards of Mayo Medical Center and Olmsted Medical Center approved the study. One hundred seventy-five residents of Olmsted County were diagnosed with Crohn s disease from 1970 to 1993, and 169 patients gave permission to have their records reviewed. The complete (inpatient and outpatient) medical records of all 169 potential cases were reviewed, and the diagnosis of Crohn s disease was reconfirmed by using previously defined criteria. 8,12 Medical records were reviewed until December 31, 1995, for development of fistula. A diagnosis of a fistulizing episode was made if there was radiographic, endoscopic, surgical, or clinical evidence of a fistula. For example, the diagnosis of perianal fistulas is often based on physical examination findings and might not be confirmed by additional testing, whereas the diagnosis of enteroenteric fistulas is made either radiologically or at the time of surgery. For purposes of the data analysis, patients who were diagnosed with fistula before Crohn s disease diagnosis were assumed to have developed their first fistula on the day after diagnosis. Data Abstraction The medical records of patients with fistulas were abstracted through the date of last follow-up or November 1999 for demographic information, date of diagnosis of Crohn s disease, extent of involvement, dates of fistulizing episodes, sites of fistulas, dates of hospitalizations, and medical or surgical therapy for fistulas. Statistical Analysis The data were summarized with percentages, medians, and ranges. The cumulative risk of fistulas (both overall and perianal alone) in the entire inception cohort of Crohn s disease was estimated with the Kaplan Meier product-limit method. Patients were followed up from the time of diagnosis of Crohn s disease until development of the first fistula, date of last follow-up, or December 31, Ninetyfive percent confidence intervals (95% CI) for the cumulative risk of fistulas at 1, 5, 10, and 20 years were estimated with Greenwood s formula. The association of surgical fistula treatment with perianal vs. nonperianal fistula was examined in 2 ways that yielded similar results. In one approach, the first fistula in each patient was analyzed by using a 2 test for association. Including all fistulas, a generalized estimating equations logistic regression model was used to account for the multiple fistulas within some patients. The association between potential risk factors and the development of a fistula at least 30 days after Crohn s disease diagnosis was investigated by using a Cox proportional hazards regression model, in which the time to first fistula from 30 days to 2 years after diagnosis was the dependent variable. Potential risk factors studied included age at Crohn s disease diagnosis, sex, and disease extent at diagnosis. Results Demographic Characteristics At least 1 fistula episode occurred between January 1, 1970, and December 31, 1995, in 59 patients (35% of the entire cohort) diagnosed with Crohn s disease from 1970 to At least 1 perianal fistula occurred in 33 patients (20% of the cohort). Thirty-two patients with fistulas were women (54%), resulting in a female to male ratio of 1.2:1; this is identical to the sex ratio in the members of the Crohn s disease cohort who did not develop a fistula. The median age at diagnosis of Crohn s disease was 27.7 years (range, 9 to 83 years), similar to a median age at diagnosis of 28.3 years (range, 8 to 84 years) in the nonfistulizing patients. Twelve patients (20%) developed a fistula at least 30 days before the diagnosis of Crohn s disease, and 17 patients (29%) were diagnosed with a fistula within 30 days of the Crohn s diagnosis. In the remaining 30 patients with fistulas (51%), the median time from diagnosis of Crohn s disease to the first fistula was 5.5 years (range, 37 days to 20.3 years). Ileal Crohn s disease was present in 11 patients (19%), 35 patients (59%) had ileocolonic involvement, and disease confined to the colon was noted in 13 patients (22%). The extent of disease in the 110 patients without fistulas was ileal in 21 (19%), ileocolonic in 44 (40%), and colonic in 45 (41%). Development of a fistula was associated with extent of disease at diagnosis (P 0.03), with a greater proportion of those with ileocolonic extent ever developing a fistula. A proportional hazards regression model in patients who had not developed a fistula before or within 30 days of
3 April 2002 NATURAL HISTORY OF CROHN S FISTULAS 877 Figure 1. Cumulative incidence of overall fistulas (solid line) and perianal fistulas (dashed line) among 176 Olmsted County, Minnesota residents diagnosed with Crohn s disease from 1970 to Crohn s disease diagnosis suggested that the ileocolonic extent of Crohn s (relative to ileal only) was associated with development of a fistula between 31 days and 2 years after diagnosis (hazard ratio, 2.7), but this was not statistically significant (95% CI, ). A significant association was not detected for sex or age at diagnosis, although this analysis had limited power to detect associations. Cumulative Incidence of Fistulas The cumulative incidence of fistulas overall in the Crohn s disease inception cohort, with follow-up until December 31, 1995, is depicted in Figure 1. The cumulative risk of at least 1 fistula (any site) after 1 year was 21% (95% CI, 14% to 27%), after 5 years was 26% (95% CI, 19% to 32%), after 10 years was 33% (95% CI, 25% to 40%), and after 20 years was 50% (95% CI, 35% to 61%) (Figure 1). The cumulative risk of at least 1 perianal fistula after 1 year was 12% (95% CI, 7% to 17%), after 5 years was 15% (95% CI, 9% to 20%), after 10 years was 21% (95% CI, 14% to 28%), and after 20 years was 26% (95% CI, 16% to 36%) (Figure 1). Fistula Characteristics (All Fistulas) There were 88 fistulizing episodes in the 59 patients (Figure 2A). Thirty-nine patients (66%) had only 1 fistulizing episode. In the remaining patients, 13 (22%) experienced 2 fistulizing episodes, and 7 (12%) had 3 fistulizing episodes. Forty-eight fistulizing episodes (55%) were caused by perianal fistulas. Twenty-one fistulizing episodes (24%) were from enteroenteric fistulas. The remaining fistulizing episodes comprised 8 rectovaginal fistulas (9%), 5 enterocutaneous fistulas (6%), 3 enterovesical fistulas (3%), and 3 entero-intra-abdominal fistulas (3%) (Figure 3). Figure 2. (A) Number of Crohn s disease patients with 1, 2, or 2 fistulizing episodes (any fistula). (B) Number of Crohn s disease patients with 1, 2, or 2 fistulizing episodes (perianal fistula). Perianal Fistula Characteristics At least 1 perianal fistula occurred in 33 patients (21%). The median age at diagnosis of Crohn s disease in this group was 26.9 years (range, 8.8 to 82.9 years). Fifteen patients (45%) had developed a perianal fistula before, or at the time of, the diagnosis of Crohn s disease. In the remaining 18 patients, the median interval be- Figure 3. Percentage of fistulas by type (perianal, enteroenteric, rectovaginal, and other).
4 878 SCHWARTZ ET AL. GASTROENTEROLOGY Vol. 122, No. 4 Nine patients (15%) were placed on maintenance therapy with agents reported to be active for fistulizing disease (AZA, 6-MP, methotrexate, or anti tumor necrosis factor agents). All of these patients had follow-up longer than 6 months (median, 3.6 years; range, 0.6 to 5.8 years). Only 1 patient placed on maintenance therapy (11%) developed a recurrent fistula. Figure 4. Flowchart showing the natural history of perianal fistulizing Crohn s disease in 33 patients. tween diagnosis and first perianal fistula was 4.8 years (range, 8 days to 18.7 years). There were 48 perianal fistulizing episodes in the 33 patients (Figure 2B). Twenty-two (67%) had only 1 fistulizing episode, 8 (24%) experienced 2 fistulizing episodes, and 3 (9%) had 3 fistulizing episodes. Treatment and Outcomes Seventy-two of 88 (82%) fistulizing episodes were treated surgically; however, the proportion of perianal fistulas treated surgically was lower than that of nonperianal fistulas. On the basis of the 59 first fistulizing episodes, the surgical rates were 71% and 93%, respectively (P 0.03, 2 ). Including all 88 episodes among the 59 patients, the surgical rates were 71% and 95%, respectively (P 0.01, generalized estimating equations logistic regression). Among the 34 perianal fistulizing episodes treated surgically, 11 (32%) required major surgery, including proctocolectomy with ileostomy (n 7), segmental resection of proximal disease (n 3), or proctectomy with sigmoid colostomy (n 1) (Figure 4). The median time to fistula closure in the entire cohort, including both medically and surgically treated fistulas, was 14.2 weeks (range, 1 day to 429 weeks). Among the 15 fistulizing episodes that were treated with medical therapy alone, the median time to fistula closure was 14.1 weeks (range, 1.4 to 429 weeks). In the 20 patients who had at least 1 recurrent fistula, the median time between fistulizing episodes was 2.8 years (range, 14 days to 13.4 years). Medications used specifically to treat fistulas included antibiotics in 38 episodes (44%), sulfasalazine or 5-aminosalicylates in 32 (37%), steroids in 32 (38%), purine analogs (azathioprine [AZA] or 6-mercaptopurine [6-MP]) in 9 (10%), cyclosporine in 1 (1%), anti tumor necrosis factor agents in 2 (2%), and methotrexate in 1 (1%). Discussion The cumulative incidence of fistulizing Crohn s disease in this population-based cohort was 33% after 10 years and 50% after 20 years. The only other populationbased study of fistulizing Crohn s disease 7 found the incidence of fistulas to be only 23%. However, this study focused exclusively on perianal fistulas. When the subgroup of our patients who developed perianal fistulas was examined separately, the cumulative incidence (26% after 20 years) was remarkably similar to that reported by Hellers et al. 7 (23%). The incidence of fistulizing disease in this study was also similar to that reported in other referral-center series. 4 6 Previously, the natural history of fistulizing Crohn s disease was reported to be one of frequent relapses and long episodes of actively draining fistulas. For example, in a study of 90 patients treated with surgery, medical therapy, or both at a German referral center, 42 patients (47%) developed recurrent fistulas. The median time to reactivation was 3.8 months. The risk of recurrent fistula activity was 48% at 1 year and 59% at 2 years. 13 Similarly, in a recent controlled trial of infliximab for fistulizing Crohn s disease, the median duration of fistula closure in infliximab-treated patients was 12 weeks. 13 Other investigators have also noted an increased rate of recurrent disease, delayed healing, or both associated with fistulizing Crohn s disease In contrast, most of the patients (66%) in our population-based cohort had only 1 fistulizing episode. Moreover, many of the patients who developed a recurrent fistula did so at least 2 years after their initial fistula closed. These differences in outcomes may be caused by the inherent tendency of referral-center cohorts to be biased toward patients with a more severe disease presentation when compared with population-based cohorts. Our study was a true population-based study, with inclusion of nearly 100% of cases from within a defined geographic area. Many of our patients (44%) developed a fistula at or before the time of their diagnosis of Crohn s disease, similar to the fraction of patients (45%) who developed perianal fistulas at least 6 months before the diagnosis of Crohn s disease reported in the population-based study from Stockholm County. 7 This observation can be attrib-
5 April 2002 NATURAL HISTORY OF CROHN S FISTULAS 879 uted to a number of factors. First, it has been estimated that approximately 5% of patients with Crohn s disease will present with isolated perianal disease. 18 Unless a clinician suspects Crohn s disease as a possible cause for a fistula or abscess, the process is considered to be secondary to a simple fistula in ano. In our series, 15 patients (45%) developed a perianal fistula at or before the formal diagnosis of Crohn s disease. Second, a large percentage of patients who present initially with obstructive symptoms and undergo operation will be found to have an enteroenteric fistula associated with an area of stricturing. Thus, the diagnoses of Crohn s disease and the fistula are made simultaneously. In general, fistulas rarely heal without treatment. In the past, the primary treatment of these fistulas was antibiotics, 19 surgery, or both. 15,20 23 The high surgery rate (83%) and the fact that the most commonly prescribed medication for these patients was an antibiotic reflects this historical treatment approach. However, during the last decade, there has been an increasing use of immunosuppressive agents (i.e., AZA, 6-MP, and cyclosporine) for the treatment indication of fistula closure More recently, a randomized, double-blind, placebo-controlled trial showed that infliximab, a monoclonal antibody to tumor necrosis factor, is effective for fistula closure. 28 The low percentage of patients in our population treated with these medications can be explained by the fact that most of the patients in this cohort developed a fistula before the widespread use of immunosuppressive medications for fistulizing disease. (The incidence cohort included only patients who were diagnosed with Crohn s disease from 1970 to 1993.) This may also explain why so many patients were treated with 5-aminosalicylates and corticosteroids medications now widely believed to be ineffective for fistulizing disease. The optimal therapy for fistulas (primary medical therapy, primary surgical therapy, or combination medical and surgical therapy) is unclear. This is particularly true for patients with perianal fistulas for which nonresective procedures, such as incision and drainage of perianal abscesses, fistulectomy, and placement of draining setons, may be used. It is interesting to note that only 1 of the 9 patients who were placed on maintenance therapy with an immunosuppressive agent active in fistulizing disease developed a recurrent fistula. This is significantly less than the recurrence rate observed in the other patients in our population (19 of 50; 38%). However, the number of patients is too small to determine whether these agents protect against recurrent fistulas. In conclusion, fistulas occurred in up to 35% of patients with Crohn s disease (perianal fistulas occurred in 20% of patients). Recurrent fistulas were uncommon; 66% of patients had only 1 fistula episode, 22% had 2 episodes, and only 12% had 3 or more episodes. The majority of fistulas were treated surgically (83% overall, 72% in patients with perianal fistulas). Studies that evaluate the optimal induction and maintenance therapy for fistulas (primary medical therapy, primary surgical therapy, or combination medical and surgical therapy) are needed. References 1. Greenstein AJ, Lachman P, Sachar DB, Springhorn J, Heimann T, Janowitz HD, Aufses AH. Perforating and non-perforating indications for repeated operations in Crohn s disease: evidence for two clinical forms. Gut 1988;29: Gasche C, Scholmerich J, Brynskov J, D Haens G, Hanauer SB, Irvine EJ, Jewell DP, Rachmilewitz D, Sachar DB, Sandborn WJ, Sutherland LR. 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Crohn s disease in Olmsted County, Minnesota, : incidence, prevalence and survival. Gastroenterology 1998;114: Melton LJ III. History of the Rochester Epidemiology Project. Mayo Clin Proc 1996;71: Kurland LT, Molgaard CA. The patient record in epidemiology. Sci Am 1981;245: Melton LJ III. The threat to medical-records research. N Engl J Med 1997;337: Panaccione R, Sandborn WJ, Loftus EV, Tremaine WJ, Harmsen WS, Zinsmeister AR. Phenotypic classification of Crohn s disease patients in Olmsted County, Minnesota: application of the Vienna classification (abstr). Gastroenterology 1999;116:A Makowiec F, Jehle EC, Starlinger M. Clinical course of perianal fistulas in Crohn s disease. Gut 1995;37: Halme L, Sainio AP. Factors related to frequency, type, and outcome of anal fistulas in Crohn s disease. Dis Colon Rectum 1995;38: Williamson PR, Hellinger MD, Larach SW, Ferrara A. Twenty-year review of the surgical management of perianal Crohn s disease. Dis Colon Rectum 1995;38: Marks CG, Ritchie JK, Lockhart-Mummery HE. Anal fistulas in Crohn s disease. Br J Surg 1981;68: Williams JG, Rothenberger DA, Nemer FD, Goldberg SM. Fistulain-ano in Crohn s disease. Results of aggressive surgical treatment. Dis Colon Rectum 1991;34:
6 880 SCHWARTZ ET AL. GASTROENTEROLOGY Vol. 122, No Lockhart-Mummery HE. Crohn s disease: anal lesions. Dis Colon Rectum 1975;18: Bernstein LH, Frank MS, Brandt LJ, Boley SJ. Healing of perineal Crohn s disease with metronidazole (letter). Gastroenterology 1980;79: Pescatori M, Interisano A, Basso L, Arcana F, Buffatti P, Di Bella F, Doldi A, Forcheri V, Gaetini R, Pera A. Management of perianal Crohn s disease. Results of a multicenter study in Italy. Dis Colon Rectum 1995;38: Sangwan YP, Schoetz DJ Jr, Murray JJ, Roberts PL, Coller JA. Perianal Crohn s disease. Results of local surgical treatment. Dis Colon Rectum 1996;39: Wolff BG, Beahrs OH. Preservation of the anorectum. Adv Surg 1984;18: Nordgren S, Fasth S, Hulten L. Anal fistulas in Crohn s disease: incidence and outcome of surgical treatment. Int J Colorectal Dis 1992;7: Present DH, Korelitz BI, Wisch N, Glass JL, Sachar DB, Pasternack BS. Treatment of Crohn s disease with 6-mercaptopurine. A long-term, randomized, double-blind study. N Engl J Med 1980; 302: Hinterleitner TA, Petritsch W, Aichbichler B, Fickert P, Ranner G, Krejs GJ. Combination of cyclosporine, azathioprine and prednisolone for perianal fistulas in Crohn s disease. Z Gastroenterol 1997;35: Egan LJ, Sandborn WJ, Tremaine WJ. Clinical outcome following treatment of refractory inflammatory and fistulizing Crohn s disease with intravenous cyclosporine. Am J Gastroenterol 1998; 93: Lowry PW, Weaver AL, Tremaine WJ, Sandborn WJ. Combination therapy with oral tacrolimus (FK506) and azathioprine or 6-mercaptopurine for treatment-refractory Crohn s disease perianal fistulae. Inflamm Bowel Dis 1999;5: Present DH, Rutgeerts P, Targan S, Hanauer SB, Mayer L, van Hogezand RA, Podolsky DK, Sands BE, Braakman T, De Woody KL, Schaible TF, van Deventer SJ. Infliximab for the treatment of fistulas in patients with Crohn s disease. N Engl J Med 1999; 340: Received July 11, Accepted December 13, Address requests for reprints to: Edward V. Loftus, Jr., M.D., Division of Gastroenterology and Hepatology, Mayo Clinic, 200 First Street, S.W., Rochester, Minnesota Fax: (507) Supported by Schering-Plough and grant AR30582 from the National Institutes of Health, and the Mayo Foundation for Medical Education and Research. Presented in part at the 101st Annual Meeting of the American Gastroenterological Association, San Diego, California, May 21 24, 2000 (Gastroenterology 2000;118:A337). Participation in educational events indirectly sponsored by Schering- Plough: Drs. Panaccione and Sandborn; consultant for Schering- Plough: Drs. Loftus and Sandborn.
Percent Cumulative. Probability. Penetrating. Inflammatory. Stricturing. Months Patients at risk N =
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