Cutaneous extravascular necrotizing granuloma (Winkelmann granuloma): Confirmation of the association with systemic disease
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1 Cutaneous extravascular necrotizing granuloma (Winkelmann granuloma): Confirmation of the association with systemic disease Gregory J. Wilmoth, MD, and Charles Perniciaro, MD Jacksonville, Florida Background: An unusual palisading granuloma has been described in patients with immunoreactive diseases. Multiple names have been given to this lesion. Objective: Our aim was to verify whether a distinct palisading granuloma can be used as a marker for systemic disease. We also propose unifying nomenclature. Methods: Thirty-four biopsy specimens from 22 patients were selected for study on the basis of histologic criteria. The medical histories of these patients were subsequently reviewed for clinical information. Results: At least 21 of the 22 patients with cutaneous extravascular necrotizing granuloma had evidence of an underlying immunoreactive systemic illness. In each, the systemic disease preceded or was diagnosed concurrently with the cutaneous lesions. Conclusion: The cutaneous extravascular necrotizing grmnuloma has unique clinical and histologic features. In a great majority of cases, a systemic immunoreactive disease is present. (J AM ACAO D~I~IVIATOL 1996;34:753-9.) In 1978, seven patients who had cutaneous lesions with distinctive histologic features were described by Dicken and Winkelmann. 1 These patients all had unusual palisading granulomas within the skin. Microscopically, the lesions resembled the "allergic granulomas" initially described by Churg and Strauss 2 as part of the syndrome of allergic granulomatosis. In recognition of their original description, the name "Churg-Strauss granuloma" was proposed for this unique cutaneous lesion. However, only one of the seven patients reported by Dicken and Winkelmann had allergic granulomatosis. The other patients had various types of systemic vasculifts not related to allergic granulomatosis. Since this original review, identical palisading granulomas have been shown to coexist with various "immunoreactive" systemic diseases. The term cutaneous extravascular necrotizing granuloma has been suggested as a synonym for Churg-Strauss granuloma.3, 4 Other authors have described similar lesions using varied nomenclature. 5-1a From the Department of Dermatology, Mayo Clinic Jacksonville. Accepted for pubfication Oct. 2, Reprint requests: Charles Perniciaro, MD, Mayo Clinic Jacksonville, 4500 San Pablo Rd., Jacksonville, FL Copyright 1996 by the American Academy of Dermatology, Inc /96 $ /1/69821 We review our findings in 22 patients with this distinctive cutaneous palisading granuloma and suggest terminology that unifies the large number of confusing names given to this lesion. METHODS In the patients chosen for study, biopsy had been performed between Jan. 1, 1983, and Dec. 31, Patients were initially selected on the basis of histologic criteria as described by Dicken and Winkelmann 1 and Finan and Winkelmann, 3 without prior knowledge of any patient's medical history. All patients had biopsy specimens that showed zones of basophilic necrobiotic collagen interspersed with neu~opinls and neutrophilic debris. In most cases, a palisading array of histiocytes surrounded the basophilic areas of necrosis ("classic" pattern). Less often, histiocytes were present in increased numbers but did not completely surround the areas of necrosis ("focal basophilic necrosis"). From our archival collection, we selected 26 biopsy specimens from 16 patients; these specimens were all categorized as "Churg-Strauss granuloma." Additionally, we reviewed 787 specimens collected during the same 10-year period that were categorized as "granuloma annulare" (723), "palisading granuloma" (42), "rheumatoid nodule" (11), and "necrobiotic granuloma" (11). Infectious granulomas were excluded. Eight biopsy specimens from six patients were selected through this review. The final cohort thus included 22 patients. The medical records of these 22 patients were reviewed 753
2 754 Wilmoth and Perniciaro Fig. 1. Case 8. Symmetric papules on elbows. in detail to assess concurrent medical problems, laboratory data, treatment, and follow-up. One patient (case 20) has been described previously.12 RESULTS Lesions were present in 14 women and 8 men. Their ages ranged from 25 to 76 years (mean, 49.4 years). All 22 patients had firm skin-colored to erythematous to violaceous papules or nodules (Fig. 1). Eighteen patients had multiple lesions that generally were symmetric in distribution. Nine patients had umbilicated lesions, and this feature correlated with histologic "perforation" of the lesion through the epidermis. In most patients, lesions were described as tender, although some were asymptomatic. Elbows were the most frequent location (15 patients), followed by the fingers and thumb (9 patients). One patient had generalized lesions. Rarely, lesions were ulcerated. In 21 of the 22 patients, an underlying systemic illness was identified on review of the medical record. Most often, these illnesses were types of systemic vasculitis or connective tissue diseases. In all patients, cutaneous extravascular necrotizing granulomas developed concurrently with the systemic illness or after diagnosis of the systemic illness. Concurrent lesions were present in nine patients (41%). In one patient (case 3), skinlesions developed concurrent with the detection of proteinuria and an unspecified renal mass. The patient declined additional investigation and was lost to follow-up. The clinical and histologic findings are summarized in Table I. Skin lesions generally receded with treatment of the systemic disease, particularly when prednisone or other immunosuppressive medications were ad- Joumal of the American Academy of Dermatology May 1996 Fig. 2. Case 10. Cutaneous extravascular necrotizing granuloma (Winkelmann granuloma). Necrobiotic collagen interspersed with neutrophils and leukocytoclastic debris, surrounded by palisading histiocytes. (Hematoxylin-eosin stain; original magnification x40.) ministered. The skin lesions spontaneously healed without treatment in a few patients. Lesions were not responsive to topical corticosteroids but did clear with intralesional corticosteroid injections in one patient. Histologic findings Thirty-four skin biopsy specimens were reviewed. The predominant pattern was a palisading granuloma with central basophilic necrosis composed of necrobiotic collagen, neutrophils, and neutrophilic debris. This central area of necrosis was surrounded by histiocytes ("classic" pattern) in 29 specimens from 18 patients (Figs. 2 and 3). In four patients the specimens exclusively demonstrated focal basophilic necrosis (Fig. 4), without a palisading pattern. One patient had a classic palisading pattern in one specimen and focal basophilic necrosis in a specimen from another lesion. All necrotizing granulomas were extravascular, and most specimens showed no significant histologic changes within dermal blood vessels. However, five patients had small-vessel leukocytoclastic vasculitis within the same specimen as the necrotizing granuloma. Three of these five patients with cutaneous vasculitis had a focal basophilic necrosis pattern in the extravascular areas, suggesting that this pattern may represent early or incompletely developed lesions. Scattered eosinophils were present within the granulomas in two patients (cases 3 and 18). One patient (case 3) did not have peripheral eosinophilia, and one (case 18) had marked leukocytosis and eosinophilia.
3 Journal of the American Academy of Dermatology Volume 34, Number 5, Part 1 Wilmoth and Perniciaro 755 Table I. Clinical and histologic findings in 22 patients with cutaneous extravascular necrotizing granuloma Patient No. Age at diagnosis Location of skin of skin lesion (yr) Sex lesions Temporal relation of skin lesions to systemic illness Systemic illness Histolo~e pattern Comments 53 F Wrist, ankle, 5 yr later Multiple sclerosis PG elbows 28 F Both index A: 21 yr later A: Hemolytic PG (3 biopsies) fingers, B: 6 yr later uremic syn- thumbs drome B: Thrombotic thrombocytopenic purpura 69 M Wrist Concurrent Unspecified FBN 10 cm kidney mass 25 F Elbow 14 yr later Rheumatoid ar- PG thrifts 40 M Elbow Concurrent Allergic granulo- PG (2 biopsies) matosis 50 F Fingers, elbow 3 yr later Rheumatoid PG (perforating) arthritis 67 F Thigh, elbow A: Concurrent A: Drug reaction PG (2 biopsies) B: 6 mo later (penicillin) B: Sj6gren's syndrome 8 58 F Elbows Concurrent Unclassified, PG (2 biopsies) overlap connective tissue diseases 9 76 M Fingers 1 yr later Metastatic adeno- PG carcinoma, prostate F Elbow 5 yr later Wegener's PG (perforating) M Elbow, knee, Concurrent Streptococcal in- PG (3 biopsies: 1 palm fection with LCV, 1 Bloody diarrhea perforating) (cause unknown) F Fingers, 2 yr later Rheumatoid FBN (with LCV) elbows arthritis F Elbows, fore- 4 yr later Systemic vasculi- FBN (with LCV) arms, tis (unclassifingers fled) + Proteinnria-- lost to follow-up Erosive bone lesions: RF 1:128 Neuropathy, asthma, eosinophilia RF 1:2560, ANA 1:320 EM-like lesions also present, +biopsy for Sj6gren's syndrome + Gottron's papules, interstitial lung disease, ANA 1:160 canca 1:128, Wegener' s lesion: nasal septum ASO titer 170 U (normal, 0-85 U), diarrhea and skin lesions cleared without therapy + Cryoglobulins, RF 1:5420, ANA 1:640 Polyart)u'itis, nailfold infarcts, diarrhea, aphthous ulcers ANA, Antinuclear antibody; ASO, antistreptolysin O; canca, antineutrophil cytoplasmic antibody; CVA, cerebrovascular accident; EM, erythema multiforme; FBN, focal basophilic necrosis; LCV, leukocytoctastic vasculitis; PG, palisading ~:anuloma ("classic type"); RF, rheumatoid factor. *Case previously reported. 12 Con#nued on page 756
4 756 Wilmoth and Perniciaro Journal of the American Academy of Dermatology May 1996 Table I. Cont'd Age at I Lo ation Patient ofskm I of skin No. lesion (yr) Sex lesions Temporal relation of skin lesions to systemic illness Systemic illness Histologie pattern Comments M Elbows * F Elbows F Elbows M Generalized Concurrent 3 yr later Concurrent 2 yr later F Elbows, Concurrent fingers, toes F Fingers, hands, Concurrent elbows M Thumb, fro- 2 yr later gers, palms F Thumb, fingers 5 yr later M Forearms, calf Concurrent Mixed cryoglobuline- 1) PG mia 2) FBN Wegener's PG Allergic granuloma- PG (2 biopsies) tosis Chronic lymphocytic FBN (with LCV) leukemia Allergic granulo- PG matosis Seronegative erosive PG (2 biopsies) arthritis Takayasu's arteri- PG (2 biopsies: 1 tis with LCV) Myelodysplastic PG syndrome Wegener's PG (2 biopsies) + Cryoglobulins, mononeuritis multiplex, RF 1: ,000 leukocytes with 60% eosinophils ANA 1:320, + Raynaud's phenomenon, RF nonreactive + Asthma, + CVA, seizures, + arthralgias Histologic perforation of the abnormal collagen through the epidermis was observed in three patients. A biopsy specimen was obtained for direct immunofluorescence examination in seven patients. Three of these patients (cases 11, 14, and 22) had multiple immunoreactants (C3, IgM, and fibrinogen) within dermal blood vessels. C3 and fibrinogen were present within the dermal blood vessels in case 17, and C3 alone was seen in case 20. The remaining two patients had negative studies. DISCUSSION Cutaneous extravascular palisading granulomas were initially described as a manifestation of allergic granulomatosis by Churg and Strauss in ' 13 These authors noted unique "allergic granulomas" with palisading macrophages surrounding a central area of necrotic collagen, eosinophils, and cellular debris. This characteristic histopathologic lesion (in the skin and other organs) was thought to be a specific component of the Churg-Strauss syndrome of allergic granulomatosis. However, in 1977, Hu, O'Laughlin, and Winkelmann 14 noted cutaneous necrotizing palisading granulomas in patients with Wegener' sgranulomatosis. Thesefindings wereidentical to those described in allergic granulomatosis. In 1978, Dicken and Winkelmann 1 described seven additional cases of cutaneous necrotizing palisading granulomas in patients with allergic granulomatosis as well as other systemic diseases including lupus erythematosus, Wegener's granulomatosis, rheumatoid arthritis, and subacute bacterial endocarditis. Tissue eosinophilia was not a prominent finding in any of their cases. The authors attributed this to the lack of peripheral blood eosinophilia in this group of patients. They noted neutrophils and leukocytoclastic debris interspersed with altered collagen in the center of the granulomas, giving them a characteristic basophilic appearance. Dicken and Winkelmann chose to designate these lesions by the eponym "Churg-Strauss granuloma," in recognition of the original description by Churg and Strauss. Unfortunately, many erroneously concluded that the cutaneous "Churg-Strauss granuloma" is synonymous with allergic granulomatosis or Churg-Strauss granulomatosis. Indeed, this lesion can be found in many systemic diseases. In the largest series of cases reported to date, Finan and Winkelmann 3 studied 27 patients with cutaneous extravascular necrotizing granulomas. Twenty-six had an associated autoimmune or immunoreactive systemic disease, and seven had aller-
5 Journal of the American Academy of Dermatology Volume 34, Number 5, Part 1 Wilmoth and Perniciaro 757 Fig. 3. Case 10. Higher-power photomicrograph. Note fractured and necrotic basophilic collagen. (Hematoxylin-eosin stain; original magnification xl60.) Fig. 4. Case 17. Focal basophilic necrosis of collagen without tree palisading granuloma. (Hematoxylin-eosin stain; original magnification x250.) gic granulomatosis. Other illnesses included systemic vasculitis, lupus erythematosus, rheumatoid arthritis, lymphoproliferative diseases, endocarditis, hepatitis, and inflammatory bowel disease. One patient had vasculitis limited to the skin. These authors emphasized the presence of neutrophilic dermal inflammation and neutrophils within the granulomas. Tissue eosinophilia was not a prominent finding. Perniciaro and Winkelmann 12 subsequently described identical cutaneous granulomas in a patient with Takayasu' s arteritis. Several other investigators have noted similar necrotizing granulomas in patients with Wegener's granulomatosis and lymphoproliferative diseases A group of other diseases has been reported that are characterized by cutaneous papules and nodules that on biopsy reveal neutrophilic inflammation, collagen degeneration, and granulomatous inflammarion (most often palisading). These diseases include rheumatoid papules, 5, 6 superficial ulcerating rheumatoid necrobiosis, 7,8 interstitial granulomatous dermatitis with arthritis, 9 palisaded neutrophilic and granulomatous dermatitis, l and rheumatoid neutrophilic dermatitis. 11 In all these reports there was an association with an tmderlying illness. Limited cutaneous Wegener's granulomatosis also has been used as a term to describe these lesions. 2 The "Churg-Strauss phenomenon" has been proposed as an additional synonym.* In all but one of our patients, an autoimmune or immunoreactive systemic disease was present. The final patient was lost to follow-up before his evalu- ation was completed. In each patient, cutaneous extravascular necrotizing granuloma developed with or after the systemic illness. Our findings support the conclusions of Finan and Winkelmann. 3 We believe that cutaneous extravascular necrotizing granuloma is a distinct clinicopathologic entity that develops in patients with systemic diseases of an immunoreactive nature. The presence of this unique granulomatous lesion in the skin should prompt a search for an underlying systemic disorder. Even the two previously reported patients with supposed cutaneous [only] Churg Strauss syndrome had accompanying Raynaud's phenomenon (one patient) and Hashimoto's thyroiditis (one patient). 21 The clinical features of cutaneous extravascular necrotizing granuloma are distinctive. The characteristic clinical pattern consists of multiple discrete, skin-colored to erythematous to violaceous papulonodules located predominantly on the elbows or the distal upper extremities and fingers. Often the papulonodule has a central umbilication or necrosis. Lesions tend to be symmetrical in distribution. The predominant location of cutaneous extravascular necrotizing granuloma on the elbows and hands suggests that local trauma may play a role in its development. The histopathologic findings are those of an extravascular palisading granuloma with a central basophilic core consisting of fractured, granular, necrobiotic collagen, neutrophils, and leukocytoclastic debris. Interstitial dermal neutrophilic inflammarion also may be present. Less organized granulomas (noted in five of our cases as "focal basophilic necrosis") are characterized by infiltrates of neutrophils, leukocytoclastic debris, and histiocytes inter- *From the 32nd Annual Meeting of the American Society of Dermatopathology, Evening Slide Symposium, New Orleans, La., Feb. 3, 1995.
6 758 Wilmoth and Perniciaro Journal of the American Academy of Dermatology May 1996 spersed between collagen bundles associated with basophilic collagen alteration. A palisading pattern is not seen in the less organized granuloma. This lesion may represent part of a specmma of disease in which the granuloma is not fully developed. The clinical lesions were identical in our cases, whether focal basophilic necrosis or true palisading granulomas were seen histologically. Five of our specimens also demonstrated leukocytoclastic vasculitis in the same specimen as the cutaneous extravascular necrotizing granuloma. This spectrum of histopathologic findings, together with evidence of immunoreactants in the vessel walls on direct immunofluorescence studies in five of seven patients, suggests a pathogenesis involving immune complexes, vasculitis, and granuloma formation. Chu, Connolly, and LeBoit 1 suggested that these lesions begin as leukocytoclastic vasculitis and evolve to a more granulomatous stage. Similar vascular findings also have been observed in some patients with granuloma annulare and necrobiosis lipoidica diabeticomm Histopathologic differentiation from other palisading granulomas is usually straightforward because of the unique basophilic collagen degeneration and neutrophilic inflammation of cutaneous extravascular necrotizing granuloma. Extensive basophilic necrosis is not a feature of granuloma annulare. On occasion, rheumatoid nodules have central basophilic necrosis with scattered inflammatory cells within the areas of fibrinoid necrosis. The degree of neutrophilia is less and the granular and fractured quality of collagen degeneration is absent in rheumatoid nodules when contrasted with cutaneous extravascular necrotizing granuloma. Other disease processes with prominent neutrophilia also can be confused with cutaneous extravascular necrotizing granuloma. In cases of folliculitis, abscess, or ruptured cyst, the diagnosis generally can be established by reviewing serial histologic sections that show a follicle, sinus tract, or keratin debris. Infectious palisading or necrotic lesions also must be excluded by means of stains or cultures. NeutrophiIic dermatoses, such as Sweet's syndrome, may occasionally be misinterpreted as cutaneous extravascular necrotizing granuloma. However, Sweet's lesions lack the collagen degeneration of cutaneous extravascular necrotizing granuloma, and a palisading pattern is not present. Some cases of Wells' syndrome can be confused with cutaneous extravascular necrotizing granuloma; however, the latter does not have eosinophilic flame figures. The characteristic basophilic collagen degeneration in cutaneous extravascular necrotizing granuloma is associated with leukocytoclasis and fractured collagen, not eosinophilia. When eosinophils are present, they do not predominate. In Wells' syndrome, the flame figures result from many eosinophils and eosinophil granules adhering to collagen bundles. Neutrophilic palisading granulomas manifesting as papulonodular lesions have been described under various other names, as previously noted. 5-1, 20 We are convinced that most represent the same disease as cutaneous extravascular necrotizing granuloma. The cases described by Chu, Connolly, and LeBoit 1 as palisaded neutrophilic and granulomatous dermatiffs are clearly identical. We concur with Finan 25 that patients described with rheumatoid papules had cutaneous extravascular necrotizing granuloma. Patients with rheumatoid papules had leukocytoclastic vasculitis in the same biopsy specimen. 5 Five patients in our series had typical findings of cutaneous extravascular necrotizing granuloma in the same specimen with leukocytoclastic vasculitis. Clinically, these lesions were identical to the others in our series. The disease associations in our five cases included not only rheumatoid arthritis but also chronic lymphocytic leukemia, unclassified systemic vasculitis, streptococcal infection with bloody diarrhea, and Takayasu's arteritis. Our findings demonstrate that leukocytoclastic vasculitis and cutaneous extravascular necrotizing granuloma can occur in patients who do not have rheumatoid arthritis. Rheumatoid neutrophilic dermatitis is described as elevated red plaques and nodules characterized histologically by a neutrophilic infiltrate without collagen alteration, similar to Sweet' s syndrome This entity does appear to be different from cutaneous extravascular necrotizing granuloma. One report of rheumatoid neutrophilic dermatitis, however, appears to represent a cutaneous extravascular necrotizing granuloma.11 Symmetric papular lesions, predominantly on the elbows and hands, can develop in patients with a wide variety of immunoreactive diseases. The histopathologic findings are consistent and unique. The multiple names that have been used for this process have led to confusion, hampering efforts at further clinical study. A unifying nomenclature is necessary. We propose the unifying name cutaneous extravascular necrotizing granuloma of Winkelmann. This name describes the central features of this palisading
7 Journal of the American Academy of Dermatology Volume 34, Number 5, Part 1 Wilmoth and Perniciaro 759 granuloma and recognizes the physician responsible for describing the histopathologic features and recognizing the clinical significance of these lesions. REFERENCES 1. Dicken CH, Winkelmann RK. The Churg-Strauss granuloma: cutaneous, necrotizing, palisading granuloma in vasculitis syndromes. Arch Pathol Lab Med 1978; 102: Churg J, Strauss L. Allergic granulomatosis, allergic angiiris, and periarteritis nodosa. Am J Patho11951 ;27: Finan MC, Winkelmann RK. The cutaneous exlravascular necrotizing granuloma (Churg-Strauss granuloma) and systemic disease: a review of 27 cases. Medicine (Baltimore) 1983;62: Finan MC, Winkelmarm RK. Cutaneous extravascular necrotizing granuloma and lymphocytic lymphoma. Arch Dermatol 1983;119: Smith ML, Jorizzo JL, Semble E, et al. Rheumatoid papules: lesions showing features of vasculiris and palisading granuloma. J AM ACAD DFa~MATOL 1989;20: Higaki Y, Yamashita H, Sato K, eta1 Rheumatoid papules: a report on four patients with histopathologic analysis. J AM ACAD DERMATOL 1993;28: Jorizzo JL, Olansky A J, Stanley RJ. Superficial ulcerating necrobiosis in rheumatoid arthritis: A variant of the necrobiosis lipoidica-rheumatoid nodule specmam? Arch Dermatol 1982;118: Patterson JW, Demos PT. Superficial ulcerating rheumatoid necrobiosis: a perforating rheumatoid nodule. Curls 1985;36: Ackerman AB, Guo Y, Vitale P, et al. Clues to diagnosis in dermatopathology. Vol. 3. Chicago: American Society of Clinical Pathologists Press, 1993: Chu P, Connolly MK, LeBoit PE. The histopathologic spectrum of palisaded neutrophilic and granulomatous dermatitis in patients with collagen vascular disease. Arch Dermatol 1994;130: Lowe L, Komfeld B, Clayman J, et al. Rheumatoid neutrophilic dermatitis. J Cutan Pathol 1992;19: Pemiciaro C, Winkelmann RK. Cutaneous extravascular necrotizing granuloma in a patient with Takayasu's aortitis. Arch Dermatol 1986;122: Strauss L, Churg J, Zak FG. Cutaneous lesions of allergic granulomatosis: a histopathologic study. J Invest Dermatol 1951; 17: Hu CH, O'Loughlin S, Winkelmann RK. Cutaneous man- gestations of Wegener granulomatosis. Arch Dermatol 1977;113: Patten SF, Tomecld KJ. Wegener's granulomatosis: cutaneous and oral mucosal disease. J AM ACAD DERMATOL 1993;28: Frances C, Du LT, Piette JC, et al. Wegener's granulomatosis: dermatological manifestations in 75 cases with clinicopathologic correlation. Arch Dermatol 1994;130: Barksdale SK, Hallahan CW, Kerr GS, et al. Cutaneous pathology in Wegener's granulomatosis: a clinicopathologic study of 75 biopsies in 46 patients. Am J Surg Pathol 1995;19: Daoud MS, Gibson LE, DeRemee RA, et al. Cutaneous Wegener's granulomatosis: cfinical, histopathologic, and immunopathologic features of thirty patients. J AM ACAD DERMATOL 1994;31: Winkelmann RK, Dicken CH. Cutaneous Churg-Strauss granuloma associated with lymphoprolgerative disease. Rev Argent Derrnatol 1980;61: Mader RD, Fabr6 VC, Zax RH, et al. Granulomatous cutaneous vasctditis without systemic manifestations [Abstract]. South Med J 1994;87:$ Winkelmann RK, Connolly SM, Quimby SR, et al. Cutaneous Churg-Strauss syndrome: granuloma annulare-like histology in the spectrum of vasctdiris. Eur J Dermatol 1993 ;3: Dahl MV, Ullman S, Goltz RW. Vasculitis in granuloma annulare: histopathology and direct immunofluorescence. Arch Dermatol 1977;113: Ackerman AB. Histologic diagnosis of inflammatory skin diseases: a method by pattern analysis. Philadelphia: Lea & Febiger, 1978: Ullman S, Dahl MV. Necrobiosis hpoidica: an immunofluorescence study. Arch Dermatol 1977;113: Finan MC. Rheumatoid papule, cutaneous extravascular necrotizing granuloma, and Churg-Strauss granuloma: Are they the same entity? [Letter] J AM ACAD DEI~ATOL 1990;22: Ackerman AB. Histologic diagnosis of inflammatory skin diseases: a method by pattern analysis. Philadelphia: Lea & Febiger, 1978: Scherbenske JM, Benson PM, Lupton GP, et al. Rheumatoid neutrophilic dermatitis. Arch Dermatol 1989;125: Sanchez JL, Cruz A. Rheumatoid neutrophilic dermatitis. J AM ACAD DERMATOL 1990;22:922-5.
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