Effectiveness of pulmonary rehabilitation in post-COVID-19 patients: A pre- and post-interventional study

ABSTRACT

Background:

The need of pulmonary rehabilitation (PR) for COVID-19 patients with long-term effects was desperately felt. The study’s objective was to measure the effect of PR on functional capacity and health-related quality of life (HRQOL) in patients with post COVID conditions.

Methods:

Pulmonary medicine department of a teaching hospital conducted this pre-experimental study. The patient underwent a pre and post-assessment, including a six-minute walk test (6MWT) measuring distance, oxygen desaturation, pulse rate, and HRQOL. The intervention had six components; education to patients and caregivers, breathlessness relieving exercises, postural correction, aerobic training, strength training, and stretching exercises. These activities were carried out twice a week for eight weeks, supervised, unsupervised in homes, and a combination.

Results:

The study enrolled 155 post-COVID patients (Males, 102 and female, 53), out of which 28 (18.1%) had mild, 55 (35.5%) had moderate and 72 (46.5%) had severe COVID. Paired t-test showed improvement in resting pulse rate (P = 0.001) and resting oxygen saturation (P < 0.0001). Distance walking for six minutes increased after rehabilitation (P < 0.0001). After eight weeks of pulmonary rehabilitation, there was an improvement (P < 0.001) in all domains of quality of life, that is, mobility, self-care, pain and discomfort, usual activity, sleep, anxiety and depression.

Conclusion:

Pulmonary rehabilitation is beneficial for post-COVID patients in improving their quality of life and six-minute walk test parameters, resulting in improved functional capacity and overall quality of life.

INTRODUCTION

Pulmonary rehabilitation (PR) awareness in the society underwent sea change during the COVID-19 pandemic at a global level. PR is a comprehensive intervention based on patient assessment followed by patient-tailored therapies that include exercise training and counselling designed to improve the physical and psychological condition of people with the chronic respiratory disease along with optimal pharmacotherapy.[1,2] PR was restricted to COPD and chronic respiratory disorders before the COVID-19 pandemic. After treating COVID-19 patients for few months, or health professionals worldwide started observing patients with post-COVID condition and realized the need for PR in these patients.[3] The COVID-19 pandemic proved to be a catalyst for increasing PR awareness in the community and, certainly, accelerating implementation of PR in eligible patients. Before the COVID pandemic, sensitization efforts about PR in the community appeared like a monologue of concerned experts. However, during the COVID pandemic, active dialogue began between various stakeholders about translating the guidelines into practice.

WHO defines Post COVID condition as ‘The illness that occurs in people with a history of probable or confirmed SARS-CoV-2 infection, usually within three months from the onset of COVID-19, with symptoms and effects that last for at least two.[4] Clinical features include fatigue, breathlessness and joint pain post-COVID period. The causes of these symptoms are multiple. Prolonged ICU stay, steroid use, post-ventilatory muscle deconditioning, extensive pulmonary involvement and post-COVID cardiac/musculoskeletal/neurological complications. Pharmacotherapy alone may not cure or alleviate these symptoms.[5] Patients need exercise training to condition the muscles and breathing exercises to reduce breathlessness. WHO and the Government of India recommended PR for the post-COVID condition.[6,7,8]

The first coronavirus case was confirmed in India on Jan 27, 2020. During the COVID pandemic, 2020-2021, Maharashtra state had many COVID-19 patients. Our private medical college and hospital in Pune, Maharashtra, was one of the COVID-19 dedicated centres during the pandemic. Approximately 10,000 patients were treated in our hospital. Post-COVID outpatient department clinic was started in August 2020 in the department of respiratory medicine. Many of these patients needed nutritional advice, psychological counselling, and exercise training; hence with corporate social responsibility (CSR) support from a company, our hospital established the PR centre in February 2021. Under this program, patients with ‘post-COVID 19 condition’ were sensitized about the advantages of PR, and eligible patients were given PR along with nutritional advice and counselling.

We undertook the study to assess the effect of PR on functional capacity and HRQOL in Post COVID patients.

MATERIALS AND METHODS

Study design and setting

This was desk research that is, an analysis of available patient data who were provided PR services. It had both components three months past data and prospectively recorded data. We compared the recorded parameters before PR and after PR. The authors conducted the study at the PR centre under the Department of Pulmonary Medicine.

Study duration

Data from February 2021 to March 2022.

Patient population

The post-COVID patients attending our pulmonary medicine department were included in the study. The patients were categorized as, mild, moderate or severe COVID disease based on ICMR (Indian council of medical research) guidelines.[9] We also collected clinical information at the time of enrolment. The inclusion criteria were patients above the age of 18 years diagnosed with post-COVID condition, visiting post-COVID clinic after 21 days of a positive RTPCR report. The exclusion criteria were patients with signs of unstable cardiovascular parameters like unstable angina, cardiac arrhythmias, uncontrolled hypertension, thromboembolic phenomenon and cognitive impairments.

The COVID patients admitted to our hospital were contacted at the time of discharge/after discharge to understand their current medical status and were counselled about the need for PR. The patients visited the Pulmonary Medicine outpatient department (OPD) for follow-up. After undergoing consultation with the pulmonologist and performing relevant investigations, the patient was enrolled in the PR program.

The PR program consisted of eight weeks of intervention in physiotherapy. Some patients express inability to come to the institutions and some agreed to attend whenever possible. They promised to follow the training instructions in home. Thus, there were three categories.

• (1)Supervised PR program: The patients may attend an eight-week PR program with twice-a-week supervised sessions either at the centre or online.
• (2)Home-based PR program: The patient may complete an eight-week PR program at home after induction at the centre. (Except using devices/equipment’s). Adherence to rehabilitation was confirmed while counselling the patients during subsequent follow-up visits in outpatient department.
• (3)Hybrid PR program: The patient may attend an eight-week PR program after induction at the centre whenever possible and remaining sessions at home.

Outcome measures

• (1)The HRQOL was measured using the EQ-5D-5L questionnaire. The HRQOL is measured under five domains: Mobility, self-care, usual activities, pain and discomfort, anxiety, and depression; we added sleep as sixth domain. The scoring was done on a Likert scale of 1 to 5 where one = ‘No problem,’ two = ‘Slight problems,’ three = ‘Moderate problems’, four = ‘Severe Problems,’ and five = ‘Extreme problems/Unable to.[10]
• (2)The functional capacity was assessed using the six-minute walk test (6MWT). This is a self-paced submaximal test where the patient walks as far as possible in six minutes and the distance in meters is recorded along with the vital parameters like pulse rate, SpO2 before test, SpO2 after test; the difference is labelled as desaturation.[2]

Intervention

The patient underwent a pre-program assessment by a physiotherapist, using a 6MWT and administering a HRQOL. Then the patient attended the first physiotherapy session or the induction session. A patient-tailored and structured exercise program was designed, considering factors like symptom assessment, age, occupation, disease severity, comorbidities, performance in a six-minute walk test, physical activity status, underlying neurological or orthopaedic condition and vital parameters.

A typical PR session lasted 45 minutes to one hour, and the exercises progressed as tolerated by the patient.

The components of the PR session were as follows;

• (1)Disease-specific patient and caregiver education.
• (2)Breathlessness relieving strategies, breathing exercises, like diaphragmatic breathing, pursed lip breathing, chest expansion exercises, and segmental breathing.
• (3)Postural correction.
• (4)Aerobic training was given for 10-15 minutes based on the above-mentioned factors and was given using a cycle ergometer or treadmill and arm ergometer. The vital parameters were monitored, and perceived dyspnoea and fatigue were recorded using the modified Borg scale.
• (5)Strength training was given using dumbbells, weight cuffs, and elastic bands, and weight was chosen as tolerated by the patient targeting major muscle groups of upper and lower limbs, that is, shoulder flexors, abductors, horizontal adductors, elbow flexors, elbow extensors, hip flexors, hip abductors, hip extensors, knee curls, knee extensors, dorsiflexors, and plantar flexors. The strengthening exercises were given with two to three sets of 10 repetitions as tolerated by the patients. Once the patient could perform three sets of 10 repetitions, the weight was increased by 0.5 kg.
• (6)Stretching exercises were given for three repetitions with a 30-second hold for each.

The authors assessed the progression based on the response to vital parameters and modified the Borg score of perceived exertion. The patient underwent a post-program assessment after completion of eight weeks from the date of the induction session, a 6MWT, HRQOL.[11,12,13,14]

Sample size and sampling

We did not calculate sample size. The authors offered services to all the patients during the period. The data collected during providing services is analysed. There was no sampling of any type.

Statistical analysis

We performed the statistical analysis using SPSS version 21. The study applied paired t-test, χ² test, and Wilcoxon signed rank test. A probability <0.05 was considered significant.

RESULTS

A total of 155 patients with post-COVID condition (males, 102 and females, 53) were enrolled in the PR program during the study period. The patients enrolled into the program and patients who completed the program along with the drop outs are mentioned in the flow chart (Figure 1: Number of patients enrolled and completed pulmonary rehabilitation program in tertiary care hospital, Pune, India). Table 1 provides the demographic characteristics of the patients. Table 2 gives some clinical information about the patients. Among comorbidities, hypertension was commonest (Figure 2: Comorbidities among patients undergone pulmonary rehabilitation in a tertiary care hospital, Pune, India, 2021-2022). Out of 155 participants, 73 (47.1%) had no associated comorbidity, and 82 (52.9%) were with comorbidity, 49 (31.6%) had one comorbidity, 28 (18.1%) had two comorbidities, 5 (3.2%) had three comorbidities. These morbidities were patient reported while taking history. Additionally, 39 patients were diagnosed diabetes during investigations. About one-third, 50 (32.3%), completed the supervised type of intervention, 42 (27.1%) completed it in their homes unsupervised, and the remaining completed it in hybrid mode (40.6%). The results in these groups were similar.

Figure 1.

Patients enrolled and completed PR Prog

Table 1.

Demographic characteristics of post COVID-19 patients of PR program from a teaching hospital, India, 2022

Demographic Characteristics	Number (%)*
Mean age in years	52.19±13.89
Gender
Males	102 (65.8%)
Females	53 (34.2%)
Education
No formal education	8 (5.2%)
Secondary education	47 (30.3%)
Higher education	21 (13.5%)
Graduation	54 (34.8%)
Post-graduation	18 (11.6%)
Missing data	7 (4.5%)
Occupation
Unemployed	5 (3.2%)
Employed	58 (37.4%)
Self-employed	30 (19.4%)
Retired	20 (12.9)
Housewife	42 (27.1%)

*Mean age in years and standard deviation

Table 2.

Clinical information of enrolled patients for pulmonary rehabilitation, from a teaching hospital, India, 2022

	Number (%)
Presenting complaints
Cough	7 (4.5%)
Breathlessness	130 (83.9%)
Fatigue	56 (36.1%)
Generalized weakness	21 (13.5%)
Knee pain	4 (2.6%)
Back pain	2 (1.3%)
Joint pain	10 (6.5%)
Lower limb pain	9 (5.8%)
Palpitations	52 (33.5%)
	Frequency
Diagnosis
Post COVID	148 (95.5%)
Post COVID + COPD	5 (3.2%)
Post COVID + ILD	1 (0.6%)
Post COVID + Asthma	1 (0.6%)
COVID-19 severity
Mild	28 (18.1%)
Moderate	55 (35.5%)
Severe	72 (46.5%)

Figure 2.

Comorbidities among patients

All four parameters of 6MWT improved after eight weeks of PR [Table 3]. Paired ‘t’ test was applied, which showed significant improvement in resting pulse rate and resting oxygen saturation, and an increase in the distance walked during six minutes after eight weeks of rehabilitation. However, the difference in mean desaturation was not significant.

Table 3.

Six-minute walk test parameters of participants before and after eight weeks of pulmonary rehabilitation in India

Pre-pulmonary rehabilitation	Post-pulmonary rehabilitation	t	P
Resting mean pulse rate (before walk test)
94.02 (16.14)	89.38 (14.25)	3.29	0.001
Resting (before walk test ) mean SpO2
95.34 (2.90)	96.30 (1.83)	-4.13	<0.0001
Mean desaturation (SpO2 difference between before and after walk test)
2.64 (2.58)	2.91 (2.69)	-0.81	0.416
Mean distance covered in meters
209.22 (159.12)	287.97 (125.78)	-7.15	<0.0001

HRQOL was another outcome parameter. Changes in scores in different domains pre- and post-PR are outlined in Table 4. HRQOL parameters are ordinal variables, so for comparing pre-PR and post-PR QOL parameters, Wilcoxon signed-rank test was applied. Results are shown in Table 4. It offers a significant increase in the number of patients reporting to have ‘No problems’ at baseline and the end of the program in all the domains of QOL, that is, Mobility (χ² = 68.26, P < 0.0001), Self-care (χ² = 83.112, P < 0.0001), Usual activity (χ² = 24.2, P < 0.0001), Pain and discomfort (χ² = 10.27, P = 0.001), Anxiety and depression (χ² = 12.08, P = 0.0005), Sleep (χ² = 5.6, P = 0.018). After eight weeks of PR, there was a statistically significant overall improvement in all domains of HRQOL.

Table 4.

Health-related quality of life levels reported as number of patients using the EQ 5D 5L Questionnaire for 155 patients, Pune

Levels (problem)	Mobility no (%)		Self-care no (%)		Usual activities no (%)		Pain and discomfort no (%)		Anxiety and depression no (%)		Sleep no (%)
	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post
Level 1 (No)	30 (19.4)	103 (66.5)	70 (45.2)	145 (93.5)	37 (23.9)	80 (51.6)	71 (45.8)	100 (64.5)	100 (64.5)	128 (82.6)	107 (69.0)	126 (81.3)
Level 2 (Slight)	49 (31.6)	45 (29.0)	53 (34.2)	7 (4.5)	64 (41.3)	59 (38.1)	42 (27.1)	41 (26.5)	34 (21.9)	22 (14.2)	28 (18.1)	23 (14.8)
Level 3 (Moderate)	59 (38.1)	7 (4.5)	24 (15.5)	2 (1.3)	41 (26.5)	13 (8.4)	1 (0.6)	13 (8.4)	14 (9.0)	3 (1.9)	10 (6.5)	2 (1.3)
Level 4 (Severe)	11 (7.1)	0	3 (1.9)	1 (0.6)	7 (4.5)	3 (1.9)	34 (21.9)	1 (0.6)	5 (3.2)	1 (0.6)	7 (4.5)	3 (1.9)
Level 5 (Unable)	2 (1.3)	0	5 (3.2)	0	6 (3.9)	0	7 (4.5)	0	2 (1.3)	1 (0.6)	3 (1.9)	1 (0.6)
Overall Z*	-8.905		-7.495		-6.342		-5.453		-3.982		-3.435
P	<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		0.001

*Wilcoxon Signed Rant Test

Table 5 shows that the magnitude of improvement with relation to the type of PR, gender and presence of comorbidity. Though the difference was statistically insignificant, improvement by a minimum of two points in the score of all domains of HRQOL was more in the proportion of patients who opted for supervised PR compared to home-based and hybrid PR except pain domain. Also, in patients without comorbidity compared to patients having at least one comorbidity. More proportion of female patients benefitted compared to male patients.

Table 5.

The magnitude of improvement in health-related quality of life scores using the EQ 5D 5L Questionnaire at a teaching hospital, Pune

Factors	Mobility		Self-care		Usual activities		Pain and discomfort		Anxiety and depression		Sleep
	No change or worsened %	Improved by 2 points %	No change or worsened %	Improved by 2 points %	No change or worsened %	Improved by 2 points %	No change or worsened %	Improved by 2 points %	No change or worsened %	Improved by 2 points %	No change or worsened %	Improved by 2 points %
Comorbidity
No	26.0	42.5	45.2	20.5	38.4	15.1	50.7	27.4	64.4	11.0	72.6	5.5
At least one	35.4	29.3	51.2	18.3	54.9	15.9	62.2	19.5	75.6	12.2	75.6	12.2
Gender
Male	31.4	32.4	53.9	12.	50.0	15.7	58.8	19.6	70.6	11.8	75.5	7.8
Female	30.2	41.5	37.7	32.1	41.5	15.1	52.	30.	69.8	11.3	71.7	11.3
Type of PRP
Supervised	28.0	46.0	30.0	28.0	44.0	18.0	56.0	22.0	70.0	18.0	72.0	12.0
Hybrid	31.7	30.2	54.0	12.7	46.0	12.7	60.	23.8	63.5	9.5	69.8	11.1
Home based	33.3	31.0	61.9	19.0	52.	16.7	52.	23.	81.0	7.1	83.3	2.4.0

In the supervised PR cohort, less proportion of patients showed worsening or no change in score compared to home-based PR in usual activity, self-care, mobility and sleep domains.

The proportion of patients reporting ‘No change or worsening’ was greater in patients with at least one comorbidity than in patients without any comorbidity.

DISCUSSION

Although the Government of India has recommended PR, the number of institutions that started the PR in the spirit of the letter has yet to be discovered. Naturally the effective documentation is lacking. There are very few Indian studies conducted, and this is the study with the largest sample size among the referred studies. We were compelled to have three categories of patients anticipating problems in accessing PR centre due to the strict lockdown and restriction on movements during COVID-19 pandemic in Pune city. There was no mortality among the enrolled participants during the follow-up period. This study showed that PR is effective and safe in post-COVID patients. This is in accordance with a case series by Tozato et al. 2020 in Brazil which found that a structured PR program based on the principles of cardiopulmonary rehabilitation has a positive impact on the patients and showed improvement in functional capacity, muscle strength, dyspnoea scores and vitals irrespective of the disease severity.[15]

The PR program was conducted for a minimum of eight weeks as per an earlier study and recommendation.[1,14] The sessions were conducted on OPD basis in our PR centre. WHO and Indian guidelines advised PR for moderate/severe COVID-19 patients who remain symptomatic after the acute episode.[4,6] In our study we enrolled symptomatic Post COVID patients for PR after the acute phase of COVID disease was over that is, after 21 days of a positive RTPCR report.[3] However, a study by Goodwin et al. emphasise the importance of initiating an early PR program, specifically in patients with severe diseases who may benefit from early mobilization and functional independence.[16]

Since our hospital did not have a PR facility for hospitalized COVID-19 patients, patients faced the challenge of accessing the PR facility at the centre due to the lockdown and unavailability of suitable transport.[17] Hence, we gave an option of hybrid and home-based PR to patients after a pulmonologist and cardiorespiratory physiotherapist’s evaluation. WHO and Indian guidelines have recommended home-based PR and online sessions. American thoracic guidelines 2021 also strongly advocate patient-friendly hybrid or home-based PR after an initial centre-based assessment.[11] In a systematic review conducted by Debeuf et al. 2020, there was an improvement in pulmonary, psychosocial and physical function even in patients who underwent home-based rehabilitation.[18] Thus, the patients having difficulty visiting the centre can be recommended a hybrid or home-based program after well educating the patient and conducting the necessary number of supervised sessions.[19] A randomized controlled trial conducted in Uttar Pradesh, India, in 2020 showed telerehabilitation to be effective in Post COVID-19 following discharge from hospitals.[20]

In the present study, the 6MWT and HRQOL were used as outcome measures. Both showed statistically significant improvement. A retrospective analysis conducted by Busching et al. in 2020 found similar results when they compared patients with COVID-19 pneumonia with patients having other types of pneumonia using 6MWT, functional independence measure (FIM) and chronic respiratory questionnaire (CRQ). They found significant improvement in 6MWT in COVID patients compared to another group. In contrast, both groups had similar FIM and CRQ scores.[21] A study conducted in 2021 on the effectiveness of PR in post COVID-19 patients with respiratory failure observed rapid recovery in exercise capacity among COVID-19 patients compared to non- COVID-19 patients after undergoing PR. They recommended initiating some PR components early in the ward or even in the ICU.[22] A prospective, observational cohort study conducted on 50 patients by Gloeckl R, et al. showed good results irrespective of the severity of COVID-19 disease, even within three weeks of PR.[23] Another large study by Zampogna E et al., which included 140 COVID-19 recovering patients of all types of severity and mobility, demonstrated the safety and efficacy of PR.[24] In these two studies, patients were admitted to rehabilitation centres for PR.

According to the American Association of Cardiovascular Pulmonary Rehabilitation, the essential components of comprehensive assessment in PR are exercise capacity, HRQOL, dyspnoea, nutritional status and occupational status. We did not correlate the nutritional status and physical activity related to occupation. This is the limitation of the study. Pune city was one of the hot spots during first and second waves of the pandemic in India. There was a strict lockdown during that period, so most of our patients were not working; hence we could not assess the occupational reintegration after PR and since the nutritionist’s support was not available during the early phase of the study, we could not assess the nutritional status. This study compared exercise capacity and HRQOL of post-COVID patients before and immediately after completion of the PR program. It was a service-oriented study, and it would have been unethical to deprive patients of PR services particularly after government guidelines. There is scope for such studies in the future.[11,24]

Strengths and limitations

It was a fairly large study. Specialists in the subject assessed and gave advice to the patients.

We did not have a non-COVID respiratory patient cohort for comparison. Another limitation of the study was that we did not have a control group of post-COVID patients who did not receive PR. Hence, the results cannot be solely attributed to PR. There could be some element of natural recovery. We did not strictly monitor the home-based compliance.

Data availability statement

The data is available with the corresponding author and may be provided on reasonable request.

Ethical consideration

The study was initiated after obtaining ethical clearance from the Institutional Ethics Committee, Bharati Vidyapeeth (Deemed to be University) Medical College, Approval No: BVDUMC/IEC/13. We obtained written informed consent from all the patients.

Conflicts of interest

There are no conflicts of interest.

Funding Statement

The Cipla Foundation, Mumbai, India, since February 2021, has funded the PR center under the department of Pulmonary Medicine. (CSR/HO/859/2020-21: 01/01/2021-29/12/2021, CSR/HO-BC/13/2021-22: 01/11/2021-31/03/2022, CSR/HO-BC/1122/2022-23: 01/04/2022-31/03/2023).