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Reconstruction of the burned breast poses several clinical challenges, since scarring can adversely affect the development, contour and positioning of the breast as well as the cosmetic appearance of the skin surface. Conventional management entails contracture release and thick split-thickness skin grafting. We investigated an alternative approach employing dermal regeneration template (Integra) for breast reconstruction in 12 consecutive patients who had suffered anterior chest wall burns in childhood. Integra is a bilayer material consisting of a collagen and chondroitin-6-sulfate dermal regeneration template and a temporary silicone epidermal layer. Portions of the scar contracture preventing the breast from assuming the desired shape and position were excised. Unmeshed Integra sheets were applied to the wound bed immediately following excision. Sufficient vascularization of the forming neodermis occurred within 28 days on average to enable removal of the silicone layer and placement of unmeshed 0.005 in. epidermal autografts. Upon histological examination one month postoperatively, naturally-formed collagen fibres were observed in the dermal regeneration template. By one year, host collagen had typically completely replaced the Integra matrix, and elastic fibres were evident throughout the neodermis. Durable improvements in breast contour and shape were attained in all patients, and clinically-relevant recontracture of the graft site did not occur within the follow-up period. A statistically significant improvement of 6.0 (95% CI, 5.0–6.5) in Vancouver Scar Scale score was demonstrated at one year. A very high level of satisfaction in the outcome of reconstruction was expressed by 92% of the patients. Grafting with Integra provides an effective and well-tolerated alter-native to thick split-thickness grafting for breast reconstruction. Chief advantages are the availability of a biocompatible material in unlimited quantity that can be tailored to the particular wound site and the avoidance of a deep donor site wound with attendant potential for infection, scarring and permanent pigment changes.
Significant burns on the anterior chest wall in young girls can damage skin and nipple-areola complex, resulting in abnormal development of the breast. The breast bud itself lies in a relatively deep plane and is often protected from injury, and a longitudinal study of 28 girls revealed that, even with significant thermal injury involving the nipple-areolar complex, all patients developed breasts in adolescence.
However, stimulation of viable breast tissue growth subsequent to thermal injury can be inhibited by the tight burn scar in the overlying breast envelope, and these scars frequently distort the contour of the breast and alter its position relative to the contralateral breast.
Aesthetic considerations play an important role in reconstruction of the burned breast, since contour deformities of the breast are likely to affect the emotional well-being of young women adversely. Therefore, the goal in all breast reconstruction is aesthetic recontouring
and minimum creation of other wound sites that can contribute to psychological distress.
Conventional treatment for breast contour deformities has entailed contracture release by incision or excision of the restricting burn scar, followed by a thick split-thickness skin graft.
Other approaches for reconstruction of postburn breast deformities have included cutaneous flaps and Z-plasty, fasciocutaneous flaps, musculocutaneous flaps or skin expansion.
One drawback in the use of thick split-thickness grafts and flaps is the creation of an additional wound at the donor site. These donor site wounds are subject to infections and scarring, as well as changes in pigmentation that vary directly with the thickness of dermis taken in the graft.
Since dermis taken from a donor site does not regenerate, the residual dermal layer at that site remains thinner permanently. Moreover, graft donor sites can be a source of considerable pain and discomfort due to delayed healing. It is not uncommon for patients to complain more about the pain at the donor site than at the primary surgical site.
Split-thickness skin graft donor site management. A randomized prospective trial comparing a hydrophilic polyurethane absorbent foam dressing with a petrolatum gauze dressing.
Arch Otolaryngol Head Neck Surg.1995; 121: 1145-1149
The advent of a permanent skin substitute that contains a dermal regenerate template (Integra® Dermal Regeneration Template, Ethicon, Inc, Somerville, New Jersey, USA) has provided a new option for reconstruction of the burned breast. This bilayer membrane system for skin replacement has been shown effective in treatment of primary acute full- and partial-thickness burn injuries and in reconstructive surgery.
The porous Integra dermal regeneration template stimulates the synthesis of normal connective tissue matrix fibers from native fibroblasts and creation of a neodermis, without inflammation, foreign-body reaction or immunologic response.
Integra's silicone epithelial substitute is replaced with a very thin epidermal autograft once the dermal regeneration template becomes sufficiently vascularized. This study was undertaken to evaluate the utility of Integra in the reconstruction of the burned breast and its ability to minimise donor site morbidity because of the need for only a thin epidermal autograft.
2. Patients and methods
Over a 28-month period (November 1998 through February 2001), twelve consecutive female patients (12–27 years of age) with thoracic wall scars resulting from childhood burns underwent breast reconstruction using Integra dermal regeneration template. A total of 14 breasts were treated, with two patients undergoing bilateral breast treatment. In one patient correction of a tuberous contralateral breast was also needed to achieve symmetry of the breasts. Only one patient had prior reconstructive surgery—a Z-plasty—on the burned site. All patients gave their written informed consent for the surgical procedures and serial biopsies.
2.1 Dermal replacement template
Integra® Dermal Regeneration Template, a bilayer membrane system for skin replacement, is comprised of a three-dimensional porous matrix composed of cross-linked bovine collagen and shark chondroitin-6-sulfate covered by a temporary silicone epidermal substitute.
The biodegradable dermal replacement layer serves as a matrix for the infiltration of host fibroblasts, macrophages and endothelial cells from the surrounding tissue. Gradually endogenous collagen deposited by fibroblasts replaces the dermal matrix, and a neodermis is formed during a 2–3 week period.
The dermal layer is covered by a temporary silicone layer that serves to control moisture loss from the wound and minimise bacterial invasion during wound bed closure. After adequate vascularization of the dermal layer and upon availability of donor autograft material, the silicone layer is removed and a thin epidermal autograft is placed over the neodermis. Integra, which exhibits excellent biocompatibility and extended shelf life, is available in unlimited quantity and can be tailored to the wound site.
2.2 Surgical technique
Initially, the tight skin envelope of the burned breast was released by excising those parts of the scar contracture preventing the breast from assuming the desired position and shape. The operative plan for excision location and extent was based on the individual burn scar characteristics. Areas of scar contracture not contributing to the distorted breast contour were not excised. With appropriate excision and release, the inframammary fold was successfully established in our patients. Integra sheets were applied in unmeshed form to the excised wound bed immediately following excision and tailored to the wound site. Integra, which was placed on mammary gland tissue, fascia or hypodermis, was positioned to conform to the natural tension lines. Integra sheets were overlapped at their junctions to avoid hypertrophic scarring at the seams. Care was taken to achieve meticulous haemostasis of the surgical wound in order to prevent haematoma formation, which could result in reduced take. Integra was fixed in place with staples and covered with a dressing of gauze impregnated with nitrofurazone, and povidone-iodine was used to treat the edges of the defect. The wounds were examined on the first, second and fifth postoperative days for haematomas, template movements and local infection. In the first five days following surgery, bandages were attached with staples. Subsequently, bandages could be held in place by a brassiere. Dressings were changed twice per week on an outpatient basis. No special home care was required.
The neodermis was judged to be adequately vascularized when it was slightly white to ivory in color. Vascularization of the dermal replacement template occurred on average 28 days after Integra placement. The silicone epidermal layer was then removed from the vascularized matrix, and a thin split-thickness skin graft (0.005 in.) was harvested with a Zimmer dermatome (Zimmer, Dover, Ohio, USA) and placed on the neodermis. Autografts were harvested from the thighs in 11 patients and from the lateral lower chest in one patient. Donor sites were treated with silver sulfadiazine. The unmeshed autografts were stapled and covered with the same type of dressing employed after Integra placement.
2.3 Postoperative care and follow-up
Postoperative graft care was in accordance with the standard protocol at our institution. All patients received prophylactic ciprofloxacin antibiotic therapy following both the Integra graft and the autograft.
Serial postoperative biopsies using 3–4 mm cutaneous punches were performed at 1, 6 and 12 months after Integra placement in seven patients. In two patients, biopsies were also performed 2 years postoperatively. Specimens were fixed in formaldehyde, and hematoxylin eosin staining was performed. Staining techniques were also used to evaluate elastic fibres (Verhoeff's Van Giesen) and calcium (Von Kossa's method). Immunohistochemical staining using the avidin-biotin complex technique was used to assess the intermediate filament protein vimentin, which is indicative of mesenchymal cells; the smooth muscle proteins actin and desmin; collagen types I and IV; and the endothelial cell marker CD34.
Scar appearance at 6 and 12 months was scored using a modified Vancouver Scar Scale, which scores scars on pigmentation, pliability, vascularity and height and has a maximum score of 14.
Photographs were also taken to document results. In addition, at 6 and 12 months patients completed a short questionnaire that asked them to rate their satisfaction on a scale of 1–10 and included a visual analog scale to assess adverse events such as pain, dryness, pruritus and tightness.
2.4 Statistical analysis
The median difference in Vancouver Scar Scale score before and after treatment and its 95% confidence interval (95% CI) were determined by exact Hodges-Lehman estimation.
3. Results
Integra was used alone in eleven patients (12 breasts). For one patient, Integra was used on both breasts as a complement to lateral thoracic fasciocutaneous flaps and silicone implants. The amount of Integra used for each breast ranged from 8 to 190 cm2, with an average of 110.5 cm2. Take of the Integra graft was 100% in all patients, and no infections occurred. One patient developed a haematoma in the first 24 h after Integra placement, but it resolved satisfactorily and did not compromise take.
Partial autograft loss occurred on two breasts, but only one required further surgical management. The autografts healed within 8–25 days. Donor sites healed at approximately one week without complications, except for minor hypopigmentation or hyperpigmentation changes, which usually resolved by 6–12 months. The patients were discharged on average 5.5 days after each of the two stages of surgery, and follow-up of the patients ranged from 12 to 40 months, with an average of 21 months.
3.1 Histological findings
One month following Integra placement the dermal regeneration template was found to contain new, naturally-formed collagen fibres that were slightly thicker and shorter than those of normal dermis, as well as young granulation tissue (Fig. 1(a)) . Myofibroblasts were the most common cell type, staining positive for vimentin and actin and negative for desmin. As indicated by CD34 staining, new vascular channels were forming. Elastic fibres and cutaneous appendages were not present. In agreement with a histological study of acute burn patients who had received an Integra graft,
we observed giant cells in association with the remaining Integra collagen fibres. These giant cells, formed by a syncytium of macrophages, were seen in 6 of 7 patients examined histologically.
Fig. 1(a) At one month after Integra grafting, neodermis characterized by thick collagen fibres was present interspersed among still remaining Integra collagen matrix. New vessel formation was evident. Elastic fibres and cutaneous appendages were not present in the Integra graft, but elastic fibres, stained black with the Verhoeff Van Giesen method, were present in adjacent normal tissue (lower section of image). Biopsy was taken prior to autograft, and thus epidermis is not present. (b) At one year after Integra placement, neodermis is highly vascularized and contains a thick layer of organized host collagen. Elastic fibres of irregular configuration and distribution are present, as well as small areas of residual Integra matrix. Rete ridges have formed at the dermal-epidermal junction. No cutaneous appendages are present. Magnification of 100×.
By 5–6 months, the neodermis contained a thick layer of organized host collagen, and myofibroblasts were no longer detectable. Some short and thin elastic fibres were identified at the top of the neodermis in apposition to those elastic fibres of the papillary dermis portion of the autograft. Elastic fibres were also detectable in the lower neodermis in contact with the patient's underlying tissue, but the middle section of the neodermis contained no elastic fibres. Some residual Integra fibres were still detectable.
At one year after reconstructive surgery, host collagen had typically completely replaced the Integra matrix, and elastic fibres were present throughout the neodermis (Fig. 1(b)). However, the pattern of elastic fibers differed from that of normal tissue, being of more irregular configuration and distribution. In cases with persisting Integra fibers, elastification was less dense, and the elastic fibers were thinner and shorter. At two years postoperative, no residual Integra matrix was present.
3.2 Clinical findings
All patients achieved improved breast contour and shape, and these results were maintained throughout the follow-up period (Fig. 2, Fig. 3, Fig. 4, Fig. 5) . Recontracture of the graft site did not occur, except in one patient who was treated bilaterally and developed a slight recontracture in her left breast. Based on modified Vancouver Scar Scale scores at one year, the operative sites exhibited good or excellent pliability, height and vascularity and fair pigmentation. For the 14 treated breasts Vancouver Scar Scale scores declined postoperatively by a median of 6.0 (95% CI, 5.0–6.5) compared with the preoperative scores. The improvement in scar appearance was statistically significant (Table 1) .
Fig. 2Preoperative (a) frontal and (b) oblique view. (c, d) At 14 months follow-up, bilaterally treated breasts are of good shape and contour, but hypertrophic scars have occurred at the edges of the Integra graft where normal skin and graft meet. Scars were treated twice with locally-injected corticosteroids at an interval of one month. Some tightness has reoccurred in the left breast, but a re-release is not needed at this time.
Fig. 3Frontal view (a) before surgery and (b) at 8 months follow-up, at which time the right breast had attained a much improved shape and contour and good symmetry with the contralateral breast. (c) The lateral thoracic donor site at 8 months of follow-up has achieved an excellent cosmetic out-come.
Fig. 4Preoperative (a) frontal and (b) oblique view, showing tight skin envelope on right burned breast. (c, d) At 1 year follow-up this 27-year-old patient now has good mammary contour, and contracture has not recurred.
Fig. 5Preoperative (a) frontal and (b) oblique view. (c, d) At 6 months of follow-up, the breast has improved shape and contour, but hyperpigmentation has occurred at the graft site. (e, f) At 14 months, improvement of breast contour has been maintained, and hyperpigmentation, although still present, has lessened.
One 13-year-old patient who had undergone bilateral breast reconstruction developed hypertrophic scars in the graft margins of both breasts, but these responded well to two local injections of corticosteroids spaced one month apart (Fig. 2).
Hyperpigmentation also occurred at the Integra graft site in all patients (Fig. 5), but in all cases was observed to improve slowly over the follow-up period. By 12–18 months postoperatively, significant improvements in hyperpigmentation was evident.
Two patients experienced moderate pruritus in the early postoperative period, which resolved with pressure therapy and body lotion without need for medication. Five patients experienced persistent graft dryness, which could be remedied with body lotion, and by one-year follow-up this adverse effect was insignificant in all patients. No patient complained of local pain at either the graft or donor sites.
Eleven patients reported that they were very satisfied with the results. The remaining patient rated her outcome as satisfactory. The median satisfaction score was 8 out of a possible 10 (range, 6–9).
4. Discussion
This is the first report to focus on the use of Integra dermal regeneration template for reconstruction of the burned breast. This series of 12 patients demonstrates that Integra can be of value for this type of reconstructive surgery. Both good aesthetic and functional graft site outcomes could be achieved with the use of Integra, and donor site morbidity was minimal. Skin grafting of breast tissue is particularly amenable to this approach, because haemostasis and post-graft immobilization of the site during healing are readily achieved for this tissue type.
Excision of the burn scar from the breast produces a tissue plane which is fatty and often uneven. Integra can be readily shaped to match the wound site with a single sheet. Therefore, seams can be avoided, and the breast can assume a normal contour. The thickness of the dermal portion of Integra and formation of compliant, durable neodermis help avoid any step deformities such as those that can occur with conventional split-thickness grafts. The replacement dermis formed after dermal regeneration template application functions as normal dermis rather than as scar tissue. Similar to full-thickness grafts, Integra appears to minimise long-term postoperative recontraction. Moreover, the quality of the resulting skin was greatly improved. By six months postoperatively, grafted skin sites were generally comparable to normal skin in suppleness, pliability and elasticity.
An important advantage of this approach is the less extensive harvest from the donor site that is required. Neale recommends coverage of breast reconstructive sites with split thickness sheet grafts 0.016 in. or greater, but harvest of such thick grafts creates significant donor site scarring.
With Integra, a much thinner autograft is required. We harvested autografts of 0.005 in. thickness, only a third of what would have been necessary with a standard thick split-thickness autograft. All donor sites healed within a week without significant discomfort and regained a similar appearance to that of the surrounding skin between 6 and 12 months after surgery. Patients also usually experience little discomfort at the Integra graft site.
Another advantage of the dermal regeneration template, unlike autologous grafts, is that it does not require immediate vascularization. This eliminates a major concern for graft viability on large donor sites with substantial subcutaneous fat. Vascularization and the formation of the neodermis can proceed at a variable pace depending upon the individual donor site area without risk of losing the graft. In our series, the take for Integra grafts was 100%. We also were able to achieve a high take with the epidermal autografts, which we attribute in part to waiting until the dermal replacement template had become sufficiently vascularized, normally about one month after the first stage of surgery.
Use of this material involves a two-stage reconstruction. The silicone epidermal analog is purely prosthetic and must be removed and replaced with epidermal autograft several weeks after Integra placement. Also, Integra is devoid of intrinsic immunologic defenses and hence must be kept free of microorganisms. Therefore, it is essential that Integra only be placed on a fresh, clean wound bed with meticulous attention to haemostasis.
Recontracture and scarring were very limited with Integra use. Only one patient with bilateral breast reconstruction developed hypertrophic scars and tightness of one breast. This patient was among the youngest treated, and younger patients are much more likely to form hypertrophic scars than are older patients.
The reasons for this proclivity of the anterior chest to develop hypertrophic scars are unknown; however, skin tension, motion and regional vascularity may play a role.
Pruritus and dryness of the area were the most common troublesome symptoms for the patients. Histological studies have demonstrated that adnexal structures do not regenerate in Integra neodermis.
The lack of sweat glands is likely to contribute to dryness. In any case, the five patients who experienced persistent dryness could readily manage this adverse effect through application of body lotion. Transient pruritus in the early post-operative period occurred in two patients. Moiemen and colleagues in a study of reconstructive surgery patients reported an infiltration of the neodermis with large numbers of eosinophils, which could account for the pruritus.
In this study, we performed sequential histologic examinations on tissue samples from seven patients to correlate structural elements of the matrix with clinical appearance. Other histological studies of Integra have been reported, one in patients with acute burns
As in the previous studies, we observed the gradual formation of a well-structured neodermis. Moiemen et al noted that in the reconstructive surgery patients vascularization was not as rapid as that reported in the acute burn patient study of Stern et al, which showed vascularization throughout the entire thickness of the Integra matrix to be complete by the second week.
Moiemen reported that patent vascular channels at the superficial layer of the matrix were present only at the end of the fourth week. We also saw a slower vascularization than that reported by Stern et al. Moreover, in the acute patient study, the disappearance of the Integra fibres was reported to have occurred by 30 days.
In our population of reconstructive patients, Integra fibres persisted for at least 5–6 months. Therefore, the time frame of neodermis formation may be different in acute burn and reconstructive surgery patients, but all develop a compliant, durable neodermis.
Growth of subsequent breast tissue requires that the skin envelope expand over time. Integra graft sites have been shown to accommodate subsequent growth. Burke et al demonstrated a 250% expansion of Integra when applied to burned pediatric extremities.
In our current study population, we have not yet observed whether the Integra graft sites will accommodate subsequent breast growth successfully.
In summary, several noteworthy advantages are apparent with use of Integra in comparison with alternative approaches for reconstruction of the burned breast. Utilization of Integra minimises scarring, pigmentation change and contracture at the donor site. Integra allows the burned breast to assume a desirable contour and is much less prone to postoperative contracture compared with split-thickness autografts. In comparison to the various type of flap approaches, a better tissue match can be achieved with Integra, and the surgery is less invasive. Finally, use of Integra resulted in uniformly high patient satisfaction with the reconstructive surgery outcomes. Procedures employing of Integra offer a cost-effective and attractive option for reconstructive surgery of the burned breast.
References
McCauley R.L
Beraja V
Rutan R.L
et al.
Longitudinal assessment of breast development in adolescent female patients with burns involving the nipple-areolar complex.
Split-thickness skin graft donor site management. A randomized prospective trial comparing a hydrophilic polyurethane absorbent foam dressing with a petrolatum gauze dressing.
Arch Otolaryngol Head Neck Surg.1995; 121: 1145-1149
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