Introduction
Oral tongue is the most common site of intraoral carcinoma.Reference Kerawala, Roques, Jeannon and Bisase1,Reference de Vicente, de Villalaín, Torre and Peña2 The mainstay of treatment for oral tongue cancer is surgery in the early stages of the disease, and surgery combined with radiotherapy or chemoradiotherapy in the advanced stage.Reference Kerawala, Roques, Jeannon and Bisase1,Reference Tarsitano, Vietti, Cipriani and Marchetti3 Because the tongue has an essential role in speech and swallowing function, a glossectomy may have a significant impact on quality of life.Reference Lam and Samman4,Reference Bokhari and Wang5 The aims of tongue reconstruction following a glossectomy should include adequate wound healing and successful functional rehabilitation.Reference Lam and Samman4,Reference Bokhari and Wang5 A small defect involving less than a quarter of the tongue can be closed primarily, or left to heal by secondary intention; a more substantial defect requires flap reconstruction, with the options being local, regional or vascularised free flaps.Reference Bokhari and Wang5,Reference Brown, Rogers and Lowe6
The radial forearm free flap has become one of the most common and accepted vascularised flaps used in reconstruction following oral tongue resection.Reference Lam and Samman4 However, not every patient is a suitable candidate for a microvascular procedure; therefore, pedicled flaps may have an important role in older patients or those with co-existing morbidities.Reference Sittitrai, Srivanitchapoom, Reunmakkaew and Yata7 The submental island flap has been recognised as being a useful local flap for oral cavity reconstruction given its reliability, the low donor site morbidity and the short operative time.Reference Sittitrai, Srivanitchapoom, Reunmakkaew and Yata7,Reference Martin, Pascal, Baudet, Mondie, Farhat and Athoum8 This study aimed to compare the complications and functional outcomes in oral tongue cancer patients who underwent surgical resection followed by reconstruction with a submental island flap or a radial forearm free flap.
Materials and methods
We conducted a retrospective study of patients with squamous cell carcinoma of the tongue who were surgically treated between November 2010 and May 2017. All procedures contributing to this work complied with the ethical standards of the relevant national and institutional guidelines on human experimentation, and with the Helsinki Declaration of 1975, as revised in 2008, and have been approved by the Research Ethics Committee of the Faculty of Medicine at Chiang Mai University.
Patients who underwent oral tongue resection and immediate reconstruction with a submental island flap or a radial forearm free flap were included in the study. Patients with recurrent oral cavity cancer, those who required a segmental mandibulectomy, or patients who had undergone previous neck surgery or radiotherapy, or who underwent tongue base resection of more than 1 cm posterior to the circumvallate papillae, were excluded from the study.
All patients underwent comprehensive or selective neck dissection, and either unilateral or bilateral neck dissection, depending on the clinical status of the cervical lymph node. Patients with a primary tumour extending through the mylohyoid muscle, or a level I cervical lymph node larger than 1.5 cm in diameter, were contraindicated for a submental island flap reconstruction but not for a radial forearm free flap reconstruction; otherwise, the method of reconstruction was based on patient preference. Post-operative adjuvant therapies including radiotherapy or chemoradiotherapy were considered if the tumours were of an advanced stage (stages III–IV), had close or invaded surgical margins, or exhibited extracapsular extension of the lymph nodes.
Patients’ speech was evaluated post-operatively and rated on a scale of 1 to 5 according to the understandability during the conversation. The criteria are as follows: 5 = all speech is understood (excellent); 4 = speech is sometimes not understood (good); 3 = speech can be understood when conversational content is already known (fair); 2 = speech can sometimes be understood (poor); and 1 = nothing is understood (bad).Reference Tarsitano, Vietti, Cipriani and Marchetti3,Reference Brown, Rogers and Lowe6,Reference Yanai, Kikutani, Adachi, Thoren, Suzuki and Iizuka9
Swallowing capacity was assessed, and categorised and rated on a scale of 1 to 5 according to the functional eating status. The criteria are as follows: 5 = full diet; 4 = soft diet; 3 = liquid diet; 2 = combined oral and gastric tube required; and 1 = exclusively gastric tube.Reference de Vicente, de Villalaín, Torre and Peña2,Reference Paydarfar and Patel10
Surgical complications and outcomes related to speech and swallowing function were evaluated in every patient at least one year after treatment.
Statistical analysis was performed using SPSS software, version 20.0 for Windows (IBM, Armonk, New York, USA). Clinical demographics and disease variables were analysed using non-parametric qualitative and quantitative tests. Fisher's exact test, independent t-test, chi-square test and odds ratio with 95 per cent confidence intervals were used to compare the data. A p-value of less than 0.05 was considered statistically significant.
Surgical techniques
Submental island flap
The flap is harvested before performing the neck dissection. The skin island is drawn with the point for upper incision lying just below the mandibular margin, and with the lower limit being governed by a pinch test to assess primary closure. The subplatysmal dissection is performed, and the anterior belly of the ipsilateral digastric muscle is included in the flap. The level Ia and bilateral level Ib cervical lymph nodes are identified and carefully dissected from the flap, while the submental vessels, facial vessels and marginal mandibular nerves are preserved (Figures 1–3).Reference Sittitrai, Srivanitchapoom, Reunmakkaew and Yata7,Reference Martin, Pascal, Baudet, Mondie, Farhat and Athoum8
Fig. 1. Submental island flap with vascular pedicle on the right side (white arrow).
Fig. 2. Submental island flap was placed to reconstruct tongue defect on the right side.
Fig. 3. Oral tongue, one month after reconstruction with a submental island flap. (A problem with hair-bearing skin resolved spontaneously after radiotherapy.)
Radial forearm free flap
The flap harvesting is performed in a two-team approach. After outlining the skin paddle, the dissection begins at the distal end to identify, ligate and divide the radial artery and venae comitantes. The antebrachial fascia is elevated and included with the flap. The paratenon is left to cover the flexor carpi radialis tendon and palmaris. The dissection is carried proximally as the vascular pedicle travels under the brachioradialis muscle and tendon. The cephalic vein is taken with the flap. Microvascular anastomosis is performed using the facial artery or the superior thyroid artery, and branches of the internal jugular vein or the external jugular vein. The forearm donor site is repaired with a split-thickness skin graft. The patient's forearm and wrist are immobilised with a volar splint.Reference Yang, Chen, Gao, Liu, Li and Jiang11
Results
A total of 54 patients were enrolled in the study. Twenty-nine patients underwent submental island flap reconstruction and 25 patients underwent radial forearm free flap reconstruction. Patients with stage T1 tumours were not included in the study because the defects were primarily closed, and very advanced neck nodal disease (N3) was not detected in the included patients.
Patients’ demographics and the clinical characteristics of both groups are summarised in Table 1. There were no significant differences in age, sex, T staging, N staging, type of neck dissection or extent of tumour resection (amount of the oral tongue affected, involvement of the anterior floor of the mouth, and whether marginal mandibulectomy was performed). However, the mean operative time was significantly shorter in the submental island flap group compared with the radial forearm free flap group (181 minutes vs 413 minutes, respectively; p < 0.001).
Table 1. Demographics and clinical characteristics of patients*
* Oral tongue cancer patients who underwent reconstruction with a submental island flap or a radial forearm free flap.
† n = 29;
‡ n = 25.
** Indicates significant difference
The surgical complication data are demonstrated in Table 2. Regarding recipient site complications, orocutaneous fistula was recorded in one patient in the radial forearm free flap group; no such complication was recorded in the submental island flap group. This patient had the fistula repaired, which involved necrotic tissue debridement followed by resuturing of the wound. Haematoma was detected in two patients in the radial forearm free flap group and in one patient in the submental island flap group; all of these patients were treated successfully with wound reopening and collection removal. Other complications, including wound dehiscence and minor wound infections, were comparable in both groups, and they responded well to wound resuturing and local wound care.
Table 2. Surgical complications of patients*
* Oral tongue cancer patients who underwent reconstruction with a submental island flap or a radial forearm free flap.
† n = 29;
‡ n = 25.
** Indicates significant difference
There were no records of donor site complications in the submental island flap group, including no marginal mandibular branch paralysis. The donor site defects in all cases were primarily closed, with pleasing cosmesis and without restricted neck extension. However, in the radial forearm free flap group, there was partial loss of the skin graft in 6 patients (24 per cent), and arm function – including grip strength, pinch strength and wrist movements – was restricted in 14 patients (56 per cent).
Regarding flap complications, neither group had total flap loss, but there was partial flap loss (partial epithelial loss) in five patients (17.2 per cent) in the submental island flap group; in all patients, re-epithelialisation was complete within four weeks with conservative management. Two patients in the radial forearm free flap group had less than 10 per cent loss of the flap volume; these patients were treated with tissue debridement and wound resuturing. There was flap congestion in one patient in the radial forearm free flap group, and the venous anastomosis was revised within 6 hours of the first operation.
There were no statistically significant differences in speech and swallowing function between the two groups (Table 3). No patients had poor or bad speech function, and most of the patients in both groups had excellent to good speech results (82.8 per cent in the submental island flap group and 92 per cent in the radial forearm free flap group). Most of the patients in both groups were able to take at least a soft diet (79.3 per cent in the submental island flap group and 88 per cent in the radial forearm free flap group). None of the patients required a feeding tube. Mean duration of hospital stay was significantly shorter in the submental island flap group than in the radial forearm free flap group (15.9 days vs 26.5 days, respectively; p < 0.001).
Table 3. Functional outcomes of patients*
* Oral tongue cancer patients who underwent reconstruction with a submental island flap or a radial forearm free flap.
† n = 29;
‡ n = 25.
** Indicates significant difference
Possible factors predicting dissatisfaction with speech (fair speech) and swallowing (liquid diet) functions, including age, sex, tumour stage, type of neck dissection, amount of oral tongue resection, anterior floor of the mouth resection, marginal mandibulectomy and post-operative therapy, were evaluated. In the univariate analysis, only anterior floor of the mouth resection was significantly associated with an increased risk of poor swallowing function (p = 0.001). Regarding this risk factor, both the submental island flap and radial forearm free flap patient groups were evaluated separately. This revealed that resection of this anatomical area was significantly associated with poor swallowing function in the submental island flap group but not in the radial forearm free flap group (p = 0.003 and p = 0.997, respectively).
There were no significant differences between the groups concerning: mean follow-up time, pathological results of surgical margins and level I cervical lymph nodes, and tumour recurrence both in the primary site and the cervical lymph node (Table 4).
Table 4. Oncological outcomes of patients*
* Oral tongue cancer patients who underwent reconstruction with a submental island flap or a radial forearm free flap.
† n = 29;
‡ n = 25.
** All six patients had multiple cervical lymph node recurrences at levels I and II.
Discussion
Currently, the use of a vascularised free flap has been the preferred method for reconstruction after resection of the oral cavity cancer.Reference Kerawala, Roques, Jeannon and Bisase1–Reference Brown, Rogers and Lowe6 However, the use of a pedicled flap remains a valuable technique in the treatment of older patients, or those at risk of severe co-morbidities such as poor nutrition, aggressive medical conditions or other incurable diseases, as these patients are not suitable surgical candidates for a prolonged microvascular operation.Reference Sittitrai, Srivanitchapoom, Reunmakkaew and Yata7,Reference Chow, Chan, Chow, Fung and Lam12,Reference Karmer, Böhrnsen, Moser and Schliephake13 The submental island flap is reliable, with no difference in flap survival rate compared with traditional flaps.Reference Sittitrai, Srivanitchapoom, Reunmakkaew and Yata7,Reference Yang, Chen, Gao, Liu, Li and Jiang11,Reference Karmer, Böhrnsen, Moser and Schliephake13–Reference Howard, Nagel, Donald, Hinni and Hayden16 The size of the skin paddle harvested in the case of the submental island flap can be as large as 12 × 6 cm, which is sufficient for reconstruction in any T stage of a tumour, and the donor site defect can be primarily closed without a functional or cosmetic deficit.Reference Sittitrai, Srivanitchapoom, Reunmakkaew and Yata7
One of the major advantages of the submental island flap reconstruction is the associated short operative time. In this study, the mean operating time in the submental island flap group was approximately 3 hours, compared with almost 7 hours in the radial forearm free flap group.
In relevant literature, wound dehiscence of the donor site has rarely been reported (7.4 per cent) in the case of the submental island flap,Reference Paydarfar and Patel10 and this complication was not observed in our study. On the contrary, partial loss of the skin graft and restricted arm function were detected in a significant number of patients who underwent reconstruction using a radial forearm free flap (24 per cent and 56 per cent, respectively). These findings are consistent with previous reports (19–53 per cent and 17–100 per cent, respectively).Reference de Vicente, de Villalaín, Torre and Peña2,Reference Lutz, Wei, Chang, Yang and Chen17,Reference Camaioni, Loreti, Damiani, Bellioni, Passali and Viti18 An orocutaneous fistula was detected in one patient in the radial forearm free flap group, but did not occur in the submental island flap group. This complication rarely occurred in oral cavity defects reconstructed with the submental island flap because the musculofascial component of the flap occludes the dead space and ensures watertight closure of the defect.Reference Sittitrai, Srivanitchapoom, Reunmakkaew and Yata7 Total flap loss was not observed in any patients in either group. However, one patient in the radial forearm free flap group required revision of the venous anastomosis.
The functional outcomes of oral tongue reconstruction are determined by the mobility and the volume of the reconstructed tongue.Reference Hsiao, Leu, Liu, Tung and Lin19 Radial forearm free flaps are pliable and thin, while submental island flaps provide an adequate bulkiness. Therefore, speech and swallowing functions in our study were comparable between the two groups. The majority of the patients had excellent to good speech results (82.8 per cent in the submental island flap group and 92 per cent in the radial forearm free flap), and no patients required tube feeding. These results are consistent with a previous report.Reference Paydarfar and Patel10
In order to improve the functional outcomes, possible factors predicting dissatisfaction with speech and swallowing were evaluated. The findings revealed that resection of the anterior floor of the mouth was significantly associated with poor swallowing function in patients who underwent submental island flap reconstruction but not in those who underwent radial forearm free flap reconstruction. Therefore, in oral tongue cancer patients who require resection of the anterior floor of the mouth, the defect should be reconstructed with a more pliable tissue such as a radial forearm free flap. Accordingly, the swallowing function in this particular resection may be ameliorated by the increased mobility of the reconstructed tongue.
As primary lymphatic drainage of oral cavity cancer involves submental and submandibular lymph nodes, the oncological safety of using the submental island flap has been a cause for concern.Reference Chow, Chan, Chow, Fung and Lam12,Reference Parmar and Goldstein15,Reference Howard, Nagel, Donald, Hinni and Hayden16 However, in patients with a level I cervical lymph node smaller than 1.5 cm in diameter, with no clinical signs of extracapsular spread, who have the sentinel lymph nodes carefully dissected during flap harvesting, the submental island flap can be used without compromising locoregional recurrence.Reference Sittitrai, Srivanitchapoom, Reunmakkaew and Yata7 With careful pre-operative evaluation and intra-operative dissection, our results demonstrate no significant differences in primary tumour and cervical lymph node recurrence between the two groups.
• Submental island flap reconstruction was compared to radial forearm free flap reconstruction
• Speech and swallowing function were comparable, with less donor site morbidity with submental island flap reconstruction
• Submental island flap can be used to reconstruct the oral tongue without compromising oncological outcome
• Submental island flap is appropriate when the tumour does not extend through mylohyoid muscle or a level I cervical lymph node is smaller than 1.5 cm
• Submental island flap is reliable and suitable for oral tongue reconstruction, particularly in patients unsuitable for microvascular surgery
Conclusion
Submental island flap reconstruction of the oral tongue has comparable functional outcomes to radial forearm free flap reconstruction, with less donor site morbidity, shorter operative time and shorter duration of hospital stay. Therefore, this flap is suitable for the reconstruction of oral tongue defects following cancer resection, particularly for patients who are poor candidates for microvascular surgery, without compromising the oncological outcomes.
Competing interests
None declared
