Professional Documents
Culture Documents
Oral Oncology
journal homepage: www.elsevier.com/locate/oraloncology
Review
a r t i c l e
i n f o
Article history:
Received 30 August 2012
Received in revised form 30 November 2012
Accepted 5 December 2012
Available online 4 January 2013
Keywords:
Head and neck cancer
Swallowing
Trismus
Eating
Interventions
Systematic review
s u m m a r y
Purpose: The incidence of head and neck cancer (HNC) is increasing, and treatment advances have contributed to improvements in survival. However, a growing number of HNC survivors now live with the
long-term consequences of cancer treatment, in particular, problems with eating. The combined effects
of HNC cancer, intensive chemotherapy, radiotherapy and surgery have a profound impact on functional,
psychological, social and physical aspects of eating. Evidence is needed to underpin new rehabilitation
approaches to address these complex problems. This review aimed to identify and summarise the evidence for rehabilitation interventions aimed at alleviating eating problems after HNC treatment.
Methods: A systematic review of studies indexed in Medline, CinAHL and PsycINFO using search terms
relevant to a wide range of aspects of eating. Publications reporting empirical ndings regarding physical,
functional and/or psychosocial factors were included.
Results: Twenty-seven studies were identied. Fifteen focussed on swallowing exercises, eight on interventions to improve jaw mobility and four on swallowing and jaw exercises. None included interventions
to address the complex combination of functional, physical and psychological problems associated with
eating in this patient group.
Conclusions: This review highlights that, whilst there is some evidence to support interventions aimed at
improving swallowing and jaw mobility following treatment for HNC, studies are limited by their size
and scope. Larger, high quality studies, which include patient-reported outcome measures, are required
to underpin the development of patient-centred rehabilitation programmes. There is also a particular
need to develop and evaluate interventions, which address the psychological and/or social aspects of
eating.
2012 Elsevier Ltd. All rights reserved.
Background
Over half a million head and neck cancers worldwide are diagnosed each year and these numbers are predicted to increase
steadily.1 In the last decade, UK oral cancer incidence rates alone
have risen by more than a quarter2 and in Scotland, head and neck
cancers (HNCs) are now recognised as the 6th most common cancer.3 Advances in the treatment of HNC, namely less invasive surgical techniques (e.g. laser surgery) and chemo-radiation therapy
388
Table 1
Search terms used and databases searched.
Search architecture
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
PsyclNFO, Cinahl
Medline
DE Swallowing
DE Aphagia
DE Dysphagia
DE Eating Behaviour
DE Chewing
DE Oral Health
DE Taste Disorders
DE Taste Perception
TX (head and neck cancer) or TX (head and neck neoplasms) or TX (head and
necktumo)
S1 or S2 or S3 or S4 or S5 or S6 or S7 or S7 or S8
S9 and S10
(MH Deglutition)
(MH Deglutition Disorders)
(MH Eating)
(MH exp Eating Behaviour)
(MH Mastication)
(MH Masticatory Muscles)
(MH Trismus)
(MH Taste)
(MH exp Taste Disorders)
(MH exp Head and Neck Neoplasms)
S12 or S13 or S14 or S15 or S16 or S17 or S18 or S19 or S20
S21 and S22
S11 or S23
Exp
Exp
Exp
Exp
Exp
Exp
Exp
Exp
Exp
Deglutition/
Deglutition disorders/
Eating/
Mastication/
Trismus/
Mouth Rehabilitation/
Taste/
Taste Disorder/
Ageusia/
Exp Dysgeusia/
Exp Taste Perception/
Exp Taste Threshold/
Exp Head and Neck Neoplasms
S1 or S2 or S3 or S4 or S5 or S6 or S7 or S8 or S9 or S10 or S11 or S12
S13 and S14
Databases searched: Cinahl, PsyclNFO and Medline. Search architecture based on subject headings for each database.
389
Table 2
Criteria for including and excluding publications in the review.
Criteria
Include if
publication
Includes patients with head and neck cancer who have been treated with surgery, chemotherapy and/or radiotherapy (either singly or in
combination)
Focuses on non-medical interventions specically designed to alleviate or improve eating and drinking difculties (i.e. interventions that could be
delivered by nurses or allied health professionals (AHPs))
Assesses the effect of an intervention on the ability to eat and drink
Reports empirical data from quantitative (e.g. RCT, Survey, Cohort, Interrupted time series, Systematic review and meta-analysis) qualitative
studies (e.g. in-depth interview, focus group, ethnography) or case study
Exclude if
publication
only two had adequate allocation concealment, and for the majority of studies it was unclear if blinded outcome assessment had taken place. Interventions and therapists were not blinded, but it is
recognised that blinding in trials of non-pharmacological interventions is more difcult to achieve.29 Only two30,31 of the case-control/cohort studies were eligible for methodological quality
assessment by our criteria. There were no issues regarding selec-
390
Table 3
Summary of included papers.
Author
Year
Country
Study type
Population
Swallowing/
jaw mobility
status
Intervention
Schedule
Outcomes measured
Case study
N = 1. Right
retromolartrigone
SCC. Neo-adjuvant
CT, surgery and RT.
4 months after
surgery
Gastrostomy
fed. Taking no
foods or
liquids by
mouth
Teaching of three
swallows:
1. Supraglottic
2. Super-supraglottic
3. Mendelsohn
2 3 ml swallows
for each manoeuvre.
Duration not
specied
VF assessed
components of
oropharyngeal
swallow
Logemann
1997
USA
Prospective
case series
N = 9. Mixed
oropharyngeal
cancer. High dose RT
and CT. Intervention
during or up to
5 years after
treatment
Severe
swallowing
problems
perceived by
physician
during or after
treatment
Instructed how to
perform supersupraglottic swallow
2 13 ml swallow
with and without
manoeuvre
VF assessed
components of
oropharyngeal
swallow
Logemann
1997
USA
Quasiexperimental
N = 92 (total n = 102,
stroke). Mixed oral
cancer. Surgery.
Intervention after
treatment
Swallowing
problems
Given instruction on
how to perform
range of motion
exercises (concurrent
with speech therapy)
510 min of
exercises, 10 times
per day
Cavalot
2009
USA
Retrospective
cohort study
N = 43. Glottis or
supraglottic SCC.
Subtotal
laryngectomy.
Intervention. Before
(n = 18) or 10 days
after (n = 25)
treatment
NG tube
feeding
Complimentary
procedures:
Compensatory
postures (head
rotated, head bent
forward, head bent
laterally), increase of
sensory stimulus and
changes in size and
consistency of bolus
and swallowing
exercises
Therapeutic
procedures: patients
taught swallowing
techniques
(supraglottic
swallow, supersupraglottic swallow,
forced deglutition,
Mendelsohn
manoeuvre, Valsalva
technique and
Masako manoeuvre).
All completed
concurrent with
speech therapy
No details given
Time taken to
resumption of
swallowing (days)
Lazarus
2002
USA
Case study
N = 3. Recurrent or
primary SSC of the
larynx or vocal fold.
Surgery and postoperative RT or CRT.
After treatment
Mild
swallowing
problems on
evaluation
Subjects were
instructed in each of
the four manoeuvres
in turn:
1. Effortful swallow
2. Super-supraglottic
swallow
3. Mendelsohn
manoeuvre
4. Tongue-hold
manoeuvre
2 3 ml liquid for
no-manoeuvre and
the four instructed
manoeuvres
Concurrent
manometric and VF
assessed swallow
and degree of residue
Logemann
2009
USA
RCT
N = 19. A variety of
head and neck
cancers. CRT with/
without surgery. At
least 3 months after
CRT or 1 month
post-surgery
Prolonged
oropharyngeal
dysphagia and
aspiration of at
least 3 months
Shaker exercises or
traditional therapy
(super-supraglottic
swallow,
Mendelsohn
manoeuvre and
tongue base
exercises)
Shaker exercise
(appendix 2).
Traditional therapy:
ve times per day.
Both for 6 weeks
Primary aim: VF
assessed occurrence
of aspiration.
Secondary aims:
Location of residue in
the oral cavity,
valleculae or piriform
sinuses and the
Performance Status
Diet Scale
391
Year
Country
Study type
Population
Swallowing/
jaw mobility
status
Intervention
Schedule
Outcomes measured
Carroll
2008
USA
Retrospective
matched case
control study
N = 18. Advanced
SCC of oropharynx,
hypopharynx and
larynx. CRT. 2 weeks
before treatment
(n = 9) or after
treatment as
swallowing
problems
arose(n = 9, control)
Instructions given to
perform:
Each exercise
performed 10 times,
ve times per day
with the exception of
shaker exercises
(performed as per
description,
appendix 2)
VF assessed
functional swallow
3 months post
treatment. Timing of
PEG removal up to
12 months.
1. Tongue hold
2. Tongue resistance
3. Effortful swallow
4. Mendelsohn
manoeuvre
5. Shaker exercises
Kulbersh
2006
USA
Quasiexperimental
N = 37. Primary
hypopharyngeal,
laryngeal or
oropharyngeal SCC.
RT or CRT. 2 weeks
before treatment
(n = 25) or at the
rst visit after
treatment (n = 12)
No details
given
University of
Alabama at
Birmingham, (UAB)
protocol:
1. Mendelsohn
manoeuvre
2. Shaker exercises
3. Tongue hold
4.Tongue resistance
10 repetitions, ve
times per day, except
shaker exercises
(performed as per
description,
appendix 2)
M.D. Anderson
Dysphagia Inventory
(MDADI) assessed
dysphagia-specic
quality of life (QoL),
performed an
average of 14 months
after treatment
Kotz
2012
USA
RCT
N = 26. Newly
diagnosed mixed
oral/oropharynx. RT
and CCRT. Before
CCRT
No difference
in pretreatment
swallowing
function
between
groups
Exercise regime: 1.
Effortfull swallow
2. 2 Tongue based
retraction exercises
3. Super Supraglottic
swallow
4. Mendelssohn
Manoeuvre
Each exercise to be
performed 10 times
3 daily
Performance Status
Scale for Head and
Neck Cancer (PSSH&N), Functional
Oral Intake Scale
(FOIS)
before,1 week after
completion of CCRT,
3, 6, 9 and 12 months
after
Conrmed
swallowing
difculty and
restricted diet
Neuromuscular
electrical stimulation
(NMES) with
(experimental) or
without (control)
conventional
rehabilitation
strategies (oral motor
exercises, pharyngeal
swallowing
exercises, use of
compensatory
strategies during
meals, thermal/
tactile stimulation,
Mendelsohn
manoeuvre and diettexture modications
The functional
dysphagia scale
(FDS), the clinical
dysphagia scale
(CDS), the American
speech-languagehearing association
national outcome
measurement system
swallowing level
scale (ASHA NOMS)
and the M.D.
Anderson dysphagia
inventory (MADI)
Langmore
2006
USA
Prospective
case series
(abstract
only)
N = 7. Mixed HNC.
2 years post-RT
Chronic
dysphagia
Electrotherapy and
swallowing exercises
20 min of
electrotherapy per
day followed by
exercises for 10 min,
repeated three times
per day, 6 days a
week, for 3 months
Count of recurrence
of penetration and
aspiration on VF.
Self-perception of
QoL. Diet type.
Lin
2009
China
RCT
N = 20.
Nasopharyngeal
carcinoma. Over one
year post-RT.
Swallow
function less
than 6 on the
Dysphagia
Outcome and
Severity Scale
(DOSS)
Functional electrical
stimulation (FES)
group (experimental)
or home
rehabilitation
programme (HRP)
group (control)
FES: 15 60 min
sessions, 13 times
per week.
VF assessed swallow,
penetration
aspiration scale and
QoL questionnaire
(MDADI)
392
Table 3 (continued)
Author
Year
Country
Study type
Population
Swallowing/
jaw mobility
status
Intervention
Schedule
Outcomes measured
N = 20, mixed
oropharyngeal
cancer. Postsurgical and/or RT
Conrmed
swallowing
difculty
Teaching of
Mendelsohn
manoeuvre and
sEMG biofeedback
Daily, excluding
weekends, for 50 min
sessions. Plus 2 home
therapy sessions per
day (using portable
biofeedback unit).
Continued until the
patient and clinician
agreed that further
progress was
unlikely or further
therapy was
unnecessary
Change in functional
oral intake using the
Functional Oral
Intake Scale (FOIS),
number of therapy
sessions to discharge,
estimated cost per
unit of functional
charge
Denk
1997
Austria
Quasiexperimental
N = 33. Mixed
oropharyngeal
cancer. Surgery +/RT. 949 days after
treatment or
between 4 and
24 months after
treatment
Prolonged
post-operative
aspiration
(>1 week). NG
or PEG tube fed
Conventional
swallowing therapy
tailored to the
patient including:
thermal stimulation
with ice, exercises for
the lips, tongue,
laryngeal closure and
elevation, effortful
swallow,
Mendelsohn
manoeuvre,
supraglottic swallow,
super-supraglottic
swallow , dietary
measures, with or
without
videoendoscopic
biofeedback
5 45 min sessions
per week for 3 weeks
(inpatient), then 2
3 45 min sessions
per week
(outpatient) until the
patient returned to
full intake diet. The
biofeedback group
received biofeedback
on a weekly basis
Restoration of
exclusively oral
nutrition with food of
all consistencies
without moderate or
severe aspiration (Y/
N). Assessed using
videoendoscopic
swallowing study
and VF
Bryant
1991
USA
Prospective
case study
N = 1. SCC of the
tongue with
metastatic
lymphatic
recurrence. Surgery
and post-operative
RT
NG tube
feeding
Biofeedback
monitoring as an
adjunct to Valsalva
technique and
Mendelsohn
manoeuvre
10 weeks ending
when the patient
could support full
oral intake
Biofeedback readings
and modied barium
swallow. Subjective
patient progress
Range from no
alteration to
severe
alteration in
jaw mobility,
temporomandibular
joint function
and pain
No exercise (control).
Two experimental
groups performing
mandibular exercises
as described by
Buchbinder or Santos
Both experimental
groups completed
the same set of 4
mandibular exercises
with: Group 1
(Buchbinder): 10
repetitions of each
exercise, six times
per day
Group 2 (Santos): 5
repetitions of each
exercise, three times
per day, chew 2
tablets of gum
(trydent)
immediately after for
15 min
Boley gauge to
measure mouth
opening (mm)
measured one day
prior to radiotherapy
and the day of the
nal radiotherapy
session
No details
given
No exercises
(control) or written
instruction on 4
mandibular exercises
(experimental).
Exercises performed
twice per day.
Advised to continue
until follow-up
appointment,
wherein the
radiation oncologist
encouraged them to
continue the
exercises
indenitely.
Dental gap
measurements
(taken with a ruler:
upper incisor to
lower incisor, or gum
to gum if edentulous)
taken at 0 months
and a maximum of
10 follow-up
measurements, with
the rst follow up at
1 month.
Rose
2009
Canada
Quasiexperimental
393
Year
Country
Study type
Population
Swallowing/
jaw mobility
status
Intervention
Schedule
Outcomes measured
Dijkstra
2007
The
Netherlands
Retrospective
case note
review
N = 29 (total n = 37,
non-HNC). mixed
HNC with/without
recurrence. 90%
received RT.
Intervention during
or post-treatment.
Referred to
physical
therapy for
treatment of
trismus
Exercises: active
range of motion, hold
relax techniques,
manual stretching
and joint distraction.
Therapeutic tools:
rubber plugs, tong
blades, dynamic bite
opener, Therabite
apparatus.
Intervention used
until mouth opening
did not improve any
further or when a
functionally
acceptable degree of
mouth opening for
the patient was
reached. No other
data.
Buchbinder
1993
USA
RCT
N = 21. RT.
Intervention up to
5 years posttreatment (majority
within 1 year)
Maximal
interincisal
opening of
30 mm or less.
Group 1 (Control):
Unassisted exercise
involving opening to
maximal interincisal
distance, closing and
then moving
maximally to the left,
right and
protrusively. Group 2
(Experimental): The
same unassisted
exercises as Group 1
but, in addition, they
used stacked tongue
depressors to provide
static stretch. Group
3 (Experimental):
The same unassisted
exercises, coupled
with the use of the
Therabite System
Group 1 (Control): 10
cycles per day of
unassisted exercise.
610 exercises
sessions completed
each day for
10 weeks. Group 2:
Each stretch held for
30 s, performed ve
times each session,
for 610 sessions per
day, for 10 weeks.
Group 3: Therabite
System used to
achieve and sustain a
maximum
comfortable stretch
for 30s. This stretch
was repeated ve
times per session, 6
10 sessions per day,
for 10 weeks
Maximal Interincisor
opening (MIO) and
measures of lateral
and protrusive
movements,
measured at 2 week
intervals to 10 weeks
Retrospective
case series
N = 20 Total n = 48
(dental treatment/
oral surgery/stroke).
Post RT to H&N.
<40 mm
Interincisal
distance
Range of motion
therapy with
Dynaspinttrismus
system (DTS). Fitting
and training of the
DTS. Verbal and
written instructions
provided
Maximal interincisal
distance (MID)
Brunello
1995
Australia
Case study
N = 1. SSC of the
mucous lining of the
oropharynx. Surgery
and RT. 3 months
post-treatment
Severe
restriction of
mouth
opening
(maximum
opening
15 mm)
Dynamic opening
device
No details given
Cohen
2005
USA
Prospective
case series
N = 7. SSC of the
oropharynx. Surgery
with/without RT.
Within 6 weeks
postoperatively
Initial average
maximal
interincisor
opening
30 mm
Therabite mechanical
mobilisation device
Instructed to perform
6 repetitions, holding
the mouth open for 6
s each time, six times
per day. Initial range
setting 25 mm which
was increased as
tolerated. Follow up
1248 weeks postsurgery. Compliance
was assessed by
patient self-reporting
Maximal Interincisor
opening (MIO). A 5question selfassessment
telephone survey
Stubbleeld
2010
USA
Retrospective
cohort study
Patients
referred for
evaluation and
treatment of
trismus
Dynamic opening
device. (Pain
medications and
botulinum toxin
injections prescribed
as appropriate)
Change in maximal
interincisor distance
(MID)
Verbal or written
instructions on 2
Multi-dimensional
assessment protocol:
394
Table 3 (continued)
Author
Year
Country
Study type
Population
Swallowing/
jaw mobility
status
Intervention
Schedule
Outcomes measured
rehabilitation
approached:
VF, Maximum
interincisor mouth
opening (MIO),
weight changes, BMI.
FIOS, study specic
questionnaire for QoL
evaluation and a
visual analogue scale
(VAS) for pain
Speech pathologist:
10 repetitions of
Mendelsohn
manoeuvre and 5
repetitions of tongue
mobility exercises,
performed at least
once (preferably
twice) per day until
3 months after
treatment.
Physiotherapist:
Muscle
strengthening
exercises twice daily
until 6 months after
treatment. Active
maximal mouth
opening assisted
with the JTS
10 20 s, twice per
day
Manual palpation of
swallow (5 and 15 ml
boluses). Aspiration.
Head and neck range
of movement and
mouth opening (IID
between upper and
lower left front
teeth). Body weight.
Hospital and Anxiety
Depression Scale
(HADS), European
Organization for
Research and
Treatment of Cancer
(EORTC-QLQ-C30,
EORTC-H&N35) and a
project specic
questionnaire.
Primary outcome:
Weight loss and
2 year survival.
Secondary outcomes:
sick leave, selfreported loss of
function, HRQoL and
anxiety/depression
Group 1 (control): 5
stretch exercises and
3 strengthening
exercises (effortful
swallow, masako
manoeuvre and
super-supraglottic
swallow)
Group 2
(experimental): 4
Jaw stretch exercises
and 1 swallow
strengthening
exercises with
Therabite device
Ahlberg
2011
Sweden
Quasiexperimental
No details
given
Speech pathologist
led Mendelsohn
manoeuvre and
tongue mobility
exercises
Physiotherapy led
muscle stretching
exercises and use of
the Acute Medic Jaw
Trainer and Stretcher
(JTS).
Tang
2010
China
RCT
N = 43.
Nasopharyngeal
carcinoma. RT. After
treatment for
3 months
No details
given
Dysphagia: Tongue
ROM exercises,
effortful swallow,
Mendelsohn
manoeuvre, sensory
stimulation,
postures. Trismus:
ROM exercises for
the temporomandibular jaw, use
of Therabite
Each exercise
practiced for 15
cycles, three times
per day
Dysphagia: Water
swallow test.
Trismus: the LENT/
SOMA score and
Interincisor distance
(IID)
Carnaby
Mann
2012
USA
RCT
No history of
non-oral
feeding
Randomised to one of
three groups:
Usual care:
supervision for
feeding and
precautions for safe
swallowing Sham:
buccal extension
manoeuvre
valchuff twice daily
under direction, 10
repetition over 4
cycles of 10 min
(45 min sessions),
dietary modication
Primary outcome
muscle size and
composition
(determined by T2weighted magnetic
resonance imaging)
395
Year
Country
Study type
Population
Swallowing/
jaw mobility
status
Intervention
Schedule
Outcomes measured
Usual care
Sham swallowing
intervention
Active swallowing
exercises
(pharyngocise)
Pharyngocise: twice
daily exercises using
falsetto, tongue
press, hard swallow,
and jaw resistance/
strengthening using
the Therabite 10
repetitions over 4
cycles of 10 min
(45 min sessions)
Secondary outcomes:
functional
swallowing ability,
dietary intake,
chemosensory
function, salivation,
nutritional status,
and dysphagiarelated
complications
VF = Video Fluouroscopy.
Table 4
Methodological quality assessment.
Authors
RCT/quasiexperimental
Allocation
concealed
Blinded outcome
assessment
Blinded therapy
provider
Blinded
participants
Intention to treat
analyses
Basic description of
intervention
Logemann (2009)
Ryu (2009)
Lin (2009)
Buchbinder (1993)
van der Molen (2011)
Tang (2010)
Kulbersh (2006)
RCT
RCT
RCT
RCT
RCT
RCT
Quasiexperimental
Quasiexperimental
Quasiexperimental
Quasiexperimental
Quasiexperimental
Quasiexperimental
RCT
RCT
Unclear
YES
Unclear
Unclear
Unclear
Unclear
NO
YES
YES
Unclear
Unclear
Unclear
Unclear
Unclear
NO
NO
NO
NO
NO
NO
NO
NO
NO
NO
NO
NO
NO
NO
NO
NO
YES
YES
YES
Unclear
Unclear
YES
YES
YES
YES
YES
YES
YES
NO
Unclear
NO
NO
Unclear
YES
NO
Unclear
NO
NO
Unclear
NO
NO
Unclear
NO
NO
Unclear
YES
NO
Unclear
NO
NO
YES
YES
NO
Unclear
NO
NO
Unclear
YES
YES
Unclear
YES
YES
NO
NO
NO
NO
YES
YES
YES
YES
Logemann (1997)
Denk (1997)
Rose (2009)
Grandi (2007)
Ahlberg (2011)
Carnaby-Mann (2012)
Kotz (2012)
tion bias in the study by Cavalot et al.30 however, the potential for
bias in the Carroll31 study was difcult to assess due to lack of
information. It was not clear whether there was any information
bias or confounding.
Fifteen of the included publications focussed on swallowing
exercises, 8 focussed on jaw mobility interventions and 4 focussed
on swallowing exercises combined with interventions to improve
jaw mobility. Each of these groups is reported separately below.
No papers focussed on managing taste, psychological and/or social aspects of eating and drinking. The vast majority of studies
used objective measures to assess swallowing or jaw mobility.
Few included patient-reported outcome or quality of life measures
to ascertain the subjective impact of the intervention or its effects
on broader aspects of everyday life.
Swallowing exercises
All 15 studies used one or more of the specic forms of exercise
shown in Table 5. Nine studies focussed on swallowing exercises
alone, three on swallowing exercises with electrical stimulation
and three on swallowing exercises with biofeedback.
Swallowing exercises alone
All nine studies were conducted in the USA. Six of these were
published in the last 10 years.
Experimental evidence
Four publications provided experimental evidence, including
two RCTs. The rst32 compared the Shaker exercise with Traditional therapy (super-supraglottic swallow, Mendelsohn manoeuvre and tongue base exercises) in 19 patients with HNC. There was
a signicantly greater reduction in the occurrence of post-swallow
aspiration in the Shaker group (60%) compared to the traditional
group (0%) (p = 0.028; Fishers exact test). However, patients who
received traditional therapy demonstrated signicant improvements in a number of biomechanical measures of swallow (superior laryngeal movement (p = 0.009) and superior hyoid
movement (p = 0.044) on 3-ml paste swallows, and anterior laryngeal movement on 3-ml liquid boluses (p = 0.026; ANOVA). The
authors concluded that exercises should be selected according to
the particular swallowing difculty. The second RCT,27 published
after our original search took place, compared a prophylactic swallowing exercise programme (involving effortful and super supraglottic swallow, tongue hold manoeuvre, tongue retraction and
Mendelsohn manoeuvre), with referral to a speech and language
therapist for assessment and symptomatic treatment. Despite the
small number of participants (n = 26), signicant differences on
the Functional Oral Intake Scale (FOIS) were found in favour of
the intervention group at 3 and 6 months after the intervention
(median 3-month intervention score 7 [range 57] vs. median control score 5 [range 37] p = 0.03) and median 6-month intervention
score 7 [range 67] vs. median control score 6 [range 37]
(p = 0.009; Fishers exact test).
396
Table 5
Swallowing exercises.
Exercise
Target
Procedure
Patient is to swallow and when the larynx reaches the highest position
during the swallow they are to hold it there for a few seconds, then relax
Tongue resistance6567
Shaker67
Sustained hold
Repetitive
Jaw exercises
Mendelsohn
62,63
37
Patient is to hold their tongue between their teeth and swallow hard
The remaining studies were quasi-experimental. The rst33 assessed the relationship between the total amount of swallowing
therapy received 13 months post-operatively and changes in oropharyngeal swallow. A weak but signicant correlation (Pearsons r
coefcient 0.23; p = 0.03) was found between total exercise time
and oropharyngeal swallowing efciency (OPSE) on liquids. Additionally, there was a signicant improvement in OPSE for liquid
(mean difference 7.6 (SE 3.9) vs. 7 (SE 3.6) p = 0.01) and paste
(mean difference 9.5 (SE 4.5) vs. 4.6 (SE 4.4); p = 0.04) in those
who performed swallowing exercises compared to those who did
not (unpaired t-test).
Kulbersh et al.34 evaluated the utility of pre-treatment swallowing exercises on post-treatment swallowing quality of life (QoL) as
measured by the MD Anderson Dysphagia Inventory (MDADI).
There was a signicant improvement in three of the four domains
(global, emotional and physical) of QoL in those who received the
pre-treatment swallowing exercises compared to those who received post-treatment swallowing exercises only. After controlling
for site of tumour, age, gender and race, patients performing swallowing exercises scored signicantly higher on the global assessment score (74.4 9.9 vs. 32.9 15.8 (p = 0.0002); t-test).
Three publications focussed on swallowing exercises with electrical stimulation. Two trials assessed the effect of electrical stimulation on swallowing function. Ryu et al.38 evaluated
neuromuscular electrical stimulation (NMES) in HNC patients suffering from post-treatment dysphagia, whilst Lin et al.39 focussed
specically on patients with dysphagia secondary to irradiated
nasopharyngeal carcinoma.
Different control interventions were used in each study. Ryu
et al. randomised patients to NMES with traditional therapy
(experimental) or traditional therapy alone (control). Traditional
therapy consisted of oral motor exercises, pharyngeal swallowing
exercises, use of compensatory strategies during meals, thermal/
tactile stimulation, Mendelsohn manoeuvre and diet-texture modications. The experimental group showed a signicantly larger
improvement in functional dysphagia scale (FDS) (11.4 8.1) compared to the control group (3.3 14.0); p = 0039). Lin et al. randomised patients into a functional electrical stimulation (FES)
group (experimental) and a home rehabilitation program (HRP)
397
control group (exercises only). The majority of swallowing outcomes improved signicantly in the experimental group but not
in the control group.
A prospective case series reported in a conference abstract40 assessed the effect of electrical stimulation on swallow function and
found that aspiration reduced from 50% to 14%, residues were reduced from 90% to 70% and oral diet levels were improved.
Three studies focussed on swallowing exercises with biofeedback. The earliest study, published in 199141 assessed the use of
biofeedback as an adjunct to the Valsalva technique and Mendelsohn manoeuvre, in a patient with tongue cancer who relied on
nasogastric (NG) tube feeding. The patient regained swallowing
function and returned to full oral intake after 10 weeks of the
intervention.
The second US publication42 evaluated the functional benets of
dysphagia therapy using adjunctive surface electromyographic
(sEMG) biofeedback in patients with HNC and stroke. Functional
oral intake of food/liquid increased in 80% of the HNC group.
An Austrian study43 compared the value of conventional swallowing therapy with (experimental) or without (control) the use of
videoendoscopic biofeedback. Swallowing therapy included a variety of swallowing exercises, diet modications and thermal stimulation. Patients were NG or gastrostomy fed prior to the
intervention. In the rst 40 days after the intervention was initiated, patients with videoendoscopic biofeedback had a 2.3-fold
chance of regaining exclusively oral nutrition than those receiving
conventional swallowing therapy alone. After 40 days, there was
no difference between the two groups, therefore the authors recommend that this method is used in the early phase of
rehabilitation.
398
cant difference being that the experimental group showed less residue on video-uoroscopy, after swallowing cake (p < 0.021; Wilcoxen signed rank test). However, there were differences in the
gender, pain experience and compliance of the groups and this
may have accounted for some of the differences in outcome.
One RCT28 in this category was published after our original
search took place. This studied the effectiveness of a preventative
behavioural intervention (Pharyngocise) compared with a sham
intervention and usual care during CCRT. This well-designed study
used a comprehensive range of objective and subjective outcomes,
nding signicantly less deterioration in swallowing musculature
in the active treatment arm than in the two control groups (e.g.
change in genioglossus length 0.5 vs. 3.67 (usual care) and 1.5
(sham) (p < 0.03; ANOVA and similar trends in mylohyoid thickness and hyoglossus length deterioration). Outcomes for functional
swallowing ability, mouth opening, taste, smell and salivation
were also superior in the Pharyngocise group. However, there were
no observable differences between the groups on videouoroscopy, and improvements in many of the outcome measures were
also seen in the sham group. Additionally, a greater proportion of
patients complied with the sham intervention, which involved a
less intensive buccal extension manoeuvre, suggesting that any
swallowing exercise is better than none.
A quasi-experimental study, published in 201154 investigated
the effectiveness of an early preventative rehabilitation programme on swallowing and trismus. This programme introduced
self-directed swallowing and jaw mobility interventions prior to
treatment, although the exact timing of the intervention was
not clear. A range of different outcomes were measured including
a project specic questionnaire which encompassed swallowing
difculties, chewing difculties and reduced mouth opening ability. The control group was signicantly less likely to report loss of
function 6 months after treatment (proportional odds ratio (OR)
of 2.3 (95% CI 1.34.0; MannWhitney U and proportional odds
model) on this self-report questionnaire. No positive effects
(weight loss, QoL or 2-year survival) of early preventative rehabilitation were identied. The authors comment on the potential
need for closer interaction between patients and therapists, recommending that an RCT of early rehabilitation should be conducted, including more regular surveillance and physical
evaluation.
In both of these recently published studies, approximately half
the study group were lost to follow-up and in the Carnaby-Mann
study28 a very small proportion of patients were included in the
trial (13%), therefore it is possible that systematic bias may have
been introduced. Also, it is important to note that there is relatively little information about compliance in the RCTs of swallowing exercises. Where this information is available, more
than half the patients stopped performing the exercises during
treatment.53
Discussion
This review identied and summarised the evidence for rehabilitation interventions aimed at alleviating the physical, functional
and psychosocial difculties with eating and drinking following
treatment for HNC. Despite using a wide search strategy, we did
not identify any empirical papers that focussed on managing taste,
psychological and/or social aspects of eating and drinking. Twentyseven publications were included in the review, and all of these
evaluated functional interventions for swallowing and/or trismus.
Studies of different methodological types were included in order to identify the range and breadth of evidence available to support rehabilitation interventions. This inevitably meant that the
quality of some publications was poor and the level of evidence
tional therapies, are likely to improve functional outcomes in patients with head and neck cancer, particularly if they are introduced before treatment starts. Furthermore, a recent costeffectiveness analysis suggests that preventative swallowing exercises result in less dependence on tube feeding and fewer hospital
admission days than usual care.56 However, the evidence base is
poor and it is impossible to conduct any formal meta-analysis of
ndings as the interventions, outcome measures and populations
are so heterogeneous.
Conclusion
It is clear from this review that the evidence-base for rehabilitation interventions aimed at alleviating difculties with eating and
drinking following treatment for HNC is limited. In particular, we
found no empirical studies pertaining to interventions focussed
on psychological and/or social aspects of eating and drinking.
One trial evaluated zinc sulphate in the management of taste57
but as this was a pharmacological intervention it was excluded
from our review. With growing evidence that such difculties have
signicant negative consequences for patients,9,10 there is an urgent need to develop holistic interventions which address the complexity of eating and drinking rather than just the individual
functions involved.
Interestingly, our search revealed a small number of publications reporting benets from interventions such as mindful eating58 and support groups,59 illustrating the potential for
psychosocial intervention in this area. The mindful eating study58
provides auto-biographical accounts of patients who report
improvement in a variety of symptoms, including dry mouth and
taste changes. Patients identied mindful eating as a way to manage fear and anxiety around eating and often expressed a deep
appreciation for being given tools to reconnect with the experience
of eating as a part of living. The quasi-experimental study by
Vakharia et al.59 demonstrated that those patients who participated in the HNC support group achieved signicantly better
scores in the domains of eating, emotion, and pain as well as in
the global bother and response to treatment questions of the
HNQOL instrument compared with those patients who did not participate. In the context of cancer cachexia, a range of studies support a psychosocial approach to supporting self-management for
eating and drinking.60,61 These ndings suggest that patients with
HNC may also benet from such an approach, and further evidence
is needed.
High quality studies of swallowing and jaw mobility interventions in large study populations are also required. Although such
research is likely to be highly complex given existing variations
in practice across treatment centres as well as between countries,
in the absence of such evidence, current practice remains variable
and inconsistent.
Strengths and limitations of this review
Where previous authors have focussed on functional outcomes
related to different types of HNC treatment, a strength of this review is that it specically sought evidence for interventions to address the functional outcomes themselves. The broad nature of the
search strategy facilitated identication of any intervention aimed
at alleviating eating difculties in HNC patients, and enabled us to
identify a greater range of studies than previous reviews.16 Furthermore, our focussed inclusion and exclusion criteria allow us
to be condent about the gaps in current evidence as well as where
the evidence exists. Whilst leading speech and language therapists
in the Netherlands, Sweden and the UK were contacted, we did not
contact all key authors in the eld.
399
This review highlights that, while evidence exists to address difculties with swallowing and jaw mobility following treatment for
HNC, this is limited. Larger, high quality studies, which include patient-reported outcomes as well as objective functional measures,
are required in order to direct future rehabilitation programmes.
There is also a particular need for interventions to address the psychological and/or social aspects of eating and drinking.
None declared.
Acknowledgements
This study was supported by a grant from Macmillan Cancer
Support as part of the Consequences of Cancer Treatment
workstream of the National Cancer Survivorship Initiative
www.ncsi.org.
References
1. Cancer Research UK. Cancer Stats Cancer Worldwide; 2011.
2. Cancer Research UK. Cancer Stats Key Facts Oral, Cancer; 2012.
3. Information Services Division. Cancer in Scotland: NHS National Services
Scotland; 2010.
4. Haddad RI, Dong M. Recent advances in head and neck cancer. N Engl J Med
2008;359:114354.
5. Mittal BB, Pauloski BR, Haraf DJ, Pelzer HJ, Argiris A, Vokes EE, et al. Swallowing
dysfunction-preventative and rehabilitation strategies in patients with headand-neck cancers treated with surgery, radiotherapy, and chemotherapy: a
critical review. Int J Radiol Oncol Biol Phys 2003;57(5):121930.
6. National Institute for Clinical Excellence. Guidance on Cancer Services:
Improving Outcomes in Head and Neck Cancers The Manual; 2004.
7. Eades M, Chasen M, Bhargava R. Rehabilitation: long term physical and
functional changes following treatment. Semin Oncol Nurs 2009;25(3):22230.
8. Manikantan K, Khode S, Sayed SI, Roe J, Nutting CM, Rhys-Evans P, et al.
Dysphagia in head and neck cancer. Cancer Treat Rev 2009;35:72432.
9. Ramaekers BL, Joore MA, Grutter JP, van den Ende P, Jong J, Ouben R, et al. The
impact of late treatment-toxicity on general health-related quality of life in
head and neck cancer patients after radiotherapy. Oral Oncol 2011;47:76874.
10. Langendijk JA, Doornaert P, Verdonck-de Leeuw IM, Leemans CR, Aaronson NK,
Slotman BJ. Impact of late treatment-related toxicity on quality of life among
patients with head and neck cancer treated with radiotherapy. J Clin Oncol
2008;26:37706.
11. Talwar B. Chapter 11: head and neck cancer. In: Shaw C, editor. Nutrition and
cancer. Blackwell; 2010.
12. Scottish Intercollegiate Guidelines Network. Diagnosis and management of
head and neck cancer, vol. 90, 2006.
13. British Association of Head and Neck Oncologists B. BAHNO Standards; 2009.
14. National Cancer Action Team. Rehabilitation care pathway: Head and neck:
Crown Copyright; 2009.
15. Roe J, Ashworth KM. Prophylactic swallowing exercises for patients recieving
radiotherapy for head and neck cancer. Curr Opin Otolaryngol Head Neck Surgery
2011;19(3):1449.
16. van der Molen L, van Rossum MA, Burkhead LM, Smeele LE, Hilgers FJ.
Functional outcomes and rehabilitation strategies in patients treated with
chemoradiotherapy for advances head and neck cancer: a systematic review.
Eur Arch Otorhinolaryngol 2009;266(6):889900.
17. Manikantan K, Khode S, Dwivedi RC, Palav R, Nutting CM, Rhys-Evans P, et al.
Making sense of post-treatment surveillance in head and neck cancer: when
and what to follow-up. Cancer Treat Rev 2009;35(8):74453.
18. Urquhart C, Hassanali H, Kanatas A, Mitchell D, Ong T. The role of the specialist
nurse in the review of patients with head and neck cancer is it time for a
rethink of the review process? Eur J Oncol Nursing 2011;15:185.
19. Garg S, Yoo J, Winquist E. Nutritional support for head and neck cancer patients
recieving radiotherapy: a systematic review. Support Care Cancer
2010;18:66777.
20. Furness S, Worthington HV, Bryan G, Birchenough S, McMillan R. Interventions
for the management of dry mouth: topical therapies. Cochrane Database Syst
Rev 2011;(12).
21. Bensadoun RJ, Riesenbeck D, Lockhart PB, Elting LS, Spijkervet FK, Brennan MT.
Trismus section, oral care study group, Multinational Association for
Supportive Care in Cancer (MASCC)/International Society of Oral Oncology
(ISOO). A systematic review of trismus induced by cancer therapies in head and
neck cancer patients. Support Care Cancer 2010;18(8):10338.
22. Dijkstra PU, Kalk WWI, Roodenburg JLN. Trismus in head and neck oncology: a
systematic review. Oral Oncol 2004;40:87989.
400
23. Schoen PJ, Reinstema H, Raghoebar GM, Vissink A, Roodenburg JL. The use of
implant retained mandibular prostheses in the oral rehabilitation of head and
neck cancer patients. A review and rationale for treatment planning. Oral Oncol
2004;40(9):86271.
24. Tang JA, Rieger JM, Wolfaardt JF. A review of functional outcomes related to
prosthetic treatment after maxillary and mandibular reconstruction in patients
with head and neck cancer. Int J Prosthetics 2008;21(4):33754.
25. Emerson JD, Burdick E, Hoaglin DC, Mosteller F, Chalmers TC. An empirical sudy
of the possible relation of treatment differences to quality scores in controlled
randomized clinical trials. Control Clin Trials 1990;11(5):33952.
26. Higgins JPTA, Douglas G. Assessing risk of bias in included studies. The Cochrane
Collaboration; 2011.
27. Kotz T, Federman A, Kao J, Milman L, Packer S, Lopez-Prieto C, et al. Prophylactic
swallowing exercises in patients with head and neck cancer undergoing
chemoradiation: a randomised trial. Arch Otolaryngol Head Neck Surgery
2012;138(4):37682.
28. Carnaby-Mann G, Crary M, Schmalfuss I, Amdur R. Pharyngocise: randomized
controlled trial of preventative exercises to maintain muscle structure and
swallowing function during head-and-neck chemoradiotherapy. Int J Radiat
Oncol Biol Phys 2012;83(1):2109.
29. Boutron I, Moger D, Altman DG, Schulz KF, Ravaud P. Extending the CONSORT
statement to randomised trials of nonpharmacological treatment: explanation
and elaboration. Ann Intern Med 2008;148:259305.
30. Cavalot AL, Ricci E, Schindler A, Roggero N, Albera R, Utari C, et al. The
importance of preoperative swallowing therapy in subtotal laryngectomies.
Otolaryngol Head Neck Surgery 2009;140:8225.
31. Carroll WR, Locher JL, Canon CL, Bohannon IA, McColloch NL, Magnuson JS.
Pretreatment swallowing exercises improve swallow function after
chemoradiation. Laryngoscope 2008;118:3943.
32. Logemann JA, Rademaker A, Pauloski BR, Kelly A, Stangl-McBreen C, Antinoja J,
et al. A randomized study comparing the shaker exercise with traditional
therapy: a preliminary study. Dysphagia 2009;24:40311.
33. Logemann JA, Pauloski BR, Rademaker AW, Colangelo LA. Speech and
swallowing rehabilitation for head and neck cancer patients. Oncology
1997;11(5):6519.
34. Kulbersh BD, Rosenthal EL, McGrew B, Duncan RD, McColloch NL, Carroll WR,
et al. Pretreatment, preoperative swallowing exercises may improve dysphagia
quality of life. Laryngoscope 2006;116:8836.
35. Lazarus C, Logemann JA, Gibbons P. Effects of manouvers on swallowing
function in a dysphagic oral cancer patient. Head Neck 1993;15(5):41924.
36. Lazarus C, Logemann JA, Song CW, Rademaker AW, Kahrilas PJ. Effects of
voluntary maneuvers on tongue base function for swallowing. Folia Phoniatrica
et Logopaedica 2002;54:1716.
37. Logemann AJ, Pauloski BR, Rademaker AW, Colangelo LA. Super-supraglottic
swallow in irradiated head and neck cancer patients. Head Neck
1997;19(6):5335540.
38. Ryu JS, Kang JY, Park JY, Nam SY, Choi SH, Roh JL, et al. The effect of electrical
stimulation therapy on dysphagia following treatment for head and neck
cancer. Oral Oncol 2009;45:6658.
39. Lin PH, Hsiao TY, Chang YC, Ting LL, Chen WS, Chen SC, et al. Effects of
functional electrical stimulation on dysphagia caused by radiationg therapy in
patients
with
nasopharyngeal
carcinoma.
Support
Care
Cancer
2009;19(1):919.
40. Langmore SE. Electrical stimulation for dysphagia in head and neck cancer
patients; 2006.
41. Bryant M. Biofeedback in the treatment of a selcted dysphagic patient.
Dysphagia 1991;6:1404.
42. Crary MA, Carnaby-Mann GD, Groher ME, Helseth E. Functional benets of
dysphagia therapy using adjunctive sEMG biofeedback. Dysphagia
2004;19:1604.
43. Denk DW, Kaider A. Videoendoscopic biofeedback: a simple method to improve
the efcacy of swallowing rehabilitation of pateints after head and neck
surgery. Oto-Rhino-Laryngology 1997;59:1005.
44. Grandi G, Silva ML, Streit C, Wagner JCB. A mobilization regimen to prevent
mandibular hypomobility in irradiated patients: an analysis and comparison
of two techniques. Medicina Oral Patologia Oral y Circugia Bucal 2007;12(2):
1059.
45. Rose T, Leco P, Wilson J. The development of simple daily jaw exercises for
patients receiving radical head and neck radiotherapy. J Med Imaging Radia Sci
2009;40:327.
46. Buchbinder D, Currivan RB, Kaplan AJ, Urken ML. Mobilization regimens for the
prevention of jaw hypomobility in the radiated patient: a comparison of three
techniques. J Oral Maxillofacial Surgery 1993;51:8637.
47. Dijkstra PU, Sterken MW, Pater R, Spijkervet FKL, Roodenburg JLN. Exercise
therapy for trismus in head and neck cancer. Oral Oncol 2007;43:38994.
48. Stubbleeld MD, Maneld L, Riedel ER. A preliminary report on the efcacy of a
dynamic jaw openng device (dynasplint trismus system) as part of the
multimodal treatment of trismus in patients with head and neck cancer. Arch
Phys Medicine Rehabil 2010;91:127882.
49. Cohen EG, Deschler DG, Walsh K, Hayden RE. Early use of a mechanical
stretching device to improve mandibular mobility after composite resection: a
pilot study. Arch Phys Med Rehabil 2005;86(7):14169.
50. Shulman DH, Shipman B, Wllis FB. Treating trismus with dynamic splinting: a
cohort, case series. Adv Ther 2008;25(1):915.
51. Brunello DL. The use of a dynamic opening device in the treatment of radiation
induced trismus. Aust Prosthodontic J 1995;9:458.
52. Tang Y, Shen Q, Wang Y, Lu K, Wang Y, Peng Y. A randomised prospective study
of rehabilitation therapy in the treatment of radiation-induced dysphagia and
trismus. Strahlenther Onkol 2010;187:3944.
53. van der Molen L, van Rossum MA, Burkhead LM, Smeele LE, Rasch CRN, Hilgers
FJM. A randomized preventative rehabilitation trial in advanced head and neck
cancer patients treated with chemoradiotherapy: feasability, compliance, and
short-term effects. Dysphagia 2011;26:15570.
54. Ahlberg A, Engstrom T, Nikolaidis P, Gunnarsson K, Johansson H, Sharp L, et al.
Early self-care rehabiliation of head and neck cancer patients. Acta Otolaryngol
2011;131:55261.
55. Carter J, Humbert I. E-stim for dysphagia: yes or no? The ASHA Leader; 2012.
56. Retel V, van der Molen L, Hilgers F, Rasch C, LOrtye A, Steuten L, et al. A costeffectiveness analysis of a preventive exercise program for patients with
advanced head and neck cancer treated with concomitant chemo-radiotherapy.
BMC Cancer 2011;11:475.
57. Ripamonti C, Zecca E, Brunelli C, Fulfaro F, Villa S, Balzarini A, et al. A
randomized, controlled clinical trial to evaluate the effects of zinc sulfate on
cancer patients with taste alterations caused by head and neck irradiation.
Cancer 1998;82(10):193845.
58. Meyers S, Ott MJ. Mindful eating as a clinical intervention for survivors of head
and neck cancer. Top Clin Nutr 2008;23(4):3406.
59. Vakharia KT, Ali MJ, Wang SJ. Quality-of-life impact of participation in a head
and neck cancer support group. Otolaryngol Head Neck Surgery
2007;136:40510.
60. Hopkinson J, Fenlon D, Okamoto I, Wright D, Scott I, Addington-Hall J, et al. The
deliverability, acceptability, and perceived effect of the macmillan approach to
weight loss and eating difculties: a phase II, cluster-randomized, exploratory
trial of a psychosocial intervention for weight- and eating-related distress in
people with advanced cancer. J Pain Symptom Manage 2010;40(5):68495.
61. Hopkinson J. The emotional aspects of cancer anorexia. Curr Opin Supportive
Palliative Care 2010;4(4):2548.
62. Logemann JA, Kahrilas PJ. Relearning to swallow after stroke application of
maneuvers and indirect biofeedback: a case study. Neurology 1990;40:11368.
63. Kahrilas PJ, Logemann JA, Krugler C, Flanagan E. Volitional augmentation of
upper esophageal sphincteropening during swallowing. Am J Physiol
1991;260:G4506.
64. Fujiu M, Logemann JA. Effect of tongue-holding maneuver on posterior
pharyngeal wall movement during deglutition. Am J Speech-Language Pathol
1996;5(1):2330.
65. Corbin-Lewis K, Liss JM, Sciortino KL. Chapter 7 Clinical Anatomy & Physiology of
the Swallowing Mechanism 2005:21315.
66. Jordan K. Rehabilitation of patients with dysphagia. Ear Nose Throat J
1979;58:867.
67. Shaker R, Kern M, Bardan E, Taylor A, Stewart E, Hoffmann R, et al.
Augmentation of deglutitive upperesophageal sphincter opening in the
elderly by exercise. Am J Physiol 1997;272(6 Pt. 1):G151822.
68. Larsen G. Conservative management for incomplete dysphagia paralytica. Arch
Phys Med Rehabil 1973;54:1805.