Abstract
Progress in (reconstructive) surgery and radiotherapy tends to improve survival and reduce oral functional deficits. Despite the growing sophistication of cancer treatment, patients still report deterioration in tongue function. Sensory function, mobility, and force of the tongue were determined in 45 patients with a carcinoma of tongue and/or floor of mouth. Measurements were performed before surgery, shortly after surgery, shortly after radiotherapy, 6, and 12 months after surgery. Surgery had a negative impact on tongue sensory function and mobility. Post-surgery radiotherapy did not further deteriorate sensory function, mobility, or force of the tongue. Patients in the surgery-radiotherapy group (SRG) had significantly worse tongue sensory function and mobility than patients in the surgery group (SG), probably caused by more advanced tumour stage and more extensive reconstructions and related scar tissue. The tongue force in patients in both groups significantly increased in the first 6 months after surgery, but this increase disappeared in the next 6 months. The authors conclude that surgery had a significant negative influence on tongue function, especially in the group of patients treated with radiotherapy. No further deterioration of tongue function was observed after post-surgical radiotherapy within the first year after surgery.
Patients with cancer in the tongue and/or floor of mouth region run a high risk of deteriorated tongue function caused by the tumour or induced by treatment. Progress in (reconstructive) surgery and radiotherapy tends to improve survival and reduce oral functional deficits . Despite the growing sophistication of cancer treatment, patients still report deterioration in tongue function .
The tongue plays a major role in mastication, deglutition of food, oral hygiene, and speech. The strength of the tongue, its great flexibility, and ability to take variable shapes are conditioned by the activity of the intrinsic tongue muscles and the extrinsic floor of the mouth muscles, that are complementary to one another . The tongue is vital for the transport and positioning of food between the molars, selecting fragments for further comminution, incorporation of fragments with saliva, posterior transport of the resulting bolus, and its final deposition into the oropharynx .
During the oral stage of swallowing, the tongue presses against the hard and soft palate and moves sequentially in an anterior to posterior direction to propel the bolus to the pharynx . The ability to take variable shapes, flexibility, and strength of the tongue is important in articulation to produce consonants and vowels either lingual or palatal . The sensory mechanisms of the tongue are necessary to accomplish the changes in shape and position of the tongue and floor of the mouth required for mastication, deglutition, and proper articulation . The perception of the bolus is important for the efficacy of mastication and deglutition. The sensory function of lips, tongue, and teeth overlap on the primary somatosensory cortex . Deterioration of peripheral afferent input of the tongue causes a disturbance in the central control of the cortex during mastication, deglutition and articulation . Loss of sensory function in the oral cavity will thus hamper full functional rehabilitation.
The aim of this prospective cohort study was to examine and quantify the effect of surgery, with or without radiotherapy, on tongue function in patients with malignancies in the tongue and/or floor of mouth. The authors measured tongue sensory function, tongue mobility, and maximum tongue force at various moments before and after surgery and radiotherapy. They determined the influence of tumour size, tumour location, and surgical intervention on the deterioration of tongue function as measured shortly after surgery. Relationships between these deteriorations in tongue function were determined. The outcomes of the patients were compared with the outcomes of healthy controls. The first hypothesis was that treatment would significantly deteriorate tongue function. The second hypothesis was that treatment with surgery and radiotherapy, compared to surgery only, would have significantly more negative influence on tongue function.
Materials and methods
From January 2007 until January 2008, a group of 45 patients with a primary malignancy in tongue and/or floor of mouth and a group of 60 healthy controls matched for age were recruited for this study. Exclusion criteria were previous, synchronous or recurrent malignancies in the head and neck area, cognitive impairment, and inability to understand Dutch. Patients were treated with curative intend by surgery only ( N = 23) or by surgery and radiotherapy ( N = 22). In 4 dental practices, 60 healthy people matched for age and gender were recruited. More details of the control group have been published . The protocol was approved by the Ethics Committee of University Medical Center Utrecht and Radboud University Nijmegen Medical Centre. All subjects received a written explanation of the study, and informed consent was obtained from each subject before the start of the study.
Postoperative radiotherapy (Intensity-Modulated Radiation Therapy) was given within 6 weeks of surgery when indicated, according to the treatment guidelines of the Dutch Head and Neck Oncology Group, based on the histology of the resection specimen. Pathological tumour stage (pT) , resection site, and reconstruction were collected from the patient’s medical data. Patient characteristics are summarized in Table 1 .
| SG ( N = 23) | SRG ( N = 22) | p value | |
|---|---|---|---|
| Pathological Tumour stage (pT) | |||
| T1 | 18 | 5 | |
| T2 | 5 | 9 | 0.001 *** |
| T3 | 0 | 4 | |
| T4 | 0 | 4 | |
| Resection site | |||
| Tongue | 17 | 10 | |
| Floor of mouth | 4 | 5 | |
| Floor of mouth & Slice mandible | 2 | 4 | 0.233 |
| Tongue & Floor of mouth | 0 | 2 | |
| Tongue & Floor of mouth & Slice mandible | 0 | 1 | |
| Reconstruction | |||
| Primary closure | 17 | 5 | |
| Local flap | 1 | 0 | 0.001 *** |
| Myocutaneous or free flap | 5 | 17 | |
| Bone graft/flap | 0 | 0 | |
Patients were measured at maximal 4 weeks before surgery, shortly (4–6 weeks) after surgery, shortly (4–6 weeks) after radiotherapy, 6, and 12 months after surgery. Healthy persons were measured once. The following variables were determined: thermal sensory function; tactile sensory function; protrusion; lateralization; and maximum force of the tongue.
Sensory function of tongue
Thermal sensory function (thin afferent fibres) and tactile sensory function (thick afferent fibres) were tested by presenting pairs of stimuli: a real stimulus and a sham one. The real and sham stimuli were presented in random order, during two periods of attention that were announced by the examiner whilst the patient kept their eyes closed. After each pair, the patient had to report the order of real and sham stimulation (forced-choice procedure). Three pairs of stimuli were presented. The magnitude of the test stimulus was chosen as the value at which control subjects could just detect this stimulus with nearly zero errors, so that patients could consistently make the correct choice for uninjured sites. The test sites (right and left) were as close as possible to 10 mm from the tongue tip and 10 mm from the right and left edge of the tongue. For analyses the outcome of the (most) affected site was used. Thermal sensory function was tested using a heat-conducting aluminium rod (diameter 2.0 mm) as a real stimulus (22 °C; touch as well as cold sensory function). The sham stimulus was produced by a non-heat-conducting Perspex rod. Tactile sensory function was evaluated using a Semmes–Weinstein monofilament (Semmes–Weinstein Aesthesiometer, Stoelting Co., Wood Dale, IL, USA) with index number 3.22 . The real stimulus was a touch with the filament. The sham stimulus was achieved by approaching the patient with the device whilst the filament was turned away. The score for reduced thermal or tactile sensory function was 0 and for normal sensory function 1. A detailed description of this procedure has recently been published .
Tongue mobility
Tongue mobility was determined by measuring tongue protrusion and lateralization . Tongue protrusion was rated on a three point scale: the tongue cannot touch the lower lip (0 points); can touch the lower lip (1 point); passes the lower lip (2 points). Lateralization was rated on a three point scale as well: the tongue cannot touch the mouth corner (0 points); can touch the mouth corner (1 point); passes the mouth corner (2 points). The right and left tongue lateralization were averaged for the outcome measure of tongue lateralization.
Maximum tongue force
Maximum tongue forces were measured in cranial direction. The device for measuring the tongue force consisted of a strain gauge mounted on a mouthpiece. The strain gauge had a surface area of 110 mm 2 and a vertical height of 4.5 mm. The strain gauge element was placed between the tongue and the palate at the midline of tongue, 5 mm from the tip. The patient’s task was to press the tongue as hard as possible to the palate. The task was performed twice. The highest tongue force of both efforts was used in the study.
Sample size
To detect differences between the SG and the SRG, using ANOVA, the authors assumed a minimal effect size of 0.40 at an α of 0.05 and a power ( β ) of 0.80. This effect size was used to detect small differences between the two treatment groups. Consequently, using an effect size of 0.40 at least 20 persons were needed per treatment group in this study.
Statistical analysis
The presentation of results is primarily descriptive with means, standard deviations (sd), and standard error of the means (SEM). Characteristics of the two patient groups before intervention were compared using a χ 2 test. In each treatment group (i.e. SG and SRG) changes in time of sensory function, mobility, and maximum force of the tongue were analysed by repeated measures of analysis of variance (ANOVA) for continuous data and by a Friedman test for ordinal data. Repeated measures ANOVA and the Friedman test determine possible differences amongst all measurement moments. These tests are susceptible to missing data, due to patients who died, stopped, or missed a measurement. To avoid this disadvantage, the authors also performed paired t tests (continuous data) and Wilcoxon signed rank tests (ordinal data) to test differences between two measurement moments only. For nominal data McNemar tests between two measurement moments were performed. Differences between the SG and the SRG, and the healthy controls were analysed by independent-samples t tests (continuous data), Mann–Whitney U -tests (ordinal data), and χ 2 tests (nominal data). One-way ANOVA and Kruskal–Wallis tests were used to find explanatory factors for the changes of outcomes of tongue function before and shortly after surgery for all patients. Relationships between the various tongue function results before and shortly after surgery were determined with Spearman correlations and Cramer’s V tests. A p -value less than 0.05 was considered statistically significant. All analyses were performed with SPSS 15.0 software (SPSS, Inc., Chicago, IL, USA).
Results
Forty-five patients, with a squamous cell carcinoma of tongue and/or floor of mouth, were included in this study. Twenty-three patients were included in the SG, 9 women and 14 men aged 63.9 ± 14.0 years (mean ± sd). Twenty-two patients were included in the SRG, 6 women and 16 men aged 61.8 ± 10.0 years. Characteristics of pT, resection site, and type of reconstruction are listed in Table 1 . χ 2 tests revealed that patient numbers were significantly different for both intervention groups with respect to pT and type of reconstruction ( Table 1 ).
Figure 1 is a flow-chart of the measurement moments and measured patients. Two patients were not measured between surgery and the start of radiotherapy, because of time constraints. Two patients (SG) had an additional resection within a month after surgery. One patient (SRG) had a reconstructive procedure between 6 and 12 months after surgery because of extensive osteoradionecrosis.
Thermal and tactile sensory function of tongue
Significant decreases in thermal and tactile sensory function due to surgery occurred in the SRG only ( Fig. 2 ). Patients in the SRG had lower thermal and tactile sensory function scores than the surgery patients. Before surgery, patients in both treatment groups had similar thermal sensory function scores as healthy controls. Patients in the SG also had similar tactile sensory function as controls, whereas the patients in the SRG had significantly lower tactile sensory function scores than the controls ( Table 2 ). At all measurement moments after surgery, patients in both treatment groups had significantly worse thermal and tactile sensory function of the tongue as compared to the healthy controls, with the exception of thermal sensory function in the SG 6 and 12 months after surgery.
| Patients | SG | SRG | SG | SRG |
|---|---|---|---|---|
| Controls | Controls | Controls | Controls | |
| Sensory function a | Thermal sensory function | Tactile sensory function | ||
| Before intervention | 1.000 | 0.268 | 0.074 | 0.017 ** |
| Shortly after surgery | 0.001 ** | 0.000 *** | 0.001 ** | 0.000 *** |
| Shortly after radiotherapy | – | 0.000 *** | – | 0.000 *** |
| Six months after surgery | 0.070 | 0.000 *** | 0.004 ** | 0.000 *** |
| Twelve months after surgery | 0.056 | 0.000 *** | 0.003 ** | 0.000 *** |
| Tongue mobility b | Protrusion | Lateralization | ||
| Before intervention | 0.022 * | 0.004 ** | 0.001 ** | 0.000 *** |
| Shortly after surgery | 0.000 *** | 0.000 *** | 0.000 *** | 0.000 *** |
| Shortly after radiotherapy | – | 0.000 *** | – | 0.000 *** |
| Six months after surgery | 0.019 * | 0.000 *** | 0.000 *** | 0.000 *** |
| Twelve months after surgery | 0.000 *** | 0.000 *** | 0.000 *** | 0.000 *** |
| Maximum tongue force c | Force | |||
| Before intervention | 0.097 | 0.022 * | ||
| Shortly after surgery | 0.012 * | 0.044 * | ||
| Shortly after radiotherapy | – | 0.040 * | ||
| Six months after surgery | 0.199 | 0.841 | ||
| Twelve months after surgery | 0.026 * | 0.015 * | ||
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