Hypopigmented parapsoriasis en plaque, a new, overlooked member of the parapsoriasis family: A report of 34 patients and a 7-year experience
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1 Hypopigmented parapsoriasis en plaque, a new, overlooked member of the parapsoriasis family: A report of 34 patients and a 7-year experience Mohammad A. El-Darouti, MD, Marwa M. Fawzy, MD, Rehab A. Hegazy, MD, and Rania M. Abdel Hay, MD Cairo, Egypt Background: In the past 7 years we have extensively studied an uncommon hypopigmented disorder that, apart from hypopigmentation, showed many common features with parapsoriasis en plaque (PSEP), both clinically and histopathologically. Objective: We sought to verify whether this disorder should be considered a hypopigmented variant of PSEP and thus be referred to as hypopigmented PSEP. Methods: A total of 34 patients presenting with this peculiar hypopigmented disorder were included ( ). Patients were subjected to a predesigned algorithm excluding all possible differential diagnoses of hypopigmented lesions. Results: Our findings indicated that this disorder can be diagnosed as hypopigmented PSEP. These findings included: (1) exclusion of all other disorders causing similar hypopigmented lesions; (2) shape and size of the lesions being very similar to those of classic small PSEP (small-plaque parapsoriasis [SPP]); (3) similar distribution of the lesions (trunk, proximal upper and lower limbs) to the classic PSEP; (4) digitiform extensions of most the lesions (70.5% of our patients) as in SPP; (5) absence of itching as in PSEP (SPP type); (6) good response to narrowband ultraviolet B in 76.4% of the patients (n = 26); and (7) during follow-up 5 patients (14.7%) converted into hypopigmentd mycosis fungoides. Limitations: A limitation in our study is that we did not perform clonal T-cell receptor gene rearrangement because of limited resources. Conclusion: Based on our findings we believe that this hypopigmented disorder is a well-defined new variant of the PSEP family that shows, apart from the hypopigmentation, all the features of PSEP, particularly the SPP variant, and accordingly could be referred to as hypopigmented PSEP. ( J Am Acad Dermatol 2012;67: ) Key words: digitiform extensions; follow-up; hypopigmented; mycosis fungoides; parapsoriasis en plaque; phototherapy. Parapsoriasis en plaque (PSEP) is a chronic dermatosis whose biological distinction from early mycosis fungoides (MF) is still not clearly defined. Two types of parapsoriasis have been delineated: large-plaque parapsoriasis (LPP) and small-plaque parapsoriasis (SPP). 1 Abbreviations used: LPP: large-plaque parapsoriasis MF: mycosis fungoides PSEP: parapsoriasis en plaque SPP: small-plaque parapsoriasis From the Dermatology Department, Faculty of Medicine, Cairo University. Funding sources: None. Conflicts of interest: None declared. Accepted for publication February 24, Reprints not available from the authors. Correspondence to: Rania M. Abdel Hay, MD, 13th Abrag Othman, kornish El Maadi, Cairo, Egypt omleila2@yahoo. com. Published online March 29, /$36.00 Ó 2012 by the American Academy of Dermatology, Inc. doi: /j.jaad
2 JAM ACAD DERMATOL VOLUME 67, NUMBER 6 El-Darouti et al 1183 CAPSULE SUMMARY LPP presents as large, flat, red or brown patches, generally greater than 6 cm in diameter, whereas the lesions of SPP are well-circumscribed round or oval pink patches, slightly scaly, less than 5 cm in diameter, and frequently show digitate extensions. Lesions mainly occur over the trunk and proximal extremities. Histopathologically LPP shows a papillary dermal inflammatory infiltrate formed by numerous lymphocytes that might assume a bandlike pattern. In some cases single lymphocytes can be observed in the epidermis in the absence of spongiosis, whereas SPP shows nonspecific changes that may be similar to those of a mild eczema, including spongiosis, exocytosis of small lymphocytes, and a papillary dermal perivascular inflammatory infiltrate. 2 Data on progression rates to MF are conflicting, ranging from 0% to 46%. 3 In the past 7 years we have extensively studied an uncommon hypopigmented disorder that, apart from hypopigmentation, showed many common features with small PSEP both clinically and histopathologically. Accordingly this study was performed to answer the following questions: (1) Should this disorder be considered a variant of PSEP and should it be referred to as hypopigmented PSEP? (2) Can hypopigmented PSEP progress to hypopigmented MF in the same way as classic PSEP can proceed to classic MF? METHODS The study was performed according to the regulations approved by the Dermatology Research Ethics Committee Office, Faculty of Medicine, Cairo University. A total of 34 patients from the outpatient dermatology clinic in Cairo University Hospital presenting with this peculiar hypopigmented disorder were included in our study, from May 2003 until February A written informed consent was obtained from every patient regarding participation, biopsy, and photography. All patients were subjected to a predesigned algorithm to exclude all possible differential diagnoses of hypopigmented lesions including hypopigmented MF, pityriasis alba, pityriasis versicolor, postinflammatory hypopigmentation, sarcoidosis, d d d Two types of parapsoriasis have been delineated: large-plaque parapsoriasis and small-plaque parapsoriasis. The current study presented a welldelineated hypopigmented disorder that could be considered a new variant of the parapsoriasis family that shows, apart from the hypopigmentation, all the features of parapsoriasis en plaque particularly the small parapsoriasis en plaque variant. As small parapsoriasis en plaque can progress to mycosis fungoides, awareness of this entity is required when examining patients with idiopathic hypopigmented macular eruption. tuberculoid leprosy, syphilis, 4 progressive macular hypopigmentation, 5 and other systemic causes of hypopigmentation. 6 This algorithm included the following. (1) History taking included age and sex of the patient; onset, course, and duration of the disease; associated or previous diseases; and exposure to chemicals that would have been followed by hypopigmentation. (2) General and dermatologic examination of patients documented general health and skin phototype. Regarding the hypopigmented disorder, the number, sites, size, shapee including presence of digitiform extensionseand color of the lesions and the presence of associated atrophy, scaling, or poikiloderma were reported. Wood light examination was performed for all patients to exclude progressive macular hypopigmentation (red fluorescence). (3) Laboratory investigations were done to exclude any associated disorders such as hypothyroidism, pernicious anemia, syphilis, and kala azar. (4) Histopathological examination was performed on two biopsy specimens taken from two different lesions of every patient, stained by hematoxylin and eosin. The histopathological examination was performed by two blinded qualified dermatopathologists. (5) Serial sections from the previously taken biopsy specimens were studied by immunohistochemical staining for CD3, CD4, CD7, CD8, and S100 protein. All included patients were off any systemic or topical treatment apart from emollients for a period of 2 weeks before taking biopsy specimens. Statistical analysis Data were coded and entered using software (Statistical Package for Social Science [SPSS] Version 17, SPSS Inc, Chicago, IL). Data were summarized using mean 6 SD for quantitative variables and percentages for qualitative variables. RESULTS The current study included 34 patients, 22 male (64.7%) and 12 female (35.3%); their age ranged between 12 and 43 years (mean 6 SD years) and the disease duration ranged between
3 1184 El-Darouti et al JAM ACAD DERMATOL DECEMBER 2012 Fig 1. Hypopigmented parapsoriasis. A, Case presented with small macules. B, Another case presented with large patches. C, Third case presented with apparent digitiform extension of most of lesions (fingerlike projections). 5 months and 3 years (mean 6 SD months). Clinically, all patients presented with multiple oval to round persistent and/or progressive hypopigmented patches that were present mainly on the chest, back, and proximal upper and lower limbs, ie, showing a nonsun-exposed distribution. Extension to the face and forearm was seen in 6 patients (17.6%) (in such patients lesions started on the trunk before extending to the face and forearm). The lesions presented as small macules (\2 cm) in 73.5% of the patients (n = 25) (Fig 1, A) oraslarge patches ( $ 6 cm in the longest axis) in 26.5% of the patients (n = 9) (Fig 1, B). Uniformity was evident in 59% of the patients (n = 20). An important clinical feature was the digitiform extension of most of the lesions (fingerlike projections detected in 24 of 34 patients [70.5%]) (Fig 1, C ). Apart from hypopigmentation and occasional mild scaliness, erythematous hue, atrophy, poikiloderma, and itching were not encountered in any of our patients. Histopathologically, all biopsy specimens showed similar findings of mild epidermal hyperplasia, reduced basal pigmentation, and decreased number of melanocytes at the base of the epidermis. Focal parakeratosis, foci of mild spongiosis, and focal exocytosis were encountered in the majority of the included cases (n = 32, 94.1%). The dermis showed scanty superficial perivascular infiltrate of lymphocytes and histiocytes with frequent extension into the papillary dermis. There were no interface changes or atypical lymphoid cells in any of the examined biopsy specimens (Fig 2, A). Immunohistochemical staining showed universal CD3 immunopositivity. CD8 1 T cells predominance over CD4 1 T cells was reported in the majority of cases (88.2%), n = 30. None of our cases showed fewer then 10% CD7 1 T cells. S100 immunostaining showed a reduction of basal pigmentation and of the number of melanocytes between affected and unaffected skin (Fig 2, B and C ). Follow-up The follow-up period extended for up to 2 years for patients who completed the study (31 patients). All patients were kept on phototherapeutic treatment of narrowband ultraviolet B, 3 times weekly. In all, 26 of 34 (76.4%) patients showed complete clearance of their lesions in a duration ranging between 10 to 25 weeks ( weeks). The cumulative dose ranged between and 42 J/cm 2 ( J/cm 2 ). Five patients (14.7%) while on narrowband ultraviolet B therapy developed hypopigmented MF. Development of MF was suspected clinically by observing enlargement of lesion size,
4 JAM ACAD DERMATOL VOLUME 67, NUMBER 6 El-Darouti et al 1185 Fig 2. A, Hypopigmented parapsoriasis with focal loss of pigment at base of epidermis, few lymphocytes arranged focally at lower border of epidermis and scanty superficial perivascular lymphohistiocytic infiltrate. B, Photomicrograph showing S100 immunostaining of normalappearing skin from patient with hypopigmented parapsoriasis showing average number of melanocytes. C, Photomicrograph showing S100 immunostaining of hypopigmented lesion from same patient showing marked decrease of melanocytes. appearance of erythema, scaling, and itching. The diagnosis of MF was confirmed histologically through detection of epidermotropism, haloed lymphocytes in the basal layer of the epidermis, epidermal lymphocytes larger than those of the dermis, fibrosis in the papillary dermis, and the presence of atypical lymphocytes and immunohistochemically through detecting depletion of CD7 1 T cells (\10%). Three patients (8.82%) were lost during the followup period. Accordingly the diagnosis of hypopigmented PSEP was based on the following findings: (1) exclusion of all other disorders causing similar hypopigmented lesions (Table I); (2) shape and
5 1186 El-Darouti et al JAM ACAD DERMATOL DECEMBER 2012 Table I. Differential diagnosis of hypopigmented lesions and exclusion clues DD Acromia paresthetica Progressive macular hypomelanosis of trunk Indeterminate leprosy Postinflammatory hypopigmentation Pityriasis alba Hypopigmented MF Exclusion criteria Follows tinea versicolor Clinically it affects trunk only, shows no digitate pattern and may show confluence in center Microscopically: intrafollicular bacteria (Propionibacterium acnes) with perifollicular infiltrate Widespread lesions should happen only in clinical setting of LL Other features of LL should be obvious Preceded by well-delineated inflammatory disorders such as psoriasis or pityriasis rosea Affects mainly exposed areas (face, forearms) and is usually associated with atopic dermatitis; it is more common in children (rare in adults) Lesions are in bathing suit area; lesion size [6 mm, with no digitate forms; atrophy, poikiloderma, erythema, scaling, and pruritus are present in some cases Pathologically: epidermotropism, atypical lymphocytes; more dense superficial perivascular infiltrate 7 DD, Differential diagnosis; LL, lepromatous leprosy; MF, mycosis fungoides. size of the lesions that was very similar to those of the classic small PSEP; (3) development of the lesions on the trunk, proximal upper and lower limbs occurring in the same sites as the classic small PSEP; (4) digitiform extensions in 70.5% of our patients as in small PSEP; (5) absence of itching as in PSEP (SPP type); (6) good response to narrowband ultraviolet B in 76.4% of the patients (n = 26) (see below); (7) during follow-up 5 of the patients (14.7%) converted into hypopigmented MF. DISCUSSION The current study presented 34 patients with a well-delineated hypopigmented disorder that could be considered a new variant of the parapsoriasis family. We choose to call it hypopigmented parapsoriasis en plaque. The evidence on which such a diagnosis was made was based on two important findings. First is exclusion of all other possible disorders that present with hypopigmented lesions 4-6 through an extensive workup including clinical, histopathological, and immunohistochemical studies (Table I). Second are the similar features detected during the current work connecting this disorder to the classic types of the PSEP family (Table II). It is noteworthy that the digitate extension of the hypopigmented lesions documented in 70.5% (n = 24) of our cases is an important characteristic feature of the classic small PSEP, so much so that small PSEP is known as the digitate dermatosis. 7 The absence of pruritus, atrophy, and poikiloderma in our patients is further proof that the hypopigmented variant of PSEP belongs to the small type of parapsoriasis (SPP) that represents the benign end of the parapsoriasis spectrum. It is known that the largeplaque type (LPP) in contrast to the small type might be associated with mild pruritus, poikiloderma, and scaling. 8 The histopathological findings in the majority of our cases (n = 32, 94.1%) included mild epidermal hyperplasia, focal parakeratosis, mild spongiosis, and exocytosis. Moreover, all our cases showed superficial perivascular infiltrate of lymphocytes, and occasional histiocytes with no atypical lymphoid cells. The infiltrate frequently extended into the papillary dermis but exocytosis was rare. Those histopathological features are the characteristic features of the classic PSEP (small type). 9 Immunohistochemically, the positive immunostaining for CD3 (a pan T-cell marker) detected in all our patients is similar to that of PSEP, which belongs to the cutaneous T-cell lymphoproliferative disorders. 8 An intriguing finding was the CD8 1 T-cell phenotype predominance over the CD4 1 T cell in 30 patients (94.1%). This finding is different from that expected to be found in PSEP in which the superficial lymphoid infiltrates is composed primarily of CD4 T cells. 10 We hypothesize that the CD8 predominance in our patients might partially account for the hypopigmented presentation of the PSEP in a way similar to hypopigmented MF. The cause of hypopigmentation in hypopigmented MF has been suggested to be secondary to the cytotoxic effect of the predominant CD8 cells, frequently detected in hypopigmented MF, on melanocytes During our Internet search we were surprised to find out that hypopigmented PSEP, as a new variant of PSEP, was suggested in 2005 by Das and
6 JAM ACAD DERMATOL VOLUME 67, NUMBER 6 El-Darouti et al 1187 Table II. Comparison between hypopigmented and classic types of parapsoriasis en plaque (small- and large-plaque parapsoriasis) Item PSEP (SPP) 17 PSEP (LPP) 18,19 PSEP (hypopigmented type) No. Few Numerous Variable (few-numerous) Sites Mainly upper part of trunk Trunk/extremities Trunk/extremities and extremities Shape and size 2-6 cm (regular) Long axis may reach up to cm [6 cm 2-6 cm (regular) Long axis may reach up to cm Digitate forms 1 _ 1 Color Erythematous/xanthomatous Erythematous Hypopigmented Atrophy/poikiloderma _ 6 _ Histopathology Superficial perivascular lymphocytic infiltrate (CD4 and CD8 T cells) Exocytosis Spongiosis 6 Superficial perivascular lymphocytic infiltrate (CD4 and CD8 T cells) Exocytosis Spongiosis 6 Superficial perivascular lymphocytic infiltrate (CD4 and CD8 T cells) Exocytosis Spongiosis 6 and reduced basal pigmentation and melanocytes Immunohistochemistry CD4 predominance CD4 predominance CD8 predominance Change to MF 0%-10% 7%, 14%, 35% 14% LPP, Large-plaque parapsoriasis; MF, mycosis fungoides; PSEP, parapsoriasis en plaque; SPP, small-plaque parapsoriasis. Gangopadhyay, 14 who described a patient with features similar to our own patients. Interestingly during our 7-year study 5 patients (14.7%) showed clinical and histopathological transformation to MF. The signs of conversion into MF included enlargement in size, development of erythema, scaling, and mild pruritus in addition to the detection of epidermotropism and atypical lymphocytes upon histopathological examination. This transformation adds further proof to the similarity of this disorder to the conventional PSEP, which since its first description by Dowling 15 showed the probability of evolution into MF. 16 The conversion rate (14.7%) reported in the current work is close to that reported in small-type PSEP, in which the rate of progression to MF was reported to be 10% in one study, 17 versus 35% in the large-plaque type (LPP). Of note, the data on the progression rates to MF in PSEP are conflicting, ranging from 0% to 45%. 18,19 It is worth noting that the hypopigmented presentation is known to occur in other lymphoproliferative diseases including the pityriasis lichenoides chronica 20,21 and MF 22 and it seems that the hypopigmented variants might be more common among dark-skinned patients, as the aforementioned presentation of hypopigmented pityriasis lichenoides chronica was reported in dark-skinned individuals. Also hypopigmented MF shows a higher prevalence among individuals with dark complexions. 23 Of note, our patientseegyptiansehave dark skin types, mainly skin types III and IV, which could partially account for the prevalence of hypopigmented presentation of PSEP. A limitation in our study is that we did not perform clonal T-cell receptor gene rearrangement. This was basically a result of limited resources. Moreover, the detection of monoclonality/polyclonality in itself is not mandatory in differentiating between PSEP and other disorders. This is because monoclonality is not always synonymous with malignancy as many benign dermatoses including inflammatory stages of vitiligo, lymphomatoid papulosis, Mucha-Habermann disease, psoriasis, 23,24 and classic types of PSEP 9 may show monoclonality. Meanwhile, clinically obvious T-cell tumors can sometimes lack demonstrable clonal T-cell receptor gene rearrangements by either Southern blot or polymerase chain reaction analysis. 3 In conclusion, we believe that hypopigmented PSEP is a well-defined new variant of the PSEP family that shows, apart from the hypopigmentation, all the features of PSEP particularly the small PSEP variant. Moreover, as small PSEP it can progress to MF. Awareness of this entity is required especially when evaluating patients with idiopathic hypopigmented macular lesions, bearing in mind that these patients require biopsy and follow up to evaluate for possible evolution to MF. REFERENCES 1. Sehgal VN, Srivastava G, Aggar Wal AK. Parapsoriasis: a complex issue. Skin Med 2007;6:280-6.
7 1188 El-Darouti et al JAM ACAD DERMATOL DECEMBER Bordignon M, Belloni-Fortina A, Pigozzi B, Saponeri A, Alaibac M. The role of immunohistochemical analysis in the diagnosis of parapsoriasis. Acta Histochem 2011;113: Klemke CD, Dippel E, Dembinski A, P onitz N, Assaf C, Hummel M, et al. Clonal T-cell receptor gamma-chain gene rearrangement by PCR-based GeneScan analysis in the skin and blood of patients with parapsoriasis and early-stage mycosis fungoides. J Pathol 2002;197: Faye O. Diagnosing hypopigmented lesions in black skin. Ann Dermatol Venereol 2006;133: Relyveld GN, Menke HE, Westerhof W. Progressive macular hypomelanosis: an overview. Am J Clin Dermatol 2007;8: Robson KJ, Piette WW. Cutaneous manifestations of systemic diseases. Med Clin North Am 1998;82: Pimpinelli N, Olsen EA, Santucci M, Vonderheid E, Haeffner AC, Stevens S, et al. Defining early mycosis fungoides. J Am Acad Dermatol 2005;53: Wood GS, Hu CH. Parapsoriasis. In: Freedberg IM, Eisen AZ, Wolff K, Austen KF, Goldsmith LA, Katz SL, editors. Dermatology in general medicine. 6th ed. New York: McGraw-Hill; pp Nair PS. A clinical and histopathological study of pityriasis lichenoides. Indian J Dermatol Venereol Leprol 2007;73: Haeffner AC, Smoller BR, Zepter K, Wood GS. The differentiation and clonality of lesional lymphocytes in small plaque parapsoriasis. Arch Dermatol 1995;131: Dawson B, Trapp RG. Basic and clinical biostatistics. 3rd ed. New York: Lange Medical Books-McGraw Hill; Wain EM, Orchard GE, Whittaker SJ, Spittle M Sc MF, Russell-Jones R. Outcome in 34 patients with juvenile-onset mycosis fungoides clinical, immunophenotypic and molecular study. Cancer 2003;98: El-Darouti MA, Marzouk SA, Azzam O, Fawzi MM, Abdel-Halim MR, Zayed AA, et al. Vitiligo vs hypopigmented mycosis fungoides (histopathological and immunohistochemical study, univariate analysis). Eur J Dermatol 2006;16: Das J, Gangopadhyay A. Large plaque parapsoriasis in a child. Indian J Dermatol 2005;50: Dowling GB. Case of parapsoriasis (Brocq). Proc R Soc Med 1926;19: Belousova IE, Vanecek T, Samtsov AV, Michal M, Kazakov DV. A patient with clinicopathologic features of small plaque parapsoriasis presenting later with plaque-stage mycosis fungoides: report of a case and comparative retrospective study of 27 cases of non progressive small plaque parapsoriasis. J Am Acad Dermatol 2008;59: Vakeva L, Sarna S, Vaalasti A, Pukkala E, Kariniemia AL, Ranki A. A retrospective study of the probability of the evolution of parapsoriasis en plaques into mycosis fungoides. Investigative report. Acta Derm Venereol 2005;85: Lazar AP, Caro WA, Roenigk HH Jr, Pinski KS. Parapsoriasis and mycosis fungoides: the Northwestern University experience, 1970 to J Am Acad Dermatol 1989;21: Stachowitz S, Mempel M, Schm ockel C, Von Spanyl R, Abeck D. Variable course of patients with plaque psoriasis: lack of transformation into tumors mycosis fungoides. Blood 2000;95: Clayton R, Warin A. Pityriasis lichenoides chronica presenting as hypopigmentation. Br J Dermatol 1979;100: Lane TN, Parker SS. Pityriasis lichenoides chronica in black patients. Cutis 2010;85: El Shabrawi-Caelen L, Cerroni L, Mederios IJ, McCalmont TH. Hypopigmented mycosis fungoides: frequent expression of a CD8 1 T-cell phenotype. Am J Surg Pathol 2002; 26: Vega F, Luthra R, Mederios IJ, Dunmire V, Lee SJ, Duvic M, et al. Clinical heterogeneity in mycosis fungoides and its relationship to clinical course. Blood 2002;100: Cribier B, Snatinelli F, Lipsker D, Gosshans E. Vitiligo with inflammatory raised border mimicking mycosis fungoides: a clinicopathological study of 4 cases. Am J Dermatopathol 2000;4:349.
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