Evaluation of Tongue Functions After Free Flap Reconstruction

Abstract

Squamous cell carcinoma of the tongue is the most common malignancy of the oral cavity, the lateral border being the commonest site. The treatment strategies mandate surgery followed by appropriate reconstruction as the first line of management. There are many suitable methods of reconstruction of tongue defects after surgery, but the principle of an ideal reconstruction method should provide not only satisfactory structural cosmesis, but also good restoration of function. We present our experience with the skin lined free flaps reconstruction for defects of the tongue and floor of mouth, and present analyses of the functional outcomes of reconstruction. This prospective longitudinal study included 93 patients and was conducted in a tertiary care center in Punjab. All patients underwent free flap reconstruction after tumor removal. The functional outcome of the tongue following reconstruction was evaluated 9 months after the completion of treatment. Functions were assessed and matched with sexes and age-matched normal individuals. The data obtained were analyzed by the student ‘t’ test and the p values < 0.05 were considered statistically significant. The duration of swallowing in patients with FRF flap and ALT flap when compared to the normative was significant (< 0.05). There were changes in configuration and volume of the oral cavity after surgery which generates resonant and articulatory alterations, thus the intelligibility of the patient’s speech is lowered. There is also a restriction in the tongue movements and reduction in the sensations of the reconstructed part of the tongue. Both the free ALT flap and the FRF flap can provide acceptable functional restoration of the tongue after radical tumor resection.

Introduction

Squamous cell carcinoma (SCC) of the oral tongue is an aggressive disease and constitutes 22%–39% of oral cavity cancers [1]. It is the most common malignancy of the oral cavity. The commonest site involved is the lateral border followed by the tongue, base and, the tip of the tongue. The current treatment strategies mandate surgery with appropriate reconstruction which depends upon the residual tongue tissue left along with adjuvant therapy as indicated. There are many suitable methods of reconstruction of tongue defects after surgery but for the larger defects, the reconstruction is a challenge for the surgeon, because in an ideal reconstructive method a satisfactory structural cosmesis is pertinent along with the possible restoration of function. Contemporary tongue reconstruction has been largely aided by free flaps, due to the ease to tailor the flap precisely to the defect [2]_. Skin lined free flaps, such as FRF and ALT flaps, are commonly used to reconstruct oral cavity and oropharynx following tongue cancer extirpation surgery [3].

However, the data in literature does not accurately provide substantial evidence regarding the functional status after skin lined free flap reconstruction of the tongue. We present our experience with the skin lined free flap reconstruction for defects of the tongue and floor of the mouth, highlighting the reasons for its versatility and benefits, and presenting analyses of the functional results.

Materials and Methods

This prospective longitudinal study was conducted in the department of ENT and Head and Neck surgery at a tertiary care center in Punjab, India. This study included 93 patients with (SCC) squamous cell carcinoma of the tongue (T2, T3, and T4a according to the UICC 2002 TMN staging classification). These patients underwent tumor resection with intraoral defect reconstruction either by FRF flap or ALT flap. The following were the criteria for the selection of patients.

Inclusion Criteria

1. All patients with T2, T3, and T4a SCC of the tongue, who underwent tumor resection and defect reconstruction by either ALT flap or FRF flap in the same seating, were enrolled for the study.

Exclusion Criteria

1. Patients with T1 SCC of the tongue, as they underwent primary closure after tumor resection.

2. Patients who had resection of the mandible along with the tongue during tumor resection or involvement of the base of the tongue were excluded.

3. Patients with free flap failures that could not be salvaged were excluded.

4. Patients who showed any evidence of recurrence within 9 months after the completion of the treatment were excluded.

5. Patients with prior history of any surgery of the aerodigestive tract were excluded.

The decision between ALT flap and FRF flap was taken based on the volume of tumor resection and by surgical risk assessment through application of the National Surgical Quality Improvement Program (NSQIP) of the American College of Surgeons (ACS) [4]_. The functional outcome of the reconstructed tongue was assessed 9 months after the completion of the treatment. The evaluation included.

1. Swallowing: Barium swallow studies were done. The patient was further asked to swallow 100 ml of clear water at room temperature and the total time taken to swallow that water was noted.

2. Speech assessment: The functional integrity of the tongue was assessed using the speech task. The speech of the patient was assessed subjectively and objectively. The procedure was as follows:

(a) Objective assessment: The formants F1 and F2 of the vowels (/a/, /i/, /u/, and /ae/) were assessed. Since the frequency of the F1 is determined by the height of the tongue i.e. F1 is inversely proportional to the tongue height, it helps in determining the pliability of the movement of the tongue. High vowels (/u/, / i/), mid vowel /a/ and low vowel /ae/ were recorded using PRAAT software version 6.

(b) Subjective assessment: For the place of articulation the patients were given a word list consisting of high-frequency words, which included vowels and consonants in the initial, final, and medial position. To save time only a particular sound from the phonatory inventory was chosen viz. (p) for bilabials, (k) for velars, (ch) for alveolar, (t) for dental, and (r) for palatal. The speech was assessed by noting SODA errors (substitution, omission, distortion, and addition) of each phoneme.

3. Movements of the tongue: It included protrusion, retraction, and touching the palate.

4. Sensations: Touch, pain, and taste sensations of the reconstructed part of the tongue were tested.

The above functions were also assessed and matched with normal individuals (normative). The age and sexes were matched with the patients. The data obtained were analyzed by the student ‘t’ test and the p values < 0.05 were considered statistically significant. All patients had given their written informed consent. This study was approved by the Ethics Committee of the institute.

Results

In this study of 93 patients of SCC tongue, 72 were males which constituted 77% of our patients and 21(23%) were females. The mean age was 52.8 years. The age of the youngest patient was 32 years and the oldest was 74 years.

40 patients staged as T2 (43%), 46 patients were staged as T3 (49.46%), and 7 patients (7.5%) were staged as T4a disease. In N classification, 33 patients (35.5%) had N0 disease, 28 patients (30.1%) had N1 disease, and 34 patients (34.4%) had N2 disease. Of 93 patients, 58 (62.4%) patients were reconstructed with FRF flap, while 35 (37.6%) patients had reconstruction with ALT flap. There was a vascular crisis in 4 patients of FRF flap and 5 patients of ALT flap and hence secondary treatment was needed and hence they were not included in the study. So of 84 patients, 10(11.9%) patients did not receive any adjuvant therapy, 40(47.6%) patients had adjuvant radiation and 34 patients (40.4%) had both adjuvant radiation and chemotherapy. 11 patients were lost to follow-up and another 12 patients had a recurrence and were excluded from the study. So the data of the rest 61 patients was compiled and analyzed.

The duration of swallowing in normative was 5.2 ± 1.2seconds while in patients with FRF flap it was 7.5 ± 3.18secs while in patients with ALT flap it was 10.23 ± 4.02secs. Most (> 80%) of the patients with ALT flap finished the water in two gulps instead of one. When compared to the normative the p value was 0.03(significant) in FRF flaps while it was 0.001(highly significant) when compared with the ALT flap patients. None of the patients revealed any evidence of aspiration in the barium study. Acoustic analysis (Tables 1, 2, 3and 4) shows the vowel space between F1 and F2 of /ae/ and /u/ are significantly different in FRF flap and ALT flap (p < 0.001). F2 of /u/ and /ae/ and F2 of /a/ and /i/ are more affected in ALT flap. In FRF flap only F2 of /ae/ and /u/ shows a significant difference than the normative. In the articulation assessment task, the most common errors were substitutions of consonants viz. palatal sound (palatal stops such as t, d). Velaric sounds were substituted by dental sounds e.g. /k/–/t/ in FRF flap. Apart from these errors distorted affricates and fricatives, de-aspiration was also observed in patients with ALT flap. Speech intelligibility of all the participants were better (Mean = 2, SD = 0.5) than the ALT flap patients (Mean = 4, SD = 0.5). In both, the groups the bilabials and nasal consonants were spared. The tongue movements (protrusion, retraction, and elevation) were significantly reduced in patients of ALT flap. The result of the evaluation of the tongue sensations revealed that there was no taste sensation in either of the flaps and even sensation of touch was unremarkable in-spite of anastomosis of the distal part of the lingual nerve with superficial branch of the radial nerve in the FRF flap and lateral cutaneous nerve of the thigh in ALT flap, but sensation for pain was appreciated in 70.6% (24 out of 34 patients) of FRF flap and 62% (15 out of 27 patients) of ALT flap. Sensation for pain was not significant when both the groups were compared to the normative.

Table 1.

Comparison of mean of vowel space, F1-F2 in Normatives and ALT flap

	Normatives (n = 61)		ALT FLAP (n = 27)		‘t’ value	P value
	Mean	± SD	Mean	± SD
f1-f2 a	686.18	202.41	796.49	315.38	0.996	0.331
f1-f2 ae	790.05	27.02	1106.68	184.99	6.663	< 0.001**
f1-f2 i	1576.61	240.42	1684.40	102.79	1.127	0.273
f1-f2 u	2759.44	90.58	1088.11	441.18	14.418	< 0.001**

Student ‘t’ test: *p < 0.05; Significant; **p < 0.001; Highly significant

Table 2.

Comparison of mean of vowel space, F1-F2 in Normatives and FRF flap

	Normatives (n = 61)		FRF FLAP (n = 34)		‘t’ value	P value
	Mean	± SD	Mean	± SD
f1-f2 a	686.18	202.41	549.79	211.98	1.515	0.145
f1-f2 ae	790.05	27.02	1008.59	368.61	2.333	0.030*
f1-f2 i	1576.61	240.42	1392.05	363.74	1.466	0.157
f1-f2 u	2759.44	90.58	815.13	359.55	20.153	< 0.001**

Student ‘t’ test: *p < 0.05; Significant; **p < 0.001; Highly significant

Table 3.

Comparison of F1 and F2 of all the vowels used in assessment of ALT flap and normatives

	Normatives (n = 61)		ALT FLAP (n = 27)		‘t’ value	P value
	Mean	± SD	Mean	± SD
af1Hz	664.48	15.72	682.01	108.09	0.631	0.535
af2Hz	1350.66	200.66	1478.50	338.62	1.116	0.278
aef1Hz	659.73	17.83	628.04	71.12	1.660	0.113
aef2Hz	1449.79	25.50	1734.74	170.64	6.493	< 0.001**
if1Hz	323.75	52.63	382.77	97.50	1.863	0.077
if2Hz	1900.36	244.80	2047.95	140.03	1.474	0.156
uf1Hz	424.78	47.08	434.81	41.88	0.480	0.636
uf2Hz	3184.22	84.14	1522.91	447.39	14.235	< 0.001**

Student ‘t’ test: *p < 0.05; Significant; **p < 0.001; Highly significant

Table 4.

Comparison of F1 and F2 of all the vowels used in assessment of FRF flap and normatives

	Normatives (n = 61)		FRF FLAP (n = 34)		‘t’ value	P value
	Mean	± SD	Mean	± SD
af1Hz	664.48	15.72	735.06	63.07	4.176	< 0.001**
af2Hz	1350.66	200.66	1284.85	182.01	0.772	0.449
aef1Hz	659.73	17.83	669.14	92.42	0.389	0.701
aef2Hz	1449.79	25.50	1677.73	351.96	2.549	0.019*
if1Hz	323.75	52.63	537.80	318.66	2.588	0.017*
if2Hz	1900.36	244.80	1929.85	342.81	0.239	0.813
uf1Hz	424.78	47.08	487.93	123.89	1.776	0.090
uf2Hz	3184.22	84.14	1303.06	397.15	17.951	< 0.001**

Student ‘t’ test: *p < 0.05; Significant; **p < 0.001; Highly significant

Discussion

The impairment in the functional outcome of the tongue is due to loss of bulk, musculature, damage of innervations, post-operative and post radiotherapeutic fibrosis [5]. Previous studies showed that speech intelligibility is closely linked with the mobility of the remaining normal tongue and that swallowing capacity had a strong relationship with the volume of the reconstructed tongue. So the principle of reconstruction involves not only the restoration of bulk, shape, mobility, sensation but its functional aspects as well, like articulation, speech, mastication, and swallowing [6–8]_. So to achieve these goals one has to choose the most appropriate reconstruction method. When the tongue defect is small, primary closure can be done but it is unable to restore the tongue volume. It is demonstrated that the resected volume of the tongue was inversely proportional to the functional outcomes. Therefore, if there is a large defect after tongue resection, loco-regional pedicled, or free flaps are necessary to restore the volume and functional outcome of the tongue [9]_. There are various techniques described in the literature to reconstruct the tongue defects. Transfer of skin-lined free flaps is the optimal method for oral cavity reconstruction [10]. The first free ALT flap was reported by Song et al. in 1984 [11].Since then the free ALT flap has become very popular in body soft tissue defect reconstruction because it is reliable and versatile [12–14], but it is too thick to reconstruct tongue defects. Although secondary debulking procedures can be performed [15] they impose additional burdens and stress on patients. So the conquest for a thin skin flap for tongue defects made Yang et al. report their first FRF flap in 1981 [16], thereafter this was widely used for tongue reconstruction. The FRF flap too is not free from morbidity as it leaves behind a conspicuous aesthetic deformity in the forearm and also carries the risk of exposing important structures, such as tendons and nerves, which may result in potential dysfunction such as hand stiffness, pain, anesthesia, and poor visual appearance [17, 18]. However, there is no consensus on the ideal reconstructive method [9].

In the present study though there was no swallowing defect or evidence of aspiration in both group of patients of flap reconstruction as compared to the normative, there was significant variation (p = 0.03) in the duration of swallowing i.e. 7.5 ± 3.18 secs in FRF flap, while in patients with ALT flap it was 10.23 ± 4.02 secs (p < 0.001) as compared to 5.2 ± 1.2 sec in normative.

Vowels are identified by their formants. The formant F1 values are not only related to the vertical movements of the tongue but also influenced by the closing of the mouth and narrowing of the pharynx. The formant F2 values are related to the anterior position of the tongue or its lowering in the posterior region [19–21]. Our first finding in an acoustic analysis showed that although statistically, the vowels showed a significant difference in /ae/ and /u/. The difference in F1-F2 (Tables 1 and 2) showed that the speakers had a significantly smaller vowel space in ALT flap, which explains the overall centralization of vowels and overall poor intelligibility in speakers with ALT flap. Secondly in our study, we found that the vowels/ae/ and /u/ were more affected in both the group of patients. Earlier studies have reported that usually front vowel /i/ and the back vowel /u/ both are difficult sound for post-glossectomy patients to produce [22]. The first possibility is that for ALT flap the bulk of the muscle tissue helps in touching the palate and hence the production of /i/ is spared. On the other hand, the vowels/ae/ and/u/ needs the tongue to be protruded forward in the cavity which is not quite achieved. Secondly, it is interesting to note that the /i/ vowel in English is produced more frontal compared to Indo-Aryan languages [23] which explains earlier observations. Hence we might conclude that linguistic variation of phonemes is essential to consider in acoustic evaluation.

After wide excision of defect and reconstruction by ALT and FRF flap, the changes in configuration and volume of the oral cavity generate resonant and articulatory alterations, thus intelligibility of the patient’s speech is lowered. Review of previous literature reveals that the there are studies which have evaluated the functional outcomes of the reconstructed tongue based on subjective assessment and feedback questionnaires from the patients [9, 21]. This usually is confounded by patient’s biases and inadequate information. In our study we have done objective assessment like acoustic and phonetic assessment with other tongue function tests to support and obtain an evidence based research.

This study compared the postoperative speech and swallowing function of 61 patients who underwent ALT and FRF flap reconstruction after glossectomy with sexes and age-matched normative, and statistically analyzed the effects on the speech in telligibility and acoustic spectrographic characteristics of the formants of oral vowels. Hsiao et al. reported that speech outcomes were better with primary closure; however, the swallowing function was better with flap reconstruction after hemiglossectomy. That study has several limitations; it included only a limited number of patients, and a significant proportion of patients underwent mandibulotomy, which could adversely influence speech and swallowing outcomes [2]. Regarding postoperative swallowing function, the tongue is essential for propelling a food bolus toward the pharynx, and the shape and bulk of the reconstructed tongue are closely related to postoperative swallowing outcomes. This was supported by our study, where despite the increasing volume of the defect, none of the patients reported any swallowing difficulty or any features of aspiration.

Wide surgical resection of the tongue results in the severing of the lingual nerve, affecting sensation. The loss of specific tongue sensations could affect a person's oral function and quality of life [24]. In this study, we explored the sensation in the reconstructed part of the tongue by ALT and FRF flap and compared it with age and sexes matched normatively. Sensations tested were touch, pain, and taste. Results indicated that the type of surgical nerve repair did not have a significant impact on overall sensory outcomes. Pain sensation was appreciated by the patient but there was no response to touch and taste sensation. In the literature, too mixed results have been reported for either nerve repair techniques. The poorest sensory outcomes were observed in patients with the lingual nerve severed, while all patients with lingual nerve intervention exhibited deteriorated taste sensation on the affected tongue side. Overall, the patients with oropharyngeal reconstruction with lingual nerve intervention exhibited decreased levels of sensation on the operated tongue-side, with minimal differences between types of lingual nerve repair. The earliest return of sensation to touch was recorded 3 months after surgery in patients with Nakajima fan flaps and Karapandzic fan flaps and the latest 24 months with radial forearm free non innervated flap postoperatively, while some patients failed to regain any flap sensation after follow up of 25 and 18 months, especially in patients reconstructed with pectoralis major myocutaneous flaps and radial forearm free flaps [24].

We evaluated the sensation after 9 months after the treatment while the literature report 24 months for the reinnervation period. The goal of glossectomy de fects repair is to maximize the movement of the tongue and to minimize the morbidity of the surgery. This study and review of literature too ensures that neither of the flaps restores speech nor swallowing function to the same level as that in normal individuals, but the results are still acceptable [2] and in our study also we found that the patients achieved satisfactory tongue functions.

Conclusions

In summary, we evaluated the tongue functions after free flap reconstruction and found that for the restoration of the tongue functions to near normal we should aim to the restoration of structural support, bulk, and mobility. It won’t be wrong if we conclude that both the free ALT flap and the FRF flap can provide acceptable functional restoration after radical tumor resection of the tongue.

Funding

The research did not receive any funding.

Availability of Data and Materials

The study is purely observational study of human participants done under the first author and is transparent without any manipulations or fraud statements.

Compliance with ethical standards

Conflict of interest

None.

Consent to Participants

Proper consent was taken from patient whenever needed.

Ethical Approval

Approved by colleges ethical committee.