Effects of Liuzijue Qigong on respiratory function among patients with Parkinson’s disease: a randomized clinical trial

Abstract

Background

Respiratory dysfunction is a common nonmotor symptom in patients with Parkinson’s disease that may be easily overlooked. Incorporating respiratory function rehabilitation into routine rehabilitation programs for these patients is important. However, previous studies have focused primarily on professional devices and training processes that require additional professional guidance, making wide implementation challenging.

Methods

In this assessor-masked, randomized clinical trial, eligible participants were randomized into an experimental group and a control group. The experimental group received Liu Zi Jue Qigong exercise for 12 weeks, while the control group underwent conventional rehabilitation exercises. Primary outcomes included measures of respiratory function, such as forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1), the ratio of forced expiratory volume in 1 s to forced vital capacity(FEV1/FVC), peak expiratory flow (PEF), maximal inspiratory pressure (MIP), and maximal expiratory pressure (MEP). Secondary outcomes included motor symptoms, quality of life, depression, and anxiety.

Results

The results from a study involving 51 Parkinson’s disease patients showed significant improvements in the FVC, FEV1, PEF, and MEP in the experimental group compared to those in the control group after the 12-week intervention. Additionally, there was a noticeable decrease in depression and anxiety scores in the experimental group, with statistically significant reductions compared to those in the control group.

Conclusions

Liuzijue Qigong exercise has the potential to enhance respiratory function and mental health in patients with Parkinson’s disease in the early and middle stages. These findings could serve as a valuable reference for implementing home-based rehabilitation techniques for individuals with Parkinson’s disease.

Trial Registration

Chinese Clinical Trial Registry: ChiCTR2200056762(Retrospectively registered, Registration Date: February 15, 2022).

Background

Parkinson’s disease (PD) is a prevalent neurodegenerative condition among elderly individuals characterized by a range of motor and nonmotor symptoms [1]. Respiratory dysfunction, although a common nonmotor symptom in PD patients, is often underestimated. Studies have reported that the incidence of restrictive ventilation dysfunction is 28-94% [2,3,4], and the incidence of upper airway obstruction is 6.7-67.0% [3, 5, 6]. The motor impairments and altered perception of hypoxemia in PD can mask respiratory symptoms, leading to potential complications such as aspiration pneumonia and dyspnea [7]. Research has shown that respiratory muscle weakness can contribute to various issues, such as swallowing difficulties, speech disorders, weak coughing, and breathlessness, in PD patients, significantly impacting their quality of life [2, 8]. Additionally, respiratory failure is a leading cause of mortality in advanced PD patients [9, 10]. Hence, integrating respiratory function rehabilitation into the overall care plan for Parkinson’s disease patients is crucial for improving patient outcomes and quality of life.

A recent systematic review on the effects of respiratory muscle training for patients with Parkinson’s disease (PD) concluded that respiratory exercises have positive effects on PD patients, leading to improvements in respiratory function [11]. Specifically, inspiratory muscle training has been found to effectively enhance cardiopulmonary function and exercise capacity and reduce fatigue. On the other hand, expiratory muscle training can enhance airway clearance and protect the airway. However, the current training methods discussed in recent studies often involve the use of specialized devices and require additional professional guidance during practice, making them challenging to widely implement, especially for PD patients at home [12,13,14]. Consequently, patient compliance tends to be low, and adherence to the training regimen can be difficult. Therefore, it is crucial to explore a convenient, simple, and user-friendly approach to respiratory rehabilitation that can be easily adopted by PD patients to promote better compliance and overall effectiveness.

Liuzijue Qigong, a traditional Chinese health exercise, emphasizes breathing and exhalation.In 2007, the General Administration of Sport in China redefined Liuzijiu, forming a standardized and comprehensive qigong training protocol [15]. This protocol integrates several components of modern pulmonary rehabilitation, like physical exercise, respiratory muscle conditioning, and psychological support, in line with the primary criteria.Liuzijiu is characterized by exhaling while reciting six specific words: ‘xu,’ ‘he,’ ‘hu,’ ‘si,’ ‘chui,’ and ‘xi,’ and utilizing deep, slow breathing with reverse abdominal respiration to strengthen respiratory muscle function The physical exercises within Liuzijiu target the full body’s muscles, with a particular emphasis on the skeletal muscles of the arms and legs.Liuzijiu also aims to bolster the mental resilience of individuals undergoing the training.

Liuzijue is characterized by its strengths in safety, efficacy, and economic viability. the practice involves uncomplicated movements, with a manageable exercise intensity and controllable exercise volume and duration.Numerous studies have validated the rehabilitative benefits of Liuzijue. Comprehensive analyses indicate that Liuzijue can significantly enhance the quality of life, exercise capacity, and pulmonary function in patients with chronic obstructive pulmonary disease (COPD) [16].Liuzijue exercise showed more changes than conventional respiratory training in improving trunk control ability, respiratory muscle functions, and activities of daily living ability in patients at an early recovery stage from stroke [17]. A research showed that Liuzijue and Tai chi might be the most significantly effective mind-body exercise intervention for mitigating depression among breast cancer survivors [18]. Additional, Liuzijue is an affordable option to learn, featuring a small set of movements that are simple to grasp. The practice does not necessitate any specific location or equipment, making it accessible and cost-efficient to implement.

In this study, we aimed to explore the use of Liuzijue Qigong as a home exercise regimen to assess its impact on respiratory function and quality of life in Parkinson’s disease patients. By doing so, we seek to offer PD patients a practical and suitable home rehabilitation technique.

Methods

Design

This single-blind randomized controlled trial received approval from the Medical Ethics Committee of the First Affiliated Hospital of Chongqing Medical University (reference No: 2021 − 550) and was registered on the Chinese Clinical Trials Registry Platform (Identifier: ChiCTR2200056762). The trial adhered to the Consolidated Standards of Reporting Trials guidelines and followed the ethical standards outlined in the Declaration of Helsinki. All participants provided written informed consent, and their data were anonymized.

To prevent any “contamination” of the intervention study, participants were clearly informed during the informed consent process that the study was exploratory in nature and that its effectiveness could not be predetermined. Upon completion of the study, relevant information and videos will be made available for publication. Participants in the control group had the option to download and study this material if they were interested, but they were instructed not to practice it during the study to prevent interference with the results.

Participants

The study was conducted at the First Affiliated Hospital of Chongqing Medical University from July 2021 to March 2023. Participants were recruited through convenience sampling from the Outpatient Department of Neurology. The inclusion criteria were as follows:

• 1. Individuals diagnosed with PD [19].

• 2. Patients at H-Y stage 1–3.

• 3. The dosage and type of oral anti-Parkinson’s drugs were stable for the past 3 months.

The exclusion criteria included the following:

• 1. Current use of medications that may affect muscle structure and lung function (such as corticosteroids, immunosuppressants, etc.).

• 2. History of severe skeletal and spinal deformities.

• 3. History of other diseases causing respiratory muscle damage.

• 4. Patients with severe cognitive impairment.

• 5. Patients with concurrent lung infections.

The dropout criteria were defined as follows:

• 1. Unwillingness to continue training and voluntary withdrawal during the trial.

• 2. Loss to follow-up or missed scheduled revisits.

• 3. Noncompliance with the study’s training regimen (total training frequency < 70% or each training session less than 70% of the required time and intensity).

• 4. Concurrent adoption of other respiratory rehabilitation training methods or participation in other drug trials.

Screening, baseline testing, and randomization

After prescreening in the Neurology Outpatient Department, eligible participants underwent baseline assessments. Subsequently, the participants were randomly assigned to either the experimental or control group at a 1:1 ratio using the random number table method.

Intervention

Both groups were provided with an information booklet containing instructions for home practice and maintained their original doses of anti-Parkinson medications. Any changes in medication were carefully recorded by the observer, who also calculated whether the equivalent dose of levodopa was altered.

The control group engaged in rehabilitation program at home that included gait training, core muscle group exercises, and activities focused on enhancing daily living abilities. The specific training components and intensity were tailored to each participant’s functional status and exercise habits. The regimen was reviewed by two physiotherapists to ensure its effectiveness. Each training session lasted 30 min and was conducted once a day, five days a week, over a period of 12 weeks.

Participants in the experimental group underwent Liuzijue Qigong training, which was designed based on the Liuzijue Qigong manual (People’s Sports Press, 2021, Fig. 1) published by the State Sports General Administration. This practice involved controlled inhalation through the nose and exhalation through various mouth forms, represented by the sounds Xu, He, Hu, Si, Chui, and Xi. The respiratory flow was required to be slow and continuous and synchronized with body movements (see supplemental appendix S1). Each sound was repeated six times, with each session lasting 30 min. Training was conducted once daily, five days a week, for a total of 12 weeks. After one week of learning, the participants officially commenced the trial. To support home practice, participants were provided with a video recording by the experimenter. While participants were not expected to achieve perfect pronunciation or exact limb movements, the primary focus was on mastering the coordination of breathing and pronunciation.

Fig. 1

The body movements and mouth shape of Liuzijue Qigong

Outcome measures

All participants underwent standardized assessments conducted by the experimenter both before and after the 12-week intervention period. The outcome assessors will be blinded to the patients’ group allocation.In cases where participants experienced motor complications such as wearing off or on-off phenomena, assessments were carried out during the drug onset or “on” period to ensure consistency and accuracy in the evaluation process.

Primary outcome

The primary outcome measure was respiratory function, which was assessed using a portable pulmonary function instrument (XEEK, X1, Xiamen, China), It will automatically generate estimated values for various examination indicators based on the height, weight, and age of the examinee. The estimated values are obtained by referring to the 2017 Chinese 4–80 year old population lung ventilation function estimation equation. After the examinee completes the examination, the results are expressed as measured values, estimated values, and percentages of estimated values. The participant needs to sit on a chair, step on the ground with both feet, wear a nose clip, and use a disposable mouth for testing.Before the examination, experimenter will introduce, demonstrate, and guide the examinee through the inspection actions, following the guidelines for pulmonary function and respiratory muscle strength examinations jointly published by the American Thoracic Society (ATS) and the European Respiratory Society (ERS) in the European Respiratory Journal.To ensure accuracy and reliability, each index was measured three times, and the best result was recorded as the final outcome.The following parameters were used, including forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1),the ratio of forced expiratory volume in 1 s to forced vital capacity(FEV1/FVC), peak expiratory flow (PEF), maximal inspiratory pressure (MIP), and maximal expiratory pressure (MEP).

Secondary outcomes

In addition to the primary outcome measure of respiratory function, secondary outcomes included the Movement Disorder Society-Unified Parkinson’s Disease Rating Scale Part III (MDS-UPDRS-III), the 39-item Parkinson’s Disease Questionnaire (PDQ-39), the Hamilton Depression Scale (HAMD) and the Hamilton Anxiety Scale (HAMA). These secondary outcome measures were utilized to assess various aspects related to Parkinson’s disease symptoms, quality of life, depression, and anxiety levels among the participants.

Adverse events

During the intervention sessions, adverse events were monitored by assessing participants for any significant discomfort, pain, or harm resulting from the intervention. Participants were instructed to promptly inform the research team if they experienced any adverse events related to the study. This proactive approach ensured that any potential negative effects of the intervention could be identified and addressed promptly to safeguard the well-being of the participants.

Statistical methods

The data analysis was conducted using the statistical software SPSS (version 25.0). Continuous variables with a normal distribution are presented as the mean ± standard deviation (SD), nonnormally distributed data are presented as the median (interquartile range [IQR]), and categorical variables are presented as the number (percentage).

For variables that met the assumptions of a normal distribution and homogeneity of variance, a paired sample t test was used to analyze differences within the group, while an independent samples t test was used to compare differences between groups. In cases where the data did not meet the requirements for parametric tests, the Wilcoxon signed-rank test was employed to compare differences within the group, and the Mann‒Whitney U test was used to compare differences between groups. A p value less than 0.05 was considered to indicate a significant difference between the results.

Results

A total of 94 patients with Parkinson’s disease were initially screened for the study. Of these, 19 patients did not meet the eligibility criteria, and an additional 15 patients declined to participate, resulting in an enrollment rate of 63.8% (Fig. 2). The 60 participants who were randomized were evenly divided into a control group and an experimental group, with 30 patients in each group. During the course of the experiment, 5 patients from the experimental group withdrew from the study, while 4 patients from the control group refused to participate in the follow-up. Ultimately, 51 participants (85%) completed the intervention, with 25 in the experimental group and 26 in the control group. This resulted in an overall dropout rate of 15% (9 out of 60). The compliance rates for home practice during the intervention period were 83.3% (25 out of 30) for the Liuzijue group and 86.7% (26 out of 30) for the control group. These compliance rates indicate the level of adherence to the prescribed home practice regimen during the study.

Fig. 2

Flow Diagram

Baseline characteristics of the participants

Table 1 Presents the baseline demographic and clinical characteristics of the participants included in the study. There were no statistically significant differences observed between the intervention and control groups. The mean (SD) age of the participants was 57.92 (9.14) years, with an age range of 49 to 82 years. Of the 51 participants, 27 were female, accounting for 52.94% of the total. The mean (SD) BMI (body mass index) of the participants was 20.74 (1.96). The mean (SD) duration of the disease among the participants was 6.09 (3.56) years, with a range of 1 to 12 years.

Tabel 1 Baseline comparision of demographics between the two groups

Primary outcome

Table 2 presents the comparisons of within-group outcomes, while Table 3 illustrates the changes in the main outcomes between the two groups after treatment. In this study, FVC, FEV1, FEV1/FVC, PEF, MIP, and MEP were utilized to assess respiratory function. After the treatment period, the experimental group exhibited significant improvements in FVC, FEV1, PEF, and MEP (FVC: 0.39 [95% CI, 0.11 to 0.54]; P = 0.033; FEV1: 0.45 [95% CI, 0.18 to 0.71]; P = 0.024; PEF: 0.62 [95% CI, 0.03 to 1.11]; P = 0.049; MEP: 8.71 [95% CI, 0.08 to 15.67]; P = 0.046). Moreover, compared to those in the control group, these improvements were statistically significant (FVC: 0.46 [95% CI, 0.02 to 0.91]; P = 0.003; FEV1: 0.33 [95% CI, 0.01 to 0.76]; P = 0.021; MEP: 5.35 [95% CI, 0.54 to 12.16]; P = 0.047).

Table 2 Comparison of the Treatment Effects Between 2 Groups and Baseline

Table 3 Comparison of outcomes Between Two Groups After treatment

Secondary outcomes

The study utilized the MDS-UPDRS-III and PDQ-39 as secondary outcome measures to evaluate the motor function and quality of life of the participants. In the experimental group, significant reductions in PDQ-39 scores were observed postintervention compared to preintervention (-4.82 [95% CI, -7.35 to -1.51]; P = 0.036). In the control group, both the MDS-UPDRS-III and PDQ-39 scores decreased significantly from baseline (MDS-UPDRS-III: -2.35 [95% CI, -4.66 to 0.64]; P = 0.037; PDQ-39: -2.82 [95% CI,-5.64 to -0.66]; P = 0.042). At the end of the treatment period, there was no statistically significant difference in the improvement in the MDS-UPDRS-III and PDQ-39 scores between the two groups (MDS-UPDRS-III: 2.35 [95% CI, -6.35 to 11.05]; P = 0.088; PDQ-39: -1.56 [95% CI, -4.67 to 2.81]; P = 0.157).

Furthermore, the mental states of the participants were assessed using HAMD and HAMA scores. In the experimental group, there were significant reductions in both the HAMD and HAMA scores at the end of the treatment period (HAMD: -0.96 [95% CI, -2.57 to -0.31]; P = 0.042; HAMA: -1.07 [95% CI, -2.34 to -0.49]; P = 0.037). Compared to those in the control group, the reductions in HAMD and HAMA scores were statistically significant (HAMD: 0.32 [95% CI, 0.12 to 0.57]; P = 0.043; HAMA: 0.35 [95% CI, 0.08 to 0.77]; P = 0.031).

Adverse events

One participant (4.0%) from the experimental group reported temporary mild backache, which resolved with the use of plaster. Two participants (7.7%) from the control group reported temporary mild knee pain when stretching but required no medical attention. No serious adverse events were reported.

Discussion

To our knowledge, this is the first randomized clinical trial targeted at determining the effectiveness of Liuzijue Qigong on respiratory function in patients with PD. Our results indicate that Liuzijue Qigong can improve the lung function, including expiratory function and respiratory muscle strength, of PD patients and has a beneficial effect on regulating the patient’s mood.

Liuzijue Qigong, a traditional Qigong practice centered around breathing and exhaling, involves six unique methods of exhaling accompanied by simple body movements and mental focus. It follows the fundamental principles of “nose breathing, mouth exhaling, deep and slow breathing” for respiratory training. This type of breathing, akin to pursed-lip breathing, utilizes specific sounds in practice to serve distinct purposes. For example, the sound “xu” in Liuzijue Qigong simulates pursed-lip breathing through slow exhalation with the accompanying sound, aiding in maintaining proper airway pressure, preventing premature closure of the airway, and reducing airway obstruction. By adjusting the breathing pattern through lowering the respiratory rate and prolonging exhalation, pulmonary ventilation is enhanced [20, 21]. The controlled slow exhalation exercises in Liuzijue Qigong engage and strengthen the respiratory muscles, thereby improving respiratory efficiency and lung ventilation function. Unlike simple pursed-lip breathing, Liuzijue Qigong involves corresponding movements with each sound, primarily involving bilateral upper limb abduction or raising. These movements help increase the body’s intake and expand chest capacity, ultimately enhancing respiratory function. Given that Parkinson’s disease can lead to restricted chest expansion due to abnormal posture, gait, and muscular rigidity, resulting in reduced lung capacity and restrictive pulmonary disease [22], the combination of breathing techniques and movements in Liuzijue Qigong may offer advantages in improving respiratory function beyond simple pursed-lip breathing alone.

Our study did not demonstrate improvements in physical outcomes related to motor symptoms or mobility compared to those of the control group. One possible explanation for this discrepancy could be the nature of the movements involved in Liuzijue Qigong. Liuzijue Qigong primarily focuses on breathing techniques and simple body movements, with less emphasis on active engagement of the legs. In contrast, the control group engaged in exercises specifically designed to target the motor symptoms of Parkinson’s disease, such as gait training and balance training. These findings highlight the importance of considering the specific needs and symptoms of patients with PD when designing intervention programs. Tailoring interventions to address diverse aspects of the condition, including both motor and nonmotor symptoms, may lead to more comprehensive and effective treatment outcomes.

The experimental group demonstrated a more significant reduction in depression and anxiety symptoms than did the control group at the conclusion of the intervention. Liuzijue Qigong, an exercise technique that harmonizes movement, breath, and mindfulness, emphasizes the guidance of qi with the mind and body. During practice, the use of elegant music and gentle movements aids in relaxing the body and mind, potentially stimulating the vagus nerve, thereby reducing stress and alleviating anxiety [23]. Moreover, the incorporation of abdominal core muscle training and limb-guiding actions within Liuzijue Qigong can improve body flexibility, enhance balance, and boost attention and concentration. These benefits contribute to the overall improvement of physical and mental health [24]. Additionally, the social interactions fostered by engaging in Liuzijue Qigong can help individuals with Parkinson’s disease establish robust support networks, easing feelings of loneliness and psychological strain [25]. Numerous studies have demonstrated the positive impact of Qigong-based interventions on the physical and mental well-being of patients with chronic conditions [26, 27].

Both groups exhibited significant decreases in PDQ-39 scores compared to preintervention scores, without any statistically significant differences. It is widely recognized that the quality of life of individuals with Parkinson’s disease can be impacted in a multidimensional manner, encompassing physical function, mental health, and social support [28]. In our study, the control group experienced an improvement in quality of life primarily through the amelioration of motor symptoms. In contrast, Liuzijue Qigong contributed to overall enhancement by addressing both physical and mental states. This finding aligns with findings from another study, which also supports the effectiveness of Qigong in enhancing motor function, mental health, and quality of life in patients with mild to moderate Parkinson’s disease.

These results underscore the holistic benefits of integrating practices such as Liuzijue Qigong in the management of Parkinson’s disease. By addressing both the physical and mental aspects of the condition, approaches such as Qigong offer a comprehensive and integrative strategy to improve the well-being of individuals with Parkinson’s disease.

Conclusions

In summary, Liuzijue Qigong has shown promising benefits in improving patients’ respiratory function, enhancing quality of life, and reducing stress levels, all of which are crucial for promoting the rehabilitation of individuals with Parkinson’s disease. Moreover, the ease of operation and the flexibility of this method make it accessible and convenient for patients, as it is not constrained by space requirements. This makes it suitable for home-based practice and community settings, facilitating its widespread application and promotion among individuals with Parkinson’s disease. Overall, the positive outcomes and practicality of Liuzijue Qigong suggest its potential as a valuable addition to the holistic care and management of Parkinson’s disease.

Study limitations

This study specifically focused on Parkinson’s disease patients in the early and middle stages, highlighting the need for further research to explore the effects of rehabilitation and feasibility of implementing these interventions for advanced-stage patients. Additionally, it is important to note that the sample size in this study was relatively small, and there is a lack of follow-up tracking on the effectiveness.In future studies, expanding the sample size and adding the follow-up period will be crucial for obtaining more comprehensive and objective evidence. By conducting research with a larger and more diverse group of participants over an extended period, we can gain deeper insights into the effectiveness and long-term benefits of interventions such as Liuzijue Qigong for individuals with Parkinson’s disease across different stages of the condition.