Introduction
Head and neck radiotherapy (RT) is a highly effective
therapeutic intervention in the treatment of head and
neck cancer. Side effects of RT, such as cutaneous reactions,
xerostomia, and mucositis, can have a negative impact
on function and quality of life. However, the effects
of RT or chemoradiotherapy (ChRT) on mastication are
less well understood. Trismus, or restricted mouth opening,
is a significant late effect of head and neck tumor irradiation
that can cause difficulties with everyday activities
such as chewing, swallowing, eating, breathing, and
speaking.[,] Pain, loss of weight, and poor oral hygiene
can all complicate the clinical scene. The disruption of
the temporomandibular joint, tumor invasion into masticator
muscles and mouth-closing muscles, and the
presence of additional treatments such as surgery and
chemotherapy can all increase the risk of trismus. The
severity of trismus is affected by the patient's tolerance as
well as several treatment-related factors such as the size
of RT fields, the total dose of RT, and concurrent chemotherapy.[-] The restriction of mouth opening usually
begins 2.5-3 months after the completion of RT and
progresses over time. A 35mm cut-off value is widely accepted
as the criterion for trismus.[,]
Patients at risk of trismus should begin trismus prevention
exercises as soon as possible to maintain maximum
mouth opening and jaw mobility. Once trismus
has developed, it requires a rigorous exercise regimen,
which may be supplemented with physiotherapy if necessary.[] Patients with trismus can benefit from prosthetic
appliances (dynamic bite openers) with springs
and bands that stretch their muscles.[] Compliance
with trismus exercises by patients is critical to the
success of preventative and treatment regimens. The
aim of the current study is to identify the risk factors
for trismus in patients with irradiated head and neck
cancer whose disease has not spread to the temporomandibular
joint, as well as to determine whether selfrehabilitation
exercises used after RT have an effective
therapeutic impact on mouth opening distances.
Methods
The study included 53 patients with squamous cell carcinoma
of the head and neck who were receiving RT at
Trakya University, Department of Radiation Oncology.
The study protocol was approved by the University's
Medical-Ethical Review Board. The patients were evaluated
in a multidisciplinary clinic, where they received
evaluations and treatment recommendations from a physical therapist and radiation oncologists. The measurements
were always taken by the same examiner.
The patients were instructed to completely open their
mouths, and the mouth opening distances (MOD)
were measured in millimeters using a Boley gauge.
When the maximal interincisal distance between the
upper and lower alveolus is less than 35 mm, it is considered
trismus, according to Dijkstra et al.[].
Radiotherapy: Megavoltage beams were used to
deliver RT using either a linear accelerator (6 MV) or
a Cobalt-60 treatment unit. The patients were treated
using either conventional (two lateral opposed and
supraclavicular fields) or 3D conformal irradiation
techniques. Patients were given a 66 Gy dose for T1-2
tumors and a 70 Gy dose for T3-4 tumors or persistent
lymphadenopathy. To treat subclinical disease, a radiation
dose of 50 (50-60) Gy was used.
Chemotherapy: Depending on the patients' overall
medical condition, three cycles of concurrent cisplatin
(CDDP) were administered, either every three weeks at
100 mg/m2 or at weekly intervals at 40 mg/m2.
Rehabilitation Program
Three months after RT, the patients were seen by the
physiotherapist, the first mouth opening distance
measurements were taken, and the rehabilitation
program was initiated. The patients did self-rehabilitation
exercises for three months. The second set of
measurements was taken six months after RT. The
exercises listed below are geared toward patients.[]
The exercises were performed three times a day, after
breakfast, lunch, and dinner:
• Opening the mouth completely, counting to 3 seconds
with the mouth open, and then closing the
mouth - 5 times.
• Counting to 3 seconds with the chin on the right,
then returning to the normal position - 5 times.
• Counting to 3 seconds with the chin on the left,
then returning to the normal position - 5 times.
• Counting to 3 seconds with the chin forward, then
returning to the normal position - 5 times.
Patients chewed two sticks of gum (Trident sugarless) for
15 minutes immediately following the exercises. For three
months, they repeated these exercises on a daily basis.
Statistical Analysis
The normality assumption was checked using the Shapiro-
Wilk test. The Student's t-test or Mann-Whitney
U tests were used to compare two independent groups
based on the normal distribution. The Wilcoxon signedrank
test was used to compare dependent groups. Pearson
chi-square and Fisher's exact tests were used to investigate relationships between categorical variables.
Multivariate logistic regression models were used to
detect independent risk factors for trismus before and
after physiotherapy. Descriptives were expressed as
mean and standard deviation or median and interquartile
range for numerical variables, and as frequency and
percentages for categorical variables. A p-value of less
than 0.05 was considered statistically significant. All
analyses were performed using R software version 4.0.3.
Results
In this study, 53 patients were examined. The average age
was 59 years (range: 31-84). Men made up 42 of the 53
patients (79%). The larynx was the most common primary
tumor site (32 pts, 60.3%). Prior to RT, no patients
had tumor invasion of the temporomandibular joint.
T3-4 disease was staged in 29 (54.2%) of the patients,
while N2-3 disease was staged in 28 (52.8%).
Adjuvant RT was given to 27 patients (51%) after initial
surgery. Seventeen (32.1%) of these 27 patients received
concomitant ChRT, whereas 10 (18.9%) received
only RT. There were 26 patients who had definitive RT
(49%). Seventeen (32.1%) of the 26 patients received
concomitant ChRT. Only RT was applied to 9 (17%) of
the patients. Concomitant ChRT was administered to 34
(64.1%) of the 53 patients, while RT alone was administered
to 19 (35.9%). The average dose of RT was 63.1
Gy (range: 30-72 Gy). Table 1 summarizes the patients'
characteristics based on trismus prior to treatment.
For the whole group, the rate of trismus was 41.5%
(22 of 53 pts). Although there was no statistically
significant difference between genders, trismus before
physiotherapy was found to be higher in females than in males (63.6% vs. 35.7%; p=0.198). There was
no statistically significant difference in the mean ages
of the trismus and non-trismus groups (57.6±12.3 vs.
61±12.8; p=0.335). The primary tumor site was found
to be a significant factor for trismus, as the prevalence
of trismus was found to be higher in the nasopharynx
compared to the larynx (83.3% vs. 25.0%; p=0.006).
Trismus before therapy was more prevalent in patients
who had concomitant chemotherapy (50.0% vs. 23.5%;
p=0.068). Time after RT was another significant factor
that affected trismus before physiotherapy. Trismus
prevalence was found to be higher in patients with more
than 36 months past after RT compared to less than 36
months (66.7% vs. 32.4%; p=0.025). There were no statistically
significant differences in tumor stage (early:
38.1% vs. late: 44.8%; p=0.634), nodal stage (N0-1:
36.4% vs. N2?3: 46.4%; p=0.474), primary treatment
(RT: 28.6%, RT+S: 43.5%; p=0.686), or RT doses (≤50
Gy: 20.0% vs. >50 Gy: 43.8%; p=0.389).
Table 1 Patient characteristics based on trismus before physiotherapy exercises
Before physiotherapy, the mean mouth opening
distance (MOD) for the entire group was 37.33±7.83
mm. After physiotherapy, this value was found to be
38.75±7.66 mm, and the difference was statistically significant
(p = 0.035). Time after RT, concurrent ChRT,
and primary tumor localization were statistically significant
factors in univariate analysis that could affect
MOD in terms of physiotherapy. In patients with more
than 36 months past after RT, the median MOD was
35 mm (8-48) before physiotherapy. Although patients with fewer than 36 months past after RT had a greater
MOD [40 mm (25-62)] than those with more than 36
months [35 mm (8-48)], the difference was not statistically
significant (p = 0.182). However, the median MOD
values in these two groups converged after physiotherapy
(40 mm (25-62) vs 40 mm (10-50); p = 0.791). In
patients more than 36 months following RT, physiotherapy
resulted in a substantial improvement in median
MOD values (35 mm (8-48) vs. 40 mm (10-50),
p<0.001). In patients with less than 36 months since RT,
there was no significant difference in MOD values before
and after physiotherapy (p=0.242). (Table 2).
Table 2 Relations between time after radiotherapy, concomitant chemoradiotherapy, and
primary tumor site with physiotherapy in regard to mouth opening distance (MOD)
Another risk factor for MOD was concurrent chemotherapy.
Patients who received concurrent chemotherapy
had significantly lower mean MOD values
(35.83±7.51 mm and 36.77±7.35 mm) before and after
physiotherapy than patients who did not receive concurrent
chemotherapy (40.52±7.56 mm and 42.94±6.71
mm; p=0.04 and 0.005, respectively). Although physiotherapy
improved mean MOD values somewhat in individuals
receiving concurrent chemotherapy, the change
was not significant (35.83±7.51 mm vs 36.77±7.35 mm;
p=0.313). In patients who did not receive concurrent
chemotherapy, however, physiotherapy resulted in a statistically
significant improvement in mean MOD values
(40.52±7.56 mm vs 42.94±6.71 mm; p<0.001) (Table 2).
Similarly, there were significant differences in MOD
values among primary tumor sites before and after
physiotherapy (p=0.006 and 0.027, respectively). Patients with tumors located in the nasopharynx had the
lowest mean MOD values compared to those in the larynx
and other locations before and after physiotherapy
(30.00±11.30 mm and 31.67±12.51 mm, respectively).
Although physiotherapy improved mean MOD values
slightly, differences were not significant for nasopharynx
and larynx localizations (p=0.329 and 0.479, respectively),
but significant for other localizations
(36.07±5.26 mm vs 37.87±4.56 mm; p<0.001) (Table 2).
Two multivariate logistic regression models were
built to evaluate the risk factors for trismus before
and after physiotherapy (Table 3). The variables with
p-values less than 0.20 in Table 1 were included in the
models as independent risk factors. In Model 1, where
the dependent variable was trismus before physiotherapy,
concomitant chemotherapy (OR=5.648, 95% CI:
1.043-30.596) and time passed after RT of more than 36
months (OR=8.238, 95% CI: 1.410-48.136) were found
to significantly increase the risk of trismus. However,
no significant independent risk factor was found in
Model 2, where the dependent variable was trismus after
physiotherapy. This result suggests that physiotherapy
might be effective against trismus. The multivariate
logistic regression results are visualized in Figure 1.
Table 3 Multivariate logistic regression results for independent risk factors of trismus before and after physiotherapy
Fig. 1. Error bars for multivariate logistic regression models. The bars represent odds ratios
and corresponding 95% confidence intervals.
Model 1: Dependent variable is trismus before physiotherapy (trismus: n=22, non-trismus: n=31);
Model 2: Dependent variable is trismus after physiotherapy (trismus: n=15, non-trismus: n=38).
Discussion
In this study, we aimed to determine whether selfrehabilitation
therapy, used after RT, has an effective
therapeutic impact on trismus in patients with irradiated head and neck cancer, for the first time. We discovered
that the time elapsed after RT has a significant
impact on MOD, with the longer the time elapsed after
RT resulting in less MOD. Furthermore, there was a
significant correlation in trismus incidence between
concurrent ChRT and tumor localization. It was also
discovered that self-rehabilitation exercises have a positive
impact on MOD values in patients with more than
36 months of follow-up after RT, in patients who did
not receive concurrent ChRT, and in patients whose
tumors were not located in the nasopharynx or larynx.
The prevalence of trismus in patients with head and
neck cancer ranges from 8% to 62%.[,,,-] One
reason for this variation is the lack of uniform criteria
for defining trismus. Nguyen et al.[] used 40 mm or
less of MOD for trismus, whereas Chua et al.[] used
25 mm or less. In this patient population, a MOD of
35 mm or less has been accepted as a cut-off level for
trismus. The mouth opening was 35 mm or less in 22 of
53 patients (41.5%) in our study group, which is similar
to the study of Johnson et al.,[] which found trismus
(35 mm) in 42% (29 of 69) of the patients.
Although trismus is an important RT-related side effect,
there have been only a few prospective randomized
studies comparing the rehabilitation programs.[,-] Additionally, the best rehabilitation approach is still
unclear.[] The common and traditional approach to
treating patients with RT-induced trismus is to treat
them based on their needs in the event of loss of function
in the symptomatic period.[] Another approach
is to integrate preventive rehabilitation into the existing clinical routines for all patients with or without trismus.
However, the effectiveness of this approach is controversial.
Some studies state that preventive exercises do not
yield any improvement in MOD.[] Ahlberg et al.[]
were not able to show any positive effect of early selfcare
preventive rehabilitation. In a recent meta-analysis,
the authors found no significant difference between the
standard of care and exercise therapy.[]
Physiotherapy was applied with various apparatus
in almost all studies to treat or prevent trismus.[]
Those apparatuses are used as incentives to improve
exercise compliance or therapeutic effectiveness. Rubber
plugs, wooden tongue blades, TheraBite exercisers,
and dynamic bite openers are among the devices used.
[,,,] So far, two studies have employed physiotherapy
exercises without any apparatus for the prevention
of trismus, but as with other prevention studies, no
benefit has been found with this practice.[,] Grandi
et al.[] compared two different physiotherapy exercise
methods, including the method described by Santos
et al.,[] to prevent trismus in irradiated patients.
Although there were no statistically significant differences
between the two methods, the authors stated that
there was a trend toward better clinical results in patients
who were given the exercises described by Santos
et al. In another study, Hogdal et al.[] looked at the effectiveness of early guided exercises combined with
self-care treatment on trismus in 100 individuals undergoing
head and neck irradiation. When compared to
standard treatment, the authors discovered that an early
exercise regimen did not appear to provide any additional
benefits. Unlike previous studies, in the current
study, the motion exercises without using any apparatus
described by Santos et al.[] were used for the treatment
of trismus for the first time, and improvements in MOD
values were obtained. It's possible that patients' compliance
in conducting the exercises is higher once the
problem occurs, which explains why exercises are more
effective in treating than preventing trismus.
Because trismus is a late effect of RT, which causes
fibrosis in the masticatory muscles and soft tissue of the
cheek, its occurrence and severity worsen over time. According
to studies, the restriction in MOD occurs quickly
in the first year and continues for the next four years.
Wang and colleagues investigated the long-term effects
of RT on trismus after nasopharyngeal carcinoma and
discovered that the MOD decreased significantly between
one and nine months after RT, with an overall
reduction of 32% in MOD within four years.[] Furthermore,
these findings were supported by a systematic
review, which revealed that patients have a reduced
MOD of 18% between 6 and 12 months after RT.[] In our study, time was also a prominent factor for trismus
in multivariate analysis (p=0.019). Patients with more
than 36 months past RT have less MOD than those with
less than 36 months. Self-rehabilitation had a positive
impact on MOD values in this patient group (p<0.001).
Another negative factor for trismus is applying
chemotherapy concomitantly to RT. This approach is
more intensive and leads to more fibrosis and hence
more trismus. In a study by Jeremic et al.,[] the most
independently significant factor was concurrent chemotherapy
in the multivariate analysis (p=0.0181) for
moderate to severe trismus. Bensadoun et al.[] discovered
a 30.7% prevalence of trismus in 12 studies of
concurrent ChRT in a systematic review. Similarly, in
our study, patients who had concomitant chemotherapy
had significantly lower mean MOD values than
those who did not have concomitant chemotherapy,
both before and after physiotherapy, and the application
of physiotherapy made a slight improvement,
which was not statistically significant in mean MOD
values in patients who had concomitant chemotherapy
(p=0.313). Furthermore, we discovered in multivariate
analysis that concomitant ChT, one of the risk factors
for trismus, lost significance with the application of
self-rehabilitation exercises. However, as Payakachat
et al.[] illustrate, there has been other research with
contradictory results. When comparing the surgery
and RT groups to the ChRT group, the authors discovered
that the median score differences on the open
mouth item were considerably higher in the surgery
and RT groups. Additionally, survivors in the ChRT
group had more problems with swallowing, sticky saliva,
feeding tubes, and weight gain, while survivors in
the surgery and postoperative radiation therapy groups
had more problems with trismus.
Tumor localization is one of the other risk factors
for trismus. Tumors in the nasopharynx, oral cavity,
and oropharynx involving the muscles of mastication
have been linked to trismus due to the necessity of
using a wider range of RT fields and irradiation of the
temporomandibular joint.[,,] Similarly, in our
study, it was observed that patients with tumors located
in the nasopharynx had the lowest mean MOD
values compared to those in the larynx and other
locations before and after physiotherapy. Moreover,
physiotherapy did not make a significant improvement
in MOD values in patients whose tumors were
located in the nasopharynx and larynx.
Some other additional risk factors, such as gender,
age, RT dose, and nodal status, have been found
to contribute to the development of trismus in several studies.[,,] However, their effectiveness
has yet to be proven in the majority of other studies.
[,,] In our study, none of these risk factors was
found to be significantly related to trismus.
Our research has some limitations. The first is that
our study was not a randomized controlled trial. Furthermore,
self-rehabilitation exercises were used in our
study, and it is clear that it is impossible to determine the
patient's compliance with these exercises and the extent
to which the patients did these exercises as instructed.
As a result, we believe it is prudent to approach our findings
with caution. Furthermore, no apparatus was used
in the exercises. It should be noted, however, that we discovered
a significant contribution to MOD in our entire
patient group with exercises performed on their own.
Conclusion
In conclusion, for the first time, the self-rehabilitation
method used in this study, which did not include any
apparatus, was found to be an effective method for
treating trismus in irradiated patients with head and
neck cancer. We also discovered that self-rehabilitation
improves the MOD values of the entire patient
group, especially in patients who have had more than
36 months of follow-up after RT, in patients who did
not receive concurrent ChRT, and in patients whose
tumors were not in the nasopharynx or larynx. These
findings were obtained following a three-month period
of exercise. We believe that long-term exercises would
be more beneficial to MOD. Future randomized and
multicenter studies are needed to characterize the associated
risk factors for trismus and to determine the
best treatment or prevention method.
Ethics Committee Approval: The study was approved by
the Trakya University Faculty of Medicine Non-Interventional
Clinical Research Ethics Committee (no: 19/20, date:
19/09/2012).
Authorship contributions: Concept - V.Y.Ç., F.Ö.; Design
- V.Y.Ç., F.Ö., S.Y., M.Ç.; Supervision - V.Y.Ç., M.Ç.; Funding
- V.Y.Ç., F.Ö., M.Ç.; Materials - V.Y.Ç., F.Ö., S.Y., G.T.; Data
collection and/or processing - V.Y.Ç., F.Ö., S.Y., G.T.; Data
analysis and/or interpretation - S.K., M.Ç.; Literature search
- V.Y.Ç., M.Ç.; Writing -V.Y.Ç., M.Ç.; Critical review - M.Ç.
Conflict of Interest: All authors declared no conflict of interest.
Use of AI for Writing Assistance: Not declared.
Financial Support: None declared.
Peer-review: Externally peer-reviewed.
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