CHEST

Original Research
ASTHMA

Allergic Rhinitis and Sinusitis in

Asthma*
Differential Effects on Symptoms and Pulmonary
Function
Anne E. Dixon, MD, FCCP; David A. Kaminsky, MD, FCCP;
Janet T. Holbrook, PhD, MPH; Robert A. Wise, MD, FCCP;
David M. Shade, JD; and Charles G. Irvin, PhD

Background: Allergic rhinitis and sinusitis are frequently associated with asthma. The purpose of
this study was to determine the impact of self-reported allergic rhinitis and sinusitis on lower
airway disease in a large cohort of participants with well-characterized asthma.
Methods: A cohort study of participants in two trials of the American Lung Association-Asthma
Clinical Research Centers: 2,031 asthmatics in the Safety of Inactivated Influenza Vaccine in
Asthma in Adults and Children (SIIVA) trial and 488 asthmatics in the Effectiveness of Low Dose
Theophylline as Add-on Treatment in Asthma (LODO) trial. At baseline, participants reported
the presence of allergic rhinitis and sinusitis, and then lung function and asthma control were
measured. During the trials, participants were monitored for asthma exacerbations.
Results: More than 70% of participants reported either allergic rhinitis or sinusitis. Sinusitis was
more common in female patients (odds ratio, 1.46 [SIIVA]), those with gastroesophageal reflux
disease (odds ratio, 2.21 [SIIVA]), and those of white race (odds ratio, 1.53 [SIIVA]). Similar
associations were seen for allergic rhinitis. LODO participants with allergic rhinitis and sinusitis
had increased asthma symptoms and a trend toward more sleep disturbance. Participants with
allergic rhinitis had higher baseline lung function than those without allergic rhinitis measured
by peak flow (91.2% vs 95.8% in the SIIVA trial). Participants with sinusitis had similar lung
function to those without sinusitis. Participants with and without allergic rhinitis had similar
exacerbation rates. In the LODO trial only, participants with sinusitis had increased asthma
exacerbations (5.68 per patient per year vs 3.72 per patient per year).
Conclusion: Allergic rhinitis and sinusitis are associated with more severe asthmatic symptoms
and, in patients with poorly controlled asthma, more exacerbations but are not associated with
low lung function.
(CHEST 2006; 130:429 435)
Key words: allergic rhinitis; asthma; gastroesophageal reflux disease; pulmonary function tests; sinusitis
Abbreviations: ALA-ACRC American Lung Association-Asthma Clinical Research Centers; AQLQ Asthma
Quality of Life Questionnaire; ASUI asthma symptom utility index; ESS Epworth sleepiness scale;
GERD gastroesophageal reflux disease; LODO Effectiveness of Low Dose Theophylline as Add-on Treatment in
Asthma; PEFR peak expiratory flow rate; PSQI Pittsburgh sleep quality index; SIIVA Safety of Inactivated
Influenza Vaccine in Asthma in Adults and Children

llergic rhinitis is a risk factor for sinusitis, and

A asthmatics
are known to be at increased risk for
1

sinusitis.2,3 Nasal and sinus symptoms are clearly

very common in asthma, and some studies3,4 have
suggested that sinusitis is a risk factor for severe
asthma, whereas others5,6 have not. Similarly, there
are reports7,8 that allergic rhinitis is associated with
more severe asthma, but another study9 has found
the opposite.
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The roles of allergic rhinitis and sinusitis in asthma

are controversial, and one possible explanation is that
they have differential effects based on asthma disease severity. The American Lung AssociationAsthma Clinical Research Centers (ALA-ACRC)
conducted two clinical trials: one trial that enrolled a
general population sample of asthmatics, most with
mild disease, and a second trial that enrolled participants with poorly controlled asthma. Both trials
CHEST / 130 / 2 / AUGUST, 2006

429

acquired information on self-report of allergic rhinitis and sinusitis, asthma symptoms, pulmonary function, and exacerbation frequency by asthma diary.
These data sets provided a unique opportunity to
examine the relationship of allergic rhinitis and
sinusitis to asthma in two well-characterized cohorts
of patients with different levels of asthma severity.
Materials and Methods

excluded. At baseline, asthma severity was rated according to

symptoms by the ASUI and according to lung function by peak
flow and spirometry (before and after bronchodilator). Quality of
life12 and sleep disturbance13,14 were assessed at baseline according to validated questionnaires. Severity of symptoms related to
cough was assessed by the question pertaining to cough from the
Asthma Quality of Life Questionnaire (AQLQ).12 During the
trial, participants were randomized to one of three treatment
groups (theophylline, montelukast, or placebo) and monitored
over 6 months for exacerbations, defined as described above for
the SIIVA trial.
Classification of Disease of the Nose and Sinuses

Participants
We evaluated baseline cross-sectional data obtained from two
cohorts of patients enrolled in the ALA-ACRC Safety of Inactivated Influenza Vaccine in Asthma in Adults and Children
(SIIVA) and Effectiveness of Low Dose Theophylline as Add-on
Treatment in Asthma (LODO) trials. The primary results of the
SIIVA trial have been published10; those of the LODO trial have
been submitted for publication. In brief, the SIIVA trial was a
multicenter, double-blind, placebo-controlled, crossover study to
determine the safety of the influenza vaccine in asthmatic
participants. The LODO trial was a randomized, double-blind,
placebo-controlled trial of low-dose theophylline vs montelukast
vs placebo as add-on therapy for poorly controlled asthma. Both
trials were approved by the institutional review boards of all
participating institutions, and informed consent was obtained
from all participants.
The SIIVA trial enrolled 2,031 participants 3 years old with
a history of physician-diagnosed asthma. Participants were not
selected based on the severity of their asthma. Asthma severity
was rated by lung function with peak flow and according to
symptoms by the asthma symptom utility index (ASUI).11 In
addition, 995 participants underwent spirometry (without bronchodilator). During the trial, exacerbations within 14 days of an
injection (placebo or influenza vaccine) were measured. These
were defined as any one of the following: (1) a decrease of at least
30% in the peak expiratory flow rate (PEFR); (2) an increase in
the daily use of rescue medication (eg, four or more puffs of
albuterol above baseline); (3) an increase in, or addition of,
systemic corticosteroids for asthma; or (4) an unscheduled
health-care visit for asthma.
The LODO cohort comprised 488 participants 15 years old
with poorly controlled asthma (regardless of baseline treatment
regimen) as measured by a score of 1.5 on the Juniper asthma
control questionnaire. Participants who had smoked within the
last 6 months or who had a 20 pack-year smoking history were
*From Pulmonary and Critical Care Medicine (Drs. Dixon,
Kaminsky, and Irvin), University of Vermont, Burlington, VT;
and Department of Medicine (Drs. Wise and Shade) and
Bloomberg School of Public Health (Dr. Holbrook), Johns
Hopkins University, Baltimore, MD.
None of the authors have any conflicts of interest in the content
of this article.
Funding was provided by the American Lung Association and
grant K23 RR019965.
Manuscript received December 20, 2005; revision accepted
February 15, 2006.
Reproduction of this article is prohibited without written permission
from the American College of Chest Physicians (www.chestjournal.
org/misc/reprints.shtml).
Correspondence to: Anne E. Dixon, MD, FCCP, Pulmonary and
Critical Care Medicine, Patrick 204, Fletcher Allen Health Care,
111 Colchester Ave, Burlington, VT 05401; e-mail: anne.
dixon@vtmednet.org
DOI: 10.1378/chest.130.2.429
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The diagnosis of disease of the nose and sinuses was determined by response to a structured questionnaire, as is common
practice in other studies, such as the European Community
Respiratory Health Surveys15,16 and the National Health and
Nutrition Examination Survey.17 The presence of sinusitis was
defined as patient report of sinusitis. The presence of allergic
rhinitis was defined as a patient report of allergic rhinitis or hay
fever.
Statistical Analysis
Descriptive statistics were used to describe the study population, followed by bivariate and multivariate analyses using logistic
regression to explore the association between demographic and
health characteristics and the presence of allergic rhinitis and
sinusitis. Variables significant at p 0.05 by univariate analysis
were considered for inclusion in the final model.
We compared symptom scores and exacerbation rates in
LODO participants with and without allergic rhinitis and sinusitis
using the Wilcoxon rank-sum test. We compared the proportion
of SIIVA participants with an exacerbation after injection by
Pearson 2 test. We investigated whether there was an interaction
between baseline asthma severity and either allergic rhinitis or
sinusitis on asthma symptoms and exacerbations by creating an
interaction term using baseline percentage of predicted peak flow
80% predicted, and presence of allergic rhinitis and sinusitis,
respectively. We pooled data from the SIIVA and LODO trials
and examined the effect of these interaction terms on the ASUI
symptom score by regression techniques using baseline peak flow
as a covariate.
We studied asthma severity by lung function measures in
participants with and without both allergic rhinitis and sinusitis
by univariate and multivariate regression. All analyses were
performed using statistical software (STATA 8; StataCorp; College Station, TX).

Results
Baseline Demographics
The SIIVA trial enrolled 2,031 participants (age
range, 3 to 83 years). The distribution of race and age
is shown in Table 1. The LODO trial enrolled 488
participants 15 years old; age and race distribution
are shown in Table 1. The SIIVA cohort included
significantly more children: 38% of the participants
were 20 years old, compared with 10% in the
LODO trial.
Prevalence of Allergic Rhinitis and Sinusitis
Allergic rhinitis and sinusitis were the most common comorbidities reported in these participants;
Original Research

Table 1Baseline Demographics of Participants in the

SIIVA and LODO Trials of the ALA-ACRC*
Demographics

SIIVA (n 2,031)

LODO (n 488)

Female gender
Age, yr
20
2130
3140
4150
5160
60
Smoking status
Active smoker
Ever smoker
Race
White
African American
Hispanic
Other

1,233 (62)

360 (74)

771 (38)
215 (11)
309 (15)
345 (17)
257 (13)
132 (7)

47 (10)
93 (19)
106 (22)
115 (24)
80 (16)
47 (10)

96 (5)
430 (22)

0
90 (18)

1,289 (63)
498 (24)
123 (6)
123 (6)

296 (61)
142 (29)
39 (8)
11 (2)

*Data are presented as No. (%). Among the 2,031 participants in the
SIIVA trial, all but 42 had complete data analysis for demographic
variables.

together, they affected 73% of the SIIVA cohort and

79% of the LODO cohort (Fig 1). In the SIIVA trial,
57% reported allergic rhinitis and 51% sinusitis (35%
reported both allergic rhinitis and sinusitis). In the
LODO trial, 70% reported allergic rhinitis and 41%
reported sinusitis (36% reported both allergic rhinitis and sinusitis).
Factors Associated With Allergic Rhinitis and
Sinusitis
Gastroesophageal reflux disease (GERD), female
sex (apart from LODO participants with allergic
rhinitis), and white race were associated with ex-

Figure 1. Prevalence of self-reported rhinosinus disease in

participants in the SIIVA (n 2,031) and LODO (n 488)
trials.
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trathoracic airway disease, but active smoking was

not (data for allergic rhinitis and sinusitis are shown
in Table 2).
Allergic Rhinitis and Sinusitis, and Asthma
Symptoms
Allergic rhinitis was associated with more severe
symptoms in the LODO cohort but not the SIIVA
cohort; a lower score on the ASUI is indicative of
more severe symptoms (Table 3). Overall, participants in the LODO trial had more severe symptoms
than participants in the SIIVA trial, as would be
anticipated from the inclusion criteria for the studies. As the SIIVA trial included both adults and
children, we performed a separate analysis restricted
to SIIVA patients 15 years old. Overall, patients
15 years old with allergic rhinitis in the SIIVA trial
still had similar symptom scores to those without
allergic rhinitis (data not shown).
Sinusitis was associated with more severe symptoms in both the LODO and SIIVA trials (Table 3).
Sinusitis was also associated with a more severe
symptom score related to cough, worse asthmarelated quality of life, and more sleep disturbance as
measured by the Epworth sleepiness scale (ESS) and
the Pittsburgh sleep quality index (PSQI); similar
trends were seen for cough and sleep disturbance for
LODO participants with allergic rhinitis (Table 3).
Interaction Between Allergic Rhinitis and Sinusitis,
and Asthma-Symptom Severity
We found that the effect of both allergic rhinitis
and sinusitis on symptoms depended on baseline
asthma severity. Using pooled data from the LODO
and SIIVA trials, the presence of allergic rhinitis was
associated with a decrease in the ASUI of 0.02
(n 2,270, p 0.002). We then included an interaction term for baseline peak flow 80% predicted
and the presence of allergic rhinitis (using baseline
peak flow as a covariate); the presence of allergic
rhinitis in those with peak flow 80% predicted was
associated with a decrease in the ASUI of 0.04 points
(p for interaction term 0.02). This indicates a
more significant effect of allergic rhinitis on symptoms for patients with a combination of lower baseline lung function and allergic rhinitis, ie, those with
more severe asthma.
Similarly, using pooled data from the LODO and
SIIVA trials, the presence of sinusitis was associated
with a decrease in the ASUI of 0.03 (n 2,269,
p 0.001). We then included an interaction term
for baseline peak flow 80% predicted and the
presence of sinusitis (using baseline peak flow as a
covariate); the presence of sinusitis in those with
peak flow 80% predicted was associated with a
CHEST / 130 / 2 / AUGUST, 2006

431

Table 2Risk Factors for Allergic Rhinitis and Sinusitis in Participants Participating in the LODO and SIIVA
Trials*
Variables

Unadjusted Odds Ratio

95% Confidence Interval

Adjusted Odds Ratio

95% Confidence Interval

1.01
1.40
1.34
1.59
0.75

1.011.02
1.141.72
1.121.61
1.321.92
0.481.17

1.00
1.22
1.21
1.52

1.001.01
0.991.52
1.001.47
1.281.86

1.00
2.45
1.32
1.80

0.991.02
1.533.92
0.862.04
1.212.67

2.32
1.32
1.67

1.453.72
0.852.06
1.122.49

1.01
2.45
1.63
1.55
1.00

1.001.01
1.993.03
1.361.95
1.291.87
1.001.02

1.00
2.21
1.46
1.53
1.01

1.001.01
1.782.75
1.201.77
1.261.85
0.631.63

1.01
2.39
1.72
1.56

1.001.02
1.623.54
1.142.61
1.082.26

1.01
2.29
1.74
1.45

0.991.02
1.543.41
1.142.67
0.992.12

Allergic rhinitis
SIIVA trial
Age
GERD
Female gender
White race
Current smoker
LODO trial
Age
GERD
Female gender
White race
Sinusitis
SIIVA trial
Age
GERD
Female gender
White race
Curent smoker
LODO trial
Age
GERD
Female
White race

*Current smokers were excluded from the LODO trial; n 1,983 for the SIIVA trial and n 488 for the LODO trial.

decrease in the ASUI of 0.06 points (p for interaction

term 0.002). This indicates a more significant effect of sinusitis on symptoms for patients with a
combination of lower baseline lung function and
sinusitis, ie, those with more severe asthma.

Table 3Effect of Allergic Rhinitis and Sinusitis on

Symptoms, Quality of Life, and Related Comorbidities
in the LODO Trial, and Symptom Score in the SIIVA
Trial*
Variables
Allergic rhinitis
SIIVA trial
ASUI
LODO trial
ASUI
AQLQ
Cough
ESS
PSQI
Sinusitis
SIIVA trial
ASUI
LODO trial
ASUI
AQLQ
Cough
ESS
PSQI

No Disease

With Disease

n 836
0.84 0.17
n 146
0.73 0.13
4.2 1.1
4.2 1.5
8.1 4.8
7.4 3.5

n 1,133
0.83 0.17
n 341
0.67 0.16
4.2 1.1
4.1 1.6
8.7 5.0
8.0 3.9

n 949
0.85 0.15
n 266
0.70 0.14
4.3 1.1
4.3 1.6
8.3 5.0
7.4 3.7

n 1,019
0.82 0.18
n 222
0.66 0.16
4.1 1.1
3.9 1.6
8.8 4.8
8.3 3.8

p Value

Severity of Lung Disease in Participants With

Rhinosinusitis
Participants with allergic rhinitis had higher lung
function measured by peak flow than those without
allergic rhinitis (Table 4). FEV1 was also higher in
SIIVA subjects with allergic rhinitis, and a similar
trend was observed in LODO subjects. Similar
trends toward higher FEV1 and peak flow were seen
in participants with sinusitis in both the LODO and
SIIVA trials, but these were not statistically significant (Table 4).
Asthma Exacerbations

0.61
0.01
0.5
0.4
0.2
0.2

0.01
0.01
0.02
0.01
0.06
0.01

*Values shown are mean SD.

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In both the SIIVA and LODO trials, participants

with allergic rhinitis had similar exacerbation rates to
those without allergic rhinitis (Table 5). In the
LODO trial, participants with sinusitis had increased
exacerbations compared to those without sinusitis;
this was not the case for SIIVA participants overall or
when considering only SIIVA participants 15 years
old (data not shown).
Discussion
In our study, self-reported allergic rhinitis and
sinusitis were very common in asthma. GERD,
female gender, and white race were particularly
Original Research

Table 4 Severity of Lung Disease in Participants With Allergic Rhinitis and Sinusitis Adjusted for Demographic
Factors and Other Comorbidites*
Variables

No Allergic Rhinitis

Allergic Rhinitis

SIIVA trial
FEV1, % predicted
FVC, % predicted
PEFR, % predicted
LODO trial
FEV1, % predicted
% BD change
FVC, % predicted
PEFR, % predicted

n 367
84.7 21.0
89.2 21.0
91.2 22.6
n 145
77.1 17.5
8.3 12.7
88.4 16.8
79.0 20.9

n 625
87.9 20.0
92.2 19.1
95.8 24.4
n 339
79.3 16.4
9.4 11.0
87.2 14.9
83.7 19.4

Adjusted p Value
0.03
0.025
0.001
0.17
0.40
0.42
0.02

No Sinusitis

Sinusitis

n 451
86.1 21.5
91.0 21.5
93.8 22.7
n 263
77.4 16.8
9.5 11.4
87.0 15.7
81.4 20.1

n 540
87.2 19.4
91.2 18.4
94.0 24.7
n 540
80.2 16.6
8.6 11.7
88.2 15.2
83.4 19.8

Adjusted p Value
0.24
0.39
0.93
0.07
0.30
0.38
0.27

*Values shown are mean SD. Covariates included use of inhaled corticosteroids and smoking history.
BD percent increase in FEV1 following bronchodilator.

associated with both allergic rhinitis and sinusitis.

Both allergic rhinitis and sinusitis were associated
with more severe symptoms in those with more
severe asthma at baseline; in one cohort, sinusitis
(but not allergic rhinitis) was associated with increased exacerbations. Participants with allergic rhinitis and sinusitis tended to have higher lung function than those without allergic rhinitis and sinusitis.
We analyzed data separately from the two cohorts
because the trials recruited different types of asthmatics. Indeed, SIIVA participants had fewer severe
symptoms and better lung function at baseline. We
studied both allergic rhinitis and sinusitis, as we
wanted to determine if these disease processes had
similar demographic associations and a similar effect
on asthma; our findings are consistent with the
concept that allergic rhinitis and sinusitis are part of
a disease continuum.
The main limitation of our analysis is that crosssectional prevalence data reported by participants
may not accurately reflect upper airway disease
activity assessed by more objective measures such as
sinus CT. Reports of the correlation between sinus
symptoms and actual sinus CT abnormalities vary,

Table 5Exacerbations in Participants With Allergic

Rhinitis and Sinusitis Reported Separately*
Variables
Allergic rhinitis
SIIVA trial
LODO trial
Sinusitis
SIIVA trial
LODO trial

Exacerbations

Disease
Absent

Disease
Present

After placebo
Exacerbation rate

28.1%
4.69

26.9%
4.59

0.53
0.85

After placebo
Exacerbation rate

26.1%
3.72

28.5%
5.68

0.24
0.01

p Value

*For the SIIVA trial, the proportion of participants with an exacerbation over the 14-day period after injection of placebo is reported (results after vaccine were not different), n 1,994. For the
LODO trial, exacerbations per subject per year are reported,
n 488.
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with one study18 reporting that 66% of subjects with

sinus symptoms had an abnormal sinus CT finding,
and another study19 (specifically of asthmatics) reporting significant sinus CT abnormalities in 80% of
participants with nasal symptoms. However selfreport is commonly used in large studies in which
more invasive measures to document these diseases
would be prohibitively expensive (such as the National Health Interview Survey and the European
Community Respiratory Health Study20), and the
rates of allergic rhinitis and sinusitis that we report
are similar to those previously described in the
literature (reviewed by de Benedictis and Bush21).
Demographic factors associated with allergic rhinitis and sinusitis in asthma have not previously been
reported in a large cohort of asthmatics. We found
that female gender was associated with an increased
risk of allergic rhinitis and sinusitis; this is consistent
with data from the National Health Interview Survey.22 White race was also associated with both
allergic rhinitis and sinusitis; similarly, Chen et al23
found that among asthmatics, white patients were
more likely to have allergic rhinitis than African
Americans. Sinusitis has previously been associated
with active smoking17; however, given the small
number of smokers in our asthmatic population, we
had limited power to detect a small increased risk.
We also found that GERD was associated with both
allergic rhinitis and sinusitis, as has previously been
reported.24,25
Symptom scores were increased in LODO participants with both allergic rhinitis and sinusitis; in
particular, symptoms related to cough tended to be
higher. Similarly, Bousquet et al26 reported that
participants with seasonal allergic rhinitis and asthma
had increased cough, and in the general population
allergic rhinitis and sinusitis are associated with
chronic cough.27,28 We also found a trend toward
increased sleep disturbance in LODO participants
with allergic rhinitis and sinusitis. This has also been
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433

reported previously in nonasthmatics.29 Nasal obstruction likely contributes to sleep disturbance

through increased airflow resistance. However, we
did not find more severe symptoms in SIIVA participants with allergic rhinitis. As SIIVA participants
had milder asthma, we pooled from the LODO and
SIIVA trials. Both allergic rhinitis and sinusitis had a
more pronounced effect on symptoms in those with
more severe asthma at baseline. This suggests that
allergic rhinitis and sinusitis have a differential impact on patients depending on the baseline level of
asthma severity: they may be a minor irritation to
people with mild asthma, but they substantially add
to the burden of disease in patients with more severe
asthma.
We found similar exacerbations in SIIVA participants with and without allergic rhinitis and sinusitis,
but in LODO participants we found that sinusitis
(but not allergic rhinitis) was associated with increased exacerbations. Studies7,30 have typically
found increased exacerbations in patients with allergic rhinitis. Some but not all studies8,31 show that
treatment of allergic rhinitis decreases asthma exacerbations. Our data suggest that although allergic
rhinitis and sinusitis are common in asthmatics with
all levels of disease severity, they contribute to poor
asthma control in terms of symptoms and exacerbations only in those with more severe asthma.
There was a trend toward better lung function in
participants with allergic rhinitis and sinusitis; this
has been reported in other studies.26 The observation that allergic rhinitis and sinusitis did not affect
lung function is consistent with results from experimental models: sinusitis in rabbits does not alter
baseline lung function but does increase airway
responsiveness,32 and nasal provocation in humans
increases bronchial hyperreactivity without affecting
baseline lung function.33 The link between the upper
and lower airway is thought to be related to a
common mechanism inciting disease in both places,
possibly a postnasal drip mechanism.32 But this
dissociation between symptoms and exacerbations,
and lung function suggests that changes in lung
function may be mediated through a different pathophysiologic pathway than the process associated with
inflammation of the nose and sinuses. It is noteworthy that although remodeling is apparent in the lower
airway of asthmatics, it is not so readily apparent in
the nasal mucosa.34 In other words, lower airway
disease has distinct features that may lead to dissociation in some measures of disease severity between
the upper and lower airways.
Our findings suggest that self-reported allergic
rhinitis and sinusitis are present in the vast majority
of asthmatics. They contribute to increased symptoms and sleep disturbance in patients with poorly
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controlled asthma, and may also contribute toward

exacerbations. Additionally, it seems reasonable to
postulate that treatment of allergic rhinitis and sinusitis in all asthmatics may improve symptoms attributed to asthma through mechanisms unrelated to
improvement in pulmonary function.
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