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SYSTEMATIC REVIEW
Peninsula College of Medicine & Dentistry, Primary Care Research Group, Institute of Health Services Research, Exeter, Devon, UK
Cochrane Airways Group, St Georges, University of London, London, UK
Chinese Cochrane Centre, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Submitted 9th September 2009; revised 28th April 2010; accepted 12th May 2010; online 18th July 2010
Abstract
Aims: To assess the efficacy of herb and plant extracts in the management of asthma.
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Method: Systematic review and meta-analysis. Multiple database searches identified randomised placebo controlled trials of herbal
interventions reporting at least one primary outcome measure. Where possible data were combined for meta-analysis. Primary outcome
measures were lung function, exacerbations and reduction in corticosteroid use. Secondary outcome measures were symptoms and
symptom scores, use of reliever medications, changes in rates of consultation and adverse effects.
Results: Twenty-six studies reporting on 20 herbal preparations were included. Two of six studies reporting change in FEV1 were positive.
Little data was available on frequency of exacerbations. For primary outcomes single studies of Boswellia, Mai-Men-Dong-Tang,
Pycnogenol, Jia-Wei-Si-Jun-Zi-Tang and Tylophora indica showed potential to improve lung function, and a study of 1.8-Cineol (eucalyptol)
showed reduced daily oral steroid dosage.
Conclusions: Improvements in symptoms were not strongly supported by objective changes. Most trials were of small sample size, short
duration, and poor methodology. Further adequately powered trials are needed to assess these compounds. Such trials should conform
to CONSORT guidance, report standardised spirometry, and use validated symptom and severity scores. No recommendations for herbal
treatment of asthma can be made from the current evidence.
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Introduction
The use of complementary or alternative medicine (CAM) is
widespread in asthma. Only 41% of UK asthma sufferers have
not used CAM and of those two-thirds would consider using it
in the future.1 Herbal remedies are a consistently popular form
of CAM in asthma1-3 and proprietary asthma drugs are derived
from herbal remedies for example, ephedrine was developed
from the traditional Chinese remedy 'ma huang', and tea
leaves are the herbal origin of theophylline.4 Caffeine, related
to theophylline, has been used for centuries to treat asthma
* Corresponding author: Dr Christopher Elles Clark, Peninsula College of Medicine & Dentistry, Primary Care Research Group, Institute of Health
Services Research, Smeall Building, St Lukes Campus, Magdalen Rd, Exeter, Devon, EX12LU, United Kingdom
Tel: +44 (0)1884 860205 Fax: +44 (0)1884 860887 Email: christopher.clark@pms.ac.uk
PRIMARY CARE RESPIRATORY JOURNAL
www.thepcrj.org
doi:10.4104/pcrj.2010.00041
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Searching
#1 ASTHMA (MeSH)
#2 asthma*
#3 wheez*
#4 bronchospas*
#5 bronch* NEAR spas*
#6 bronch* NEAR constrict*
#7 bronchoconstrict*
#8 #1 or #2 or #3 or #4 or #5 or #6 or #7
#9 MEDICINE, HERBAL (MeSH)
#10 PLANT PREPARATIONS (MeSH)
#11 PLANTS, MEDICINAL (MeSH)
#12 PHYTOTHERAPY (MeSH)
#13 MEDICINE, TRADITIONAL (MeSH)
#14 herb*
#15 plant*
#16 phyto*
#17 botanic*
#18 tradition* NEAR medicine*
#19 chinese* NEAR medicine*
#20 ayurvedic*
#21 kampo*
#22 #9 or #10 or #11 or #12 or #13 or #14 or #15 or #16 or
#17 or #18 or #19 or #20 or #21
#23 #8 AND #22
Methods
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Inclusion criteria
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(CEC & EA). Potentially relevant trials were identified from title,
abstract and keywords and we retrieved the full texts to assess
studies for inclusion, obtaining translations where necessary.
Data were extracted independently by two authors (CEC & EA)
using a standard data extraction form and disagreement was
resolved by discussion and/or the third author (TJL). Trialists were
contacted for further information and unpublished data if
necessary, and data were estimated from graphs presented in
two RCTs.13,14 Data were entered into Review Manager
software15 by one author (EA) and checked for accuracy by
another (TJL).
Risk of bias was assessed in terms of generation of the
randomisation sequence, allocation concealment, and blinding
as adequate, uncertain or inadequate using Cochrane criteria.16
Data analysis
Separate analyses were conducted for each type of herbal
preparation against placebo. Treatment effects were
calculated as the relative risk (RR) with 95% confidence
intervals (95%CI) for dichotomous data. For continuous data,
we calculated mean difference (MD) with 95% confidence
intervals for outcomes reported in the same scale, and a
standardised mean difference (SMD) with 95% confidence
intervals for outcomes reported in different scales. Analysis
employed a fixed-effects model in comparing sub-groups of
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Results
Records screened
(n=2757)
Records excluded
(n=2535)
Full-text articles
excluded, with reasons
(n=226)
Description of studies
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Studies included in
qualitative synthesis
(n=26)
Studies included in
quantitative synthesis
(meta-analysis)
(n=25)
No placebo (160)
Not RCT or quasi
RCT (30)
Not stable asthma (17)
Not reporting primary
outcome (8)
Duplicate
publication (5)
Not a herbal study (4)
Intervention was
smoking (1)
Not a human trial (1)
Methodological quality
Primary outcomes
The majority of studies reported no significant differences in
measures of lung function or corticosteroid dosage. Individual
studies showed significant differences in measures of FEV1 for
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Name
Ingredients or origin
Traditional Chinese
Medicines
Mai-Men-Dong-Tang
Liu-Wei-Di-Huang-Wan
Shen-Ling-Bia-Shu-San
Jai-Wei-Si-Jun-Zi-Tang
Ding Chuan Tang*
Tylophora indica
Devadaru compound
Indian
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Pulmoflex
Herbal compound
DCBT4567-Astha-15
TJ-96 "Saiboku-to or
Chai-pu-tang
Other
Borage
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Japanese
0%
Yes (low risk of bias)
25%
50%
Unclear
75%
100%
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Figure 3. Tylophora indica vs. placebo, symptom score improvement >50% (week 1).
Treatment
Study or Subgroup
Events Total
Control
Events Total
Risk ratio
Risk ratio
Weight
Gupta 1979
18
71
11
64
39.8%
Mathew 1974
34
59
15
64
60.2%
128
100.0%
130
52
26
0.2
0.5
Favours treatment
Favours control
15
64
24.0%
33
53
16
57
27.0%
58
103
29
92
49.0%
213
100.0%
34
Shivpuri 1969
Shivpuri 1972
Total (95% CI)
Total events
215
125
Events Total
Weight
59
Mathew 1974
Risk ratio
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Events Total
Risk ratio
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Study or Subgroup
Control
Treatment
Figure 4. Tylophora indica vs. placebo, total clinical improvement >50% (week 1).
60
0.2
0.5
Favours control
Favours treatment
Secondary outcomes
Symptoms
Medication use
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Adverse effects
Pooled data for three studies of Tylophora indica showed that
significantly more study than control subjects reported side
effects after one week (RR 3.94; 95%CI 2.26 to 6.86,
p<0.001, n=428, Figure 5);25,36,37 they reported loss of salt
taste, sore mouth, abdominal pain, nausea and vomiting. A
further study of tylophora not included in the analysis
reported similar side effects.21 Gastrointestinal side effects
were also reported with Boswelia (nausea, epigastric pain and
hyperacidity),22 1.8-cineol (eucalyptol) (heartburn and
gastritis),30 Traditional Chinese Medicine (TCM) (abdominal
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Figure 5. Tylophora indica vs. placebo, number of patients experiencing side effects (week 1).
Treatment
Study or Subgroup
Events Total
Mathew 1974
11
Shivpuri 1969
Shivpuri 1972
Risk ratio
Risk ratio
Weight
59
64
20.5%
28
53
57
40.3%
17
103
92
39.2%
213
100.0%
Control
Events Total
215
56
14
0.1
0.5
10
Favours control
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0.2
Favours treatment
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Discussion
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Conclusions
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None known.
Acknowledgements
We are grateful to Vasiliy Vlassov for translating the Russian paper, to Dorota Olszak
for translating the Polish paper, to Veronica Stewart of the Cochrane Airways Group,
and to Eric Manheimer of the Cochrane Complementary Health Field helped in
obtaining full-text papers. We also thank Carl Hederos and Eman Haggag who
supplied further information on their studies.
Funding sources
EA and TJL were funded by St Georges, University of London UK, and CEC was
funded by Peninsula College of Medicine and Dentistry/ Plymouth teaching PCT UK.
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30. Juergens UR, Dethlefsen U, Steinkamp G, Gillissen A, Repges R, Vetter H. Antiinflammatory activity of 1.8-cineol (eucalyptol) in bronchial asthma: A doubleblind placebo-controlled trial. Resp Med 2003;97(3):250-6. http://dx.doi.org/
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31. Ebden P, Bevan C, Banks J, Fennerty A, Walters EH. A study of evening primrose
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34. Lee DKC, Haggart K, Robb FM, Lipworth BJ. Butterbur, a herbal remedy, confers
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37. Shivpuri DN, Singhal SC, Parkash D. Treatment of asthma with an alcoholic
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38. Thiruvengadam KV, Haranath K, Sudarsan S, et al. Tylophora indica in bronchial
20. Gabrielian ES, Narimanian MZ, Aslanian G, Amroyan EA, Panossian AG. A
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41. Blanc PD, Kuschner WG, Katz PP, Smith S, Yelin EH. Use of herbal products,
coffee or black tea, and over-the-counter medications as self-treatments
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42. Begg C, Cho M, Eastwood S, et al. Improving the quality of reporting of
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25. Mathew KK, Shipvuri DN. Treatment of asthma with alkaloids of tylophora
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Participants &
inclusion criteria
Study
Badria 2004
(Egypt)18
Chan 2006
(Taiwan)19
Ebden 1989
(UK)31
Gabrielian
2004
(Armenia)20
Guinot 1987
(France)32
Gupta 1979
(India)21
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Double-blind placebo
controlled randomised trial.
Placebo contains
Ipecacuanha to mask side
effect of nausea &
vomiting. Treatment group
given powder of 200mg
tylohophora leaves and
160mg spinach leaves
dried. Two packs of
powder daily for 6 days
Double-blind placebo
controlled randomised trial
of 2 capsules of 400 mg
PulmoFlex per day for 3
weeks.
Double-blind placebo
controlled randomised,
crossover trial of two
Efamol capsules (Evening
Primrose oil) 4 times daily
for 8 weeks.
C
28/24
Primary
outcomes
extracted
SG = Adequate
AC = Unclear
B = Adequate
SG = Unclear
AC = Unclear
B = Adequate
SG = Unclear
AC = Unclear
B = Adequate
SG = Unclear
AC = Unclear
B = Adequate
71/64
8/8
21/9
12/12
ci
et
FEV1, PEFR,
reduction in use of
prescription
medicines
FEV1
PEFR
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SG = Adequate
AC = Unclear
B = Adequate
ht
P
SG= Unclear
AC = Unclear
B = Adequate
Intervention
Patients experiencing
deterioration,
judged by examining
doctor
Secondary
outcomes
extracted
No significant differences
No significant difference
No significant differences
No significant differences
Results
C Clark et al.
SG = Adequate
AC = Unclear
B = Adequate
SG = Unclear
AC = Unclear
B = Unclear
SG = Inadequate
AC = Unclear
B = Adequate
SG = Unclear
AC = Inadequate
B = Adequate
Hederos 1996
(Sweden)23
Hosseini 2001
(Iran)33
Hsieh 1996
(China)13
Hsu 2005
(China)24
12/10
PEFR, number of
days with extra
asthma
medication.
Change in FEV1,
FVC and PEFR,
number of
asthma attacks
during the
treatment period.
Primary
outcomes
extracted
http://www.thepcrj.org
800mg bd:40
400mg bd:40
Placebo:20
Group A: 32/34
Group B: 74/64
Group C: 55/44
22/22
ci
et
FEV1%
predicted, non of
subjects
experiencing
>5%
improvement in
FEV1 after 4
months
Change in early
morning and
evening PEFR
FEV1; FEV1/FVC
ratio
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P
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SG = Unclear
AC = Unclear
B = Adequate
Gupta 1998
(India)22
40/40
Group taking
treatment have
more severe
disease
Intervention
Participants &
inclusion criteria
Study
Symptom scores
grading cough
wheeze and
breathlessness each
as 0 asymptomatic
to 3 severe; total
score 0 to 9
reported
No significant differences
Results
Symptom score
graded 0
asymptomatic to 4
severe on 5 point
scale
Symptom scores
graded 1 mild
intermittent to 4
severe persistent
Symptom scores
Secondary
outcomes
extracted
30/30
http://www.thepcrj.org
SG = Unclear
AC = Unclear
B = Adequate
SG = Unclear
AC = Unclear
B = Unclear
Mansfeld
1998
(Germany
translated)35
Mathew 1974
(India)25
SG = Adequate
AC = Adequate
B = Adequate
SG = Unclear
AC = Adequate
B = Adequate
Lau 2004
(USA)14
59/64
Total 28,
distribution
not clear.
16/16
ci
et
FEV1, FVC, VC
Primary
outcomes
extracted
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ht
P
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SG = Adequate
AC = Adequate
B = Adequate
Juergens 2003
(Germany)30
16/16
Intervention
Participants &
inclusion criteria
Study
Symptom scores
graded from 0 no
symptoms adding 1
for every 1/2 hour
symptoms/day
Total clinical
improvement
(calculated from scoring
of rhionchi. Drug use
and symptom score)
at 1 and 12 weeks
Dyspnoea score
Patient global
assessment of
efficacy
Physician global
assessment of
efficacy. Assessed
using validated
scales which are not
described.
No significant differences
Results
Secondary
outcomes
extracted
Primary
outcomes
extracted
SG = Unclear
AC = Unclear
B = Unclear
SG = Unclear
AC = Adequate
B = Adequate
SG = Unclear
AC = Adequate
B = Adequate
SG = Unclear
AC = Unclear
B = Adequate
Placebo-controlled trial of
Devadaru Compound 3
tablets three times daily or
liquid or placebo.
Double-blind placebocontrolled randomised trial
of chopped Tylophora
indica leaves vs spinach
leaves (placebo) cut into
small pieces; one leaf daily
for 6 days with follow up
until the 12th week.
Double-blind placebocontrolled randomised trial
of dry alcholic extract of
Tylophora leaves with 1g
glucose powder for 6 days
with follow up until the
12th week.
Placebo-controlled,
randomisation and doubleblinding not described, trial
of nebulized menthol 10
mg twice a day
(manufactured by Hohei
Co.) for 4 weeks.
60 in or outpatients with
asthma, illness duration
6-24months. Ages & gender
not stated. 50% smoked
Sekhar 2003
(India)17
Shivpuri 1969
(India)36
Shivpuri 1972
(India)37
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Tamaoki 1995
(Japan)28
Amount of
prescribed drugs
taken in 24 hours;
53/57
11/10
103/92
PEFR
20/20/20
Amount of
prescribed drugs
which had
to be taken.
ci
et
46/46
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SG = Unclear
AC = Unclear
B = Unclear
Asthmatics receiving
treatment for >12 months,
age gender and smoking
status not stated
Rouhi 2006
(Iran)27
ht
P
rig
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y
SG = Adequate
AC = Adequate
B = Adequate
Murali 2006
(India)26
22/24
Intervention
Participants &
inclusion criteria
Study
Use of reliever
inhalers (puffs/week)
recorded in diary
Total clinical
improvement at 1
and 12 weeks (as
used by Matthew
1974)
Total clinical
improvement at 1
and 12 weeks (as
used by Matthew
1974)
Presence or absence
of dyspnoea,
wheeze and chest
tightness symptoms.
Symptom scores
grading dyspnoea,
wheeze, cough,
sleep disturbance
from 0 absent to 3
severe.
Secondary
outcomes
extracted
No significant differences
Results
Thomas 2006
(Scotland)39
Urata 2002
(Japan)40
Ziboh 2004
(USA)29
32/32
8/7
FEV1, PEFR
ci
et
VC PEFR, MBC
(maximum breathing
capacity), wheezing
attacks, nocturnal
dyspnoea, cough
chest tightness
Primary
outcomes
extracted
SG = Unclear
AC = Unclear
B = Adequate
SG = Unclear
AC = Unclear
B = Adequate
27/27
32/32
FEV1
FEV1, FVC
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SG = Unclear
AC = Unclear
B = Adequate
SG = Unclear
AC = Unclear
B = Adequate
ht
P
rig
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y
Thiruvengadam
1978 (India)38
Intervention
Participants &
inclusion criteria
Study
Symptom score
graded 0
asymptomatic to 3,
severe attacks on
>4/days per week
Asthma control
questionnaire (ACQ).
Leicester cough
questionnaire
Secondary
outcomes
extracted
Results
http://www.thepcrj.org