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Review Series: Palliation of dyspnea
Nonpharmacological interventionsfor managing respiratory symptomsin lung cancer
Janelle Yorke1, Alison Brettle1 and Alex Molassiotis2
AbstractPatients with lung cancer experience significant symptom burden, particularly symptoms of a respiratorynature. Such symptom burden can be distressing for patients and negatively impact their functional statusand quality of life. The aim of this review is to evaluate studies of nonpharmacological and noninvasiveinterventions for the management of respiratory symptoms experienced by patients with lung cancer. Intotal, 13 studies met the inclusion criteria for this review and included 1383 participants of which 1296were lung cancer patients. The most frequently assessed and reported symptom was breathlessness(n ¼ 9 studies). Cough and haemoptysis were reported in one study. A variety of outcome measurementtools were used and a broad range of intervention strategies evaluated. Lack of consistency betweenstudies impinged on the ability to combine studies. It is not possible to draw any firm conclusion as tothe effectiveness of nonpharmacological interventions for the management of respiratory symptoms inlung cancer. Nonpharmacological interventions may well have an important role to play in themanagement of some of the respiratory symptoms (or combinations of respiratory symptoms), but morework of higher quality is necessary in the future.
KeywordsLung cancer, complementary therapies, breathlessness, cough, nonpharmacological interventions
Introduction
Patients with lung cancer experience significant
symptom burden, particularly symptoms of a respira-
tory nature. The symptom experience can vary widely
among patients and generally is the result of the dis-
ease and its progression or its treatments.1 Respiratory
symptoms, such as breathlessness, cough, wheeze,
haemoptysis and hoarseness are reported by patients
with lung cancer, occurring in 20% to 90% of
patients.2 Such symptom burden can be distressing for
patients and negatively impact their functional status
and quality of life (QOL).3–5
There is limited work in the development and test-
ing of nonpharmacological interventions for the man-
agement of respiratory symptoms. Much of this work
concerns breathlessness, but little or no work exists
in relation to other respiratory symptoms. Breathless-
ness is a complex subjective experience defined as an
uncomfortable awareness or sensation of breathing.6
Breathlessness represents one of the most common and
distressing symptoms in lung cancer.7 Patients with all
stages of lung cancer, who report breathlessness, also
experience a significantly lower QOL,8 and those with
the most severe breathlessness experience more pain
and anxiety.4,8,9 A longitudinal study of 105 patients
with advanced lung cancer demonstrated that breath-
lessness increased overtime, most dramatically during
the first 3 months, while QOL declined over the same
1 School of Nursing, Midwifery and Social Work, University ofSalford, Manchester, UK2 School of Nursing, Midwifery and Social Work, University ofManchester, Manchester, UK
Corresponding author:Alex Molassiotis, School of Nursing, Midwifery and Social Work,Jean McFarlane Building, University of Manchester, Oxford Road,Manchester M13 9LPEmail: [email protected]
Chronic Respiratory Disease9(2) 117–129ª The Author(s) 2012Reprints and permission:sagepub.co.uk/journalsPermissions.navDOI: 10.1177/1479972312441632crd.sagepub.com
period.4 Optimal management of breathlessness
requires a combination of pharmacological and non-
pharmacological interventions.10 The evidence base
for pharmacological interventions has been reported
in several systematic reviews.10,11 These reviews indi-
cate a limited evidence base for the use of opioids for
symptom relief; benzodiazepines to relieve anxiety;
and the use of oxygen. Pharmacological interventions
alone often do not relieve breathlessness adequately
and the use of drugs to treat breathlessness is some-
times limited as they can cause adverse effects and
require careful titrating.10,12 As breathlessness is a sub-
jective experience, nonpharmacological interventions
as an adjunct to drug treatments offer promise for the
management of this distressing symptom.
Cough presents a significant burden for people
with lung cancer and is reported to be present in
40% to 70% of patients with lung cancer at initial pre-
sentation and as the disease progresses.2 Cough may
exacerbate breathlessness13,14 and has a profound
effect on QOL, particularly its psychosocial aspects.5,15
In lung cancer, the aetiology for cough is multifactorial
and can be the result of direct anatomic effects of the
cancer (obstruction), indirect effects of cancer (pleural
effusion or pneumonitis secondary to radiation or che-
motherapy), or underlying chronic conditions (asthma,
COPD and postnasal drip).16,17 There are few manage-
ment options for cough in lung cancer that are evidence
based.18,19 One of the oldest medications for the con-
trol of cough is codeine that suppresses the central ner-
vous symptoms responsible for triggering cough.20
Other pharmacological treatments are largely based
on the use of antitussive drugs (cough suppressants) –
opioids or nonopioids – for which the evidence base is
minimal or conflicting. A Cochrane review of interven-
tions (pharmacological and nonpharmacological) for
cough in cancer concluded that research in this area
was limited with poor quality and significant methodo-
logical problems.18 The Cochrane review reported that
a range of pharmacological treatments (e.g. codeine,
morphine, dihydrocodeine, sodiumcromoglycate and
butamirate citrate linctus – cough syrup) showed some
improvements in cough, although all studies had sig-
nificant risk of bias. Molassiotis et al.18 also included
studies that evaluated the efficacy of invasive treat-
ments, such as brachytherapy and photodynamic ther-
apy, and reported encouraging results. No studies that
evaluated the effectiveness of nonpharmacological and
noninvasive interventions for the management of
cough in cancer were included in the review as no stud-
ies were identified.18 Interventions that encompass a
broad range of psychosocial, behavioural, educational
and environmental strategies may provide a more com-
prehensive approach to ameliorating the effects of this
distressing symptom.
Other respiratory symptoms such as haemoptysis,
hoarseness and wheeze are much less common than
breathlessness and cough. At presentation, up to
20% of patients report mild haemoptysis,21 and
approximately 9% of patients have reported haemop-
tysis in the last 8 weeks of life.22 While much less pre-
valent than breathlessness and cough, haemoptysis
can be alarming for both patients and their families.
Intrusive interventions target bronchial vessels since
these vessels supply the airways and are under higher
pressure than pulmonary arteries. At present, there are
no clinical trials specifically evaluating the efficacy of
these invasive interventions to treat haemoptysis in
patients with lung cancer. Other, less common symp-
toms are also likely to cause distress, such as hoarse-
ness and wheeze, and may also occur as a result of the
cancer or underlying comorbidity such as asthma and
COPD. In the context of lung cancer, it is not known
whether nonpharmacological interventions have a
role to play in ameliorating the distressing effects of
these symptoms.
Given the multitude of respiratory symptoms
patients can experience, alleviating discomfort and
symptom distress often requires several treatment
modalities to reach an acceptable outcome. In addition,
symptom incidence and distress levels may vary over
time and lung cancer treatment, making their manage-
ment challenging. Usually managed as isolated symp-
toms, they often occur simultaneously. It may be that
interventions that include behavioural, psychosocial
and/or educational strategies assist patients to better
cope with distressing symptomology.
The aim of this review is to evaluate studies of
nonpharmacological and noninvasive interventions
for the management of respiratory symptoms experi-
enced by patients with lung cancer. We aimed to
include studies that incorporated a broad range of
interventions including psychosocial, behavioural,
educational, complementary therapies and environ-
mental/service delivery strategies.
Methods
Searches were conducted on a range of electronic
databases, covering a range of perspectives. These
included Medline (Ovid interface; biomedical), Psy-
chinfo (Ovid interface; psychological), Amed (Ovid
118 Chronic Respiratory Disease 9(2)
interface; complementary and allied health, Cinahl
(EBSCO interface; nursing and allied health), Cochrane
Library (Wiley; systematic reviews and randomised
controlled trials (RCTs) in health care). A combina-
tion of thesaurus and free text terms were combined
to maximise sensitivity for the following keywords
including lung cancer, symptoms, psychological
therapies and complementary therapies. No date or
research methodology restrictions were applied.
Studies were included in the review if they were a
report of a RCT or quasi-experimental designs.
Patients of either gender and any age with lung cancer
at any stage, including primary and secondary malig-
nancy, were included. If an article included a hetero-
geneous group, then the study was only included if
greater than 70% of participants had a diagnosis of
lung cancer. We included articles that reported one
or more respiratory outcomes (including breathless-
ness, cough, haemoptysis, wheeze, or hoarseness) as
a primary or secondary outcome. Such outcomes
were required to be reported as a separate outcome,
either on a symptom-specific questionnaire – for
example, a Visual Analogue Scale (VAS)23 or
Numerical Rating Scale (NRS)24 or extracted from
a questionnaire that contains symptom-specific
items (e.g. Symptom Distress Scale (SDS)).25 Due
to the low number of studies that reported single
symptoms, except breathlessness, we extended our
inclusion criteria to include studies that reported
combined/overall symptom scores – this included
studies that only reported, for example, a total score
for the SDS and Rotterdam Symptom Checklist.26
Results
Searches resulted in 1289 records that were uploaded
onto endnote, de-duplicated and filtered for relevance
to the review question. A additional three studies were
located by checking reference lists of relevant systema-
tic reviews. This process resulted in 54 articles that
were further scrutinised for relevance to this review.
Studies were further excluded because they were
reviews or opinion articles (n ¼ 15), case studies or
descriptive studies (n ¼ 11). Other studies were
excluded because the sample was heterogenous or
respiratory symptoms were not grouped. Noncancer
participants or cancer patients with mixed aetiology
or respiratory symptoms were not included as an out-
come measure (n ¼ 10). Further five studies were
excluded because the intervention was not classified
as nonpharmacological.
Description of included studies
In total, 13 studies27–39 met the inclusion criteria for
this review and included 1383 participants of which
1296 were lung cancer patients. Please see Table 1 for
detailed information on the included studies. The
most frequently assessed and reported symptom was
breathlessness (n ¼ 9).27–34,39 Cough was included
as a single outcome measure in one study35 and hae-
moptysis was reported separately in the same study.
No other respiratory symptoms related to lung cancer
were reported as a single outcome measure in any
included studies. Studies included in the review were
categorised and reported in terms of respiratory symp-
tomatology: (a) studies reporting breathlessness as a
single outcome measure; (b) studies reporting cough
as a single outcome measure; (c) studies reporting hae-
moptysis as a single outcome measure; and (d) studies
that reported combined/overall symptom scores.
Breathlessness
Breathlessness was the primary outcome for six
studies27,28,30–32,39 and was a secondary outcome in
three studies.29,33,35 This section presents details
relating to the method of breathlessness assessment
used in the review studies and types of interventions
evaluated, where breathlessness was measured as a
single symptom.
Methods of breathlessness assessment. A variety of
methods were used to assess breathlessness (see
Table 2 for a description of the instruments used). Six
studies used VAS23 and two studies used NRS.24 The
scaling range used for the VAS and NRS measures
was 0–10, except for Chan et al.29 who used 0–100
and Connors et al. who did not specify a scaling range.
The majority of studies measured breathlessness
intensity on a VAS or NRS at ‘best’ or ‘worst’ breath-
lessness over the preceding 24-h period. In a feasibility
RCT, Barton et al.27 used area under the curve analysis
and concluded that the NRS measures of ‘worst’ and
‘average’ breathlessness over the past 24 h were the
most useful assessments. The majority of studies that
applied the VAS and NRS to assess the intensity of
breathlessness also used the same scaling method to
assess distress associated with breathlessness.27,28,30–33
The European Organisation for Research and
Treatment of Cancer–lung cancer quality of life ques-
tionnaire (EORTC-LC13)41 is a multidimensional
QOL instrument that contains three items relating to
breathlessness. Moore et al. used the EORTC-LC13
Yorke et al. 119
Tab
le1.
Char
acte
rist
ics
ofin
cluded
studie
s
Ref
eren
cean
dco
untr
yT
ype
ofst
udy
Inte
rven
tion
Dia
gnost
icgr
oups
Sym
pto
ms/
outc
om
esas
sess
edre
leva
nt
toth
isre
view
Res
ults
Bar
ton
etal
.27
UK
Feas
ibili
tyR
CT
Hig
h(�
3se
ssio
ns)
vs.lo
w(�
1se
ssio
n)
inte
nsi
tytr
ainin
gin
bre
athin
g
Lung
cance
r(n¼
22)
Bre
athle
ssnes
sN
RS;
bri
efC
OPE;
bre
athle
ssnes
sdis
tres
s;H
AD
SN
oef
fect
iven
ess
dat
a:‘w
ors
t’an
d‘a
vera
ge’
pas
t24
hm
ost
use
fulas
sess
men
t
Bre
din
etal
.28
UK
Multic
entr
eR
CT
Nurs
ein
terv
ention
–bre
athle
ssnes
sfo
cus,
musc
lere
laxat
ion,
psy
choso
cial
support
vs.st
andar
dca
re
Lung
cance
r(n¼
119)
Bre
athle
ssnes
sV
AS
–bes
tan
dw
ors
e,an
dre
late
ddis
tres
sR
ott
erdam
Sym
pto
mC
hec
klis
t
Sign
ifica
nt
impro
vem
ent
inbre
athle
ssnes
sbes
t;b/n
ess
dis
tres
s;dep
ress
ion;phys
ical
sym
pto
ms
Chan
etal
.29
Hong
Kong
RC
TPsy
choed
uca
tional
vs.usu
alca
reLu
ng
cance
r(n¼
140)
‘Sym
pto
mcl
ust
er’an
dse
par
ate
bre
athle
ssnes
ssc
ore
son
VA
SSi
gnifi
cant
impro
vem
ent
insy
mpto
mcl
ust
eran
dsp
ecifi
csy
mpto
ms
–bre
athle
ssnes
sC
onnors
etal
.30
UK
Cohort
study
Phys
ioth
erap
y–
teac
hin
gbre
athin
gco
ntr
ol,
rela
xat
ion,en
ergy
conse
rvat
ion
Lung
cance
r(n¼
169),
only
15
com
ple
ted
pro
toco
lBre
athle
ssnes
ssc
ore
son
VA
Sat
wors
tan
dbes
t;an
das
soci
ated
dis
tres
s
Hig
hat
tritio
n,bre
athle
ssnes
sim
pro
ved
but
not
stat
istica
lly
Corn
eret
al.3
1U
KR
CT
Nurs
ein
terv
ention
–co
unse
lling,
bre
athin
gre
trai
nin
g,re
laxat
ion,
copin
gst
rate
gies
vs.co
ntr
ol
(spea
kfr
eely
about
bre
athle
ssnes
sbut
no
trai
nin
gor
counse
lling)
Lung
cance
r(n¼
20)
Bre
athle
ssnes
san
das
soci
ated
dis
tres
son
VA
SSi
gnifi
cant
impro
vem
ents
com
par
edw
ith
the
contr
oli
nbre
athle
ssnes
sat
bes
t(p
<0.0
2)
and
wors
t(p
<0.0
5),
dis
tres
sca
use
dby
bre
athle
ssnes
s(p
<0.0
1)
Fils
hie
etal
.32
UK
Open
pilo
tpre
test
–post
test
Ster
nal
and
L14
acupunct
ure
poin
tsPri
mar
yor
seco
ndar
ylu
ng
cance
r(n¼
20)
Bre
athle
ssnes
s,an
xie
ty,an
dre
laxat
ion
on
VA
SW
ithin
group
sign
ifica
nt
impro
vem
ent
inal
lsy
mpto
ms
atle
ast
up
to6
hpost
tx;
max
imal
at90
min
Hat
ely
etal
.33
UK
Pre
test
–post
test
Spec
ialis
tphys
ioth
erap
yse
ssio
ns
Lung
cance
r(n¼
30)
Bre
athle
ssnes
san
das
soci
ated
dis
tres
sR
ott
erdam
Sym
pto
mC
hec
klis
t
Sign
ifica
ntim
pro
vem
ent(w
ithin
sam
ple
)in
all
VA
Ssc
ore
s,R
ott
erdam
score
s
McC
ork
leet
al.3
4U
SAR
CT
Spec
ialis
thom
enurs
ing
care
vs.
stan
dar
dhom
eca
revs
.cl
inic
care
Lung
cance
r(n¼
166)
Sym
pto
mD
istr
ess
Scal
eSi
gnifi
cant
diff
eren
cein
Sym
pto
mD
istr
ess
Score
Moore
etal
.35
UK
RC
TN
urs
e-le
dfo
llow
-up
vs.co
nve
ntional
med
ical
follo
w-u
pA
dva
nce
dlu
ng
cance
r(n¼
203)
EO
RT
CQ
OL
score
and
lung
cance
rm
odule
–bre
athle
ssnes
s,co
ugh
,hae
mopty
sis
Sign
ifica
ntly
impro
ved
bre
athle
ssnes
sbutnot
cough
and
hae
mopty
sis
at3
month
s,none
at6
month
sPort
eret
al.3
6U
SAR
CT
Car
egiv
er-a
ssis
ted
copin
gsk
ills
trai
nin
gvs
.ed
uca
tion/s
upport
incl
udin
gca
regi
ver
Lung
cance
r(n¼
239)
FAC
T-L
with
bre
athle
ssnes
san
dco
ugh
subsc
ales
Pat
ient:
sign
ifica
nt
impro
vem
ents
infu
nct
ional
wel
l-bei
ng,
sym
pto
ms;
Car
e-gi
ver:
sign
ifica
nt
impro
vem
ents
inan
xie
tyan
dse
lf-ef
ficac
ySa
rna3
7U
SAR
CT
Stru
cture
dnurs
ing
asse
ssm
ent
Lung
cance
r(n¼
48),
new
lydia
gnose
d,nee
dpap
erSy
mpto
mD
istr
ess
Scal
eFa
tigu
ew
asth
em
ost
seve
rely
dis
tres
sing
sym
pto
m;m
ultiv
aria
tem
odel¼
chem
oth
erap
yan
dsy
stem
atic
nurs
ing
asse
ssm
ent
wer
eas
soci
ated
with
less
sym
pto
mdis
tres
sove
rtim
eSk
rutk
ow
skiet
al.3
8
Can
ada
RC
TPiv
ot
nurs
ein
onco
logy
Lung
cance
r(n¼
113)
and
bre
ast
cance
r(n¼
77)
Sym
pto
mD
istr
ess
Scal
e–
no
spec
ific
sym
pto
ms
SDS
–no
sign
ifica
nt
diff
eren
cebet
wee
ngr
oups
Vic
kers
etal
.39
USA
RC
TA
cupunct
ure
vs.pla
cebo
Lung
cance
r80%
;bre
ast
20%
(n¼
47)
Bre
athle
ssnes
s–
NR
SN
oef
fect
–95%
CIe
xcl
udes
the
pre
spec
ified
MC
Dofa
20%
grea
ter
impro
vem
ent
inac
upunct
ure
group
EO
RT
C:T
he
Euro
pea
nO
rgan
isat
ion
for
Res
earc
han
dT
reat
men
tofC
ance
r;FA
CT
-L:F
unct
ional
Ass
essm
entofC
ance
rT
reat
men
t–
Lung
cance
r;M
CD
:Min
imal
clin
ical
diff
eren
ce;N
RS:
Num
er-
ical
Rat
ing
Scal
e;Q
OL:
qual
ity
oflif
e;R
CT
:ra
ndom
ised
contr
olle
dtr
ial;
SDS:
Sym
pto
mD
istr
ess
Scal
e;V
AS:
Vis
ual
Anal
ogu
eSc
ale.
120
Tab
le2.
Inst
rum
ents
use
dto
asse
ssre
spir
atory
sym
pto
ms
Mea
sure
Rev
iew
study
Const
ruct
Var
iable
Scal
ing
range
Conte
nt
Rec
allper
iod
Gen
eral
com
men
ts
Vis
ual
Anal
ogu
eSc
ale
for
bre
athle
ssnes
san
ddis
tres
s23
Bre
din
etal
.28
Unid
imen
sional
Inte
nsi
ty0–10
Bes
t,w
ors
t,av
erag
ePas
t24
hD
istr
ess
0–10
Rel
ated
tobre
athle
ssnes
sC
han
etal
.29
Unid
imen
sional
Inte
nsi
ty0–100
Not
spec
ified
Not
spec
ified
Connors
etal
.30
Unid
imen
sional
Inte
nsi
tyN
ot
spec
ified
Bes
t,w
ors
tN
ot
spec
ified
Dis
tres
sN
ot
spec
ified
Not
spec
ified
Corn
eret
al.3
1U
nid
imen
sional
Inte
nsi
ty0–10
Bes
t,w
ors
t,av
erag
ePas
t24
hD
istr
ess
0–10
Rel
ated
tobre
athle
ssnes
sFi
lshie
etal
.32
Unid
imen
sional
Inte
nsi
ty0–10
Not
clea
rC
urr
ent
Dis
tres
s0–10
Rel
ated
tobre
athle
ssnes
sC
urr
ent
Hat
ely
etal
.33
Unid
imen
sional
Inte
nsi
ty0–10
Bes
t,w
ors
tPas
t24
hours
Dis
tres
s0–10
Not
spec
ified
Num
eric
alR
atin
gSc
ale
for
bre
athle
ssnes
san
ddis
tres
s24
Vic
kers
etal
.39
Unid
imen
sional
Inte
nsi
ty0–10
Ave
rage
for
7day
sC
urr
ent:
bef
ore
and
afte
r1
htr
eatm
ent;
aver
age
dai
lyle
vel
Bar
ton
etal
.27
Unid
imen
sional
Seve
rity
0–10
Ave
rage
,w
ors
tdis
tres
sPas
t24
h;not
spec
ified
Feas
ibili
tyst
udy
–av
erag
ean
dw
ors
tsc
ore
sm
ost
sensi
tive
Sym
pto
mD
istr
ess
Scal
e25
McC
ork
leet
al.3
415-I
tem
sym
pto
mlis
t,pro
vides
ato
tal
score
Deg
rees
ofdis
tres
s1–5:1
(bre
athe
norm
ally
orse
ldom
coug
h)to
5(a
lmos
tal
way
sha
vese
vere
trou
ble
brea
thin
gor
pers
iste
nce
seve
reco
ugh)
One
bre
athle
ssnes
sitem
and
one
cough
item
Feel
ing
late
lySy
mpto
m-s
pec
ific
item
snot
report
edse
par
atel
y,only
tota
lsc
ore
sm
easu
red
Sarn
a37
As
above
As
above
As
above
As
above
As
above
Sym
pto
m-s
pec
ific
item
snot
report
edse
par
atel
y,only
tota
lsc
ore
sm
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and reported separate scores for breathlessness. Like-
wise, the Chronic Respiratory Questionnaire,42 a QOL
instrument for use in chronic respiratory diseases, was
applied in Corner et al.’s31 study, and a separate score
for the dyspnoea subscale was reported in that study.
Multisymptom scales, including the Functional
Assessment of Cancer Treatment–Lung cancer
(FACT-L),40 SDS,25 and the Rotterdam Symptom
Checklist,26 were also used in studies included in this
review but separate scores for breathlessness were not
provided (see Table 2). Breathlessness is a multidi-
mensional experience and consists of different sensa-
tions with different intensities,10 yet no study
included in this review applied a measure to reflect
the entirety of this symptom.
Description of interventions with breathlessness as adiscrete symptom. A variety of interventions aimed at
improving the patient’s experience of breathlessness
were included in this review. Interventions for breath-
lessness were difficult to categorise as many of the
interventions included more than one component,
provided by various professionals and in different
settings. Therefore, categories were grouped accord-
ing to the main mode of treatment delivery and
included (a) multimodal interventions with a nursing
focus; (b) multimodal interventions with a phy-
siotherapy or multiprofessional focus; and (c) acu-
puncture/acupressure.
1. Multimodal interventions with a nursing focus
Three studies were included that evaluated interven-
tions that consisted of a broad range of psychosocial,
educational and behavioural strategies, included a
specific measure of breathlessness, and were led by
nurses.28,31,35 The intervention strategies used across
these studies were reasonably similar, with each study
including elements of relaxation techniques, counsel-
ling and anxiety management.
The seminal studies by Corner et al.31 and Bredin
et al.28 tested the combination of a nurse-led multimo-
dal intervention that combined breathing and relaxa-
tion training, counselling and teaching coping and
adaptive strategies. Both studies included the inten-
sity of breathlessness as the primary outcome mea-
sured on a VAS, 0–10 scaling range. In Corner’s
feasibility study, 34 participants with lung cancer
were included of which 19 were randomized to the
intervention and 15 to the control group.31 The inter-
vention group attended weekly sessions with a nurse
practitioner over 3–6 weeks. Breathlessness at ‘rest,’
at ‘worst,’ and distress caused by breathlessness were
reduced over time in the intervention group but not in
the control group.31 The feasibility study was
stopped early since the intervention group showed
a clear benefit.
The subsequent adequately powered trial28
included 119 participants of which 103 were included
in the final analysis. The intervention was similar
between the two studies; however, in Bredin’s study
the intervention strategy was tailored to individual
patient’s needs.28 This included detailed assessment
of the meaning of breathlessness and factors that con-
tribute or help to relief it. The intervention strategy
also incorporated supportive measures for patients’
family members. After 8 weeks, the intervention
group showed significant improvement in breathless-
ness at ‘best’ but there was no significant improve-
ment in breathlessness at ‘worst’ or distress caused
by breathlessness.
Moore et al.35 examined the effects of a nurse-led
follow-up service compared to conventional medical
follow-up. The nurse-led intervention consisted of
clinical assessment, access to the nursing clinics and
communication with the general practitioner and pri-
mary care team. Participants randomized to the inter-
vention were allocated to one of two clinical nurse
specialists and were assessed monthly to identify
signs of disease progression, symptoms warranting
intervention, or serious complications. The nurse spe-
cialists provided information and support and coordi-
nated input from other services. Breathlessness was
measured41 using EORTC-LC13 and separate breath-
lessness scores were provided. Three months after
study commencement, participants rated their breath-
lessness severity significantly less severe than partici-
pants in the conventional follow-up. There was no
difference in breathlessness after 6 months but again
there was a significant difference after 12 months.
In addition, participants in the intervention group had
significantly improved scores for emotional function-
ing and treatment satisfaction was significantly higher
in the intervention group for both patients and carers.
A nurse-delivered psychoeducational intervention
was tested by Chan et al.29 in Hong Kong. The inter-
vention group received a 40-min education session on
symptom management and coaching in the use of pro-
gressive muscle relaxation delivered 1 week prior to
commencing radiotherapy, and repeated after 3
weeks. The intervention was delivered by registered
nurses who had attended a 2-day training session
focusing on the educational package and practice of
122 Chronic Respiratory Disease 9(2)
progressive muscle relaxation. Symptom data were
collected prior to the intervention, 3 weeks, 6 weeks
and 12 weeks postintervention. A total of 140 patients
consented to participate in the study and the overall
attrition rate at week 12 was 27%, with the sole reason
being attributed to death. Breathlessness was one of
the primary outcomes and was measured on a
100 mm VAS. The study aimed to assess the efficacy
of the psychoeducational intervention on symptom
clusters in lung disease – breathlessness, fatigue and
anxiety. We discuss the specific outcomes for breath-
lessness intensity measured on the VAS here. There
was a significant improvement in breathlessness
intensity scores between the 2 study groups at week
6 and week 12, although the effect sizes were small
(partial Z2 ¼ 0.04 and 0.043, respectively).43
2. Multimodal interventions with a physiotherapy
or multiprofessional focus
Two nonrandomised studies30,33 assessed
physiotherapy-led multimodal interventions for
patients with lung cancer. In a single-centre study,
Hately et al.33 evaluated an intervention strategy for
patients with lung cancer including physiotherapist-
led reviews in a specialist outpatient breathlessness
clinic. Patients were monitored by the senior phy-
siotherapists at 3 sessions, each lasted a maximum
of 90 min, over a period of 4–6 weeks. The interven-
tion consisted of a range of strategies, including
breathing retraining, relaxation techniques, activity
pacing and psychosocial support. Compared to other
studies included in this review, the inclusion of a
specific-activity pacing component was a unique
feature of this intervention. Forty-five patients partici-
pated in the pretest–posttest study, of whom 15 (33%)
deteriorated or died before completion – results refer
to the 30 patients who were able to complete the entire
study period. Patient-reported outcomes included a
VAS for breathing at worst and at best in the preced-
ing 24 h as well as the distress caused by breathless-
ness. There was a statistically significant
improvement in all VAS breathlessness outcomes
from pre- to postintervention. These results should
be interpreted with caution due to the small and non-
randomised sample.
Over a 4-year period, Connors et al.30 evaluated a
physiotherapist-led breathlessness programme for
patients with intrathoracic malignancies. The pro-
gramme consisted of an individual 1-h session on 4
consecutive weeks and a review session 1 month later.
The sessions involved a broad range of strategies
including breathing control, relaxation, anxiety man-
agement, energy conservation, goal setting and life-
style readaption. This programme suffered high
attrition – 160 patients were recruited at baseline, but
only 14 completed the programme. The investigators
acknowledged that patient selection was the likely
reason for the high dropout, since the sample was
selected from the entire lung cancer population which
included the frail and patients receiving cancer treat-
ments. In contrast, similar studies included patients
who had completed active cancer treatments.28,31
Connors et al.30 reported nonsignificant changes in
breathlessness measured on a VAS for breathless-
ness at best and at worst, distress caused by breath-
lessness, and the dyspnoea subscale of Chronic
Respiratory Questionnaire.42
The feasibility of high- versus low-intensity train-
ing in breathing techniques for breathless patients
with lung cancer delivered by a specialist phy-
siotherapists or lung cancer specialist nurse was tested
by Barton et al.27 This was a single-centre, non-
blinded RCT designed to assess recruitment and
retention, best end point and variability of breathless-
ness scores to inform a subsequent powered study.
The intervention consisted of training in diaphrag-
matic breathing, pacing, anxiety management and
relaxation during an hour-long clinic session. The
control group (low intensity) received the session
once and the intervention group (high intensity)
received subsequent sessions at weeks 2 and 3. Both
groups also received written and DVD reinforcement
material and a telephone call from their therapist a
week after the last training session. Because this was
a feasibility study, no primary or secondary outcome
measures were assigned. Breathlessness was
recorded on a NRS for worst, average and now, dis-
tress caused by breathlessness and coping with
breathlessness. Over a 12-month period, 22 patients
were randomised with a 40% dropout rate by week
4. From this study, it was concluded that the most
useful NRS scores for breathlessness severity were
for worst and average over past 24 h.
3. Acupuncture/Acupressure
In this category, two studies were included – one was
an RCT39 and the other was an open pilot study with
no randomisation exploring the safety and efficacy of
acupuncture.32 Vickers et al.39 used a single session of
acupuncture or placebo followed by true or placebo
Yorke et al. 123
acupressure. True treatment points were chosen on the
basis of traditionally used points for breathlessness.
Placebo points were allocated in body areas away
from true acupressure points. Following the single
acupuncture session, participants were requested to
apply pressure to semipermanent acupressure studs
by making small circular movements with fingers – the
study protocol recommended 2 or 3 cycles per second
for 1 or 2 min per point. The subjective sensation of
breathlessness was assessed with a NRS (0–10) imme-
diately before and after acupuncture treatment and
daily for a week thereafter. In this study, 47 partici-
pants were randomized and 45 provided follow-up
data. Participants in the acupuncture/acupressure and
control group improved, but there were no differences
between the groups at 7 days.
In the second acupuncture study, 20 patients whose
breathlessness was directly related to primary or sec-
ondary malignancy underwent a single acupuncture
session using sternal and L14 acupressure points.32
Breathlessness and anxiety were rated by patients
using pre and post VADS (- 10) treatment. There was
a significant improvement in VAS scores for breath-
lessness and anxiety at least up to 6-h postacupunc-
ture, which were maximal at 90 min. A reduction in
respiratory rate was also reported, which was sus-
tained for 90 min postacupuncture.
Cough
There was no study identified that reported cough as
the primary outcome measure. Only one study
reported a specific cough outcome. In an RCT, Moore
et al.35 applied the EORTC-LC13 which41 includes
one item that refers to the frequency of cough in the
past week. Responses for this single item were
reported 3, 6 and 12 months following either nurse-
led follow-up or conventional medical follow-up.
There was no significant improvement in the single
cough item in the nurse-led follow-up group com-
pared to conventional group at any of the three post-
randomisation follow-up points.
Haemoptysis
There was no study identified that reported haemopty-
sis as the primary outcome measure. As with cough,
Moore et al.35 provided the only measure of haemop-
tysis. The EORTC-L13 contains41 one item that
assesses how often participants coughed up blood in
the past week. In that study, the scores for haemopty-
sis at each data collection point were zero.
There was no study that identified the reported
outcome measures for less common respiratory symp-
toms in lung cancer, such as wheeze and hoarseness.
Trials with combined/overall symptom scores
Four studies applied an instrument that assessed a
range of symptoms and associated distress and
reported total scores only, that is, no specific symp-
tom either measured by a single item or subscale was
provided.34,36–38 In this section, we present these stud-
ies because each of the instruments used contain at
least one item that represents the experience of breath-
lessness, cough, or haemoptysis. None of these instru-
ments record experience of less common respiratory
symptoms of hoarseness and wheeze.
The SDS25 was used in an RCT to test the effects of
three home care treatment regimens on the psycholo-
gical well-being of patients with lung cancer.34 The
three treatment groups included standard home care;
specialised oncology home care; and an office care
group who received standard care by the physician.
The specialised oncology intervention was delivered
by specialised cancer nurses. The SDS measures the
patients’ perceived level of distress in response to 13
symptoms, including breathlessness, cough and hae-
moptysis.25 A total of 166 patients were randomised
and 78 completed 4 interview points and were
included in the final analysis at 12 weeks. There was
a significant improvement in symptom distress in the
two nursing home programmes compared to the
office care group.
Sarna37 tested the effectiveness of structured nur-
sing assessment of symptom distress in patients with
advanced lung cancer compared to usual care. Both
groups (N ¼ 48) completed the SDS25 every month
for a 6-month period. In a multivariate model, che-
motherapy and systematic nursing assessment were
associated with less symptom distress over time.
Skrutkowski et al.38 conducted an RCT to test the
impact of a ‘pivot’ nurse in oncology on symptom dis-
tress experienced by patients with lung cancer
(n ¼ 113) or breast cancer (n ¼ 77). The intervention
consisted of an experienced palliative care nurse who
had received additional training in symptom manage-
ment. The pivot nurse conducted an in-depth assess-
ment of the patient’s symptom burden, family and
support situation, provided training for symptom
management, additional support and initiated
follow-up telephone calls. No significant difference
in SDS scores between the two groups was found.
124 Chronic Respiratory Disease 9(2)
The efficacy of a caregiver-assisted coping skills
training was tested in an RCT involving 233 patients
with lung cancer and their caregivers.36 Two condi-
tions were tested in this study: caregiver-assisted cop-
ing skills training and an education/support condition.
The caregiver training condition included training on
symptom management where the caregiver’s role was
described as that of a ‘coach,’ with the goal of helping
the patient learn and apply coping skills. The second
condition included the provision of information
regarding lung cancer and its treatment. Both patients
and caregivers were involved in session for both condi-
tions. The FACT-LC13 was used to assess symptoms40
from the patients’ perspective. The FACT-LC13 con-
sists of items assessing shortness of breath and cough-
ing. Patients in both treatment conditions showed
improvements in the FACT-LC13 scores. Exploratory
analyses suggested that the caregiving-coping inter-
vention was more beneficial to patients with stage II
and III cancers/caregivers, whereas the education/
support intervention was more beneficial to patients
with stage I cancer/caregivers.
Discussion
This review of the effectiveness of nonpharmacologi-
cal interventions for improving the experience of
respiratory symptoms in patients with lung cancer
found that interventions have largely focused on
breathlessness and reflect a broad range of strategies.
Given the multitude of respiratory symptoms patients
with lung cancer can experience, alleviating symp-
tom burden often requires several treatment modal-
ities. Thirteen studies were included in this review
although only one of these assessed cough and hae-
moptysis as distinct symptoms.
Measurement issues
Breathlessness is the most commonly reported
respiratory symptom in patients with lung cancer.7
There is no gold standard measure currently available
that has been validated to capture this multifaceted
construct.44 In this review, the VAS and NRS were
mostly used to measure breathlessness. It has been
suggested that, in the absence of a gold standard
all-encompassing measure for breathlessness, these
unidimensional, single-item scales be used for the
assessment of breathlessness in palliative care44 and
advanced disease.10 There are limitations to their use.
Both VAS and NRS scales have two anchors that are
unique to each individual, making comparison
between people difficult.10,45 There are no apparent
standard principles to regulate their consistent use:
they have been adapted to measure different aspects
of breathlessness, such as ‘uncomfortable breathing,’
‘severity of breathlessness,’ ‘intensity of breathless-
ness,’ ‘best,’ ‘worst,’ ‘average’ and so on as well as
difference in scaling ranges (e.g. 0–10 or 0–100), and
different recall period (e.g. now, today, or past
24-hours). This makes comparisons between studies
problematic. In our review, it was not possible to
combine the results from individual studies in any
meaningful way to obtain an overall effect size for
studies that evaluated similar interventions and
included a VAS or NRS for breathlessness assessment.
Because breathlessness is highly correlated with anxi-
ety and distress, some authors applied a VAS to capture
‘distress’ associated with breathlessness.27,28,30–33
Studies that reported breathlessness as a single item
extracted from of a list of symptoms (e.g. SDS25) are
also limited to the quantification of symptom fre-
quency and intensity only.
There is evidence that breathless patients use a
variety of descriptors to describe the experience of
breathlessness and that these descriptors represent
sensory quality and affective dimensions of breath-
lessness. In this review, no study included a unified
measure of breathlessness that reflects its multidimen-
sionality. The Dyspnoea-12 is a recently developed
instrument46 that captures the sensory quality ‘physi-
cal’ and emotional dimensions of breathlessness. It
consists of 12 items, each ranging from 0 ‘none’ to
3 ‘severe’, 7 items measure the patient’s physical per-
ceptions of breathlessness and 5 items measure affect.
It has been reported as a valid and reliable measure of
breathlessness in patients with cardiac46 and respira-
tory conditions,47–49 but it is yet to be validated for
use in lung cancer.
In this review, no study included a specific instru-
ment to measure cough, haemoptysis and other less
common respiratory symptoms. Since cough is fre-
quently reported in the lung cancer population,7 its
inclusion as a specific outcome measure in studies
designed to assist patients to better cope with distres-
sing symptomology warrants greater attention.
Recently, a cough scale has been developed for use
with lung cancer patients and could be used as an out-
come for such trials, focusing on cough.50 Given the
broad range of strategies applied in the interventions
included in this review, it is likely that any resilience
and coping mechanisms adopted by study participants
are likely to influence patients’ perceptions of the
Yorke et al. 125
burden of multiple symptoms and not just breathless-
ness. One study35 did report a separate score for cough
and haemoptysis extracted40 from the EORTC-LC13.
This practice is not ideal because the instrument was
not designed to provide individual symptom scores
but a combined score for the lung cancer module.
Other studies reported total scores that incorporate a
variety of symptoms including the SDS25 and Rotter-
dam Symptom Checklist.26 Such lists are useful for
providing overall scores of symptom burden, although
it is difficult to discern the full experience and impact
of prominent symptomatology, notably breathlessness
and cough, with such lists.
Studies involving patients with lung cancer suffer
from high attrition. Limiting participant research bur-
den plays a key role in successful study recruitment
and retention. Introducing a battery of questionnaires
for every possible symptom, both respiratory and oth-
erwise, is not a viable option. This presents a chal-
lenge for lung cancer researchers to strike a balance
between adequately capturing patient-related out-
comes and patient burden. The choice of the most
appropriate symptoms to include as specific study
outcomes and the instruments used to capture these
depend on the focus on the intervention and desired
outcomes. It would appear that at the least, breathless-
ness and cough warrant inclusion as specific outcome
measures, but it is equally important that the multidi-
mensionality of these symptoms is captured. It is
likely that the broad range of strategies used in the
interventions included in this review will have great-
est impact on affect and ability to cope with distres-
sing symptoms rather than severity only. As noted
by Bausewein et al.,10 studies to date have largely
focused on the management of symptoms rather their
assessment. To gauge the benefits of interventions
that require significant health care resources and com-
mitment from patients and their families, measure-
ment tools that reflect the experience of symptoms
in lung cancer, and are sensitive enough to detect
change in response to interventions need to be
applied.
Interventions
The interventions evaluated in this review covered a
broad range of strategies. The variability and incon-
sistent use of interventions for respiratory symptoms
are also evident in clinical practice, as shown in a
UK survey of respiratory management practices.51
Since the focus of this review was to evaluate
nonpharmacological interventions for respiratory
symptoms in lung cancer, we categorised studies
according to symptoms: breathlessness, cough and
haemoptysis. As evidenced in this review, to date
breathlessness has been the area of focus for research
in the area of nonpharmacological interventions. We
elected to further categorise these studies according
to the mode of delivery. The majority of these studies
included a multimodal intervention that was delivered
by nurses.28,29,31,35 Taking account of sample size,
dropout rate, outcome measures and repeatability of
interventions, feasible interventions emerge from a
few nurse-led therapies.28,29,35 The interventions
evaluated in these three studies had some common
foundations including a focus on breathlessness man-
agement, psychological support and an element of
patient education. However, key difference also exists
in relation to the extent that interventions were tai-
lored to the needs of individual patients, context of
comparison groups and functional state of patients
at recruitment. Additionally, Bredin et al.28 and Chan
et al.29 measured breathlessness on a VAS but used
different anchor descriptors and different scaling
ranges, and Moore et al. extracted single scores for
breathlessness, cough and haemoptysis from items
located on the FACT-LC.42 Based on these results,
no definitive conclusion for the effect of nurse-led
multimodal interventions could be made.
Two studies reflected the interventions led by phy-
siotherapist but these were nonrandomised.30,33 Simi-
lar to the nurse-led studies, these interventions
included a broad range of strategies. It is not possible
to draw any firm conclusions from these studies due
to the weak methodological approaches used, the small
sample size included in Hately et al.33 study, and the
remarkably high dropout rate experienced by Connors
et al.30 where 160 patients were recruited at baseline
yet only 14 completed the programme. Explanations
for the high dropout rate are provided by the authors,
including broad inclusion criteria and subsequent fragi-
lity of participants and many were receiving cancer
treatments. This study is important because it high-
lights important considerations when developing study
protocols for interventional studies including patients
with lung cancer. The nonstatistical result drawn from
these studies is likely to reflect inherent methodologi-
cal flaws as opposed to the mechanism of intervention
delivery by physiotherapists.
Complementary and alternative medicine use has
become increasingly popular throughout the Western
world, as patients seek supplemental strategies to
126 Chronic Respiratory Disease 9(2)
medical care.52 We located two small studies that
evaluated the effect of acupuncture in a nonrando-
mised study32 and a single acupuncture session fol-
lowed by acupressure in an RCT.39 Although Filshie
et al.32 describe a significant within-group improve-
ment in breathlessness up to 6 h postintervention,
the lack of a control group limits the applicability of
the results. Vickers et al.39 found no difference in
reported breathlessness between acupuncture and pla-
cebo groups. The timing of assessment was also dif-
ferent in the two approaches described, and it may
be that acupuncture has only short-lived effects. In the
context of management of respiratory symptoms for
people with lung cancer, no recommendations for
acupuncture can be made.
To our surprise, only one study,35 a nurse-led mul-
timodal intervention, assessed cough and haemopty-
sis. No difference in cough experience was found
between the intervention and control groups. Hae-
moptysis was the single symptom in that study, which
no patients reported and the pre- and postintervention
scores were zero. It is difficult to gauge the true mean-
ing of these results since the symptoms were assessed
as part of the EORTC41 instrument.
Due to the lack of studies that included specific
respiratory symptoms, we elected to review studies
that only included a total score from symptom lists.
Three studies measured symptoms on the SDS to eval-
uate the efficacy of a nurse-led intervention.34,37,38
Although the same outcome measure was used in these
studies, the intervention strategies and comparison
groups were varied. Positive results were reported in
two of these studies,34,37 but it was not possible to com-
bine studies due to the differences between the studies.
The FACT-LC41 was used to assess the effect of pro-
viding caregivers of people with lung cancer specific
training in coping skills. The positive outcomes
reported for the caregiver-assisted coping skills train-
ing group provide promise for the involvement of care-
givers in nonpharmacological interventions. Because
these studies did not include any outcome measures for
single symptoms, it is not possible to assess the relative
effect of these interventions.
Conclusions
Lung cancer carries significant mortality and morbid-
ity. Management of distressing respiratory symptoms
is complex. There is a need to provide patients with
viable options to help them better cope with lung
cancer symptomatology. The evidence related to
nonpharmacological interventions to help address this
need has been reviewed in this article. The majority of
studies refer to breathlessness or a list of multiple
symptoms. The interventions included in this review
mostly included a broad range of strategies. Based
on these facts, it is not possible to draw any firm con-
clusion as to the effectiveness of nonpharmacological
interventions for the management of respiratory
symptoms in lung cancer. Nonpharmacological inter-
ventions may well have an important role to play in
the management of some of the respiratory symptoms
(or combinations of respiratory symptoms), but more
work of higher quality is necessary in the future.
Funding
This research received no specific grant from any funding
agency in the public, commercial, or not-for-profit sectors.
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