Original Article
Interferon Alfa-2a Therapy for Life-Threatening Hemangiomas of Infancy
N Engl J Med 1992; 326:1456-1463May 28, 1992
- Abstract
- Abstract
Background and Methods.
Most hemangiomas are small, harmless birthmarks that appear soon after birth, proliferate for 8 to 18 months, and then slowly regress over the next 5 to 8 years, leaving normal or slightly blemished skin. In rare cases, hemangiomas can endanger vital structures, with a mortality of up to 60 percent. About a third of these life-threatening hemangiomas respond to treatment with corticosteroids, but for the others there is no safe and effective treatment. We evaluated the effects of daily subcutaneous injections of interferon alfa-2a (up to 3 million units per square meter of body-surface area) in 20 neonates and infants with life-threatening or vision-threatening hemangiomas that failed to respond to corticosteroid therapy.
Results.
In 18 of the 20 patients the hemangiomas regressed by 50 percent or more after an average of 7.8 months of treatment (range, 2 to 13). One infant died of refractory proliferation of a lesion and consumptive coagulopathy. The condition of three other patients who had large hemangiomas associated with consumptive coagulopathies that were unresponsive to conventional therapies stabilized after seven days of treatment with interferon alfa-2a alone. Transient side effects of treatment with interferon alfa-2a included fever, neutropenia (one patient), and skin necrosis (one patient). No long-term toxicity has been observed after a mean follow-up of 16 months.
Conclusions.
Interferon alfa-2a appears to induce the early regression of life-threatening corticosteroid-resistant hemangiomas of infancy. (N Engl J Med 1992;326: 1456–63.)
Media in This Article
Figure 1
Changes in Fibrinogen Levels, Partial-Thromboplastin Times, and Platelet Counts in Response to Various Treatments.Figure 2
Large Hemangioma of the Posterior Thorax in Patient 3 at Birth (Panel A); at 2 Weeks of Age, When the Lesion Was Growing Rapidly (Panel B); after 1 Month of Treatment with Interferon Alfa, at Which Time There Was Visible Regression (Panel C); and at 1 Year of Age, after 11 Months of Treatment, at Which Time Involution Was Nearly Complete (Panel D).Article Activity
- Article
HEMANGIOMA of infancy is an angiomatous disorder characterized by the proliferation of capillary endothelium, with multilamination of the basement membrane1 , 2 and the accumulation of mast cells, fibroblasts, and macrophages.3 , 4 In this angiogenic disease, the abnormal growth of capillaries results in tissue damage, sometimes with fatal consequences.5
Hemangioma is the most common tumor of infancy, occurring in 10 to 12 percent of whites6 and in up to 22 percent of preterm babies weighing less than 1000 g.7 Hemangioma has a female-to-male preponderance of 3 to 1.8 , 9 Hemangiomas most commonly appear in the skin, usually as a single tumor, although multiple cutaneous lesions also occur, often with involvement of other organ systems (generalized hemangiomatosis). Rarely is a cutaneous hemangioma fully grown at birth. The tumor usually appears during the first few weeks of life, manifested by an erythematous macule, a blanched spot, or localized telangiectasia.10 The natural history of hemangioma is characterized by rapid postnatal growth for 8 to 18 months (proliferative phase), followed by very slow but inevitable regression for the next 5 to 8 years (involutive phase).8 , 11 12 13 14 There is complete resolution of hemangiomas in over 50 percent of children by the age of 5 years and in over 70 percent by the age of 7 years, with continued improvement in the remaining children until the age of 10 to 12 years.8 , 11 12 13 The rate of regression is not related to the sex or age of the infant, the duration of the proliferative phase, or the site, size, or appearance of the hemangioma.8 , 9 , 12
Most hemangiomas are small, harmless birthmarks that involute to leave either normal or slightly blemished skin. Even a small hemangioma, however, can obstruct the airway or impair vision. A large hemangioma in the liver or an extensive cutaneous hemangioma can divert a considerable volume of blood through the extensive labyrinth of capillaries and produce high-output heart failure.15 , 16 The increased capillary endothelial surface that characterizes a giant hemangioma can also trap platelets and may cause a thrombocytopenic coagulopathy (Kasabach—Merritt syndrome).17 "Alarming hemangioma" is a term introduced by Enjolras and her coworkers to categorize the lesions that impair vital structures or cause life-endangering complications.18
High-dose corticosteroids are the primary means of controlling hemangioma pharmacologically. The rate of response to the systemic or intralesional administration of corticosteroids is 30 to 60 percent.19 20 21 Enjolras et al. report a variable response to corticosteroids in infants with life-threatening hemangiomas: the response was excellent in 30 percent, doubtful in 40 percent, and absent in 30 percent.18 The mortality rate can be as high as 54 percent for life-threatening visceral or hepatic hemangiomatosis22 and may be 30 to 40 percent with platelet-consumptive coagulopathy despite the administration of steroids.23
Interferon alfa-2a was developed as an antiviral agent. In the course of clinical trials in patients with the acquired immunodeficiency syndrome, an unexpected finding was that therapy with interferon alfa-2a improved Kaposi's sarcoma, the vascular tumor associated with human immunodeficiency virus (HIV) infection.24 25 26 27 White and colleagues observed remarkable regression of pulmonary hemangiomatosis in a seven-year-old boy after interferon alfa-2a therapy.28 Orchard et al. reported two cases of hemangioma in infants with thrombocytopenic coagulopathy, one in the pterygopalatine space and the other in the peritoneum. Both tumors regressed after the administration of interferon alfa-2a.29 White et al. also described two infants with life-threatening hemangiomas treated with interferon alfa-2a: one responded, but the other child died after less than two months of treatment.30
The anecdotal reports of encouraging clinical results, the observation that interferon inhibits the locomotion of capillary endothelium in vitro,31 and the finding that interferon alfa-2a inhibits angiogenesis in mice32 led us to examine the effectiveness of a recombinant form of the drug in the treatment of 20 patients with life-threatening or vision-threatening hemangiomas of infancy or childhood who had not responded to corticosteroid therapy.
Methods
Patients
This study involved 20 infants and children with life-endangering or vision-threatening hemangiomas, defined as lesions that invaded or obstructed vital organs or tissues, such as the airway, oropharynx, ear, orbit or adnexa, retroperitoneum, and viscera (i.e., the gastrointestinal tract, lungs, heart, or liver). Congestive heart failure and marked thrombocytopenia, complications of large hemangiomas, were also urgent indications for the institution of interferon therapy. To be eligible for the study, infants had to have a life-threatening or vision-threatening hemangioma that failed to respond to a two-week course of corticosteroid therapy (2 mg per kilogram of body weight per day). The study was approved by the institutional review board of Children's Hospital in Boston, and informed consent was obtained from the parents or guardians of all patients. No patients who met these entry criteria were excluded.
Study Medication
Recombinant human interferon alfa-2a (specific activity, 3 million units per 0.5 ml) was supplied as a sterile solution for injection by Dr. Judith Prestifillipo of Hoffmann—LaRoche, Nutley, New Jersey. Each patient received a daily subcutaneous injection of up to 3 million units per square meter of body-surface area, which was given in combination with other drugs as needed.
Monitoring for Efficacy
Premature regression was defined as an obvious decrease of 50 percent or more in the dimensions of the hemangioma that was sustained for at least six months during treatment or after the withdrawal of the medication. Growth was considered to have stabilized if the dimensions of the lesion did not increase within six months after the initiation of treatment. The size or extent of visceral lesions was monitored by ultrasonography, CT scanning, or magnetic resonance imaging. The course of the infants who had coagulopathy associated with the Kasabach—Merritt syndrome was monitored by measuring the platelet count, fibrinogen level, prothrombin time, and partial-thromboplastin time. Treatment was considered to have failed if the dimensions of the lesion increased by 50 percent or thrombocytopenia persisted, blood loss continued, or the patient died. During a 24-month period, a total of 20 patients were entered into the protocol for interferon-alfa therapy. The age at the onset of treatment ranged from 3 weeks to 2 years; the duration of treatment ranged from 1 to 13 months. There were 16 girls and 4 boys. Ten patients had destructive cervicofacial lesions or obstruction of the airway. Three patients had periorbital lesions that compromised vision. Four patients had thrombocytopenic coagulopathy and anemia associated with large cutaneous retroperitoneal lesions. Three infants had visceral lesions, involving primarily the liver in one, the right atrial appendage in one, and the brain in one.
Monitoring for Potential Toxicity
A complete blood count and tests of hepatic and renal function were performed monthly. The levels of neutralizing anti—interferon alfa-2a antibodies were measured if the initial response to therapy was followed by rebound growth during continued treatment with interferon alfa-2a.
Results
Characteristics of the Study Population
Among the 20 neonates, infants, and young children referred for treatment of life-threatening hemangiomas, the tumors regressed by 50 percent or more in 18 patients after an average of 7.8 months of treatment (range, 2 to 13). In two infants, stabilization of the tumor was followed by a gradual improvement in their condition. One infant died despite all therapeutic attempts, including low-dose radiation, corticosteroids, four weeks of interferon alfa-2a, and vigorous supportive care.
Case Reports
Hemangiomas Associated with Thrombocytopenic Coagulopathy (Kasabach—Merritt Syndrome)
Patient 1 presented with a rapidly growing hemangioma of the neck, thrombocytopenia, and consumptive coagulopathy (Table 1Table 1
Patients' Characteristics and Outcome of Interferon Alfa-2a Treatment.). Despite treatment with high-dose systemic corticosteroids, platelet and cryoprecipitate transfusions, and low-dose heparin, the coagulopathy failed to improve and the hemangioma continued to proliferate. Treatment with interferon alfa-2a, gamma irradiation, chemotherapy, transfusion, and supportive care were all ineffective, and the infant died at the age of three months. Histologic analysis of the lesion revealed numerous mitoses and a spindle-cell pattern reminiscent of Kaposi's sarcoma.Patient 2, a child with a giant hemangioma of the thigh and the Kasabach—Merritt syndrome (Fig. 1Figure 1
Changes in Fibrinogen Levels, Partial-Thromboplastin Times, and Platelet Counts in Response to Various Treatments.), had only a transient response to treatment with prednisone, concentrated platelet transfusions, and cryoprecipitate infusion, and no response to low-dose heparin; the hemangioma continued to grow. After five days of interferon alfa-2a therapy, the coagulopathy resolved and the platelet count increased to 20×103 per cubic millimeter, with no evidence of bleeding. After 32 weeks of the drug, the platelet count was 100×103 per cubic millimeter, fibrinogen levels and prothrombin time were normal, and there was a 50 percent reduction in the size of the lesion. However, two weeks after the treatment was discontinued, the lesion began to grow again, and the platelet count fell to 6×103 per cubic millimeter. Interferon treatment was reinstated, and after three days, the platelet count increased to 150×103 per cubic millimeter and there was further regression of the lesion (Fig. 1). Interferon therapy was continued until the diameter of the lesion had diminished to less than 5 cm, since the Kasabach—Merritt syndrome has not been reported in lesions smaller than this.Patient 3 (Fig. 2AFigure 2
Large Hemangioma of the Posterior Thorax in Patient 3 at Birth (Panel A); at 2 Weeks of Age, When the Lesion Was Growing Rapidly (Panel B); after 1 Month of Treatment with Interferon Alfa, at Which Time There Was Visible Regression (Panel C); and at 1 Year of Age, after 11 Months of Treatment, at Which Time Involution Was Nearly Complete (Panel D).) presented at birth with a raised hemangioma of the posterior thorax, which enlarged rapidly over the next two weeks (Fig. 2B). The ecchymotic appearance of the lesion was typical of the Kasabach—Merritt syndrome. The lesion was refractory to two weeks of corticosteroids and conventional therapy. After one week of treatment with interferon alfa-2a, the coagulopathy stabilized, and after four weeks of treatment there was visible regression of the hemangioma (Fig. 2C). After 11 months of treatment there was no evidence of coagulopathy, and the tumor had almost disappeared (Fig. 2nd).Patient 4 presented with a rapidly growing lesion that was similar in distribution to the hemangioma shown in Figure 2. Associated coagulopathy was noted at the age of six weeks and failed to respond to conventional therapies. An improvement in the coagulopathy was observed after 10 days of treatment with interferon alfa-2a alone. After six months of treatment there was 95 percent regression of the lesion, and treatment was stopped. At the most recent follow-up, the child was free of symptoms, with no recurrence of the lesion or the coagulopathy.
Cervicofacial Hemangioma
Airway lesions. Ten infants had a compromised airway as a result of intraluminal or extraluminal obstruction by a hemangioma of the head, neck, or mediastinum. The patients in this group tended either to present in the first months of life with rapidly enlarging lesions or to present after nine months of age with large hemangiomas.
Patient 6 presented at two years of age with a giant cervicofacial hemangioma (Table 1, Fig. 3AFigure 3
A Large, Right-Sided Cervicofacial Hemangioma Causing 90 Percent Occlusion of the Airway and Necessitating Tracheostomy in Patient 6 at the Age of Two Years.), which continued to enlarge despite treatment with a high dose of corticosteroids. The child required tracheostomy, oxygen, and treatment with a cardiac inotropic agent (digoxin) and thiazide diuretics. After 13 months of treatment with interferon, her hemifacial hemangioma had regressed (Fig. 3B). The degree of tracheal occlusion (as measured in a cross-sectional area) improved from 90 percent before interferon treatment to 5 percent after treatment. After 15 months of treatment the child no longer required oxygen or digoxin, and the tracheostomy was removed.Periorbital hemangioma. Three infants presented with orbital or adnexal lesions resulting in exophthalmos and in some cases compromised vision (Table 1). Patient 15 had an unusual course in that at the age of two years there was still active growth of hemangioma in the upper and lower eyelids, despite multiple intralesional injections of corticosteroid. After one year of treatment with interferon alfa-2a, the upperlid tumor responded more than the lower-lid tumor. Histologic examination of hemangioma after resection of the lower eyelid confirmed the persistence of endothelial hyperplasia. The other infants who presented with eyelid hemangiomas responded well to treatment with interferon alfa-2a, initiated at the ages of five and six months.
Other hemangiomas. Three patients had visceral hemangioma, two of whom also had lesions on the skin (Table 1). Patient 18 presented at birth in heart failure with a bloody pericardial effusion caused by a large hemangioma of the right atrial appendage. There was no response to two weeks of prednisone therapy; therefore, treatment with interferon was begun at the age of three weeks. The response of the cardiac lesion was documented by magnetic resonance imaging (Fig. 4AFigure 4
Magnetic Resonance Images of the Sagittal Plane of the Chest of Patient 18, Who Was Born in Congestive Heart Failure Caused by a Hemangioma of the Right Atrial Appendage (Asterisk) below the Thymus (T).); there was complete resolution after six months of therapy (Fig. 4B). Myriad tiny skin lesions were also present, and they too regressed with treatment. At the most recent follow-up, five months after treatment with interferon was stopped, there was no evidence of new growth.Patient 19 presented shortly after birth with high-output congestive heart failure due to hemangioma of the liver (Fig. 5AFigure 5
Longitudinal Sonograms of the Liver of Patient 19.). Treatment with interferon alfa-2a was begun but was interrupted because of a urinary tract infection and liver failure. The child's condition stabilized, and treatment with interferon alfa-2a was resumed. The extensive hemangioma of the liver resolved entirely after five weeks of the second course of therapy (Fig. 5B), and the child was discharged from the hospital free of all medication. At the most recent follow-up, nine months after interferon was discontinued, there was no regrowth of the tumor and her development was normal.Toxicity
One patient (Patient 5 in Table 1) had a vigorous initial response to therapy, with superficial dermal sloughing of the cheek and subsequent healing. Because of rebound growth, treatment was resumed eight weeks later, with no untoward effects. This patient also had a low titer (1:100) of anti—interferon alfa-2a antibodies. Patient 13 had transient neutropenia, which subsequently resolved. All the patients were febrile. No other toxic effects were observed. The mean duration of follow-up after the completion of treatment was 16 months (range, 5 to 30).
Discussion
The natural history of hemangiomas in infants has been well documented by several clinical studies involving hundreds of patients.8 , 9 , 11 12 13 These tumors grow rapidly during the first year of life and then slowly involute over the ensuing five to eight years, making it difficult to evaluate any therapeutic intervention. The difficulty is confounded by the fact that the size, number, and anatomical sites of the lesions are heterogeneous. Nonetheless, even small untreated lesions rarely regress within the first year of life. Most hemangiomas are cutaneous and remain small and harmless, but a few grow to an alarming size or proliferate simultaneously in several organ systems, causing life-endangering complications, such as soft-tissue destruction, deformation or obstruction of vital structures, serious bleeding, congestive heart failure, and sepsis. Treatment is necessary for such life-endangering hemangiomas; however, only 30 percent respond to corticosteroids, and the mortality is 40 to 60 percent.18 , 22 , 23 There are no dependable, safe, and effective treatment alternatives, although there are anecdotal reports of favorable outcomes with embolization,33 , 34 radiation,35 and cyclophosphamide therapy.36 , 37
Encouraged by two earlier reports of improvement in a small number of infants with hemangiomas that were treated with interferon alfa-2a, we prospectively evaluated this agent in infants with life-threatening hemangiomas that were unresponsive to corticosteroids. Such lesions are often fatal because they usually do not resolve until the age of five years. Because of the difficulties of evaluating the efficacy of a treatment regimen in this disorder without the use of control subjects, we treated the infants until the hemangiomas were no longer life-threatening, and if growth recurred, we resumed treatment. We evaluated the response by ultrasonography, magnetic resonance imaging, CT scanning, and photography. In this open-labeled trial, daily subcutaneous injections of interferon alfa-2a seemed to reduce the local and systemic complications and appeared to shorten the length of time to involution in 18 of 20 neonates and infants who presented with life-threatening hemangiomas. Sustained therapy for 9 to 14 months appeared to be desirable, since earlier withdrawal was followed by regrowth of the lesions that was halted and reversed by the reintroduction of the drug. Interferon alfa therapy was not accompanied by toxic effects other than fever, and this occurred in all patients for the first week and responded to treatment with acetaminophen. One patient (Patient 5) had a superficial loss of the skin overlying the hemangioma, which healed with dermal scarring, and she was subsequently found to have a low titer of antibodies to interferon alfa-2a. Skin loss did not occur in our other patients; however, on the basis of this experience, we began subsequent courses at a dose of 1 million units per square meter and increased the dose to 3 million units per square meter during the first month of treatment. With the exception of transient neutropenia in one patient, no other obvious toxic effects were noted.
Since the combination of thrombocytopenic coagulopathy with extensive or large hemangioma (Kasabach—Merritt syndrome) has a high mortality, our finding that interferon therapy was highly effective for this complication is particularly encouraging. In patients with this syndrome, a hematologic response to interferon alfa-2a was observed after only one week of therapy, although the size of the lesions did not change. The withdrawal of interferon therapy resulted in thrombocytopenia but not coagulopathy, and the platelet count rose rapidly on reinitiation of therapy. Treatment with interferon was continued until the hemangioma was reduced to less than one third of its initial volume, at which time the withdrawal of treatment was not accompanied by thrombocytopenia. The course of Patients 2, 3, and 4, who had the Kasabach—Merritt syndrome, was similar to the course of one infant described by Orchard and colleagues29 and of another described by White et al.30 Thus, accumulating evidence suggests a role for interferon alfa-2a in the treatment of this type of hemangioma-associated coagulopathy.
The one child who died had extensive truncal and retroperitoneal tumors that resembled Kaposi's sarcoma, though she was negative for HIV. Histologic analysis revealed abnormal blood vessels lined with flat endothelial cells and lobules of spindle-shaped cells. The lesions were devoid of mast cells, a characteristic of the proliferative phase of benign hemangiomas.3 , 4 Five other fatal cases have been described in infants with retroperitoneal involvement, severe thrombocytopenia, and a histologic pattern resembling that of Kaposi's sarcoma.38 This collective experience suggests that these lesions may represent a malignant variant of infantile hemangioma that appears to be resistant to all known treatments.
This clinical trial suggests that interferon alfa-2a is an effective antiangiogenic therapy for severe hemangiomas of infancy.39 No obvious short-term side effects have been seen to date, and the children's growth and development appear to be normal. Long-term follow-up will be necessary to assess possible long-term toxicity of this treatment.
Supported by grants (M01 RR-02172 and P01 CA-45508 [Dr. Folkman]) from the National Institutes of Health.
We are indebted to our colleagues, the house staff, and the nurses at Children's Hospital, especially those at the General Clinical Research Center; to the referring physicians, who all played an invaluable part in caring for these children; to Jennifer Willworth, the nurse coordinator of the study, for her outstanding efforts; to Dr. Judith Prestifillipo of Hoffmann—LaRoche for supplying the drug free of charge and providing valuable advice; and to Marsha Kartzman for assistance in the preparation of the manuscript.
Source Information
From the Division of Hematology and Oncology (R.A.B.E.), the Division of Plastic Surgery (J.B.M.), and the Departments of Surgery (J.B.M., J.F.), Anatomy and Cellular Biology (J.F.), and Pediatrics (R.A.B.E.), Children's Hospital, Dana–Farber Cancer Institute, and Harvard Medical School, Boston. Address reprint requests to Dr. Ezekowitz at the Department of Pediatrics, Children's Hospital, Enders Bldg., 7th Fl., 300 Longwood Ave., Boston, MA 02115.
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