Original Article
A Controlled Trial of High-Dose Intravenous Immune Globulin Infusions as Treatment for Dermatomyositis
N Engl J Med 1993; 329:1993-2000December 30, 1993
- Abstract
Background
Dermatomyositis is a clinically distinct myopathy characterized by rash and a complement-mediated microangiopathy that results in the destruction of muscle fibers. In some patients the condition becomes resistant to therapy and causes severe physical disabilities.
Methods
We conducted a double-blind, placebo-controlled study of 15 patients (age, 18 to 55 years) with biopsy-proved, treatment-resistant dermatomyositis. The patients continued to receive prednisone (mean daily dose, 25 mg) and were randomly assigned to receive one infusion of immune globulin (2 g per kilogram of body weight) or placebo per month for three months, with the option of crossing over to the alternative therapy for three more months. Clinical response was gauged by assessing muscle strength, neuromuscular symptoms, and changes in the rash. Changes in immune-mediated muscle abnormalities were determined by repeated muscle biopsies.
Results
The eight patients assigned to immune globulin had a significant improvement in scores of muscle strength (P<0.018) and neuromuscular symptoms (P<0.035), whereas the seven patients assigned to placebo did not. With crossovers, a total of 12 patients received immune globulin. Of these, nine with severe disabilities had a major improvement to nearly normal function. Their mean muscle-strength scores increased from 74.5 to 84.7, and their neuromuscular symptoms improved. Two of the other three patients had mild improvement, and one had no change in his condition. Of 11 placebo-treated patients, none had major improvement, 3 had mild improvement, 3 had no change in their condition, and 5 had worsening of their condition. Repeated biopsies in five patients of muscles whose strength improved to almost normal showed an increase in muscle-fiber diameter (P<0.04), an increase in the number and a decrease in the diameter of capillaries (P<0.01), resolution of complement deposits on capillaries, and a reduction in the expression of intercellular adhesion molecule 1 and major-histocompatibility-complex class I antigens.
Conclusions
High-dose intravenous immune globulin is a safe and effective treatment for refractory dermatomyositis.
Media in This Article
Figure 1
Effect of Intravenous Immune Globulin (IVig) in a Placebo-Controlled Crossover Study of 15 Patients with Dermatomyositis.Figure 2
Hands of a Patient with Dermatomyositis before (Panel A) and after (Panel B) Treatment with Intravenous Immune Globulin.Article Activity
- Article
Polymyositis, dermatomyositis, and inclusion-body myositis are distinct groups of inflammatory myopathies, each with characteristic immune-mediated mechanisms1-6. In polymyositis and inclusion-body myositis, sensitized CD8+ cytotoxic T cells recognize heretofore unidentified muscle antigens, leading to phagocytosis and fiber necrosis1,7-9. Dermatomyositis, a clinically distinct entity because of the rash it causes, is characterized by an intramuscular microangiopathy mediated by the complement C5b-9 membranolytic attack complex, leading to loss of capillaries, muscle ischemia, muscle-fiber necrosis, and perifascicular atrophy10-14. In spite of its distinct characteristics, however, dermatomyositis has not been treated separately but as part of the inflammatory-myopathy complex1-6,14,15. Various uncontrolled studies1-3,14,15 have used combinations of prednisone, methotrexate, azathioprine, cyclophosphamide, and cyclosporine as treatment, but in many patients the condition becomes resistant to all therapies, and they remain physically disabled. The need for more efficacious and safe immunotherapy prompted this controlled study of high-dose intravenous immune globulin, a potent immunomodulating agent whose efficacy has been demonstrated in other neuromuscular diseases16,17 as well as in three uncontrolled pilot studies in a total of 10 patients with dermatomyositis18-20.
Methods
Patients
We studied 15 patients (10 women and 5 men), 18 to 55 years of age (mean, 36), selected from patients referred to us because of therapy-resistant dermatomyositis. Eligible patients had active disease characterized by progressive muscle weakness, an impaired ability to perform fully the activities of daily living (ADL), and a rash. All patients had undergone a diagnostic muscle biopsy1-6 immediately before enrollment. The disease had become unresponsive or poorly responsive to high-dose prednisone or therapeutic doses of another immunosuppressant (methotrexate, azathioprine, or cyclophosphamide) given for at least four to six months. Patients with coronary artery disease, IgA deficiency, or kidney dysfunction were excluded, as were bedridden patients and pregnant women. The protocol was approved by the institutional review board, and the patients, who gave their written informed consent, were admitted to the Clinical Center at the National Institutes of Health.
Study Design
The protocol, a double-blind, placebo-controlled design, specified the administration of one infusion of immune globulin or placebo, consisting of dextrose in half-normal saline, per month for three months. The patients were assigned to receive immune globulin or placebo by a block-randomization procedure designed to ensure groups balanced for disease severity. After a washout period of one month, the patients had the option of crossing over to the alternative therapy for another three months. All patients, including those who did not cross over, were followed for up to three months after the completion of their infusions. The code was not broken until all the patients completed the study and a second muscle biopsy was performed. The physicians, nurses, physical therapists, photographer, and statistician were unaware of which treatment was administered. Randomization was performed at the pharmacy, and the bottle of immune globulin or placebo, wrapped in aluminum foil, was then brought to the patient's room. The whole intravenous set was covered by an opaque plastic bag so that any possible fluid turbidity or frothing would not be evident to the investigators or patients. None of the laboratory values were entered into the computer or the patients' charts.
Before the study, each patient had a physical examination and a diagnostic muscle biopsy, and muscle strength was assessed by two neurologists experienced in neuromuscular diseases. Before and after each infusion and monthly thereafter, routine blood chemical values were determined, serum muscle enzymes were measured, a complete blood count was performed, and an immunologic profile, including lymphocyte subgroups and serum immunoglobulin levels, was determined.
The dose of immune globulin was 2 g per kilogram of body weight divided into two doses of 1 g per kilogram each, as described elsewhere21. The doses and kinds of immunosuppressive medication remained unchanged during the study and for two to three months before and after the study. The patients were encouraged to continue their routine daily activities while at home.
Assessment
Response was assessed with the neuromuscular-symptom scale, the ADL scale, a modified Medical Research Council (MRC) scale to measure muscle strength, and photographs of the rash obtained under the same photographic conditions before and after each infusion.
The neuromuscular-symptom score was based on 20 activities that test the function of specific muscle groups: raising the arms over the head, taking off a sweater, opening jars, turning keys, buttoning, climbing stairs, arising from a low chair, lifting the feet, tripping, turning over in bed, moving from a lying to a sitting position, chewing, swallowing, blowing, holding up the head, being tired after minimal exertion, being tired after mild exertion, being tired after prolonged exertion, writing, and putting on shoes or socks. Patients received a score on each activity as follows: 0 (severe impairment), 1 (moderate impairment; done with great difficulty), 2 (mild impairment; done with noticeable difficulty), or 3 (no impairment; done without difficulty). A score of 60 was considered to indicate normal function.
The ADL score was based on the Barthel Index,22 the validity of which has been established for patients with marked physical impairment, and was used only for patients with severe muscle weakness. A score of 100 was considered to be normal.
Standard manual muscle testing was performed on 18 proximal muscle groups: the right and left deltoid, biceps brachii, brachioradialis, triceps brachii, iliopsoas, gluteus maximus, quadriceps femoris, and hamstring muscles, as well as the neck flexors and neck extensors. The responses were rated according to the MRC scale23,24 (in which 0 is the lowest score and 5 the highest), but with a slight modification21. When the patient was able to sustain action against gravity and offered only minor resistance (customarily rated as a score of 4-), he or she was assigned a score of 3.5; when the patient offered more resistance and had a moderate deficit, he or she was assigned a score of 4; and when the muscle was overcome with difficulty and the patient offered major resistance (customarily rated as a score of 4+), he or she was assigned a score of 4.5. The maximal MRC score was 90. Each patient was evaluated throughout the study by the same neurologist.
In our previous study,24 a net increase of one or two grades of strength in at least two muscle groups or of one grade in an involved area of function was considered to indicate improvement, but the result did not differ from that produced by the placebo effect. For this reason, and in view of the high cost of immune globulin, we took a more conservative approach, considering improvement to be major when the total MRC and total neuromuscular-symptom scores increased by five or more grades each and to be mild when they increased by two to four grades each.
Repeated Muscle Biopsies
In five patients who had a major improvement after the third infusion, we performed another open-muscle biopsy on the biceps muscle opposite the one used for the pretreatment biopsy. Before the code was broken, the pretreatment and post-treatment biopsy specimens were processed for histochemical and immunocytochemical analysis of muscle enzymes to determine whether MHC-I (major histocompatibility complex class I), intercellular adhesion molecule 1 (ICAM-1), and Leu-19 (used as a measure of the regeneration of muscle fibers) were expressed and to measure lymphocyte subgroups; monoclonal antibodies were used in an immunoperoxidase technique, as described previously25,26. The capillaries were visualized by immunofluorescence and immunoperoxidase staining with Ulex europaeus lectin, which stains the capillary endothelial cells12. The number of capillaries was counted, and their diameter was measured in five randomly selected perifascicular regions at the low, original (x40) magnification, each region corresponding to a surface area of 6.4 × 104 micrometers2. This approach allowed us to survey the capillaries in a large surface area of the whole muscle specimen. In the same field and the same sections, the total number of muscle fibers was counted, and their size was assessed by measuring the length and width of their cross sections. The ratio of muscle fibers to capillaries was calculated in the same areas and compared not only with that of the pretreatment biopsy specimens but also with that of five biopsy specimens from patients with limb-girdle dystrophies. An investigator who was unaware of the patient's identity did all the counting, using photographs of the immunoperoxidase-stained preparations, where the outlines of the capillaries and muscle fibers were distinct. We also examined the biopsy specimens for deposits of the membranolytic attack complex on the capillaries or muscle fibers with dual immunostaining of the sections with antibodies to the complex followed by fluorescein isothiocyanate-conjugated anti-IgG and biotinylated U. europaeus lectin and then by avidin-rhodamine, using single- and double-exposure techniques, as described previously1,12,26.
Statistical Analysis
Block randomization, based on the initial MRC score, was used to assign the patients to treatment groups. Wilcoxon statistics,27 based on two-tailed P values obtained by normal approximation with continuity corrections, were used to document the efficacy of immune globulin by comparing the base-line MRC and neuromuscular-symptom scores with those attained after the first three months of treatment in each group (immune globulin or placebo). Analysis of variance was used to compare the number and diameter of the capillaries and muscle fibers in the pretreatment and post-treatment biopsy specimens. A P value of less than 0.05 was considered to indicate statistical significance.
Results
Randomized Phase
Of the 15 patients, 8 were randomly assigned to receive immune globulin, and 7 to receive placebo (Table 1Table 1
Response to Intravenous Immune Globulin in a Placebo-Controlled Study of Patients with Dermatomyositis.). The two groups were well balanced with respect to neuromuscular symptoms, duration of disease, immunosuppressive therapy, and serum creatine kinase level. All the patients were taking prednisone (mean daily dose, 25 mg). In the group receiving immune globulin, three patients were also taking azathioprine and two methotrexate. In the placebo group, two patients were also taking azathioprine, and one each was taking methotrexate and cyclophosphamide. The creatine kinase level was elevated in five patients in the immune globulin group (mean, 1076 U per liter) and in four patients in the placebo group (mean, 842 U per liter). Although there was no inadvertent disclosure of treatment assignments, all but one of the patients who showed objective signs of improvement correctly identified the type of treatment they were receiving.After three months of therapy, the eight patients randomly assigned to receive immune globulin (Figure 1Figure 1
Effect of Intravenous Immune Globulin (IVig) in a Placebo-Controlled Crossover Study of 15 Patients with Dermatomyositis.) had a significant improvement in muscle strength (P<0.018) and neuromuscular symptoms (P<0.035), whereas the patients assigned to receive placebo had no change (Table 1). Five patients with severe muscle weakness who were treated with immune globulin had a major improvement: their mean (±SD) MRC score increased by 12 grades (from 75 ±4 to 87 ±3), and their mean neuromuscular-symptom score increased by 14 grades (from 39 ±3 to 53 ±5). These patients had not felt so strong since the onset of their disease two to six years earlier (mean, three). Those using wheelchairs were able to get up from the wheelchair, run, climb stairs, and behave normally. Their ADL scores increased to 100 (normal) from a low of 65. Two other patients treated with immune globulin had a mild improvement, with their mean MRC score increasing by 2.5 grades (from 82 to 84.5) and their neuromuscular-symptom score increasing by 4 grades (from 52 to 56). One patient's condition remained unchanged.The condition of three of the seven patients who received placebo worsened (Figure 1), with their mean MRC score decreasing by 3 grades and their mean neuromuscular-symptom score decreasing by 5 grades. Two patients had no change in their condition, but two others had a mild improvement, with their mean MRC score increasing by 2.5 grades (from 85.5 to 88) and their mean neuromuscular-symptom score by 2.5 grades (from 55 to 57.5)
Crossover Phase
The improvement observed after immune globulin therapy was clearly strengthened by the results obtained when the patients crossed over to the alternative treatment. Four of the eight patients who received immune globulin crossed over to the placebo arm (Figure 1), and their condition either worsened or remained unchanged, although the MRC scores of two reflected a mild placebo effect. The condition of the other four patients, who had a major improvement with immune globulin therapy, worsened after three months without immune globulin; all returned to their base-line condition (two to wheelchairs).
In contrast, four of the seven patients given placebo, who had severe disease, crossed over to immune globulin therapy (Figure 1), and all had a major improvement. Their mean MRC score increased by 9 grades (from 73.6 ±5.8 to 82.5 ±6.0), and their mean neuromuscular-symptom score increased by 11 grades (from 38.2 ±8.8 to 49.0 ±11.0). Their ADL scores increased to 100 from a low of 70.
Summary of Treatment
Overall, of 12 patients treated with immune globulin, 9 had a major improvement in their condition, as demonstrated by an increase in the mean total MRC score from 74.5 ±4.9 to 84.7 ±4.5 and in the mean total neuromuscular-symptom score from 38.6 ±5.9 to 51.0 ±8.0; 2 patients had a mild improvement; and 1 had no change. Of 11 patients given placebo, 3 had a mild improvement in their condition, 3 had no change, and 5 had a worsening.
Clinical Course
The improvement became noticeable about 15 days after the first infusion of immune globulin, but it was clear only after the second infusion, and definite by the third. Maximal improvement occurred by the second infusion in only two of the patients who responded; in all others it occurred between the second and third infusions. Eight patients had marked clearance of the active violaceous rash or the chronic, scaly eruptions on their knuckles (Figure 2Figure 2
Hands of a Patient with Dermatomyositis before (Panel A) and after (Panel B) Treatment with Intravenous Immune Globulin.) preceding or coinciding with the improvement in muscle strength. Serum creatine kinase levels, which were up to 10 times normal in seven of the patients treated with immune globulin, fell by 50 percent after the first infusion and decreased further or normalized by the second infusion. The levels remained elevated, were unchanged, or increased during placebo infusions, and they returned to base line in the patients given immune globulin 6 to 10 weeks after the patients crossed over to placebo therapy or the immune globulin infusions were stopped. Immune globulin had no apparent effect on lymphocyte subgroups.Patients tolerated the immune globulin infusions well. In two patients, severe headache recurred with each infusion, necessitating treatment with narcotics. Both these patients, who had a major improvement in their condition, stated that the benefit from immune globulin far outweighed this adverse effect.
Follow-up
Of the patients who completed the study, including those participating in the crossover phase, seven of the nine who responded sought independently to obtain open-label immune globulin before the code was broken. They believed that the drug was the only therapy that had proved beneficial, without troublesome adverse effects, since the onset of their disease. Six patients who managed to get the drug now require an infusion approximately every six weeks.
Repeated Muscle Biopsies
The repeated biopsies showed that immune globulin therapy markedly improved histologic muscle findings, as shown in Figure 3Figure 3
Randomly Selected Cross Sections of Fresh-Frozen Muscle-Biopsy Specimens from a Patient with Dermatomyositis (Hematoxylin and Eosin, x90).. The mean number of muscle fibers, counted in the five regions mentioned earlier in all five patients, decreased from 34 ±2 before treatment to 25 ±8 after treatment because of a mean increase in muscle-fiber diameter from 54 ±11 micrometers to 71 ±15 micrometers (P<0.04). No endomysial inflammatory infiltrates were noted, except for sparse CD8+ cells in two specimens with the most prominent pretreatment inflammation (data not shown). The regenerating (Leu-19-positive) muscle fibers, prominent before therapy, became sparse (data not shown). The mean number of capillaries increased from 14 ±3 before treatment to 18 ±5 after treatment (normal, 20 ±7), and their mean diameter decreased from 11 ±3 to 7 ±2 (normal, 6 ±0.1) (P<0.01), as exemplified in Figure 4Figure 4
Randomly Selected Cross Sections of Fresh-Frozen Muscle-Biopsy Specimens from a Patient with Advanced Dermatomyositis (x375).. The mean ratio of muscle fibers to capillaries also decreased, from 3.4 to 1.5 (normal, 1.2), and the ratio normalized in three patients.The expression of MHC-I, which had been prominent on the periphery of the fascicles, was barely detectable after treatment (Figure 5AFigure 5
Randomly Selected Cross Sections of Fresh-Frozen Muscle-Biopsy Specimens from a Patient with Dermatomyositis. and Figure 5B). ICAM-1, which had been markedly expressed on the endothelial cells, lymphocytic infiltrates, and occasional perifascicular muscle fibers, was weakly expressed (Figure 5C and Figure 5D), in a pattern resembling that seen in normal muscle28. Deposits of the MAC, which had been prominent on the capillaries and several muscle fibers, were undetectable after treatment in the whole specimens (data not shown).Discussion
Immune globulin is a safe and effective therapy for refractory dermatomyositis, as demonstrated by our findings of major improvement in objective measures of muscle strength and the ability to perform ADL, clearance of the rash, and marked improvement or resolution of the histologic and immunopathological findings on the repeated muscle biopsies. In most patients, the improvement was obvious despite the double-blind study design. The reliability of the results is strengthened by the balanced randomization and double-blind study design; the negative effect in the placebo group; the responses in the crossover phase; the follow-up observations made before the code was broken; the use of strict, conservative, and unbiased criteria to define improvement; the elimination of confounding factors by keeping the doses of immunosuppressive medications unchanged; and the quantitative measurements in the muscle-biopsy specimens.
In adults with dermatomyositis, the earliest and most specific pathologic target is thought to be the capillaries10-12. The process may begin with activation of the classic complement pathway followed by endocapillary deposition of C5b-9 membranolytic attack complex, presumably by antibodies bound to microvascular components11,12,29. This results sequentially in the loss of capillaries, ischemia-induced damage to muscle fibers, necrosis of muscle fibers mediated by the membranolytic attack complex,30 inflammatory infiltrates, regenerating muscle fibers, and eventually, perifascicular atrophy and marked capillary loss, with dilatation of the remaining capillaries1-4,11-14. A T-cell-mediated and MHC-I-restricted cytotoxic process may play an additional part, as suggested by the MHC-I-positive muscle fibers and the CD8+ endomysial lymphocytes12,14. Our findings in the repeated muscle biopsies of patients whose strength improved with immune globulin indicate that all these proposed immunopathologic mechanisms are directly related to the cause and development of muscle weakness. The deposits of the membranolytic attack complex disappeared from the capillaries and necrotic muscle fibers. There was restoration of the capillary network, a reduction in the number of regenerating muscle fibers and lymphocytic infiltrates, an increase in the size of the perifascicular muscle fibers, and reduced expression of MHC-I. How does immune globulin affect these processes?
Among the postulated immunomodulating actions of immune globulin,17,31-33 several are relevant to dermatomyositis. One is the blockade by immune globulin of Fc receptors on the vascular wall. In dermatomyositis, this could prevent the attachment of immune complexes by competition for the Fc receptors of blood vessels between the Fc portion of the complexes and the Fc portion of the IgG present in the preparation of immune globulin. Such a possibility is supported by our finding of abundant IgG deposits around muscle fibers and capillaries in the repeated muscle-biopsy preparations (data not shown). Another action is based on the inhibition by immune globulin of the effector functions of activated T cells and the released cytokines and lymphokines,31,33 or its competition with MHC molecules34. Cytokines induce cell activation, promote cellular expression of ICAM-1 and MHC-I,35 and facilitate the adhesion of lymphocytes to endothelial cells, thereby contributing to the onset and progression of the inflammatory process. In the muscles of patients with dermatomyositis, this process is inhibited after therapy with immune globulin, as evidenced by the suppression of the endomysial inflammation and the decrease in the expression of both ICAM-1 and MHC-I. Finally, supraphysiologic levels of immune globulin neutralize complement neoantigens36 and inhibit the formation of the membranolytic attack complex from the activated C4b and C3b fragments,37 thereby preventing its subsequent binding to target cells. Consequently, the administration of immune globulin to patients with active dermatomyositis can arrest the ongoing complement-dependent immune damage to endothelial cells and the necrosis of muscle fibers mediated by the membranolytic attack complex, as indicated by the disappearance of deposits of membranolytic attack complex in our repeated muscle-biopsy specimens. Furthermore, after treatment, not only did the number of endomysial capillaries increase as a result of neovascularization, but the compensatory dilatation of the microvasculature also decreased.
The efficacy of immune globulin was short-lived (mean duration, six weeks), and repeated treatments were needed for long-term benefit. Even though the patients contended that the gains in their functional capabilities, without concomitant adverse effects, far outweighed the cost of the drug, the high cost of immune globulin may affect its long-term use as maintenance therapy. Immune globulin is safer and better tolerated than corticosteroids or the other immunosuppressive medications and, in spite of the cost, may be considered the first-line drug for use as a steroid-sparing agent. Whether immune globulin is also effective in the treatment of polymyositis and inclusion myositis, as small, open trials have suggested,18-21 is unclear. We are currently conducting a controlled study of immune globulin for the treatment of these conditions.
Supported by a grant (SAF92/0228) from the Comision Interministerial de Ciencia y Technologia (to Dr. Illa).
We are indebted to Dr. Robert Rothlein of Boehringer-Ingelheim Pharmaceuticals for providing anti-ICAM antibodies; to Miles Inc., Pharmaceutical Division, for supplying the immune globulin; to George J. Grimes, Jr., and Judy Sterling, Pharmacy Department, Clinical Center, National Institutes of Health, for their support; to B.J. Hessie for expert editing; and to the nursing staff of the Clinical Center, National Institutes of Health.
Source Information
From the Neuromuscular Diseases Section, Medical Neurology Branch, and the Biometry and Field Studies Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Md.
Address reprint requests to Dr. Dalakas at the Neuromuscular Diseases Section, Bldg. 10, Rm. 4N248, NINDS, NIH, Bethesda, MD 20892.
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