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Supportive Care in Cancer

https://doi.org/10.1007/s00520-021-06068-1

ORIGINAL ARTICLE

Impact of rehabilitation treatment on swallowing during adjuvant


radiotherapy following surgery in patients with oral
and oropharyngeal cancer
Nao Hashida 1 & Hironari Tamiya 1 & Takashi Fujii 2

Received: 11 June 2020 / Accepted: 9 February 2021


# The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature 2021

Abstract
Background Patients with advanced oral or oropharyngeal cancer sometimes require surgery and adjuvant postoperative radio-
therapy (PORT), which may cause dysphagia. However, the efficacy of rehabilitation treatment for PORT-induced dysphagia
remains unclear. This study aimed to determine whether rehabilitation treatment during PORT after surgery is effective for
dysphagia.
Methods We retrospectively studied 55 patients with oral or oropharyngeal cancer who received PORT. Of these, 25 received
rehabilitation treatment for swallowing during PORT. The Functional Oral Intake Scale (FOIS) score at 6 months after treatment
was used as the swallowing outcome. We performed multivariate linear regression and stratified analyses using the FOIS score
(poor oral intake group: FOIS score <5, good oral intake group: FOIS score ≧5) before PORT.
Results The median (interquartile range) FOIS scores at 6 months post-PORT were 6 (5–6) and 6 (4–7) in the non-rehabilitation
and rehabilitation groups, respectively. Multivariate linear regression revealed that rehabilitation treatment was a significant
independent factor for a better FOIS score. Stratified analysis of the changes in the FOIS score from pre-PORT values to those
obtained 6 months after treatment showed a significant difference in the good oral intake group between the rehabilitation and
non-rehabilitation groups. There was no significant difference in the FOIS score from pre-PORT values to those obtained 6
months after treatment between the rehabilitation and non-rehabilitation groups in the poor oral intake group.
Conclusion Rehabilitation treatment during PORT may achieve better swallowing outcomes in patients with advanced oral or
oropharyngeal cancer.

Keywords Dysphagia . Head and neck cancer . Radiotherapy . Rehabilitation treatment

Introduction organs for communication, swallowing, and breathing, the


treatment of HNC requires a balance between treatment effi-
Head and neck cancer (HNC), which consists mainly of squa- cacy and side effects. Treatment for HNC, including surgery,
mous cell carcinoma of the mouth, pharynx, and larynx, is radiotherapy (RT), and chemoradiotherapy (CRT), often
increasingly prevalent worldwide. Although the number of causes dysphagia, which may affect the quality of life
new HNC diagnoses was approximately 700,000 in 2005, (QOL) or lead to a poor prognosis [2, 3]. Patients with ad-
more than 900,000 new patients were diagnosed with HNC vanced HNC, especially oral cancer or oropharyngeal cancer,
in 2015 [1]. Since the head and neck region contains important and a high risk of recurrence sometimes require surgery plus
adjuvant postoperative radiotherapy (PORT) or CRT to im-
prove survival rate [4]. However, surgery and PORT may
* Nao Hashida result in poor swallowing function, including aspiration, oral
hashida1223@gmail.com and pharyngeal residue, chewing dysfunction, and a high risk
of developing malnutrition [5–7]. Swallowing dysfunction af-
1
Department of Rehabilitation, Osaka International Cancer Institute, ter surgery and PORT may necessitate diet modification or
3-1-69, Otemae, Chuo-ku, Osaka City 541-8567, Japan restriction of food intake, leading to poor QOL [8].
2
Department of Head and Neck Surgery, Osaka International Cancer Rehabilitation treatment for patients with swallowing dys-
Institute, Osaka City, Japan function after HNC treatment is often provided by a multi-
Support Care Cancer

disciplinary team including speech-language pathologists used to provide an opportunity for patients to withdraw from
(SLPs) [2]. Treatment of dysphagia includes nutritional as- the study. General consent regarding the possibility of using
sessment and management, assessment and recommendation their clinical data was obtained from all patients at the time of
of appropriate food preparation techniques, and assessment of operation.
the risk of aspiration as well as therapeutic rehabilitation and
adapted swallowing techniques [3, 9]. Recent reports have Assessments of swallowing outcome
detailed the impact of rehabilitation treatment on dysphagia
caused by RT/CRT [10–12]. However, the effect of rehabili- As the primary outcome, swallowing outcome was assessed
tation treatment for HNC patients during PORT remains using the Functional Oral Intake Scale (FOIS) score, which is
unclear. a seven-point scale comprising level 1 (nothing by mouth),
Therefore, this study aimed to determine whether rehabili- level 2–3 (tube depending), level 4 (total oral intake with a
tation treatment that includes exercises, assessment of dyspha- single consistency), level 5 (total oral diet with multiple con-
gia and nutritional status, nutritional management, and recom- sistencies but requiring special preparation or compensations),
mendations of food texture during PORT is useful for patients level6 (total oral diet with multiple consistencies without spe-
with dysphagia who underwent surgery and PORT for oral or cial preparation, but with specific food limitations), and level
oropharyngeal cancer. 7 (total oral diet with no restrictions) [13]. The FOIS scores
were assessed by a SLP. Although the FOIS score has no
direct correlation with oropharyngeal dysphagia, it reflects
Materials and methods the swallowing outcome of patients who undergo surgery
and PORT for oral or oropharyngeal cancer, which can cause
Patients difficulty with oral transport or mastication [14]. In addition,
among Japanese HNC patients, the FOIS score is correlated
We conducted a retrospective cohort study of patients who with the MD Anderson Dysphagia Inventory, a validated and
underwent surgery and PORT for oral or oropharyngeal can- reliable self-completion questionnaire for assessing QOL in-
cer in the Department of Head and Neck Surgery at Osaka duced by dysphagia in patients with HNC [15, 16]. We
International Cancer Institute between 1 January 2014 and 31 assessed the FOIS score before and 6 months after PORT.
December 2019. Patients were eligible if they were over 20
years old, had completed a full dose (≥50Gy) of PORT, and Swallowing rehabilitation treatment
required tube feeding after surgery. All patients were provided
with rehabilitation treatment by SLPs after surgery for HNC The purpose of the swallowing rehabilitation treatment is to
during hospitalization; some were also provided with rehabil- maintain the range of motion of the oral, pharyngeal, and
itation treatment during adjuvant PORT. We excluded pa- laryngeal structures involved in swallowing and to counteract
tients with a history of dysphagia induced by prior treatment the radiation-induced fibrosis that leads to a restricted range of
for HNC, cerebrovascular disease, and Parkinson’s disease. motion and dysphagia.
Patients who underwent surgeries that do not typically affect Swallowing rehabilitation treatment includes swallowing
swallowing (i.e., neck dissection without primary tumor re- exercises, assessment of dysphagia and nutritional status,
section or endoscopic submucosal dissection), those who management and recommendations of food texture, and en-
underwent total laryngectomy, and those who refused to par- couragement of patients to continue oral intake as much as
ticipate were also excluded from the study. possible. The swallowing exercises consisted of neck and oral
Age, sex, tumor location, tumor size (T stage), lymph node range of motion exercises, lingual resistance exercises, breath-
stage, surgical procedure, dentition (Eichner Index (EI) clas- ing training, the shaker maneuver, and the Mendelsohn ma-
sification A or B/C), radiotherapy procedures (dose, fraction- neuver. The patients were taught the swallowing exercises and
ation, presence of chemotherapy with radiotherapy), treatment the rest of the interventions by SLPs and instructed to perform
plan (three-dimensional conformal radiation therapy, them at home. They were given the swallowing exercises face
intensity-modulated radiotherapy, or volumetric modulated to face at the hospital at least once a week to assist with
arc therapy), and radiation field (unilateral or bilateral irradia- compliance with therapy.
tion, presence of the irradiation to the pharyngeal constrictors
muscles and/or the base of the tongue) were recorded. This Statistics analysis
study was approved by the ethics committee of the Osaka
International Cancer Institute (approval number 20056). The The patients were not randomized owing to the retrospective
committee waived the need for informed consent in view of nature of the study. The rehabilitation and non-rehabilitation
the retrospective nature of the study. Instead, an opt-out tech- groups differed in variables influencing pre-PORT
nique through an announcement on the hospital webpage was swallowing ability, such as tumor size, tumor site, and
Support Care Cancer

swallowing ability. Multivariate linear regression analysis was Discussion


performed and adjusted for age, pre-PORT FOIS score, tumor
site (oral cavity or oropharynx) (model 1), model 1 with ad- This retrospective cohort study included patients who
justment for tumor size (model 2), and model 1 adjusted for underwent surgery and PORT for oral or oropharyngeal can-
the presence of chemotherapy (model 3) was used to assess cer and aimed to determine whether dysphagia rehabilitation
the effect of rehabilitation during PORT for the FOIS score at during PORT leads to better swallowing outcomes. There
6 months post-PORT. were two important findings of this study. First, rehabilitation
We also performed post hoc stratified analysis of the changes treatment for swallowing during PORT is likely to lead to a
in the FOIS score from the values obtained before PORT to those positive swallowing outcome. Second, the swallowing func-
obtained 6 months after PORT using a study group (poor oral tion might improve from the beginning of PORT (after sur-
intake group: FOIS score <5, good oral intake group: FOIS score gery) to 6 months post-PORT.
≥5) to assess whether the impact of rehabilitation varied between The results showed that rehabilitation treatment during
patients with poor and good baseline swallowing ability. PORT may achieve better swallowing outcomes. In patients
Parametric data are presented as mean ± standard deviation, who undergo RT/CRT, dysphagia may occur due to poor
non-parametric data are shown as median and interquartile range retraction of the base of the tongue, poor epiglottic reflection,
(IQR), and categorical data are shown as percentages. Fisher’s reduced laryngeal elevation, delayed pharyngeal transit, and/
exact test and the Mann-Whitney U-test were used to examine or poor coordination of swallowing muscles [18]. In patients
rehabilitation treatment-dependent differences. P values of less who undergo surgery plus PORT, PORT has an additional
than 0.05 were considered statistically significant. negative impact on swallowing function by increasing fibrosis
All statistical analyses were performed using EZR (Saitama of the irradiated head and neck tissues as well as surgical
Medical Center, Jichi Medical University, Saitama, Japan), a influence [19]. On the other hand, in a randomized clinical
graphical user interface for R (The R Foundation for Statistical trial, swallowing exercises during CRT for HNC affect
Computing, Vienna, Austria) [17]. More precisely, it is a mod- swallowing ability and muscle maintenance [10]. In addition,
ified version of R Commander that was designed to add sta- in patients who underwent surgery plus adjuvant RT/CRT,
tistical functions frequently used in biostatistics. swallowing exercises may have enabled the ingestion of solid
foods compared with the control group [20]. In a study using
both videofluorography and fiberoptic endoscopic evaluation
Results of swallowing, patients had worse penetration aspiration
scores and pharyngeal residue scores in solid bolus
A total of 92 patients with oral or oropharyngeal cancer met swallowing after RT for HNC. This may be due to a reduction
the inclusion criteria in this study. Of the 92 patients, 37 were in the posterior movement of the tongue and pharyngeal con-
excluded from the study because of death, recurrence, or loss traction [21]. Therefore, swallowing exercises during PORT
to follow-up (Fig. 1). may contribute to preventing swallowing impairment. The
Table 1 compares the patient characteristics between the mechanism underlying the impact of swallowing exercise on
groups. The mean patient age was 61 ± 11 and 61 ± 14 years, swallowing function remains elusive. However, there are
male patients were 18 and 18, while the median pre-PORT FOIS some reports on the effect of swallowing exercise on
score was 5 (5–6) and 4 (3–5) in the non-rehabilitation and re- swallowing function in patients who received CRT [22].
habilitation groups, respectively. All patients were Asian. Carroll et al. reported that in patients who received CRT for
The median FOIS score at 6 months post-PORT was 6 (5– HNC, swallowing exercise improved the tongue base to pos-
6) and 6 (4–7) in the non-rehabilitation and rehabilitation terior pharyngeal wall approximation and led to better epiglot-
groups, respectively. Table 2 shows the results of the multi- tic inversion while Carnaby-Mann et al. reported that the
variate linear regression of the FOIS score at 6 months post- swallowing exercise called pharyngocise contributed to
PORT. In the three models, the rehabilitation group was an preventing swallowing muscle atrophy [10, 22]. Moreover,
independent positive factor for FOIS score at 6 months after the effect of oral exercise on dry mouth was reported [23].
PORT (model 1: coefficient, 0.56, 95% confidence interval Since dry mouth has a negative impact on swallowing func-
(CI), 0.02 to 1.10, P = 0.042; model 2: coefficient, 0.54, tion after RT, swallowing exercise may contribute to dry
95% CI, 0.01 to 1.07, P = 0.048; model 3: coefficient, 0.56, mouth and swallowing function. Therefore, rehabilitation
95% CI, 0.02 to 1.11, P = 0.042). treatment including swallowing exercises during PORT is
Table 3 shows the results of the stratified analysis of the likely to have a positive impact on swallowing ability.
changes in the FOIS score. In the good oral intake group, there The post hoc stratified analysis showed a significant differ-
was a significant difference between the rehabilitation and ence between the rehabilitation and non-rehabilitation sub-
non-rehabilitation groups. However, there was no significant groups in the good oral intake group; however, there was no
difference in the poor oral intake group. significant difference in the poor oral intake group. There was
Support Care Cancer

Fig. 1 Flowchart of the cohort

a possibility that compared with those with good pre-PORT rehabilitation treatment included the assessment of dysphagia
swallowing function, patients with worse pre-PORT and nutritional status, food texture management and recommen-
swallowing function tended to undergo surgery that was more dations, and swallowing exercises. Poor swallowing ability
likely to affect swallowing function. Patients who undergo resulting from RT/CRT-induced malnutrition requires rehabilita-
wide resection of oral or oropharyngeal cancer have a high tion and nutritional management [7, 18, 27]. In addition, eating
risk of chewing or transportation of bolus, which causes lim- orally as much as possible during RT/CRT for HNC benefits
ited food texture and a low FOIS score [2, 6]. Therefore, the patients’ swallowing function owing to the continuous use of
impact of rehabilitation during PORT may be smaller in the the swallowing musculature [25, 28]. There is also a report that
poor oral intake group than in the good oral intake group. In recommended swallowing of maximal tolerated volumes as a
contrast, most patients in the good oral intake group swallowing exercise during PORT [26]. Dysphagia after PORT
underwent rehabilitation, but most patients in the poor oral was attributed to various factors including prior surgery,
intake group did not undergo rehabilitation and the pre- swallowing musculature fibrosis, and malnutrition. Although
PORT FOIS score was 5 (5–6) and 4 (3–5) in the non- continuing swallowing exercises for pain may be difficult, a
rehabilitation and rehabilitation groups, respectively. One comprehensive approach may help prevent poor swallowing
possible explanation is that patients with a poor oral intake function.
ability might have had more hope of rehabilitation. This result The results also suggested that the swallowing outcome
shows that rehabilitation treatment is needed for better assessed by the FOIS score improved after cancer treatment,
swallowing function after PORT despite a good pre-PORT including surgery and PORT. It is well known that RT/CRT
swallowing function. may worsen swallowing function [2]. However, the
Comprehensive intervention, which includes early swallowing outcomes evaluated by the FOIS score were better
swallowing exercise during PORT as well as nutritional manage- at 6 months post-PORT (6 [5–6] and 6 [4–7]) in the non-
ment and food recommendation, was likely to have a positive rehabilitation and rehabilitation groups, respectively than at
impact on the swallowing ability. Within 4 to 5 weeks of starting pre-PORT (5 [5–6] and 4 [3–5]) in the non-rehabilitation
RT, patients suffer from mucositis, pain, copious mucous pro- and rehabilitation groups, respectively. PORT is reportedly a
duction, xerostomia, and edema of the soft tissues, which may factor of poor swallowing function at 1 year after treatment,
cause aspiration, malnutrition, and feeding tube dependency and patients who received PORT demonstrated only slight
[11]. Side effects, especially pain, make it difficult for patients swallowing improvements [29, 30]. On the other hand,
to perform swallowing exercises [24]. As such, starting rehabil- Lazarus et al. reported that, in patients with oral or oropharyn-
itation treatment early during PORT when patients do not have geal cancer, the swallowing function and tongue strength were
pain is likely to lead to superior base of the tongue retraction, reduced after CRT but improved at 6 and 12 months after
epiglottic inversion, and muscle maintenance resulting in im- CRT [31]. In the present study, swallowing ability was im-
proved swallowing function [25, 26]. Moreover, our proved in patients who had dysphagia due to surgery and/or
Support Care Cancer

Table 1 Patients’ characteristics

Non-rehabilitation Rehabilitation
(n = 30) (n = 25)

Male 18 (60.0) 18 (72.0)


Female 12 (40.0) 7 (28.0)
Age (mean ± SD) 61.3 ± 11.4 61.9 ± 13.9
Primary site
Oral cavity 23 (76.7) 20 (84.0)
Tongue 13 (43.3) 15 (60.0)
Lower gingiva 4 (13.3) 1 ( 4.0)
Floor of mouth 2 ( 6.7) 1 ( 4.0)
Buccal mucosa 3 (10.0) 2 ( 8.0)
Retromolar trigone 1 ( 3.3) 1 ( 4.0)
Oropharynx 7 (23.3) 5 (20.0)
Tonsil 2 ( 6.7) 4 (16.0)
Base of the tongue 1 ( 3.3) 0 ( 0.0)
Others 4 (13.3) 1 ( 4.0)
T stage
T1 1 ( 3.3) 0 ( 0.0)
T2 13 (43.3) 6 (24.0)
T3 4 (13.3) 10 (40.0)
T4 12 (40.0) 9 (36.0)
N stage
N0 11 (36.7) 2 ( 8.0)
N1 3 (10.0) 0 ( 0.0)
N2 15 (50.0) 18 (72.0)
N3 1 ( 3.3) 5 (20.0)
Surgery
Oral cavity resection without reconstruction 1 ( 3.3) 1 ( 4.0)
Partial glossectomy 0 (0.0) 1 ( 4.0)
Others 1 ( 3.3) 0 (0.0)
Oral cavity resection with reconstruction 17 (56.7) 17 (68.0)
Partial glossectomy 1 ( 3.3) 0 ( 0.0)
Hemiglossectomy 5 (16.7) 7 (28.0)
Subtotal glossectomy 6 (20.0) 7 (28.0)
Total glossectomy 1 ( 3.3) 1 ( 4.0)
Others 4 (13.3) 2 ( 8.0)
Segmental mandibulectomy with reconstruction 3 (10.0) 1 ( 4.0)
Segmental mandibulectomy without reconstruction 2 ( 6.7) 1 ( 4.0)
Oropharynx resection without reconstruction 1 ( 3.3) 0 ( 0.0)
Oropharynx resection with reconstruction 6 (20.0) 5 (20.0)
Tonsilectomy 2 ( 6.7) 4 (16.0)
Others 4 (13.3) 1 ( 4.0)
Eichner Index
A 15 (50.0) 10 (40.0)
B/C 15 (50.0) 15 (60.0)
PORT procedures
Dose (median [IQR]) 66 [59.4, 66] 66 [66, 66]
Fractionation 33 33
Presence of chemotherapy
Radiotherapy alone 14 (46.7) 11 (44.0)
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Table 1 (continued)

Non-rehabilitation Rehabilitation
(n = 30) (n = 25)

Chemo-radio therapy 16 (53.3) 14 (56.0)


Treatment plan
VMAT 30 (100.0) 25 (100.0)
Radiation field
Pharyngeal constrictors muscles and/or base of the tongue 18 (60.0) 21 (84.0)
Unilateral irradiation 21 (70.0) 15 (60.0)
Bilateral irradiation 9 (30.0) 10 (40.0)
FOIS before PORT (median [IQR]) 5.00 [5.00, 6.00] 4.00 [3.00, 5.00]

SD, standard deviation; IQR, interquartile range; VMAT, volumetric modulated arc therapy; FOIS, Functional Oral Intake Scale; PORT, post-operative
radiotherapy

PORT. Therefore, the swallowing outcome is likely to be addition, more effective medicines for HNC have been devel-
improved, and this finding is useful for predicting the oped, which are expected to improve prognosis. Thus, im-
swallowing ability of patients who require surgery plus adju- proving the swallowing ability is important for survival and
vant RT/CRT. In addition, FOIS is one of the most common QOL. In addition, as our intervention method does not always
scales and is sensitive to changes in functional oral intake and require a face-to-face session, we believe it is feasible.
is associated with patients’ QOL [8, 32]. Consequently, reha- This study has several limitations. First, although our insti-
bilitation treatment during PORT may be useful for patients’ tute is among the largest cancer centers treating HNC, a small
QOL as well as for improving swallowing ability. number of patients were included because nearly half of the
Patients with advanced cancer who undergo surgery and patients dropped out for recurrence or death due to advanced
PORT for HNC may live longer after treatment. In this study, HNC. Thus, there are concerns such as insufficient adjustment
among the 92 patients, 55 did not show recurrence. In of background factors in multivariate analysis and the possi-
bility of low statistical power in post hoc stratified analysis.
This is in addition to the inherent limitation of post hoc strat-
Table 2 Multivariable linear regression for FOIS at 6 months follow-up ified analysis. Second, we used the FOIS score as a
swallowing outcome, but it does not directly assess dysphagia,
Coefficients (Β) 95 % CI P value unlike videofluorography [33]. However, we believe that the
FOIS score is useful for evaluating swallowing ability and
Model 1
swallowing-related QOL. Third, since our rehabilitation ses-
Age −0.02 −0.04 to 0.01 0.146
sions were not always face-to-face, we did not have correct
FOIS before PORT 0.78 0.57 to 0.99 < 0.001
information about patient compliance to the swallowing exer-
Primary Site (Oral cavity) −0.32 −0.99 to 0.36 0.351
cises. In a Cochrane review, low compliance to swallowing
Rehabilitation 0.56 0.02 to 1.10 0.042
therapy was reported to be due to pain following RT [24].
Model 2
Considering low compliance after week four or five, our re-
Age −0.02 −0.04 to 0.01 0.122
habilitation program included other interventions in addition
FOIS before PORT 0.73 0.51 to 0.95 < 0.001
Primary Site (Oral cavity) −0.17 −0.88 to 0.53 0.627
Rehabilitation 0.54 0.01 to 1.07 0.048 Table 3 Stratified analysis of FOIS score’s changes from pre-PORT to
T stage −0.20 −0.49 to 0.08 0.157 PORT between with rehabilitation and without rehabilitation
Model 3
n Mean ± SD P value
Age −0.02 −0.04 to 0.01 0.187
FOIS before PORT 0.79 0.58 to 1.00 < 0.001 FOIS<5 Rehabilitation 16 1.25 ± 1.18 0.304
Primary Site (Oral cavity) −0.33 −1.02 to 0.36 0.342 Non rehabilitation 7 0.71 ± 0.95
Rehabilitation 0.56 0.02 to 1.11 0.042 FOIS≧5 Rehabilitation 9 1.00 ± 0.70 0.006
CRT 0.13 −0.35 to 0.62 0.587 Non rehabilitation 23 0.21 ± 0.67

FOIS, Functional Oral Intake Scale; PORT, post-operative radiotherapy; FOIS, Functional Oral Intake Scale; n, number of patients; SD, standard
CRT, chemoradiotherapy deviation
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N.A., H.T., and T.F. approved the version to be published and agreed to struction: a prospective, observational study. Surg Oncol 27(3):
be accountable for all aspects of the work in ensuring that questions 490–494
related to the accuracy or integrity of any part of the work are appropri- 7. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H,
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