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Oral Oncology 49 (2013) 387400

Contents lists available at SciVerse ScienceDirect

Oral Oncology
journal homepage: www.elsevier.com/locate/oraloncology

Review

A systematic review of interventions for eating and drinking problems


following treatment for head and neck cancer suggests a need to look beyond
swallowing and trismus
Nadine Cousins a, Fiona MacAulay b, Heidi Lang d, Steve MacGillivray c, Mary Wells d,
a

School of Medicine, University of Dundee, Ninewells Hospital, Dundee DD1 9SY, UK


NHS Tayside, Ninewells Hospital and Medical School, Speech & Language Department, Dundee DD1 9SY, UK
Social Dimensions of Health Institute, University of Dundee, 11 Airlie Place, Dundee DD1 4HJ, UK
d
School of Nursing and Midwifery, University of Dundee, 11 Airlie Place, Dundee DD1 4HJ, UK
b
c

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

Corresponding author. Address: Cancer Nursing, School of Nursing and


Midwifery, University of Dundee, 11 Airlie Place, Dundee DD1 4HJ, UK. Tel.: +44
1382 388643; fax: +44 1382 388534.
E-mail addresses: n.l.cousins@dundee.ac.uk (N. Cousins), ona.macaulay@nhs.net (F. MacAulay), h.v.lang@dundee.ac.uk (H. Lang), s.a.macgillivray@dundee.ac.uk
(S. MacGillivray), e.m.wells@dundee.ac.uk (M. Wells).
1368-8375/$ - see front matter 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.oraloncology.2012.12.002

(CRT), have contributed to an improvement in the survival rates


of HNC patients.4 However, whilst intensive treatment regimens
improve survival, a growing number of patients are met with the
burden of long-term negative treatment-related side-effects.5
The long-term side-effects of treatment for HNC are often severe,
with the majority of people being left with impairment in vital functions such as eating and drinking.6,7 Such impairments include difculties with swallowing (dysphagia), opening the mouth (trismus),
chewing ability, dry mouth and altered taste perception. Several
studies have shown that such impairments and difculties have
important negative consequences, both in terms of physical health
(through an increased risk of malnutrition, weight loss and aspiration),8 and psychosocial wellbeing (through a reduction in the pleasure of eating, social interaction and quality of life).9,10
Given the multifactorial challenges of maintaining quality of
life, nutrition, and particularly oral intake, in this patient group11

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N. Cousins et al. / Oral Oncology 49 (2013) 387400

it is vital that interventions to support eating and drinking address


the range of problems which interfere with the physical, functional
and psychosocial aspects of opening the mouth, chewing, tasting
and swallowing food. Current guidelines emphasise the need for
a multidisciplinary approach to head and neck cancer care6,12,13
and The National Institute of Health and Clinical Excellence
(NICE),6 for example, recommends that Each local support team
should have access to the expertise required to manage the aftercare and rehabilitation needs of all of its patients. . .. However, despite the publication of standards14 for such rehabilitation, services
are variable15 and reliable evidence for effective interventions is
lacking.16 Clearer evidence to underpin rehabilitation and selfmanagement approaches is increasingly important, as the growing
number of HNC survivors is likely to create a strain on existing
medically-led models of HNC follow-up, which are largely directed
at reducing recurrence17 and may be unsustainable.18
So far, reviews of interventions to improve eating problems
have concentrated on nutritional support19 or the alleviation of
specic symptoms such as dry mouth,20 and their conclusions
highlight that more evidence is needed. Other reviews provide useful data on interventions to address individual functional problems, such as dysphagia or trismus5,21,22 or on specialist oral
rehabilitation/prosthetic interventions, which clearly have a role
in the management of patients with altered oral anatomy.23,24
However, only one review has considered the related nature of
HNC symptoms by identifying interventions to relieve loss of function incorporating both dysphagia and trismus.16 Given the multifactorial nature of HNC treatment side-effects, reviews of
interventions that address the physical, functional and psychosocial complexity of eating and drinking problems are required. The
van der Molen review16 has made an important contribution to
this knowledge base, but its primary focus was on the functional
outcomes of treatment rather than the interventions to relieve
them. Although the review found two studies of interventions in
this area, the search strategy was limited, and it is likely that other
studies exist.
The aim of this review was therefore to examine the nature and
scope of current evidence, by identifying studies of interventions

aimed at alleviating the physical, functional and/or psychosocial


difculties with eating and drinking following treatment for HNC.
The review did not seek studies of nutritional support, surgical
interventions, dental/prosthetic implants or prescription medicines. Rather, the focus of the review was on any rehabilitation
or supportive intervention, which could be implemented by therapists and/or specialist nurses within a rehabilitative clinic setting.
Methods
Search methods for identication of studies
A review of the literature (June 2011) was conducted for all
published articles containing data regarding any rehabilitation
strategies used to alleviate eating problems in patients following
surgery, radiotherapy, or combined treatment modalities for
HNC. Relevant literature was identied by searching three electronic databases through the OVID (Medline) and EBSCO Host (CinAHL and PsycINFO) platforms. Subject headings were mapped
using search terms related to a wide range of different aspects of
eating and drinking. The Boolean operator AND was used to combine the search string with subject headings related to HNC (see
Table 1). No limits or lters were applied.
Data collection and analysis
Identied publications were independently scrutinised by two
reviewers (NC, MW or HL). Publications were either included or excluded according to the criteria outlined in Table 2.
Publications meeting all of the inclusion criteria were retrieved
in full. One member of the research team examined the full-text
copies of the retrieved papers. Consensus was reached following
discussion with a second member of the research team.
The titles of the references of selected articles were then
screened and relevant studies identied. Full-text copies of publications were examined and included if they met inclusion criteria.
The process was repeated using the references of newly identied
publications until no new references were identied.

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.

N. Cousins et al. / Oral Oncology 49 (2013) 387400

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

Does not report data evaluating interventions i.e. not empirical


Relates to surgical, dental/prosthetic implant, interventional radiology or pharmacological interventions or complementary therapies
Focuses on the management of acute oral mucositis
Focuses on the management of xerostomia
Focuses on nutritional support e.g. enteral feeding or dietary guidance
Is a single-autobiographical or non-research based rst-hand account
Focuses on participants under 18 years old
Focuses on end of life care

Expert author searches were also completed in Google Scholar


for two prominent authors in the topic area (Lazarus CL, Logemann
JA). Based on the title, full-text copies of relevant publications were
obtained and a decision was made whether to include or exclude
the paper according to the criteria outlined in Table 2. Review articles were excluded at this stage.
All included publications were arranged according to type of
intervention. Details of intervention, impairment targeted and
key ndings related to the review focus were extracted.
Methodological quality assessment
Studies were assessed for methodological quality according to
individual elements of quality rather than with a summary scale.
For the assessment of quantitative studies (e.g. Randomised Controlled Trials RCTs) the use of such summary scales is not supported by empirical evidence25 and is actively discouraged.26
Methodological components assessed for RCTs and quasi-experimental studies were randomisation, blinding, allocation concealment and reporting of an Intention to Treat Analysis. For casecontrol and cohort studies comparing outcomes in different HNC
groups, the possible presence of selection bias in cases/controls,
and information bias or confounding variables were assessed.
The methodological quality of any case-studies and case-series,
including those which compared outcomes between cancer and
non-cancer groups, was not assessed, accepting that whilst the
information they can convey is useful, the potential for bias and
confounding variables is high and the level of evidence they provide is limited.
Results
Of the 3355 publications identied from the initial search, 73
publications were retrieved in full following screening of the title
and abstract (Fig. 1). Forty-nine of these publications were excluded following examination of the full-text. Five further publications were identied from the initial reference search and 1
additional publication identied from the expert author search.
Five reviews were then excluded. Of the 54 excluded publications,
35 reported non-empirical or review ndings. Two further studies27,28 (both RCTs) published since the search was conducted were
also included.
Of the 27 publications included, 8 were RCTs, 6 were quasiexperimental, 6 were case-control/cohort studies and 7 were case
studies or small case series (Table 3). Tabulation of the assessment
of methodological quality of the RCT and quasi-experimental studies is seen in Table 4. For the RCTs and quasi-experimental studies,

Figure 1 Flowchart of included studies in review.

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-

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Table 3
Summary of included papers.
Author

Year

Country

Swallowing exercises alone


Lazarus
1993 USA

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

Total therapy time


and VF assessed
oropharyngeal
swallow efciency
(OPSE) on liquid and
paste at 1 and
3 months post
treatment

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

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Table 3 (continued)
Author

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)

PEG tube fed

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

NMES for 30 min,


followed by
conventional
rehabilitation
treatment for 30 min,
for 5 days per week
for 2 weeks

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)

Swallowing exercises combined with electrical stimulation


Ryu
2009 Korea
RCT
N = 46
(experimental
n = 21, control
n = 25). Mixed
oropharyngeal
cancer. Intervention
post- curative
surgical and/or RT
treatment

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)

HRP: Twice daily


strengthening
exercises (ROM,
resistance exercises,
tongue hold exercise,
effortful swallow,
shaker exercise) each
repeated 10 times.
(continued on next page)

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Table 3 (continued)
Author

Year

Country

Study type

Swallowing exercises combined with biofeedback


Crary
2004 USA
Retrospective
case note
review

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.

Jaw mobility exercises(with/without mechanical devices)


Grandi
2007 South
QuasiN = 54. Mixed HNC.
America
experimental
Radiotherapy.
Intervention during
treatment

Rose

2009

Canada

Quasiexperimental

N = 45. Mixed HNC.


Radical RT with/
without CT. During
treatment.

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N. Cousins et al. / Oral Oncology 49 (2013) 387400


Table 3 (continued)
Author

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.

Mouth opening (mm)

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

Use of DTS device for


2030 min, three
times per day, with
gradual increases in
time and tension as
tolerated every
2 weeks, for
6 months

Maximal interincisal
distance (MID)

Mechanical devices alone


Shulman
2008 USA

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

Mouth opening (mm)

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

N = 20. Mixed HNC.


Surgery and/or CT
and/or RT.
Intervention posttreatment

Patients
referred for
evaluation and
treatment of
trismus

Dynamic opening
device. (Pain
medications and
botulinum toxin
injections prescribed
as appropriate)

30 min. Three times


per day

Change in maximal
interincisor distance
(MID)

76% tube fed

Verbal or written
instructions on 2

Group 1: Each stretch


exercise repeated 3

Multi-dimensional
assessment protocol:

Swallowing interventions combined with jaw mobility interventions


van der
2011 The
RCT
N = 55, advanced
Molen
Netherlands
(stage 3 and 4) HNC

(continued on next page)

394

N. Cousins et al. / Oral Oncology 49 (2013) 387400

Table 3 (continued)
Author

Year

Country

Study type

Population

Swallowing/
jaw mobility
status

SCC, Pre-, peri- and


postchemoradiation
therapy

Intervention

Schedule

Outcomes measured

rehabilitation
approached:

times and each


strengthening
exercises repeated
ve times. Total of 3
sessions per day
Group 2: Each stretch
exercise repeated
three times per day
and each swallow
exercise repeated
10 times per day, 3
sessions per day

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

N = 190, Mixed HNC.


Curative external
beam RT. Group 1:
Before, during and
after treatment.
Group 2: No early
rehabilitation

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

N = 58. Head and


neck cancer of
oropharyngeal
region Planned for
radiotherapy or
chemoradiation

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

N. Cousins et al. / Oral Oncology 49 (2013) 387400


Table 3 (continued)
Author

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).

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N. Cousins et al. / Oral Oncology 49 (2013) 387400

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

To increase the extent and duration of laryngeal


elevation and prolong cricopharyngeal opening
times
Glossopharyngeus muscle responsible for tongue
base retraction and medialisation of the
pharyngeal constrictors
To improve range and strength of tongue

Shaker67
Sustained hold
Repetitive

To strengthen the suprahyoid muscle complex


(specically the mylohyoid, geniohyoid and
digastric muscles)

Jaw exercises

To improve and retain movement of the


mandible
Provides volitional airway protection

Mendelsohn

62,63

Masako or tongue hold64

Supraglottic swallow or breath hold68


Super-supraglottic swallow

37

Valsalva62 or effortful swallow


Tongue-base retraction65

A technique used when there is reduced closure


of the airway entrance
Increases posterior tongue base movement, to
increase pharyngeal strength
To develop strength in the base of tongue and
reduce vallecular residue

Patient is to hold their tongue between their teeth and swallow hard

Patient is to move tongue up/down, in/out, or side to side against


resistance e.g. a spatula
The patient is instructed to lie on their back, either on the oor or the bed.
Lift their head up so that they can see their toes, but dont lift up their
shoulders. Hold for 1 min, and then rest for 1 min. Repeat three times.
Then lift their head up to look at their toes 30 times quickly
Range of exercises described in Corbin-Lewis et al., 2005 p21565
Patient is to take a deep breath, hold the breath while they swallow then
exhale forcefully with a cough. They then swallow and cough again
Patient is to inhale and hold the breath tightly, bearing down, and
swallow hard, then exhale forcefully with a cough. They then swallow
and cough again
Patient is instructed to swallow hard
The patient is to pull the base of their tongue back towards the posterior
pharyngeal wall with lots of effort and hold it there for a few seconds

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).

Case study/series based-evidence


There were two case studies in this group. The rst35 evaluated
the effects of three swallowing manoeuvres on swallowing function in one HNC patient, using reference values from a small normal population for comparison purposes. The Mendelsohn
manoeuvre (dose and duration unspecied) resulted in a more normalised swallow, improved clearance of bolus, less pharyngeal residue and elimination of aspiration. After 6 months of dependence
on gastrostomy feeding, the patient resumed oral intake. The second36 assessed the effects of four voluntary manoeuvres on tongue
base swallowing function in three post-treatment patients. It
showed that tongue base to pharyngeal wall pressures and contact
duration increased with the use of all exercises, in particular the
Mendelsohn manoeuvre.
A prospective case series37 evaluated the use of super-supraglottic swallow in 9 patients during or after treatment for oropharyngeal malignancy. Overall, this study observed that the supersupraglottic swallow was associated with fewer swallowing disorders, including aspiration.

Case-control/cohort study based evidence


There were two case control/cohort studies. Cavalot et al.30
examined the value of swallowing therapy before and after subtotal laryngectomy for HNC. The time to resumption of swallowing
(days) was signicantly less in those who received pre-treatment
swallowing therapy (16.38 2.9 days) compared to those who only
received swallowing therapy after surgery (27.76 5.2 days)
(p < 0.001; t-test).
The matched case control study31 evaluated the effect of pretreatment swallowing exercises on post-treatment swallow function. Epiglottis inversion was signicantly better maintained in patients receiving pre-treatment swallowing therapy (89% vs. 33%;
p = 0.02; t-test). The position of the tongue base during swallowing
was also signicantly closer to the posterior pharyngeal wall in
these patients (15.2 5.47 vs. 22 6.23; p = 0.025; t-test). There
were no other signicant differences seen on videouoroscopy between the two groups. Maintenance of oral intake was not assessed
and PEG tube use was similar in both groups.

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)

Swallowing exercises with electrical stimulation

N. Cousins et al. / Oral Oncology 49 (2013) 387400

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.

A Dutch retrospective case note review47 studied the effects of


exercise therapy on HNC-related trismus, as compared with trismus from other causes. Mouth opening increased signicantly in
all, but the mean increase in mouth opening in the HNC group
was 5.5 mm, signicantly less than the increase in mouth opening
in the non-cancer group. The authors concluded that HNC-related
trismus is difcult to treat with exercise therapy.

Swallowing exercises with biofeedback

Mechanical devices alone

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.

Four studies (1 cohort, 1 case series and 2 case studies) focussed


on the use of mechanical devices. The retrospective cohort study,48
examined the effectiveness of the Dynasplint Trismus System
(DTS) as part of a multimodal treatment strategy for trismus in patients with HNC. Mouth opening (maximal interincisal distance) in
patients who were compliant with the DTS improved from 16 to
27 mm (p < 0.001; Wilcoxen signed rank test).
A prospective case series49 evaluated the use of the Therabite
device in the early post-operative management of trismus in 11 patients. The average MIO improved signicantly. Four of ve assessable patients had minimal or no limitation on overall quality of life
relative to jaw opening at the end of the intervention. No complications were associated with the use of the device.
A retrospective case study50 aimed to evaluate the effect of the
DTS in patients diagnosed with trismus following radiation therapy, dental treatment, oral surgery or after stroke. There was a statistically signicant increase (mean 13.6 mm) in MID (p < 0.0001;
t = 10.3289; standard deviation = 9.14; 1 way ANOVA) in the HNC
group.
A further case study51 assessed the use of a dynamic opening
device in the treatment of radiation induced trismus in one patient.
The patient experienced little or no difculty in adapting to the
appliance and within approximately 4 weeks, his degree of jaw
movement had increased signicantly.

Jaw mobility interventions


Of eight publications, 4 focussed on jaw mobility exercises with
or without mechanical devices (e.g. Therabite) and 4 on focused on
mechanical devices alone.
Jaw mobility exercises alone
Two publications44,45 evaluated jaw mobility exercises alone.
Both were quasi-experimental studies measuring the degree of
mouth opening following mandibular exercises. Grandi et al.44
compared a control group to the use of two different physiotherapy
exercises designed to prevent trismus. There were no statistically
signicant differences between the two forms of exercise.
Rose et al.45 compared the use of four mandibular exercises
(experimental group) with no jaw exercises (control group). Patients in the experimental group were able to open their mouth
wider than the control group (Wald test; p = 0.01). Furthermore,
there was a persistent deterioration in mouth opening ability 2
3 years after treatment in those who did not perform jaw exercises.
Jaw mobility exercises combined with mechanical devices
There were two studies in this group.46,47 An RCT46 aimed to
compare and evaluate the use of unassisted exercises (group 1),
tongue blades (group 2) and the Therabite Jaw Motion Rehabilitation System (group 3) in post-irradiated HNC patients. The results
demonstrated that at 6 weeks and thereafter, the net increase in
maximal incisal opening (MIO) in group 3 was signicantly greater
than groups 1 or 2 (13.6 mm 1.6 vs. 6 mm 1.8 and 4.4 mm 2.1;
p < 0.05; t-test). Furthermore, the rate of improvement in groups 1
and 2 leveled after 4 weeks whereas the rate of gain in MIO in
group 3 continued at 10 weeks.

Swallowing interventions combined with jaw mobility interventions


Four publications focussed on swallowing and jaw mobility. All
studies were published within the last 2 years and included swallowing exercises and jaw mobility exercises with or without the
addition of a mechanical device. Three of these studies were
RCTs28,52,53 and 1 a quasi-experimental study.54
An RCT published in 201052 aimed to evaluate the effect of rehabilitation therapy on radiation-induced dysphagia and trismus in
nasopharyngeal patients after treatment. The efcacy rate (percentage of patients with excellent or effective results in the water
swallow test) in the rehabilitation group was signicantly higher
than in the control group (77% vs. 43%; p = 0.02; v2). Mouth opening pre- and post-treatment did not change greatly in the rehabilitation group, whereas in the control group it signicantly
decreased post-treatment (Interincisor distance post-treatment
1.1 0.36 cm vs. 1.8 0.56 cm; p = 0.001) and this trend continued
in the following months. The mouth opening efcacy rate was
also signicantly higher in the rehabilitation group (64% vs. 28%;
p = 0.02).
The second RCT53 aimed to assess the effect of (preventative)
rehabilitation on swallowing and mouth opening after concomitant chemoradiotherapy (CCRT). Forty-nine patients were randomised into a standard (swallowing and jaw exercises) or
experimental (standard exercises plus Therabite) arm. A multidimensional assessment protocol was used to evaluate functional
outcomes before and after CCRT, including videouoroscopy,
mouth opening, weight changes, functional oral intake scale and
visual analogue for pain. The authors concentrate on changes in
outcome before and after treatment. Few data were presented
comparing outcomes in randomised groups, with the only signi-

398

N. Cousins et al. / Oral Oncology 49 (2013) 387400

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

weak. The vast majority of studies (n = 18) were conducted in the


USA and the study populations were generally small. Only 8of
the 27 publications identied were RCTs, and several were of poor
quality. The validity and reliability of the evidence summarised in
this review cannot, therefore, be regarded as compelling and it is
not clear whether the results of studies conducted in North America, Australia, Asia and mainland Europe can be extrapolated to
other settings such as the UK. However, this review has identied
a number of important ndings and gaps, with implications for
practice and research.
Whilst acknowledging their methodological limitations, most of
the included studies of swallowing therapy reported some positive
results. In particular, they highlighted a potential role for pre-treatment exercises. The value of adjuncts such as electrical stimulation
and biofeedback is also suggested, but controversy exists around
the specicity of e-stimulation and the quality of current research
in this area.55 The majority of studies also rely on clinician/researcher assessed outcomes to evaluate the effectiveness of swallowing exercises, therefore providing little information on the
impact of swallowing therapy on patients perceptions of everyday
eating and drinking outside the clinical assessment setting. Additionally, the study samples were small and few studies reported
data on the degree to which patients were actually able to undertake the exercises. Given the level of toxicity associated with treatment for HNC and the nature and characteristics of the patient
group, effective compliance strategies and measures need to be
incorporated into studies of this type.
Of the 8 studies evaluating interventions to improve jaw mobility, the majority used mechanical devices (such as Therabite) with
or without jaw exercises. There was some evidence to suggest benet from the use of each of these interventions. Such benet, however, was assessed almost entirely by the degree of mouth opening
achieved (in millimetres). Although dimensions of mouth opening
are clearly an important pre-requisite to eating and drinking, it is
unlikely that such measures are particularly meaningful to patients. None of the studies appeared to take into account the relationship between mouth opening and being able to eat. Again, the
quality of studies was poor, the sample sizes were small and there
was only 1 RCT, published in 1993.46
Three28,53,54 of the four most recent studies evaluated interventions focussing on more than one functional issue, including a combination of swallowing and jaw mobility exercises. All used
patient-reported as well as observer-rated and instrumental measures, providing a more comprehensive picture of the impact of
interventions on outcomes. However, the patient-reported outcome may not match the level of impairment detected on instrumental assessment and this is an important distinction and area
for future research. Although three were RCTs, they were small
and have not yet reported long-term outcome data. Given that an
increasing number of HNC survivors have HPV-related disease
which appears to respond more favourably to treatment, it is vital
that the long-term consequences of cancer therapy are carefully
evaluated. Additionally, the van der Molen53 and Carnaby-Mann28
studies highlight the need for future studies to explore the dose
response effect of high and low intensity interventions.
The study by Ahlberg et al.54 is interesting in that it is the only
study which demonstrates no benet from swallowing and/or jaw
mobility interventions. The authors offer a potential explanation
for this, suggesting that closer and more regular interaction between patients and therapists during and after treatment is
needed. An additional explanation not discussed is that signicantly more patients in the study group received chemotherapy,
and this may account for the poorer than expected outcomes in
those having early self-care rehabilitation.
Overall, the studies included in this review suggest that exercises directed at swallowing and trismus, with or without addi-

N. Cousins et al. / Oral Oncology 49 (2013) 387400

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

Implications for future research

Conict of interest statement

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.
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