Clinicopathologic Evaluation of Nodular Cutaneous Lesions of Behçet Syndrome
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1 Anatomic Pathology / NODULAR CUTANEOUS LESIONS OF BEHÇET SYNDROME Clinicopathologic Evaluation of Nodular Cutaneous Lesions of Behçet Syndrome Cuyan Demirkesen, MD, 1 Nükhet Tüzüner, MD, 1 Cem Mat, MD, 2 Mustafa Senocak, PhD, 3 Nesimi Büyükbabani, MD, 5 Yalçin Tüzün, MD, 2 and Hasan Yazici, MD 4 Key Words: Behçet syndrome; Erythema nodosum-like lesions; Skin; Histopathology Abstract Among the cutaneous manifestations, nodular lesions are rather common in Behçet syndrome. The histologic nature of these lesions has been a matter of controversy. To establish their distinguishing features, biopsy specimens from nodular lesions of 24 patients with Behçet syndrome, 25 with nodular vasculitis (NV), and 20 with erythema nodosum (EN) were compared. Statistical analysis revealed insignificant differences between most of the histologic features of Behçet syndrome and NV. However, neutrophil-predominating infiltrate in the subcutis was more common in Behçet syndrome, while necrosis and granuloma formation were encountered more frequently in NV. The differences between Behçet syndrome and EN were more significant. Septal panniculitis, lymphocytepredominating infiltrate, absence of many vascular changes as well as vasculitis, and necrosis were features in favor of EN. Nodular lesions of Behçet syndrome are mainly neutrophilic vascular reactions with histologic features similar to NV but significantly differing from EN associated with other systemic diseases. Nodular lesions at the lower extremities are frequently encountered in Behçet syndrome. Reports about their histologic features have been conflicting. 1-6 Some authors indicated these lesions resembled erythema nodosum (EN), 1 while others have reported findings of neutrophilic vasculitis and pointed out that septal or lobular panniculitis, granuloma formation, and necrosis were secondary to vasculitis. 2-6 In the present study, we attempted to evaluate the histologic features of these lesions in a blinded manner with control groups composed of nodular vasculitis (NV) and EN. Materials and Methods Nodular lesions of 24 patients with Behçet syndrome, 20 with EN, and 25 with NV were compared. Biopsy specimens of the nodular lesions of Behçet syndrome were obtained from 36 volunteer patients who fulfilled the criteria for complete Behçet syndrome and attended a dedicated Behçet syndrome outpatient clinic in Cerrahpasa Medical Faculty, Istanbul, Turkey. Seven of these biopsy specimens were unsuitable for histologic evaluation. Moreover, 5 patients with Behçet syndrome with nodular lesions due to superficial thrombophlebitis were excluded. For comparison, histologic specimens of 17 consecutive volunteer patients with EN and 19 with NV attending a dedicated dermal vasculitis outpatient clinic, whose diagnoses had been established both clinically and by histologic examination, were selected. In addition, the pathologic slides of representative cases of 3 EN and 6 NV were selected from the archives of our pathology department by one of the pathologists (C.D.). Of the total biopsies, 25 were punch biopsy, 0.6 cm in width, and 44 were excisional biopsies. American Society of Clinical Pathologists Am J Clin Pathol 2001;116:
2 Demirkesen et al / NODULAR CUTANEOUS LESIONS OF BEHÇET SYNDROME A checklist of histologic parameters Table 1 was prepared by one of the pathologists (C.D.). Among these parameters, the type of panniculitis (septal, lobular, or mixed), the nature of the inflammatory cells and their ratio in subcutis, vascular changes, necrosis, necrobiosis, and granuloma formation were assessed. When the number of neutrophils was greater than the number of mononuclear inflammatory cells, mostly lymphocytes, the infiltrate was named as neutrophil (PNL) predominating or vice versa. Vascular changes such as fibrinoid material and the inflammatory cells in the vessel wall, leukocytoclasia, endothelial swelling, extravasated erythrocytes, microthrombi, perivascular PNL, and lymphocytic infiltration were sought specifically. The presence of the inflammatory cells within and around the vessel wall, with or without the deposition of fibrinoid material, was defined as vasculitis. The term neutrophilic vasculitis was used when the inflammatory cells were mainly neutrophils. Biopsy sequences were coded and interpreted, masked to the diagnostic groups, by an experienced pathologist (N.T., first observer) and a dermatopathologist (N.B., second observer). To quantitate the interobserver variation in assessing the 20 different histologic parameters, we first calculated a frequency figure of a specific histologic parameter (ie, leukocytoclasia) observed by either observer in each disease category. The denominator of this frequency figure was the total number of histologic specimens in that disease category (Table 1). Following this, a paired t test was done (2-tailed, 59 df) to assess whether the frequency of the observations of one observer for a specific histologic parameter differed significantly from that of the other across all 3 disease categories (n = 60). The P values thus derived are somewhat approximate and are likely to be slightly lower than true values in that the histologic parameters measured were not strictly independent of each other. Because there was no appreciable interobserver variation (see the Results section), we then calculated a mean frequency for each histologic parameter (n = 20) for each disease category. This mean frequency was arrived at by expressing the average of the 2 observers counts as a fraction of the total number of histologic specimens for a particular disease category. This was followed by calculating a paired t test (2-tailed, 19 df) between each disease category, testing whether there was a significant difference in the frequency of the histologic parameters in question between the 3 disease categories. The frequency of each histologic parameter for each disease category also was compared by constructing frequency distribution graphs Figure 1 and Figure 2. Finally, a multivariate logistic regression test was done to check whether any of these parameters could be considered diagnostic for Behçet syndrome. Table 1 Histologic Features of Behçet Syndrome, Nodular Vasculitis, and Erythema Nodosum According to Two Observers Behçet Syndrome (n = 24) Nodular Vasculitis (n = 25) Erythema Nodosum (n = 20) Observer Observer Observer Histologic Parameter 1 2 MF 1 2 MF 1 2 MF Type of panniculitis Septal Lobular Mixed Inflammatory cell infiltrate PNL predominating Lymph predominating Vascular changes AV involvement Involvement of A Involvement of V Fibrinoid material in vessel wall Inflammatory cells in vessel wall Leukocytoclasia Endothelial swelling Extravasated erythrocytes Microthrombi Perivascular PNL Perivascular lymph Vasculitis Necrosis Necrobiosis Granuloma A, small and medium-sized arteries; AV, arterioles and venules; lymph, lymphocytes; MF, mean frequency; PNL, neutrophils; V, small and medium-sized veins. 342 Am J Clin Pathol 2001;116: American Society of Clinical Pathologists
3 Anatomic Pathology / ORIGINAL ARTICLE BS NV EN BS-NV BS-EN NV-EN Mean Frequency Results S L M PNL LY AV A V FIBR INF LEU END EX MIC P-PNL P-LY VAS NEC NECB GRA Figure 1 Feature frequencies in Behçet syndrome (BS), nodular vasculitis (NV), and erythema nodosum (EN). A, small or medium-sized artery involvement; AV, arterioles and venules; END, endothelial swelling; EX, extravasated erythrocytes; FIBR, fibrinoid material in the vessel wall; GRA, granuloma; INF, inflammatory cells in the vessel wall; L, lobular panniculitis; LEU, leukocytoclasia; LY, lymphocytepredominating cell infiltrate in subcutis; M, mixed panniculitis; MIC, microthrombi; NEC, necrosis; NECB, necrobiosis; P-LY, perivascular lymphocytes; PNL, neutrophilpredominating cell infiltrate in subcutis; P-PNL, perivascular neutrophils; S, septal panniculitis; V, small or medium-sized vein involvement; VAS, vasculitis. Clinical Findings Of 24 patients with Behçet syndrome included in this study, 17 were male and 7 were female (mean ± SD age, 30.4 ± 8.6 years). Twenty patients with EN (2 male, 18 female (mean ± SD age, 40.8 ± 12.7 years) and 25 with NV (9 male, 16 female; mean ± SD age, 47.8 ± 11.7 years) constituted the control group. The duration of the nodular lesions with these 3 diagnoses (data available for most patients) varied from 1 to 14 days with an average of 6 days. The location of the nodules was the lower extremities, except for 1 case of EN in which the nodules were on the upper and lower extremities. Thirteen patients with Behçet syndrome, 12 patients with NV, and all patients with EN had multiple nodules. The number of patients with more than 3 nodules were 8 in Behçet syndrome, 7 in NV, and all 20 in EN. Histologic Findings The histologic features of the nodular lesions of patients with Behçet syndrome, EN, and NV, read by the 2 observers, as well as the mean frequencies are seen in Table 1. Mean Frequency S L M PNL LY AV A V FIBR INF LEU END Mixed panniculitis (both septal and lobular) was the most common type of panniculitis in all 3 diseases. In addition, septal panniculitis was observed occasionally in EN. In most cases of NV and EN, the inflammatory cell infiltration was composed mainly of lymphocytes in the subcutis, while a neutrophil-predominating infiltrate was a more common feature in Behçet syndrome compared with EN and NV. This feature was observed in half of the patients with Behçet syndrome Image 1 and Image 2. Histologic changes of neutrophilic vasculitis were detected both in NV (32% [8/25]) and in Behçet syndrome (first observer, 42% [10/24]; second observer, 46% [11/24]), whereas no vasculitis was noted in EN Image 3, Image 4, and Image 5. The involved vessels were mostly arterioles and venules in all 3 diseases. However, the involvement of small and medium-sized arteries was more common in NV and never seen in EN. On the other hand, the involvement of veins was detected more often in Behçet syndrome. Granuloma formation, necrosis, and necrobiosis were more frequent findings in NV than in EN and Behçet syndrome. There was no significant interobserver variation in the frequency with which various histologic features were observed (t = 0.87; P =.39) (Table 1). EX MIC P-PNL VAS P-LY NEC NECB GRA Figure 2 Differences in feature frequencies in Behçet syndrome vs nodular vasculitis (BS-NV), Behçet syndrome vs erythema nodosum (BS-EN), and nodular vasculitis vs erythema nodosum (NV-EN). A, small or medium-sized artery involvement; AV, arterioles and venules; END, endothelial swelling; EX, extravasated erythrocytes; FIBR, fibrinoid material in the vessel wall; GRA, granuloma; INF, inflammatory cells in the vessel wall; L, lobular panniculitis; LEU, leukocytoclasia; LY, lymphocyte-predominating cell infiltrate in subcutis; M, mixed panniculitis; MIC, microthrombi; NEC, necrosis; NECB, necrobiosis; P-LY, perivascular lymphocytes; PNL, neutrophil-predominating cell infiltrate in subcutis; P-PNL, perivascular neutrophils; S, septal panniculitis; V, small or medium-sized vein involvement; VAS, vasculitis. American Society of Clinical Pathologists Am J Clin Pathol 2001;116:
4 Demirkesen et al / NODULAR CUTANEOUS LESIONS OF BEHÇET SYNDROME Image 1 Behçet syndrome. Neutrophil-predominating cell infiltrate in subcutis (H&E, 400). Inset, Necrobiosis (H&E, 400). In the paired t tests done on the frequencies of the 20 histologic parameters taken as a group in Behçet syndrome vs NV, Behçet syndrome vs EN, and NV versus EN, there was no difference between Behçet syndrome and NV (t = 0.62; P =.54). However, there were significant differences between Behçet syndrome and EN (t = 3.14; P =.005) and between NV and EN (t = 3.56; P =.002), showing that the histologic findings in EN differed in general from those found in Behçet syndrome or in NV. None of the histologic parameters mentioned in Table 1 was found individually diagnostic for any of these 3 diseases Image 2 Lymphocyte-predominating inflammatory cell infiltrate in the subcutis in Behçet syndrome (H&E, 400). using the multivariate logistic regression test. However, when the mean frequencies for each pair of diseases were considered (Figure 1, Figure 2), the histologic parameters somewhat favoring each disease could be observed Table 2. Discussion Many of the reports indicated the common underlying pathology of Behçet syndrome is vasculitis, although histologic confirmation is not always possible. 2-4 Some authors Image 3 Lobular panniculitis, as well as the deposition of fibrinoid material within the vessel wall of arterioles and venules in Behçet syndrome (H&E, 200). Image 4 In the arterioles, the presence of fibrinoid material and inflammatory cells within the vessel wall in Behçet syndrome (H&E, 400). 344 Am J Clin Pathol 2001;116: American Society of Clinical Pathologists
5 Anatomic Pathology / ORIGINAL ARTICLE Image 5 Neutrophilic vasculitis in a small artery in Behçet syndrome (H&E, 400). postulated that the nonspecific skin reactivity response (pathergy reaction) has the main role in the pathogenesis of the cutaneous lesions. 7 Kim and LeBoit 2 noted vasculitis in all 11 sections of EN-like lesions of Behçet syndrome in their series. They mentioned that lymphocytic vasculitis was evident in 8 specimens, leukocytoclastic vasculitis in 4, and pustular vasculitis in 1. Moreover, vascular changes reminiscent of polyarteritis nodosa were documented in other studies. 3,6 On the other hand, Chun et al 1 detected lymphocytic vasculitis in 40% (12/30) of their cases and indicated it was a spilling phenomenon rather than a primary Table 2 Histologic Parameters Potentially Useful for the Differential Diagnosis of Behçet Syndrome, Nodular Vasculitis, and Erythema Nodosum Behçet Nodular Erythema Syndrome Vasculitis Nodosum Septal panniculitis ± + Lobular panniculitis + + ± Neutrophil-predominating infiltrate Lymphocyte-predominating infiltrate Involvement of arteries + ++ Involvement of veins Fibrinoid material in the vessel wall Leukocytoclasia Microthrombi ++ + Vasculitis Necrosis + ++ Necrobiosis Granuloma , absent; ±, very rare; +, sometimes; ++, frequently. vasculitis. In addition, in some other studies, the vascular changes in cutaneous lesions of Behçet syndrome were found to be mild or absent. 8,9 In the present study, differing from the previous studies, disease features were interpreted by 2 observers in a blinded manner, and histologic specimens from 2 disease control groups, NV and EN, were used. These 2 conditions, we reasoned, had clinical and histologic features that could easily be confused with those observed in Behçet syndrome, hence constituting suitable control groups for a specificity study. In the present study, neutrophilic vasculitis was noted in 42% (10/24, first observer) and 46% (11/24, second observer) of nodular lesions in Behçet syndrome. A neutrophil-predominating inflammatory cell infiltrate also was a statistically important parameter in favor of Behçet syndrome compared with NV and EN. This finding supports the earlier observations by Jorizzo et al 3 and Nazzaro 4 that EN-like lesions of Behçet syndrome are neutrophilic vascular reactions, as are papulopustular and pathergy lesions. Other authors have indicated that some lesions in their series were noted to contain a perivascular mononuclear cell infiltrate. 1,2,9 In the present study, 29% (7/24, first observer) and 42% (10/24, second observer) of cases of Behçet syndrome demonstrated lymphocyte-predominating cell infiltrate (Image 2). It can be speculated that the lymphocyte-predominating reaction might be following in time, a neutrophilic vascular reaction during the evolution of these lesions, as proposed by Jorizzo et al 3 for pustular lesions of Behçet syndrome. However, our data with a limited number of cases did not confirm this hypothesis when the duration of the lesions was considered. But still, it should be sought out in larger series. Although the diagnosis of Behçet syndrome usually is not established on the basis of histologic features detected in nodular lesions, we wanted to find out if there were any distinguishing features from other common types of panniculitis, EN and NV (Table 2). The statistical analyses of the histologic features seen in Behçet syndrome vs those found in EN established that the histologic features of Behçet syndrome differed significantly from those of EN. Septal panniculitis, lymphocyte-predominating infiltrate in the subcutis, and absence of vasculitis were in favor of EN. Necrobiosis was another helpful feature in the differential diagnosis of Behçet syndrome and EN, in favor of Behçet syndrome. In contrast, histologic features of the nodular lesions in Behçet syndrome vs those found in NV showed no differences. However, a lymphocyte-predominating infiltrate in the subcutis, necrosis, and granuloma formation were features seen more commonly in NV. Finally, as expected from the direction of the precious discussion, the histologic features of NV also differed significantly from those found in EN. American Society of Clinical Pathologists Am J Clin Pathol 2001;116:
6 Demirkesen et al / NODULAR CUTANEOUS LESIONS OF BEHÇET SYNDROME Conclusion EN-like lesions of Behçet syndrome are mainly neutrophilic vascular reactions with accompanying changes in subcutis. Their histologic features are more akin to NV than to EN. This, in turn, suggests that these nodular lesions of Behçet syndrome may indeed be due to vasculitis. On the other hand, the histologic features of these nodular lesions have enough specificity to differentiate them from EN associated with other diseases. From the Departments of 1 Pathology, 2 Dermatology, 3 Biostatistics, and 4 Internal Medicine, Division of Romatology, Cerrahpasa Medical Faculty, University of Istanbul; and 5 Pathology, Istanbul Medical Faculty, University of Istanbul, Istanbul, Turkey. Supported by TÜBITAK (Turkish Scientific and Technical Research Council) SBAG-Ü-16/7, Ankara, Turkey. Address reprint requests to Dr Demirkesen: Eminalipasa Cad. No 1, Köknar sok, Dumankaya Sit. D Blok D 10, Altintepe, Istanbul, Turkiye. Acknowledgment: We thank Ethem Erginöz, MD, for contributions and Banu Sener for skillful technical assistance. References 1. Chun SI, Su WPD, Lee S, et al. Erythema nodosum-like lesions in Behçet s syndrome: a histopathologic study of 30 cases. J Cutan Pathol. 1989;16: Kim BS, LeBoit PE. Erythema nodosum-like lesions in Behçet s disease: is vasculitis the main pathological feature [abstract]? J Cutan Pathol. 1998;25: Jorizzo JL, Abernethy JL, White WL, et al. Mucocutaneous criteria for the diagnosis of Behçet s disease: an analysis of clinicopathologic data from multiple international centers. J Am Acad Dermatol. 1995;32: Nazzaro P. Cutaneous manifestations of Behçet s disease. In: Monacelli M, Nazzaro P, eds. International Symposium on Behçet s Disease in Rome. Basel, Switzerland: Karger; 1966: Magro CM, Crowson AN. Cutaneous manifestations of Behçet s disease. Int J Dermatol. 1995;34: Liao YH, Hsiao GH, Hsiao CH. Behçet s disease with cutaneous changes resembling polyarteritis nodosa. Br J Dermatol. 1999;140: Gül A, Esin S, Dilten N, et al. Immunohistology of skin pathergy reaction in Behçet s Disease. Br J Dermatol. 1995;132: Chun SI, Su WP, Lee S. Histopathologic study of cutaneous lesions in Behçet s syndrome. J Dermatol. 1990;17: Gilhar A, Winterstein G, Turani H, et al. Skin hyperreactivity response (pathergy) in Behçet s disease. J Am Acad Dermatol. 1989;21: Am J Clin Pathol 2001;116: American Society of Clinical Pathologists
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