Reconstructive surgery using an artificial dermis (Integra): results with 39 grafts
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1 British Journal of Plastic Surgery (200), 54, 659~ The British Association of Plastic Surgeons doi: 0.054/bjps BRITISH JOURNAL OF ~ PLASTIC SURGERY Reconstructive surgery using an artificial dermis (Integra): results with 39 grafts E. Dantzer and E M. Braye* Centre de Traitement des Br~tl6s, HOpital L6on B&ard, Hyeres; and *Centre de Traitement des Braids, HOpital E. Herriot, Lyon, France SUMMARY. Integra was initially developed for the primary coverage of acute burns. It acts as a network for dermal reconstruction. An epidermal graft overlay is necessary after 3 weeks to achieve the in vivo reconstruction of a fullthickness skin equivalent. The quality of the functional and aesthetic results achieved led us to evaluate the potential of Integra in the treatment of s and for general reconstructive surgery. We present a series of 3 patients who underwent Integra grafting for reconstructive surgery at a total of 39 operational sites. The average area grafted per procedure was 267 cm 2. Complications (silicone detachment, failure of the graft, haematoma) were observed in nine cases. The length of follow-up ranged from 0.5 year to 4 years. Two patients (two sites) were lost to follow-up; the final results in the remaining patients were considered to be good in 28 cases, average in six cases and poor in three cases. The disadvantages of using Integra in reconstructive surgery are the necessity of two operations, the risks of infection under the silicone layer, of the silicone becoming detached and of recurrence of contraction. On the other hand, Integra has many advantages including its immediate availability, the availability of large quantities, the simplicity and reliability of the technique, and the pliability and the cosmetic appearance of the resulting cover. In the light of these preliminary results, Integra appears as a new alternative to full-thickness skin grafting, skin expansion and even skin flaps for reconstructive surgery The British Association of Plastic Surgeons Keywords: skin substitute, artificial dermis, reconstructive surgery, burn sequelae. The treatment of extensive s requires multiple surgical procedures, using flaps and full-thickness skin autografts. The surfaces of the initial burn wounds and the repeated harvesting of grafts during the acute phase of burn injury result in insufficient amounts of healthy skin for burn reconstruction. Integra (Integra Life Sciences Corporation, Plainsboro, USA) was initially developed to improve the functional results after the acute phase of burns. -3 It is a bilayered dermal substitute. The first layer is a matrix of bovine collagen and chondroitin-6-sulfate, cross-linked with glutaraldehyde; after grafting, the recipient fibroblasts infiltrate the matrix network and synthetise a neodermis, which is histologically very close to normal human dermis. 4 The second layer is a silicone membrane, which acts as a temporary epidermis. This healing guide becomes revascularised within 2-3 weeks, and must then be covered with an ultra-thin epidermal graft, which can be meshed. The resulting coverage is pliable, not adherent to the deeper structures and shows no mesh pattern. This protocol permits, therefore, in return for two surgical operations, separated by a 3 week interval, and an ultra-thin epidermal graft, the in vivo reconstruction of large surfaces of full-thickness skin equivalent. The good aesthetic and functional results obtained in the treatment of acute burns 5 suggest an application in general plastic surgery. We report here our experience of 3 patients (39 different sites) who underwent reconstruction using Integra, either for the treatment of burns or for general plastic surgery. Patients and methods Patients Between February 997 and June 2000, in two different centres, 3 patients underwent lntegra grafting for functional reconstructive surgery in a total of 39 operations. There were 6 women and 5 men. The average age was 36 years (range: 3-77 years) and the series included six children under 5 years of age. The operative sites and the indications are reported in Table. Surgical technique In every case, Integra was grafted during the same operation as the removal of the scar tissue or skin tumour. To release scar contractures, we performed only simple scar incisions in the early cases, but later performed larger excisions, and, when possible, complete scar removals (Fig. A,B). All efforts were made to obtain a complete range of motion intraoperatively. This strategy was permitted by the large amounts of skin coverage provided by Integra. On average, an area of 246 cm 2 was grafted per session (range: cruz). As in a classic full-thickness skin graft, the surgeon aimed to obtain a well-vascularised bed with perfect haemostasis. In most cases non-meshed 659
2 660 British Journal of Plastic Surgery Integra was used. W h e r e haemostasis was difficult, we m a d e a few incisions with a bladed bistoury to avoid a possible haematoma. The Integra was attached to the edges of the w o u n d b y either sutures or staples (Fig. C). Stitched compression dressings were used on movable Table Locations of and indications for the Integra grafts Location Indication face after-effects of surgery for rhinophyma orbital basal cell carcinoma bum scar bum scar giant naevus repair of a flap donor site chronic wound donor site of full-thickness skin graft tumour removal neck hand upper limb lower limb trunk total Number of grafts areas for a week. In every case, strict clinical surveillance was necessary to track d o w n and drain h a e m a t o m a t a and possible infections under the silicone layer. The second operation took place, on average, 22 days (range: 2-45 days) after the Integra grafting. Ultra-thin (0. m m ) autografts were applied, singly or meshed, d e p e n d i n g on the surface to be covered (Fig. D,E). After definitive healing (Fig. IF), an intensive rehabilitation p r o g r a m m e was imposed, as we would do after any reconstruction of burn sequelae, which consisted of static and d y n a m i c splints, massages, pressure garments and silicone application. The patients were systematically re-examined. The criteria used for final evaluation were the rate of complications and the comparison of the result with the preoperative functional and aesthetic goals. The results were considered to be good w h e n the preoperative goal was totally achieved, average w h e n the result was not c o m plete and poor if there was a return to the initial state. Results We treated 3 patients using Integra grafting to a total of 39 different sites. Immediate complications are shown in Table 2. Contact was lost with two patients. We clinically evaluated the r e m a i n i n g 29 patients (37 sites) an average of 2 years (range: 6 m o n t h s to 4 years) postoperatively. Good results, compared with the initial objective, were achieved in 28 cases, average results in six cases and poor results in three cases (Table 3). Figure I - - A girl aged years, who suffered burns to 80% of her body surface at the age of 6 years. (A) Preoperative view; circumferential s on the thorax are responsible for restrictive respiratory insufficiency and a delay in breast development. (B) Resection of the to a width of 0cm in both the longitudinal and the transverse directions. (C) Integra artificial skin is put into position and stapled. (D) Appearance after 22 days; the dermis is becoming vascularlsed as confirmed by the characteristic yellow-pink coloration and opacity. (E) Application of an ultra-thin.5 meshed epidermal-graft overlay. (F) Intraoperative view after 6 months; the grafted zone has enlarged to 3 cm in width and is non-adherent to the deep tissues. The mesh of the epidermal graft is not visible and the aesthetic aspect of the grafted zone is much better than that of the surrounding scar.
3 Reconstructive surgery using an artificial dermis (Integra): results with 39 grafts 66 In a case of amputation, we found the coverage to be solid enough for the use of a prosthesis (Fig. 2). When used over tendons (back of the hand or foot) the engraftment was complete and free motion of the tendons was observed under the Integra (Fig. 3). In a case of carpaltunnel syndrome, the clinical symptoms disappeared after Table 2 Early complications of 39 sites receiving an Integra graft for reconstructive surgery Initial complication n Consequences n haematoma drained without consequence detachment of silicone 2 without consequences 2 infection 5 without consequences 4 total loss incomplete take of 3 controlled healing epidermal graft re grafting 2 total scar incision and Integra grafting. Dermal replacement resulted in skin of a uniform colour and texture, and no recurrence of hypertrophic scarring was observed (Fig. 4). In every case, the resultant coverage was flexible and non-adherent to the deep tissue (Fig. 5). There is usually an inflammatory and contraction period between 2 months and 6 months postoperatively, which does not compromise the final result. Two patients complained of pain, there was one case of pruritis and three cases of dry skin. In all cases, intensive rehabilitation was necessary, as it is after other kinds of grafting, 6 to limit inflammatory phenomena and to maintain the joint mobility obtained intraoperatively. Discussion It is now possible to save patients burnt over more than 90% of their body surface. In spite of intensive rehabilitation, a few years later these patients (especially children) Table 3 Surgical procedures and results for the 3 patients who underwent Integra grafting for reconstructive surgery Patient Age Sex Location Indication Area grafted Complications Follow-up Result a (years) (cm 2) (years') 5 M lower limb burn sear F breast M neck M lower lip F thorax F abdomen F lower limb F abdomen F breast M neck M hand F neck F axillaryfold F neck F both hands M upperlimb F lowerlimb F left hand F right elbow F upper limb F upper limb M lower lip M knee M upper limb M lower limb F lip, chin, neck F nose F lower limb F neck M abdomen M amputation M abdomen donor site M orbit tumour excision M lower limb chronic wound M trunk tumour excision M nose rhinophyma M lower limb flap donor site F upper limb congenital naevus F plantar foot flap donor site 25 none good haematoma average none 3.5 good infection, full-thickness graft losttofollow-up none 3 good none 2.5 good none.5 good lost halfofepidermal 2.5 good graft, second graft none 3.5 average refused rehabilitation poor refused rehabilitation poor none 4 good none 4 good none 3 average none 3 good none l good loss of one quarter of 3 average epidermis, contracture none 2.5 good none 2.5 good infection underlntegra 2 poor detachment ofsilicone losttofollow-up none.5 good detachment of silicone 2 average contracture.5 poor infection under Integra.5 good none 0.5 good none good infection good none good loss ofepidermis good infection 2.5 good none.5 good none.5 good none 0.5 good none 0.5 good a The results were considered as good when the preoperative goal was totally attained, average when the result was not complete and poor if there was a return to the initial state.
4 662 British Journal of Plastic Surgery Figure A 26-year-old man who sustained a thigh amputation and 30% total body surface area burns in a car accident. (A) Graft adherence resulted in decreased mobility of the thigh for abduction and retropulsion. (B) Extensive scar resection involving the whole thigh and the lower abdomen. (C) Postoperative result 5 months later; the coverage is solid enough for the patient to use a prosthesis. Figure A 3-year-old woman presented with s on 57% of her total body surfalce. (A) Hypertrophic and retractile scarring on the dorsum of the hand resulted in complete ankylosis. (B) Radiograph showing metacarpal subluxation. (C) Result year after complete resurfacing with Integra, showing a satisfactory range of motion and a good cosmetic aspect of the new skin. will suffer from scars affecting function. Furthermore, in children these contractures worsen with, and can hinder, growth. The repair of burn sequelae often requires large areas of healthy skin. Local flaps, micro-anastomosed flaps and full-thickness skin grafts 6 can be used. In most cases, a preliminary expansion of the donor site of the flap or full-thickness graft is required to obtain a sufficient amount of skin] This involves two operations, separated by 2 or 3 months of expansion. This is particularly difficult for children whose schooling must continue. Even when large expanders are used, the increase in the area of skin is still limited, and the failure rate of the procedure must be considered. 8 The removal of the expanders leaves scarring that must be taken into account in planning a therapeutic project. Finally, in the most extreme cases there are no areas of healthy skin available for secondary repair. From a general point of view, plastic surgery can equally require large areas of full-thickness grafting to ensure skin closure after the removal of large skin tumonrs, either benign or malignant, or to reduce the after-effects of the harvesting of large flaps. A few surgeons have now used Integra for general reconstructive surgery. 9,0 Our initial results for s were poor, with recurrence of retraction, because we perfornaed only simple
5 Reconstructive surgery using an artificial dermis (Integra): results with 39 grafts 663 A Figure 4--A 44-year-old woman sustained thermal burns to 40% of her total body surface area. (A) Preoperative view; hypertrophic scarring of the mandibular area. (B) Result 6 months postoperatively;there was no recurrence of the hypertrophic scarring. The grafted area was pliable with no secondary retraction, as shown by the good chin-neck angle and the absence of lower lip attraction. Figure 5--Resurfacing with lntegra provides very pliable skin with no adherence to the deeper structures, which allows for a complete range of motion. incisions. With growing confidence in this procedure, we have progressively evolved our operational technique. We now use larger excisions and, when possible, complete scar removals, which seems to be a better strategy and which eliminates all peripheral skin tension. By providing large areas of satisfactory skin coverage, Integra has transformed our strategy for burn reconstruction. This technique requires rigorous haemostasis. When Integra is used over joints, tie-over dressings may avoid mechanical detachment of the silicone. The sensitivity of Integra to infection requires careful follow-up. The silicone's transparency makes it easy to observe the development of infected areas, which must be systematically excised and treated with topical antibiotics. If treated promptly, the problem is quickly resolved and does not jeopardise the final outcome. We observed three partial failures of the second procedure of epidermal grafting. The success of the epidermal graft depends on its thickness and on the viability of the dermis. The graft must not be too thin, because the presence of basal cells is necessary for the reconstruction of the epidermis. On the other hand it must not be too thick, to avoid a final mesh texture, and to prevent donor-site scarring. Careful patient selection, treating only those who will respect the immobilisation, the regular follow-ups and the rehabilitation, is essential, in so far as the use of Integra requires two operations separated by an interval of 3 weeks. In the years to come, progress in skin substitutes may lead to the development of a full-thickness skin equivalent that can be cultivated in vitro. -t4 At the moment, only Integra can provide large surfaces of thick coverage. In our series, we were able to treat increasing surface areas, up to c m 2 in a single session. The resultant coverage is supple and non-adherent to the deep tissue. This procedure results in skin of a uniform colour and texture, and no recurrence of hypertrophic scarring was observed. Due to the aesthetic quality of the final result, it is now possible to imagine replacing large scars resulting from extensive bums. This method requires the harvesting of only ultra-thin skin from the patient, which does not result in additional scarring, unlike when full-thickness grafts or flaps are used. In the light of these results, Integra appears to be a new alternative for use in reconstructive surgery. This technique, in common with other repair techniques, has advantages and disadvantages, which have to be taken into account when choosing a therapeutic method for each patient. The authors declare that they have no financial interest in this publication.
6 664 British Journal of Plastic Surgery References. Yannas IV, Lee E, Orgill DE Skrabut EM, Murphy GF. Synthesis and characterization of a model extracellular matrix that induces partial regeneration of adult mammalian skin. Proc Nat Acad Sci USA 989; 86: Burke JE Yannas IV, Quinby WC Jr, Bondoc CC, Jung WK. Successful use of a physiologically acceptable artificial skin in the treatment of extensive burn injury. Ann Sttrg 98; 94: Heimbach D, Luterman A, Burke J, et al. Artificial dermis for major burns: a multi-center randomized clinical trial. Ann Surg 988; 208: Stern R, McPherson M, Longaker MT. Histologic study of artificial skin used in the treatment of full-thickness thermal injury. J Burn Care Rehabil 990; : Sheridan RL, Hegarty M, Tompkins RG, Burke JE Artificial skin in massive burns - results to ten years. Eur J Hast Surg 994; 7: Iwuagwu FC, Wilson D, Bailie F. The use of skin grafts in postburn contracture release: a 0-year review. Hast Reconstr Surg 999; 03: Bauer BS, Vicari FA, Richard ME, Schwed R. Expanded fullthickness skin grafts in children: case selection, planning, and management. Plast Reconstr Surg 993; 92: Pisarski GE Mertens D, Warden GD, Neale HW. Tissue expander complications in the pediatric burn patient. Plast Reconstr Surg 998; 02: Suzuki S, Shin-ya K, Kawal K, Nishimura Y. Application of artificial dermis prior to full thickness grafting for resurfacing the nose. Ann Hast Surg 999; 43: Wang JCY, To EWH. Application of dermal substitute (Integra) to donor site defect of forehead flap. Br J Hast Surg 2000; 53: Butler CE, Orgill DE Yannas IV, Compton C. Effect of keratinocyte seeding on collagen-glycosaminoglycan membranes on the regeneration of skin in a porcine model. Hast Reconstr Surg 998; 0: Coulomb B, Friteau L, Baruch J, et al. Advantage of the presence of living dermal fibroblasts within in vitro reconstructed skin for grafting in humans. Hast Reconstr Surg 998; 0: Hansbrough JF, Boyce ST, Cooper ML, Foreman TJ. Burn wound closure with cultured autologous keratinocytes and fibroblasts attached to a collagen-glycosaminoglycan substrate. JAMA 989; 262: Duplan-Perrat F, Damour O, Montrocher C, et al. Keratinocytes influence the maturation and organization of the elastin network in a skin equivalent. J Invest Dermatol 2000; 4: The Authors Eric Dantzer MD, Plastic Surgeon Centre de Traitement des Brfil~s, H6pital L6on B6rard, BP 2, F Hyeres, France. Fabienne M. Braye MD, Plastic Surgeon Centre de Traltement des Brfil6s, Pavilion i, H6pital E. Herriot, Place d'arsonval, F Lyon, France. Correspondence to Dr Fabienne Braye. Paper received 20 February 200. Accepted 3 July 200, after revision. Published online 5 October 200.
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