Original Article
A Short-Term Study of Chimeric Monoclonal Antibody cA2 to Tumor Necrosis Factor α for Crohn's Disease
N Engl J Med 1997; 337:1029-1036October 9, 1997
- Abstract
Background
Studies in animals and an open-label trial have suggested a role for antibodies to tumor necrosis factor α, specifically chimeric monoclonal antibody cA2, in the treatment of Crohn's disease.
Methods
We conducted a 12-week multicenter, double-blind, placebo-controlled trial of cA2 in 108 patients with moderate-to-severe Crohn's disease that was resistant to treatment. All had scores on the Crohn's Disease Activity Index between 220 and 400 (scores can range from 0 to about 600, with higher scores indicating more severe illness). Patients were randomly assigned to receive a single two-hour intravenous infusion of either placebo or cA2 in a dose of 5 mg per kilogram of body weight, 10 mg per kilogram, or 20 mg per kilogram. Clinical response, the primary end point, was defined as a reduction of 70 or more points in the score on the Crohn's Disease Activity Index at four weeks that was not accompanied by a change in any concomitant medications.
Results
At four weeks, 81 percent of the patients given 5 mg of cA2 per kilogram (22 of 27 patients), 50 percent of those given 10 mg of cA2 per kilogram (14 of 28), and 64 percent of those given 20 mg of cA2 per kilogram (18 of 28) had had a clinical response, as compared with 17 percent of patients in the placebo group (4 of 24) (P<0.001 for the comparison of the cA2 group as a whole with placebo). Thirty-three percent of the patients given cA2 went into remission (defined as a score below 150 on the Crohn's Disease Activity Index), as compared with 4 percent of the patients given placebo (P = 0.005). At 12 weeks, 41 percent of the cA2-treated patients (34 of 83) had had a clinical response, as compared with 12 percent of the patients in the placebo group (3 of 25) (P = 0.008). The rates of adverse effects were similar in the groups.
Conclusions
A single infusion of cA2 was an effective short-term treatment in many patients with moderate-to-severe, treatment-resistant Crohn's disease.
Media in This Article
Figure 1
Rates of Clinical Response and Remission after a Single Infusion of cA2 or Placebo.Table 1
Base-Line Characteristics of the 108 Patients.Article Activity
- Article
Crohn's disease is a chronic inflammatory disorder characterized by patchy granulomatous inflammation of any part of the gastrointestinal tract.1 Patients have a spectrum of clinical features, with great variation in the course of the disease. Mesalamine is considered first-line therapy. The majority of patients have relapses requiring glucocorticoid treatment.2 Immunomodulatory agents, including azathioprine or mercaptopurine,3 methotrexate,4,5 and cyclosporine,6-9 may be used to treat severe, persistent disease that is refractory to treatment with corticosteroids, or symptoms that recur on tapering of the dose of corticosteroids.
In animal models, antibodies to tumor necrosis factor α (anti–TNF-α) prevent or reduce inflammation,10-14 suggesting that therapy with such antibodies may be useful for disorders in which chronic inflammation may be due to an increase in cytokines produced by the T helper 1 subclass of T cells. In vitro studies have shown that the production of TNF-α is increased in the mucosa of patients with Crohn's disease15,16 and that the mucosal inflammatory process reflects a shift in the balance of cytokine production by T cells toward the T helper 1 subclass.17,18 Similar findings were reported in the synovia of patients with rheumatoid arthritis,19 and anti–TNF-α reduces clinical signs and symptoms of this disease.20,21 The role of TNF-α in the pathogenesis of Crohn's disease and the successful use of anti–TNF-α in the treatment of rheumatoid arthritis stimulated an open-label trial of chimeric monoclonal antibody cA2 (infliximab, Centocor, Malvern, Pa.) for Crohn's disease. In that preliminary trial, clinical remission occurred after one infusion of cA2 in eight of nine patients with Crohn's disease.22 We report the results of a multicenter randomized, placebo-controlled, double-blind trial of cA2 for the treatment of active Crohn's disease.
Methods
Patients
To be eligible for the study, patients had to have had Crohn's disease for six months,1 with scores on the Crohn's Disease Activity Index23 between 220 and 400. The Crohn's Disease Activity Index incorporates eight variables related to the disease: the number of liquid or very soft stools, the severity of abdominal pain or cramping, general well-being, the presence of extraintestinal manifestations, abdominal mass, use of antidiarrheal drugs, hematocrit, and body weight. These items yield a composite score ranging from 0 to approximately 600. Higher scores indicate greater disease activity. Scores below 150 indicate remission, whereas scores above 450 indicate severe illness. Patients were eligible for the study if they had been receiving any of the following: mesalamine for eight or more weeks, with the dose remaining stable during the four weeks before screening; a maximum of 40 mg of corticosteroids per day for eight or more weeks, with the dose remaining stable during the two weeks before screening; and mercaptopurine or azathioprine for six or more months, with the dose remaining stable during the eight weeks before screening. Patients were excluded from the study if they had received treatment with cyclosporine, methotrexate, or experimental agents within three months before screening. Patients were also excluded if they met any of the following criteria: symptomatic stenosis or ileal strictures; proctocolectomy or total colectomy; stoma; a history of allergy to murine proteins; prior treatment with murine, chimeric, or humanized monoclonal antibodies; or treatment with parenteral corticosteroids or corticotropin within four weeks before screening.
Patients were enrolled at 18 centers in North America and Europe. The protocol was approved by the institutional review boards and ethics committees at all sites, and all patients gave written informed consent before enrolling in the trial. The study began on June 21, 1995, and concluded on March 12, 1996. A total of 203 patients were screened for the study, 95 of whom were excluded. The most common reasons for exclusion were a requirement for contraindicated medications, refusal to give informed consent, or disease activity that did not meet the study criteria.
Protocol
Subjects were screened one week before the administration of cA2 to establish base-line scores on the Crohn's Disease Activity Index and the Inflammatory Bowel Disease Questionnaire,24 and base-line C-reactive protein concentrations. The Inflammatory Bowel Disease Questionnaire, a 32-item questionnaire, evaluates quality of life with respect to bowel function (e.g., loose stools and abdominal pain), systemic symptoms (fatigue and altered sleep pattern), social function (work attendance and the need to cancel social events), and emotional status (angry, depressed, or irritable). The score ranges from 32 to 224, with higher scores indicating a better quality of life. Patients in remission usually score between 170 and 190.24
Patients were randomly assigned to receive a single dose of either placebo or 5 mg of cA2 per kilogram of body weight, 10 mg of cA2 per kilogram, or 20 mg of cA2 per kilogram in an intravenous infusion, administered over a two-hour period. The cA2 monoclonal antibody is a chimeric mouse–human IgG1 that binds to both soluble25 and transmembrane26 human TNF-α with high affinity and specificity. It neutralizes the functional activity of TNF in a variety of bioassays by blocking the binding of the factor to the p55 and p75 receptors.27 The placebo preparation contained 0.1 percent human serum albumin instead of cA2 and was identical in appearance to the cA2 solution. Patients were enrolled from June 21, 1995, to October 31, 1995. Randomization was performed centrally by an independent organization (PPD Pharmaco, Austin, Tex.). The cA2 and placebo solutions were prepared by a pharmacist at each site who was aware of the treatment assignments. The investigators, all other study personnel, and the patients were blinded to the treatment assignments.
The primary end point was defined before the initiation of the trial as a reduction of 70 points or more in the score on the Crohn's Disease Activity Index at the four-week evaluation that was not accompanied by a change in any concomitant medications. Patients who did not have a clinical response at that time were enrolled in a parallel, open-label study and received a single infusion of 10 mg of cA2 per kilogram and were followed for 12 additional weeks. Patients who were receiving mesalamine, corticosteroids, azathioprine, or mercaptopurine before the study continued to receive a stable dose during the trial period. The dose of corticosteroids could be tapered beginning eight weeks after the initiation of the study. Treatment with these drugs or with methotrexate or cyclosporine could not be initiated during the trial. After all patients had completed 12 weeks of the trial and the data were finalized, the treatment assignments were revealed.
Immunologic Investigations
Serum samples were obtained at base line and at 12 weeks for the evaluation of antinuclear antibodies and human anti-cA2. Antinuclear antibodies were detected by immunofluorescence on Hep-2 cells. Serum samples positive by immunofluorescence for antinuclear antibodies were tested for antibodies to double-stranded DNA by an enzyme-linked immunosorbent assay (North American centers) or by Crithidia immunofluorescence (European centers). Human anti-cA2 was measured by a double-antigen enzyme-linked immunosorbent assay.
Statistical Analysis
An adaptive stratified design was used to assign patients to a treatment group, with investigational site and corticosteroid use as the strata. We calculated that approximately 25 patients were needed in each treatment group to detect a difference in the number of patients who responded with 80 percent power (α = 0.05), assuming a response rate of 30 percent in the placebo group, 80 percent in the cA2 group with the greatest response, and 55 percent in the remaining cA2 groups. The original study protocol did not specify the use of intention-to-treat analysis. Two patients were assigned to a treatment but did not receive it: one declined to participate and one did not meet eligibility criteria. No further data were collected on these two patients, and they are not included in the analysis. Otherwise, all patients were analyzed according to the treatment to which they were assigned. When we assessed the response or remission rates in all evaluation periods after the initial blinded infusion, patients who received an open-label infusion or those with a change in concomitantly administered medications were considered to have had no response.
Categorical variables (clinical response and remission) were compared with use of the Mantel–Haenszel chi-square test for general association stratified according to investigational site.28 Analyses comparing each of the cA2 treatment groups with placebo were performed only when the treatment effect was considered significant (P<0.05). The changes from base line in continuous variables (Crohn's Disease Activity Index score, Inflammatory Bowel Disease Questionnaire score, and C-reactive protein concentration) were compared with use of analysis of variance, with the van der Waerden normal scores blocked according to center.29 If the treatment effect was significant, the cA2 treatment groups were compared with the placebo group with linear contrasts. All P values are two-sided.
Results
Base-Line Characteristics of the Study Patients
A total of 108 patients were studied, with 25 to 28 patients in each group. There were no significant differences in age, weight, race (all patients were white), sex, duration of disease, scores on the Crohn's Disease Activity Index and Inflammatory Bowel Disease Questionnaire, or C-reactive protein concentrations at base line among the groups, although patients in the placebo group had a lower mean concentration of C-reactive protein (Table 1Table 1
Base-Line Characteristics of the 108 Patients.). Significantly more patients had ileal disease alone in the placebo group than in the other three groups (P = 0.02), but there were no significant differences in the number who had undergone previous segmental resections among the groups. Similar numbers of patients in each group had been treated with oral corticosteroids, mercaptopurine, azathioprine, and oral mesalamine at base line. All treatment groups had a mean score on the Crohn's Disease Activity Index of approximately 300, despite concurrent treatment with drugs other than cA2; thus, the patients had moderate-to-severe, treatment-resistant Crohn's disease.Clinical Response and Remission
Week 2
Figure 1AFigure 1
Rates of Clinical Response and Remission after a Single Infusion of cA2 or Placebo. demonstrates that clinical response was achieved early: 61 percent of cA2-treated patients had a clinical response by week 2, as compared with 17 percent of patients in the placebo group (P< 0.001). At two weeks, 27 percent of cA2-treated patients were in clinical remission (defined as a score of less than 150 on the Crohn's Disease Activity Index), as compared to 4 percent of the patients in the placebo group (P = 0.06) (Figure 1B).Week 4
Four weeks after the infusion, the primary end point of a reduction of 70 or more points in the score on the Crohn's Disease Activity Index was reached in 81 percent of those given 5 mg of cA2 per kilogram (22 of 27 patients), 50 percent of those given 10 mg of cA2 per kilogram (14 of 28 patients), and 64 percent of those given 20 mg of cA2 per kilogram (18 of 28 patients), as compared with 17 percent of those given placebo (4 of 24 patients) (Figure 1A). The overall response of the cA2 groups was 65 percent (P<0.001 for the comparison with placebo). No dose–response relation was seen during this period. At four weeks, 33 percent of the cA2-treated group were in remission, as compared with 4 percent of the placebo group (P = 0.005). Thus approximately half of the patients who had a clinical response at either two or four weeks also entered remission. Consistent treatment effects were observed when the analyses for both response and remission at week 4 were stratified according to the location of disease or concurrent drug regimens (data not shown).
Changes in Clinical and Inflammatory Measures during the First Four Weeks
The mean change in the scores on the Crohn's Disease Activity Index in the cA2-treated group as a whole was significant at weeks 2 and 4 of the trial, as compared with the changes in scores in the placebo group (P<0.001) (Table 2Table 2
Measures of Clinical Response and Inflammation at Base Line and Weeks 2 and 4.). The mean decrease in the score on the Crohn's Disease Activity Index in the cA2 group as a whole was 110 at four weeks, as compared with 13 in the placebo group. Most of this decrease had occurred by week 2, with a mean decrease of 103 in the cA2 group and 16 in the placebo group.The Inflammatory Bowel Disease Questionnaire was given at base line and four weeks. There was a mean increase of 46, 30, and 32 in the groups treated with cA2 at 5, 10, and 20 mg of cA2 per kilogram, respectively, yielding a mean increase of 36 in the cA2 group as a whole, as compared with a mean increase of 5 in the placebo group (P = 0.001) (Table 2).
Concentrations of C-reactive protein were measured at base line and weeks 2 and 4. At four weeks, the mean decrease in C-reactive protein was 16.3, 11.1, and 15.0 mg per liter in the groups treated with 5, 10, and 20 mg of cA2 per kilogram, respectively, yielding a mean decrease of 14.3 mg per liter in the group as a whole, as compared with a mean increase of 2.0 mg per liter in the placebo group (P<0.001). The maximal reduction in C-reactive protein occurred within the first two weeks. At two weeks, the mean decrease in C-reactive protein in the cA2 groups as a whole was 16.0 mg per liter, as compared with a mean increase of 3.9 mg per liter in the placebo group (P<0.001).
Week 12
The differences in the rates of clinical response between the cA2-treated groups and the placebo group remained significant through the 12 weeks of follow-up: it was 48 percent in the group given 5 mg of cA2 per kilogram (13 of 27 patients), 29 percent in the group given 10 mg of cA2 per kilogram (8 of 28 patients), and 46 percent in the group given 20 mg of cA2 per kilogram (13 of 28 patients), for an overall rate of response of 41 percent (34 of 83 patients), as compared with a rate of 12 percent in the placebo group (3 of 25 patients) (P = 0.008). The difference in the percentage of patients who were in remission was not significant at 12 weeks: 30 percent of the group given 5 mg of cA2 per kilogram (8 of 27 patients), 18 percent of the group given 10 mg of cA2 per kilogram (5 of 28 patients), and 25 percent of the group given 20 mg of cA2 per kilogram (7 of 28 patients), for an overall rate of remission achieved of 24 percent (20 of 83 patients), as compared with a rate of 8 percent in the placebo group (2 of 25 patients) (P = 0.31).
Characterization of the Response to Treatment
The magnitude and duration of response were characterized through the 12-week follow-up period in the 54 patients who responded to a single infusion of cA2. The improvement in the scores on the Crohn's Disease Activity Index (clinical remission was defined as a score below 150) and Inflammatory Bowel Disease Questionnaire (remission was defined as a score between 170 and 190) in patients with a response was maintained. The mean (±SD) score on the Crohn's Disease Activity Index was 318±52 at base line, 144±67 at week 4, 151±86 at week 8, and 182±91 at week 12, and the mean score on the Inflammatory Bowel Disease Questionnaire was 121±26 at base line, 175±26 at week 4, 165±36 at week 8, and 162±35 at week 12. Concentrations of C-reactive protein (normal, <8 mg per liter) began to rise at 12 weeks, potentially indicating a relapse of disease (from 25.8±2.7 mg per liter at base line to 7.5±1.5 mg per liter at week 4, 11.0±2.1 mg per liter at week 8, and 14.1±2.2 mg per liter at week 12).
Effects of Open-Label cA2 in Patients with No Response Four Weeks after the Initial Infusion of cA2
Patients who did not have a clinical response after the first infusion were given a second infusion of open-label cA2 in a dose of 10 mg per kilogram and followed for an additional 12 weeks. Among 19 patients who initially received placebo, the response rate was 58 percent and the remission rate was 47 percent four weeks after the second infusion — rates that were similar to those in the initial, blinded study (Figure 1). By contrast, among the 29 patients who had no response to the initial cA2 infusion, the rates of response and remission after the second infusion were 34 percent (P = 0.14 for the comparison with the patients who received placebo initially) and 17 percent (P = 0.05), respectively, confirming that this group was less responsive to cA2.
Adverse Effects
Adverse effects were recorded at the time of infusion and 2, 4, 8, and 12 weeks after the infusion. In patients who received an open-label infusion 4 weeks after an infusion of placebo or cA2, adverse effects were monitored for an additional 12 weeks. As shown in Table 3Table 3
Adverse Effects., the percentages of patients with adverse effects were similar in the placebo and cA2 groups. Of the 29 patients who received two cA2 infusions, 2 had a reaction (chest pain, dyspnea, or nausea) that led to the discontinuation of the infusion. These reactions resolved spontaneously within minutes after the infusion was discontinued. In addition, complications requiring hospitalization developed in two patients (abdominal abscess in one patient in the placebo group and salmonella colitis in one patient given an infusion of 20 mg of cA2 per kilogram). Both patients were treated successfully. A bowel obstruction occurred in one patient given cA2, and a flare of Crohn's disease occurred in another.Immunologic Responses
Serum samples were screened for antibodies to double-stranded DNA at base line and at 12 weeks in 98 patients who received cA2 (in either a blinded or an open-label infusion); all patients were negative for these antibodies at base line, and 3 were positive at 12 weeks. Serum samples from 101 patients treated with cA2 (in either a blinded or an open-label infusion) were also tested for human anti-cA2; 6 patients tested positive. In two thirds of the patients, however, cA2 was still detectable in serum samples taken at 12 weeks, and this may have interfered with the assay.
Discussion
Many of our patients with moderate-to-severe Crohn's disease that was resistant to treatment had a rapid response to cA2. Other treatments for such patients have not had beneficial effects over the long term and may not be well tolerated.30-33 Our short-term study suggests that anti–TNF-α therapy with cA2 may represent a new treatment option for patients with moderate-to-severe Crohn's disease. Further studies will be necessary to determine the long-term efficacy of a single infusion of cA2 as well as the efficacy and safety of repeated treatments.
The mechanisms of the chronic mucosal inflammatory processes manifesting as Crohn's disease are not clear. However, our results add strength to the suggestion that TNF-α may have a central role in the inflammatory process in at least two thirds of the patients with Crohn's disease.22 Studies in rodent models have provided insight into the role of anti–TNF-α in the pathogenesis of Crohn's disease. Studies involving the transfer of CD45RBhigh cells to mice with severe combined immunodeficiency have shown that these cells can induce a chronic, transmural inflammatory process in the colon.34 Powrie et al. have demonstrated that this colitis can be reversed or ameliorated by the use of agents, including anti–TNF-α, capable of down-regulating the production of the T helper 1 subclass of T cells.10 These cells produce proinflammatory cytokines including interferon-γ, interleukin-2, and potentially, TNF. A mechanistic role for TNF-α in intestinal inflammation has been suggested on the basis of these studies.
Other studies involving animal models have shown that cytokines produced by the T helper 1 subclass are expressed in the mucosa of people with Crohn's disease.17,18 Anti–TNF-α may participate in the down-regulation of mucosal inflammation in this disease by inhibiting the T helper 1 population of active T cells. Extensive follow-up studies are needed to determine how the elimination of TNF affects mucosal inflammation after treatment with anti–TNF-α.
In this study, a clinical response or remission occurred in 65 percent of patients with severe Crohn's disease after a single infusion of cA2. Furthermore, results in the open-label retreatment phase corroborated the finding that patients with no response to the first infusion of cA2 were less likely to have a response to a second infusion. Thus, this group of patients may differ from those that responded. The similarities among the patients, including age, duration of disease, types of concomitant treatment, and disease activity at base line, suggest that any differences are more likely to be detected subclinically. There was no apparent dose–response relation between a dose of 5 mg of cA2 per kilogram and a dose of 20 mg per kilogram with respect to either the magnitude or the duration of the clinical response. In a previous open-label trial of cA2 doses of 1 mg, 5 mg, 10 mg, and 20 mg per kilogram, the group receiving 1 mg of cA2 per kilogram had a more transient response than the groups given the higher doses.35 This transient response was similar to that in a small trial of a different anti–TNF-α antibody.36 The results of these trials support the use of a dose of 5 mg of cA2 per kilogram in future trials.
In summary, we found that a single infusion of cA2 was an effective short-term treatment for patients with moderate-to-severe Crohn's disease that was resistant to treatment.
Supported by Centocor, Inc., and by a grant (FD-R-001276) from the Food and Drug Administration Orphan Products Development Division. Drs. Hanauer, van Deventer, Present, and Rutgeerts have received honorariums from Centocor for lectures.
Source Information
From the Cedars–Sinai Medical Center, Los Angeles (S.R.T.); the University of Chicago, Chicago (S.B.H.); Academisch Medisch Centrum, Amsterdam (S.J.H.D.); Mt. Sinai Medical Center, New York (L.M., D.H.P.); Centocor, Inc., Malvern, Pa. (T.B., K.L.D., T.F.S.); and Academisch Ziekenhuis Gasthuisberg, Leuven, Belgium (P.J.R.).
Address reprint requests to Dr. Targan at Cedars–Sinai Medical Center, Division of Gastroenterology and Inflammatory Bowel Disease Center D4063, 8700 Beverly Blvd., Los Angeles, CA 90048.
Appendix
The Crohn's Disease cA2 Study Group consists of the following centers and investigators (the number of patients enrolled at each center is given in parentheses): Massachusetts General Hospital, Boston (5 patients): D. Podolsky, B.E. Sands, M.T. Marcucci; Cedars–Sinai Medical Center, Los Angeles (20 patients): S.R. Targan, E.A. Vasiliauskas, B. Voigt, J. Gaiennie; University of Chicago Hospitals and Clinics, Chicago (11 patients): S.B. Hanauer; University of Alabama School of Medicine, Birmingham (2 patients): C.O. Elson, R.P. McCabe, Jr.; Mount Sinai Medical Center, New York (8 patients): L. Mayer, D.H. Present, C. Stamaty; Washington University School of Medicine, St. Louis (2 patients): W.F. Stenson, J.J. O'Brien; Virginia Mason Medical Center, Seattle (5 patients): R. Kozarek, M. Gelfand; Hospital of the University of Pennsylvania, Philadelphia (4 patients): D. Bachwich, G. Lichtenstein, L. Hurd; McMaster University Medical Center, Hamilton, Ont., Canada (2 patients): E.J. Irvine, S. Collins; Lahey Clinic, Burlington, Mass. (3 patients): A.S. Warner, L.J. Costa; University of North Carolina, Chapel Hill (5 patients): K.L. Isaacs; University of Maryland Medical System, Baltimore (5 patients): S. James, B. Greenwald, M.L. Mullen; University of Kentucky, Lexington (5 patients): G.W. Varilek, B. Vivian; Academisch Ziekenhuis Leiden, Leiden, the Netherlands (4 patients): R.A. van Hogezand, M.J. Wagtmans; Institute for Clinical Immunology and Rheumatology, Erlangen, Germany (1 patient): H. Schönekäs, J.R. Kalden, J.M.L. Bauer; University of Amsterdam, Amsterdam (9 patients): S.J.H. van Deventer, C.M.J. Kothe, O.J.B. de Smit; Leeds General Infirmary, Leeds, United Kingdom (4 patients): D.M. Chalmers, S. Chitturi, D. Todi; and Academisch Ziekenhuis Gasthuisberg, Leuven, Belgium (13 patients): P.J. Rutgeerts, G.R.A.M. D'Haens, A.F.M. Verstraeten.
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S. Cohen, S.M. Stemmer, G. Zozulya, A. Ochaion, R. Patoka, F. Barer, S. Bar-Yehuda, L. Rath-Wolfson, K.A. Jacobson, P. Fishman. (2011) CF102 an A3 adenosine receptor agonist mediates anti-tumor and anti-inflammatory effects in the liver. Journal of Cellular Physiology 226:9, 2438-2447
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Chureen T. Carter, Heidi C. Waters, Daniel B. Smith. (2011) Impact of infliximab adherence on Crohn’s disease-related healthcare utilization and inpatient costs. Advances in Therapy 28:8, 671-683
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A. Kumar, M. Auron, A. Aneja, F. Mohr, A. Jain, B. Shen. (2011) Inflammatory Bowel Disease: Perioperative Pharmacological Considerations. Mayo Clinic Proceedings 86:8, 748-757
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James Buchanan, Sarah Wordsworth, Tariq Ahmad, Angela Perrin, Severine Vermeire, Miquel Sans, Jenny Taylor, Derek Jewell. (2011) Managing the long term care of inflammatory bowel disease patients: The cost to European health care providers. Journal of Crohn's and Colitis 5:4, 301-316
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Michael B. Sprakes, P. John Hamlin, Lisa Warren, Dan Greer, Alexander C. Ford. (2011) Adalimumab as second line anti-tumour necrosis factor alpha therapy for Crohn's disease: A single centre experience. Journal of Crohn's and Colitis 5:4, 324-331
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M.Chaparro, P. Martínez-Montiel, M. Van Domselaar, F. Bermejo, J.L. Pérez-Calle, B. Casis, A. López-San Román, A. Algaba, J. Maté, J.P. Gisbert. (2011) Intensification of infliximab therapy in Crohn's disease: Efficacy and safety. Journal of Crohn's and Colitis
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S. G. Veerappan, C. A. O’Morain, J. S. Daly, B. M. Ryan. (2011) Review article: the effects of antitumour necrosis factor-α on bone metabolism in inflammatory bowel disease. Alimentary Pharmacology & Therapeutics 33:12, 1261-1272
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W. B. Gaertner, R. D. Madoff, M. P. Spencer, A. Mellgren, S. M. Goldberg, A. C. Lowry. (2011) Results of combined medical and surgical treatment of recto-vaginal fistula in Crohn’s disease. Colorectal Disease 13:6, 678-683
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S. Danese, J.-F. Colombel, W. Reinisch, P. J. Rutgeerts. (2011) Review article: infliximab for Crohn’s disease treatment - shifting therapeutic strategies after 10 years of clinical experience. Alimentary Pharmacology & Therapeutics 33:8, 857-869
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Alexander C Ford, William J Sandborn, Khurram J Khan, Stephen B Hanauer, Nicholas J Talley, Paul Moayyedi. (2011) Efficacy of Biological Therapies in Inflammatory Bowel Disease: Systematic Review and Meta-Analysis. The American Journal of Gastroenterology 106:4, 644-659
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M. Aguiar, N. Marçal, A.C. Mendes, A. Bugalho de Almeida. (2011) Infliximab no tratamento da sarcoidose - Experiência de um hospital central. Revista Portuguesa de Pneumologia 17:2, 85-93
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