FUNCTIONAL RECONSTRUCTION OF SOFT TISSUE OROFACIAL DEFECTS WITH MICROVASCULAR GRACILIS MUSCLE FLAP

INTRODUCTION

Free flap reconstructive surgery of middle size orofacial defects enables aesthetic and functional rehabilitation in maxillofacial region. Microvascular flap reconstructive surgery with flap survival success rate more than 90–98% is a gold standard in head and neck reconstructions. The role of the surgeon is not only to close the post-ablative defect, but also to reestablish the lost function. The gracilis muscle free flap (Figure 1) provides adequate volume for middle size oral and facial defects and enables functional rehabilitation.

Reconstructive surgery in general and not only in maxillofacial region has two major rules. The first is to reconstruct the lost tissue with most alike type of tissue. The second is to choose the simplest reconstructive option, which fulfills the criteria of aesthetic and functional rehabilitation. For small and some middle size soft tissue orofacial defects local pedicled flap is the workhorse for adequate reconstruction. Most of the small and part of middle size orofacial defects can be adequately reconstructed with one of the following local pedicled flaps: submental flap, FAMM (facial artery musclemucosal flap), nasolabial perforator flap, buccal fat pad, paramedian forehead flap or supraclavicular flap. Distal pedicled flaps such as pectoralis major flap, deltopectoral flap or latissimus dorsi flap can provide enough tissue to close middle size and large soft tissue maxillofacial defects and usually work very effectively as salvage option in case of complication or loss of the first choice flap.

For large and middle size soft tissue defects in maxillofacial region is usually one of the following microvascular flaps the reconstructive choice: anterolateral thigh (ALT) flap, forearm flap, superficial circumflex iliac artery perforator (SCIP) flap, lateral arm free flap (LAFF) or deep inferior epigastric perforator (DIEP) free flap. In defined middle size or large size soft tissue defects of the tongue, lip or cheek with ambition for functional reconstruction the gracilis free flap is the flap of choice with adequate soft tissue type and volume, but also with simple straightforward harvest and low donor side morbidity. The use of the gracilis muscle (musculus gracilis) in reconstructive surgery was first described by Pickrell in 1952 for rectal sphincter reconstruction.¹ With skin island was the gracilis pedicled myocutaneous flap described in 1972 by Orticochea.² It was one of the first myocutaneous flaps described in humans. In 1976, Harii published a series of patients reconstructed with free gracilis flaps for soft tissue cover³ and a functional free gracilis flap for facial reanimation.⁴ Gracilis flap has become one of the essential tools of the reconstructive surgeon, as a functional flap, for soft tissue coverage and for contour deformities such as in breast reconstruction. For reconstruction of head and neck defects the free gracilis muscle flap is not widely used, but has the potential to provide good results.⁵ Use of the free gracilis muscle flap has gained popularity due to its predictable vascular anatomy and minimal donor-site morbidity.⁶ The aim of this paper is to share our experiences with the gracilis muscle flap in reconstructions of orofacial defects.

Functional reconstruction of soft tissue defects of the tongue or lip with microvascular gracilis muscle flap appears to have advantage of adequate volume, straightforward flap harvest technique, acceptable pedicle length and satisfactory vessel diameter with very low donor site morbidity compared to other microvascular flap reconstructive options such as radial forearm flap, anterolateral thigh (ALT) flap, superficial circumflex iliac artery perforator (SCIP) flap, lateral arm free flap (LAFF) or deep inferior epigastric perforator (DIEP) free flap or vertical rectus musculocutaneous (VRAM) flap.

Gracilis muscle takes origin from the symphysis pubis and inserts distally into the medial surface of the proximal tibia. Gracilis is the most superficial muscle of the adductors group of the lower limb. The muscle belly length is approximately 30 cm.⁷ Distal end of the muscle lies between sartorius anteriorly and semitendinosus muscle posteriorly. The function of the muscle is to adduct, flex and medially rotate the hip and to flex the knee. The muscle is most commonly raised on the dominant vascular pedicle only, and the entire muscle may be harvested this way. Dominant pedicle is a branch of the medial femoral circumflex artery or direct branch from the deep femoral artery, usually with a caliber of 1 to 2.5 mm. In adults, the main vascular supply enters the gracilis approximately 10 cm inferior to the pubic tubercle. The course of the pedicle runs deep between adductor magnus and longus with median length of 6 cm (5–7 cm). Usually two commitant veins are found accompanying the artery. They drain into the deep femoral vein and may converge to form a larger common vein (3–4 mm diameter), a short distance before entering the deep one. There are usually two secondary segmental pedicles to the gracilis muscle that can be found distally to the main one. They are both ligated and divided when the muscle is harvested. Somatomotoric supply is provided by the anterior branch of the obturator nerve. The nerve originates from the lumbar plexus (L2–L4), runs through the obturator foramen and branches into anterior and posterior divisions beneath the pectineus muscle. The anterior division then travels between adductor longus and brevis (supplying it) before entering the gracilis muscle close to the location of the dominant pedicle. The nerve has a more oblique course proximally than the vascular pedicle and runs 2–3 cm cranially to the pedicle.⁸

Gracilis free flap (Figure 1, 2) is a versatile option for tongue reconstruction from middle size defects (hemiglossectomy) to total tongue defect after glossectomy. Advanced tongue cancer normally treated with total glossectomy with laryngeal preservation (TGLP) has a high risk of severe postoperative morbidity due to the loss of swallowing and articulation. Innervated functional gracilis musculocutaneous flap permits an appropriate dynamic reconstruction, and along with an adequate course of rehabilitation, can provide good swallowing and articulation outcomes, which permits a satisfactory long-term quality of life.⁹ Gracilis free flap is the first-line treatment used in facial palsy reanimation, with numerous advantages including low morbidity, a strong motor impulse, high reliability, and fast reinnervation. In this case cross-face facial nerve or ipsilateral masseter nerve are used for neuroanastomosis and reinnervation with excellent results.¹⁰ Proper neuroanastomosis and flap reinnervation are crucial to preserve flap volume and to achieve superior swallowing capacity.¹¹

Reconstruction of the lower and upper lip or both lips should meet both aesthetic and functional requirements, which is a major challenge particularly in extensive lip defects requiring microvascular flap reconstruction. Free fasciocutaneous flaps such as composite radial forearm flap or anterolateral thigh flap in conjunction with static tendon slings provide satisfactory results. However, neurovascular gracilis muscle transfer in recent years has been introduced to overcome noncontractile properties of these flaps and to restore oral competence by muscle contractility.⁵ The use of gracilis muscle to reconstruct lower lip defects has gained popularity since the study conducted by Ninkovic et al. in 2007; the authors used the gracilis flap arranged with the facial artery musculomucosal flap for the mucosa restoration and used a skin graft harvested from the scalp for external skin.¹² Raising the flap with the overlying skin island allows to avoid morbidity in other donor site, to avoid scar retraction of the skin graft on the gracilis that could limit its movement, and to plan aesthetical refinements such as hair transplantation or tattoo of the beard on the skin.¹³ The innervated gracilis muscle transfer became a basic choice for functional lip reconstruction.¹⁴

MATERIAL AND METHODS

We present recent less than one-year experience with functional reconstructions of middle size orofacial defects (tongue or lip) with free gracilis muscle flap in a group of 5 patients. Four patients with squamous cell carcinoma (SCC) of tongue and one with SCC of lip and cheek underwent radical resection with subsequent immediate functional microvascular gracilis muscle flap reconstruction. All five patients were males, with an average age of 59 years. In the subgroup of 4 patients post tongue resection 2 underwent pure gracilis muscle flap reconstruction only, and the other 2 composite free gracilis flap with skin island reconstruction (myocutaneous flap). Gracilis flap with skin island attached was preferred for larger tongue defects glossectomy or extended hemiglossectomy. The skin island attached to the gracilis muscle was also used to cover extraoral defect in the single-stage functional reconstruction of subtotal lower lip and unilateral cheek defect with free myocutaneous gracilis flap.

All 5 patients had confirmed SCC in diagnostic biopsy, followed by standard preoperative studies: computed tomography (CT) or magnetic resonance imaging (MRI) of the head and neck, chest X-ray and abdomen ultrasonography (USG) or CT. Microvascular flap reconstruction was planned for all patients with the aim not only for aesthetic, but also for functional reconstruction, therefore radial forearm flap was not a choice. In all 5 patients were the expected post-ablative orofacial defects of middle size, therefore free gracilis muscle was the flap of choice over ALT flap, which would be the second choice in our department.

No special preoperative studies were obtained considering gracilis free flap reconstruction. The donor site was shaved and Doppler ultrasonography was used to mark the femoral artery, and then the branch of the medial femoral circumflex artery, main gracilis muscle vascular pedicle, which is located approximately 10 cm below the pubic tubercle. The obturator nerve is usually located 2 cm (1,5–3cm) above the vascular pedicle. Position of patient during surgery is supine with flexed leg (sole at the level of contralateral knee) – well known as unilateral frog leg position. Contralateral hip is elevated for better surgical field exposure. The gracilis muscle flap was in 2 cases harvested as a pure muscle flap and in 3 cases as myocutaneous flap with skin island and in all 
5 cases as a functional flap with the anterior branch of obturator nerve. The vascular pedicle was dissected to its origin from the medial circumflex femoral vessels or directly to the deep femoral vessel to gain the maximum length.

CASE REPORT 1

A 51-year-old man referred to our department with 6-week history of complaints with tongue pain, speech impairment and dysphagia. On physical examination a tumor of the right tongue margin was noticed and histologically verified as SCC; standard preoperative examinations were performed and tumor was classified as stage T4aN2cM0. The patient was indicated for primary surgical treatment as follows: tracheostomy and bilateral neck dissection regions I–V on the left side and I–III on the right side, radical tumor resection was performed through temporary mandibular split, total glossectomy was performed with tumor-free margins confirmed intraoperatively. Second team simultaneously harvested the gracilis flap with 15 cm muscle length and skin island sized 10 x 6 cm and the defect was immediately reconstructed. The vascular pedicle was anastomosed end-to-end to the recipient left-sided vessels: lingual artery, facial vein and external jugular vein for second venous anastomosis. The obturator nerve was neuroanastomosed to left hypoglossal nerve. During the reconstruction of the tongue the flap was oriented with long axis transversally and skin island intraorally. Patient was discharged home on postoperative day (POD) 12 and underwent adjuvant postoperative radiochemotherapy, due to bilateral neck nodal involvement. (Figure 3–10.)

CASE REPORT 2

A 64-year-old patient referred with primary advanced SCC of the right tongue, with chief complaints of pain, dysphagia and 15 kg weight loss in 7 weeks. Staging CT of the head and neck showed bilateral tumor of tongue staged T3N2 and following whole body (chest and abdomen) CT confirmed M0. Primary surgical treatment was indicated as follows: tracheotomy, bilateral neck dissection in regions I–V, extended hemiglossectomy 1.5 cm into the contralateral left half of tongue to gain negative resection margins in intraoperative histopathology. The second team simultaneously harvested myocutaneous gracilis flap with skin island sized 13 x 6 cm and muscle length 12 cm. The vascular pedicle was anastomosed end-to-end to recipient right-sided vessels: facial artery, facial vein and superior thyroid vein for second vein anastomosis. The obturator nerve was neuroanastomosed to the right hypoglossal nerve. The gracilis flap was oriented in antero-posterior direction with long axis of muscle during the reconstruction. Partial isles of venous congestion were observed in the skin island of the gracilis flap during first week after surgery without any subsequent wound dehiscence or skin loss. The patient was discharged home POD 11 on oral feeding and despite extensive tumor resection was the patient able to speak and was clearly understood. The patient underwent subsequent adjuvant postoperative radiochemotherapy. (Figure 11–15.)

CASE REPORT 3

54-year-old male referred to our department with second cancer in the head and neck region, currently diagnosed SCC of the left margin of the tongue. The patient was 6 years in remission for oropharyngeal carcinoma (staged T3N2cM0) treated with primary radiochemotherapy, total dose (TD) 70Gy with concomitant cisplatin and fluorouracil (5-FU). Positron emission computed tomography (PET CT) showed a highly FDG-avid left-sided tumor of the tongue, with no local enhancement in oropharynx, neither regional neck nor whole body involvement staged T2N0M0. Salvage surgery was indicated by a tumor board, consisting of tracheostomy, unilateral neck dissection, resection of the left half of tongue (hemiglossectomy) and reconstruction with gracilis flap. The gracilis free muscle flap was harvested simultaneously with the ablative surgery, and the defect was reconstructed with muscle only flap of total length 13cm. The vascular pedicle was anastomosed end-to-end to recipient left-sided vessels: facial artery, facial vein and superior thyroid vein; and the obturator nerve to left hypoglossal nerve. Prolonged neck lymphorrhea was observed during the hospital stay. The patient was discharged POD 10, but came with a dehiscence of the wound after neck dissection two weeks post-op. The wound was revised and re-sutured primarily with successful subsequent healing despite previously irradiated neck. The patient was not indicated for adjuvant oncologic treatment and is under meticulous oncologic follow-up with PET/CT planned 3 months after surgery. (Figure 16–18.)

CASE REPORT 4

65-year-old patient presented to our department with rapid growing tumor of the right margin of the tongue, excessive pain, halitosis and impaired swallowing lasting for more than 4 weeks. Histopathology confirmed SCC, the patient subsequently underwent CT of the head and neck and standard preoperative examination and was staged T3N2M0. Primary surgical treatment was indicated by tumor board as follows: tracheotomy, unilateral right sided extended cervical dissection regions I–V, tumor resection (extended hemiglossectomy) and immediate reconstruction with microvascular gracilis flap without skin island. The vascular pedicle was anastomosed end-to-end to recipient ipsilateral vessels: lingual artery, facial vein and superior thyroid vein. The anterior branch of obturator nerve was neuroanastomosed to the right hypoglossal nerve. Even though the flap showed good vascular perfusion immediately after completing microvascular anastomoses and release of the pedicle, unfortunately soon afterwards the arterial flow decreased and during 20 minutes total arterial occlusion was noticed. The arterial anastomosis was revised with no flow in pedicle artery or in recipient lingual artery. Afterwards the flap artery was reanastomosed successfully to the facial artery with normal perfusion to the flap. After less than 24 hours was the patient transferred from intensive care unit to our ward and subsequent hospital stay was without any other complications. The patient was discharged POD 9 without nasogastric tube, with acceptable speech articulation. The patient was scheduled for adjuvant radiochemotherapy. (Figure 19–21.)

CASE REPORT 5

The last case report concerns a 63-year-old patient with newly diagnosed invasive SCC of the lower lip and left cheek, with clinical staging T4N2 and M0, confirmed by whole body CT staging scan. Standard preoperative exams were performed and primary surgical treatment was indicated. Surgical treatment consisted of tracheostomy, bilateral neck dissection region I-V, subtotal resection of lower lip with partial left cheek resection. All intraoperative frozen sections’ resection margins were clear and the reconstruction with simultaneously harvested myocutaneous gracilis flap followed. The gracilis free flap was harvested with 18 cm muscle length and skin island size of 15 x 8 cm. The whole skin island was used for extraoral defect coverage and intraorally was left uncovered gracilis muscle for secondary epithelization. No partial split thickness skin graft was used. The anterior branch of obturator nerve was anastomosed to marginal branch of left facial nerve. The vascular pedicle was anastomosed end-to-end to left sided recipient vessels: facial artery, facial vein and submental vein for second vein anastomosis. During second postoperative day a partial venostasis in skin island was observed and hirudotherapy was indicated with a temporary effect. Marginal right sided skin 
island necrosis was treated with debridement and primary resuture under local anesthesia. The patient was discharged on POD 15 and scheduled for adjuvant radiochemotherapy due to advanced cancer stage pT4N2cM0. (Figure 22–25.)

RESULTS

All five patients with oral or facial defects were successfully reconstructed with functional gracilis muscle flap, with no flap loss. We found free gracilis muscle flap harvest not to be technically demanding, with the possibility for skin island harvest if needed, and simple primary closure of donor site with very low morbidity. Hand held Doppler USG was always used preoperatively to mark the gracilis vascular pedicle position, which corresponded accurately with the real position during the surgery in all five cases. The donor site was always closed primarily with one redon drain and no major donor site morbidity was observed. In two flaps we observed minor partial skin island venous congestion and hirudotherapy was used successfully in one flap. The second skin island needed surgical debridement with primary re-suture. No wound dehiscence nor orofacial fistula was observed.

DISCUSSION

Radical surgery should be the primary treatment modality for most resectable oral cavity cancers and for T4a laryngeal/hypopharyngeal cancers and preferred modality of treatment for most early (T1–T2, N0) laryngeal and hypo/oropharyngeal carcinomas, because this strategy offers an opportunity to reserve radiotherapy for a potential recurrence or second primary tumor.¹⁵ Primary surgical treatment consists of radical resection and adequate reconstruction, both equally important. With locally advanced cancer (T3, T4) reconstruction is the prerequisite for successful radical resection. Flaps in general, both pedicled and microvascular, are the gold standard for middle size and large maxillofacial defects reconstruction, which allows to treat radically even locally advanced cancer stages considered in the past as inoperable. In general, successful radical primary surgery for head and neck cancer provides the patients with higher 5-year survival rates and better quality of life.

The potential complications of microvascular flap reconstruction in general are free flap loss, scar formation in donor or recipient site, donor site morbidity, sensorial loss. Special consideration for lip reconstruction include microstomia, loss of oral competence and loss of gingivobuccal sulcus and oral mucosa.¹⁵

According to literature, overall complication rate for free gracilis flap may be underreported and be even 9.6% with the two most commonly occurring complications: postoperative hematoma (3.6%) and infection (3.5%).¹⁶

Ablative orofacial defects incorporating mimic facial musculature/nerve cause expressive dysfunction and considerable morbidity. The disrupted branches of facial nerve provided a source for functional free muscle flap reinnervation. Reconstruction of oncologic defects including expressive facial musculature/nerve with gracilis free functioning muscle transfer can restore oral continence and facial expression primarily.¹⁷

Objective assessment of smile outcome after microvascular free gracilis transfer is challenging, and quantification of smile outcomes in the literature is inconsistent; however oral commissure excursion and facial symmetry both at rest and when smiling are evaluated.¹⁸ Terzis score for facial mimic movements´ assessment can be used. Standardizing follow-up schedule, assessing spontaneity in an objective and reproducible fashion, and use of consistent outcome measures would allow for future meta-analyses and better understanding of the options for functional reconstruction.¹⁹ Extensive defects of both lower and upper lip and commissure may require reconstruction with a free gracilis muscle combined with a forearm flap transfer for better functional result and good oral sphincter function for eating, speaking and air inspiration.²⁰ Prefabricated gracilis flap can be used for extensive lip and commissure defects. Ueda et al. reported total lower lip reconstruction in an 18-month-old boy following a dog bite. In order to obtain an optimal functional result and to avoid any additional facial scarring, a prefabricated gracilis muscle free flap was used in a two-stage procedure. This allowed both lip occlusion and normal speech development to be restored without any impairment of mandibular growth during a 4-year follow-up.²¹

Functional reconstruction of soft tissue defects of tongue or lip with microvascular gracilis muscle flap appears to have advantage of adequate volume and very low donor site morbidity compared to other microvascular flap reconstructive options, such as anterolateral thigh (ALT) flap, superficial circumflex iliac artery perforator (SCIP) flap, lateral arm free flap (LAFF) or deep inferior epigastric perforator (DIEP) free flap. Reinervation of microvascular gracilis flap should restore the movement also in the reconstructed part of the tongue or lip. In contrast, if the tongue or lip defect is reconstructed without innervated soft tissue flap with muscle component (either pedicled or microvacular), the function will be carried only by surrounding innervated healthy tissue.

CONCLUSION

Currently, head and neck reconstructive surgery is focused not only on defect occlusion and adequate aesthetic result, but the same emphasize is aimed at functional result. Functional result post tongue and lip resection means defect occlusion with the possibility of movement restoration. Microvascular gracilis muscle flap reconstruction compared to radial forearm flap reconstruction enables functional reconstruction of orofacial soft tissue defect. In all 5 patients the free gracilis flap healed primarily with adequate volume of tissue for the defect occlusion. Patients after tongue reconstruction were swallowing spoon food and oral competence was present in the patient after total lip resection before the discharge. Free gracilis muscle flap appears to be a choice for functional tongue and lip reconstruction. The functional result for the group of our patients will be evaluated each 6 months after surgery and finally evaluated after 2 years post operation considering the ability to swallow and articulate during the speech for the tongue reconstruction and the oral competence and facial mimic movements´ assessment (Terzis score) for the lip reconstruction. Post-operative rating of the gracilis flap function and the range and rate of atrophy will be the subject of further scientific evaluation.

Role of authors: Adam Stebel – lead author, conception and design of the paper, major writing. Barbora Hocková – Case report 1, 2, 3. Juraj Abelovský – Case report 4. Dorota Štorcelová – Case report 5. Dušan Poruban – draft and critical revision of the article. Rastislav Slávik – contributed to the conception and design of the article

Disclosure: The authors declare that there is no conflict of interest.

This statement is to certify that all Authors have seen and approved the manuscript being submitted. We warrant that the article is the Authors´ original work. We warrant that the article has not received prior publication and is not under consideration for publication elsewhere. On behalf of all Co-Authors, the corresponding Author shall bear full responsibility for the submission.

We declare that this study has received no financial support. All procedures performed in this study involving human participants were in accordance with ethical standards of the institutional and/or national research committee and with the Helsinki declaration and its later amendments or comparable ethical standards

Corresponding author:

Adam Stebel, MD, Dr. med. dent., MHA

Department of Maxillofacial Surgery

University Hospital with Polyclinic of F. D. Roosevelt

Nám. L. Svobodu 1, 975 17 Banská Bystrica, Slovakia

E-mail: stebel.adam@gmail.com