Abstract Background: Anxiety is a common comorbidity associated with chronic obstructive pulmonary disease (COPD), but no well-recognized method can provide effective relief. Liuzijue Qigong (LQG) is a traditional Chinese fitness method, based on breath pronunciation. This study aimed to examine the efficacy of LQG to relieve anxiety in COPD patients and to explore the factors that influence anxiety, including whether LQG is effective during the coronavirus disease 2019 (COVID-19) outbreak. Methods: We conducted an open-label, randomized, controlled, clinical trial. A total of 60 patients with stable COPD were randomly assigned to two groups. Both groups were given routine medical treatment, and the patients in the pulmonary rehabilitation (PR) group were given an extra intervention in the form of LQG, performed for 30 minutes each day for 12 weeks. Data collection was performed at baseline and 12 weeks (during the COVID-19 epidemic). The primary outcomes were the self-rating anxiety scale (SAS) scores, and the secondary outcomes were relevant information during the epidemic and analyses of the related factors that influenced SAS scores during the COVID-19 outbreak. Results: Compared with baseline, patients in both groups demonstrated varying degrees of improvements in their SAS scores (all P < 0.01). An analysis of covariance, adjusted for baseline scores, indicated that the SAS scores improved more dramatically in the PR group than in the control group (F = 9.539, P = 0.004). During the outbreak, the SAS scores for sleep disorder were higher than all other factors, reaching 1.38 ± 0.67, and the scores for “I can breathe in and out easily” for the PR group were lower than the scores for the control group (Z = −2.108, P = 0.035). Significant differences were identified between the two groups for the categories “How much has the outbreak affected your life”, “Do you practice LQG during the epidemic” and “Do you practice other exercises during the epidemic” (all P < 0.05). Compared with current reports, LQG had a relatively high adherence rate (80.95%). A multiple linear regression analysis revealed multiple predictors for SAS scores during the outbreak: group (b = −3.907, t = −3.824, P < 0.001), COPD assessment test score (b = 0.309, t = 2.876, P = 0.006), SAS score at baseline (b = 0.189, t = 3.074, P = 0.004), and living in a village (b = 4.886, t = 2.085, P = 0.043). Conclusion: LQG could effectively reduce the risks of anxiety among COPD patients, even during the COVID-19 outbreak. For those COPD patients with high COPD assessment test and high baseline SAS scores or who live in villages, we should reinforce the management and intervention of psychological factors during the epidemic.

1. ARTICLE
TMR | July 2020 | vol. 5 | no. 4 | 216
doi: 10.12032/TMR20200528183
Submit a manuscript: https://www.tmrjournals.com/tmr
Traditional Chinese Medicine
Does Liuzijue Qigong affect anxiety in patients with chronic
obstructive pulmonary disease, even during the COVID-19 outbreak?
a randomized, controlled trial
Yu-Xuan Zhang1
, Ying Quan1
, Ming-Hu Chen1
, Duo Zhang2
, Ying Zhang3
, Zhen-Gang Zhu1*
1
First Teaching Hospital of Tianjin University of Traditional Chinese Medicine, Tianjin 300381, China; 2
Tianjin University of
Traditional Chinese Medicine, Tianjin 301617, China; 3
Australian National University, Canberra 2601, Australia.
*Corresponding to: Zhen-Gang Zhu. First Teaching Hospital of Tianjin University of Traditional Chinese Medicine, No.88
Changlin Road, Xiqing District, Tianjin 300381, China. E-mail: airforcechina@aliyun.com.
Highlights
Patients with high course of chronic obstructive pulmonary disease (COPD) assessment test scores,
self-rating anxiety scale scores, or who live in rural areas, have a higher burden of anxiety and need more
attention during the outbreak. As a pulmonary rehabilitation exercise, Liuzijue Qigong (LQG) can relieve
anxiety in stable COPD patients, even during the coronavirus disease 2019 outbreak.
Traditionality
LQG has been used as a traditional Chinese Taoism (a Chinese philosophy attributed to Lao Tzu (500
B.C.E.) which contributed to the religion of the people in China) regimen for approximately 1,500 years.
The six pronunciations of “Xu, He, Hu, Si, Chui, Xi” in LQG were first recorded as a treatment in the
ancient book Yang Xing Yan Ming Lu (Records of Nourishing the Body and Prolonging Life) written by Tao
Hongjing in the Southern and Northern Dynasties (420–589 C.E.) of China. It recorded that LQG can
regulate the function of internal organs of the body to tend to balance through pronunciation, which was
conducive to the health of the body. Until 2007, it became a complete Qigong exercise by General
Administration of Sport of China. In recent years, it has been widely used in pulmonary rehabilitation for
COPD patients in China.

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doi: 10.12032/TMR20200528183
Abstract
Background: Anxiety is a common comorbidity associated with chronic obstructive pulmonary disease (COPD),
but no well-recognized method can provide effective relief. Liuzijue Qigong (LQG) is a traditional Chinese fitness
method, based on breath pronunciation. This study aimed to examine the efficacy of LQG to relieve anxiety in
COPD patients and to explore the factors that influence anxiety, including whether LQG is effective during the
coronavirus disease 2019 (COVID-19) outbreak. Methods: We conducted an open-label, randomized, controlled,
clinical trial. A total of 60 patients with stable COPD were randomly assigned to two groups. Both groups were
given routine medical treatment, and the patients in the pulmonary rehabilitation (PR) group were given an extra
intervention in the form of LQG, performed for 30 minutes each day for 12 weeks. Data collection was performed
at baseline and 12 weeks (during the COVID-19 epidemic). The primary outcomes were the self-rating anxiety
scale (SAS) scores, and the secondary outcomes were relevant information during the epidemic and analyses of the
related factors that influenced SAS scores during the COVID-19 outbreak. Results: Compared with baseline,
patients in both groups demonstrated varying degrees of improvements in their SAS scores (all P < 0.01). An
analysis of covariance, adjusted for baseline scores, indicated that the SAS scores improved more dramatically in
the PR group than in the control group (F = 9.539, P = 0.004). During the outbreak, the SAS scores for sleep
disorder were higher than all other factors, reaching 1.38 ± 0.67, and the scores for “I can breathe in and out easily”
for the PR group were lower than the scores for the control group (Z = −2.108, P = 0.035). Significant differences
were identified between the two groups for the categories “How much has the outbreak affected your life”, “Do
you practice LQG during the epidemic” and “Do you practice other exercises during the epidemic” (all P < 0.05).
Compared with current reports, LQG had a relatively high adherence rate (80.95%). A multiple linear regression
analysis revealed multiple predictors for SAS scores during the outbreak: group (b = −3.907, t = −3.824, P < 0.001),
COPD assessment test score (b = 0.309, t = 2.876, P = 0.006), SAS score at baseline (b = 0.189, t = 3.074, P =
0.004), and living in a village (b = 4.886, t = 2.085, P = 0.043). Conclusion: LQG could effectively reduce the
risks of anxiety among COPD patients, even during the COVID-19 outbreak. For those COPD patients with high
COPD assessment test and high baseline SAS scores or who live in villages, we should reinforce the management
and intervention of psychological factors during the epidemic.
Keywords: Chronic obstructive pulmonary disease, Anxiety, Self-rating anxiety scale scores, Liuzijue Qigong,
Pulmonary rehabilitation, Coronavirus disease 2019
Author contributions:
All authors made substantial contribution before submission, and all authors have read and approved the final
manuscript. Yu-Xuan Zhang designed the study, extracted and analyzed data and drafted the manuscript; Ying
Quan performed experiments, acquisition of subjects and data; Ming-Hu Chen assisted in the study design,
checked the data and critically revised the manuscript; Duo Zhang was responsible for patient recruitment and
acquisition of data, and contributed in development of study aims of the present study; Ying Zhang was involved
in literature search, statistical analyses, data interpretation; Zhen-Gang Zhu oversaw the data interpretation and
critically revised the manuscript.
Competing interests:
The authors declare no conflicts of interest.
Acknowledgments:
This study was supported by National Natural Science Foundation of China (No. 81673900).
Abbreviations:
COPD, chronic obstructive pulmonary disease; LQG, Liuzijue Qigong; COVID-19, coronavirus disease 2019;
PR, pulmonary rehabilitation; SAS, self-rating anxiety scale; GOLD, Global Initiative for Chronic Obstructive
Lung Disease; SD, standard deviation; ANCOVA, analysis of covariance; CAT, course of COPD assessment test.
Citation:
Yu-Xuan Zhang, Ying Quan, Ming-Hu Chen, et al. Does Liuzijue Qigong affect anxiety in patients with chronic
obstructive pulmonary disease, even during the COVID-19 outbreak? a randomized, controlled trial. Traditional
Medicine Research 2020, 5 (4): 216–228.
Executive editor: Rui-Wang Zhao.
Submitted: 18 April 2020, Accepted: 25 May 2020, Online: 02 June 2020.

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doi: 10.12032/TMR20200528183
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Background
Anxiety is a common complication among chronic
obstructive pulmonary disease (COPD) patients that is
often under-diagnosed and directly influences
prognosis and quality of life [1]. Therefore, anxiety
management is an indispensable component of COPD
prevention and control strategies. Studies have
confirmed that public health emergencies are likely to
increase anxiety levels. During the coronavirus disease
2019 (COVID-19) epidemic, 2.9% of patients with
COVID-19 had a history of COPD, including 8.3% of
critical intensive care unit patients [2]. Individuals who
are older than 60 years old and suffer from COPD are
more susceptible to severe acute respiratory
syndrome-coronavirus-2 infection and experience
higher mortality following COVID-19 acquisition [3].
An increase in the information available through social
media and the internet also poses a major risk to the
mental health of individuals during the COVID-19
crisis [4]. However, little attention has been paid to the
anxiety among COPD patients during the COVID-19
outbreak, and no unified standard exists for the
appropriate clinical management of COPD-related
anxiety.
Increasingly, studies [5] have shown that pulmonary
rehabilitation (PR) can be beneficial for anxiety relief.
However, fewer than 5.0% of eligible patients receive
PR [6], and some studies have reported that reduced
patient participation and high dropout rates may be due
to insufficient professional assistance, expensive
equipment maintenance, and inconvenient
transportation for patients [7–10]. Liuzijue Qigong
(LQG) is a type of traditional Chinese Taoism (a
Chinese philosophy attributed to Lao Tzu (500 BCE)
which contributed to the religion of the people in
China) regimen. Approximately 1,500 years ago, the
six pronunciations of “Xu, He, Hu, Si, Chui, and Xi”
practiced in LQG were first recorded as a treatment in
the ancient book Yang Xing Yan Ming Lu (Records of
Nourishing the Body and Prolonging Life), written by
Tao Hongjing, in the Southern and Northern Dynasties
(420–589 C.E.) of China, and was referred to as deep
breathing. During the Sui Dynasty (581–619 C.E.),
people connected the six pronunciations with internal
organs of human body, which are thought to regulate
the function of internal organs and promote balance
through pronunciation, which was believed to be
conducive to the bodily health. During the Tang
Dynasty (618–907 C.E.), Chao Yuanfang made up a
pithy formula of LQG, in Zhu Bing Yuan Hou Lun
(General Treatise on Causes and Manifestations of All
Diseases), which was easy to memorize and spread.
After the Ming Dynasty (1368–1644 C.E.), LQG
began to be associated with body movements and
became a complete Qigong exercise in 2007,
recognized by the General Administration of Sport of
China [11].
In recent years, LQG has been widely used as a type
of PR for COPD patients in China because it combines
the respiratory patterns of abdominal breathing with
pursed-lip breathing [12–14]. Therefore, in this study,
we examined the role played by LQG in the
management of anxiety by evaluating anxiety among
COPD patients.
Materials and methods
Participants
The participants were recruited from outpatients at the
First Teaching Hospital of Tianjin University of
Traditional Chinese Medicine in China, from October
10, 2019, to January 17, 2020. The diagnosis of stable
COPD was based on the guidelines established by the
Global Strategy for the Diagnosis, Management, and
Prevention of COPD (2019) [15].
Inclusion criteria
Inclusion criteria included the following: (1) diagnosis
with stable COPD; (2) age  45 years; (3) provision of
informed consent and available medical records; (4)
the ability to participate in the study, unassisted.
Exclusion criteria
The exclusion criteria included the following: (1)
instable disease(s) (e.g., severe cardiovascular,
neurological and musculoskeletal diseases) or
inpatients; (2) cognitive impairment and mobility
limitations.
Ethical standards
All patients signed informed consent forms declaring
their voluntary participation in the program and were
informed of the relevant treatment conditions. This
study was approved by the Ethics Committee of First
Teaching Hospital of Tianjin University of Traditional
Chinese Medicine (TYLL2020[K] 001).
Randomization
The sample size selection was based on previous
research [12–14]. Before starting the study, a
researcher who was not involved in the data collection
process flipped a coin (heads = control group and tails
= PR group) 60 times, writing down whether it landed
on heads or tails each time, to determine group
assignments.
Blinding
This study was performed as an open-label,
randomized, controlled trial.
Interventions
According to the Global Initiative for Chronic
Obstructive Lung Disease (GOLD) guidelines, we
provided both groups with the usual therapy (the

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inhalation of long-acting muscarinic agonists and/or
inhaled corticosteroids + long-acting beta-agonists),
smoking cessation recommendations, and education
(medical knowledge regarding COPD and standard
treatments). Patients in the control group did not
receive any PR exercises, whereas the PR group
received LQG exercises (compiled by the Chinese
Health Qigong Association) [16], consisting of six
different sections, each containing one pronunciation,
and were told to repeat all exercises six times. All
patients in the PR group completed training under the
guidance of a trained therapist and were included in
the study after passing an examination. To encourage
the PR group to participate in LQG exercises and to
ensure that the plan was executed correctly, the
patients in the PR group were given LQG videos and
exercise logs. Subsequently, patients were asked to
perform the LQG exercises every day, at home, and
once a week at the hospital, under the guidance of an
instructor, for 30 mins each time, for 12 weeks.
LQG consists of the pronunciation of “Xu, He, Hu,
Si, Chui, and Xi” while exhaling through different
mouth shapes, to adjust the ascending-descending
pattern of Qi movement. “Xu” is pronounced with the
help of teeth, keeping the upper and lower teeth
parallel and leaving some space between the teeth and
tongue. Air is exhaled from this space, and the corner
of the mouth is pulled back slightly. When exhaling
and pronouncing “He”, the sides of the tongue tap the
upper teeth, and air is exhaled between the upper jaw
and the tongue. “Hu” is assisted by the throat. Patients
should bend the sides of the tongue upward and stick
out the lips, which should form a circle, allowing air to
be exhaled through the circle. The pronunciation of
“Si” is assisted by the teeth, with a slightly open mouth
and teeth, to create a narrow space. The patient slightly
touches the lower teeth with the tip of the tongue and
exhales air between the teeth. “Chui” requires the lips,
and the tongue, the corners of the mouth, and the lips
should be pulled back, keeping the back teeth parallel
to allow breath to be exhaled from the throat, between
the sides of the tongue and the opened lips. The
pronunciation of “Xi” is assisted by the teeth. The tip
of the tongue should touch the lower teeth so that the
corners of the mouth are slightly tipped back, the
posterior teeth are closed gently, and air is exhaled
from the gap between the posterior teeth [17–19].
Outcome Measures
The following data were obtained by a telephone
questionnaire during the COVID-19 outbreak, among
patients who completed the intervention for 12 weeks.
The self-rating anxiety scale (SAS) was designed by
Zung [20], in 1971, and consists of 20 items for the
assessment of subjective symptoms among anxiety
patients. The responses are given on a 4-point scale,
ranging from 1 (none, or a little of the time) to 4 (most,
or all of the time). Participants were asked to respond
to the questionnaire based on their experiences over
the previous week. Items included both negative and
positive experiences, with the latter being
reverse-scored. Larger scores indicated higher degrees
of anxiety. The SAS has been evaluated for internal
consistency (Cronbach’s alpha = 0.82) [21] and
concurrent validity (r = 0.30 with the Taylor Manifest
Anxiety Scale) [20].
Relevant information during the epidemic. We
designed this questionnaire based on current reports
regarding the psychological impacts of the COVID-19
epidemic [22–24] (Table 1). Participants were asked to
complete this questionnaire via phone interviews,
which included questions regarding life, disease, and
exercise during the epidemic. Each question was a yes
or no question, except for “How much has the outbreak
affected your life”, with response options never, a little,
and so much, “Are you worried about the epidemic”,
with response options never, a little, and so much,
“How often do you go out during the epidemic”, with
response options never, sometimes, and every day, and
“Do you take drugs regularly during the epidemic”,
with responses regularly, irregularly, and withdrawal.
The answers to each question are expressed as a
percentage (%).
Analysis of the related factors influencing SAS
scores. To demonstrate that LQG represents an
influencing factor on the SAS score during the
epidemic, the following potential influencing factors
that may affect the SAS scores were included, based
on relevant literature. (1) Baseline characteristics: age
[25], gender [26], severity of airflow limitations [27],
place of residence [28], and living status [23]. (2)
Relevant information during the epidemic [22–24]. (3)
Course of COPD assessment test (CAT) score [29–30]:
an 8-item unidimensional measure of health status
impairment associated with COPD, including the
impacts of cough, sputum, dyspnea, and chest tightness
on health status. The score ranges from 0–40 [15],
0–10 points: “slight impact”, 11–20 points: “moderate
impact”, 21–30 points: “serious impact”, and 31–40
points: “very serious impact” [31]. (4) Baseline SAS
scores [23]. (5) Grouping: PR group and control group.
Statistical analysis
All data are presented as the mean standard deviation
(SD) or n (%), as specified. Student’s t-tests were used
to compare the ages and CAT scores between the two
groups. We used Pearson’s Chi-squared tests to exam
the following factors: gender, and items 9, 11, and 12
in the self-designed questionnaire. Continuous
correction Chi-squared tests were used to test items 2,
7, and 8 in the self-designed questionnaire. Fisher’s
exact test was used to test “Place of residence”,
“Living status”, and items 6 and 10 in the
self-designed questionnaire. Mann-Whitney U tests
were used to test the “Severity of airflow limitation”,
and items 3 and 5 in the self-designed questionnaire.

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To analyze the SAS scores between the two groups, we
first used a 2-sample rank-sum test and then used an
analysis of covariance (ANCOVA). Baseline SAS
scores were used as a covariate, group was set as a
fixed factor, and SAS scores during the epidemic were
the dependent variable. The hypothesis test examines
whether a linear relationship exists between the
covariate and the dependent variables. Multiple linear
regression analyses (step-wise) were performed to
examine the factors that can influence anxiety. The
clinical outcomes included explanatory variables, and
the SAS scores were the response variable. All
analyses were performed using the Statistical Package
for the Social Sciences, version 21.0 for Windows
(BMI SPSS 21.0), with the level of significance set at
5.0%.
Results
Baseline characteristics of participants
A total of 60 patients with stable COPD were selected.
Figure 1 shows a flow diagram of the entire study.
Initially, 33 cases were assigned to the PR group,
including 5 cases who dropped out during the study,
and 7 cases lost to follow-up during the epidemic. The
final sample included 21 patients in the PR group,
consisting of 11 females and 10 males. The minimum
age was 60 years, the maximum was age was 80 years,
and the mean age was (67.48 ± 5.05) years. The
severity of airflow limitation was evaluated using
GOLD levels 1, 2, 3, and 4 [13], which refers to the
guidelines most doctors use to classify and treat COPD,
and these levels accounted for 4.76%, 33.33%, 52.38%,
and 9.52% of the PR population, respectively. Initially,
27 cases were assigned to the control group, including
no individuals who dropped out during the study, and 3
cases lost to follow-up during the epidemic. The final
sample included 24 patients, including 6 females and
18 males. The youngest was 56 years, the oldest was
76 years, and the mean age was (67.63  5.17) years.
GOLD 1, 2, 3, and 4 levels accounted for 12.50%,
12.50%, 70.83%, and 4.17%, respectively.
Table 1 Questionnaire regarding relevant information during the epidemic
For each item below, please place a checkmark ( ) in the column which best describes how often you felt or
behaved this way during the past several days.
Life
1 Is there someone nearby diagnosed with COVID-19? ( ) Yes ( ) No
2 Do you have enough masks? ( ) Yes ( ) No
3 How much has the outbreak affected your life?
( ) Never
( ) A little
( ) So much
4 Do you focus on the epidemic? ( ) Yes ( ) No
5 Are you worried about the epidemic?
( ) Never
( ) A little
( ) So much
6 How often do you go out during the epidemic?
( ) Never
( ) Sometimes
( ) Every day
Disease
7 Do you have exacerbation(s) of COPD during the epidemic? ( ) Yes ( ) No
8 Do you have cold(s) during the epidemic? ( ) Yes ( ) No
9 Do you have enough COPD-related drugs? ( ) Yes ( ) No
10 Do you take drugs regularly during the epidemic?
( ) Regularly
( ) Irregularly
( ) Withdrawal
Exercise
11 Do you practice LQG during the epidemic? ( ) Yes ( ) No
12 Do you practice other exercises during the epidemic? ( ) Yes ( ) No
COPD, chronic obstructive pulmonary disease; LQG, Liuzijue Qigong; COVID-19, coronavirus disease 2019.

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Assessed for eligibility (n = 60)
Randomized (n = 60)
PR (n = 33) Control (n = 27)
Control (n = 27)
Excluded (n = 0)
Not eligible for stable COPD diagnosis (n = 0)
With other unstable disease(s) (n = 0)
Cognitive impairment and mobility limitation (n = 0)
Abandoned program (n = 5) Abandoned program (n = 0)
Lost to follow up (n = 7) Lost to follow up (n = 3)
Telephone questionnaire
12-week intervention
Control (n = 24)
PR (n = 21)
PR (n = 28)
During the epidemic
Obtained baseline characteristics of participants
Figure 1 Flowchart of study design. COPD, chronic obstructive pulmonary disease; PR, pulmonary rehabilitation.
Among the two groups, 91.11% of patients lived in
cities and 95.56% lived with their families. The mean
CAT score was (16.67 ± 5.52), which indicated that
COPD had a “moderate impact” on patients. No
significant differences were identified among the
demographic and clinical characteristics between the
two groups (P > 0.05), except for the SAS scores,
which were higher in the PR group. The baseline
features of the two groups are presented in Table 2.
Scores of SAS
The ANCOVA analytic method, adjusted for baseline
characteristics has been used in previous studies to
investigate differences between groups and
demonstrate certain feasibilities [32–34]. In our study,
the results of the ANCOVA, adjusted for baseline
scores, showed a significant difference in
between-group SAS scores (F = 9.539, P = 0.004). The
results of paired Student’s t-tests for SAS scores
showed remarkable decreases in both groups (all P <
0.01). After the 12-week intervention, the SAS score
for the PR group was 27.86 ± 3.47, which dropped to
14.76 ± 5.63 during the epidemic period, representing
an approximately 53.99% reduction; the SAS score for
the control group was 30.21 ± 4.40 and dropped to
6.04 ± 8.33 during the epidemic period, representing
an approximately 20.00% reduction. Outcome analysis
showed that LQG was able to effectively improve
COPD patients’ anxiety. The highest-scoring factor in
the SAS was “I fall asleep easily and get a good
night’s sleep” (reverse score). The estimation of “I can
breathe in and out easily” in the PR group (1.14 ± 0.36)
was lower than that in the control group (1.54 ± 0.72),
and the difference was statistically significant (P =

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0.035, Table 3 and Table 4).
Relevant information during the epidemic
Three aspects were assessed during the epidemic, as
shown in Table 5. (1) Life. The answers of never, a
little, and so much in response to the question “How
much has the outbreak affected your life” were 23.81%,
61.90%, and 14.29%, respectively, in PR group and
4.17%, 58.33%, and 37.50%, respectively, in the
control group, and the difference between the two
groups was significant (P = 0.023). No significant
differences between these two groups were observed
for the questions “Is there someone nearby diagnosed
with COVID-19”, “Do you have enough masks”, “Do
you focus on the epidemic”, “Are you worried about
the epidemic”, and “How often do you go out during
the epidemic”. (2) Disease. No significant differences
were detected in terms of disease between the two
groups. (3) Exercise. Among the PR group, 80.95% of
patients continued to practice LQG at home during the
epidemic, and the differences between “Do you
practice LQG during the epidemic” and “Do you
practice other exercises during the epidemic” between
the two groups were significant (P < 0.05). In the
control group, 29.17% of patients performed exercise
during the outbreak, while the remaining participants
(70.83%) did not perform any exercise.
Analysis of the related factors influencing SAS
scores
A total of 15 factors, such as gender, were included in
a multivariate analysis. Ultimately, we selected 4
variables in the model, which could explain 41.20% of
the variations in responses (P < 0.001). Group was
able to significantly predicted anxiety (b = −3.907, t =
−3.824, P < 0.001), as did CAT scores (b = 0.309, t =
2.876, P = 0.006), SAS scores at baseline (b = 0.189, t
= 3.074, P = 0.004), and living in a village (b = 4.886,
t = 2.085, P = 0.043). The standardized coefficients
demonstrated the relationships and strengths of each
predictor. Based on the summary shown in Table 6, the
fitted regression model could be listed as follows:
where Y is the response variable, SAS scores, X1 is
CAT scores, and X3 is baseline SAS scores collected
before patients were taught to perform LQG exercises.
X2 refers to the group, as follows:
τj is the fixed explanatory factor, accommodation,
where j indicates the different accommodation={“city”,
“towns”, “village”}, with the constraint: τj = τcity = 0.
Table 2 Baseline characteristics of participants
Characteristics Total PR Control Statistic P-value
Number (n (%)) 45 21 (46.67) 24 (53.33) – –
Age, years (mean ± SD) 67.56 ± 5.06 67.48 ± 5.05 67.63 ± 5.17 −0.970 0.923
Gender (n (%))
Male
female
28 (62.22)
17 (37.78)
10 (47.62)
11 (52.38)
18 (75.00)
6 (25.00)
3.572 0.059
Severity of airflow limitation (n (%))
GOLD1
GOLD2
GOLD3
GOLD4
4 (8.89)
10 (22.22)
28 (62.22)
3 (6.67)
1 (4.76)
7 (33.33)
11 (52.38)
2 (9.52)
3 (12.50)
3 (12.50)
17 (70.83)
1 (4.17)
239.500 0.742
Place of residence (n (%))
City
Town
Village
41 (91.11)
2 (4.44)
2 (4.44)
20 (95.23)
0
1 (4.76)
21 (87.50)
2 (8.33)
1 (4.17)
1.707 0.741
Living status (n (%))
Solitude
Living with family
2 (4.44)
43 (95.56)
1 (4.76)
20 (95.23)
1 (4.17)
23 (95.83)
0.009 1.000
CAT scores (mean ± SD) 16.67 ± 5.52 17.71 ± 4.81 15.75 ± 6.02 1.022 0.238
SAS scores (mean ± SD) 39.22 ± 8.49 42.62 ± 6.52 36.25 ± 9.01 −2.679 0.007
COPD, chronic obstructive pulmonary disease; PR, pulmonary rehabilitation; SAS, self-rating anxiety scale;
GOLD, Global Initiative for Chronic Obstructive Lung Disease; SD, standard deviation; CAT, course of COPD
assessment test; –, not mentioned.

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Table 3 Changes in the SAS scores for the two groups before and after the study
PR group Control group
ANCOVA
F
ANCOVA
P
Mean ± SD
Paired t-test
P
Mean ± SD
Paired t-test
P
Total scores
(baseline)
42.62 ± 6.52
< 0.001
36.25 ± 9.01
0.002 9.539 0.004
Total scores
(outbreak)
27.86 ± 3.47 30.21 ± 4.40
PR, pulmonary rehabilitation; SAS, self-rating anxiety scale; SD, standard deviation; ANCOVA, analysis of
covariance.
Table 4 Statistics of each item of SAS scale during COVID-19
Questions PR Control Mann-Whitney U Z P value
1 I feel more nervous and anxious
than usual
1.24 ± 0.44 1.38 ± 0.65 233.500 −0.546 0.585
2 I feel afraid for no reason at all 1.19 ± 0.40 1.08 ± 0.28 225.000 −0.043 0.297
3 I get upset easily or feel panicky 1.14 ± 0.36 1.25 ± 0.53 234.000 −0.617 0.537
4 I feel like I’m falling apart and
going to pieces
1.00 ± 0.00 1.00 ± 0.00 252.000 0.000 1.000
5 I feel that everything is all right
and nothing bad will happen
1.00 ± 0.00 1.13 ± 0.34 220.500 −1.658 0.097
6 My arms and legs shake and
tremble
1.05 ± 0.22 1.17 ± 0.57 242.000 −0.526 0.599
7 I am bothered by headaches neck
and back pain
1.24 ± 0.44 1.33 ± 0.48 228.000 −0.695 0.487
8 I feel weak and get tired easily 1.29 ± 0.56 1.50 ± 0.66 207.000 −1.237 0.216
9 I feel calm and can sit still easily 1.00 ± 0.00 1.08 ± 0.28 231.000 −1.338 0.181
10 I feel my heart beating fast 1.14 ± 0.36 1.21 ± 0.41 235.500 −1.567 0.571
11 I am bothered by dizzy spells 1.05 ± 0.22 1.08 ± 0.28 243.000 −0.474 0.636
12 I have fainting spells or feel like it 1.05 ± 0.22 1.00 ± 0.00 240.000 −1.069 0.285
13 I can breathe in and out easily 1.14 ± 0.36 1.54 ± 0.72 178.500 −2.108 0.035
14 I get feelings of numbness and
tingling in my fingers & toes
1.00 ± 0.00 1.08 ± 0.28 231.000 −1.338 0.181
15 I am bothered by stomach aches
or indigestion
1.14 ± 0.48 1.17 ± 0.48 245.000 −0.292 0.770
16 I have to empty my bladder often 1.19 ± 0.51 1.50 ± 0.72 193.500 −1.719 0.086
17 My hands are usually dry and
warm
1.00 ± 0.00 1.17 ± 0.38 210.000 −1.938 0.053
18 My face gets hot and blushes 1.00 ± 0.00 1.00 ± 0.00 252.000 0.000 1.000
19 I fall asleep easily and get a good
night’s sleep
1.38 ± 0.67 1.63 ± 0.77 207.500 −1.175 0.240
20 I have nightmares 1.24 ± 0.44 1.21 ± 0.41 244.500 −0.237 0.813
COVID-19, coronavirus disease 2019; PR, pulmonary rehabilitation; SAS, self-rating anxiety scale

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Table 5 Relevant information during the epidemic
Variables Total PR Control Statistic P-value
Life
1 Is there someone nearby diagnosed with COVID-19 (n (%))
Yes 0 0 0
– –
No 45 (100) 21 (100) 24 (100)
2 Do you have enough masks (n (%))
Yes 39 (86.67) 19 (90.48) 20 (83.33)
0.070 0.792
No 6 (13.33) 2 (9.52) 4 (16.67)
3 How much has the outbreak affected your life (n (%))
Never 6 (13.33) 5 (23.81) 1 (4.17)
165 0.023
A little 27 (60.00) 13 (61.90) 14 (58.33)
So much 12 (26.67) 3 (14.29) 9 (37.50)
4 Do you focus on the epidemic (n (%))
Yes 45 (100) 21 (100) 24 (100)
– –
No 0 0 0
5 Are you worried about the epidemic (n (%))
Never 12 (26.67) 7 (33.33) 5 (20.83)
235 0.653
A little 28 (62.22) 11 (52.38) 17 (70.83)
So much 5 (11.11) 3 (14.29) 2 (8.33)
6 How often do you go out during the epidemic (n (%))
Never 32 (71.11) 14 (66.67) 18 (75.00)
0.674 0.861
Sometimes 11 (24.44) 6 (28.57) 5 (20.83)
Everyday 2 (4.44) 1 (4.76) 1 (4.17)
Disease
7 Do you have exacerbation(s) of COPD during the epidemic (n (%))
Yes 3 (6.67) 2 (9.52) 1 (4.17)
0.014 0.905
No 42 (93.33) 19 (90.48) 23 (95.83)
8 Do you have cold(s) during the epidemic (n (%))
Yes 5 (11.11) 2 (9.52) 3 (12.50)
0.070 0.792
No 40 (88.89) 19 (90.48) 21 (87.50)
9 Do you have enough COPD-related drugs (n (%))
Yes 32 (71.11) 14 (66.67) 18 (75.00)
0.379 0.538
No 13 (28.89) 7 (33.33) 6 (25.00)
10 Do you take drugs regularly during the epidemic (n (%))
Regular 25 (55.56) 13 (61.90) 12 (50.00)
0.690 0.779
Irregular 10 (22.22) 4 (19.05) 6 (25.00)
Withdrawal 10 (22.22) 4 (19.05) 6 (25.00)
Exercise
11 Do you practice LQG during the epidemic (n (%))
Yes 17(37.78) 17 (80.95) 0
27.515 < 0.001
No 28(62.22) 4 (19.05) 24 (100)
12 Do you practice other exercises during the epidemic (n (%))
Yes 25 (55.56) 18 (85.71) 7 (29.17)
14.504 < 0.001
No 20 (44.44) 3 (14.29) 17 (70.83)
COPD, chronic obstructive pulmonary disease; LQG, Liuzijue Qigong; PR, pulmonary rehabilitation; COVID-19,
coronavirus disease 2019; –, not mentioned.

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Table 6 Multiple linear regression analysis of SAS scores
Variables b Std. Error t 95% CI P-value
B 19.758 2.427 8.141 14.853, 24.663 < 0.001
CAT 0.309 0.107 2.876 0.092, 0.525 0.006
Group −3.907 1.022 −3.824 −5.973, −1.842 < 0.001
SAS scores (baseline) 0.189 0.062 3.074 0.065, 0.313 0.004
Living in village 4.886 2.343 2.085 0.151, 9.622 0.043
CI, confidence interval of difference in means; B, intercept; CAT, course of COPD assessment test; R Square =
0.466, adjusted R Square = 0.412, F = 8.719, P < 0.001.
Discussion
The results suggested that LQG is beneficial for
relieving anxiety among COPD patients. Even during
the COVID-19 outbreak, compared with the control
group, the patients in the PR group considered their
lives to be less affected by the epidemic, which might
also relate to their state of mind. The autonomic
nervous system and respiratory activity have been
shown to be closely associated with the experience of
emotions [35]. Anxiety occurs when the stress
response is beyond the normal range, for an extended
duration [36], which will cause sympathetic activation
[37]. At present, the mechanism through which LQG
reduces anxiety effectively is not clear; however, many
studies have examined pursed-lip breathing and deep
breathing during LQG exercises. During LQG
exercises, participants were asked to focus on
breathing in-and-out. Breathing is a sensorimotor
behavior that is controlled by the brain; therefore, it
can be affected by training [38]. A previous study [39]
showed that pursed-lip breathing represented a change
in the breathing pattern, from a rapid respiratory rate
(associated with involuntary breathing response from
the brainstem) to a more controlled pattern (controlled
by voluntary cortical function in the brain).
Improvements in autonomic function can be observed
after the long-term practice of pranayama, whereas
parasympathetic activity increases and sympathetic
dominance decreases [40]. Furthermore, deep breaths
can assist in relieving the body’s stress response,
improving sleep, reducing muscle tension, and
decreasing the heart rate and blood pressure [41].
Another study found that deep breathing techniques
could increase the production of melatonin, which aids
in a feeling of relaxation. Our study indicated that the
most troubling symptom associated with anxiety in
patients with COPD was sleep disorder. These results
are consistent with a previous study [42]. Sleep
disturbance is a common symptom among individuals
with anxiety [43]. Hence, the shift in sympathovagal
balance induced by controlled respiration can lead to
the inhibition of negative emotions in COPD patients
[37].
COPD represents a type of chronic inflammation
that is characterized by neutrophil infiltration [44].
Another study found that the excessive or prolonged
production of proinflammatory cytokines could cause
anxiety and chronic inflammation [45]. Bratek et al.
found that anxiety test scores were positively
correlated with the relative number of neutrophils in
induced sputum. Therefore, systemic inflammation
may represent a key link between anxiety and COPD.
Thus far, studies examining proinflammatory
mediators have focused on interleukin-1 beta, tumor
necrosis factor-alpha, and C-reactive protein [46].
Moreover, nicotine dependence due to smoking can
partly explain the association between COPD and
anxiety [47] (Figure 2).
Compared with previous studies, which reported
high dropout rates among the PR group, 80.95% of
patients in this study effectively learned LQG and were
able to consciously practice the exercises at home.
LQG is a more attractive and interesting form of PR
than usual PR training and can help COPD patients in
the long-term. In addition, LQG does not require large
venues or expensive equipment, making it an easily
available and low-cost option among available PR
interventions. Performing PR exercises in community
and family settings has been shown to be as effective
as performing the same exercises in hospitals [48, 49].
In this study, paired Student’s t-tests comparing SAS
scores in the two groups indicated significant
differences in the scores before and after our study (all
P < 0.01). However, previous studies have not
observed similar results. These results may be due to
our study population not being located in an area with
a severe epidemic, and recent solutions designed to
respond to the epidemic have been very positive and
effective in China. In addition, both groups received
usual care, including smoking cessation and education,
which might decrease the SAS scores, independent of
PR interventions.
By building the regression model in our study, we
found that group was the only factor that affected

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anxiety. As a PR exercise, LQG is more suitable for
people with low incomes, anxiety tendencies, and poor
quality of life. The multiple regression analysis in our
study suggested that the risk of anxiety increased
among COPD patients with higher CAT scores, higher
baseline SAS scores, or who lived in villages. A
growing body of evidence has suggested that anxiety is
associated with worse health statuses, as assessed by
CAT scores [30]. Yao et al. proposed that patients with
pre-existing mental disorders might be at higher risks
of relapse or new episodes of their disorders due to the
stress associated with the COVID-19 outbreak [50].
Living in rural areas may also increase the risk of
anxiety among COPD patients during the epidemic,
due to the reduced availability of medical resources
compared with cities [28]. COPD treatments are
primarily designed to prevent or slow disease
progression and improve quality of life [51]. Therefore,
determining which COPD patients are at particular risk
of experiencing increased anxiety during the
COVID-19 outbreak is important. LQG provides a
good treatment option that can be used to formulate
targeted PR strategies, improving the chronic disease
management of COPD in addition to managing
anxiety.
Limitations
One of the limitations of our trial is the small sample
size, which may result in the statistical bias for the
baseline and outcome assessments. Another limitation
is that we could only obtain limited information,
through telephone questionnaires, during the epidemic.
However, this study provides valuable preliminary
information regarding the effectiveness of LQG as a
PR exercise, which may represent a low-cost and
viable option for patients with COPD.
Conclusion
This study showed that anxiety among COPD patients
who completed 12 weeks of lung PR was significantly
reduced even while facing a major public health event,
the COVID-19 epidemic. LQG was able to effectively
reduce the risk of anxiety in patients with COPD and
increase stress resistance in response to emergencies.
Moreover, LQG can improve the enthusiasm and
persistence of patients for engaging in PR. Because of
the advantages of being low-cost and easily
maneuverable, the promotion and encouragement of
using LQG techniques in COPD patients should be
considered, especially in developing countries.
Figure 2 The interaction of anxiety, COPD and LQG. COPD, chronic obstructive pulmonary disease;
COVID-19, coronavirus disease 2019; LQG, Liuzijue Qigong.
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