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Dysphagia (2010) 25:139152

DOI 10.1007/s00455-009-9247-7

REVIEW ARTICLE

Dysphagia in Head and Neck Cancer Patients


Treated with Chemoradiotherapy
Nele Platteaux Piet Dirix Eddy Dejaeger
Sandra Nuyts

Received: 22 April 2009 / Accepted: 31 July 2009 / Published online: 27 August 2009
Springer Science+Business Media, LLC 2009

Abstract Dysphagia is a very common complaint of head


and neck cancer patients and can exist before, during, and
after chemoradiotherapy. It leads to nutritional deficiency,
weight loss, and prolonged unnatural feeding and also has
a major potential risk for aspiration. This has a significant
negative impact on the patients entire quality of life.
Because treatment of dysphagia in this setting is rarely
effective, prevention is paramount. Several strategies have
been developed to reduce dysphagia. These include swallowing exercises, treatment modification techniques such
as intensity-modulated radiotherapy, selective delineation
of elective nodes, reducing xerostomia by parotid-sparing
radiotherapy, and adding of radioprotectors. However,
more research is needed to further decrease the incidence
of dysphagia and improve quality of life.

Department of Geriatrics, Leuven Cancer Institute, University


Hospitals Leuven, Campus Gasthuisberg, Leuven, Belgium

Keywords Radiotherapy Head and neck cancer


Dysphagia Intensity-modulated radiotherapy
Deglutition Deglutition disorders

Introduction
Head and neck cancer (HNC) is the sixth most common
malignancy worldwide, representing about 6% of all
tumors and accounting for an estimated 650,000 new
cases and

N. Platteaux (&) P. Dirix S. Nuyts


Department of Radiation Oncology, Leuven Cancer Institute,
University Hospitals Leuven, Campus Gasthuisberg, Herestraat
49, 3000 Leuven, Belgium
e-mail: nele.platteaux@uz.kuleuven.ac.be
E. Dejaeger

1
3

350,000 deaths every year [1]. Radiotherapy (RT) and


surgery are the main treatment modalities, although there
is an increasing role for chemotherapy. The choice of
modality depends on patient factors, primary site, clinical
stage, and resectability of the tumor. Approximately 3040% of patients present with early-stage disease, which is
treated by surgery or primary radiotherapy. Around 60%
of patients are diagnosed with a locally advanced stage,
which is associated with a poor prognosis [1]. Standard
treatment for locally advanced HNC has been surgery
followed by postoperative RT. Several trials focusing on
organ preser- vation showed a similar outcome for these
patients using chemoradiotherapy (CRT) [24].
Therefore,
concurrent
radiation
therapy
with
chemotherapy is nowadays accepted as an organpreserving approach [47].
Primary radiotherapy for HNC is conventionally given
to a total dose of 70 Gy in once daily fractions of 2 Gy, 5

1
3

fractions a week, over 7 weeks [1]. Altered (hyperfractionation and/or acceleration) fractionation schedules and the
use of concomitant chemotherapy have both been tested
and proven to improve locoregional control and overall
survival [511]. However, these intensified schedules come
at the cost of more acute and chronic side effects [1, 6, 7,
9]. The most common acute side effects of CRT for HNC
are mu- cositis, pain, dermatitis, xerostomia, loss of taste,
hoarse- ness, weight loss, myelosuppression, nausea, and
dysphagia. The most frequent late side effects are
xerostomia, loss of taste, fibrosis, trismus, and dysphagia.
Dysphagia is a common, multifactorial, and potentially
life-threatening side effect of CRT, with a potential for
aspiration and death due to aspiration pneumonia [1214].
It also results in nutritional deficiency leading to weight
loss and the need for prolonged feeding by a percutaneous
endoscopic gastrostomy (PEG) tube. This has a significant
negative impact on the global quality of life (QOL) of

14
0

N. Platteaux et al.: Dysphagia in Chemoradiotherapy Patients

potentially cured patients, causing anxiety and depression


[13, 15]. This article focuses on the incidence of dysphagia
in HNC patients treated with CRT and provides an overview of methods to prevent this important side effect.

Physiology
of
Pathophysiology

Swallowing

and

Normal swallowing is a complex process in which a large


number of cranial nerves and muscles are involved in
carrying food from the mouth through the pharynx into the
esophagus and stomach. Swallowing consists of three
phases [oral (oral preparatory), pharyngeal, and esophageal], with the voluntary oral preparatory and oral phases
followed by an involuntary reflex that must be triggered.
This process implies a rapid and precise coordination
between sensory input and motor function [1618].
Swallowing involves controlling the food in the mouth,
largely with the oral part of the tongue, to enable tasting
and chewing to occur. The oral tongue moves the food onto
the teeth to crush the food, collects the food from around
the mouth after chewing, brings it together to form a bolus,
and propels it backward out of the mouth. Thereafter, the
pha- ryngeal stage of swallowing is triggered and a number
of necessary motor activities occur: (1) hyoid movement,
(2) closure of the entrance to the nose, the velopharyngeal
port, by elevation of the soft palate to prevent food from
entering the nose, (3) closure of the airway to prevent food
from entering the lungs, (4) opening of the upper
esophageal sphincter by relaxation of the cricopharyngeal
muscles and by movement of the larynx anteriorly and
superiorly to enable the bolus to pass into the esophagus,
(5) epiglottic inversion, and (6) pharyngeal contraction to
push the food through the pharynx and the esophagus. All
these actions occur in the pharynx within 1 s and must be
appropriately coordinated for the swallow to be safe and
efficient [17, 18].
Pathophysiology of Swallowing Disorders
Post-RT swallowing disorders are due to primarily neuromuscular fibrosis and radiation-induced edema [19, 20].
RT induces hyperactivation through hydroxyl radicals of
trans- forming growth factor-b1 (TGF-b1) which plays a
role in collagen deposition and degradation. This leads to
fibrosis and the resulting abnormal motility of deglutition
muscles as impaired pharyngeal contraction and laryngeal
elevation responsible for dysphagia, aspiration, and
stenosis [21]. Second, sensory changes in the oral cavity
and the pharynx also play a role in post-RT swallowing
disorders by changing the patients perception of
swallowing [17, 22]. There are hypotheses that CRT can

have an effect on innervation of the larynx and pharynx,


causing loss of laryngeal sensation, motor function, and
normal peristalsis [18]. Obviously,

N. Platteaux et al.: Dysphagia in Chemoradiotherapy Patients

xerostomia after RT due to the inclusion of salivary


glands in the radiation field contributes to swallowing
problems. Xerostomia is associated with difficulties in
mastication and delayed initiation of the swallowing
reflex because of decreased bolus lubrication due to the
lack of saliva [17]. It also negatively affects the patients
overall perception of swallowing quality and comfort of
eating [19, 22].

Incidence of Dysphagia
Pretreatment Dysphagia and Aspiration Rate (Table 1)
Dysphagia can exist before treatment as a result of the
extent of the tumor which can involve the motility of
structures that contribute to swallowing. Dysphagia rate
and severity therefore depend on tumor stage and localization, with the most severe complaints in more advanced
locoregional stages [23]. Laryngeal and hypopharyngeal
cancer patients aspirate most frequently before treatment
which is reflected by the high degree of pharyngeal and
esophageal impairment [2426].
Post-Treatment Dysphagia (Table 2)

14
1

The severity of post-RT swallowing disorders is dependent


on several factors: total radiation dose, fraction size, fractionation schedule, target volumes, interfraction interval,
treatment techniques such as the use of intensitymodulated radiotherapy treatment (IMRT), addition of
concurrent chemotherapy, smoking during and after RT,
PEG tube feeding or prolonged ([12 weeks) nil per os,
depression, and poor mental health [17, 2730]. The metaanalysis of Machtay et al. [29] showed that older age,
advanced tumor stage, larynx/hypopharynx primary site,
and neck dissection after concurrent CRT are the main risk
factors for severe late toxicity. An average rate of 50%
dysphagia in advanced-stage HNC after CRT is reported
[31]. However, it should be noted that the incidence of
dysphagia is perhaps underreported in trials because
clinical judgment often underestimates the severity [32].
Little is known about the evolution of swallowing
problems after CRT, but dysphagia and aspiration can
begin or significantly worsen years after treatment. This is
prob- ably due to submucosal effects such as fibrosis and
vascular and nerve (sensory and motor) injury [19].
Nguyen et al. [32] reported that the severity of dysphagia
decreased in 32%, remained unchanged in 48%, and
worsened in 20% of their patients 1 year or more following
HNC treatment. Goguen et al. [33] described dysphagia as
slowly but only partly resolving after 612 months
following CRT for advanced HNC. In another study on
nasopharyngeal cancer

Table 1

Overview from literature of pretreatment dysphagia

Tumor stage/site

No. of
patients (N)

% Dysphagia

T2 or more, oral,
pharyngeal, and
laryngeal cancer
Stage IIIIV, HNC

352

Oral: 28.2%, pharyngeal:


50.9%, laryngeal: 28.6%

Stage IIIV, HNC


Stage IV, HNC
Stage IIIIV, HNC
Stage IIIIV, oropharyngeal,
nasopharyngeal cancer
All tumor stages/sites

% Aspiration

79

Refs.
Pauloski et al. [25]

Stenson et al. [26]

63
22
27

Oral cavity: 14%, oropharyngeal:


30%, laryngeal: 67%,
hypopharyngeal: 80% VFS
17% MBS
14% VFS
41% VFS (45% silent55% overt)

36

8% VFS

Feng et al. [78]

236

Grade 37: T1T2: 20%,


T3T4: 31%, oral cavity:
5%, laryngeal: 29%,
oropharyngeal: 33%,
hypopharyngeal: 52% VFS

Nguyen et al. [14]


Eisbruch et al. [12]
Rosen et al. [83]

Nguyen et al. [23]

HNC head and neck cancer, VFS videofluoroscopy, MBS modified barium swallow

Table 2

Overview from literature of post-treatment dysphagia

Tumor stage/site

Therapy

Stage IIIV, HNC

CRT

63

Locally advanced HNC

CRT

55

Stage IV, HNC

CRT

20

Stage IIIIV, oropharyngeal,


nasopharyngeal cancer

CRT

36

All stages, oropharyngeal cancer


Stage IIIIV, oral cavity, oropharynx,
hypopharynx

(C)RT
CRT

81
10

Nasopharyngeal cancer

RT

31

% Dysphagia

45% severe
39% grade 45

% Aspiration

Refs.

59% overall/ 33%


MBS

Nguyen et al. [14]

36% grade 67
MBS

Nguyen et al. [21]

65% early (13 months)


62% late (612 months)

Eisbruch et al. [12]

VFS
44% early

Feng et al. [77, 78]

8% strictures
VFS
23% grade 34
13% early

Levendag et al. [68]


Smith et al. [19]

VFS
41.9% silent

Wu et al. [84]

FEES
HNC head and neck cancer, VFS, videofluoroscopy, MBS modified barium swallow, FEES functional endoscopic evaluation of swallowing,
(C)RT (chemo)radiotherapy, RT radiotherapy

patients treated with RT, a continuous deterioration of


swallowing function over time was seen [34] (Table 3).

Measuring and Reporting Dysphagia


Subjective Scoring
Several scoring systems are available to measure and
report dysphagia.

Patient-reported dysphagia can be assessed by qualityof-life (QOL) questionnaires like the European Organization for Research and Treatment of Cancer (EORTC)
global Q30 and Head and Neck (H&N35) [31, 35]. The
latter is a specific questionnaire for HNC patients and
scores xerostomia, swallowing, and eating [35, 36]. Two
other commonly used questionnaires for subjective
assessment are the Performance Status Scale for HNC
patients (PSS-H&N) and the MD Anderson Dysphagia
Inventory (MDADI). The PSS is a rapid, clinician-rated

Table 3

Overview from literature of chronic dysphagia

Tumor stage/site

Therapy

All stages and tumor sites

CRT/surgery RT

Locally advanced HNC

% Aspiration

Refs.

74

49%
MBS

Nguyen et al. [85]

CRT/surgery RT

25

32%
VFS

Nguyen et al. [32]

Stage IIIIV, oral cavity,


oropharynx, hypopharynx cancer

CRT

10

30%
VFS

Smith et al. [19]

Locally advanced HNC

Induction
chemotherapy ? CRT

Nasopharyngeal cancer

RT

49

22% silent
VFS

Hughes et al. [86]

Nasopharyngeal cancer

RT

71

71.8%
VFS

Chang et al. [34]

122

% Dysphagia

38.5% severe
MBS

Caudell et al. [27]

HNC head and neck cancer, VFS videofluoroscopy, MBS modified barium swallow, (C)RT, (chemo)radiotherapy, RT radiotherapy

instrument consisting of three subscales: normalcy of diet,


public eating, and understandability of speech. Ratings
range from 0 to 100, with higher scores representing
closer- to-normal functioning [37, 38]. The MDADI is a
validated, dysphagia-specific QOL instrument and consists
of 20 questions with global, emotional, functional, and
physical subscales. It is patient-friendly and easy to
understand and complete by patients [39, 40]. Another
cancer-specific QOL instrument reported in literature is the
Functional Assessment of Cancer Therapy for head and
neck (FACT- G& H&N). This questionnaire is completed
by the patient and yields a global QOL score (FACT-G:
range 0120 points) comprising six subscales: physical,
social, rela- tionship with doctor, emotional and functional
well-being, and H&N concerns [37, 38, 41].
Observer-based dysphagia can be assessed by recording
acute toxicity during the first 3 months after RT using
Common Terminology Criteria for Adverse Events
(CTCAE) [42] and by recording late toxicity using the
Radiation Therapy Oncology Group (RTOG)/ EORTC
Late Radiation Morbidity Scale [43, 44].
Objective Scoring
For objective assessment of swallowing function a videofluoroscopy [VF; often known as modified barium swallow
(MBS)] can be performed (Fig. 1). It is a validated standard method, developed by Logemann, that allows viewing
and recording of the structures and dynamics of the swallowing process [45, 46]. The whole assessment focuses on
bolus manipulation, bolus control, and bolus passage
including cohesion, motility, and timing [12, 17]. The
findings of each patient are scored using the Swallowing
Performance Scale (SPS) (Table 4). This is a validated and
accurate assessment of dysphagia severity by
combining

Fig. 1 Normal swallowing function on videofluoroscopy

clinical and radiographic information. The severity of


dysphagia is graded on a scale of 17 [12, 14, 17].
Pathological Features Seen on Videofluoroscopy
Abnormal swallowing can be defined in terms of the
amount and incidence of aspiration and
penetration,
Table 4 The Swallowing Performance Scale (SPS)
Grade 1: normal
Grade 2: within functional limitsabnormal oral or pharyngeal stage
but able to eat a regular diet without modifications or swallowing
precautions
Grade 3: mild impairmentmild dysfunction in oral or pharyngeal
stage; requires a modified diet without need for therapeutic
swallowing precautions
Grade 4: mild-to-moderate impairment with need for therapeutic
precautionsmild dysfunction in oral or pharyngeal stage; requires
a modified diet and therapeutic precautions to minimize aspiration
risk
Grade 5: moderate impairmentmoderate dysfunction in oral or
pharyngeal stage, aspiration noted on exam; requires a modified
diet and swallowing precautions to minimize aspiration risk
Grade 6: moderate-severe dysfunctionmoderate dysfunction of oral
or pharyngeal stage, aspiration noted on exam; requires a modified
diet and swallowing precautions to minimize aspiration risk; needs
supplemental enteral feeding support
Grade 7: severe impairmentsevere dysfunction with significant
aspiration or inadequate oropharyngeal transit to esophagus,
nothing by mouth; requires primary enteral feeding support

laryngeal sensation (response to penetrant/aspirate), and


residue/pooling after the swallow [12]. Also, abnormal
timing or duration of each swallowing phase can be evaluated as beyond the range found in normal controls [12,
17, 25]. The most frequently found VF abnormalities after
CRT are (1) reduced inversion of the epiglottis, (2) reduced
laryngeal elevation and closure resulting in poor airway
protection and promoting penetration and aspiration, (3)
reduced base-of-tongue retraction resulting in reduced
tongue base contact with the posterior pharyngeal wall, (4)
delay in triggering the pharyngeal swallow, (5) pharyngeal
hypocontractility, (6) incomplete relaxation of cricopharyngeal muscles leading to reduced cricopharyngeal
opening which results in pooling of residue in the piriform
sinuses and valleculae [12, 17, 24, 47] (Fig. 2).
VF can ideally be combined with manometry (manofluoroscopy), first developed by Mc Connel [48].
Manometry involves measurement of the pressures in the
pharynx, upper esophageal sphincter, and esophagus. It is
most often used to look at the relaxation and the contrac-

tion of the esophageal musculature. Ideally, it can be performed by using a solid-state catheter. Manofluoroscopy
permits correlation of motion of anatomic structures with the
resulting intraluminal pressures [49].
A second objective tool to evaluate swallowing dysfunction is functional endoscopic evaluation of swallowing
(FEES), first described by Langmore [50]. It visualizes the
pharynx from above by placing an endoscopic tube, without anesthesia, transnasally such that the end of the tube
hangs over the end of the soft palate. The anatomy and
function of the soft palate, tongue base, pharynx, and

Fig. 2 Aspiration and pharyngeal hypocontraction on videofluoroscopy

larynx are assessed during speech, spontaneous movements, dry swallowing, and swallowing of various consistencies of liquid and food. Sensitivity of the pharynx is
assessed by light touch with the tip of the endoscope.
Premature leakage of food or fluid from the mouth into the
pharynx before a voluntary swallow can be assessed.
Residue in vallecula epiglottica, aryepiglottic region, and
piriform sinus can be assessed together with laryngeal
penetration and aspiration. The patients reaction to residues or aspiration can be noted [51]. FEES can be combined with sensory testing (FEESST). The sensory-testing
procedure includes air pulse stimuli delivered to the
mucosa innervated by the superior laryngeal nerve through
a port in the flexible endoscope [52].
When MBS and FEES are compared, the principal
advantage of the FEES seems to lie in the detection of
aspiration and for MBS in the dynamic evaluation of the
oral and esophageal phases of swallowing. FEES is easier
and it can be performed bedside without radiation exposure
using portable equipment. It also can frequently be repeated and is more cost-effective than VF [53, 54]. Disadvantages of FEES are that it provides only indirect
information about oral cavity function, the moment of
swallowing itself, and esophageal disease and that it is
more observer dependent [50]. Thus, FEES is often used as
an adjunct to MBS rather than an alternative [55].

Third, direct endoscopy under anesthesia can be used to


visualize strictures in the inferior pharyngeal muscles at
the postcricoid level of the hypopharynx [56].
Finally, CT scans can be used to evaluate the thickness
of several swallowing structures like the pharyngeal constrictor muscles, the supraglottic larynx, and the glottic
larynx, which is usually increased after RT [56].
Correlation Between Subjective and Objective Scoring
There is considerable discrepancy in the literature concerning the correlation between objective and subjective
swallowing evaluation. For instance, from a study of 132
HNC patients, Pauloski et al. [57] reported excellent correlation between patients perception of dysphagia and
their actual swallowing function measured with VF.
Patients with complaints of dysphagia had lower
oropharyngeal swallow efficiency, longer oral and
pharyngeal transit times, more oral and pharyngeal residue,
more aspiration, took less nutrition by mouth, and were
less able to eat all food consistencies. It appears that
pharyngeal function has a greater impact on swallowing
perception than oral function. In contrast, from a study of
116 HNC patients, Jensen et al. [58] found little correlation
between patient-assessed symptom severity and observerbased toxicity scoring. The observer-based rating of side
effects underestimated the patient-scored side effects using
QOL questionnaires.

Impact on Quality of Life


Swallowing dysfunction has a clear negative impact on the
global QOL of HNC patients. Dysphagia leads to longer
eating times, inability to eat different types of food, and
fear or inability to eat in public, which in turn results in
social isolation and depression [13]. Obviously, prolonged
unnat- ural feeding may induce major psychological
distress because it causes discomfort and distorts the
patients self- image [13]. Nguyen et al. [13] showed that
the severity of dysphagia correlates with a compromised
QOL, anxiety, and depression. Murry et al. [59] described
that swallowing and QOL are often compromised in
advanced HNC before

Table 5

treatment, they further decrease during CRT, and they


begin to improve shortly after treatment with a marked
improve- ment 6 months after treatment. They also showed
that QOL generally follows a two-stage recovery: first the
psycho- logical aspects improve, followed by the physical
aspects associated with swallowing [59]. The best predictor
of 12- month global QOL seems to be the pretreatment
global QOL [38, 60]. Langendijk et al. [15] also described
that the effect of late radiation-induced toxicity,
particularly on swallow- ing function and salivary gland
function, has a significant impact on the more general
dimensions of health-related (HR) QOL, such as physical,
social, and mental health. They further described that the
impact of radiation-induced swallowing dysfunction is
greatest in the first 12 months after completion of RT and
gradually decreases at 18 and 24 months [15]. Abendstein
et al. [61] evaluated long-term QOL 5 years after treatment
and noted an improvement in global HRQOL in 40%,
deterioration in 25%, and no change in 35% of patients.
Dysphagia also leads to prolonged tube feeding
dependence as described above. Time dependence for tube
feeding ranges in the literature from 4 to 21 months with a
median of 9 months [6, 21].

Treatment of Swallowing Disturbances


Management of swallowing disorders resulting from HNC
treatment includes both compensatory treatment
procedures and specific rehabilitation programs.
Obviously, a truly multidisciplinary team approach is
needed, consisting of the treating oncologist, a speechlanguage pathologist, a dieti- cian, and sometimes a
gastroenterologist for dilatation [17].
Compensatory Treatment Procedures
The purpose of the compensatory treatment procedure is to
improve bolus flow and reduce aspiration. These
procedures should be introduced during MBS to evaluate
the immediate results. The following compensatory
treatment procedures are generally used: postural
techniques, increasing sensory input prior to or during the
swallow, modification of bolus size/volume and
consistency of food, and deletion of

Overview from literature of the results of swallowing therapy

Tumor stage/site

Therapy

Treatment

Results

Refs.

Locally advanced HNC

CRT (n = 24)
Postoperative
RT (n = 17)

41

Swallowing therapy
for aspiration

32% improvement dysphagia


36% improvement aspiration

Nguyen et al. [87]

All stages, oral cavity,


pharyngeal-laryngeal cancer

CRT

HNC head and neck cancer, (C)RT (chemo)radiotherapy

Super-supraglottic
swallow

Elimination (1) reduction


of aspiration (2)

Logemann et al. [88]

Cervical vertebra
Trachea
Upper border of trachea

First 2 cm of esophagus

Cervical vertebra
Subglottic larynx
Upper border of trachea
6.
7.
8.

Upper esophageal
Esophagus
sphincter
Glottic
(UES)
larynx
? (GL)
m.cricopharyngeus

1.
OAR

Radioprotector amifostine (WR2721) is a cytoprotective


agent. It is a thiol compound that protects normal tissues
against radiation through the binding of the sulfhydryl
group with hydroxyl radicals. It has been tested for
mucosal protection and prevention of late dysphagia following RT for HNC with mixed results [69]. In HNC

Anterior tip of the thyroid


Posterior
cartilage
third of the tongue
Cornu of the thyroid cartilage

Widest
rhinopharynx, base of tongue, hyoid
Cervical
bone,
vertebra or prevertebral muscles
Upper
edgediameter
of hyoidofbone

Posterior border
Anterior border
Inferior border

Radioprotectors

Lower edge of hyoid bone Lower edge of cricoid cartilage Upper edge of hyoid bone

As described above, dysphagia has a significant impact on


QOL and prevention of this serious late side effect is of
paramount importance [68]. The three main approaches are
described below.

Caudal tip of pterygoid plates (hamulus)

of Dysphagia

Superior pharyngeal constrictor (SPC) muscles

Prevention

Superior border

In the case of pharyngoesophageal strictures, it is sometimes necessary to perform a pharyngeal and cervical
esophageal dilatation [18]. Ahlawat et al. [67] reported that
endoscopic dilatation of proximal esophageal strictures
gives adequate dysphagia relief in 84% of their treated
HNC patients.

UZ Leuven guidelines to delineate the dysphagia-aspiration-related structures

Dilatation of Strictures

Table 6

specific food consistencies as the last resort [17, 62, 63].


Postural changes (like head positioning) are effective 75
80% of the time in eliminating aspiration of at least one
bolus volume introduced by MBS [17, 62, 63].
Rehabilitation therapy procedures are designed to
improve the range of motion (ROM) of oral and
pharyngeal structures and sensory-motor integration. These
therapy procedures include therapy exercises and swallow
maneu- vers [17, 63]. Therapy exercises are exercises that
strengthen the tongue to increase the oral tongue and tongue base volume and function. There are also ROM exercises that should improve bolus transit and clearance from
the oral cavity and pharynx [17, 63]. So-called Shaker
exercises diminish upper esophageal sphincter (UES)related dysphagia by improving the duration and width of
the UES opening [64, 65]. Swallow maneuvers such as
supraglottic swallow, super-supraglottic swallow, Mendelsohn maneuver, effortful swallow, and tongue hold are
voluntary controls that can be used during swallow to
change selected aspects of neuromuscular control [17, 63,
64].
Logemann et al. [18] suggests that function at 6 months
after treatment predicts long-term function. It is therefore
reasonable to maximize swallowing recovery by 6 months
after CRT. Waters et al. [66] also showed less benefit to
delayed swallowing therapy. A few results from literature
are given in Table 5.

patients treated with concomitant CRT amifostine,


given before each chemotherapy cycle and less than
45 min before RT, less acute nonhematologic (mucositis,

Fig. 3 Delineation of
swallowing structures on CT
slices. (Color figure online)

xerostomia, dysphagia, loss of taste, and dermatitis) and


hematologic side effects and less chronic side effects
like radiation-induced xerostomia are observed [6971].

Table 7

Correlation between subjective and objective swallowing function, QOL, and DVH parameters

Tumor stage/site/therapy

Subjective

All stages, oropharyngeal cancer, RT


(IMRT), chemo
Locally advanced HNC, (CT) IMRT

81

Severe grade 34 dysphagia/


dysphagia QOL
(1) Patient report diet and PEG
tube persistence at 1 year

27

Objective

(2) Weight loss


All stages, oropharyngeal cancer,
(CT) RT (IMRT)
All stages, oropharyngeal,
nasopharyngeal cancer, (CT) RT
(IMRT)

67 (24)
132

Swallowing-related QOL
Swallowing-related QOL

Stage IIIIV, oropharyngeal,


nasopharyngeal cancer, CT IMRT

36

(1) Worsening patient-reported


solid swallowing and
observer-rated swallowing
scores
(4) Worsening patient-reported
liquid swallowing

Advanced stage, pharynx cancer, RT


All stages, nasopharyngeal cancer,
IMRT

35

EORTC QOL

28

Acute grade 3 dysphagia/


feeding tube duration

All stages, HNC, IMRT CT


Locally advanced HNC

96
53

Total FEES score

(1) Aspiration VFS


(2) Strictures
(3) Reduced laryngeal elevation,
epiglottic inversion

FEES variables

Aspiration/stricture MBS
Late dysphagia/QOL

DVH parameters

Refs.

Mean SPC-MPC doses: steep doseeffect relationship


(1) Doses to the aryepiglottic folds,
false vocal cords, lateral pharyngeal
walls
(2) Doses to the aryepiglottic folds

Levendag et al. [66]

Mean SPC dose


SPC dose

Teguh et al. [54]


Teguh et al. [20]

(1) Mean SPC & MPC


doses [ 60 Gy, PC V65 [
50%, GSL V50 [ 50%
(2) PC V70 [ 50%
(3) mean PC dose, mean GSL dose
(4) mean PC dose, mean esophageal
dose,
DVH of supraglottic region

Dornfeld et al. [89]

N.
Pl
att
ea
ux
et
al.
:
D
ys
ph
ag
ia
in
C
he
m
or
ad
iot
he
ra
py

Feng et al. [77, 78]

Jensen et al. [51]

Mean pharyngoesophageal dose

Fua et al. [90]

V50 larynx, V50 IPC


Mean doses and V50 of MPC/IPC/
supraglottic larynx

Caglar et al. [76]


Dirix et al. [91]

HNC head and neck cancer, RT radiotherapy, CT chemotherapy, IMRT intensity-modulated radiotherapy, QOL quality of life, EORTC European Organization for Research and Treatment of
Cancer, PC pharyngeal constrictor muscles (S superior, M middle, I inferior), GSL glottic supraglottic larynx, PEG percutaneous endoscopic gastrostomy, VFS videofluoroscopy, MBS
modified barium swallow, FEES functional endoscopic evaluation of swallowing, DVH dose volume histogram

1
3
147

N. Platteaux et al.: Dysphagia in Chemoradiotherapy Patients


b Fig. 4 Plan of patient with laryngeal cancer cT3N0 treated

15
1
with

IMRT. Delineation of following structures a tongue base (blue),


clinical and planning target volume (CTV and PTV) of elective nodes
(red), superior pharyngeal muscles (light blue), submandibular glands
(yellow, left; orange, right). b Gross tumour volume (GTV) (red),
CTV boost (red) and PTV boost (orange), CTV and PTV of elective
nodes (red), inferior constrictor pharyngeus (green) lying in the high
dose region ([65 Gy). c PTV boost (orange), CTV and PTV
of elective nodes (redred), m. cricopharyngeus (blue) lying in the
high dose region 70 Gy. (Color figure online)

alleviate dysphagia so they should be carefully evaluated


in prospective clinical trials.
Radiation Modifications

However, the risk of tumor cell protection by amifostine is


an issue that needs to be addressed [72]. Currently there is
no good level I evidence to suggest that radioprotectors can

As we know from the literature, there is a relationship


between xerostomia and dysphagia after CRT for HNC
[22]. The reduction of xerostomia by preserving the salivary gland function can possibly decrease dysphagia. This
can be done by using parotid gland-sparing conformal RT
or by using IMRT [73, 74]. IMRT modulates the intensity
of the radiation beam to decrease the doses to normal
structures without compromising the doses to the target. A
parotid gland mean dose of 26 Gy or less should be the
goal in order to spare gland function and reduce
xerostomia and dysphagia [75].
We also know from the literature that dysphagiaaspiration-related structures (DARS), damage to which
causes dysphagia and aspiration, are the superior, middle,
and inferior pharyngeal constrictor muscles (scm, mcm,
icm), cricopharyngeal muscles, esophagus, the glottic larynx, and the supraglottic larynx [56, 68, 76] (Table 6;
Fig. 3). IMRT can be used to reduce the doses to DARS by
applying dose constraints to them in an attempt to decrease
dysphagia [74, 77, 78]. Numerous retrospective studies
show a correlation between either subjective or objective
assessment of dysphagia and dose volume parameters of
anatomic swallowing structures (Table 7). These correlations suggest the reduction of the mean doses and the
volumes of the DARS structures that receive 50 Gy or
more (V50) in an attempt to reduce swallowing difficulties
[51, 68, 7678]. Partial sparing of the pharyngeal constrictors is expected to confer a benefit if primary distal
motor or sensory neural deficits and primary muscle dysfunction play a role in dysphagia [56].
Another way to decrease dysphagia is by more selective
delineation of elective nodal volumes. To spare the parotid
gland we can start to delineate the elective neck nodes of
level II at the contralateral, uninvolved neck on the subdigastric level. We know from the literature that there are no
recurrences in these nodes in selected patients [79]. This
technique leads to a decrease in xerostomia which has an
impact on swallowing. We can also delineate only the

1
3

Table 8

Studies on pretreatment swallowing exercises

Tumor stage/site

Therapy

Exercises

Advanced stage, oropharynx,


hypopharynx, larynx cancer

CRT

18 Mendelsohn maneuver, tongue hold,


tongue resistance, effortful swallow,
Shaker exercises

T2-T4, oropharynx, hypopharynx,


larynx cancer

RT/CRT 37 Pretreatment swallowing exercises

Results

Refs.

Improvement in posttreatment function on VFS

Carroll et al. [64]

Improvement in QOL

Kulbersh et al. [39]

CRT chemoradiotherapy, RT radiotherapy, QOL quality of life, VFS videofluoroscopy

lateral retropharyngeal neck nodes (medial from carotid


artery and lateral to the longus colli and capitis muscles)
while sparing the medial ones. The lateral retropharyngeal
neck nodes are involved mostly in metastasis sites, except
for the posterior pharyngeal wall where the medial nodes
also are involved [7981]. These modifications can facilitate partial sparing of the pharyngeal constrictors and the
upper parts of the glottic and supraglottic regions by using
IMRT [7779, 81].
Not only better definition of the elective nodal volumes
but also reduction of the PTV margins can have an impact
on the doses to the swallowing structures. Nowadays, the
use of online imaging and correction of setup deviations
can lead to a reduction of the PTV margins from 5 to 3 mm
[78].
Knowing the correlation between the doses to swallowing structures and dysphagia and presuming the highest
relapse rates in the therapeutic target volumes, we
hypothesize that we can reduce the doses to the elective
nodal volumes. A Belgian phase III multicenter trial that
randomizes HNC patients to receive 40 or 50 Gy to the
elective nodal volumes is ongoing. This trial aims to
decrease the severity and rate of swallowing disturbances
without compromising locoregional control (Fig. 4). Being
aware that sparing swallowing structures leads to steeper
dose falloff near the target in the vicinity of these structures, we hope to reach the same locoregional disease
control [56].
Exercises
Exercise programs are designed to improve swallow
physiology and possibly prevent or decrease the severity of
swallowing disorders before they develop. These exercises
were easily learned by the patients through instructions
from the speech pathologists [17].
ROM exercises and resistance exercises are available
for the tongue, lips, larynx, and hyoid-related structures.
The most frequently performed pretreatment swallowing
exer- cises are the Mendelsohn maneuver, tongue hold,
tongue resistance, effortful swallow, and Shaker exercise.
These exercises are performed five times a day and are

started
2 weeks before RT [39]. The literature has few
studies that

show an improvement in post-treatment swallowing function and QOL from performing pretreatment swallowing
exercises (Table 8).
Avoidance of nothing-by-mouth periods can help to
diminish difficulty swallowing after treatment. Patients
should be encouraged to swallow throughout the course
of their RT or CRT in an attempt to prevent long-term
dete- rioration in swallowing function [18, 27, 82].

Conclusion
Dysphagia is a common and serious side effect in HNC
patients. It can exist before treatment due to tumor site
and stage and/or be a sequel of treatment strategies such
as surgery and chemoradiotherapy. It has a significant
impact on the QOL because eating is impaired and this
has a major impact on social well-being. There are
subjective and objective scoring systems to measure
dysphagia severity and its impact on QOL. Treatment of
swallowing disorders by compensatory and rehabilitation
treatment procedures is rarely effective, thus prevention

is paramount. Preventing or diminishing dysphagia can be


achieved by treatment modification by using IMRT to try
to spare or decrease the doses to the dysphagia-aspirationrelated structures and the salivary glands without
compromising locoregional disease control. Other ways to
prevent or diminish dysphagia can be adding
radioprotectors or performing exercises before RT.
Diminishing dysphagia by these techniques could
potentially ameliorate the QOL of HNC patients. However,
considerable research remains to be done.
Acknowledgments This work was supported by grants from the
Flemish League Against Cancer (VLK) and the Clinical Research
Fund (KOF) from the University Hospitals Leuven. Piet Dirix is a
research assistant (aspirant) of the Research Foundation-Flandres
(FWO).

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Int J Radiat Oncol Biol Phys 2009:18 (in press).

Nele

Platteaux MD

Piet Dirix MD
Eddy Dejaeger MD, PhD
Sandra Nuyts MD, PhD

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