Cutaneous B-Cell Neoplasms Mimicking Granulomatous Rosacea Or Rhinophyma

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ONLINE FIRST Cutaneous B-Cell Neoplasms Mimicking Granulomatous Rosacea or Rhinophyma

Aviv Barzilai, MD, MSc; Hana Feuerman, MD; Pietro Quaglino, MD; Michael David, MD; Meora Feinmesser, MD; Marisa Halpern, MD; Edit Feldberg, MD; Carlo Tomasini, MD; Hilla Tabibian-Keissar, PhD; Ninette Amarilgio, PhD; Emmilia Hodak, MD

Background: Unlike T-cell neoplasms, B-cell lympho- cutaneous follicular center B-cell lymphoma in 4 cases, proliferative disorders have a limited clinical spectrum primary cutaneous marginal zone lymphoma in 6, and of skin involvement. Cutaneous B-cell neoplasms mim- skin involvement of chronic lymphocytic leukemia in 2. icking rosacea or rhinophyma are rare. All patients had an indolent course as expected for their disease. Observations: We described 12 patients with B-cell lymphoproliferative neoplasms presenting with a facial Conclusions: Cutaneous involvement of B-cell neo- eruption clinically mimicking rosacea or rhinophyma. plasms may mimic granulomatous rosacea or rhino- Eleven patients were women; ages ranged from 36 to 81 phyma. This unusual clinical presentation is more com- years. The clinical presentation included small papules mon in women and appears in the setting of preexisting on the nose and cheeks and around the eyes mimicking rosacea or as a new eruption. Proliferative B-cell disor- granulomatous rosacea; nodules on the nose, cheeks, ders should be added to the differential diagnosis of sym- chin, or forehead mimicking phymatous rosacea; or a metric papular or papulonodular eruptions of the face. combination of both. Three patients had preexisting erythematotelangiectatic rosacea and 1 had rhino- Arch Dermatol. 2012;148(7):824-831. phyma. Based on a clinicopathologic correlation and Published online April 16, 2012. B-cell clonality analysis, the diagnosis was primary doi:10.1001/archdermatol.2011.3575

-CELL NEOPLASMS CAN IN- who were referred to our tertiary dermatology volve the skin as a primary clinics from January 1, 1996, through Decem- cutaneous lymphoma or as ber 31, 2010, for a persistent facial rash. The a secondary process, includ- differential diagnoses included rosacea and ing specific infiltrates of rhinophyma. We retrieved clinical history, clinical findings, laboratory results, and nodal or extranodal lymphoma or leuke- follow-up data from the medical files and B1 mia. When involving the skin, both B- reviewed the biopsy specimens. Final diagno- cell neoplasms, lymphoma and leuke- sis was made according to the criteria of the mia, have a distinct clinical appearance, World Health Organization or the European presenting as isolated, grouped, or mul- Organization for Research and Treatment of tiple erythematous to violaceous pap- Cancer.1 The study was approved by the local ules, plaques, or nodules, usually in an ethics committees. asymmetric distribution. B-cell lymphoproliferative diseases simulating rosacea are RESULTS extremely rare.2-8 In this report, we de- scribe 12 patients who presented with rosacea or rhinophymalike lesions and dis- The patients’ clinical data and final diag- cuss various aspects of this rare clinical noses are described in Table 1. The manifestation of low-grade B-cell lym- study group included 11 women and 1 phoma/leukemia involving the face. man with a mean age of 57 (range, 36-81) years. The time elapsed from the initial presentation to the final diagnosis METHODS varied from a few months to 10 years (mean time, 23 months). The distin- Author Affiliations are listed at We performed a retrospective case analysis of guishing features of the clinical presenta- the end of this article. 12 patients with cutaneous B-cell neoplasms tion included nonpustular granuloma-

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©2012 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/24/2021 Table 1. Clinical Data and Final Diagnosis in Patients With B-Cell Neoplasms Mimicking Rosacea or Rhinophyma

Patient No./ Duration Before Final Sex/Age, y Diagnosis Clinical Presentation Initial Diagnosis Early Therapy Diagnosis 1/F/51 3 y Papulonodular eruption on the Rosacea and rhinophyma Minocycline hydrochloride, PCFCL cheeks; erythematous infiltrated topical metronidazole plaque on the nose 2/F/48 4 mo Erythematous infiltrated plaque on the Rhinophyma None PCFCL nose on top of rosacea 3/F/36 3 y Facial erythematous and skin-colored Rosacea Erythromycin, minocycline PCMZL papules with erythema and telangiectasia 4/F/67 6 mo Nodular eruption on nose, cheeks, Rosacea and rhinophyma Topical clindamycin CLL, leukemia and chin phosphate cutis 5/F/81 3 y Erythematous infiltrated plaque on the Rhinophyma None PCMZL nose 6/F/60 4 mo Erythema on the distal part of the Sebaceous hyperplasia, None PCMZL nose with 3 small nodules basaliomas; granulomatous rosacea 7/F/52 6 mo Small erythematous papules on Granulomatous rosacea None PCMZL cheeks but also on neck, nape, and chest 8/F/57 6 mo Small skin-colored to erythematous Granulomatous rosacea, None PCFCL papules on cheek, sides of the basaliomas, sebaceous nose, eyebrows, helices, and upper hyperplasia back 9/F/36 6 mo Erythematous papules around the Granulomatous rosacea, Liquid nitrogen PCMZL mouth, including the chin and on sarcoidosis, and the nose molluscum 10/M/74 10 y Erythematous infiltrated nodular Rhinophyma Azithromycin, topical CLL, leukemia lesion on the nose metronidazole cutis 11/F/70 1 y Erythematous plaques on the nose Granulomatous rosacea, Topical metronidazole PCMZL and cheeks sarcoidosis 12/F/49 6 mo Erythematous infiltrated plaque on the Granulomatous rosacea Topical metronidazole PCFCL left ala nasi

Abbreviations: CLL, chronic lymphocytic leukemia; PCFCL, primary cutaneous follicular center cell lymphoma; PCMZL, primary cutaneous marginal zone lymphoma.

Figure 1. Erythematous (granulomatous rosacea-like) papules on the right cheek in a patient with primary cutaneous follicular center B-cell lymphoma Figure 2. Rhinophymalike lesion in a patient with primary cutaneous (patient 1). marginal zone lymphoma (patient 11).

tous rosacea-like lesions and rhinophyma/phymatous plaques (Table 1, Figure 1,andFigure 2). Four The histological and immunophenotypical features patients (patients 1-3 and 10) had a history of preexist- of the cases and the results of molecular studies are ing rosacea manifesting as erythematotelangiectatic described in Table 2. Four cases revealed superficial rosacea (in 3 patients) and rhinophyma (in 1 patient) and deep nodular aggregates of centrocytes and centro- (Figure 3). Two of these patients developed rhinophy- blasts, features of follicular-center cell lymphoma malike lymphoma on the nose. Half the patients were (Figure 4). Six cases showed superficial and deep treated for rosacea with topical or systemic antibiotics nodular aggregates of small irregular B lymphocytes, or both, without any benefit (Table 1). some with a monocytoid or plasmacytoid appearance

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©2012 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/24/2021 and residual fragmented germinal centers, features of marginal cell lymphoma (Figure 5). Two cases had diffuse dermal infiltrates of mostly small regular B cells (Figure 6), consistent with skin involvement by chronic lymphocytic leukemia (CLL). Furthermore, in patient 4, results of an IgH rearrangement study showed an identical clone in the blood and skin (Figure 6), establishing the diagnosis of leukemia cutis. Demodex folliculorum was not present in any of the biopsy specimens. Based on a full workup including clinicopathologic correlation and analysis of B-cell clonality, the diagnosis re- tained was primary cutaneous follicular center B-cell lymphoma in 4 of 12 cases (33%), primary cutaneous marginal zone lymphoma in 6 (50%), and skin involvement of CLL in 2 (17%) (Table 2). All the patients had an indolent course as expected for their disease. Initial therapy, which included radiotherapy and/or excisions for 8 patients with Figure 3. Papular/granulomatous rosacea-like lesions on the background of primary cutaneous B-cell lymphoma (PCBCL), led to com- preexisting erythematotelangiectatic rosacea. Small erythematous papules that were determined to be primary cutaneous marginal zone lymphoma plete remission. However, in patients 3 and 8, new le- were found on erythema and telangiectasia (patient 3). This patient had sions developed at sites not previously treated. Intral- papules on both cheeks and also on the submental areas. esional or potent topical corticosteroids applied to these

Table 2. Histological, Immunophenotypical, and Molecular Characteristics of Cases of B-Cell Neoplasms Mimicking Rosacea and Rhinophyma

Histological Features Patient IgH Gene Final No. Architecture Cells Immunophenotype Rearrangement Diagnosis 1 Superficial and deep nodular Small and large (centrocytes, Positive for CD20 and CD10 in germinal center–like ND PCFCL centroblasts) structures; negative for bcl-2 2 Superficial and deep, nodular Small and large, regular and Positive for CD20, bcl-6, and CD10 in follicular Monoclonal PCFCL and diffuse irregular center cells; CD23 in nonfollicular center cells; and CD3 small cells between aggregates 3 Superficial and deep, nodular Small irregular and monocytoid Positive for CD20 and bcl-2 in T cells and marginal Monoclonal PCMZL and diffuse, follicular in marginal areas and areas, bcl-6 and CD10 in germinal centers, and colonization, prominent between germinal centers CD3 in small cells marginal zone 4 Diffuse infiltrate involving the Small regular and slightly Positive for CD20 and CD23; negative for CD5 Same clone in Cutaneous whole dermis, with areas of irregular, prolymphocytes the skin and localization proliferation centers and paraimmunoblasts in peripheral of B-CLL proliferation centers blood 5 Superficial and deep nodular, Irregular small lymphocytes, Positive for CD20 and bcl-2 in the small irregular Monoclonal PCMZL small remnants of germinal also at the periphery of the lymphocytes, bcl-6 in remnants of germinal centers nodules, few plasma cells centers, and CD3 in T cells at the periphery of the nodules; some plasma cells, lambda predominates 6 Superficial and deep nodular Small irregular, some Positive for CD20(ϩϩ) and CD3(ϩ)atthe Monoclonal PCMZL aggregates, few small monocytoid periphery, bcl-2 in small B and T cells, and CD10 germinal centers in germinal centers 7 Superficial and deep nodular, Small irregular cells, plasma Positive for CD20 and bcl-2 in most of the cells, Polyclonal PCMZL residual germinal centers cells bcl-6 and CD10 in residual germinal centers, and CD3 in small T cells 8 Superficial and deep nodular Small and large, regular and Positive for CD20, CD45RA, bcl-6, and CD10 in Monoclonal PCFCL aggregates, focally irregular follicle center cells; bcl-2 in some of the B cells fragmented germinal centers and in T cells; and CD3 9 Diffuse infiltrate involving the Small irregular lymphocytes, Positive for CD20 (approximately 50%) and bcl-2 in Polyclonal PCMZL whole dermis plasmacytoid and plasma B and T cells; negative for bcl-6; many plasma cells cells, lambda predominates 10 Diffuse infiltrate involving the Small and medium lymphoid Positive for CD5, CD20, and bcl-2; negative for bcl-6; Monoclonal Cutaneous deep dermis and cells, reactive T lymphocytes, clonal expression of ␬ light chain localization subcutaneous tissue few histiocytes of B-CLL 11 Nodular infiltrate involving the Small lymphocytes, reactive Negative for CD10; positive for CD20 and bcl-2; a Monoclonal PCMZL whole dermis with a grenz T cells, some histiocytes few bcl-6–positive follicle center cells; no light zone toward the epidermis chain restrictions 12 Nodular infiltrate involving the Small and medium lymphoid Positive for CD20 and bcl-6; negative for CD10; Polyclonal PCFCL whole dermis with a grenz cells, reactive T cells, few no light chain restriction zone toward the epidermis, histiocytes and plasmocytes focally germinal centers

Abbreviations: B-CLL, B-cell chronic lymphocytic leukemia; ND, testing not performed; PCFCL, primary cutaneous follicular center cell lymphoma; PCMZL, primary cutaneous marginal zone lymphoma.

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©2012 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/24/2021 reported in only 7 cases detailed in Table 3. The find- A ings of the present case series of 12 patients with B-cell lymphoproliferative diseases simulating granulomatous rosacea, rhinophyma, or both are comparable to those reports. Likewise, most of our patients were women. However, our patients were somewhat younger than those described in the previous reports (mean age, 57 vs 76 years), making the initial diagnosis of rosacea more plausible. Clinically, all our patients presented with phymatous lesions (mostly rhinophyma), granulomatous rosacea-like lesions, or both. In contrast, all previously described patients who had PCBCL had phymatous lesions.3-7 Three patients described herein and 1 B described previously6 had preexisting rosacea presenting as facial flushing, erythema, and telangiectasia. Therefore, the development of papules or rhinophyma in these patients was considered part of the preexisting rosacea. Two patients described in the literature also had pustules,2,8 and both of them had CLL. In one of those patients, earlier biopsy findings showed polymor- phonuclear leukocytes, which probably represented preexisting rosacea.2 In the other patient, histological features of the pustules were not described. Thus, pustules might have formed secondary to occlusion of the folliculosebaceous unit by the leukemic infiltrate.8 In contrast, none of the patients described herein had a pustular eruption. This unique clinical presentation of B-cell neoplasm involving the skin and simulating rosacea led to a diag- C nosis delay that ranged from months to years. Half the patients in the present series (6 of 12) and most of the patients described in the literature (6 of 7)2-7 had been initially treated with topical or systemic antibiotics for at least a few months without any benefit before a biopsy specimen was obtained. Thus, rosacea and rhinophyma should be added to the list of the unusual manifestations of B-cell neoplasms simulating other skin diseases (Table 4). The clinical differential diagnosis of these lesions does not include only rosacea. For the papular/granulomatous rosacea-like lesions, the differential diagnosis would include mostly adnexal tumors, such as basal cell carcinoma, trichoepithelioma, or sebaceous hyperplasia, and cutaneous sarcoidosis. For the phymatous lesions, granulomatous diseases (in- Figure 4. Histological features of primary cutaneous follicular center B-cell fectious or noninfectious) and T-cell lymphoma should lymphoma (patient 8). A, Superficial and deep nodular aggregates show be considered. irregular lymphoid germinal center–like areas (hematoxylin-eosin, original magnification ϫ20). B and C, The areas are composed of small and large B Fifteen of the 19 total patients (10 in the present se- lymphocytes (hematoxylin-eosin [B] and CD20 [C], original magnification ries and 5 in previously reported cases) had PCBCL, ϫ400). with the marginal zone lymphoma being the most common (10 of 19 patients, including 1 with immunocytoma, currently considered a type of marginal zone small lesions led to complete remission. The cutaneous lymphoma) followed by follicular center cell lymphoma lesions of CLL resolved completely after a course of pred- (5 of 19 patients). In 4 patients, the skin infiltrative le- nisone and chlorambucil therapy in patient 4 and ritux- sions represented leukemia cutis of CLL. In general, pri- imab and radiotherapy in patient 10. Two patients had mary cutaneous marginal zone lymphoma is uncom- only received the diagnosis at the time of this report, and monly located on the face.1 One may therefore speculate follow-up was not available. that chronic antigenic stimulation caused by a resident organism such as D folliculorum leads to the development COMMENT of the lymphoma similar to the relation between Helico- bacter pylori and gastric lymphoma.19 Although we did B-cell lymphoproliferative diseases clinically mimicking not observe Demodex organisms in any of the biopsy speci- rosacea are extremely rare and have been previously mens, such a mechanism is plausible because it would

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C D

Figure 5. Histological features of primary cutaneous marginal zone lymphoma (patient 3). A, Superficial and deep nodular aggregates are seen (hematoxylin-eosin, original magnification ϫ20). B and C, The aggregates show distended marginal zones of monocytoid B cells (hematoxylin-eosin [B] and CD20 [C], original magnification ϫ200). C, The residual germinal center reveals positive staining for CD20 and negative staining for bcl-2. D, The marginal B cells are positive for bcl-2 (original magnification ϫ200).

account for the lymphoma development and the clinical The PCBCLs were treated with excision or radio- presentation.20 Alternatively, similar to descriptions of therapy, as indicated for low-grade PCBCL.22 In con- leukemic infiltrates of CLL localized to the sites of her- trast, skin infiltrates of CLL in which most of the cells pes zoster,14,15 the lymphomatous/leukemic infiltrates are small are related to a favorable prognosis and do not localized to the face may represent the isomorphic require specific therapy.23 However, in cases in which they phenomenon on the sites of a preexisting rosacea/ pose an aesthetic problem, such as those described in the rhinophyma. present series, radiotherapy and even systemic therapy In all 19 reported cases, the diagnosis was based on may be indicated. For small papules and nodules that con- histological and immunophenotypical characteristics, tinue to appear, topical corticosteroids may be the treat- supported in most of the cases by genotypic findings. ment of choice for early lesions. This modality may be Demonstration of a monotypic plasma cell population more practical and accepted from the cosmetic point of or IgH gene rearrangement is crucial for the diagnosis view, probably without affecting the course of the dis- of primary cutaneous marginal zone lymphoma in this ease. Nevertheless, further studies are needed to vali- setting because some cases of rosacea may show dense date this approach, particularly in cases of follicular cen- lymphohistoplasmacytic infiltrate.21 It is also essential ter B-cell lymphoma. to show the identical clone of B cells in the skin infil- In summary, cutaneous involvement by B-cell neo- trate and in the blood in cases of CLL, especially if plasms may mimic rosacea or rhinophyma. This un- the findings for CD5 are negative (as in patient 4) usual clinical presentation is more common in women or when a concomitant B-cell lymphoma has to be and appears in the setting of preexisting rosacea or as a excluded. new eruption. A B-cell proliferative disorder presenting

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C D

Figure 6. Leukemia cutis of chronic lymphocytic leukemia mimicking phymatous rosacea (patient 4). A, Erythematous plaques and nodules on the nose, cheeks, and chin. B, Diffuse lymphocytic infiltrate involving the dermis (hematoxylin-eosin, original magnification ϫ40). C, The infiltrate is composed of small round lymphocytes and larger cells (prolymphocytes and paraimmunoblasts) (hematoxylin-eosin, original magnification ϫ400). D, Results of the IgH study show identical clones (dark filled peaks marked by arrows at 125 kilobase) in the skin biopsy specimen (top) and in the peripheral blood (bottom). The y-axes show peak intensity, measured in arbitrary units; the x-axes show DNA fragment size, measured in kilobases.

Table 3. Reports of B-Cell Neoplasms Mimicking Rosacea or Rhinophyma: Review of the Literature

Patient No./ Sex/Age, y Clinical Presentation/Initial Diagnosis Early Therapy Final Diagnosis Source 1/F/69 Erythematous papules and pustules on the cheeks, Tetracycline hydrochloride CLL Thomson and Cochran,2 forehead, and chin/rosacea 1978 2/F/50 Multiple erythematous infiltrated nodules and plaques Topical metronidazole, PCMZL Colvin et al,3 2003 over face and ears/granulomatous rosacea minocycline (immunocytoma) hydrochloride 3/F/86 Indurated, well-demarcated, erythematous to Topical metronidazole PCFCL Seward et al,4 2004 violaceous nodule extending from the midnasal bridge to the nasal tip/rhinophyma 4/F/83 Erythema and swelling of the nose/rhinophyma (also Minocycline PCMZL Stanway et al,5 2004 nodule on pinna of the ear and nail fold swelling) 5/F/78 Nontender erythematous nodules and plaques at tip of Erythromycin, acyclovir PCMZL Ogden and Coulson,6 nose/rhinophyma sodium 2008 6/F/80 Slightly infiltrated painless erythematous plaque Minocycline PCMZL Rosmaninho et al,7 localized on tip of nose/rhinophyma 2010 7/F/83 Infiltrated nodules and plaques on nose, cheeks, and None CLL Bennett et al,8 2010 periorbitally; papules and pustules; sebaceous hyperplasia; and telangiectasia/rosacea and rhinophyma

Abbreviations: CLL, chronic lymphocytic leukemia; PCFCL, primary cutaneous follicular center cell lymphoma; PCMZL, primary cutaneous marginal zone lymphoma.

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©2012 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/24/2021 Correspondence: Aviv Barzilai, MD, MSc, Department Table 4. Unusual Clinical Manifestations of Cutaneous of Dermatology, Sheba Medical Center, 52621 Tel- B-Cell Neoplasms Hashomer, Israel ([email protected]). Author Contributions: Drs Barzilai, Feuerman, Qua- B-Cell Neoplasm Clinical Appearance Selected Source glino, and Hodak had full access to all the data in the CLL Papules in a Wakelin et al,14 study and take responsibility for the integrity of the dermatomal 1997 data and the accuracy of the data analysis. Study concept distribution (after Claeys et al,15 herpes zoster) 2008 and design: Barzilai, Feuerman, and Hodak. Acquisition CLL Fingertip Freiman et al,16 of data: Barzilai, Feuerman, Quaglino, and Hodak. hypertrophy 2003 Analysis and interpretation of data: Barzilai, Feuerman, MZL/FCC/CLL Rosacea/rhinophyma Present series Quaglino, David, Feinmesser, Halpern, Feldberg, To- Thomson and masini, Tabibian-Keissar, Amarilgio, and Hodak. Draft- Cochran,2 1978 ing of the manuscript: Barzilai. Critical revision of the Colvin et al,3 manuscript for important intellectual content: Barzilai, 2003 Feuerman, Quaglino, David, and Hodak. Administrative, Seward et al,4 technical, and material support: Feinmesser, Tabibian- 2004 Stanway et al,5 Keissar, and Amarilgio. Study supervision: Barzilai and 2004 Hodak. Ogden and Financial Disclosure: None reported. Coulson,6 2008 Rosmaninho et REFERENCES al,7 2010 Bennett et al,8 2010 1. Willemze R, Jaffe ES, Burg G, et al. WHO-EORTC classification for cutaneous FCC/MZL Anetoderma Hodak et al,9 lymphomas. Blood. 2005;105(10):3768-3785. 2010 2. Thomson J, Cochran RE. Chronic lymphatic leukemia presenting as atypical ro- MZL Lipoma Paulli et al,11 sacea with follicular mucinosis. J Cutan Pathol. 1978;5(2):81-87. (subcutaneous) 2010 3. Colvin JH, Lamerson CL, Cualing H, Mutasim DF. Cutaneous lymphoplasmacy- Large B-cell lymphoma Cutaneous horns Dasgupta et al,10 toid lymphoma (immunocytoma) with Waldenstro¨m’s macroglobulinemia mim- 2006 icking rosacea. J Am Acad Dermatol. 2003;49(6):1159-1162. Large B-cell lymphoma, Chronic venous Garbea et al,12 4. Seward JL, Malone JC, Callen JP. Rhinophymalike swelling in an 86-year-old wom- leg type ulcer 2002 an: primary cutaneous B-cell lymphoma of the nose. Arch Dermatol. 2004; Intravascular Livedo reticularis Ro¨glin and 140(6):751-756. lymphoma and livedo Bo¨er,13 2007 5. Stanway A, Rademaker M, Kennedy I, Newman P. Cutaneous B-cell lymphoma vasculitis of nails, pinna and nose treated with chlorambucil. 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Anetoder- mic primary cutaneous B-cell lymphoma: a unique clinicopathological presen- nodular rosacea-like eruptions. tation of lymphoma possibly associated with antiphospholipid antibodies. Arch Dermatol. 2010;146(2):175-182. Accepted for Publication: December 29, 2012. 10. Dasgupta S, Mitra D, Bhattacharya A, Sur PK. B cell lymphoma with unusual clinical cutaneous presentation. J Cancer Res Ther. 2006;2(4):203-205. Published Online: April 16, 2012. doi:10.1001 11. Paulli M, Arcaini L, Lucioni M, et al. Subcutaneous “lipoma-like” B-cell lym- /archdermatol.2011.3575 phoma associated with HCV infection: a new presentation of primary extra- Author Affiliations: Departments of Dermatology (Dr Bar- nodal marginal zone B-cell lymphoma of MALT. Ann Oncol. 2010;21(6):1189- zilai) and Pathology (Drs Barzilai and Tabibian-Keissar) 1195. 12. Garbea A, Dippel E, Hildenbrand R, Bleyl U, Schadendorf D, Goerdt S. 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©2012 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/24/2021 histologic features of mycosis fungoides. J Am Acad Dermatol. 2010;62(2): 22. Senff NJ, Noordijk EM, Kim YH, et al; European Organization for Research and 320-323. Treatment of Cancer; International Society for Cutaneous Lymphoma. 19. Sagaert X, Van Cutsem E, De Hertogh G, Geboes K, Tousseyn T. Gastric MALT European Organization for Research and Treatment of Cancer and Interna- lymphoma: a model of chronic inflammation-induced tumor development. Nat tional Society for Cutaneous Lymphoma consensus recommendations for Rev Gastroenterol Hepatol. 2010;7(6):336-346. the management of cutaneous B-cell lymphomas. Blood. 2008;112(5):1600- 20. Yamasaki K, Gallo RL. The molecular pathology of rosacea. J Dermatol Sci. 2009; 1609. 55(2):77-81. 23. Kaddu S, Smolle J, Cerroni L, Kerl H. Prognostic evaluation of specific cutane- 21. Aroni K, Tsagroni E, Lazaris AC, Patsouris E, Agapitos E. Rosacea: a clinico- ous infiltrates in B-chronic lymphocytic leukemia. J Cutan Pathol. 1996;23 pathological approach. Dermatology. 2004;209(3):177-182. (6):487-494.

Notable Notes

Morbus Europaeus: Europeans Naming Syphilis for Their Enemies

The Spanish physician Rodrigo Ruiz Diaz de Isla attributed the Morbus europaeus was justified because syphilis spread entryofsyphilisinEuropetoChristopherColumbus,whobrought through all of Europe and beyond. Pietro Rostino used the itfromtheNewWorld(1493).1 AfterKingCharlesVIIIconquered term male indiano, referring to the New World; Antonio Sca- the Neapolitan kingdom, the French called syphilis maladie de naroli more precisely used mal d’America; and Francois Xavier Naples or mal napolitain. Interestingly, Italians Luca Ghini and Swediaur used mal de la baia di St Paul.5 Syphilis was named Nicola Massa used the name morbus neapolitanus in the titles of malattia del Portogallo in India because of the undesirable pres- their 2 works, respectively.2 After the battle of Fornovo, with a ence of the Portuguese Vasco de Gama in 1498 and Pedro Al- victory by the Italian League over the French army commanded varez in 1500 and their men. Firanga was the name used in by Charles VIII, syphilis was called male italiano or morbo italico.3 Calcutta, in remembrance of the Carlovingian empire. The Syphilis became the symbol of shame that was used by people Japanese called syphilis mal portoghese as an affront to the Por- to cast aspersion on their enemies. It was named morbo lusitano tuguese and ulcera della Cina or veleno di susino to offend the by the Castilians and mal castigliano by the Lusitans, showing the Chinese. Finally, the Chinese named syphilis ulcera di susino ancient acrimony between them. Castilians also called syphilis or eruzione di Canton, after the first Chinese city where syphi- mal di Galizia, referring to both Catholic kings Isabella of Cas- lis spread.6 Chinese poets compared syphilis to the budding tile and Ferdinand of Aragon. Turks used the name mal dei cris- of a flower without fear of winter, meaning that the appear- tiani, underscoring the never-ending hostility between Turks and ance of syphilis is both abrupt and startling. Christians.Intheearly16thcentury,theDutchandFlemishcalled syphilis morbo spagnolo, in commemoration of the Spanish in- Antonio Tagarelli, MD vasion. Russians used the synonyms mal dei Polacchi and mal Giuseppe Tagarelli, PhD polacco as they expanded into Poland, but the Polish, who did Paolo Lagonia, PhD not insult the Russians, used the synonym mal dei Tedeschi.4 Anna Piro, MD

Author Affiliations: National Research Council of Italy, Institute of Neurological Sciences, Mangone, Cosenza, Italy. Contact Dr A. Tagarelli at the National Research Council of Italy, Institute of Neurological Sciences, Contrade Burga, Man- gone, Cosenza 87050, Italy ([email protected]).

1. Diaz de Isla R, ed. Tractado llamado fructo de todos los santos contra el mal serpentine venido de la isla Espanola hecho y ordenado en el grande y famoso hospital de todos los santos. Seville, Spain: A Burgos; 1539. 2. Astruc J, ed. De morbis venereis libri sex. In quibus disseritur tum de origine, propagatione & contagione horumce affectuum in genere: tùm de singulorum naturà, aetiologiaˆ & therapeiaˆ, cum brevi analisi & epicrisi operum plerorumque quae de eodem argomento scripta sunt. Paris, France: G Cavelier; 1736. 3. Rondelet G, ed. Methodus curandorum omnium morbum corpis humani. De morbo gallico. Paris, France: C Maceo; 1754. 4. Pernotti di Cigliano P, ed. Storia generale e ragionata dell’origine, dell’essenza e specifica dell’infezione venerea. Turin, Italy: Stampa Reale; 1788. 5. Swediaur F, ed. Traite´ complet sur les symptomes, les effets, la nature et le traitment des maladies syphilitiques. Paris, France: Cellot; 1817. 6. Wang N, ed. Dermatologia in medicina tradizionale cinese. Milan, Italy: Ambrosiana; 1997.

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