ORIGINAL ARTICLE
Management of Neglected Periorbital Squamous Cell Carcinoma Requiring Orbital Exenteration Furkan Erol Karabekmez, MD, FEBOPRAS, Muhammed Nebil Selimoglu, MD, Ahmet Duymaz, MD, FEBOPRAS, Mehtap Sen Karamese, MD, Mustafa Keskin, MD, FEBOPRAS, and Nedim Savaci, MD
pproximately 500,000 new malignancies of the head and neck are diagnosed worldwide every year.1 Malignant tumors of the orbit and orbitomaxillary area represent 4% to 8% of head and
neck malignancies.2 Periorbital malignancies, including squamous cell carcinoma (SCC), basal cell carcinoma, and mesenchymal tumors, may develop or invade the globe, palpebrae, and orbital bony structures, especially in neglected cases. Basal cell carcinoma is the most common skin cancer of the periorbital region.3 However, orbital exenteration is not common in cases of basal cell carcinoma because of its slow progression. Squamous cell carcinoma is the second most common cancer of the periorbital region.4 It may spread into the periorbital structures, orbit, and nerves such as the branches of the trigeminal nerve, facial nerve, and extraocular nerves in the early stages because of its perineural invasion capacity.5,6 Orbital exenteration is required when the tumor invades the orbital musculature or the orbit itself. This procedure involves removal of the eye together with other orbital contents within the bony socket.5 Bony resection may be required if invasion has occurred.7 The orbital exenteration procedure results in significant morbidity in the face, which negatively affects the patient’s social life. Reconstruction of such defects may be challenging.8 Accurate reconstructive techniques should be chosen to fill the defect, establish contour symmetry with the opposite side of the face, and gain suitable soft tissue for further socket repair for prosthetics.9 Bone grafting with free soft tissue flaps or free osteocutaneous flaps has been used for exenteration cases involving concomitant defects on the orbital rims10Y12 When large amounts of soft tissue are present and bony resection is performed on both the frontal and maxillary sides together with exenteration, a bulky flap that separates the intracranial contents from the sinus cavity may be required.13 Although increased collaboration among different departments, progressive treatment planning, and consideration of reconstructive options that can cover almost all types and sizes of defects have enabled surgeons to perform adequate resection with no hesitation, patients with advanced SCC still have a 5-year survival rate of less than 50%.14Y16 We reviewed patients with SCC in the periorbital area requiring orbital exenteration in our clinic. The aim of this study was to evaluate the indications for exenteration, rate of histopathologically positive surgical margin, size of the defects, reconstruction options, location of the lesions, and survival of these patients.
From the Abant Izzet Baysal Universitesi, Tip Fakultesi, Plastic Cerrahi AD, Bolu, Turkey. Received February 17, 2013. Accepted for publication August 26, 2013. Address correspondence and reprint requests to Furkan Erol Karabekmez, MD, FEBOPRAS, Abant Izzet Baysal Universitesi, Tip Fakultesi, Plastik Cerrahi AD, 14000, Bolu, Turkey; E-mail: [email protected]; [email protected] The study protocol was approved by the local ethics committee. No funding was received for this study. The authors report no conflicts of interest. Copyright * 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000333
This study was retrospective, and ethical committee approval was obtained. A chart review of patients’ records was conducted to identify all patients with periorbital SCC requiring orbital exenteration from 2006 to 2011. A total of 9 patients who met the criteria were included in the study. Patient demographics, surgical technique, hospitalization period, necessity for postoperative intensive care, survival, defect size, surgical margins, radiotherapy and chemotherapy (RT-CT), lymphadenopathy status, distant metastasis, relapses, and operation length were assessed.
Abstract: With its perineural invasion capacity, periorbital squamous cell carcinoma (SCC) may easily invade orbital structures. When SCC invades the orbital musculature or the orbit itself, orbital exenteration, one of the most disfiguring operations on the face, is required. We reviewed elderly patients with periorbitally localized SCC requiring orbital exenteration to evaluate reconstructive options and survival. A chart review of patients’ records was conducted to identify all patients older than 65 years with periorbital malignancy requiring orbital exenteration from 2006 to 2011. A total of 9 patients who met the criteria were included in the study. The mean age at surgery was 77 T 6.7 years, and the mean defect size was 74.2 cm2. All patients had a similar history of late presentation to a doctor because of hesitation to undergo surgery. The temporoparietal fascia flap, galeal flap, free gracilis flap, and free vastus lateralis musculocutaneous flap were the treatment options for reconstruction of the defects. All patients died during follow-up, and the mean survival was 15.7 months (range, 6Y36 months). Only 2 of them had relapse before the death. Our small series suggest that elderly patients with periorbital SCC requiring orbital exenteration may not have enough survival to relapse because of the death from different causes without relapse or any sign of spreading cancer. Also, prolonged surgery with free flap reconstruction may increase the risk of postoperative intensive care unit requirement. Because local flaps may work very well for reconstructing the orbital exenteration defects, free flap option should be kept for selected cases. Key Words: Periorbital tumor, squamous cell carcinoma, orbital exenteration (J Craniofac Surg 2014;25: 729Y734)
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The Journal of Craniofacial Surgery
PATIENTS AND METHODS
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TABLE 1. Demographics, Treatments, and Outcomes of All Cases
Case 1 2 3 4 5 6 7 8 9
Age, y
Sex
Flap
Hospital Stay, d
ICU
Survival
Defect Size, cm2
Surgical Margins
RT, CT
Neck USG
Metastasis
Surgery, h
82 80 69 74 81 83 65 75 84
Female Female Female Female Female Female Male Male Female
Galea frontalis flap, STSG STSG Free gracilis Free vastus lateralis Temporalis muscle flap, STSG Temporalis muscle flap, STSG Temporalis muscle flap, STSG Temporalis muscle flap, STSG Temporalis muscle flap, STSG
15 15 10 19 35 7 7 15 21
0 0 3 4 0 0 0 0 0
7 11 7 14 12 24 36 24 12
156 80 63 64 63 36 20 36 150
Positive Negative Positive Negative Positive Positive Positive Negative Positive
RT, CT RT, CT V V RT, CT RT, CT V RT, CT V
(+) (j) (j) (j) (j) (j) (j) (j) (j)
Lung Lung V V V V V V V
3.5 4.5 7 9 4.5 3.5 3.5 3.5 4.5
Statistical Analysis Correlations among age, flap options (local flap and graft versus free flap), hospitalization period, intensive care unit (ICU) stay, survival, defect size, positive surgical margin, RT-CT status, lymphadenopathy status, lung metastasis, and duration of the surgery were evaluated using Spearman correlation coefficient test. Survival analysis was performed with a Kaplan-Meier survival curve. All statistical analyses were performed using PASW version 18 software. All tests were 2-sided, and P G 0.05 was considered to indicate statistical significance.
RESULTS Of the 9 patients studied, 2 were male, and 7 were female, with a mean age at surgery of 77 T 6.7 years (range, 65Y84 years). Patient characteristics are summarized in Table 1. All patients had biopsyproven SCC before the surgery and had indications for exenteration because of radiologically demonstrated invasion to the orbital musculature or globe. Two of the patients presented with a frontoorbital mass, 2 with a lower lid mass, 2 with a malar mass, and 2 with a medial canthal mass. Eight of the patients had ulceration of their lesions. Six patients had edema, 1 had hyperemia of the medial canthus, and 1 had loss of vision upon presentation. No patients had diplopia. One patient had a positive lymph node on ultrasonography and neck dissection. The others had negative neck ultrasonography results.
Seven patients presented with relapses of previously excised SCC, and the remaining 2 were primary cases in their first examinations. Lung metastasis was detected preoperatively in 3 patients. Six patients underwent bony resection together with orbital exenteration, and 3 underwent only orbital exenteration. The mean defect size was 74.2 cm2 (range, 20Y156 cm2). Defect reconstruction was performed with a temporoparietal fascia flap with split-thickness skin graft (STSG) in 5 patients, a galeal flap with STSG in 1 patient, only STSG in 1 patient, a free gracilis flap in 1 patient, and a free vastus lateralis musculocutaneous flap in 1 patient (Figs. 1Y7). The mean duration of surgery was 5.0 hours for all patients (range, 3.5Y9 hours). In patients treated with free and local flaps, the mean durations of surgery were 8.8 and 3.8 hours, respectively. The average length of hospitalization was 16.6 days (range, 7Y35 days). Two patients who underwent free flap reconstruction stayed 3 and 4 days, respectively, in the ICU. None of the patients who underwent reconstruction with local flaps and graft needed to stay in the ICU. Three patients had minimal graft loss; there were no complications in the remaining 6 patients. Six of the patients had positive margin in the histopathologic examination. Five patients underwent CT and RT during the postoperative period, and the rest of the patients chosen to decline therapy. All patients died during the follow-up; the mean survival was 15.7 months (range, 6Y36 months). Two had relapsed tumors before death, and the others died of unrelated causes.
Statistical Analysis All of the parameters were compared regarding to the Spearman correlation test, and the results were summarized in Table 2. Flap options (free vs local) and number of days patient stayed in ICU showed a significant positive correlation (P G 0.001). Flap options and
FIGURE 1. A, An 82-year-old patient presented with a left fronto-orbital ulcerated mass (patient 1). B, Wide resection applied. C, A galeal flap was raised to close the defect. D, The flap was extended to repair the socket.
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FIGURE 2. Same patient in Figure 1 with 1-week (A) and 1-month (B) postoperative views (patient 1).
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Neglected Periorbital SCC
FIGURE 5. A, Same patient’s intraoperative view with exenteration defect (patient 6). B, Temporalis muscle flap raised. C, Flap advanced over the lateral orbital rim. D, Donor area closed.
mentioned correlations (Table 2). For all patients, the 1-year survival rate was 50.5%, based on the Kaplan-Meier survival curve (Fig. 10).
FIGURE 3. A, A 74-year-old female patient presented with an ulcerated lesion on the left malar region, involving the ipsilateral lower lid, medial canthus, and orbit (patient 4). B, Maxillectomy and orbital exenteration were performed, and a negative surgical margin was verified by frozen section examination. C, A free vastus lateralis musculocutaneous flap was raised for reconstruction of the defect. D, Immediate postoperative view.
duration of the surgery showed a significant positive correlation (P = 0.02) (Fig. 8). Patient duration of stay in ICU and duration of the surgery also showed a significant positive correlation (P = 0.01). However, there was a strong negative correlation between defect size and survival (P = 0.02) (Fig. 9). There were no significant correlations between ages, flap options, duration of hospitalization, ICU requirement, survival, defect size, positive surgical margin, RT-CT, positive neck ultrasonography (USG), lung metastasis, and duration of the surgery except previously
FIGURE 4. A, An 83-year-old patient presented with an ulcerated lesion on her right lower lid (patient 6). B, Postoperative view after reconstruction of the exenteration defect with temporalis muscle flap and STSG repair.
DISCUSSION Squamous cell carcinoma is the second most common cancer of the eyelid, and its perineural invasion capability and relatively rapid progression create a high risk for exenteration. Huge SCC is mostly a problem of elderly patients,17 and invasion to orbital structures is seen mostly in neglected cases. Our literature search yielded no data on the survival of patients specifically with periorbital SCC requiring exenteration. In the present study, patients with advanced SCC had a 1-year survival rate of around 50%. However, it is difficult to conclude that periorbital SCC requiring exenteration always has a grave prognosis because of the small sample size, older population, and different causes of death in the current study. A larger clinical series may provide a definitive conclusion regarding the survival of patients with advanced periorbital SCC.
FIGURE 6. A, A 65-year-old male patient presented with a lesion on his left lower lid (patient 7). B, The exenteration defect. C, A temporalis muscle flap was passed under the lateral orbital rim. D, Four-month postoperative view.
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FIGURE 8. There was a significant difference between local flap and free flap reconstruction applied cases according to duration of surgery as expected (P = 0.04).
FIGURE 7. A, An 84-year-old patient presented with relapse of a previously treated SCC lesion in her left periorbital region. B, After wide resection and exenteration, the defect required free flap reconstruction. C, Development of cardiac dysrhythmia and hemodynamic instability during the operative period pushed the surgeon to finish the operation as quickly as possible. Therefore, a temporalis muscle flap and advancement of residual cheek tissue and STSG were used for reconstruction. D, A 4-week postoperative photograph showing minimal graft loss over the frontal area.
Although tumors close to vital structures such as the orbital globe may limit the decision regarding to the excision margins, the literature suggests that treatment of head and neck area’s SCC that requires orbital exenteration should be as aggressive as needed to obtain negative surgical margins. This type of aggressive excision will result in big 3-dimensional defects to be reconstructed, and both local and free flap options should be on the table. We presented
TABLE 2. Correlations Between All the Parameters Correlations
Age Local-free Hospital stay ICU stay Survival Defect size + Surgical margin RT-CT Neck USG Lung metastasis Surgery (h)
r P r P r P r P r P r P r P r P r P r P r P
Age
Local-Free
Hospital Stay
ICU Stay
Survival
Defect Size
+ Margin
RT-CT
Neck USG
Lung Metastasis
Surgery (h)
1.000 0. j0.518 0.154 0.366 0.333 j0.502 0.168 j0.203 0.601 0.504 0.166 0.274 0.476 0.433 0.244 0.274 0.476 0.207 0.593 j0.213 0.583
j0.518 0.154 1.000 0. 0.000 10.000 0.992* 0.000 j0.262 0.496 0.052 0.894 j0.189 0.626 j0.598 0.089 j0.189 0.626 j0.286 0.456 0.771† 0.015
0.366 0.333 0.000 10.000 1.000 0. 0.047 0.905 j0.297 0.437 0.562 0.115 j0.187 0.631 0.044 0.910 0.000 10.000 0.000 10.000 0.480 0.191
j0.502 0.168 0.992* 0.000 0.047 0.905 1.000 0. j0.208 0.591 0.069 0.860 j0.250 0.516 j0.593 0.092 j0.188 0.629 j0.283 0.460 0.777† 0.014
j0.203 0.601 j0.262 0.496 j0.297 0.437 j0.208 0.591 1.000 0. j0.766† 0.016 j0.139 0.722 j0.088 0.822 j0.485 0.185 j0.577 0.104 j0.418 0.263
0.504 0.166 0.052 0.894 0.562 0.115 0.069 0.860 j0.766† 0.016 1.000 0. j0.046 0.906 0.044 0.911 0.552 0.123 0.626 0.071 0.349 0.358
0.274 0.476 j0.189 0.626 j0.187 0.631 j0.250 0.516 j0.139 0.722 j0.046 0.906 1.000 0. j0.158 0.685 0.250 0.516 j0.189 0.626 j0.243 0.529
0.433 0.244 j0.598 0.089 0.044 0.910 j0.593 0.092 j0.088 0.822 0.044 0.911 j0.158 0.685 1.000 0. 0.316 0.407 0.478 0.193 j0.507 0.164
0.274 0.476 j0.189 0.626 0.000 10.000 j0.188 0.629 j0.485 0.185 0.552 0.123 0.250 0.516 0.316 0.407 1.000 0. 0.661 0.052 j0.364 0.335
0.207 0.593 j0.286 0.456 0.000 10.000 j0.283 0.460 j0.577 0.104 0.626 0.071 j0.189 0.626 0.478 0.193 0.661 0.052 1.000 0. j0.165 0.671
j0.213 0.583 0.771† 0.015 0.480 0.191 0.777† 0.014 j0.418 0.263 0.349 0.358 j0.243 0.529 j0.507 0.164 j0.364 0.335 j0.165 0.671 1.000 0
The first row for each parameter shows ‘‘r (correlation coefficient)’’ value that indicates the strength of the association between the 2 variables. Positive r values show positive correlations; negative r values show negative correlations. The second row for each parameter shows P values that indicate the significance of the correlation. *Correlation is significant at the 0.01 level (2-tailed). † Correlation is significant at the 0.05 level (2-tailed). + Margin indicates a histopathologically positive surgical margin. Bold indicates statistically significant values.
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FIGURE 9. There was a significant negative correlation between defect sizes and survival (month) (P = 0.01).
reconstruction with 2 free flaps versus 7 local flap and/or graft in the current study. However, there was no correlation between the flap choice and defect size (Table 2). This may suggest that considerably big defects due to orbital exenteration defects may be closed by local flap options, and free flap options need only bulky 3-dimensional reconstructions. Many local and free flap options for reconstruction of exenteration defects have been described in the literature.9,18Y22 Spontaneous granulation is not recommended because it takes a long period.23 We did not wait for granulation to occur in any of our patients. Free flap reconstruction provides closure of wide and extensive defects requiring bulkiness for volume closure, and it functions as a barrier between the maxillary sinus and optic nerve stump, which have a close connection with the dura mater, thus preventing serious infection.24 In the present study, 2 of the 9 patients underwent free flap reconstruction, and 7 underwent reconstruction with a local flap and graft. The gracilis muscle flap and vastus lateralis musculocutaneous flap were the free flap options used in this study. Compared with the patient who underwent coverage with the gracilis muscle flap, the patient who underwent reconstruction with the vastus lateralis muscle flap required much more tissue to fill the defect. The duration of surgery was significantly longer in patients who underwent reconstruction with free flaps than in patients treated with local flaps in our study, as reported in previous studies.25 However, hospitalization times did not show a significant difference between local and free flap reconstructions. Three of the 7 patients who had grafting had minimal graft necrosis. The prolonged wound care required for graft patients might have caused elongation of hospitalization in patients treated with the local options. The temporalis muscle flap is a well described suitable local option for closure of exenteration defects.5,26,27 Its robust vascular supply from 2 arteries allows it to cross the orbit via a bone window on the lateral wall of the orbit (transorbital) or cross over the lateral rim if necessary, and it can be grafted over without any problem.5,28 The temporalis muscle flap was used in 5 of the patients in this study. All patients with temporalis muscle flaps had visible hollowness of the temporal area, but none had concerns about it. The patients’ ages might have played an important role in the absence of such concerns. In 1 patient with another malignant skin lesion over the temporalis region that had invaded the temporalis muscle, a reverse galeal flap pedicled to the contralateral trochlear artery from the tumor-free margin on the contralateral side was used for reconstruction of the orbital defect, and both areas were grafted with an STSG.
Neglected Periorbital SCC
The temporoparietal flap has been used by some surgeons for reconstruction of exenteration defects.29 Authors have described it as a pliable flap that can be safely used for orbital defects.30 We used the supratrochlear artery pedicled galea frontalis flap in 1 case for reconstruction of exenteration defect since the donor area for temporopariteal flap or temporalis muscle flap has also another tumoral lesion on it. Galea frontalis flap was described with its versatile use around the craniofacial area in the literature.31Y34 The flap may cover not only the ipsilateral upper third of the hemiface, but also the contralateral upper third of the hemiface. This makes the galea frontalis flap useful for our first case, which has a malignant lesion that invaded to the orbital structure and another synchronous malignant lesion that invaded to the frontoparietal area in the current study (Fig. 1). Free flap reconstruction provides closure of wide and extensive defects requiring bulkiness for volume closure, and it functions as a barrier. Two of the patients with free flaps in the current study were followed up in the ICU for 3 and 4 days after surgery, respectively. Although free flaps have been successfully applied in elderly populations,35 there are significantly increased risks of staying in ICU after the surgery associated with the prolonged surgery in these patients because of accompanying comorbidities.36 A definitive conclusion regarding this issue is not possible based on our very small patient population, but surgeons should be aware of potential risks in elderly patients and the high possibility of ICU follow-up after the surgery, thereby incurring extra cost. Hence, all local options as well as free flap options should be on the table in aged patients with extensive periorbital tumors, and local options should be preferred first. Laramore at al14 revealed that RT alone and RT plus CT have significant effects on survival in patients with resectable head and neck SCC. The high risks associated with CT in patients and the common misunderstanding of the carcinogenic effect of RT may affect the treatment decisions of patients. Collaboration with oncology and radiation oncology and proper patient education about the importance of postoperative adjuvant therapies are crucial in this patient group. However, in the present study, survival did not show significant correlation with RT-CT application. Because the mean age of patients in the current study is 77 T 6.7 years, and all of the patients died of unrelated reasons without any relapse of the disease except 2, current study may not reveal any significant correlation. Most of the patients in the current study hesitated to undergo CT and RT because of the potential risks in elderly individuals.
FIGURE 10. Kaplan-Meier survival curve for all patients.
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CONCLUSIONS The longer duration of surgery and hospitalization and requirement of ICU in the free flap group might be withdrawals of aggressive reconstructive surgery techniques. Notifying the fact that periorbital SCC in elderly population that requires exenteration may have very poor prognosis without any relapse, and there was not a survival difference between local and free flap treatment groups, management with a more conservative approach might be a rational solution. Postoperative RT and CT are significant prognostic factors in elderly patients, who have considerably higher risks associated with heavy postoperative adjuvant therapies. But in this study, they could not affect the survival because of the nonrelevant deaths within an average of 15.7 months. Squamous cell carcinoma of the head and neck region requires collaboration with oncologist and radiooncologist that includes aggressive surgical therapy and decision of accompanied postoperative RT and CT. Three-dimensional free flap reconstruction is required for large defects of the face; however, all local and free flap options for periorbital reconstruction should be on the table in patients at high possibility of staying in ICU during prolonged surgery. Because local options work very well in most of the cases, and survival is not so long, free flaps may be necessary in selected cases in which local flaps are not available. Studies with larger series need definitive conclusion of management for periorbital SCC requiring exenteration.
REFERENCES 1. Jemal A, Tiwari RC, Murray T, et al. Cancer statistics, 2004. CA Cancer J Clin 2004;54:8Y29 2. Rapidis AD, Liarikos S. Malignant orbital and orbitomaxillary tumors: surgical considerations. Orbit 1998;17:77Y88 3. Bartley GB, Garrity JA, Waller RR, et al. Orbital Exenteration at the Mayo ClinicV1967Y1986. Ophthalmology 1989;96:468Y474 4. Slutsky JB, Jones EC. Periocular cutaneous malignancies: a review of the literature. Dermatol Surg 2012 5. Menon NG, Girotto JA, Goldberg NH, et al. Orbital reconstruction after exenteration: use of a transorbital temporal muscle flap. Ann Plast Surg 2003;50:38Y42 6. Cook BE Jr, Bartley GB. Treatment options and future prospects for the management of eyelid malignancies: an evidence-based update. Ophthalmology 2001;108:2088Y2098; quiz 2099Y2100, 2121 7. Kennedy RE. Indications and surgical techniques for orbital exenteration. Adv Ophthalmic Plast Reconstr Surg 1992;9:163Y173 8. Behmand RA, Guyuron B. Resection of bilateral orbital and cranial base basal cell carcinoma with preservation of vision. Ann Plast Surg 1996;36:637Y640 9. Weng CJ. Periorbital soft-tissue and socket reconstruction. Ann Plast Surg 1995;34:457Y462; discussion 454Y462 10. Cordeiro PG, Santamaria E. A classification system and algorithm for reconstruction of maxillectomy and midfacial defects. Plast Reconstr Surg 2000;105:2331Y2346; discussion 2338Y2347 11. Swartz WM, Banis JC, Newton ED, et al. The osteocutaneous scapular flap for mandibular and maxillary reconstruction. Plast Reconstr Surg 1986;77:530Y545 12. Chepeha DB, Moyer JS, Bradford CR, et al. Osseocutaneous radial forearm free tissue transfer for repair of complex midfacial defects. Arch Otolaryngol Head Neck Surg 2005;131:513Y517 13. Rodrigues ML, Kohler HF, Faria JC, et al. Reconstruction after extended orbital exenteration using a fronto-lateral flap. Int J Oral Maxillofac Surg 2009;38:850Y854
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14. Laramore GE, Scott CB, al-Sarraf M, et al. Adjuvant chemotherapy for resectable squamous cell carcinomas of the head and neck: report on Intergroup Study 0034. Int J Radiat Oncol Biol Phys 1992;23:705Y713 15. Demirdover C, Sahin B, Vayvada H, et al. The versatile use of temporoparietal fascial flap. Int J Med Sci 2011;8:362Y368 16. Savage RC. Orbital exenteration and reconstruction for massive basal cell and squamous cell carcinoma of cutaneous origin. Ann Plast Surg 1983;10:458Y466 17. Papadopoulos O, Frantzoglou M, Chrisostomidis C, et al. Neglected squamous cell carcinoma of the frontal area: a clinical report. J Craniofac Surg 2006;17:1015Y1020 18. Altindas M, Yucel A, Ozturk G, et al. The prefabricated temporal island flap for eyelid and eye socket reconstruction in total orbital exenteration patients: a new method. Ann Plast Surg 2010;65:177Y182 19. Weichel ED, Eiseman AS, Casler JD, et al. Rectus abdominus free flap in the reconstruction of the orbit following subtotal exenteration. Ophthalmic Surg Lasers Imaging 2011;42:83Y86 20. Menderes A, Yilmaz M, Vayvada H, et al. Reverse temporalis muscle flap for the reconstruction of orbital exenteration defects. Ann Plast Surg 2002;48:521Y526; discussion 526Y527 21. Chang DW, Langstein HN. Use of the free fibula flap for restoration of orbital support and midfacial projection following maxillectomy. J Reconstr Microsurg 2003;19:147Y152 22. Karacal N, Ambarcioglu O, Topal U, et al. Reverse-flow submental artery flap for periorbital soft tissue and socket reconstruction. Head Neck 2006;28:40Y45 23. Nemet AY, Martin P, Benger R, et al. Orbital exenteration: a 15-year study of 38 cases. Ophthal Plast Reconstr Surg 2007;23:468Y472 24. Spiegel JH, Varvares MA. Prevention of postexenteration complications by obliteration of the orbital cavity. Skull Base 2007;17:197Y203 25. Kroll SS, Evans GR, Goldberg D, et al. A comparison of resource costs for head and neck reconstruction with free and pectoralis major flaps. Plast Reconstr Surg 1997;99:1282Y1286 26. Cehajic J, Moody A, James RC, et al. An oculoplastic use for the temporalis muscle flap. Orbit 2009;28:281Y284 27. Yucel A, Yazar S, Aydin Y, et al. Temporalis muscle flap for craniofacial reconstruction after tumor resection. J Craniofac Surg 2000;11:258Y264 28. Shipkov CD, Anastassov YC. Orbital reconstruction after exenteration with the whole transorbital temporalis muscle flap. Ann Plast Surg 2003;51:527 29. Lai AC, Heney ML. Temporoparietal fascial flap in orbital reconstruction. Arch Facial Plast Surg 2000;2:196 30. Raffaini M, Costa P. The temporopariental fascial flap in reconstruction of the cranio-maxillofacial area. J Craniomaxillofac Surg 1994;22:261Y267 31. Cavusoglu T, Yazici I, Vargel I, et al. Reconstruction of coup de sabre deformity (linear localized scleroderma) by using galeal frontalis muscle flap and demineralized bone matrix combination. J Craniofac Surg 2011;22:257Y258 32. Kim YJ, Kim HR, Jun YJ, et al. Usefulness of vascularized galeal frontalis myofascial flap as treatment for postoperative infection in frontal sinus fracture. J Craniofac Surg 2011;22:1968Y1971 33. Duymaz A, Karabekmez FE, Tosun Z, et al. Reconstruction with galeal frontalis flap of depressed forehead region in progressive hemifacial atrophy. J Craniofac Surg 2008;19:1104Y1106 34. Zhang FG, Tang XF, Hua CG, et al. Anterior skull base reconstruction with galeal-frontalis-pericranial flap based on temporalis myofascial flap. J Craniofac Surg 2010;21:1247Y1249 35. Vaz JA, Cote DW, Harris JR, et al. Outcomes of free flap reconstruction in the elderly. Head Neck 2013;35:884Y888 36. Ger RS, Chessel ES. Prevention of major amputations in nonischemic lower limb lesions. J Am Coll Surg 2005;201:898Y905
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Management of Neglected Periorbital Squamous Cell Carcinoma Requiring Orbital Exenteration Furkan Erol Karabekmez, MD, FEBOPRAS, Muhammed Nebil Selimoglu, MD, Ahmet Duymaz, MD, FEBOPRAS, Mehtap Sen Karamese, MD, Mustafa Keskin, MD, FEBOPRAS, and Nedim Savaci, MD
pproximately 500,000 new malignancies of the head and neck are diagnosed worldwide every year.1 Malignant tumors of the orbit and orbitomaxillary area represent 4% to 8% of head and
neck malignancies.2 Periorbital malignancies, including squamous cell carcinoma (SCC), basal cell carcinoma, and mesenchymal tumors, may develop or invade the globe, palpebrae, and orbital bony structures, especially in neglected cases. Basal cell carcinoma is the most common skin cancer of the periorbital region.3 However, orbital exenteration is not common in cases of basal cell carcinoma because of its slow progression. Squamous cell carcinoma is the second most common cancer of the periorbital region.4 It may spread into the periorbital structures, orbit, and nerves such as the branches of the trigeminal nerve, facial nerve, and extraocular nerves in the early stages because of its perineural invasion capacity.5,6 Orbital exenteration is required when the tumor invades the orbital musculature or the orbit itself. This procedure involves removal of the eye together with other orbital contents within the bony socket.5 Bony resection may be required if invasion has occurred.7 The orbital exenteration procedure results in significant morbidity in the face, which negatively affects the patient’s social life. Reconstruction of such defects may be challenging.8 Accurate reconstructive techniques should be chosen to fill the defect, establish contour symmetry with the opposite side of the face, and gain suitable soft tissue for further socket repair for prosthetics.9 Bone grafting with free soft tissue flaps or free osteocutaneous flaps has been used for exenteration cases involving concomitant defects on the orbital rims10Y12 When large amounts of soft tissue are present and bony resection is performed on both the frontal and maxillary sides together with exenteration, a bulky flap that separates the intracranial contents from the sinus cavity may be required.13 Although increased collaboration among different departments, progressive treatment planning, and consideration of reconstructive options that can cover almost all types and sizes of defects have enabled surgeons to perform adequate resection with no hesitation, patients with advanced SCC still have a 5-year survival rate of less than 50%.14Y16 We reviewed patients with SCC in the periorbital area requiring orbital exenteration in our clinic. The aim of this study was to evaluate the indications for exenteration, rate of histopathologically positive surgical margin, size of the defects, reconstruction options, location of the lesions, and survival of these patients.
From the Abant Izzet Baysal Universitesi, Tip Fakultesi, Plastic Cerrahi AD, Bolu, Turkey. Received February 17, 2013. Accepted for publication August 26, 2013. Address correspondence and reprint requests to Furkan Erol Karabekmez, MD, FEBOPRAS, Abant Izzet Baysal Universitesi, Tip Fakultesi, Plastik Cerrahi AD, 14000, Bolu, Turkey; E-mail: [email protected]; [email protected] The study protocol was approved by the local ethics committee. No funding was received for this study. The authors report no conflicts of interest. Copyright * 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000333
This study was retrospective, and ethical committee approval was obtained. A chart review of patients’ records was conducted to identify all patients with periorbital SCC requiring orbital exenteration from 2006 to 2011. A total of 9 patients who met the criteria were included in the study. Patient demographics, surgical technique, hospitalization period, necessity for postoperative intensive care, survival, defect size, surgical margins, radiotherapy and chemotherapy (RT-CT), lymphadenopathy status, distant metastasis, relapses, and operation length were assessed.
Abstract: With its perineural invasion capacity, periorbital squamous cell carcinoma (SCC) may easily invade orbital structures. When SCC invades the orbital musculature or the orbit itself, orbital exenteration, one of the most disfiguring operations on the face, is required. We reviewed elderly patients with periorbitally localized SCC requiring orbital exenteration to evaluate reconstructive options and survival. A chart review of patients’ records was conducted to identify all patients older than 65 years with periorbital malignancy requiring orbital exenteration from 2006 to 2011. A total of 9 patients who met the criteria were included in the study. The mean age at surgery was 77 T 6.7 years, and the mean defect size was 74.2 cm2. All patients had a similar history of late presentation to a doctor because of hesitation to undergo surgery. The temporoparietal fascia flap, galeal flap, free gracilis flap, and free vastus lateralis musculocutaneous flap were the treatment options for reconstruction of the defects. All patients died during follow-up, and the mean survival was 15.7 months (range, 6Y36 months). Only 2 of them had relapse before the death. Our small series suggest that elderly patients with periorbital SCC requiring orbital exenteration may not have enough survival to relapse because of the death from different causes without relapse or any sign of spreading cancer. Also, prolonged surgery with free flap reconstruction may increase the risk of postoperative intensive care unit requirement. Because local flaps may work very well for reconstructing the orbital exenteration defects, free flap option should be kept for selected cases. Key Words: Periorbital tumor, squamous cell carcinoma, orbital exenteration (J Craniofac Surg 2014;25: 729Y734)
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TABLE 1. Demographics, Treatments, and Outcomes of All Cases
Case 1 2 3 4 5 6 7 8 9
Age, y
Sex
Flap
Hospital Stay, d
ICU
Survival
Defect Size, cm2
Surgical Margins
RT, CT
Neck USG
Metastasis
Surgery, h
82 80 69 74 81 83 65 75 84
Female Female Female Female Female Female Male Male Female
Galea frontalis flap, STSG STSG Free gracilis Free vastus lateralis Temporalis muscle flap, STSG Temporalis muscle flap, STSG Temporalis muscle flap, STSG Temporalis muscle flap, STSG Temporalis muscle flap, STSG
15 15 10 19 35 7 7 15 21
0 0 3 4 0 0 0 0 0
7 11 7 14 12 24 36 24 12
156 80 63 64 63 36 20 36 150
Positive Negative Positive Negative Positive Positive Positive Negative Positive
RT, CT RT, CT V V RT, CT RT, CT V RT, CT V
(+) (j) (j) (j) (j) (j) (j) (j) (j)
Lung Lung V V V V V V V
3.5 4.5 7 9 4.5 3.5 3.5 3.5 4.5
Statistical Analysis Correlations among age, flap options (local flap and graft versus free flap), hospitalization period, intensive care unit (ICU) stay, survival, defect size, positive surgical margin, RT-CT status, lymphadenopathy status, lung metastasis, and duration of the surgery were evaluated using Spearman correlation coefficient test. Survival analysis was performed with a Kaplan-Meier survival curve. All statistical analyses were performed using PASW version 18 software. All tests were 2-sided, and P G 0.05 was considered to indicate statistical significance.
RESULTS Of the 9 patients studied, 2 were male, and 7 were female, with a mean age at surgery of 77 T 6.7 years (range, 65Y84 years). Patient characteristics are summarized in Table 1. All patients had biopsyproven SCC before the surgery and had indications for exenteration because of radiologically demonstrated invasion to the orbital musculature or globe. Two of the patients presented with a frontoorbital mass, 2 with a lower lid mass, 2 with a malar mass, and 2 with a medial canthal mass. Eight of the patients had ulceration of their lesions. Six patients had edema, 1 had hyperemia of the medial canthus, and 1 had loss of vision upon presentation. No patients had diplopia. One patient had a positive lymph node on ultrasonography and neck dissection. The others had negative neck ultrasonography results.
Seven patients presented with relapses of previously excised SCC, and the remaining 2 were primary cases in their first examinations. Lung metastasis was detected preoperatively in 3 patients. Six patients underwent bony resection together with orbital exenteration, and 3 underwent only orbital exenteration. The mean defect size was 74.2 cm2 (range, 20Y156 cm2). Defect reconstruction was performed with a temporoparietal fascia flap with split-thickness skin graft (STSG) in 5 patients, a galeal flap with STSG in 1 patient, only STSG in 1 patient, a free gracilis flap in 1 patient, and a free vastus lateralis musculocutaneous flap in 1 patient (Figs. 1Y7). The mean duration of surgery was 5.0 hours for all patients (range, 3.5Y9 hours). In patients treated with free and local flaps, the mean durations of surgery were 8.8 and 3.8 hours, respectively. The average length of hospitalization was 16.6 days (range, 7Y35 days). Two patients who underwent free flap reconstruction stayed 3 and 4 days, respectively, in the ICU. None of the patients who underwent reconstruction with local flaps and graft needed to stay in the ICU. Three patients had minimal graft loss; there were no complications in the remaining 6 patients. Six of the patients had positive margin in the histopathologic examination. Five patients underwent CT and RT during the postoperative period, and the rest of the patients chosen to decline therapy. All patients died during the follow-up; the mean survival was 15.7 months (range, 6Y36 months). Two had relapsed tumors before death, and the others died of unrelated causes.
Statistical Analysis All of the parameters were compared regarding to the Spearman correlation test, and the results were summarized in Table 2. Flap options (free vs local) and number of days patient stayed in ICU showed a significant positive correlation (P G 0.001). Flap options and
FIGURE 1. A, An 82-year-old patient presented with a left fronto-orbital ulcerated mass (patient 1). B, Wide resection applied. C, A galeal flap was raised to close the defect. D, The flap was extended to repair the socket.
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FIGURE 2. Same patient in Figure 1 with 1-week (A) and 1-month (B) postoperative views (patient 1).
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Neglected Periorbital SCC
FIGURE 5. A, Same patient’s intraoperative view with exenteration defect (patient 6). B, Temporalis muscle flap raised. C, Flap advanced over the lateral orbital rim. D, Donor area closed.
mentioned correlations (Table 2). For all patients, the 1-year survival rate was 50.5%, based on the Kaplan-Meier survival curve (Fig. 10).
FIGURE 3. A, A 74-year-old female patient presented with an ulcerated lesion on the left malar region, involving the ipsilateral lower lid, medial canthus, and orbit (patient 4). B, Maxillectomy and orbital exenteration were performed, and a negative surgical margin was verified by frozen section examination. C, A free vastus lateralis musculocutaneous flap was raised for reconstruction of the defect. D, Immediate postoperative view.
duration of the surgery showed a significant positive correlation (P = 0.02) (Fig. 8). Patient duration of stay in ICU and duration of the surgery also showed a significant positive correlation (P = 0.01). However, there was a strong negative correlation between defect size and survival (P = 0.02) (Fig. 9). There were no significant correlations between ages, flap options, duration of hospitalization, ICU requirement, survival, defect size, positive surgical margin, RT-CT, positive neck ultrasonography (USG), lung metastasis, and duration of the surgery except previously
FIGURE 4. A, An 83-year-old patient presented with an ulcerated lesion on her right lower lid (patient 6). B, Postoperative view after reconstruction of the exenteration defect with temporalis muscle flap and STSG repair.
DISCUSSION Squamous cell carcinoma is the second most common cancer of the eyelid, and its perineural invasion capability and relatively rapid progression create a high risk for exenteration. Huge SCC is mostly a problem of elderly patients,17 and invasion to orbital structures is seen mostly in neglected cases. Our literature search yielded no data on the survival of patients specifically with periorbital SCC requiring exenteration. In the present study, patients with advanced SCC had a 1-year survival rate of around 50%. However, it is difficult to conclude that periorbital SCC requiring exenteration always has a grave prognosis because of the small sample size, older population, and different causes of death in the current study. A larger clinical series may provide a definitive conclusion regarding the survival of patients with advanced periorbital SCC.
FIGURE 6. A, A 65-year-old male patient presented with a lesion on his left lower lid (patient 7). B, The exenteration defect. C, A temporalis muscle flap was passed under the lateral orbital rim. D, Four-month postoperative view.
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FIGURE 8. There was a significant difference between local flap and free flap reconstruction applied cases according to duration of surgery as expected (P = 0.04).
FIGURE 7. A, An 84-year-old patient presented with relapse of a previously treated SCC lesion in her left periorbital region. B, After wide resection and exenteration, the defect required free flap reconstruction. C, Development of cardiac dysrhythmia and hemodynamic instability during the operative period pushed the surgeon to finish the operation as quickly as possible. Therefore, a temporalis muscle flap and advancement of residual cheek tissue and STSG were used for reconstruction. D, A 4-week postoperative photograph showing minimal graft loss over the frontal area.
Although tumors close to vital structures such as the orbital globe may limit the decision regarding to the excision margins, the literature suggests that treatment of head and neck area’s SCC that requires orbital exenteration should be as aggressive as needed to obtain negative surgical margins. This type of aggressive excision will result in big 3-dimensional defects to be reconstructed, and both local and free flap options should be on the table. We presented
TABLE 2. Correlations Between All the Parameters Correlations
Age Local-free Hospital stay ICU stay Survival Defect size + Surgical margin RT-CT Neck USG Lung metastasis Surgery (h)
r P r P r P r P r P r P r P r P r P r P r P
Age
Local-Free
Hospital Stay
ICU Stay
Survival
Defect Size
+ Margin
RT-CT
Neck USG
Lung Metastasis
Surgery (h)
1.000 0. j0.518 0.154 0.366 0.333 j0.502 0.168 j0.203 0.601 0.504 0.166 0.274 0.476 0.433 0.244 0.274 0.476 0.207 0.593 j0.213 0.583
j0.518 0.154 1.000 0. 0.000 10.000 0.992* 0.000 j0.262 0.496 0.052 0.894 j0.189 0.626 j0.598 0.089 j0.189 0.626 j0.286 0.456 0.771† 0.015
0.366 0.333 0.000 10.000 1.000 0. 0.047 0.905 j0.297 0.437 0.562 0.115 j0.187 0.631 0.044 0.910 0.000 10.000 0.000 10.000 0.480 0.191
j0.502 0.168 0.992* 0.000 0.047 0.905 1.000 0. j0.208 0.591 0.069 0.860 j0.250 0.516 j0.593 0.092 j0.188 0.629 j0.283 0.460 0.777† 0.014
j0.203 0.601 j0.262 0.496 j0.297 0.437 j0.208 0.591 1.000 0. j0.766† 0.016 j0.139 0.722 j0.088 0.822 j0.485 0.185 j0.577 0.104 j0.418 0.263
0.504 0.166 0.052 0.894 0.562 0.115 0.069 0.860 j0.766† 0.016 1.000 0. j0.046 0.906 0.044 0.911 0.552 0.123 0.626 0.071 0.349 0.358
0.274 0.476 j0.189 0.626 j0.187 0.631 j0.250 0.516 j0.139 0.722 j0.046 0.906 1.000 0. j0.158 0.685 0.250 0.516 j0.189 0.626 j0.243 0.529
0.433 0.244 j0.598 0.089 0.044 0.910 j0.593 0.092 j0.088 0.822 0.044 0.911 j0.158 0.685 1.000 0. 0.316 0.407 0.478 0.193 j0.507 0.164
0.274 0.476 j0.189 0.626 0.000 10.000 j0.188 0.629 j0.485 0.185 0.552 0.123 0.250 0.516 0.316 0.407 1.000 0. 0.661 0.052 j0.364 0.335
0.207 0.593 j0.286 0.456 0.000 10.000 j0.283 0.460 j0.577 0.104 0.626 0.071 j0.189 0.626 0.478 0.193 0.661 0.052 1.000 0. j0.165 0.671
j0.213 0.583 0.771† 0.015 0.480 0.191 0.777† 0.014 j0.418 0.263 0.349 0.358 j0.243 0.529 j0.507 0.164 j0.364 0.335 j0.165 0.671 1.000 0
The first row for each parameter shows ‘‘r (correlation coefficient)’’ value that indicates the strength of the association between the 2 variables. Positive r values show positive correlations; negative r values show negative correlations. The second row for each parameter shows P values that indicate the significance of the correlation. *Correlation is significant at the 0.01 level (2-tailed). † Correlation is significant at the 0.05 level (2-tailed). + Margin indicates a histopathologically positive surgical margin. Bold indicates statistically significant values.
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FIGURE 9. There was a significant negative correlation between defect sizes and survival (month) (P = 0.01).
reconstruction with 2 free flaps versus 7 local flap and/or graft in the current study. However, there was no correlation between the flap choice and defect size (Table 2). This may suggest that considerably big defects due to orbital exenteration defects may be closed by local flap options, and free flap options need only bulky 3-dimensional reconstructions. Many local and free flap options for reconstruction of exenteration defects have been described in the literature.9,18Y22 Spontaneous granulation is not recommended because it takes a long period.23 We did not wait for granulation to occur in any of our patients. Free flap reconstruction provides closure of wide and extensive defects requiring bulkiness for volume closure, and it functions as a barrier between the maxillary sinus and optic nerve stump, which have a close connection with the dura mater, thus preventing serious infection.24 In the present study, 2 of the 9 patients underwent free flap reconstruction, and 7 underwent reconstruction with a local flap and graft. The gracilis muscle flap and vastus lateralis musculocutaneous flap were the free flap options used in this study. Compared with the patient who underwent coverage with the gracilis muscle flap, the patient who underwent reconstruction with the vastus lateralis muscle flap required much more tissue to fill the defect. The duration of surgery was significantly longer in patients who underwent reconstruction with free flaps than in patients treated with local flaps in our study, as reported in previous studies.25 However, hospitalization times did not show a significant difference between local and free flap reconstructions. Three of the 7 patients who had grafting had minimal graft necrosis. The prolonged wound care required for graft patients might have caused elongation of hospitalization in patients treated with the local options. The temporalis muscle flap is a well described suitable local option for closure of exenteration defects.5,26,27 Its robust vascular supply from 2 arteries allows it to cross the orbit via a bone window on the lateral wall of the orbit (transorbital) or cross over the lateral rim if necessary, and it can be grafted over without any problem.5,28 The temporalis muscle flap was used in 5 of the patients in this study. All patients with temporalis muscle flaps had visible hollowness of the temporal area, but none had concerns about it. The patients’ ages might have played an important role in the absence of such concerns. In 1 patient with another malignant skin lesion over the temporalis region that had invaded the temporalis muscle, a reverse galeal flap pedicled to the contralateral trochlear artery from the tumor-free margin on the contralateral side was used for reconstruction of the orbital defect, and both areas were grafted with an STSG.
Neglected Periorbital SCC
The temporoparietal flap has been used by some surgeons for reconstruction of exenteration defects.29 Authors have described it as a pliable flap that can be safely used for orbital defects.30 We used the supratrochlear artery pedicled galea frontalis flap in 1 case for reconstruction of exenteration defect since the donor area for temporopariteal flap or temporalis muscle flap has also another tumoral lesion on it. Galea frontalis flap was described with its versatile use around the craniofacial area in the literature.31Y34 The flap may cover not only the ipsilateral upper third of the hemiface, but also the contralateral upper third of the hemiface. This makes the galea frontalis flap useful for our first case, which has a malignant lesion that invaded to the orbital structure and another synchronous malignant lesion that invaded to the frontoparietal area in the current study (Fig. 1). Free flap reconstruction provides closure of wide and extensive defects requiring bulkiness for volume closure, and it functions as a barrier. Two of the patients with free flaps in the current study were followed up in the ICU for 3 and 4 days after surgery, respectively. Although free flaps have been successfully applied in elderly populations,35 there are significantly increased risks of staying in ICU after the surgery associated with the prolonged surgery in these patients because of accompanying comorbidities.36 A definitive conclusion regarding this issue is not possible based on our very small patient population, but surgeons should be aware of potential risks in elderly patients and the high possibility of ICU follow-up after the surgery, thereby incurring extra cost. Hence, all local options as well as free flap options should be on the table in aged patients with extensive periorbital tumors, and local options should be preferred first. Laramore at al14 revealed that RT alone and RT plus CT have significant effects on survival in patients with resectable head and neck SCC. The high risks associated with CT in patients and the common misunderstanding of the carcinogenic effect of RT may affect the treatment decisions of patients. Collaboration with oncology and radiation oncology and proper patient education about the importance of postoperative adjuvant therapies are crucial in this patient group. However, in the present study, survival did not show significant correlation with RT-CT application. Because the mean age of patients in the current study is 77 T 6.7 years, and all of the patients died of unrelated reasons without any relapse of the disease except 2, current study may not reveal any significant correlation. Most of the patients in the current study hesitated to undergo CT and RT because of the potential risks in elderly individuals.
FIGURE 10. Kaplan-Meier survival curve for all patients.
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CONCLUSIONS The longer duration of surgery and hospitalization and requirement of ICU in the free flap group might be withdrawals of aggressive reconstructive surgery techniques. Notifying the fact that periorbital SCC in elderly population that requires exenteration may have very poor prognosis without any relapse, and there was not a survival difference between local and free flap treatment groups, management with a more conservative approach might be a rational solution. Postoperative RT and CT are significant prognostic factors in elderly patients, who have considerably higher risks associated with heavy postoperative adjuvant therapies. But in this study, they could not affect the survival because of the nonrelevant deaths within an average of 15.7 months. Squamous cell carcinoma of the head and neck region requires collaboration with oncologist and radiooncologist that includes aggressive surgical therapy and decision of accompanied postoperative RT and CT. Three-dimensional free flap reconstruction is required for large defects of the face; however, all local and free flap options for periorbital reconstruction should be on the table in patients at high possibility of staying in ICU during prolonged surgery. Because local options work very well in most of the cases, and survival is not so long, free flaps may be necessary in selected cases in which local flaps are not available. Studies with larger series need definitive conclusion of management for periorbital SCC requiring exenteration.
REFERENCES 1. Jemal A, Tiwari RC, Murray T, et al. Cancer statistics, 2004. CA Cancer J Clin 2004;54:8Y29 2. Rapidis AD, Liarikos S. Malignant orbital and orbitomaxillary tumors: surgical considerations. Orbit 1998;17:77Y88 3. Bartley GB, Garrity JA, Waller RR, et al. Orbital Exenteration at the Mayo ClinicV1967Y1986. Ophthalmology 1989;96:468Y474 4. Slutsky JB, Jones EC. Periocular cutaneous malignancies: a review of the literature. Dermatol Surg 2012 5. Menon NG, Girotto JA, Goldberg NH, et al. Orbital reconstruction after exenteration: use of a transorbital temporal muscle flap. Ann Plast Surg 2003;50:38Y42 6. Cook BE Jr, Bartley GB. Treatment options and future prospects for the management of eyelid malignancies: an evidence-based update. Ophthalmology 2001;108:2088Y2098; quiz 2099Y2100, 2121 7. Kennedy RE. Indications and surgical techniques for orbital exenteration. Adv Ophthalmic Plast Reconstr Surg 1992;9:163Y173 8. Behmand RA, Guyuron B. Resection of bilateral orbital and cranial base basal cell carcinoma with preservation of vision. Ann Plast Surg 1996;36:637Y640 9. Weng CJ. Periorbital soft-tissue and socket reconstruction. Ann Plast Surg 1995;34:457Y462; discussion 454Y462 10. Cordeiro PG, Santamaria E. A classification system and algorithm for reconstruction of maxillectomy and midfacial defects. Plast Reconstr Surg 2000;105:2331Y2346; discussion 2338Y2347 11. Swartz WM, Banis JC, Newton ED, et al. The osteocutaneous scapular flap for mandibular and maxillary reconstruction. Plast Reconstr Surg 1986;77:530Y545 12. Chepeha DB, Moyer JS, Bradford CR, et al. Osseocutaneous radial forearm free tissue transfer for repair of complex midfacial defects. Arch Otolaryngol Head Neck Surg 2005;131:513Y517 13. Rodrigues ML, Kohler HF, Faria JC, et al. Reconstruction after extended orbital exenteration using a fronto-lateral flap. Int J Oral Maxillofac Surg 2009;38:850Y854
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14. Laramore GE, Scott CB, al-Sarraf M, et al. Adjuvant chemotherapy for resectable squamous cell carcinomas of the head and neck: report on Intergroup Study 0034. Int J Radiat Oncol Biol Phys 1992;23:705Y713 15. Demirdover C, Sahin B, Vayvada H, et al. The versatile use of temporoparietal fascial flap. Int J Med Sci 2011;8:362Y368 16. Savage RC. Orbital exenteration and reconstruction for massive basal cell and squamous cell carcinoma of cutaneous origin. Ann Plast Surg 1983;10:458Y466 17. Papadopoulos O, Frantzoglou M, Chrisostomidis C, et al. Neglected squamous cell carcinoma of the frontal area: a clinical report. J Craniofac Surg 2006;17:1015Y1020 18. Altindas M, Yucel A, Ozturk G, et al. The prefabricated temporal island flap for eyelid and eye socket reconstruction in total orbital exenteration patients: a new method. Ann Plast Surg 2010;65:177Y182 19. Weichel ED, Eiseman AS, Casler JD, et al. Rectus abdominus free flap in the reconstruction of the orbit following subtotal exenteration. Ophthalmic Surg Lasers Imaging 2011;42:83Y86 20. Menderes A, Yilmaz M, Vayvada H, et al. Reverse temporalis muscle flap for the reconstruction of orbital exenteration defects. Ann Plast Surg 2002;48:521Y526; discussion 526Y527 21. Chang DW, Langstein HN. Use of the free fibula flap for restoration of orbital support and midfacial projection following maxillectomy. J Reconstr Microsurg 2003;19:147Y152 22. Karacal N, Ambarcioglu O, Topal U, et al. Reverse-flow submental artery flap for periorbital soft tissue and socket reconstruction. Head Neck 2006;28:40Y45 23. Nemet AY, Martin P, Benger R, et al. Orbital exenteration: a 15-year study of 38 cases. Ophthal Plast Reconstr Surg 2007;23:468Y472 24. Spiegel JH, Varvares MA. Prevention of postexenteration complications by obliteration of the orbital cavity. Skull Base 2007;17:197Y203 25. Kroll SS, Evans GR, Goldberg D, et al. A comparison of resource costs for head and neck reconstruction with free and pectoralis major flaps. Plast Reconstr Surg 1997;99:1282Y1286 26. Cehajic J, Moody A, James RC, et al. An oculoplastic use for the temporalis muscle flap. Orbit 2009;28:281Y284 27. Yucel A, Yazar S, Aydin Y, et al. Temporalis muscle flap for craniofacial reconstruction after tumor resection. J Craniofac Surg 2000;11:258Y264 28. Shipkov CD, Anastassov YC. Orbital reconstruction after exenteration with the whole transorbital temporalis muscle flap. Ann Plast Surg 2003;51:527 29. Lai AC, Heney ML. Temporoparietal fascial flap in orbital reconstruction. Arch Facial Plast Surg 2000;2:196 30. Raffaini M, Costa P. The temporopariental fascial flap in reconstruction of the cranio-maxillofacial area. J Craniomaxillofac Surg 1994;22:261Y267 31. Cavusoglu T, Yazici I, Vargel I, et al. Reconstruction of coup de sabre deformity (linear localized scleroderma) by using galeal frontalis muscle flap and demineralized bone matrix combination. J Craniofac Surg 2011;22:257Y258 32. Kim YJ, Kim HR, Jun YJ, et al. Usefulness of vascularized galeal frontalis myofascial flap as treatment for postoperative infection in frontal sinus fracture. J Craniofac Surg 2011;22:1968Y1971 33. Duymaz A, Karabekmez FE, Tosun Z, et al. Reconstruction with galeal frontalis flap of depressed forehead region in progressive hemifacial atrophy. J Craniofac Surg 2008;19:1104Y1106 34. Zhang FG, Tang XF, Hua CG, et al. Anterior skull base reconstruction with galeal-frontalis-pericranial flap based on temporalis myofascial flap. J Craniofac Surg 2010;21:1247Y1249 35. Vaz JA, Cote DW, Harris JR, et al. Outcomes of free flap reconstruction in the elderly. Head Neck 2013;35:884Y888 36. Ger RS, Chessel ES. Prevention of major amputations in nonischemic lower limb lesions. J Am Coll Surg 2005;201:898Y905
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