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1 Tea JOURNAL OF TNvasTJoATrvg DERMAT0L00Y Copyright by The Williams & Wilkins Co. vol. 52, No.2 Printed in U.S.A. TJLTRASTRUCTTJRAL PATHOLOGY OF ERYTHEMA DYSCHROMICUM PERSTANS* NICHOLAS A. SOTER, M.D., CHARLOTTE WAND, H.T. ASD ROBERT C. FREEMAN, M.D. Erythema dyschromicum perstans is a cutaneous pigmentary clermatosis of unknown etiology characterized by asymptomatic macules of an ashy-gray color (1 5). Pertinent light microscopical features include focal areas of cellular vacuolation (liquefaction degeneration) in the basal and lower prickle cellular layers and a perivaseular infiltration of cells in the papillary dermis including heavily-laden melanophages. This paper presents the ultrastruetural observations in erythema dyschromieum perstans with particular emphasis on the vacuolar changes in the basal and lower prickle cellular layers. MATSRIAL AND METHOD5 Skin trephine biopsies of normal and hyperpigmented skin from four patients, and a hypopigmented lesion from one of the patients, were obtained under local lidocaine anesthesia. Tissue was prepared for light microscopical study by fixation in 10 per cent formalin. For electron microscopical study tissue specimens were cut immediately into small pieces, immersed for 16 hours in 62% glutaraldehyde buffered to ph 7.0 in phosphate buffer made up with 0.1 molar citric acid and 02 molar disodium phosphate, then immersed for one hour io 1% osium tetroxide followed by washing with the same buffer. After dehydration through graded concentration of ethyl alcohols and propylene oxide, the specimens were embedded in Araldite. Two micra thick sections were used to select areas for thin sections. Selected sections were cut with glass knives on a Porter-Blum stained with either uranyl acetate or lead citrate, and studied in an RCA EMU 3F electron microscope with an accelerating voltage of 50 Ky. onservatcons Light Microscopy. Active lesions showed extensive vaeuolar changes in the basal and lower Received June 3, 1068; accepted for publication July 3, * From the Department of Dermatology, Baylor University College of Medicine, Houston, Texas We wish to acknowledge with grateful appreciation the technical assistance of Mrs. Roberta Halloran. 155 prickle cellular layers (Figs. 1, 2). In areas this vacuolar change was limited to individual cells, but elsewhere the cellular vaeuolations became confluent giving an appearance of liquefaction degeneration. The papillary dermis showed edema accompanied by a mild perivaseular infiltrate composed of lymphocytes, histiocytes, and melanophages. The inactive lesions, while showing occasional focal areas of vacuolar change in the basal cellular layer, principally showed melanophages in the papillary dermis (Fig. 3). Electron Microscopy. Alterations in ultrastructure were seen in both the epidermis and dermis. The principal changes occurred in the epidermal basal cellular layer corresponding to the vaeuolation seen on light microscopy. Both intercellular and intracellular abnormalities were present. Two striking changes were noted in epidermal cells. Large translucent areas devoid of cytoplasmie organdies surrounded the nuclei. Within these areas there were vaeuoles delimited by a membrane (Figs. 4, 5). The vacuoles were either single or multiple and at times indented the nuclear envelope (Fig. 6). This vaeuolar change occurred in the basal and lower prickle cellular layers. The remainder of the epidermal cellular morphology appeared unchanged. The intercellular spaces were dilated often, especially in the basal cellular layer, bitt also between prickle cells (Fig. 7). In these areas there was complete separation and retraction of the cells and the presence of amorphous material of low electron density in the intervening spaces. In focal areas the cells were separating with the desmosomes, although apparently normal in morphology, retracting to one cell or the other (Fig. 5). Separation occurred alternately through the attenuated cytoplasm adjacent to the desmosomes. The number and structure of melanoeytes did not appear altered. The remainder of the epidermis appeared unchanged. The basal lamina (Fig. 9) was interrupted by defects; the lucent zone was unchanged.
2 t. a- a L. S 4'*. 'tt'._'t2 L '1 St * j.4t I a a I Fie. 1. Active lesion showing vacuolar changes in lower epidermal cells accompanied by perivascular infiltrate H & E X 276. FIG. 2. High power of active lesion showing vacuolar change in basal and lower prickle cellular layers H & E X 1,
3 4 a ía 1 '4 S Fia. 3. Inactive lesion showing principally heavily-laden melanophages in the papillary dermis H & E X 276. FIG. 4. Detail of keratinocyte showing membrane-free clear cells (C) and vacuole (V). X 16,
4 0 csl v 4 - I - Fic. 5. Detail of basal cell showing multiple vacuoles (V) enclosed by a unit membrane, and dilated intercellular space (I). X 16,065. FIG. 6. Keratinocyte showing vacuoles (V) indenting the nuclear envelope of the nucleus (N). x 9,
5 ERYTHEMA DYSCHROMICUM PERSTANS 159 r 1t4 $ -, 'WI FIG. 7. Dilation of intercellular spaces (I) in the lower epidermal layers above the basal lamina (B). X 6,840. FIG. 8. Detail showing desmosomal retraction (D) and beginning dilation of intercellular spaces. X 18,400.
6 160 THE JOURNAL OF INVESTIGATIVE DERMATOLOGY F -. r.:.wq. a FIG. 9. Detail of epidermal-dermal junction showing defects in the basal lamina (B) mdicated by arrows. Special fibrils (14) (F) are seen joining the underside of the basal lamina (indicated by triangles). X 20,665. FIG. 10. Cell in papillary dermis containing melanin granules in aggregates enclosed by a unit membrane. X 40,500.
7 ERYTHEMA DYSCHROMICUM PERSTANS 161 There was neither duplication nor change in thickness or density of the basal lamina. In the papillary dermis there were mononuclear cells containing melanin granules in aggregates enclosed by a unit membrane (Fig. 10). Except for an inflammatory infiltrate, the remainder of the dermis was normal. The described ultrastructural changes were seen in all four patients in both hyperpigmented and hypopigmented lesions. Uninvolved skin from these patients showed no changes. Similar changes were seen by electron microscopical study in lesions considered by light microscopical study to be active and inactive stages. The principal difference discerned was the greater severity of the alterations in active lesion,s. DISCUSSION The distinctive cutaneous pigmentary dermatosis, erythema dyschromicum perstans, clearly reveals characteristic ultrastructural pathological alterations. The cellular vacuolation, known as liquefaction degeneration when seen by light microscopical study, appeared to have an ultrastructural counterpart. Liquefaction degeneration is defined as a type of degeneration causing vacuolation of the basal cells (6). Ultrastructurally this feature was manifested by translucent areas devoid of organdies and containing membrane limited vacuoles. The dilation of intercellular spaces was a feature observed too. In a study of hchcn planus (7), a disease known to manifest liquefaction degeneration (8), a major ultrastructural change present in the basal cellular layer was dilation of intercellular spaces. Accompanying the intercellular dilation in the present study were areas of cellular separation with retraction of normal desmosomes alternately to one cell or the other. In a study of stripped epidermis, Mishiina and Pinkus (9) noted widening of the intercellular spaces in the basal and prickle cellular areas. The desmosomes in their study were retracted in a picture reminiscent of the change seen in our material. The precise nature of the ultrastructural vacuolcs is unclear. Odland and Reed (10) point out that normal basal cells may contain one or more vcsicles thought to be lipid droplets, but the biochemical nature of these vacuoles is not known with certainty. Nix, et ol. (11 12) in studies of epidermal cellular alterations induced by ultraviolet irradiation noted the appearance of both single and multiple vacuoles and membrane-free spaces in cells of the basal and prickle cellular layers. Tn a study of experimental vesiculation utilizing collagcnases, Kahl and Pearson (13) noted basal cellular damage manifested by pcrinuclear vacuoles, at times indenting the nuclear envelope. The vacuolar changes, as well as the widening of intercellular spaces with dcsmosomal retraction, in these studies and indeed in the present study may represent epidermal cellular response to injury, whatever be its etiology. Melanin granules within dermal melanophages account for the hyperpigmentation manifested clinically as an ashy color. The discontinuity of the basal lamina could provide a route of egress for melanin granules from injured epidermal cells into dermal melanophages. The liquefaction degeneration may result in incontinence of pigment. SUMMARY Erythema dyschromicum perstans is a cutaneous pigmcntary dermatosis with a characteristic ultrastructural pathology. Changes observed were widening of intercellular spaces, desmosomal retraction, vacuolar changes and membrane-free clear spaces in both basal and prickle cells, discontinuity of the basal lamina, and dermal melanophagcs. These ultrastructural changes, individually nonspecific and seen separately in various dermatoses, together clearly provide a consistent ultrastructural composite for erythcma dyschromicum perstans. REFERENCES 1. Ramircz, C. 0.: Los Cenicientos, Problema Clinico. Memoria dcl Primer Congreso Centroamericano de Dermatologia, San Salvador, 5 S Diciembrc, Convit, J., Kerdel-Vegas, F. and Rodriquez, G.: Britema discromicao pcrstans. Dermatologia Venezolana, 2: 118, Convit, J., Kerdel-Vegas, F. and Rodriquez, C.: Erythema dysehromicum perstans. J. Invest. Derm., 36: 457, Stevenson, J. R. and Miura, M.: Erythema dyschromicum pcrstans (Ashy dermatosis). Arch. Derm., 94: 196, Knox, J. M., Dodge, B. C. and Freeman, R. G.: Erythema dyschromicum perstans. Arch. Derm., 97: 262, 1968.
8 162 THE JOURNAL OF INVESTIGATIVE DERMATOLOGY 6. Lever, W. F.: p. 775, Histopathology of the Skin, J. B. Lippincott Co., Philadelphia, Johnson, F. R. and Fry, L.: Ultrastructural observations on lichen planus. Arch. Derm., 95: 596, Ellis, F. A.: Histopathology of lichen planus based on analysis of one hundred biopsy specimens. J. Invest. Derm., 48: 143, Mishima, V. and Pinkus, H.: Electron microscopy of keratin layer stripped human epidermis. J. Invest. Derm., 50: 89, Odland, C. F. and Reed, T. H.: Epidermis, pp , Ultrostructure of Normal and Abeormol Skin, Ed., Zelickson, Alvin S., Lea & Febiger, Philadelphia, Nix, T. E.: Ultraviolet-induced changes in epidermis, pp , Ultrostructure of Normal and Abnormal Skin. Ed., Zelickson, Alvin S., Lea & Febiger, Philadelphia, Nix, T. E., Nordquist, H. E., Scott, J. H. and Everett, M. A.: Ultrastructural changes induced by ultraviolet light in human epidermis. Basal end spinous layers. J. Invest. Derm., 45: 52, KahI, F. H. and Pearson, H. W.: Ultrastructural studies of experimental vesieulation. II. Collagenase. J. Invest. Derm., 49: 616, Swanson, J. L. and Helwig, E. B.: Special fibrds of human epidermis. J. Invest. Derm., 50: 195, 1968.
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