Original Article
A Comparison of Budesonide with Prednisolone for Active Crohn's Disease
N Engl J Med 1994; 331:842-845September 29, 1994
- Abstract
Background
Patients with active Crohn's disease are often treated with corticosteroids, but the treatment has many side effects. Budesonide is a potent, well-absorbed corticosteroid, but because of a high rate of first-pass metabolism in the liver, its systemic bioavailability is low.
Methods
We conducted a randomized, double-blind, 10-week trial comparing the efficacy and safety of an oral controlled-release form of budesonide with the efficacy and safety of prednisolone in 176 patients with active ileal or ileocecal Crohn's disease (88 patients in each treatment group). The dose of budesonide was 9 mg per day for eight weeks and then 6 mg per day for two weeks. The dose of prednisolone was 40 mg per day for two weeks, after which it was gradually reduced to 5 mg per day during the last week.
Results
At 10 weeks, 53 percent of the patients treated with budesonide were in remission (defined as a score ≤ 150 on the Crohn's disease activity index), as compared with 66 percent of those treated with prednisolone (P = 0.12). The mean score on the Crohn's disease activity index decreased from 275 to 175 in the budesonide group and from 279 to 136 in the prednisolone group (P = 0.001). Corticosteroid-associated side effects were significantly less common in the budesonide group (29 vs. 48 patients, P = 0.003). Two patients in the prednisolone group had serious complications (one had intestinal perforation and one an abdominal-wall fistula). The mean morning plasma cortisol concentration was significantly lower in the prednisolone group than in the budesonide group after 4 weeks (P<0.001) and 8 weeks (P = 0.02) of therapy, but not after 10 weeks.
Conclusions
Among patients with active Crohn's disease, both controlled-release budesonide and prednisolone are effective in inducing remission. In this trial, prednisolone reduced scores on the Crohn's disease activity index more, whereas with budesonide there were fewer glucocorticoid-associated side effects and less suppression of pituitary-adrenal function.
Media in This Article
Figure 1
Mean (+SE) Proportion of Patients with Crohn's Disease in Remission after 2, 4, 8, and 10 Weeks of Treatment with Prednisolone or Budesonide.Figure 2
Mean (±SE) Scores on the Crohn's Disease Activity Index at Base Line and after 2, 4, 8, and 10 Weeks of Treatment with Prednisolone or Budesonide.Article Activity
- Article
Corticosteroids are effective therapy in patients with active Crohn's disease, but they have important systemic side effects. These may occur even during short-term treatment, and some, such as skin striae or cataracts, are irreversible. A variety of corticosteroid analogues that are topically active but systemically much less active than conventional corticosteroids have been developed for the treatment of asthma and rhinitis1. One of these analogues, budesonide, which has a strong affinity for the corticosteroid receptor and is a potent antiinflammatory agent,2 has been used in patients with inflammatory bowel disease. When given orally or rectally, it suppresses inflammation in the bowel. Its systemic bioavailability, however, is low (10 to 15 percent) because it is rapidly metabolized by cytochrome P-450 enzymes in the liver3. When given as an enema, a 2-mg dose of budesonide is as efficacious as a 25-mg dose of prednisolone sodium phosphate for the treatment of patients with active distal ulcerative colitis but causes little or no suppression of pituitary-adrenal function4-6. A controlled-ileal-release formulation of budesonide has been developed to deliver the active drug to the ileal and ileocecal area,7 and in a pilot study budesonide formulated in this way was effective in a small group of patients with active ileal or ileocecal Crohn's disease8. In this study we compared the efficacy and safety of oral controlled-release budesonide with the efficacy and safety of prednisolone in patients with active ileal and ileocecal Crohn's disease.
Methods
Selection of Patients
The study was performed in accordance with the Declaration of Helsinki and was approved by the ethics committees at all centers. All patients gave written or oral informed consent. We studied 176 patients 18 years of age or older who had active Crohn's disease, defined as a score of 200 or higher on the Crohn's disease activity index (described below), that was confined to the ileal or ileocecal region (with or without involvement of the ascending colon) and in whom treatment with an oral corticosteroid alone was judged suitable by the investigator.
Patients were not eligible if they had had an ileostomy or small-bowel resection exceeding 100 cm; had complications including abscesses, perforations, and active fistulas; or had discontinued corticosteroid therapy within the preceding two weeks. Patients with concomitant active peptic ulcer or clinically important hepatic, renal, cardiovascular, or psychiatric conditions were excluded, as were patients considered to be candidates for immediate surgery -- for example, those with known fibrous intestinal strictures.
Study Drugs
The controlled-ileal-release gelatin capsules of budesonide used in the study (Entocort CIR, Astra Draco, Lund, Sweden) contain acid-stable microgranules of budesonide in ethylcellulose and are coated with a layer of methacrylic acid copolymer (Eudragit L100-55) that dissolves at a pH above 5.5. The formulation releases budesonide during passage through the distal part of the ileum and the ascending colon7. In normal subjects, the absorption of budesonide administered in this way ranges from 52 to 79 percent; the mean absorption time is 6.4 hours, and the systemic bioavailability averages 9.3 percent7. Prednisolone was obtained from AS Hydro Pharma (Elverum, Norway). The drugs were provided in blister packages that were turned in by the patient at each clinic visit. Unopened packages were counted to determine compliance. Patients were considered noncompliant if they returned more than 25 percent of the packages unused.
Trial Design
The trial was a randomized, double-blind, double-dummy study performed at 11 centers in Europe. There was separate randomization of patients in blocks of four at each center. The mean duration of treatment was 10 weeks. The study drugs were taken in the morning before breakfast. Patients treated with prednisolone received 40 mg daily for two weeks, 30 mg for two weeks, and 25 mg for two weeks. The daily dose was then decreased by 5 mg each week for the last four weeks. Patients treated with budesonide received 9 mg daily for eight weeks and then 6 mg daily for the last two weeks. All patients received budesonide capsules and prednisolone tablets simultaneously, but in each case one of the pills was an identical-appearing placebo. No medications for Crohn's disease, other than antidiarrheal drugs such as loperamide or diphenoxylate, were allowed.
Disease activity was assessed before treatment and after 2, 4, 8, and 10 weeks with two clinical indexes, the Crohn's disease activity index9 and the Harvey-Bradshaw index,10 and three measures of inflammation: the erythrocyte sedimentation rate and the serum concentrations of C-reactive protein and orosomucoid. The Crohn's disease activity index is based on symptoms and signs, clinical examination, and the hematocrit value, and scores range from 0 (no active disease) to 700 (severe disease). The Harvey-Bradshaw index is a similar index, with scores ranging from 0 to 25. The patients were asked to record on diary cards each day their general well-being, the characteristics and frequency of their stools, and their intake of antidiarrheal drugs. Generally, each patient was examined by the same investigator, who then used the diary results and examination findings to calculate each index. Safety assessments at each visit consisted of the recording of any symptoms, clinical chemical and hematologic measurements, and an examination by the investigator for corticosteroid-associated side effects. Blood samples to measure plasma cortisol were drawn at each visit between 8 and 10 a.m., always at the same time for each patient. The samples were analyzed at Astra Draco by modified high-performance liquid chromatography11. The normal reference range for plasma cortisol was 5.4 to 19.6 μg per deciliter (150 to 540 nmol per liter).
Statistical Analysis
On the basis of data from the National Cooperative Crohn's Disease study,12 the remission rate in the prednisolone group was expected to be 70 percent. We assumed that the remission rate among patients treated with budesonide would be similar. The primary variable in the study was the score on the Crohn's disease activity index after 4, 8, and 10 weeks of treatment. The two groups were compared with respect to the rates of remission (defined as a score of 150 or lower on the Crohn's disease activity index) or success (defined as a score of 150 or lower or a decrease of at least 100 units in the score) at each visit. For all variables assessed, t-tests were used to compare the two treatment groups with respect to the changes from entry. Comparisons of proportions were made by chi-square tests with Yates' correction. The analyses were based on all patients treated. When a patient was lost to follow-up, the last available values were used in the analyses. All statistical tests were two-tailed. P values of 0.05 or below were considered to indicate statistical significance.
Results
The 88 patients assigned to each treatment group were well matched (Table 1Table 1
Base-Line Characteristics of Patients with Active Crohn's Disease Treated with Budesonide or Prednisolone.). Thirty-one patients withdrew from the study (16 in the budesonide group and 15 in the prednisolone group), mostly as a result of therapeutic failure (14 patients in the budesonide group and 9 in the prednisolone group). Two serious adverse events (an intestinal perforation in one patient and an abdominal-wall fistula in another) caused treatment to be discontinued in two patients in the prednisolone group. Other reasons for discontinuation were noncompliance (two patients), drug allergy (one patient), pregnancy (one patient), and erroneous inclusion in the study (two patients). Two patients in each group withdrew before week 2 and are therefore not included in the efficacy analysis. The number of patients studied at the 11 centers ranged from 5 to 44.Clinical Efficacy
After two weeks of treatment, 39 patients (45 percent) in the budesonide group and 48 patients (56 percent) in the prednisolone group were in clinical remission (P = 0.22). The respective figures were 40 percent and 67 percent (P<0.001) at 4 weeks, 52 percent and 65 percent (P = 0.12) at 8 weeks, and 53 percent and 66 percent (P = 0.12) at 10 weeks (Figure 1Figure 1
Mean (+SE) Proportion of Patients with Crohn's Disease in Remission after 2, 4, 8, and 10 Weeks of Treatment with Prednisolone or Budesonide.). The pattern of success rates was similar: 52 patients (60 percent) in the budesonide group and 64 patients (74 percent) in the prednisolone group fulfilled the requirements for treatment success after 10 weeks (P = 0.06). There was no significant difference between centers with respect to remission and success rates.Scores on the Crohn's disease activity index decreased in both groups after two weeks of treatment (Figure 2Figure 2
Mean (±SE) Scores on the Crohn's Disease Activity Index at Base Line and after 2, 4, 8, and 10 Weeks of Treatment with Prednisolone or Budesonide.). The mean decrease in the budesonide group at that time was 101 points, as compared with 130 in the prednisolone group. During the 10-week treatment period, the mean score decreased from 275 to 175 in the budesonide group and from 279 to 136 in the prednisolone group (P = 0.001). Each variable used in the Crohn's disease activity index was also analyzed separately. The patients in the prednisolone group had a greater decrease in the number of liquid or soft stools and a greater increase in body weight and general well-being at most time points. The pattern of changes in the Harvey-Bradshaw index was similar, but the values had a larger coefficient of variation.Indicators of Inflammation
The mean (±SD) erythrocyte sedimentation rates were 27 ±18 and 25 ±18 mm per hour in the budesonide group before the study and after eight weeks, respectively, and 25 ±21 and 17 ±14 mm per hour, respectively, in the prednisolone group. The difference in the changes between the two groups was statistically significant (P = 0.001) only at four weeks. At entry and after eight weeks the respective mean (±SD) serum C-reactive protein concentrations were 25 ±27 and 20 ±23 mg per liter in the budesonide group and 23 ±29 and 15 ±20 mg per liter in the prednisolone group; the difference in the changes was not significant. The mean (±SD) serum orosomucoid concentration decreased slightly in the prednisolone group (from 1.3 ±0.6 to 1.2 ±0.4 g per liter) but not in the budesonide group (1.3 ±0.4 g per liter at both times).
Corticosteroid-Associated Side Effects
Twenty-nine patients (33 percent) in the budesonide group and 48 patients (55 percent) in the prednisolone group had one or more side effects associated with corticosteroid therapy (P = 0.003) during the study. These side effects are summarized in Table 2Table 2
Side Effects of Corticosteroid Therapy in Patients with Active Crohn's Disease before and during Treatment with Budesonide or Prednisolone.. After two weeks of treatment, corticosteroid-associated side effects were identified in 13 patients in the budesonide group and 16 in the prednisolone group. The respective numbers were 16 and 31 patients at 4 weeks, 15 and 34 patients at 8 weeks, and 12 and 30 patients at 10 weeks.The mean base-line plasma cortisol concentrations were 15.0 μg per deciliter (415 nmol per liter) in the budesonide group and 13.5 μg per deciliter (373 nmol per liter) in the prednisolone group. The decrease in plasma cortisol concentrations was significantly greater in the prednisolone group than in the budesonide group after 2 weeks (P<0.001), 4 weeks (P<0.001), and 8 weeks (P = 0.02) of treatment, but not after 10 weeks (P = 0.07) (Figure 3Figure 3
Mean (±SE) Plasma Cortisol Concentrations in Patients with Active Crohn's Disease at Base Line and after 2, 4, 8, and 10 Weeks of Treatment with Prednisolone or Budesonide.). At the end of the study (when the prednisolone dose was 5 mg), the mean value in the prednisolone group was lower than the mean values recorded at any time in the budesonide group. The proportion of patients with plasma cortisol values below 5.4 μg per deciliter (150 nmol per liter) was significantly higher in the prednisolone group at all times (89 percent vs. 37 percent at 2 weeks, P ≤ 0.001; 94 percent vs. 39 percent at 4 weeks, P<0.001; 76 percent vs. 34 percent at 6 weeks, P = 0.001; and 53 percent vs. 29 percent at 10 weeks, P = 0.003).The mean fasting blood glucose concentration increased significantly from 83 to 97 mg per deciliter (4.6 to 5.4 mmol per liter) in the prednisolone group and from 81 to 83 mg per deciliter (4.5 to 4.6 mmol per liter) in the budesonide group (P<0.001) during the 10-week treatment period. Hyperglycemia developed in one patient in the prednisolone group (fasting blood glucose, 271 mg per deciliter [15 mmol per liter]) after four days of treatment. The mean serum creatinine concentration had increased significantly more in the prednisolone group than in the budesonide group at four and eight weeks, and the mean serum potassium concentration had decreased significantly more in the budesonide group at four weeks.
Discussion
We found that a topical intestinal formulation of budesonide was nearly as effective as prednisolone and associated with fewer side effects in patients with active Crohn's disease. Budesonide is particularly suited for topical intestinal therapy because its affinity for the corticosteroid receptor is high (15 times that of prednisolone) and its systemic bioavailability is low. The formulation of budesonide used in this study contains small pellets that leave the stomach reliably,13 and the drug is delivered to the ileocecal region7. The release of budesonide is probably similar in patients with Crohn's disease and normal subjects, since Miller et al. found no significant difference in small-bowel transit time between these two groups regardless of whether the patients with Crohn's disease had had bowel resections14.
In the Canadian placebo-controlled, dose-finding study15 of budesonide in patients with active ileal and ileocecal Crohn's disease, the remission rate in patients treated with 9 mg was 51 percent at eight weeks, similar to the results in this study (52 percent). The remission rate in the placebo group in the Canadian study was 20 percent. In a recent 16-week controlled trial of mesalamine in patients with active Crohn's disease,16 the remission rate was 43 percent in patients treated with 4 g of mesalamine and 18 percent in the placebo group. These results suggest that budesonide is an effective treatment for active Crohn's disease.
In this trial, the mean score on the Crohn's disease activity index decreased more in the prednisolone group than in the budesonide group. The decrease in both groups occurred during the first two weeks of treatment, after which there was little change. Thus, topical therapy is as rapidly effective as systemic therapy. Prednisolone was somewhat more effective in improving systemic well-being and stimulating weight gain. The greater decreases in scores on the Crohn's disease activity index in the prednisolone group have to be weighed against the increased number of corticosteroid-associated side effects and greater suppression of pituitary-adrenal function. Twice as many patients in the prednisolone group as in the budesonide group had corticosteroid-associated side effects. Furthermore, prednisolone had to be discontinued in two patients because of septic complications. The fact that the morning plasma cortisol concentration decreased more in the patients treated with prednisolone is additional evidence that budesonide had a less powerful systemic effect. The importance of the suppression of pituitary-adrenal function during short-term treatment can be questioned, but the recovery of endogenous pituitary-adrenal function in patients treated for long periods is slow, and adrenal insufficiency may occur during the recovery period. The extent to which long-term therapy with budesonide (or larger doses of the drug) may cause pituitary-adrenal suppression is not known.
In conclusion, both controlled-release budesonide and prednisolone are effective in inducing remission in patients with active ileal and ileocecal Crohn's disease. Budesonide therapy is associated with fewer side effects and less suppression of pituitary-adrenal function.
Supported by Astra Draco.
Source Information
From the Department of Gastroenterology, Leuven University Hospital, Leuven, Belgium (P.R.); the Department of Gastroenterology, Huddinge University Hospital, Huddinge, Sweden (R.L.); Akademisches Lehrkrankenhaus der Universitat zu Koln, Leverkusen, Germany (H.M.); the Department of Gastroenterology and Hepatology, University Hospital, Leiden, the Netherlands (C.L.); the Department of Gastroenterology, University Hospital, Linkoping, Sweden (G.O.); the Gastroenterology Unit, Radcliffe Infirmary, Oxford, United Kingdom (D.J.); the Medical Department, University Hospital, Umea, Sweden (A.D.); Medizinische Klinik und Poliklinik der Universitat Essen, Essen, Germany (H.G.); Medical Department C, Herlev University Hospital, Herlev, Denmark (O.O.T.); Stadtisches Krankenhaus Friedrichshafen, Friedrichshafen, Germany (H.L.-M.); Hammersmith Hospital, London (H.H.); and the Departments of Biostatistics and Data Processing (T.P.) and Clinical Research and Development (C.S.), Astra Draco, Lund, Sweden.
Address reprint requests to Dr. Rutgeerts at University Hospital, B-3000 Leuven, Belgium.
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