Vasculitis in Chronic Urticaria: An Immunopathologic Study
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1 22-22X/ Bl / 762- I 3$2./ TH E JOURNAL OF INV ESTIGATIVE DERMATOLOGY, 76: 13-17, Copy right IH8 1 by The Willia ms & Wilkins Co. Vol. 76, No.2 Printed in U.S.A. Vasculitis in Chronic Urticaria: An Immunopathologic Study EuGENE W. MoNROE, M.D., CARYN I. ScHuLz, M.D., JoHN C. MAIZE, M.D., AND RoBERT E. JoRDON, M.D. The Cutaneous Immunopathology Unit, R esearch Service, Veterans Administration Medical Center, Wood (Milwauhee), Wisconsin; the Dermatology Section, Department of M edicine, the M edical College of Wisconsin, Milwauhee, Wisconsin; Milwa.ulzee Medical inic, S. C., Milwauhee, Wisconsin; The Department of Dermatology, State University of New Yorh at Buffalo, Buffalo, New Yorh, U.S.A. Forty-five patients with chronic urticaria were studied to determine: (1) the histologic incidence of leukocytoclastic vasculitis and (2) the clinical, laboratory and immunopathologic parameters that characterized this patient group. By histopathologic examination a spectrum of changes were noted as 9 patients showed leukocytoclastic vasculitis, 15 a dense perivascular infiltrate of lymphocytes and eosinophils, and 21 only a sparse lymphocytic perivascular infiltrate. Both the vasculitis and the dense infiltrate groups had an increased incidence of circulating immune complexes, as detected by q binding and monoclonal rheumatoid factor inhibition radioassays. Direct immunofluorescence showed blood vessel deposition of immunoglobulins, complement, and/or fibrin in 33% of the vasculitis group, 13% of the dense infiltrate group, and 9% of the sparse infiltrate group. These studies suggest that a meaningful number of patients with chronic urticaria have histologic and immunopathologic findings of vasculitis. Chronic urticaria is a reaction pattern in the skin that results from many different stimuli, both immunologic and nonimmunologic. The typical histologic features of urticaria include dermal edema, vascular dilatation, and a sparse perivascular cellular infiltrate [1]. Vasculitis, like urticaria, is not a specific disease per se, but represents a reaction pattern in the skin caused by a wide variety of substances involving different pathogenic mechanisms including deposition of immune complexes. The lesions of cutaneous vasculitis may be pleomorphic, but are usually represented by palpable purpura. Histologically, cutaneous necrotizing vasculitis is characterized by the following: (1) Endothelial cell swelling of the blood vessels (venules), (2) perivascular leukocytic infiltrate usually rich in neutrophils, (3) extravasation of red blood cells, (4) fibrinoid deposits in and around the venules, and (5) leukocytoclasis (fragmentation of the leukocytes with nuclear debris) [2-5]. Some authors state that the latter 2 criteria are most critical since they represent direct signs of vessel injury [ 4]. In the past few years, isolated cases have been reported in which the a bove 2 skin reaction patterns-urticaria and vasculitis-have overlapped [6-21]. These reports suggest that some patients may present clinically as urticaria which, by skin Manuscript received March 26, 198; accepted for publication July 28, 198. This work was supported by Research Grant AI-1456 from the National Institute of Health, United States Public Health Service, and by the Veterans Administration. Dr. Jordon is the recipient of a Medical Career lnvestigatorship of the Veterans Administration. Presented in part at the Central Meeting of the Society for Investigative D ermatology, Chicago, Illinois, November 3, Reprint requests to: Eugene W. Monroe, M.D., Reseru ch Service/ 151, Veterans Administration Medical Center, Wood, Wisconsin Abbreviations: ESR: erythrocyte sedimentation rate IF: immunofluorescence mrf: monoclonal rheumatoid factor biopsy, shows leukocytoclastic vasculitis. Some of these patients have displayed various laboratory and clinical abnormalities, including the following: Elevated sedimentation rate (ESR), hypocomplementemia, circulating immune complexes, arthralgias, abdominal pain, fever, lymphadenopathy, and glomerulonephritis. The purpose of our current study was to prospectively determine in a group of patients with chronic idiopathic urticaria: ( 1) The histologic incidence of leukocytoclastic vasculitis, and (2) the clinical, laboratory, and immunopathologic parameters characterizing this subgroup. MATERIALS AND METHODS This prospective study included 45 consecutive patients who presented with the diagnosis of chronic idiopathic urticaria. This disease was defin ed clinically as urticaria which had persisted for at least 6 weeks on a daily basis and with no detectable underlying etiology. The group consisted of 3 women and 15 men ranging from 4 to 8 yr of age. Thirty-one of the patients were seen at the Milwaukee Medical inic, S.C. (a private practice, multispecialty medical clinic) and 14 patients were seen at the teaching hospitals of the Medical College of Wisconsin (Milwaukee County Medical Complex and Wood Veterans Administration Medical Center). Twenty-three of the patients were referred to om study by practicing dermatologists or allergists in the community. The remaining 22 patients were seen initially by us for evaluation of their problem. All patients were either on no medications or minimal antihistamine therapy for at least 48 hr prior to the initial laboratory and biopsy procedures. The following laboratory studies were performed in all patients: CBC and differential count, platelet count, urinalysis, sedimentation rate, blood chemistries (SMA-12), VDRL, quantitative immunoglobulins (lgg, IgM, IgA, lge), antinuclear antibodies, rheumatoid factor, cryoglobulins, cryofibrinogens, hepatitis B antigen, and total hemolytic complement. Circulating immune complexes were measured by 2 radioassays-the q binding and monoclonal rheumatoid factor (mrf) inhibition assays recently described in detail (23]. Briefly, sera for immune complex studies were sepru ated fro m freshly clotted blood and kept frozen at -7 C until tested. The q binding assay was performed by the method of Nydegger et al (24), with modifications described by Tappeiner et al (25]. The mrf inhibition assay was performed by the method of Luthra et al (26). Punch biopsies were obtained from 2 different urticarial lesions which, by history, were of recent onset (less than 24 lu old). One biopsy specimen was fixed in 1% formalin solution, stained with hematoxylin and eosin, and examined by light microscopy. The second biopsy specimen was tested by direct immunofluorescent (IF) staining according to established methods using monospecific fluorescein-la beled antisera to IgG, IgM, lga, C3, and fibrin (Meloy Laboratories, Inc., Springfield, VA) [27). Histop athology RESULTS Biopsies of lesions from 45 chronic urticaria patients led to the establishment of 3 histologic categories (Ta ble). Twentyone patients (47%) were classified as a "sparse infiltrate" group (Fig la and 1b). This group presented the typical textbook histologic features of urticaria including (1) dermal edema, (2) vascular dilatation of small cutaneous blood vessels, and (3) sparse perivascular cellular infiltrate consisting primarily of lymphocytes and a few eosinophils. Except for vascular dilatation, the blood vessels displayed no abnormal alterations. Fifteen patients (33%) were classified as a "dense infiltrate" 13
2 14 MONROE ET AL inical, laboratory, and immunopathologic findings in histologic subgroups of chronic urticaria patients Leukocytoclastic vasculitis Dense infiltrate Sparse infiltrate (%) (%) (%) Patients Positive direct IF of blood vessels Circulating immune com plexes q assay mrf assay Individual lesions persisting >24 hr Elevated ESR Arthralgias Pressure urticaria Vol. 76, No. 2 vasculitis" group (Fig 3a, 3b, and 3c). Each of these patients had to have at least leukocytoclasis (fragmentation of the leukocytes with nuclear debris) and/or fibrinoid deposits in and around the vessel walls. Each of the 9 patients had both leukocytoclasis and fibrinoid deposits present in varying degrees. These patients displayed a moderate to dense perivascular cellular infiltrate usually rich in neutrophils but also containing lymphocytes and eosinophils. Extravasation of red blood cells was also occasionally present. Direct Immunofluorescence Direct IF of urticarial lesions revealed various combinations of immunoglobulins, complement and fibrin in the vessel walls of 16% of the patients (Fig 4). These patterns were typical of the vessel wall fluorescence seen in patients with cutaneous vasculitis. Positive immunofluorescence was found in 33% of the leukocytoclastic vasculitis group, 13% of the dense inftltrate group, and 9% of the sparse inflltrate group. Two of the patients in the leukocytoclastic vasculitis group also had dermal-epidermal junctional IF. Circulating Immune Complexes By the q binding and mrf inhibition radioassays, 44% of the leukocytoclastic vasculitis group had detectable circulating immune complexes, 44% by the q assay and 22% by the mrf... ~ ~ ( 1: ~..., J I ;J l A ~ :. ~.. FIG 1. A, Sparse inftltrate group. Biopsy of urti ca ~i a l l es ion showing sparse perivascular cellular infiltrate, consisting mostly of ly mphocytes and a few eosinophils (hematoxylin-eosin, reduced from x 16). B, Fig la, reduced from X 4. group (Fig 2a and 2b). This group also demonstrated dermal edema and vascular dilatation but differed from the sparse infiltrate group in the amount and type of perivascular cellular inflltrate present. These patients had moderate to dense perivascular infiltrates composed primarily of lymphocytes and eosinophils. Some patients had marked eosinophilic inflltrates with eosinophilic degranulation. None of the patients, however, had evidence of vasculitis as defined below. Nine patients (2%) were classified as a "leukocytoclastic FIG 2. A, Dense infiltrate group. Biopsy of l.o"ticariallesion shov!ing dense perivascular cell ul ar inftltrate, composed mainly of lymphocytes and eosinophils (h ematoxylin-eosin, reduced from X 16). B, Fig 2A, reduced from X 4.
3 Feb VASCULITIS IN CHRONIC URTICARIA 15 FIG 4. Direct IF of urticarial lesion demonstrating deposition of IgM in cutaneous blood vessels (reduced from x 5). FIG 3. A, Leukocytoclastic vasculitis group. Biopsy of urticarial lesion showing dense perivascular ceuulru infiltrate composed of neutrophils, lymphocytes, and eosinophils. Leukocytoclasis and fibrinoid deposits are present in and around the vessel walls (hematoxylin-eosin, assay (Fig 5). The dense infiltrate group (53%) had detectable circulating immune complexes, 13% by the q assay and 47% by the mrf assay. Only 5% of the sparse infiltrate group had detectable circulating immune complexes and these only with the mrf assay. Laboratory Studies The only frequently abnormal laboratory test was the erythrocyte sedimentation rate (ESR) which was elevated in 56% of the leukocytoclastic vasculitis group, 4% of the dense infiltrate group, and 29% of the sparse infiltrate group. Patients (27%) had elevated IgE levels, but these were evenly distributed among the 3 groups. No other laboratory abnormalities were commonly found in any of the 3 groups by the several other tests performed. Of interest only one of the 45 patients had hypocomplementemia. This patient was subsequently diagnosed as having systemic lupus erythematosus. Signs and Symptoms The duration of individual urticarial lesions varied among the 3 histologic groups. Individual lesions persisted for more than 24 hr in 67% of the leukocytoclastic vasculitis group. Only 33% of the dense infiltrate group and 19% of the sparse infiltrate group, however, had in'dividuallesions persisting for more than 24 hr. Arthralgias were also more common in the leukocytoclastic vasculitis group (44%) and the dense inftltrate group (4%) when compared to the sparse infiltrate group (29%). Pressure urticaria (i.e., urticaria which, by history, was induced by physical pressure to the skin), was more common in leukocytoclastic vasculitis group (67%) and the dense infiltrate group reduced fi om X 16). B, Fig 3A, reduced from X 4. C, Biopsy of urticarial lesion from a different patient showing leukocytoclastic vasculitis (hematoxylin-eosin, reduced from X 4).
4 16 MONROE ET AL Vol. 76, No.2 E " LEUKOCYTOCLASTIC OENSE SPARSE VASCULITIS INFILTRATE INFILTRATE 4 / 9 2 / 9 2 / 15 7 / 15 /21 1/ 21 POSITIVE POSITIVE POSITIVE POSITIVE POSITIVE POS ITIVE 1 - QJ 4 - <( ::: o o FIG 5. Scattergram demonstrating q (e) and MRF ( ) reactivity in serum samples from patients with different histologic categories of chronic urticaria. Serum samples with normal levels of q and MRF reactive materials (:5 5 ug Agg IgG eq/ ml) are included in the hatched areas. (53%) than the sparse infiltrate group (24%). Angioedema was equally distributed among the 3 groups. Gastrointestinal pain was present in only one patient who was subsequently found to have shigellosis. Fever, lymphadenopathy, and glomerulonephritis were not present in any of the patients. DISCUSSION In the past few years, isolated case reports have appeared in the literature in which patients present with a clinical picture of urticaria which, when biopsied, shows ieukocytoclastic vasculitis rather than the usual histologic features of urticaria [6-21]. The few studies reported to date are conflicting as to the incidence of vasculitis in typical chronic idiopathic urticaria. Phanuphak et al [22) recently presented 42 consecutive patients with chronic urticaria; 22 patients displayed vasculitis on biopsy. Vasculitis in this study was defined by the presence of inflammatory cell inflltrates within the blood vessel wall. Synkowski et ar[28] reported 14 randomly chosen patients with acute and chronic urtic~ria, but found no histologic evidence of vasculitis in any of their patients. In the present prospective study of 45 patients with chronic idiopathic urticaria, a spectrum of changes were apparent by histologic examination. Twenty percent of the patients demonstrated a leukocytoclastic vasculitis. In order to be classified as leukocytoclastic vasculitis in our study, histologic evidence of leukocytoclasis and/or fibrinoid deposits in and around the vessel walls was required. In addition, a moderate to dense perivasc\}lar cell infiltrate, extravasation of red blood cells, and vascular endothelial cell swelling was apparent. Fifty percent of the patients demonstrated a dense perivascular inflltrate with or without evidence of vasculitis. The remaining 5% demonstrated more typical histologic pictures of urticaria, including a sparse perivascular cellular infiltrate. Although no single serologic or immunopathologic parameter was characteristic of any of our histologic subgroups, certain patterns were clearly present. Both the leukocytoclastic vasculitis and dense inftltrate groups manifested an increased incidence of positive direct IF of blood vessels. Immunoglobulins, complement, and fibrin deposition are frequently observed in lesions of vasculitis by direct IF [29-32]. Sixteen percent of the total group of patients and 33% of the vasculitis group had positive vessel wall IF typical of the pattern seen in leukocytoclastic vasculitis. Circulating immune complexes are frequently detected in leukocytoclastic vasculitis, and increasing evidence exists that the deposition of these immune complexes in blood vessel walls is involved in the pathogenesis [23, 33-38). In the isolated case reports of "urticarial vasculitis," circulating immune complexes were often detectable. In our series of chronic urticaria patients, 44% of the vasculitis group and 53% of the dense inflltrate group had detectable circulating immune complexes. Hypocomplementemia was not a significant finding in our study. Only 1 of our 45 patients had depressed total complement, and this patient was subsequently found to have systemic lupus erythematosus. On the other hand, the vast majority of previously reported cases of "urticarial vasculitis" had depressed complement levels. In these cases, although different complement components were depressed, the total hemolytic complement was always abnormal. Hypocomplementemia may be an important distinguishing parameter between urticarial vasculitis and typical chronic idiopathic urticaria associated with histologic evidence of leukocytoclastic vasculitis. The importance of an elevated ESR is noteworthy. In the majority of reported cases of "urticarial vasculitis," the ESR is elevated. In addition, some reports suggest that urticaria patients without evidence of necrotizing venulitis invariably have a normal ESR (39], a finding not supported by our study. Thirty-six percent of the total group of chronic urticaria patients had elevated ESRs. This finding was more common in the vasculitis group where 56% had elevated ESRs. Some of the patients with vasculitis histologically, however, had a normal ESR, while some with no evidence of vasculitis had an elevated ESR. Although a nonspecific test, the ESR is useful because its elevation should suggest further investigation of the possibility of an underlying vasculitis. A normal ESR, on the other hand, does not preclude an underlying vasculitis. Certain clinical signs and symptoms may also be useful in distinguishing the different histologic groups of chronic urticaria patients. Traditionally, individual urticariallesons persist for less than 24 hr. Sixty-seven percent of our vasculitis group had individual lesions which persisted for periods greater than 24 hr. This finding is similar to the previously reported cases of "urticarial vasculitis" where individual lesions frequently persisted for more than 24 hr, and occasionally resolved leaving purpuric changes. Arthralgias were present in approximately one-third of all our chronic urticaria patients, but were somewhat more common in the vasculitis group. Similar findings have been noted in previously reported cases of "urticarial vasculitis." Pressure urticaria was also a common clinical finding in the vasculitis and dense infiltrate groups. Other systemic signs such as arthritis, fever, gastrointestinal pain, lymphadenopathy, and glomerulonephritis were occasionally noted in reported cases of "urticarial vasculitis". None of these latter fmdings were apparent in our group of urticaria patients. It is our contention that "urticarial vasculitis" is an entity requiring 2 features-a clinical picture of urticaria which, by skin biopsy, shows leukocytoclastic vasculitis. The probable underlying pathogenic mechanism in this condition is one of immune complex deposition. Possessing the above features are a heterogeneous group of patients displaying a spectrum of clinical, laboratory, and immunopathologic changes. The patients described in this study represent the less severely affected end of this spectrum. Our patients were chru acterized by idiopathic chronic urticaria, minimal signs or symptoms of systemic disease except for frequent arthralgias, some serologic and immunopathologic findings suggestive of vasculitis, and normal complement levels. The isolated case reports of urticarial vasculitis [6-21] appearing under the names of "hypocomplementemic vasculitis", "unusual SLE-related syndrome," or "urticaria with vasculitis" represent a more severely involved part of this spectrum. These patients often had features which distinguished them from the patients reported in our study. Some of these distinguishing features were the following: additional skin lesions which were purpuric or erythema multiforme-like; clinical signs or symptoms of multisystem disease such as arthralgias, arthritis, fever, gastrointestinal pain, lymph-
5 Feb VASCULITIS IN CHRONIC URTICARIA 17 ade nopathy, and glomerulonephritis; a higher incidence of serologic and immunopathologic findings suggestive of vasculitis, and hypocompjementemia. Whether some of these patie n ts represent a subset of collagen-vascular disease remains to be determined. Finally, the most severe end of the spectrum of " urticarial vasculitis" is represented by those patients with systemic lupus eryth ematosus who present with urticarial-like lesions [ 4]. In summary, chronic urticaria patients show a spectrum of changes on histologic examination including leukocytoclastic vasculitis. In a ddition, a m eaningful number of these chronic urticaria patients show other serologic and immunopathologic findings suggestive of vasculitis. In subdividing chronic urticaria patients by various criteria, including histopathology and IF, ow understanding of the pathogenic m echanisms involved in this perplexing condition should improve. The findings of vasculitis and immune complex disease in some patients with chronic urticaria may improve our future ability to predict the course and to individualize treatment in t h ese patients. REFERENCES I. Lever WF, Schaumburg-Lever G: Histopathology of the Skin, 5th ed.. J.B. Lippincott, Philadelphia, 1975, p Goltz RW: Cutaneous manifestations of allergic angiitis. Lancet 1: , Winkelman RK, Ditto WB: Cutaneous and visceral syndromes of necrotizing: "Allergic" vasculitis. A study of 38 cases. Medicine 43:59-89, Cox AJ: Pathologic changes in hypersensitivity angiitis, The Skin Edited by EB Helwig, FK Mostofi. Williams & Wilkins, Baltimore, 1971, pp Soter NA, Mihm MC Jr, Gigli I, Dvora k HF, Austen KR: T.wo distinct cellular patterns in cutaneous necrotizing angiitis. J Invest Dermatol 66:344-35, McDuffie FC, Sams WM Jr, Maldonado JE, Audreini PH, Conn DL, Samayoa EA: Hypocomplementemia with cutaneous vasculitis and arthritis. Possible immune complex syndrome. Mayo inic P roc 48:34-348, Sissons JGP, Williams DG, Peters OK, Boul ton-jones JM: Skin lesions, angioedema and hypocomplementemia. Lancet 2: , Soter NA, Austen KF, Gigli I: Urticaria and arthralgias as manifestations of necrotizing angiitis (vasculitis). J Invest Dermatol 63: , Agnello V, Ruddy S, Winchester RJ, Christian CL, Kunkel HG: Hereditary C2 defi ciency in systemic lupus erythematosus and acquired complement abnormalities in an unusual SLE-related syndrome. Birth Defects 11 : , Ballow M, Ward GW Jr, Gershwin ME, Day NK: C, -bypass complement-activation pathway in patients wi th chronic w ticaria and angioedema. Lancet 2:248-25, Tuffanelli DL: Cutaneous immunopathology: Recent observations. J Invest Dermatol 65: , Agnello V, Gabriel A Jr, Tai M: Detection of immune complexes. J Invest Dermatol 67: Feig PU, Soter NA, Yager HM, Caplan L, Rosen S: Vasculitis with urticaria, hypocomplementemia, and multiple system involvement. JAMA 236: , Geha RS, Akl KF: Skin lesions, angioedema, eosinophilia, and hypocomplementemia. J Pediatr 89: , Marder RJ, Rent R. Choi EYC, Gewurz H: q deficiency associated with urticarial-like lesions and cutaneous vasculitis. Am J Med 61 :56-565, Oishi M, T akano M, Miyachi K, Ichikawa Y, Homma M: A case of unusual SLE-related syndrome characterized by erythema multiforme, angioneurotic edema, marked hypocomplementemia, and q precipitins of the low molecular weight type. Int Arch Allerg Appl Immunol 5: , Mathison DA, Arroyave CM, Bhat KN, Hurewitz OS, Marnell OJ: Hypocomplementemia in chronic idiopathic urticaria. Ann Intern Med 886: , Soter NA: Chronic urticaria as a mannifestation of necrotizing ve nulitis. N Eng! J Med 296: , Phanuphak P, aman HN, Kohler PF: Urticarial vasculitis. N Eng! J Med 297: , Agnello V: Complement deficiency states. Medicine 57: 13-15, Gammon WR, Wheeler CE: Urticarial vasculitis: Report of a case and r eview of the li terature. 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Br J Dermatol 89: , Braverman IM, Yen A: Demonstration of immune complex in pontaneous- and histamine-induced lesions and in normal skin of patients with leukocytoclastic angiitis. J Invest Dermatol 64: , Cream JJ: inical and immunological aspects of cutaneous vasculitis. Quart J Med 178: , Sams WM Jr, Thorne EG, Small P, Mass MF, Mcintosh RM. Stanford RE: Leukocytoclastic vasculitis. Arch Dermatol 11 2: , Lambert PH, Dixon FJ, Zubler RH, Agnello V, Cambiaso C. Casali P, arke J, Cowdery JS, McDuffie FC, Hay FC, MacLennan ICM, Masson P, Muller-Eberhard HJ, Penttinen K, Smith M, Tappeiner G, Theofuopoulos AN, Verroust P: A WHO collaborative study for the evaluation of 18 methods for detecting immune complexes in serum. J in Lab Immunol 1: 1-15, And.! ews BS, Cains G, Mcintosh J, Petts V, Perry R: Circulating and tissue immune complexes in cutaneous vasculitis. J in Lab Immunol 1:311-32, Soter NA: Urticarial vasculitis. N Eng! 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t Dr. Small is a Fellow of the Medical Research
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