Restoration of Facial Form and Function After Severe Disfigurement from Burn Injury by a Composite Facial Allograft
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1 American Journal of Transplantation 2011; 11: Wiley Periodicals Inc. Case Report C 2011 The Authors Journal compilation C 2011 The American Society of Transplantation and the American Society of Transplant Surgeons doi: /j x Restoration of Facial Form and Function After Severe Disfigurement from Burn Injury by a Composite Facial Allograft B. Pomahac a, *,J.Pribaz a, E. Eriksson a,d. Annino b, S. Caterson a,c.sampson a, Y. Chun a, D. Orgill a,d.nowinski a and S. G. Tullius c a Division of Plastic Surgery, b Division of Otolaryngology and c Division of Transplant Surgery, Department of Surgery, Brigham and Women s Hospital, Harvard Medical School, Boston, MA *Corresponding author: Bohdan Pomahac, bpomahac@partners.org Composite facial allotransplantation is emerging as a treatment option for severe facial disfigurements. The technical feasibility of facial transplantation has been demonstrated, and the initial clinical outcomes have been encouraging. We report an excellent functional and anatomical restoration 1 year after face transplantation. A 59-year-old male with severe disfigurement from electrical burn injury was treated with a facial allograft composed of bone and soft tissues to restore midfacial form and function. An initial potent antirejection treatment was tapered to minimal dose of immunosuppression. There were no surgical complications. The patient demonstrated facial redness during the initial postoperative months. One acute rejection episode was reversed with a brief methylprednisolone bolus treatment. Pathological analysis and the donor s medical history suggested that rosacea transferred from the donor caused the erythema, successfully treated with topical metronidazol. Significant restoration of nasal breathing, speech, feeding, sensation and animation was achieved. The patient was highly satisfied with the esthetic result, and regained much of his capacity for normal social life. Composite facial allotransplantation, along with minimal and well-tolerated immunosuppression, was successfully utilized to restore facial form and function in a patient with severe disfigurement of the midface. Key words: Composite tissue allotransplantation, electrical burn, facial allograft, facial disfigurement, immunosuppression, restorative surgery Abbreviations: CTA, Composite Tissue Allotransplantation; CTA, Computer tomography angiography; ENT, Ear, nose and throat; FTA, Facial tissue allotransplantation; IRB, Institutional Review Board; MMF, Mycophenolate mofetil; r-atg, Rabbit antithymocyte globulin. Received 14 September 2010, revised 08 November 2010 and accepted for publication 09 November 2010 Introduction Facial tissue allotransplantation (FTA) is gaining clinical acceptance for the treatment of severe and complex facial deformities that cannot be effectively treated by the traditional reconstructive surgical modalities. FTA offers the unique option to treat complex facial defects secondary to traumatic injuries or oncologic resections by replacing missing anatomic structures in one major operation. The central region of the face is particularly difficult to reconstruct with conventional techniques. Multiple major staged procedures are usually required and the functional and esthetic outcomes still remain poor. A composite facial allograft encompassing the necessary soft tissue and bone requirement provides an excellent en bloc replacement of the entire three-dimensional missing component of the anatomically complex facial structures. Goals of this procedure are the restoration of the anatomy of nasal, oral, sinus and orbital cavities and the reestablishment of critical functions such as salivation, sensation and animation. A total of 13 face transplantations have been performed worldwide to date, of which some have been reported (1 5). Overall, results have been encouraging so far with regards to both functional and esthetic outcomes. It has been demonstrated that FTA has the potential to restore facial sensation, motor function, nasal breathing, articulation, as well as the oral intake of liquids and solid foods. Of note, esthetic and functional results have been far superior to those attainable by conventional reconstructive modalities. Successful FTA, however, requires lifelong immunosuppression. As the knowledge on specific aspects of the immunogenicity or the immune response following composite tissue allotransplants (CTA) is limited, most of our current experience in applying immunosuppression following CTA is based on the experience in whole organ transplants. The most commonly used maintenance therapy has been a combination of mycophenolate mofetil, tacrolimus and corticosteroids (6). Both IL-2 receptor antibodies and 386
2 Restoration with Composite Facial Allograft antithymocyte globulin have been used as induction treatments (1 4). In addition, adjunctive therapies such as extracorporeal photochemotherapy, bone-marrow transplantation and donor transplant irradiation have been reported (1,2). Moreover, transplantation of the face and limbs offers a unique opportunity to assess visible signs of rejection as well as to provide topical treatments. Until very recently, characteristic signs of chronic rejection had not been reported in CTAs. Early detection of skin changes and an immediate and successful treatment of acute rejections may help to reduce the risk for under-immunosuppression and represent an advantage compared to other organ transplants (6). However, chronic rejections have been reported most recently in recipients of hand transplants when immunosuppression had been reduced drastically (7). We report the results of our FTA, which led to a successful integration of the transplanted unit with functional and esthetic restoration of the face through the first year postoperatively. We report on a detailed analysis of immunosuppressive and antirejection treatment, including aspects of donor immunosuppression and the transfer of rosacea from the donor representing the clinical picture of rejection. Material and Methods The recipient was a 59-year-old male of Native American and Japanese background who suffered a high voltage electrical burn injury which resulted in a complex bony and soft tissue defect of his midface (Figure 1A). He was initially treated with serial debridements and reconstruction using an anterolateral fasciocutaneous free flap to separate the oral and the nasal cavities (Figure 1B and C). After an intensive screening by a multidisciplinary team of plastic, transplant and ear, nose and throat (ENT) surgeons, infectious diseases and evaluations by two psychiatrists (in their role as coinvestigator and study-independent specialists) and a social worker, the local Institutional Review Board (IRB) approved the patient s enrollment to the Facial Transplant Study. The functional deficits of the patient included inability to chew solid foods, drooling, absence of intelligible speech, restricted mouth opening, absence of nasal airway and bilateral epiphora. The patient s enrollment in the study was voluntary and the informed consent process was completed and documented. Extensive preoperative workup was then performed according to the study protocol (IRB Protocol Number: 2008P000550). This included a computer tomography angiography (CT) with three-dimensional Figure 1: (A) Patient on admission following high voltage injury to face. (B) Patient after debridement. (C) Patient after reconstruction with anterolateral thigh flap. American Journal of Transplantation 2011; 11:
3 Pomahac et al. Figure 2: 3D CT scan depicting the extent of midfacial bone defect, including the entire maxilla, nasal bone and zygomatic bones. (3D) reconstruction to outline the bony defect and vascular anatomy for precise surgical planning (Figure 2). The patient was enrolled on the transplant wait-list in January The donor was a 60-year-old Caucasian male who suffered irreversible brain damage during heart transplantation. Donor and recipient were blood group compatible (O and A), and had a 3/6 HLA mismatch. Serologies were cytomegalovirus (CMV) positive for the donor and CMV negative for the recipient. Surgical and technical details of the FTA have been described previously (5). Briefly, the nasal, oral and maxillary sinus mucosa, zygomatic and maxillary bones including teeth, nasal cartilage, muscles of facial animation, with accompanying nerves and skin were included in the composite graft. Following the donor procedure which lasted 6 h, the graft was taken from the operative field and immediately flushed with cold University of Wisconsin solution. Secured in a sterile double bag containing ice slurry, the graft was brought to the adjacent recipient operating theater. The procurement of the facial graft was followed by recovery of solid organs by the transplant surgery team. On completion of solid organ recovery, a prosthetist fashioned a mask over the major tissue defect to restore the donor s facial appearance. Revascularization between external carotids on the left side and facial arteries on the right side with corresponding veins was accomplished in 75 min during which the graft was maintained cooled. Remnants of recipient s maxilla were removed to the level of pterygoid processes corresponding to the level of retrieved maxilla of the donor. Following reconnection of buccal and infraorbital nerves, the bone was miniplated at the nasal root, and infraorbital rims. Neurorrhaphy was subsequently performed of five facial nerve branches on the right and six on the left side of the face at the level immediately anterior to the parotid gland. The skin was trimmed appropriately to allow a moderate redundancy covering the vascular anastomoses. A radial sentinel forearm flap was used to monitor rejection. In this particular case, it also served the purpose to release a first web-space contracture of the right hand. This contracture was a sequela from the electrical burn injury. Scar release and coverage of the resulting defect with the radial forearm flap improved the range of motion of the right thumb. Prior to reperfusion, the recipient had received 500 mg of methylprednisolone and rabbit antithymocyte globulin (r-atg, 1.5 mg/kg) and the patient had received 1000 mg mycophenolate mofetil (MMF) prior to surgery. Maintance immunosuppression was continued with MMF 1000 mg bid, tacrolimus (adjusted to trough level of ng/ml) and Steroid taper (20 mg on day 5) (Figure 3). Antiviral and bacterial prophylaxis consisted of Cefazolin (1 gm) perioperatively, Trimetoprim Sulfamethoxasole Figure 3: Induction immunosuppressive therapy. 388 American Journal of Transplantation 2011; 11:
4 Restoration with Composite Facial Allograft (400 mg/day) for 6 months and Valganciclovir (900 mg/day) for 1 year. Total operative time was 17 h. Estimated blood loss during the procedure was <100 cc. The patient was followed up according to the study protocol with regular evaluations by our multidisciplinary CTA team, including plastic and transplant surgery, pharmacy, infectious disease, ENT, psychiatry, nutrition, physical, speech and swallow and occupational therapy, as well as social services. Rejection was monitored by clinical examination and biopsies of facial and sentinel flap skin. The biopsies were obtained at regular, predetermined time-points and upon suspicion of rejection based on clinical examination. The predetermined biopsy time points were 1, 2 and 4 weeks, and 3, 6 and 12 months postoperatively. Rejection was graded I-IV according to the Classification of Clinical Acute Skin Rejection by Cendales et al. (8). Drug levels and drug toxicity were monitored. Sensory function was assessed by serial evaluations of sensation to light touch, pinprick, cold and two-point discrimination. Light touch was assessed by application of cotton swab and cold sensation by application of a metal object cooled in ice water. Evaluation of facial motor function was performed by clinical examination according to the standardized protocol. Results Early postoperative recovery proceeded without complications Wound healing of the face and radial forearm flaps proceeded without complications. The initial facial edema resolved by day 21. The mucous membranes of the oral and nasal cavities healed uneventfully and healing of the skin resulted in normotrophic scars. The patient was discharged from the hospital on postoperative day 15. Clinical events including acute rejection and transmission of rosacea The first biopsy obtained from the sentinel flap 8 days after the procedure did not show any signs of rejection. By postoperative day 17, however, the patient developed facial redness, and both facial and sentinel flap biopsies confirmed mild acute rejection which was treated with by a methylprednisolone bolus (500 mg 3). The histologic evaluations of all subsequent biopsies obtained during the first half of the first postoperative year revealed findings consistent with minimal to mild rejection (Figure 4A C). The sentinel flap biopsies were predominantly assessed as grade I, while facial biopsies were graded as I-II or II. Prednisolone was maintained at doses between 15 mg/day and 30 mg/day during this period. The patient was given 2000 mg/d of MMF for the most part during the immediate postoperative course; MMF had to be reduced in response to gastrointestinal side effects on two occasions. Consecutively, MMF was switched to mycophenolic acid at doses ranging from 720 mg/day to 1120 mg/day. Tacrolimus doses ranged from 6 12 mg/day with 12 h trough levels averaging 10 ng/ml. Steroid bolus treatments were furthermore applied for suspected acute rejections on days 74 and 107; topical treatment included clobetazol cream on days and and tacrolimus cream on days Despite this treatment the redness persisted and the facial skin biopsy on day 105 still showed evidence of grade II acute rejection (Figure 5). The therapeutic failure and the discrepancy between facial and sentinel biopsies prompted us to look for other causes of the facial redness and cutaneous lymphocytic infiltrates. A donor history of rosacea was brought to our attention at this time. Indeed, the histologic picture of rosacea is indistinguishable from that of low-to-moderate acute rejection. Subsequently, the patient was immediately started on metronidazol cream on day 115 and the facial redness disappeared effectively, suggesting the diagnosis of rosacea. The facial skin biopsy at 6 and 12 months demonstrated no signs of rejection. One hundred and sixty days after the procedure, the patient s immunosuppression was adjusted to a daily regimen of 5 mg bid of tacrolimus, 720 mg of mycophenolic acid and 10 mg prednisolone. Subsequently tacrolimus levels have been lowered to 1 mg bid 9 months postoperatively with average trough levels of 5 8 ng/ml and prednisone was discontinued on day 360. No further clinical signs of rejection or rosacea occurred following initiation of treatment with metronidazol for facial redness. As a side effect to the immunosuppression our patient developed new-onset insulin-dependent posttransplant diabetes. HbA1c levels have been stable, and since the discontinuation of steroid treatment the insulin requirements have been substantially reduced to the current regimen of Humalog mix 75/25, 25 U in the morning and 10 U at night. The patient s renal function remained stable with norm values for serum creatinine throughout his follow-up and no infectious complications were observed posttransplant. The composite facial allograft restored facial form Restoration of normal midfacial anatomy was achieved by the facial allograft. The scars, although fine, were visible and created a demarcation line between the donor and the native recipient facial skin. This effect is an inevitable disadvantage with partial facial transplantation. Initially, the esthetic outcome was negatively compromised by a somewhat mask-like appearance with accentuated soft tissue ptosis. A secondary revision procedure with trimming of redundant cheek skin was performed 6 months after the initial transplant procedure. Thereafter, facial animation gradually improved which markedly enhanced overall facial appearance due to increased resting tone. At 1-year followup, the esthetic outcome was assessed to be excellent by the investigating team, and the patient was highly satisfied with the result (Figure 6A). The control CT performed 15 months after the procedure, showed successful skeletal integration with union between donor and recipient facial bones (Figure 6B). American Journal of Transplantation 2011; 11:
5 Pomahac et al. Figure 4: (A) Diagram of biopsies and antirejection treatment. The rejection grade was generally higher on biopsies obtained from the face compared to sentinel flap biopsies. (B and C) Histologic picture corresponding to grade II rejection persisted in face biopsies despite systemic and topical antirejection treatment. Histology can be interpreted as rosacea. The composite facial allograft restored facial functions Oral intake was initiated successfully after 3 days postoperatively. Speech improved immediately following the transplantation due to restoration of the hard palate. Patient s functional nasal airway was immediately established, improving his ability to breath and smell. Sensation corresponding to the second division of the trigeminal nerve was gained gradually between the third and sixth postoperative months. By 6 months, the patient had sensation to light touch, pinprick, cold, and a two-point discrimination of 15 mm throughout the entire facial flap. Motor function of the facial nerve was slower to acquire, nonetheless, continued to improve gradually during the second half of the first postoperative year. By 1 year postoperatively, the patient was able to smile symmetrically with approximately 2 3 cm excursion of the corners of his mouth, and gained control of the transplanted upper lip. However, ability to pucker or blow with his lips is absent to date. Psychosocial The patient returned to his living facility within 5 weeks after the operation and became fully reintegrated into the community with enhanced social capacity. No significant 390 American Journal of Transplantation 2011; 11:
6 Restoration with Composite Facial Allograft Figure 5: Appearance of the patient 2 months after surgery. The persistent facial redness during the first four postoperative months was mainly caused by rosacea transferred from the donor. issues emerged regarding the patient s facial appearance. Although the donor s wife reported being able to recognize her husband s nose in the patient, the patient considered it to be a close match to his original nose in size and shape. Following the procedure the patient reconnected with his daughter and his divorced wife. The concern about function of the new facial part prevailed in the patient s mind over esthetic appearance. Discussion We present the 1-year postoperative outcome of a composite facial allograft performed in a patient with severe facial disfigurement from electrical burn injury. Facial form and function were successfully restored to the extent unattainable by conventional reconstructive modalities. This achievement was the result from a coordinated multidisciplinary team approach with current efforts of evaluating additional patients for face and now also hand transplants based on approved IRB protocols. The need for life-long immunosuppression is one of the main concerns with CTA. Over-immunosuppression is associated with risks for serious side effects such as nephrotoxicity, diabetes mellitus, skin cancers and infections, while under-immunosuppression may lead to repeated episodes of acute rejection, which ultimately increase the risk for chronic rejection. We used an induction treatment Figure 6: (A) Appearance of the patient 12 months following transplantation. (B) 3D CT obtained 12 months after surgery, depicting skeletal integration of transplanted donor maxillary bone. with four doses of r-atg and a maintenance immunosuppression with tacrolimus, mycophenolate mofetil and steroids. This has been the most widely used and thoroughly evaluated maintenance protocol for CTA of face and upper extremity. Chronic rejection has only been reported in recipients who discontinued or reduced the immunosuppression substantially (7). In our patient, the diagnosis of acute rejection was inadvertently suspected due to the clinical sign of facial redness and histopathologic finding of cutaneous lymphocytic infiltrates, when in actuality, the symptoms were caused by rosacea transferred from the donor. Given the differences between the tissues of the facial allograft and the monitoring sentinel flap, and greater American Journal of Transplantation 2011; 11:
7 Pomahac et al. content of lymphatic tissue in the face, we did not consider negative mucosal or sentinel flap biopsies to be reliable. The positive clinical and histological signs of rejection in the facial allograft lead us to treat it as such. Treatment against suspected acute rejection was given systemically and topically at repeated occasions and maintenance therapy was adjusted to slightly higher levels. Thus, our patient might have been relatively over-immunosuppressed before the diagnosis of rosacea was made and appropriate antirosacea treatment was started. Long term, however, we could keep our patient on an overall minimal and steroidfree immunosuppression. In retrospect it remains difficult to determine the precise number of true acute rejection episodes with certainty. However, we can assume that, overall, acute rejection episodes were mild and well controlled by the therapy provided. The only observed side effect was a new onset posttransplant diabetes. This condition had improved significantly following the discontinuation of steroids. The patients HbA1c stayed between 5.8 and 7.8 and his insulin requirement is continuously declining. The facial rosacea illustrates the potential issue of donorto-recipient disease transfer in organ transplantation. The routine donor workup screens for all relevant malignancies and infections prior to organ procurement. However, the practice of CTA introduces new concerns for transferring dermatological conditions. To our knowledge, this is the first reported case with transfer of a benign, chronic dermatological disease with CTA. Rosacea is a dermatosis of unknown etiology primarily found in Caucasians of north European descent. The frequency of rosacea has been difficult to establish, mainly because of differences in diagnostic criteria. A frequently cited Swedish study reports a prevalence of 10% (9). The pathogenesis includes chronic inflammation with vasodilatation and extravasation of plasma proteins. Facial redness is the main clinical symptom, and histologic changes usually consist of rather unspecific perivascular and perifolicular lymphocytic infiltrates. Based on the relatively high incidence of rosacea and its clinical presentations similar to acute skin rejection this condition should be kept in mind as a possible differential diagnosis when evaluating persistent facial redness despite antirejection treatment in future FTA cases, especially in Caucasians. The restoration of complex facial functions requires the identification and reconnection of nerves of facial sensation and animation. In accordance with previously published cases, sensory function was gained gradually to near normal levels over the first 3 6 postoperative months. We performed a meticulous neurorrhaphy of all involved sensory nerves. Others have reported on comparable return of sensory functions by 3 6 months follow-up without having performed sensory nerve coaptation (2 4). Thus, return of sensation can be expected without surgical reestablishment of sensory nerve continuity, a phenomenon most probably explained by outgrowth and sprouting of free sensory nerve endings. However, we believe that sensory nerves should be reconnected whenever possible in order to provide the best probability of early and complete return of sensory functions. Similarly, the importance of both sensory and motor neurorrhaphies for the restitution of nerve functions in facial CTA was recently demonstrated in a murine model for heterotopic composite midface allotransplantation (10). As expected, facial nerve function returned more slowly and facial animation continued to make progress throughout the first postoperative year. Guo et al. reported poor facial nerve function at 2-year follow-up which was expected considering the suboptimal anatomic conditions for reliable facial nerve anastomosis at the stylomastoid foramen in their case (2). The Cleveland team performed bilateral facial nerve trunk coaptation with interpositional nerve grafts, and presented symmetric smiling and upper lip occlusion at 6-month follow-up (4). Lantieri et al. anastomosed the facial nerve main trunks in their case of FTA in a patient with neurofibromatosis, and demonstrated return of spontaneous mimicry after 9 months (3). Dubernard et al. performed distal neurorrhaphy at the inferior branch of the left facial nerve, and their patient had a normal smile after 18 months (1). We performed multiple bilateral neurorrhaphies at a level anterior to the parotid glands. This distal anatomic approach involving multiple nerve branches was chosen to provide the best possible conditions for targeted motor innervation. Interestingly, in addition to a steady and symmetric return of voluntary facial animation, the patient did not present with any synkinesis during the entire postoperative period. Physical, occupational and speech therapy started during the first postoperative week. We anticipated facial motor and sensory function to return by postoperative months 3 6. At that time occupational and speech therapy became critical to augment the return of spontaneous motor function. Direct comparisons of outcomes between facial transplant cases are, however, difficult. This is mainly due to the variability of the extent of the underlying facial disfigurement, but also due to a lack of uniform protocols and methods for outcome analysis. Importantly, considering the importance of facial animation for the ability to express emotions and to communicate with others, we believe that no efforts should be spared to optimize the conditions facial nerve regeneration. Our patient s acceptance of his face transplant and his appearance were unequivocally positive. From the beginning, enhancement of function was his priority, appearance a secondary concern. The patient integrated well into his environment and became more socially active. Our facial transplant case has successfully restored significant facial form and function in a severely disfigured patient. This achievement is attributed to the invaluable multidisciplinary approach, addressing all aspects of FTA, from preoperative preparations and review of the details of surgical technique, to long-term follow-up of the patient s somatic as well as psychological condition. This experience 392 American Journal of Transplantation 2011; 11:
8 Restoration with Composite Facial Allograft is the basis for our current efforts in expanding our composite tissue transplant program. Acknowledgments We thank Drs. Francisco Marty, Frank Rybicki, Edgar Milford and Anil Chandraker. Disclosure The authors of this manuscript have no conflicts of interest to disclose as described by the American Journal of Transplantation. References 1. Dubernard JM, Lengele B, Morelon E et al. Outcomes 18 months after the first human partial face transplantation. N Engl J Med 2007; 357: Guo S, Han Y, Zhang X et al. Human facial allotransplantation: A 2-year follow-up study. Lancet 2008; 372: Lantieri L, Meningaud JP, Grimbert P et al. Repair of the lower and middle parts of the face by composite tissue allotransplantation in a patient with massive plexiform neurofibroma: A 1-year follow-up study. Lancet 2008; 372: Siemionow M, Papay F, Alam D et al. Near-total human face transplantation for a severely disfigured patient in the USA. Lancet 2009; 374: Pomahac B, Lengele B, Ridgway EB et al. Vascular considerations in composite midfacial allotransplantation. Plast Reconstr Surg 2010; 125: Whitaker IS, Duggan EM, Alloway RR et al. Composite tissue allotransplantation: A review of relevant immunological issues for plastic surgeons. J Plast Reconstr Aesthet Surg 2008; 61: Kanitakis J, Jullien D, Petruzzo P et al. Clinicopathologic features of graft rejection of the first human hand allograft. Transplantation 2003; 76: Cendales LC, Kirk AD, Moresi JM, Ruiz P, Kleiner DE. Composite tissue allotransplantation: Classification of clinical acute skin rejection. Transplantation 2006; 81: Berg M, Liden S. An epidemiological study of rosacea. Acta Derm Venereol 1989; 69: Siemionow M, Klimczak A. Advances in the development of experimental composite tissue transplantation models. Transpl Int 2010; 23: American Journal of Transplantation 2011; 11:
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