MICROSURGERY
True Functional Reconstruction of Total or Subtotal Glossectomy Defects Using a Chimeric Anterolateral Thigh Flap With Both Sensorial and Motor Innervation Ozlenen Ozkan,* Omer Ozkan,* Alper Tunga Derin,Þ Gamze Bektas, MD,þ Anı Cinpolat,* Ahmet Duymaz,* Samir Mardini,* Emanuele Cigna,* and Hung-Chi Chen*
he tongue is the most common site of primary cancer of the oral cavity, and glossectomy is effective in achieving local control of tongue malignancy.1 Reconstructive procedures and functional
restorations after tongue cancer resection are crucial for rehabilitation of speech, deglutition, and swallowing, and remain one of the greatest challenges for the plastic surgeon. The main principles of tongue reconstruction include preservation of the native tongue bulk, mobility, shape, and sensitivity.2,3 Sensing food in the oral cavity permits the individual to move it around during mastication and then to swallow it.3 Numerous techniques have been used for reconstruction in large defects of the tongue, including split-thickness skin grafts and locoregional, or free f laps. However, most did not achieve satisfactory results and had poor functional outcomes; swallowing problems, difficulties in eating in public, restriction of mouth opening, dental problems, and salivary dysfunction are the main complains of patients.4 Recently, functional muscle transfers have been popularized. However, these f laps involve either motor reinnervation, such as rectus abdominis myocutaneous f laps,5 gracilis f laps,6 and vastus lateralis muscle (VLM) f laps,7 or sensory reinnervation involving the radial forearm f lap (RFF), anterolateral thigh (ALT) f lap,8,9 or lateral arm f lap.10 The RFF and ALT f lap still continue to enjoy worldwide acceptance, widespread application, and popularity for the restoration of glossectomy defects.11Y14 However, there has been a greater tendency to use the ALT f lap in this field. This is because the thin RFF is insufficient to provide bulk for total or subtotal glossectomy defect, and harvesting the RFF necessitates the sacrifice of a major artery in the upper extremity. It also has high donor-site morbidity, such as delayed healing, the need for a skin graft, edema of the hand, and unsightly scars.14Y16 In contrast to the RFF, using the ALT f lap does not cause noticeable donor-site deformity or loss of a major artery, but provides more bulky tissue. Additionally, the ALT f lap can be raised in combination with the VLM as a composite musculocutaneous f lap. To improve functional outcomes and achieve better results in tongue reconstruction, both motor and sensory innervations need to be provided, because the organs are highly specialized and have complex motor and sensory properties. In the light of such considerations, the purpose of the current study was to assess the effectiveness of chimeric ALT in the reconstruction of the total or subtotal glossectomy defect f laps. Our clinical study of 6 patients with chimeric ALT/VLM innervated f laps was performed to assess speech and swallowing outcomes in the hopes of identifying good functional results.
Received March 26, 2013, and accepted for publication, after revision, July 24, 2013. From the Departments of *Plastic, Reconstructive and Aesthetic Surgery, †Otorhinolaryngology, Akdeniz University School of Medicine, Antalya; and ‡Department of Plastic, Reconstructive and Aesthetic Surgery, Tatvan State Hospital, Bitlis, Turkey. Conflicts of interest and sources of funding: none declared. Reprints: Gamze Bektas, MD, Plastik Rekonstruktif ve Estetik Cerrahi Klinigi, Tatvan Devlet Hastanesi, Bitlis, Turkey. E-mail: [email protected]. Copyright * 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0148-7043/15/7405-0557 DOI: 10.1097/SAP.0b013e3182a6add7
Between October 2002 and May 2012, 6 patients with advanced squamous cell carcinomas underwent total or subtotal glossectomy, neck dissection, and immediate reconstruction of the tongue and oral f loor defects with the chimeric ALT f lap. The subjects consisted of 4 men and 2 women, with a mean age of 49.5 years (range, 36Y73 years). The mean follow-up period was 36 months (range, 6 months-7 years). Five patients underwent total glossectomy, the other being subtotal. In terms of operative procedure, subtotal glossectomy was defined as resection of at least 70% to 75% of the
Background: The purpose of this study was to report the motor functional outcomes and sensory recovery of patients who had undergone total or subtotal glossectomy for oral squamous cell carcinomas reconstructed with chimeric anterolateral thigh (ALT) f laps. Methods: Six patients, 4 men and 2 women, with a mean age of 49.5 years (range, 36Y73 years) were included in the study. All patients were treated with chimeric ALT, including the vastus lateralis muscle with its motor nerve and skin paddle with its innervating nerve. All patients were administered functional tests involving sensory recovery, intelligibility, and swallowing. Flap sensibility was evaluated using light touch sensation with the SemmesWeinstein monofilament test, 2-point discrimination according to the Weber sensitive test, warm and cold temperature sensations, and pain sensation. Intelligibility was scored by a speech therapist on a scale from 1 to 5. Swallowing was assessed by electromyography, deglutition scores (on a scale of 1 to 8), and modified barium swallow. Donor-site morbidities were recorded. Results: Mean follow-up was 26.6 months (6 months-5 years). The f laps were successful in all 6 patients. The donor site was closed primarily and no complications were seen in the follow-up period. Normal extension of the knee joint and no evidence of lateral patella instability occurred. Speech intelligibility was good (4) in 3 patients and acceptable (3) in 3. Deglutition scores were 6 in 2 patients, 5 in 2, and 4 in 2. Modified barium swallow revealed that 4 patients experienced bolus transit, but 2 required a liquid swallow to promote bolus transit. Electromyographic recordings showed innervations of the vastus lateralis muscle with active generation of motor unit potentials in 4 patients when trying to elevate the tongue. This was not performed in 1 patient, and 1 other had macroscopic muscle contractions. All sensory tests were satisfactory in all parameters. Conclusions: The results of this reconstructive option were satisfactory in terms of motor function and sensitive assessment of the neotongue. This technique is strongly recommended for patients with total or subtotal glossectomy. Key Words: glossectomy, functional tongue reconstruction, chimeric anterolateral thigh flap (Ann Plast Surg 2015;74: 557Y564)
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tongue, and total glossectomy as complete removal of both the oral and pharyngeal tongue. All patients underwent adjuvant radiotherapy after 1 month postoperatively.
Surgical Technique All patients underwent total or subtotal glossectomy, neck dissection, and immediate reconstruction is performed by the senior author (Dr Omer Ozkan). Preventive tracheostomy is first carried out by the ear, nose, and throat surgeon. Neck dissection takes the form of modified bilateral radical neck dissection in each patient. In all patients, 1 hypoglossal nerve is preserved at the level of the digastric muscle, and the lingual nerve is harvested for motor and sensory repair, respectively; both are tagged with 7/0 prolene suture (Fig. 1). A line is drawn from the anterior superior iliac spine to the lateral border of the patella. The descending branch of the lateral circumf lex femoral pedicle is identified through an incision of the central third of the line. The skin paddle of the f lap is centered over the best perforator, and is designed according to the size of the mucosal defect of the tongue and the f loor of the oral cavity (Fig. 2). A sensory branch from the lateral femoral cutaneous nerve is identified below the anterior superior iliac spine through an incision performed superior to the f lap. The nerve is located deep in the subcutaneous tissue immediately above the fascia. The nerve was 1.5 to 2 mm in diameter in each case. Proximal subcutaneous dissection is performed to harvest a longer nerve length. The VLM and its motor nerve are then exposed to obtain a chimeric ALT f lap. The motor nerve to the muscle is located lateral to the descending branch of the lateral femoral circumf lex vessels in all cases. The nerve is then stimulated by electrodes, and contraction of the muscle portion to be used is identified. A portion of VLM together with its motor nerve branch is raised based on 3-dimensional measurements of oral f loor defects after tagging the VLM with sutures at a distance of 4 cm to estimate the correct tension at the time of muscle fixation. The muscular portion of the f lap is 10 to 14 cm in length, depending on
FIGURE 1. After total glossectomy and neck dissection; hypoglossal nerve, the lingual nerve, and superior thyroidal artery. 558
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FIGURE 2. Flap design.
defect size, including the motor nerve. The chimeric f lap is harvested (Fig. 3) and transferred to the oral cavity defect and sutured into place before microvascular anastomosis is performed (Figs. 4 and 5). The lateral femoral cutaneous sensory nerve of the ALT f lap and motor nerve of the VLM are sutured to the proximal stump of the lingual nerve and hypoglossal nerve in each case, with 10-0 nylon epineurial stitches in a 180-degree position circumferentially, respectively. The nerve repair should be performed before final f lap positioning. This is because this will cover the proximal stump of the lingual and hypoglossal nerves, making it impossible to carry out the repair. The VLM is tightly sutured to the posterior aspect of the mandible through drill holes and attached anteromedially to the hyoid bone with sutures placed circumferentially around the hyoid body with 2/0 polypropylene. The deglutition muscles involving the geniohyoid and the anterior belly of the digastric, mylohyoid, and genioglossus muscles are thus replaced by the transferred VLM. In case of the partially remaining deglutition muscles, these are then directly sutured to the muscular portion of the f lap. The fasciocutaneous parts of the flap
FIGURE 3. Chimeric ALT f lap. * 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Functional Reconstruction of Glossectomy Defects
FIGURE 4. A, The fasciocutaneous parts of the f lap are folded on themselves to achieve a tongue shape. B, Transfer to the oral cavity defect.
are then sutured to one other (or folded on themselves) to achieve a tongue shape with a narrow waist. The tip of the neotongue is left as free and mobile as possible. The rest of the fasciocutaneous part of the chimeric flap is anchored (with watertight closure) to the gingival mucosa anteriorly and the pharyngeal mucosa posteriorly (inferiorly). Finally, microvascular arterial anastomoses are performed in an end-toend manner between the vascular pedicle and superior thyroid artery. Venous anastomoses are again performed in an end-to-end manner between the venous pedicle and external jugular vein. The cervical flaps are closed and the suction drains installed (Fig. 6).
Functional Assessment Functional assessments were carried out 6 to 12 months after surgery.
Sensory Evaluation At the time of the sensory tests, the patients were requested to keep their eyes closed in order not to affect the reliability of the tests. All tests were carried out on the neotongue surface. The sensory tests were as follows3,13,18: 1. Light touch sensation with the Semmes-Weinstein monofilament test. 2. Two-point discrimination (TPD) according to the Weber sensitive test using a neurological graduated compass. Outcomes were reported using 3 levels as follows: 5 mm or less, 5 to 10 mm, and greater than 10 mm. 3. Pain perception by sharp versus blunt discrimination by applying the stimulus with a needle and blunt instrument. 4. Warm (45-CY50-C) and cold (4-C) sensations using a tube containing water at appropriate temperatures.
Speech Evaluation Speech was evaluated postoperatively by a speech therapist after the method described by Lyos et al,17 in which the patient’s speech is rated on a scale of 1 to 5 by a speech therapist according to its comprehensibility in conversation. The scores are defined as follows: 1. Gross errors, unintelligible speech, or speech that cannot be understood at all. 2. Multiple errors, intelligible speech if the subject is known to the therapist. 3. Multiple errors, intelligible speech if the subject is unknown to the therapist. 4. Minor errors, acceptable intelligible speech, speech is occasionally misunderstood. 5. No errors, normal intelligible speech, speech can be clearly understood.
To analyze the final outcome in relation to other clinical factors, speech intelligibility was classified more simply as good (scores, 4Y5), acceptable (score, 3), or poor (scores, 1Y2). * 2015 Wolters Kluwer Health, Inc. All rights reserved.
FIGURE 5. After microvascular anastomosis. www.annalsplasticsurgery.com
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FIGURE 6. l˙mmediate postoperative view.
Swallowing Evaluation Swallowing was assessed by modified barium swallow (MBS),11 electromyography (EMG), and a deglutition scale as follows19: 1. 2. 3. 4. 5. 6. 7. 8.
severe dysphagia, nonYoral feeding only; partial oral, partial nonYoral feeding; liquid diet only; liquid and soft food only, must wash soft food back with liquid; liquid and soft food only, does not need to wash food back; liquid, soft food and mechanical soft foodVbeginning mastication; all food types except tough, fibrous meats; and normal deglutition, normal mastication, regular diet.
RESULTS Decannulations were achieved within 2 weeks after surgery except for 1 case that underwent total laryngectomy at the time of glossectomy. All f laps survived and tolerated the radiotherapy well. No complications were seen in the donor sites, which were closed primarily in each case. Wound healing occurred in 12 to 14 days without
dehiscence. Venous compromise occurred in 1 case, and the f lap was salvaged using a vein graft. No postoperative f lap failures occurred. No patient required gastrostomy. Two cases died due to distant organ metastasis 7 and 11 months postoperatively. We were not able to have satisfactory functional outcome assessment in these patients. All other patients are still alive (Figs. 7Y10).
Speech Intelligibility All 6 patients received postoperative speech therapy. The last speech evaluations were carried out after 6 to 73 months in the postoperative period. The assessment evaluated speech intelligibility as a 4 (good) in 3 cases, and 3 (acceptable) in the other 3.
Swallowing Evaluation Swallowing therapy started with liquid diets 7 to 8 days postoperatively, and continued with soft foods and then regular diets. Feeding was initially supplemented by nasogastric intubation in all patients and by intermittent oroesophageal tube feeding.
Swallowing Scale Deglutition scores were 6 in 2 patients, 5 in 2 patients, and 4 in 2.
FIGURE 7. Five years after the total glossectomy and reconstruction with the chimeric ALT f lap. 560
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FIGURE 8. Five years after the total glossectomy and reconstruction with the chimeric ALT f lap. * 2015 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 9. Appearance 6 months after surgery due to advanced SCC. Total glossectomy, neck dissection, and reconstruction with the chimeric ALT f lap.
MBS Evaluation The MBS assessment revealed that 4 patients experienced bolus transit, but 2 required a liquid swallow to promote bolus transit (Figs. 11 and 12).
EMG Analyses Electromyographic recordings of patients showed innervations of the VLM with active generation of motor unit potentials in 4 patients when patients tried to elevate the tongue. This was not performed in 1 patient, and 1 patient had macroscopic muscle contractions.
Sensory Testing All sensory testing was performed in 4 patients with follow-up of 12 months or longer.
Functional Reconstruction of Glossectomy Defects
Although many techniques have been described for reconstruction of the glossectomy, the RFF and ALT f lap are widely preferred.8,9,14,15 The ALT f lap based on septocutaneous branches of the descending branch of the lateral circumf lex femoral artery was first described by Song et al.20 Since 1984, the f lap has gained popularity for reconstruction of regional as well as distant defects. It can be used as a chimeric f lap for restoration of large defects and complex soft tissue loss. A chimeric f lap with the skin paddle and muscle component (vastus lateralis, rectus femoris, and tensor fascia lata) raised on a separate perforator permits independent insetting of the f lap and gives a better reconstructive outcome in cases with extensive composite defects, requiring soft tissue bulk for filling very large defects. Additionally, an innervated ALT f lap can also be provided by inclusion of the lateral femoral cutaneous nerve to the f lap. Moreover, addition of the motor nerve to the VLM to achieve motor function can be used for reconstruction of the soft tissue defect requiring dynamic function, as in our clinical study.21,22 No statistically significant differences between speech intelligibility and tongue mobility in patients with hemiglossectomy defects reconstructed with the RFF or ALT f lap were noted by de Vicente et al14 or Farace et al15 in their clinical reports. However, the RFF has many disadvantages related to donor-site morbidity. Although these complications do not occur frequently; delayed wound healing, hypo/hyperpigmentation in the skin graft donor site, unacceptable scarring, loss of soft tissue, sensory changes, edema of the hand, limited wrist motion, and the necessary disruption of the major artery of the forearm can be seen.9,14Y16 Although alternative techniques have been described to manage some of these disadvantages, such as tissue expansion, they have not been overcome satisfactorily. In addition, the RFF does not provide enough bulk for dead space obliteration and cannot be harvested as a chimeric flap with a muscle and its motor nerve. Methods of tongue reconstruction in the literature focus on the following 3 main areas: 1. The appearance of reconstructed tongue and filling of defects. 2. The sensorial innervated neotongue together with the appearance of the reconstructed tongue and filling of defects.3
TPD Test The 4 patients could feel the discriminator; 1 patient had a TPD of less than 5 mm and 3 patients of 5 to 10 mm.
Semmes-Weinstein Monofilament Testing Although 2 patients had 3.61 mg in anterior tongue (the tip of the tongue), and 4.31 mg in posterior tongue (dorsum of the tongue), 2 patients had 4.56 mg in anterior and 6.65 mg in posterior of the tongue.
Pain and Temperature Assessments Of all patients tested, pain and temperature sensations were perceived (both hot and cold) in the anterior and posterior of the neotongue.
DISCUSSION Excision of the tongue may cause serious functional problems in swallowing, mastication, deglutition, and impaired communication, and result in a worsened quality of life.3 In terms of swallowing and speech, total or near-total glossectomy is associated with insufficient outcomes and poorer results compared to patients with partial resection of the tongue.11 The priorities in tongue reconstructions are preservation of native tongue bulk, mobility, length, and shape. * 2015 Wolters Kluwer Health, Inc. All rights reserved.
FIGURE 10. Appearance 6 months after surgery due to advanced SCC. Total glossectomy, neck dissection, and reconstruction with the chimeric ALT f lap. www.annalsplasticsurgery.com
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FIGURE 11. MBS results after reconstruction. 3. Dynamic or functional reconstruction of the glossectomy defects together with the appearance of the reconstructed tongue and filling of defects.6
However, no technique involving these 3 areas has previously been reported in the literature. As mentioned in the introduction, sensing the food in the oral cavity allows patients to move the tongue around during mastication. Although sensory tests could not be 562
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performed in 2 cases, the results of the sensory tests in the other 4 were satisfactory in all parameters. A sensate neotongue may also protect against burn injuries secondary to hot food. Complex mobility of the tongue in all directions cannot be obtained completely. Yet some degrees of movement may be gained to restore swallowing capacity by adding the VLM with its motor nerve to the ALT f lap, as in our cases. The swallowing functions begin with the elevation of the tongue, narrowing the oropharyngeal * 2015 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 12. MBS results after reconstruction.
space, followed by elevation of the hyoid bone by suprahyoid muscle contractions. Securing the VLM between the posterior border of the mandible and the hyoid bone, as in the detailed description of the surgical technique, made these acts of deglutition possible because the genioglossus and other suprahyoid muscles functioned. Speech intelligibility and swallowing capacity were satisfactory in our patients. Oral feeding was achieved with liquid and soft food in all patients, although 2 patients needed to wash food back. Although * 2015 Wolters Kluwer Health, Inc. All rights reserved.
a potential weakness of our study may be an absence of validated quality of life or functional status questionnaires, no patients were dependent on tube feeding and no aspiration episodes were observed in any patient in the follow-up period. However, replacement of the intrinsic tongue muscles was not possible with our technique. This meant that the speech intelligibility evaluations in 3 cases resulted in scores of 3, meaning ‘‘multiple errors, intelligible speech if subject is unknown to the therapist.’’ www.annalsplasticsurgery.com
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No statistical relationship was determined between sensory recovery and motor-functional outcomes, or also flap sizes and planning, due to the small size of our patient group. The disadvantages of the chimeric ALT f lap are that it requires tedious dissection of musculocutaneous perforators, may be hairy in some patients, which is unacceptable in the oral cavity, and the presence of thick subcutaneous adipose tissue in obese patients. These can be resolved by deepithelization of the f lap after a few weeks postoperatively for hairy cases, and with the harvesting of an ultrathin f lap for obese patients. These difficulties were not seen in our patients. In conclusion, this report evaluates the sensation, speech, and swallowing abilities during a period of 35 months in patients with tongue cancer requiring total or near-total glossectomy. The results of the study strongly suggest that reconstruction of total/near-total tongue defects using the chimeric ALT f lap with both sensory and motor innervations can result in good swallowing outcomes and aesthetic appearance, better functional speech, than techniques previously described for patients with advanced tongue cancer.
8. Huang CH, Chen HC, Huang YL, et al. Comparison of the radial forearm flap and the thinned anterolateral thigh cutaneous flap for reconstruction of tongue defects: an evaluation of donor-site morbidity. Plast Reconstr Surg. 2004; 114:1704Y1710.
ACKNOWLEDGMENTS The authors thank the Akdeniz University Faculty of Medicine for its support for this project. REFERENCES 1. Gourin CG, Johnson JT. Surgical treatment of squamous cell carcinoma of the base of tongue. Head Neck. 2001;23:653Y660. 2. Davison SP, Grant NN, Schwarz KA, et al. Maximizing flap inset for tongue reconstruction. Plast Reconstr Surg. 2008;121:1982Y1985. 3. Biglioli F, Liviero F, Frigerio A, et al. Function of the sensate free forearm flap after partial glossectomy. J Craniomaxillofac Surg. 2006;34:332Y339. 4. Pierre CS, Dassonville O, Chamorey E, et al. Long-term quality of life and its predictive factors after oncologic surgery and microvascular reconstruction in patients with oral or oropharyngeal cancer. Eur Arch Otorhinolaryngol. 2013. 5. Yamamoto Y, Sugihara T, Furuta Y, et al. Functional reconstruction of the tongue and deglutition muscles following extensive resection of tongue cancer. Plast Reconstr Surg. 1998;102:993Y998; discussion 999Y1000. 6. Yoleri L, Mavio?lu H. Total tongue reconstruction with free functional gracilis muscle transplantation: a technical note and review of the literature. Ann Plast Surg. 2000;45:181Y182. 7. Kerawala CJ. Reconstruction of defects after hemiglossectomy using a chimeric vastus lateralis free flap. Br J Oral Maxillofac Surg. 2009;47:126Y128.
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9. Hsiao HT, Leu YS, Liu CJ, et al. Radial forearm versus anterolateral thigh flap reconstruction after hemiglossectomy: functional assessment of swallowing and speech. J Reconstr Microsurg. 2008;24:85Y88. 10. Thankappan K, Kuriakose MA, Chatni SS, et al. Lateral arm free flap for oral tongue reconstruction: an analysis of surgical details, morbidity, and functional and aesthetic outcome. Ann Plast Surg. 2011;66:261Y266. 11. Rieger JM, Zalmanowitz JG, Li SY, et al. Functional outcomes after surgical reconstruction of the base of tongue using the radial forearm free flap in patients with oropharyngeal carcinoma. Head Neck. 2007;29: 1024Y1032. 12. O’Connell DA, Rieger J, Harris JR, et al. Swallowing function in patients with base of tongue cancers treated with primary surgery and reconstructed with a modified radial forearm free flap. Arch Otolaryngol Head Neck Surg. 2008; 134:857Y864. 13. Yu P. Reinnervated anterolateral thigh flap for tongue reconstruction. Head Neck. 2004;26:1038Y1044. 14. de Vicente JC, de Villalaı´n L, Torre A, et al. Microvascular free tissue transfer for tongue reconstruction after hemiglossectomy: a functional assessment of radial forearm versus anterolateral thigh flap. J Oral Maxillofac Surg. 2008; 66:2270Y2275. 15. Farace F, Fois VE, Manconi A, et al. Free anterolateral thigh flap versus free forearm flap: functional results in oral reconstruction. J Plast Reconstr Aesthet Surg. 2007;60:583Y587. 16. Ahn HC, Choi MS, Hwang WJ, et al. The transverse radial artery forearm flap. Plast Reconstr Surg. 2007;119:2153Y2160. 17. Lyos AT, Evans GR, Perez D, et al. Tongue reconstruction: outcomes with the rectus abdominis flap. Plast Reconstr Surg. 1999;103:442Y447; discussion 448-9. 18. Guerin-Lebailly C, Mallet Y, Lambour V, et al. Functional and sensitive outcomes after tongue reconstruction: about a series of 30 patients. Oral Oncol. 2012;48:272Y277. 19. Archontaki M, Athanasiou A, Stavrianos SD, et al. Functional results of speech and swallowing after oral microvascular free flap reconstruction. Eur Arch Otorhinolaryngol. 2010;267:1771Y1777. 20. Song YG, Chen GZ, Song YL. The free thigh flap: a new free flap concept based on the septocutaneous artery. Br J Plast Surg. 1984;37:149. 21. Haughey BH, Taylor SM, Fuller D. Fasciocutaneous flap reconstruction of the tongue and floor of mouth: outcomes and techniques. Arch Otolaryngol Head Neck Surg. 2002;128:1388Y1395. 22. Mardini S, Lin LC, Moran SL, et al. Tensor Fascia Lata Flap. In: Wei FC, Mardini S, eds. Flaps and Reconstructive Surgery. China: Elsevier Inc; 2009:545Y560.
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True Functional Reconstruction of Total or Subtotal Glossectomy Defects Using a Chimeric Anterolateral Thigh Flap With Both Sensorial and Motor Innervation Ozlenen Ozkan,* Omer Ozkan,* Alper Tunga Derin,Þ Gamze Bektas, MD,þ Anı Cinpolat,* Ahmet Duymaz,* Samir Mardini,* Emanuele Cigna,* and Hung-Chi Chen*
he tongue is the most common site of primary cancer of the oral cavity, and glossectomy is effective in achieving local control of tongue malignancy.1 Reconstructive procedures and functional
restorations after tongue cancer resection are crucial for rehabilitation of speech, deglutition, and swallowing, and remain one of the greatest challenges for the plastic surgeon. The main principles of tongue reconstruction include preservation of the native tongue bulk, mobility, shape, and sensitivity.2,3 Sensing food in the oral cavity permits the individual to move it around during mastication and then to swallow it.3 Numerous techniques have been used for reconstruction in large defects of the tongue, including split-thickness skin grafts and locoregional, or free f laps. However, most did not achieve satisfactory results and had poor functional outcomes; swallowing problems, difficulties in eating in public, restriction of mouth opening, dental problems, and salivary dysfunction are the main complains of patients.4 Recently, functional muscle transfers have been popularized. However, these f laps involve either motor reinnervation, such as rectus abdominis myocutaneous f laps,5 gracilis f laps,6 and vastus lateralis muscle (VLM) f laps,7 or sensory reinnervation involving the radial forearm f lap (RFF), anterolateral thigh (ALT) f lap,8,9 or lateral arm f lap.10 The RFF and ALT f lap still continue to enjoy worldwide acceptance, widespread application, and popularity for the restoration of glossectomy defects.11Y14 However, there has been a greater tendency to use the ALT f lap in this field. This is because the thin RFF is insufficient to provide bulk for total or subtotal glossectomy defect, and harvesting the RFF necessitates the sacrifice of a major artery in the upper extremity. It also has high donor-site morbidity, such as delayed healing, the need for a skin graft, edema of the hand, and unsightly scars.14Y16 In contrast to the RFF, using the ALT f lap does not cause noticeable donor-site deformity or loss of a major artery, but provides more bulky tissue. Additionally, the ALT f lap can be raised in combination with the VLM as a composite musculocutaneous f lap. To improve functional outcomes and achieve better results in tongue reconstruction, both motor and sensory innervations need to be provided, because the organs are highly specialized and have complex motor and sensory properties. In the light of such considerations, the purpose of the current study was to assess the effectiveness of chimeric ALT in the reconstruction of the total or subtotal glossectomy defect f laps. Our clinical study of 6 patients with chimeric ALT/VLM innervated f laps was performed to assess speech and swallowing outcomes in the hopes of identifying good functional results.
Received March 26, 2013, and accepted for publication, after revision, July 24, 2013. From the Departments of *Plastic, Reconstructive and Aesthetic Surgery, †Otorhinolaryngology, Akdeniz University School of Medicine, Antalya; and ‡Department of Plastic, Reconstructive and Aesthetic Surgery, Tatvan State Hospital, Bitlis, Turkey. Conflicts of interest and sources of funding: none declared. Reprints: Gamze Bektas, MD, Plastik Rekonstruktif ve Estetik Cerrahi Klinigi, Tatvan Devlet Hastanesi, Bitlis, Turkey. E-mail: [email protected]. Copyright * 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0148-7043/15/7405-0557 DOI: 10.1097/SAP.0b013e3182a6add7
Between October 2002 and May 2012, 6 patients with advanced squamous cell carcinomas underwent total or subtotal glossectomy, neck dissection, and immediate reconstruction of the tongue and oral f loor defects with the chimeric ALT f lap. The subjects consisted of 4 men and 2 women, with a mean age of 49.5 years (range, 36Y73 years). The mean follow-up period was 36 months (range, 6 months-7 years). Five patients underwent total glossectomy, the other being subtotal. In terms of operative procedure, subtotal glossectomy was defined as resection of at least 70% to 75% of the
Background: The purpose of this study was to report the motor functional outcomes and sensory recovery of patients who had undergone total or subtotal glossectomy for oral squamous cell carcinomas reconstructed with chimeric anterolateral thigh (ALT) f laps. Methods: Six patients, 4 men and 2 women, with a mean age of 49.5 years (range, 36Y73 years) were included in the study. All patients were treated with chimeric ALT, including the vastus lateralis muscle with its motor nerve and skin paddle with its innervating nerve. All patients were administered functional tests involving sensory recovery, intelligibility, and swallowing. Flap sensibility was evaluated using light touch sensation with the SemmesWeinstein monofilament test, 2-point discrimination according to the Weber sensitive test, warm and cold temperature sensations, and pain sensation. Intelligibility was scored by a speech therapist on a scale from 1 to 5. Swallowing was assessed by electromyography, deglutition scores (on a scale of 1 to 8), and modified barium swallow. Donor-site morbidities were recorded. Results: Mean follow-up was 26.6 months (6 months-5 years). The f laps were successful in all 6 patients. The donor site was closed primarily and no complications were seen in the follow-up period. Normal extension of the knee joint and no evidence of lateral patella instability occurred. Speech intelligibility was good (4) in 3 patients and acceptable (3) in 3. Deglutition scores were 6 in 2 patients, 5 in 2, and 4 in 2. Modified barium swallow revealed that 4 patients experienced bolus transit, but 2 required a liquid swallow to promote bolus transit. Electromyographic recordings showed innervations of the vastus lateralis muscle with active generation of motor unit potentials in 4 patients when trying to elevate the tongue. This was not performed in 1 patient, and 1 other had macroscopic muscle contractions. All sensory tests were satisfactory in all parameters. Conclusions: The results of this reconstructive option were satisfactory in terms of motor function and sensitive assessment of the neotongue. This technique is strongly recommended for patients with total or subtotal glossectomy. Key Words: glossectomy, functional tongue reconstruction, chimeric anterolateral thigh flap (Ann Plast Surg 2015;74: 557Y564)
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tongue, and total glossectomy as complete removal of both the oral and pharyngeal tongue. All patients underwent adjuvant radiotherapy after 1 month postoperatively.
Surgical Technique All patients underwent total or subtotal glossectomy, neck dissection, and immediate reconstruction is performed by the senior author (Dr Omer Ozkan). Preventive tracheostomy is first carried out by the ear, nose, and throat surgeon. Neck dissection takes the form of modified bilateral radical neck dissection in each patient. In all patients, 1 hypoglossal nerve is preserved at the level of the digastric muscle, and the lingual nerve is harvested for motor and sensory repair, respectively; both are tagged with 7/0 prolene suture (Fig. 1). A line is drawn from the anterior superior iliac spine to the lateral border of the patella. The descending branch of the lateral circumf lex femoral pedicle is identified through an incision of the central third of the line. The skin paddle of the f lap is centered over the best perforator, and is designed according to the size of the mucosal defect of the tongue and the f loor of the oral cavity (Fig. 2). A sensory branch from the lateral femoral cutaneous nerve is identified below the anterior superior iliac spine through an incision performed superior to the f lap. The nerve is located deep in the subcutaneous tissue immediately above the fascia. The nerve was 1.5 to 2 mm in diameter in each case. Proximal subcutaneous dissection is performed to harvest a longer nerve length. The VLM and its motor nerve are then exposed to obtain a chimeric ALT f lap. The motor nerve to the muscle is located lateral to the descending branch of the lateral femoral circumf lex vessels in all cases. The nerve is then stimulated by electrodes, and contraction of the muscle portion to be used is identified. A portion of VLM together with its motor nerve branch is raised based on 3-dimensional measurements of oral f loor defects after tagging the VLM with sutures at a distance of 4 cm to estimate the correct tension at the time of muscle fixation. The muscular portion of the f lap is 10 to 14 cm in length, depending on
FIGURE 1. After total glossectomy and neck dissection; hypoglossal nerve, the lingual nerve, and superior thyroidal artery. 558
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FIGURE 2. Flap design.
defect size, including the motor nerve. The chimeric f lap is harvested (Fig. 3) and transferred to the oral cavity defect and sutured into place before microvascular anastomosis is performed (Figs. 4 and 5). The lateral femoral cutaneous sensory nerve of the ALT f lap and motor nerve of the VLM are sutured to the proximal stump of the lingual nerve and hypoglossal nerve in each case, with 10-0 nylon epineurial stitches in a 180-degree position circumferentially, respectively. The nerve repair should be performed before final f lap positioning. This is because this will cover the proximal stump of the lingual and hypoglossal nerves, making it impossible to carry out the repair. The VLM is tightly sutured to the posterior aspect of the mandible through drill holes and attached anteromedially to the hyoid bone with sutures placed circumferentially around the hyoid body with 2/0 polypropylene. The deglutition muscles involving the geniohyoid and the anterior belly of the digastric, mylohyoid, and genioglossus muscles are thus replaced by the transferred VLM. In case of the partially remaining deglutition muscles, these are then directly sutured to the muscular portion of the f lap. The fasciocutaneous parts of the flap
FIGURE 3. Chimeric ALT f lap. * 2015 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 4. A, The fasciocutaneous parts of the f lap are folded on themselves to achieve a tongue shape. B, Transfer to the oral cavity defect.
are then sutured to one other (or folded on themselves) to achieve a tongue shape with a narrow waist. The tip of the neotongue is left as free and mobile as possible. The rest of the fasciocutaneous part of the chimeric flap is anchored (with watertight closure) to the gingival mucosa anteriorly and the pharyngeal mucosa posteriorly (inferiorly). Finally, microvascular arterial anastomoses are performed in an end-toend manner between the vascular pedicle and superior thyroid artery. Venous anastomoses are again performed in an end-to-end manner between the venous pedicle and external jugular vein. The cervical flaps are closed and the suction drains installed (Fig. 6).
Functional Assessment Functional assessments were carried out 6 to 12 months after surgery.
Sensory Evaluation At the time of the sensory tests, the patients were requested to keep their eyes closed in order not to affect the reliability of the tests. All tests were carried out on the neotongue surface. The sensory tests were as follows3,13,18: 1. Light touch sensation with the Semmes-Weinstein monofilament test. 2. Two-point discrimination (TPD) according to the Weber sensitive test using a neurological graduated compass. Outcomes were reported using 3 levels as follows: 5 mm or less, 5 to 10 mm, and greater than 10 mm. 3. Pain perception by sharp versus blunt discrimination by applying the stimulus with a needle and blunt instrument. 4. Warm (45-CY50-C) and cold (4-C) sensations using a tube containing water at appropriate temperatures.
Speech Evaluation Speech was evaluated postoperatively by a speech therapist after the method described by Lyos et al,17 in which the patient’s speech is rated on a scale of 1 to 5 by a speech therapist according to its comprehensibility in conversation. The scores are defined as follows: 1. Gross errors, unintelligible speech, or speech that cannot be understood at all. 2. Multiple errors, intelligible speech if the subject is known to the therapist. 3. Multiple errors, intelligible speech if the subject is unknown to the therapist. 4. Minor errors, acceptable intelligible speech, speech is occasionally misunderstood. 5. No errors, normal intelligible speech, speech can be clearly understood.
To analyze the final outcome in relation to other clinical factors, speech intelligibility was classified more simply as good (scores, 4Y5), acceptable (score, 3), or poor (scores, 1Y2). * 2015 Wolters Kluwer Health, Inc. All rights reserved.
FIGURE 5. After microvascular anastomosis. www.annalsplasticsurgery.com
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FIGURE 6. l˙mmediate postoperative view.
Swallowing Evaluation Swallowing was assessed by modified barium swallow (MBS),11 electromyography (EMG), and a deglutition scale as follows19: 1. 2. 3. 4. 5. 6. 7. 8.
severe dysphagia, nonYoral feeding only; partial oral, partial nonYoral feeding; liquid diet only; liquid and soft food only, must wash soft food back with liquid; liquid and soft food only, does not need to wash food back; liquid, soft food and mechanical soft foodVbeginning mastication; all food types except tough, fibrous meats; and normal deglutition, normal mastication, regular diet.
RESULTS Decannulations were achieved within 2 weeks after surgery except for 1 case that underwent total laryngectomy at the time of glossectomy. All f laps survived and tolerated the radiotherapy well. No complications were seen in the donor sites, which were closed primarily in each case. Wound healing occurred in 12 to 14 days without
dehiscence. Venous compromise occurred in 1 case, and the f lap was salvaged using a vein graft. No postoperative f lap failures occurred. No patient required gastrostomy. Two cases died due to distant organ metastasis 7 and 11 months postoperatively. We were not able to have satisfactory functional outcome assessment in these patients. All other patients are still alive (Figs. 7Y10).
Speech Intelligibility All 6 patients received postoperative speech therapy. The last speech evaluations were carried out after 6 to 73 months in the postoperative period. The assessment evaluated speech intelligibility as a 4 (good) in 3 cases, and 3 (acceptable) in the other 3.
Swallowing Evaluation Swallowing therapy started with liquid diets 7 to 8 days postoperatively, and continued with soft foods and then regular diets. Feeding was initially supplemented by nasogastric intubation in all patients and by intermittent oroesophageal tube feeding.
Swallowing Scale Deglutition scores were 6 in 2 patients, 5 in 2 patients, and 4 in 2.
FIGURE 7. Five years after the total glossectomy and reconstruction with the chimeric ALT f lap. 560
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FIGURE 8. Five years after the total glossectomy and reconstruction with the chimeric ALT f lap. * 2015 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 9. Appearance 6 months after surgery due to advanced SCC. Total glossectomy, neck dissection, and reconstruction with the chimeric ALT f lap.
MBS Evaluation The MBS assessment revealed that 4 patients experienced bolus transit, but 2 required a liquid swallow to promote bolus transit (Figs. 11 and 12).
EMG Analyses Electromyographic recordings of patients showed innervations of the VLM with active generation of motor unit potentials in 4 patients when patients tried to elevate the tongue. This was not performed in 1 patient, and 1 patient had macroscopic muscle contractions.
Sensory Testing All sensory testing was performed in 4 patients with follow-up of 12 months or longer.
Functional Reconstruction of Glossectomy Defects
Although many techniques have been described for reconstruction of the glossectomy, the RFF and ALT f lap are widely preferred.8,9,14,15 The ALT f lap based on septocutaneous branches of the descending branch of the lateral circumf lex femoral artery was first described by Song et al.20 Since 1984, the f lap has gained popularity for reconstruction of regional as well as distant defects. It can be used as a chimeric f lap for restoration of large defects and complex soft tissue loss. A chimeric f lap with the skin paddle and muscle component (vastus lateralis, rectus femoris, and tensor fascia lata) raised on a separate perforator permits independent insetting of the f lap and gives a better reconstructive outcome in cases with extensive composite defects, requiring soft tissue bulk for filling very large defects. Additionally, an innervated ALT f lap can also be provided by inclusion of the lateral femoral cutaneous nerve to the f lap. Moreover, addition of the motor nerve to the VLM to achieve motor function can be used for reconstruction of the soft tissue defect requiring dynamic function, as in our clinical study.21,22 No statistically significant differences between speech intelligibility and tongue mobility in patients with hemiglossectomy defects reconstructed with the RFF or ALT f lap were noted by de Vicente et al14 or Farace et al15 in their clinical reports. However, the RFF has many disadvantages related to donor-site morbidity. Although these complications do not occur frequently; delayed wound healing, hypo/hyperpigmentation in the skin graft donor site, unacceptable scarring, loss of soft tissue, sensory changes, edema of the hand, limited wrist motion, and the necessary disruption of the major artery of the forearm can be seen.9,14Y16 Although alternative techniques have been described to manage some of these disadvantages, such as tissue expansion, they have not been overcome satisfactorily. In addition, the RFF does not provide enough bulk for dead space obliteration and cannot be harvested as a chimeric flap with a muscle and its motor nerve. Methods of tongue reconstruction in the literature focus on the following 3 main areas: 1. The appearance of reconstructed tongue and filling of defects. 2. The sensorial innervated neotongue together with the appearance of the reconstructed tongue and filling of defects.3
TPD Test The 4 patients could feel the discriminator; 1 patient had a TPD of less than 5 mm and 3 patients of 5 to 10 mm.
Semmes-Weinstein Monofilament Testing Although 2 patients had 3.61 mg in anterior tongue (the tip of the tongue), and 4.31 mg in posterior tongue (dorsum of the tongue), 2 patients had 4.56 mg in anterior and 6.65 mg in posterior of the tongue.
Pain and Temperature Assessments Of all patients tested, pain and temperature sensations were perceived (both hot and cold) in the anterior and posterior of the neotongue.
DISCUSSION Excision of the tongue may cause serious functional problems in swallowing, mastication, deglutition, and impaired communication, and result in a worsened quality of life.3 In terms of swallowing and speech, total or near-total glossectomy is associated with insufficient outcomes and poorer results compared to patients with partial resection of the tongue.11 The priorities in tongue reconstructions are preservation of native tongue bulk, mobility, length, and shape. * 2015 Wolters Kluwer Health, Inc. All rights reserved.
FIGURE 10. Appearance 6 months after surgery due to advanced SCC. Total glossectomy, neck dissection, and reconstruction with the chimeric ALT f lap. www.annalsplasticsurgery.com
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FIGURE 11. MBS results after reconstruction. 3. Dynamic or functional reconstruction of the glossectomy defects together with the appearance of the reconstructed tongue and filling of defects.6
However, no technique involving these 3 areas has previously been reported in the literature. As mentioned in the introduction, sensing the food in the oral cavity allows patients to move the tongue around during mastication. Although sensory tests could not be 562
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performed in 2 cases, the results of the sensory tests in the other 4 were satisfactory in all parameters. A sensate neotongue may also protect against burn injuries secondary to hot food. Complex mobility of the tongue in all directions cannot be obtained completely. Yet some degrees of movement may be gained to restore swallowing capacity by adding the VLM with its motor nerve to the ALT f lap, as in our cases. The swallowing functions begin with the elevation of the tongue, narrowing the oropharyngeal * 2015 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 12. MBS results after reconstruction.
space, followed by elevation of the hyoid bone by suprahyoid muscle contractions. Securing the VLM between the posterior border of the mandible and the hyoid bone, as in the detailed description of the surgical technique, made these acts of deglutition possible because the genioglossus and other suprahyoid muscles functioned. Speech intelligibility and swallowing capacity were satisfactory in our patients. Oral feeding was achieved with liquid and soft food in all patients, although 2 patients needed to wash food back. Although * 2015 Wolters Kluwer Health, Inc. All rights reserved.
a potential weakness of our study may be an absence of validated quality of life or functional status questionnaires, no patients were dependent on tube feeding and no aspiration episodes were observed in any patient in the follow-up period. However, replacement of the intrinsic tongue muscles was not possible with our technique. This meant that the speech intelligibility evaluations in 3 cases resulted in scores of 3, meaning ‘‘multiple errors, intelligible speech if subject is unknown to the therapist.’’ www.annalsplasticsurgery.com
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No statistical relationship was determined between sensory recovery and motor-functional outcomes, or also flap sizes and planning, due to the small size of our patient group. The disadvantages of the chimeric ALT f lap are that it requires tedious dissection of musculocutaneous perforators, may be hairy in some patients, which is unacceptable in the oral cavity, and the presence of thick subcutaneous adipose tissue in obese patients. These can be resolved by deepithelization of the f lap after a few weeks postoperatively for hairy cases, and with the harvesting of an ultrathin f lap for obese patients. These difficulties were not seen in our patients. In conclusion, this report evaluates the sensation, speech, and swallowing abilities during a period of 35 months in patients with tongue cancer requiring total or near-total glossectomy. The results of the study strongly suggest that reconstruction of total/near-total tongue defects using the chimeric ALT f lap with both sensory and motor innervations can result in good swallowing outcomes and aesthetic appearance, better functional speech, than techniques previously described for patients with advanced tongue cancer.
8. Huang CH, Chen HC, Huang YL, et al. Comparison of the radial forearm flap and the thinned anterolateral thigh cutaneous flap for reconstruction of tongue defects: an evaluation of donor-site morbidity. Plast Reconstr Surg. 2004; 114:1704Y1710.
ACKNOWLEDGMENTS The authors thank the Akdeniz University Faculty of Medicine for its support for this project. REFERENCES 1. Gourin CG, Johnson JT. Surgical treatment of squamous cell carcinoma of the base of tongue. Head Neck. 2001;23:653Y660. 2. Davison SP, Grant NN, Schwarz KA, et al. Maximizing flap inset for tongue reconstruction. Plast Reconstr Surg. 2008;121:1982Y1985. 3. Biglioli F, Liviero F, Frigerio A, et al. Function of the sensate free forearm flap after partial glossectomy. J Craniomaxillofac Surg. 2006;34:332Y339. 4. Pierre CS, Dassonville O, Chamorey E, et al. Long-term quality of life and its predictive factors after oncologic surgery and microvascular reconstruction in patients with oral or oropharyngeal cancer. Eur Arch Otorhinolaryngol. 2013. 5. Yamamoto Y, Sugihara T, Furuta Y, et al. Functional reconstruction of the tongue and deglutition muscles following extensive resection of tongue cancer. Plast Reconstr Surg. 1998;102:993Y998; discussion 999Y1000. 6. Yoleri L, Mavio?lu H. Total tongue reconstruction with free functional gracilis muscle transplantation: a technical note and review of the literature. Ann Plast Surg. 2000;45:181Y182. 7. Kerawala CJ. Reconstruction of defects after hemiglossectomy using a chimeric vastus lateralis free flap. Br J Oral Maxillofac Surg. 2009;47:126Y128.
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9. Hsiao HT, Leu YS, Liu CJ, et al. Radial forearm versus anterolateral thigh flap reconstruction after hemiglossectomy: functional assessment of swallowing and speech. J Reconstr Microsurg. 2008;24:85Y88. 10. Thankappan K, Kuriakose MA, Chatni SS, et al. Lateral arm free flap for oral tongue reconstruction: an analysis of surgical details, morbidity, and functional and aesthetic outcome. Ann Plast Surg. 2011;66:261Y266. 11. Rieger JM, Zalmanowitz JG, Li SY, et al. Functional outcomes after surgical reconstruction of the base of tongue using the radial forearm free flap in patients with oropharyngeal carcinoma. Head Neck. 2007;29: 1024Y1032. 12. O’Connell DA, Rieger J, Harris JR, et al. Swallowing function in patients with base of tongue cancers treated with primary surgery and reconstructed with a modified radial forearm free flap. Arch Otolaryngol Head Neck Surg. 2008; 134:857Y864. 13. Yu P. Reinnervated anterolateral thigh flap for tongue reconstruction. Head Neck. 2004;26:1038Y1044. 14. de Vicente JC, de Villalaı´n L, Torre A, et al. Microvascular free tissue transfer for tongue reconstruction after hemiglossectomy: a functional assessment of radial forearm versus anterolateral thigh flap. J Oral Maxillofac Surg. 2008; 66:2270Y2275. 15. Farace F, Fois VE, Manconi A, et al. Free anterolateral thigh flap versus free forearm flap: functional results in oral reconstruction. J Plast Reconstr Aesthet Surg. 2007;60:583Y587. 16. Ahn HC, Choi MS, Hwang WJ, et al. The transverse radial artery forearm flap. Plast Reconstr Surg. 2007;119:2153Y2160. 17. Lyos AT, Evans GR, Perez D, et al. Tongue reconstruction: outcomes with the rectus abdominis flap. Plast Reconstr Surg. 1999;103:442Y447; discussion 448-9. 18. Guerin-Lebailly C, Mallet Y, Lambour V, et al. Functional and sensitive outcomes after tongue reconstruction: about a series of 30 patients. Oral Oncol. 2012;48:272Y277. 19. Archontaki M, Athanasiou A, Stavrianos SD, et al. Functional results of speech and swallowing after oral microvascular free flap reconstruction. Eur Arch Otorhinolaryngol. 2010;267:1771Y1777. 20. Song YG, Chen GZ, Song YL. The free thigh flap: a new free flap concept based on the septocutaneous artery. Br J Plast Surg. 1984;37:149. 21. Haughey BH, Taylor SM, Fuller D. Fasciocutaneous flap reconstruction of the tongue and floor of mouth: outcomes and techniques. Arch Otolaryngol Head Neck Surg. 2002;128:1388Y1395. 22. Mardini S, Lin LC, Moran SL, et al. Tensor Fascia Lata Flap. In: Wei FC, Mardini S, eds. Flaps and Reconstructive Surgery. China: Elsevier Inc; 2009:545Y560.
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