Delayed reepithelialization and scarring deregulation following drug-induced toxic epidermal necrolysis

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1 burns 33 (2007) available at journal homepage: Delayed reepithelialization and scarring deregulation following drug-induced toxic epidermal necrolysis P. Paquet a, *, E. Jacob b, P. Quatresooz a, D. Jacquemin c, G.E. Piérard a a Department of Dermatopathology, University Hospital Sart Tilman, CHU, Sart Tilman, B-4000, Liège, Belgium b Intensive Care Department, University Hospital Sart Tilman, Liège, Belgium c Burn Center, Department of Plastic Surgery, University Hospital Sart Tilman, Liège, Belgium article info Article history: Accepted 26 April 2006 Keywords: Scar Lyell syndrome Graft abstract A 51-year-old Caucasian woman developed severe drug-induced toxic epidermal necrolysis (TEN) due to allopurinol. The withdrawal of the culprit drug was unfortunately delayed, and dramatic retardation of reepithelialization was observed. At that stage of disease evolution, an inflammatory cell infiltrate was present in the dermis. Coverage of eroded lesions by frozen cultured keratinocyte allografts failed to hasten reepithelialization compared to ungrafted sites. This unusual protracted TEN evolution was followed by the development of extensive hypertrophic and keloid scars. Several biopsies were taken over 6 months. The histologic presentation of the grafted and ungrafted eroded scar tissues looked similar. Both the number and size of the Factor XIIIa-positive dermal dendrocytes, as well as the number of a-actin-positive myofibroblasts showed a marked increase between weeks 2 and 12 after grafting. They were reduced after 6 months when the scarring process was stabilized. a1 [IV] collagen was never expressed over the eroded scars. Similar to burn patients, delayed reepithelialization might be a risk factor for abnormal scarring in TEN. Cultured keratinocyte allograft apparently offered no improvement in reepithelialization and did not prevent abnormal scarring in this TEN patient. # 2006 Elsevier Ltd and ISBI. All rights reserved. 1. Introduction Toxic epidermal necrolysis (TEN) is a rare potentially lethal disease characterized by sudden necrosis involving the epidermis as well as the genital and oropharyngeal mucosae [1]. The disease corresponds to an adverse drug reaction, especially to sulfonamides, phenytoin, antibiotics, non-steroidal anti-inflammatory drugs and allopurinol. Fatal outcome may occur in about one-third of the patients. Various longterm sequels can affect the lungs, heart, joints, kidneys and gut. However, the most common persistent damage involves the eyes, nails, genital mucosae and skin. In survivors under supportive care, reepithelialization of the eroded lesions is notoriously rapid [1]. The dermis remains uninvolved by the disease except an early increased number of Factor XIIIa positive type I-dendrocytes (DD-1) in the adventitial sector [2]. As a rule, there is no or little scarring of the involved skin. In particular, and in contrast with burns, there is apparently no increased risk for hypertrophic or keloidal scarring [1]. We report a patient who developed severe TEN with unfortunate delayed withdrawal of the culprit drug. Unusual protracted skin erosions were followed by extensive hypertrophic and keloidal scarring despite coverage of the eroded areas by cultured keratinocyte allografts. The clinical impact of the delayed withdrawal of the culprit drug is discussed in relation to the retarded epidermal repair and the abnormal scarring. The usefulness * Corresponding author. Tel.: ; fax: address: P.Paquet@chu.ulg.ac.be (P. Paquet) /$30.00 # 2006 Elsevier Ltd and ISBI. All rights reserved. doi: /j.burns

2 burns 33 (2007) of keratinocyte allografts in TEN treatment is also questioned. 2. Case report The patient is a 51-year-old woman who suffered from systemic lupus erythematous responsible for a moderate alteration of the renal function. She received allopurinol 200 mg daily for controlling elevated serum levels of uric acid. The patient developed a cutaneous rash corresponding to TEN 14 days after initiation of this oral treatment. The erythematous rash was studded with discrete bullae which progressively spread during the next 10 days over the back and limbs. She complained of general malaise with fever, headache and conjunctivitis, but she did not discontinue the allopurinol intake. On the 11th day after TEN onset, she consulted a dermatologist who biopsied a bullous lesion. The diagnosis of Fig. 1 (a and b) Erosive scars on the abdomen (a) and left thigh (b) 2 months after TEN onset. (c and d) Similar thickness and redness of the hypertrophic scars on the abdomen (treated with cultured keratinocytes) and the left thigh (control) 1 year after TEN onset.

3 102 burns 33 (2007) Fig. 2 Post-TEN keloidal scars of the right arm evolving for 1 year. TEN was confirmed histologically on the basis of the presence of a subepidermal blister with rare inflammatory mononuclear cells scattered between confluent necrotic keratinocytes. The patient was hospitalized in a burn unit where she was placed on a fluidized bed. Lesions were treated with topical antiseptics. The patient also benefited from supportive care including daily baths. Intravenous immunoglobulins [IVIg] were perfused at a 1 g/kg daily dosage for three consecutive days. Corticosteroids were not administered. Despite IVIg treatment, blisters and epidermal sloughing worsened to reach more than 80% of the body surface 7 days after admission. Erosions of the ocular, genital and oral mucosae also developed. Three cutaneous biopsies were performed at 2-day intervals in both taut blisters and clinically uninvolved skin searching for histological clues explaining the severe course of the disease and predicting its outcome compared to the TEN biopsies retrieved from our files. The only singularity found in the present patient was the small number of Factor XIIIa+ DD-1 cells dispersed in a lymphoid infiltrate. The patient s general condition progressively improved during the following weeks. Partial reepidermization took place, but large eroded areas of the trunk, thighs and upper limbs were not yet closed 1 month after admission. Daily cutaneous swabs performed over several sites of the eroded areas always remained sterile. No septicemiaoccurred.onemonthafteradmission,i.e.more than 40 days after the onset of the disease, biopsies were performed again in TEN involved and uninvolved skin. Immunohistochemistry revealed the presence of sparse Factor XIIIa+ DD-1 expression cells. There was a moderate amount of CD45R0+ T lymphocytes admixed with numerous CD68+macrophages. Myofibroblasts enrichedin a-actin were almost absent. The a1 (IV) collagen chain was not expressed in the eroded dermis. A first allograft (600 cm 2 ) of frozen cultured keratinocytes (Cryoceal 1, Xcellentis, Ghent, Belgium) was applied on randomized eroded areas of the body, followed by two other allografts performed 8 days (900 cm 2 ) and 15 days (800 cm 2 ) later. Before each allograft procedure, skin biopsies were taken from two TEN eroded lesions located on the grafted site of the abdomen and on the ungrafted site of the left thigh, respectively (Fig. 1a and b). Repeated skin swabs remained sterile during this treatment phase. No clinical difference was noted between the treated and the control eroded areas. Immunohistochemical examinations did not show any difference between the two sites with regard to the numerical densities in Factor XIIIa+ DD-1, a-actin+ myofibroblasts, CD68+, macrophages and CD45RO+ T cells, respectively. Considering the evolution in time, Factor XIIIa+ DD-1 increased in number at D8 and D15 post-grafting. No other change was disclosed in the dermis during that period. At both sites, no deposits of a1 (IV) collagen chain were disclosed on top of the dermis. There was no sign of vasculitis or infection. The retarded epithelialisation delayed the hospital discharge until 2 months after admission. At that time, some small eroded areas were still present on the arms. At the end of hospitalization, both the keratinocytetreated and control areas progressively developed similar erythematous hypertrophic scarring. Similar lesions developed on other previously TEN-affected areas, especially on the upper limbs and chest. The colour of the scars as assessed by narrow band spectrophotometry (Mexameter 1 MX16, C+K electronic, Cologne, Germany) showed no difference in the erythema index E on the two comparative sites. Ten months after hospital discharge, i.e. 1 year after the TEN onset, the hypertrophic scars of the keratinocytetreated and control areas began to flatten simultaneously (Fig. 1c and d). Conventional histology and immunohistochemistry performed on skin biopsies taken 3 and 6 months after grafting looked similar on both sites. At D90, they showed numerous large dendritic and globular Factor XIIIa+ DD-1 expression cells admixed with fewer and smaller a- actin+ myofibroblasts. At D180, a marked thickening of the collagen bundles was present. Moderate numbers of Factor XIIIa+ DD-1, CD68+ macrophages and a-actin+ myofibroblasts were present throughout the dermis. Eighteen months after TEN onset, the abnormal scarring on the upper arms presented as thick and erythematous keloidal tumours (Fig. 2). Histological sections showed a massive accumulation of thickened hyalinized collagen bundles. These lesions were treated by repeated triamcinolone injections and by endermology pressure therapy. A moderate improvement was observed 6 months after initiating this treatment.

4 burns 33 (2007) Discussion Fibroblasts and myofibroblasts play key roles in the scarring process [3,4]. In addition, inflammatory cells, DD-1 and keratinocytes, which orchestrate the normal healing process may also influence fibroblasts via the secretion of multiple growth factors and cytokines [3,5 8]. Macrophages can possibly initiate abnormal scarring by releasing fibroblastactivating cytokines such as transforming growth factor-b (TGFB-b) and platelet-derived growth factor (PDGF). They also produce interleukin-1 (IL-1) which is important for the extracellular matrix degradation by inducing the metalloproteinase release and activity [5,9]. In addition, many lymphocyte-mediated cytokines modulate fibroplasia, especially TGFb, tumour necrosis factor-b and interferon b [5,7]. Persistence of activated keratinocytes in predisposed individuals or a prolonged time to reepithelialization could lead to hypertrophic or keloidal scar formation [3]. Indeed, the epidermis of hypertrophic scars was found to exhibit reduced IL-1a expression and increased PDGF expression. IL-1a plays a role in the extracellular matrix degradation at the wound site whereas PDGF is involved in tissue fibrosis [5,9]. Keratinocytes covering keloids also increase TGF-b1 expression in fibroblasts suggesting that besides causing an excess in production of collagen, an increased resistance to apoptosis may develop in keloid fibroblasts [10]. In our TEN patient, frozen keratinocyte allografts failed to show any effect on the Factor XIIIa+ DD-1, a-actin+ myofibroblasts, CD45RO T lymphocytes and CD68+ macrophages. They also had no clinical impact on the healing process since no difference was evidenced between the grafted and ungrafted sites. In the presently reported TEN patient, the number of Factor XIIIa+ DD-1 was surprinsingly low in the early stage of the disease. This contrasted with the usual DD-1 hyperplasia found in TEN [2]. As discussed below, the DD-1 rarefaction in our patient might be related to the late withdrawal of the culprit drug. Later on, at the initiation of reepithelialization of the protracted erosions, an increased Factor XIIIa+ DD-1 population was disclosed, suggesting a positive effect on wound closure. It is noteworthy that the changes in the number of Factor XIIIa+ DD-1 are associated with an increase in their size. They became first more dendritic at D15 postgrafting, and they appeared globular at D90. They resumed a normal aspect at D180. These variations in cell tensegrity may be found in Factor XIIIa+ DD-1 present in some connective tissue disorders [11,12]. The tensegrity changes in the Factor XIIIa+ DD-1 observed in the present TEN case were not seen in other dermal cells, particularly in the a-actin+ myofibroblasts. These cells are normally involved in wound healing when contraction of the granulation tissue takes place. This process, which occurs after loss of dermal tissue to ensure wound contraction [4], is not operative in TEN healing. In the present case, there was no immunohistochemical sign suggesting dermal cell mobility during the protracted healing process. It has been postulated that the phagocytic properties of DD- 1 contribute to limit any evolving fibrotic process. Indeed, DD- 1 are able to remove fragmented collagen fibers [13]. However in this TEN case, the overexpression of Factor XIIIa+ DD-1 did not prevent hypertrophic scarring. Usually TEN skin erosions heal without dermal scarring [1] and hypertrophic or keloid scars have been rarely described [14]. The keloid and hypertrophic pattern in our patient may be linked to the late withdrawal of the culprit drug with a prolonged and intense effect on keratinocytes. This situation probably led to high levels of proapoptotic and proinflammatory keratinocyte-derived cytokines production, and to a dense inflammatory infiltrate composed of T lymphocytes and reactive macrophages that can in turn influence the fibroblast function. Moreover, high concentrations of TNF-a, that is one of the major cytokines involved in TEN lesions, might be toxic for Factor XIIIa+ DD-1 thus impairing their function in the healing process. Clinically, abnormal scarring most commonly occurs after reepithelialization has been delayed [15]. Autologous and allogenic cultured keratinocyte sheets or suspensions have been previously used in burn patients to prevent or to treat abnormal scarring [16,17]. They have also been employed to boost healing in TEN patients [18]. It has also been demonstrated that cryopreserved cultured keratinocytes retain their healing potential [19]. In the present TEN patient, no differences were found in the healing rate and in the quality of scarring between the keratinocyte-grafted and ungrafted areas. The main cause of failure of cultured keratinocytes in wound treatment is a bacterial overload in the wound bed [19], but this was not the case in our TEN patient. In conclusion, TEN may be associated with delayed healing, especially after late withdrawal of the culprit drug. Prolonged TEN cutaneous erosions can lead to keloidal and hypertrophic scarring. In the present TEN case, allogenic cultured keratinocytes did not improve the healing rate and the quality of the scarring process. references [1] Fritsch PO, Sidoroff A. Drug-induced Stevens-Johnson syndrome/toxic epidermal necrolysis. Am J Clin Dermatol 2000;1: [2] Paquet P, Paquet F, Al Saleh W, Reper P, Vanderkelen A, Pierard GE. Immunoregulatory effector cells in druginduced toxic epidermal necrolysis. Am J Dermatopathol 2000;22: [3] Lim IJ, Phan TT, Bay BH, Qi R, Huynh H, Tan WT, et al. Fibroblasts cocultured with keloid keratinocytes: normal fibroblasts secrete collagen in a keloid like manner. Am J Physiol Cell Physiol 2002;283:C [4] Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 2003;200: [5] Quatresooz P, Henry F, Paquet P, Pierard-Franchimont C, Harding K, Pierard GE. Deciphering the impaired cytokine cascades in chronic leg ulcers. Int J Mol Med 2003;11: [6] Machesney M, Tidman N, Waseem A, Kirby L, Leigh I. Activated keratinocytes in the epidermis of hypertrophic scars. Am J Pathol 1998;152: [7] Boyce DE, Ciampolini J, Ruge F, Murison MS, Harding KG. Inflammatory cell subpopulations in keloid scars. Br J Plast Surg 2001;54: [8] Lim IJ, Phan TTP, Song C. Investigation of the influence of keloid-derived keratinocytes on fibroblast growth and proliferation in vitro. Plast Reconstr Surg 2001;107:

5 104 burns 33 (2007) [9] Niessen FB, Spauwen PH, Schalkwijk, Kon M. On the nature of hypertrophic scars and keloids: a review. Plast Reconstr Surg 1999;105: [10] Funayama E, Chodon T, Oyama A, Sugihara T. Keratinocytes provide proliferation and inhibit apoptosis of the underlying fibroblasts: an important role in the pathogenesis of keloid. J Invest Dermatol 2003;121: [11] Hermanns-Lê T, Piérard GE. Factor XIIIa-positive dendrocyte rarefaction in Ehlers-Danlos syndrome, classic type. Am J Dermatopathol 2001;23: [12] Quatresooz P, Hermanns-Lê T, Ciccarelli A, Beckers A, Pierard GE. Tensegrity and type I dermal dendrocytes in acromegaly. Eur J Clin Invest 2005;35: [13] Hermanns-Lê T, Paquet P, Piérard-Franchimont C, Arrese JE, Piérard GE. Regulatory function of factor XIIIa-positive dendrocytes in incipient toxic epidermal necrolysis and graft-versus-host reaction. Dermatology 1999;198: [14] Kavanagh GM, Page P, Hanna MM. Silicone gel treatment of extensive hypertrophic scarring following toxic epidermal necrolysis. Br J Dermatol 1994;130: [15] Bhashan M, Brooke R, Hewitt-Symond SM, et al. Prolonged toxic epidermal necrolysis due to lamotrigine. Clin Exp Dermatol 2000;25: [16] Paquet P, Vanderkelen A, Gielen V, Lapière ChM. The skin equivalent: its use in vivo. Cytotechnology 1989;50:S [17] Burd A, Chan E. Keratinocyte-keloid interaction. Plast Reconstr Surg 2002;110: [18] Klein L, Mericka P, Strakova H, Jebavy L, Nozickova M, Blaha M, et al. Biological skin covers in treatment of two cases of the Lyell s syndrome. Ann Transplant 1997;2:45 8. [19] Paquet P, Quatresooz P, Braham C, Piérard GE. Tapping into the influence of keratinocyte allografts and biocenosis on healing of chronic leg ulcers: split-ulcer controlled pilot study. Dermatol Surg 2005;31:431 5.

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