Exercise Training Programs Improve Cardiorespiratory and Functional Fitness in Adults With Asthma: A SYSTEMATIC REVIEW AND META-ANALYSIS : Journal of Cardiopulmonary Rehabilitation and Prevention

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Exercise Training Programs Improve Cardiorespiratory and Functional Fitness in Adults With Asthma

A SYSTEMATIC REVIEW AND META-ANALYSIS

Valkenborghs, Sarah R. PhD, BSc(Hons); Anderson, Sophie L. MSc, BSc(Hons); Scott, Hayley A. PhD, BND(Hons); Callister, Robin PhD, MSc, BPharm

Author Information
Journal of Cardiopulmonary Rehabilitation and Prevention: November 2022 - Volume 42 - Issue 6 - p 423-433
doi: 10.1097/HCR.0000000000000698

Asthma is a chronic inflammatory disease of the airways, affecting approximately 235 million individuals globally.1 It is characterized by airway inflammation and variable airway obstruction, leading to the development of symptoms including cough, breathlessness, chest tightness, and wheeze.1 Adequate control of exercise-induced bronchoconstriction may be achieved through chronic use of asthma medication2 but, despite this, high perceived asthma symptom burden and fear of exacerbating asthma symptoms are commonly perceived barriers to participation in exercise and physical activity (PA) among adults with asthma.3,4 People with asthma engage in lower levels of total, moderate, and vigorous PA5–7 and have lower adherence to PA guidelines compared with those without asthma.8

Satisfying PA guidelines is associated with a substantially reduced risk of morbidity, as well as all-cause and cause-specific mortality.8,9 Asthma is associated with an increased risk of cardiovascular disease (CVD) and all-cause mortality,10 with physical inactivity likely a key contributor. Health-related physical fitness (HRPF) consists of those components of physical fitness that have a relationship with good health.11 Higher HRPF is associated with lower risk of CVD, cancer and respiratory morbidity and mortality, as well as all-cause mortality, even after adjustment for sociodemographic and lifestyle factors.12–15 Unfortunately HRPF is lower among adults with asthma than age- and sex-matched controls.16,17 Although increases in PA often induce increases in HRPF, the two variables are substantially independent in terms of health, with cardiorespiratory fitness (CRF) established as the more powerful predictor of mortality.18

It is now well established that PA and exercise training have many benefits for asthma-related outcomes. Recent reviews demonstrate that higher levels of PA are associated with better lung function, disease control, health status, and health care use among adults with asthma.5,7 Recent reviews also show that exercise training interventions, particularly those aerobic in nature, improve asthma control and lung function.19,20 A linear relationship has also been observed between improvement in CRF and days without asthma symptoms.21

In recognition of the benefits for asthma-related outcomes, experts in the field are now calling for aerobic exercise training to be embedded within standard asthma care.22 Current asthma clinical practice guidelines do not provide specific recommendations regarding frequency, intensity, time, and type of PA, which has prompted a call for evidence-based asthma-specific PA guidelines.23 The only systematic review and meta-analysis that synthesized findings for HRPF was conducted in 2013, with the latest included study published in 2011.24 Although a recent review presented pooled findings for HRPF in children with asthma,25 there is yet to be an updated review of adult studies conducted. Many randomized controlled trials (RCTs) have now published valuable evidence regarding the characteristics and effects of exercise programs for adults with asthma that merit synthesis to inform the development of age- and asthma-specific PA guidelines.

Therefore, the research questions for this systematic review were: what are the characteristics of exercise interventions that target HRPF in adults with asthma and what are the effects of exercise interventions on HRPF in adults with asthma?

METHODS

The review was registered with PROSPERO on May 22, 2018 (CRD42018092828). During the time that elapsed between the review registration and the search being conducted, the aforementioned recent reviews reported on the effects of exercise training and/or pulmonary rehabilitation on asthma outcomes (eg, asthma control, quality of life, lung function, and inflammation)19,20; therefore, it was decided to focus this review on HRPF only. The reporting of this review adhered to the Preferred Reporting Items for Systematic Reviews (PRISMA) statement.26

IDENTIFICATION AND SELECTION OF STUDIES

A systematic search was completed in MEDLINE, CINAHL, EMBASE, and SPORTDiscus on August 12, 2021, for published studies indexed since inception. The search strategy (see Supplemental Digital Content 1, available at: https://links.lww.com/JCRP/A385) was modified to comply with each database search criterion.

Included studies were of human adults (≥18 yr) with a clinical diagnosis of asthma as the primary respiratory disease. Studies must have included an exercise training intervention (aerobic, resistance, or breathing/stretching exercises) and measured changes in ≥1 performance-based HRPF outcome (CRF [peak oxygen uptake; V˙o2peak], muscular fitness [strength dynamometer], or functional fitness [walking distance]). Experimental studies were eligible including RCTs, quasi-experimental designs, and pre-/post-experimental studies, with comparisons between exercise training and either no-training or other therapy or usual care. Only original studies published in the English language in peer-reviewed journals were included. Conference abstracts and theses were excluded.

Articles were independently screened by two reviewers. Titles and abstracts were used to classify articles as “possibly relevant” or “definitely irrelevant.” Records identified as “definitely irrelevant” by both reviewers were excluded. Records identified as “possibly relevant” by either reviewer progressed to full-text review where it was classified as “include” or “exclude.” Records classified as “include” by both reviewers were included. Conflicts between reviewers were independently reassessed by both reviewers. If agreement was not reached, consensus was sought through discussion.

QUALITY ASSESSMENT

The Physiotherapy Evidence Database (PEDro) scale27 was used to dichotomously score (0 or 1) articles against each of 10 criteria. Where a criterion was not applicable due to study design, this was scored as “n/a” (eg, cohort studies were scored as “n/a” for the “random allocation” criterion). The quality of each article was then ranked according to the total points allocated as follows: excellent (9-10), good (6-8), fair (4-5), and poor (<4).28

DATA ANALYSES

Data from included articles were extracted independently by both reviewers into a database template created in Microsoft Excel 2016 (Microsoft Corporation), which included: participant characteristics (age, sex, diagnosis, and severity of asthma); study characteristics (study design, study setting, study location, and duration of study); intervention characteristics (frequency, intensity, type and duration of exercise training, and details of adjuvant interventions); and HRPF outcomes (measures of CRF, muscular or functional fitness).

Meta-analyses were undertaken using RevMan5.429 to compare change or final values in performance-based measures of HRPF between sufficiently homogenous studies. Due to the variability of intervention components and extrapolation to a relatively generalizable asthma population, a random-effects analysis model was used.30 We assessed heterogeneity using the I2 statistic31 and interpreted values >50% as indicating substantial heterogeneity. Results were reported as unstandardized mean differences (MDs) or, in the case of different measures of fitness, standardized mean differences (SMDs) and CI. Results were deemed statistically significant at P < .05 and SMDs were interpreted according to Cohen's “rule of thumb” cut-offs (ie, small ≥0.20 to 0.49, medium ≥0.50 to 0.79, and large ≥0.80).32 If necessary and where possible, CIs were converted to SD using the RevMan online calculator. Where data were reported as median (IQR), the mean ± SD were estimated based on published methods.33,34

RESULTS

FLOW OF STUDIES THROUGH THE REVIEW

Initially 17 322 records were identified. After removing duplicates, 11 118 citations were screened by title and abstract, and 317 were progressed to full-text review. Forty-five articles were included, of which 33 reported findings for distinct samples35–61 and 12 reported findings for six overlapping samples21,62–72 (Figure 1); that is, for the purposes of this review, we were able to identify 39 separate studies with 2135 distinct participants.

F1
Figure 1.:
Flow of studies through the review.

CHARACTERISTICS OF INCLUDED STUDIES

Data were extracted from the 39 studies (see Supplemental Digital Content 2, available at: https://links.lww.com/JCRP/A386) of which there were 18 RCTs (46%),21,36–38,40,41,43,44,53,55,56,58,65,68,69,72–76 one randomized cross-over trial (3%),60 four quasi-/pseudo-RCTs (10%),48,54,62,63,77 six non-RCTs (15%),42,45,47,51,52,78 and 10 pre-post-experimental studies (26%).35,39,46,49,50,57,59,60,67,70,71 Publication year ranged from 198337 to 2021.56,74,75 Studies were conducted in 18 different countries, with 21% of studies conducted in Brazil (n = 8)21,38,41,47,68,69,72,73,75 and a further 10% conducted in the United States (n = 4)36,44,45,70,71 and the Netherlands (n = 4).56,57,61,78 Asthma was diagnosed according to the Global Initiative for Asthma criteria79 in 36% of studies (n = 14).38,41,43,47,50,52,56,57,59,68,69,72,73,75 Many studies used a combination of diagnostic criteria including the American Thoracic Society guidelines (n = 5),48,64,65,74,78 National Asthma Education and Prevention Program guidelines (n = 2),36,45 British Thoracic Society guidelines (n = 1),76 and lung function testing (n = 11, 28% of studies) (ie, forced expiratory volume in 1 sec or peak expiratory flow).36,37,44,46,48,51,54,58,61,64–67 Other criteria considered included current medical prescription (n = 6),37,38,47,59,62,63,70,71 skin prick test (n = 2),40,53 and/or diagnosis was made by a respiratory physician (n = 7).36,48–50,53,58,70,71 Asthma severity varied considerably between studies. Where reported, participants had mild (n = 2),45,53 mild-moderate (n = 6),36,50,62–67,77 moderate-severe (n = 7),21,43,47,51,58,68,69,72,73 mild-severe (n = 3),55,61,75 severe (n = 3),74,76,78 or intermittent-severe (n = 1)59 asthma. Sex of participants was reported for all but two studies,51,77 with the overall population being 66% female and the age ranged from 22±454 to 71±11 yr.49

QUALITY OF INCLUDED STUDIES

The results of the quality assessment are presented in the Table and Supplemental Digital Content 3 (available at: https://links.lww.com/JCRP/A387). Overall, no study was deemed to be of excellent quality and only 10 (26%) were defined as good quality.21,38,41,43,55,56,68,69,72–75 Twelve studies (31%) scored as fair quality37,44,45,47,48,53,54,58,61–64,66,76 and 17 (44%) scored as poor quality.35,36,39,40,42,46,49–52,57,59,60,64,67,70,71,77,78 Of the 23 studies that had a randomized or quasi-randomized design, nine (39%) were deemed to be good quality,21,38,41,43,55,56,68,69,73–75 10 (43%) were deemed to be fair quality,21,37,44,48,53,54,58,61–63,65,66,72,76 and three (13%) were deemed to be poor quality.36,40,77 Within the 23 randomized studies, most did not perform blinding of therapists (100%), participants (96%), or assessors (74%). Most (quasi-)RCTs provided point estimates and measures of variability (91%) and demonstrated that groups were similar at baseline for most important prognostic indicators (78%).

Table - Quality Assessment of (Quasi-)Randomized Controlled Trials (Listed Alphabetically)
Study Random Allocation Concealed Allocation Similar at Baseline Blinded Subjects Blinded Therapist Blinded Assessor Retention of Participants Intention-to-Treat Analysis Between-Group Comparisons Point Estimates/Variability Score (/10)
Boyd et al (2012)36 X X X X X X X 3
Bundgaard et al (1983)37 X X X X X X 4
Cambach et al (1997)61 X X X X X 5
Coelho et al (2018)38 X X X 7
Dogra et al (2010)62 and Dogra et al (2011)63 X X X X X 5
Emtner et al (1998)65 and Emtner and Hedin (2005)66 X X X X X 5
Evaristo et al (2020)73 X X 8
Farid et al (2005)40 X X X X X X X 3
França-Pinto et al (2015)41 X X X 7
Freitas et al (2017)68 and Freitas et al (2018)69 X X X X 6
Gonçalves et al (2008)43 X X X X 6
Haas et al (1987)44 X X X X X 5
Hiles et al (2021)74 X X X 7
Lage et al (2021)75 X X X 7
Majd et al (2020)76 X X X X X 5
Mendes et al (2010)21 and Mendes et al (2011)72 X X X X 6
Meyer et al (2015)48 X X X X X 5
Rekha et al (2020)77 X X X X X X X 3
Scichilone et al (2012)53 X X X X X 5
Shaw et al (2010)54 X X X X X 5
Toennesen et al (2018)55 X X X X 6
Türk et al (2020)56 X X X 7
Turner et al (2011)58 X X X X X 5

CHARACTERISTICS OF EXERCISE INTERVENTIONS

The exercise interventions used in each study are summarized in Supplemental Digital Content 4 (available at: https://links.lww.com/JCRP/A388).

TYPES OF EXERCISE TRAINING

Studies featured three main types of exercise training interventions: aerobic, resistance, and breathing/stretching exercise. Aerobic exercise was the most common, featuring in all but four of the 39 studies56,74,75,77 and consisted of treadmill training (n = 17),35,36,39,41–43,47,49,51,52,54,60,63,69,72,73,76 and/or cycling (n = 15),35,39,46,49,51,52,55,57–60,61,63,69,76 aquatics (ie, aqua aerobics and/or swimming) (n = 4),61,65,67,70 rowing (n = 4),53,57,61,63 overground walking/jogging (n = 5),38,49,58,65,66,76 step aerobics (n = 2),35,45 and other ergometers.39,51,52,63,69

Resistance exercise was investigated in 14 (36%) studies37,39,48,49,51,52,56–58,60,62,63,68,69,76,77 and consisted of free weight (n = 5),39,51,52,60,76 elastic resistance band (n = 2),48,77 and body-weight resistance (n = 1)56 exercises (often performed in a circuit37,48,51,56) targeting major muscle groups.37,39,49,52,57,58,60,62,63,68,69 Breathing/stretching exercise was investigated in 12 (31%) studies,21,37,39,41,43,49,52,54,68,69,72–74,77 of which six investigated yogic breathing/stretching exercises.21,41,43,68,69,72–74 Three studies described pursed-lip breathing, diaphragmatic breathing, and thoracic expansion exercises,39,52,54 while inspiratory resistive breathing,54 incentive spirometer breathing exercises,77 and an inspiratory muscle training device75 were investigated in one study each. Details of the breathing exercises were not reported in one (3%) study.49 Details about stretching were generally not reported beyond being “progressive”48 or “developmental,”62 and targeting major muscle groups.37,39,54

INTENSITY OF EXERCISE TRAINING

The intensity of exercise training was reported in all but five studies,37,40,74,77,78 but there was substantial variability in the way it was measured and reported. The most common method was monitoring heart rate (HR; n = 16 studies)35,36,39,44,47,48,50–52,54,61–63,65,67,72,73 and expressing it as a percentage of peak HR achieved in a baseline maximal exercise test,35,36,48,51,61–63 age-predicted HR maximum,44,54,65,67 an undefined HR maximum,39,52 HR reserve,73 or HR at anaerobic threshold.50 Six studies monitored participant rating of perceived exertion (RPE) scale.56,58,64–67,70,75 Other studies reported intensity relative to V˙o2peak or maximal oxygen uptake (V˙o2max),21,42,45,47,56,60,68,72,76 maximal workload,43,46,53,59,61 mean or maximum walking speed,49,58 or “max intensity.”55 For the purposes of this review, these measures of intensity have been interpreted according to agreed definitions for the standardized categorization of exercise intensity, where applicable.80

The most common intensity for aerobic exercise was moderate-vigorous (n = 11 studies),36,39,43,44,50,52,58,59,61–63,68 followed by vigorous intensity only (n = 7 studies),21,41,42,45,47,72,73,76 moderate intensity only (n = 5 studies),38,46,48,49,54 and vigorous-high intensity (n = 5 studies).35,51,60,65,67 Four studies trained participants at moderate-high intensity.53,55,57,70 For resistance training, one study aimed to maintain participant HR >60% peak HR during a resistance circuit (moderate intensity),48 while another study that implemented a resistance circuit aimed for a peak intensity equivalent to 90% V˙o2max or ≥7/10 on the Borg 1-10 RPE scale (high intensity).56 Turner et al58 also monitored intensity by means of perceived exertion and aimed for participants to report 12-14 on the 6-20 Borg RPE scale (ie, moderate-vigorous).

Although other resistance training studies did not report intensity per se, an indication could be derived from descriptions of repetition ranges, numbers of sets, work-to-rest ratios, and progression. Three studies prescribed resistance training based upon one repetition maximum (1RM) testing.60,68,76 Participants in one study performed two sets of 6-12 repetitions at 80% 1RM,76 and two studies had participants perform two sets of 10 repetitions beginning at a similar relative weight (4560 or 50%68 1RM), before both progressing to 70% 1RM and increasing to three sets. Bundgaard et al37 tested maximum repetitions within 30 sec for six exercises at baseline (reassessed after 1 mo [ie, mid-point of program]) and asked participants to perform 50% of their maximal repetitions of each exercise for three sets without rest. Türk et al56 provided 30 sec of rest between each of three to six sets of four exercises performed for 45 sec each (ie, 30-sec rest every 3 min). One study used a circuit training approach and performed one to four sets of alternating between seven resistance and aerobic exercises for 50 sec each, with a 30-sec rest between sets.51 Other studies did not provide details beyond participants performing 8-10 repetitions,52,77 1 set/wk only,63 or continuing until failure.62 Neither intensity nor composition of resistance training was reported by three studies.39,40,49

FREQUENCY OF EXERCISE TRAINING

Frequency of training was reported in all but two studies51,78 and was generally described as sessions/wk or d/wk. Frequency ranged from 148 to 1249 sessions/wk, with 3 sessions/wk being the most common prescription (n = 18 studies).35,36,40,42,44–46,50,51,53–58,61,63,64,70 Candemir et al60 prescribed training 5 d/wk for participants, with 3 d designated for aerobic exercise and 2 d designated for resistance exercise. Otherwise, it was more common that studies designated a certain duration of each training session toward each type of exercise.

DURATION OF EXERCISE TRAINING SESSIONS

Session durations ranged from 1175 to 12039,52 min, with 13 study sessions lasting 31-45 min.36,38,40,41,44,55,56,61,62,64–66,73 Time spent performing aerobic exercise ranged from 937 to 7053 min, with 23 studies performing ≤30 min21,35–41,43,46,47,51,52,54,55,57–60,62,64–67,70–72 (of which 12 studies performed 30 min specifically21,35,36,38,39,43,46,52,54,58,60,62,72). Time spent performing resistance training was only reported by four studies,51,56–58 in which it ranged from 551 to 4558 min. Time spent performing breathing/stretching exercise ranged from 1175 to 7574 min/session and was not reported in four studies.39,49,52,77 Twenty studies36,37,40,41,46–48,53–56,58–60,64–67,70,73 reported having a warm-up, which was most commonly 5 min.36,41,46,47,54,59,73 Thirteen studies reported performing a cool-down,36,41,46,47,54,56,60,62,64–67,70,71,73 which was most commonly 5 min.36,41,46,47,54,56,59,62,70,71,73

DURATION AND VOLUME OF EXERCISE TRAINING PROGRAM

Total program duration ranged from 239 to 5248 wk, with 12 wk being the most common (n = 16).21,36,38,44,46,47,49,51,56,57,61–63,70,72,73,76,78 Total program volume ranged from 7.559 to 14449 hr, with 24 hr being the most common.21,36,44,46,54,72,76

SETTING AND SUPERVISION OF EXERCISE TRAINING

A wide variety of settings were reported including outpatient (n = 20)35,37,38,40,41,47–49,53,56–59,61,65,67–69,73,76,78 and inpatient (n = 2) clinics,49,67 as well as other hospital (n = 8)35,39,52,55,60,65,67,77 and community settings (n = 5)36,48,51,62,63,65 (eg, swimming pools,65,67,70,71 gyms,36,65 and local sports clubs48). Although 28 studies reported implementing supervised exercise training, only 21 studies reported who it was supervised by—physiotherapists (n = 12),35,39,41,45,50,56–58,61,65,68,69,75 exercise physiologists (n = 2),45,63 a combination of physicians and exercise instructors (n = 2),48,53 exercise instructors (n = 6),37,55,70,71,73,74 and a respiratory therapist.59 Only two studies distinctly reported self-directed/unsupervised exercise interventions.38,62

ADJUVANT INTERVENTIONS

Eight studies recommended participants take prophylactic asthma medication prior to commencing exercise38,42,51,55,58,65,67,74 and eight studies encouraged participants to take asthma medication before or during exercise if/as required.36,45,50,53,55,62,63,65,70,71,73,76 It was not well reported how many participants took medication before or during exercise, nor had to cease exercise due to exercise-induced symptoms.

Twenty-two studies embedded one or more adjuvant interventions in the study intervention,21,36,38,39,41,43,47,49,52,55–57,59,60,61,67–69,72–76,78 (eg, asthma education [n = 16],21,38,41,47,49,52,57,59,60,67–69,72–76,78 psychological counseling [n = 7],52,56,57,59,60,68,69,78 diet counseling [n = 8],49,52,55–57,59,60,68,69 mindfulness [n = 1],74 PA monitors [n = 2],38,74 and antiallergenic bed linen [n = 1]36). These studies were only included in the meta-analyses if the effect of the exercise training could reasonably be isolated from the other interventions (ie, the only thing that differed between study groups was exercise training).

HEALTH-RELATED PHYSICAL FITNESS ASSESSMENTS

Cardiorespiratory fitness (V˙o2max) was the most commonly reported measure of HRPF (n = 20),21,35–37,41–45,47,48,50,51,54–56,62,63,68–72,76 assessed during an incremental treadmill21,36,37,41–44,47,50,62,63,72,76 or cycle test.35,45,48,51,54,68–71 Measures of functional fitness (walking distance) were reported by 18 studies,38–40,49,52,56–61,64,65,67,73–76,78 including the 6-min walk test (6MWT),38–40,52,56–59,61,74 12-min walk test,64,65,67 incremental shuttle walk test,49,60,73,75,76,78 and endurance shuttle walk test.60 Only four studies reported measures of muscular fitness49,58,68,69,77 including 1RM testing,68 dynamometers,49,58 or manual muscle testing.77 Measures of HRPF reported in addition to one of the above outcomes included resting/submaximal HR,35,42,61,62,66,67 anaerobic threshold,43–45,50 peak ventilation,35,42,45,48 and peak workload.35,41,46,48,51,53

EFFECTS ON HEALTH-RELATED PHYSICAL FITNESS

OVERALL HEALTH-RELATED PHYSICAL FITNESS

Results from pooling 12 (quasi-)RCTs (n = 477) indicated that experimental exercise interventions result in moderate improvements in HRPF compared with inactive controls (SMD 0.67, 95% CI, 0.46-0.89) (Figure 2). Subgroups of these experimental exercise interventions consisted of aerobic exercise alone (n = 5 studies, n = 209 participants; SMD 0.74, 95% CI, 0.45-1.03), aerobic and resistance exercise (n = 4 studies, n = 116 participants; SMD 0.52, 95% CI, 0.13-0.90), and breathing/stretching exercise alone (n = 3 studies, n = 92 participants; not significant). There were insufficient studies to perform subgroup meta-analyses for resistance training alone and aerobic exercise combined with breathing exercise.

F2
Figure 2.:
Effects of exercise interventions on measures of health-related physical fitness in adults with asthma (compared to inactive controls). This figure is available in color online (www.jcrpjournal.com).

Results from pooling three studies (n = 141 participants) that compared the effects of aerobic exercise against breathing/stretching exercise revealed a small-to-moderate superior effect (SMD 0.47, 95% CI, 0.14-0.81) in favor of groups who undertook aerobic exercise interventions (Figure 3).

F3
Figure 3.:
Comparison of aerobic exercise and breathing/stretching exercise interventions on measures of health-related physical fitness in adults with asthma. This figure is available in color online (www.jcrpjournal.com).

CARDIORESPIRATORY FITNESS

Results from pooling five (quasi-)RCTs (n = 217) found a significant difference in V˙o2max (MD 3.1 mL/kg/min, 95% CI, 1.9-4.3) (Figure 4) in favor of experimental exercise interventions compared with inactive control interventions. Three of these interventions investigated aerobic exercise alone, which resulted in a significant improvement of 3.6 mL/kg/min (95% CI, 2.2-5.0), while the aerobic and resistance exercise interventions and the breathing/stretching exercise interventions did not improve oxygen uptake.

F4
Figure 4.:
Effects of exercise interventions on relative V˙o 2peak in adults with asthma (compared to inactive controls).

FUNCTIONAL FITNESS

Results from pooling seven (quasi-)RCTs (n = 139) found a significant difference in walking distance (MD 40.5 m, 95% CI, 26.6-54.5) (Figure 5), in favor of experimental exercise interventions compared with control interventions. Subgroup analyses consisted of aerobic exercise alone (n = 2 studies, n = 80 participants; MD 43.5 m, 95% CI, 12.8-74.2), aerobic and resistance exercise (n = 2 studies, n = 65 participants; MD 30.9 m, 95% CI, 6.4-55.4), aerobic and resistance exercise (n = 1 study, n = 31 participants; MD 69.7 m, 95% CI, 33.9-105.5), and breathing/stretching exercise alone (n = 2 studies, n = 63 participants; MD 34.6 m, 95% CI, 9.9-59.2).

F5
Figure 5.:
Effects of exercise interventions on walking distance in adults with asthma (compared to inactive controls). This figure is available in color online (www.jcrpjournal.com).

MUSCULAR FITNESS

Only three (quasi-)RCTs measured muscular fitness and were not suitable to be pooled.58,68,69,77 Turner et al58 reported no significant differences in muscular fitness, while Freitas et al68,69 reported a significant improvement in all measures of muscular fitness in favor of the exercise group. Rekha et al77 compared resistance training to incentive spirometer training, and found that both interventions improved respiratory muscular fitness.

DISCUSSION

In this systematic review, the features and findings of 39 studies (from 45 published articles) were synthesized to identify characteristics and determine the effects of exercise interventions on improving HRPF in adults with asthma. Most studies used aerobic exercise either alone or in combination with resistance or breathing/stretching exercise. Meta-analyses revealed significant improvements in CRF, functional, and overall health-related HRPF in favor of groups who underwent experimental exercise training interventions.

While exercise interventions lead to moderate improvements in overall HRPF, the current evidence best supports aerobic exercise specifically. Aerobic exercise interventions improved overall HRPF, CRF, and functional fitness. Conversely, breathing/stretching exercise interventions did not significantly improve overall HRPF or CRF but did elicit small improvements in functional fitness. When directly compared, aerobic exercise (vs breathing/stretching exercise) elicited superior improvements in HRPF by a small-to-moderate effect size margin.

We observed that exercise training elicits a mean improvement in V˙o2max of 3.1 mL/kg/min in adults with asthma; this degree of improvement has been previously associated with an 8% reduction in the risk of CVD morbidity in adults free from CVD.81 Also, the increase (V˙o2max) elicited by aerobic exercise alone was equivalent to a 12% reduction in the risk of all-cause mortality in both healthy and comorbid adult populations.82 Furthermore, the improvements in walking distance were equivalent to minimum clinically important differences for comorbid adult populations (30.5 m), including those with respiratory conditions (25-48 m).83,84 These findings may have important clinical implications in addressing the increased risk of CVD and all-cause mortality among adults with asthma.10

The composition of training programs in studies included in the meta-analyses were similar to the most common exercise program characteristics of all studies included in this review (ie, supervised moderate-to-vigorous intensity exercise [mainly aerobic] performed for 30-45 min 3 d/wk). These exercise program characteristics are similar to those in studies included in a recent systematic review and meta-analysis that found improvements in clinical outcomes in adults with asthma, including asthma control and lung function but not airway inflammation.19 Elements of these exercise programs are also consistent with the World Health Organization PA guidelines, except in terms of performance of muscle strengthening activities.85

RESISTANCE EXERCISE AND MUSCULAR FITNESS

While several studies investigated resistance exercise, the descriptions of the programs were generally not reported in sufficient detail to facilitate comparison and/or replication. Further, few studies measured changes in muscular fitness and the findings were inconsistent,49,58,68,69 but this may be reflective of differences in the resistance exercise program characteristics in these studies. The studies that had the most analogous and favorable findings also provided similar duration programs (12 wk),49,68,69 whereas a 6-wk program elicited no between- or within-group effects on muscular fitness,58 which might indicate the intervention was too short. It was unclear from two exercise program descriptions49,58 what volume of resistance exercise was performed, if it was high-load (>60% 1RM) or low-load (≤60% 1RM), or if training and testing aligned in terms of specificity and/or time of day; these are all factors known to impact outcomes.86–88

There are inverse associations between muscular fitness and risk of CVD, cancer and all-cause mortality (independent of CRF).12,14 Satisfying national PA guidelines for performance of muscle-strengthening activities is also inversely associated with morbidity (including asthma)8 and all-cause mortality,9 but muscular fitness and adherence to muscle-strengthening PA guidelines among adults with asthma are very low.8,17 Considering the equivocal findings for effects of resistance exercise on muscular fitness in adults with asthma, and that the effects of resistance exercise on asthma outcomes remain to be established,19 further research in this area is merited. Elucidating the benefits of muscle-strengthening activities for this population may be an impetus for adherence to PA guidelines.

UNSUPERVISED EXERCISE PROGRAMS

The effects of unsupervised exercise programs are unclear and understudied. Given the poor adherence observed by Dogra et al,62 in addition to poor adherence to PA guidelines by adults with asthma generally, facilitating autonomous participation in PA is a research priority. Poor exercise self-efficacy has been linked to negative perspectives about exercise, exercise fear-avoidance beliefs and, consequentially, lower participation in PA in this population.4,89,90 It has been suggested that an initial period of supervision may increase exercise self-efficacy for adults with asthma.62

Two studies in this review conducted 3-yr follow-up of participants after a supervised exercise program. One found that 68% of participants had remained physically active, and improvements in functional fitness and asthma symptoms had been maintained in those who had continued to exercise 1-2 times/wk.64 The other study found that 48% had remained physically active and highlighted that exercise self-efficacy was a distinguishing characteristic between maintainers and nonmaintainers.66 Therefore, future exercise programs aimed at increasing and maintaining HRPF and PA for adults with asthma should monitor and target exercise self-efficacy through social support,89 self-management guidelines (including exercise education),91,92 and self-treatment guidelines.93

TELEHEALTH EXERCISE PROGRAMS

The lack of telehealth exercise programs identified in this review is an area of concern, given the increased reliance on these approaches for asthma management during the COVID-19 pandemic.94 This may partially explain the disproportionate prevalence of reduced PA intensity during COVID-19 lockdown among adults with asthma.95 Respiratory illnesses, particularly those of viral etiology, are often potent triggers of asthma exacerbation.96

Concern about resuming exercise activities in public facilities among asthma patients and their caregivers is therefore not baseless, given that attendance at fitness centers and group exercise classes have been linked to greater transmission of COVID-19 compared with attending other public outlets for a similar dwell time.97,98 Further, donning of facemasks during exercise seems feasible and safe for people who are disease-free but is not yet indicated for people with respiratory disease,99 and outdoor exercise can be problematic for those whose asthma is triggered by pollen and pollutants.100 Performance of evidence-based exercise programs at home via either a self-management or telehealth supervision approach may be a promising strategy for maintenance and improvement of HRPF for adults with asthma.

FUTURE DIRECTIONS

We were unable to compare the differential effects of exercise intensity, since most studies included in the meta-analyses used overlapping intensity ranges. Clinically, evidence is emerging that moderate-intensity exercise may elicit anti-inflammatory effects in the airways of adults with asthma, while vigorous-high-intensity exercise may elicit pro-inflammatory effects.101 Future studies comparing different intensities of exercise, and the necessary durations of these programs, are warranted in adults with asthma, so this can be determined.

Relatedly, there are perceptions that exercise is risky, less beneficial, and/or less tolerable for people with severe asthma,3,4 but we were unable to perform subgroup analyses to explore whether severity of asthma compromises improvement in HRPF. Several studies in this review included people with severe asthma and reported improvements in CRF, functional, and muscular fitness.21,43,47,51,55,58,59,61,68,69,72 One study stratified participants by severity and found that while 6MWT performance was negatively correlated with asthma severity, baseline 6MWT performance was also negatively correlated with responsiveness (ie, those with the most severe asthma and lowest 6MWT improved the most).59 Therefore, exercise training seems to be beneficial for adults with asthma regardless of severity.

STRENGTHS AND LIMITATIONS

The strengths of this review are two investigators screened studies for eligibility and subsequently conducted independent quality assessment and data extraction of included studies to ensure accuracy of evidence. While random-effects models were used and heterogeneity was low (I2 < 50%) in all meta-analyses conducted, the studies included in the quantitative syntheses were only of good or fair quality. For CRF, there were only sufficient studies to pool relative V˙o2peak, and thus improvements due to changes in body weight cannot be ruled out. This review focused only on the performance-based components of HRPF, as a review of interventions to improve body composition in children and adults with asthma has recently been published.102 Lastly, our review focused on adults with asthma, so these findings should not be generalized to children; instead readers should refer to the review by Joschtel et al.25

CONCLUSIONS

Supervised exercise training programs are effective in eliciting clinically significant improvements in HRPF in adults with asthma, with the best evidence existing for aerobic exercise. These findings complement those of previous reviews regarding effectiveness of aerobic exercise programs for asthma-related outcomes in adults and can be considered collectively in the formation of asthma-specific PA guidelines, to ensure they confer benefits to both asthma-related and overall HRPF outcomes. Further research regarding the benefits of resistance exercise in adults with asthma is required, alongside evidence of the effects of unsupervised and/or telehealth exercise programs in this population.

REFERENCES

1. Global Asthma Network. The Global Asthma Report. Auckland, New Zealand: Global Asthma Network; 2018.
2. Morton AR, Fitch KD. Australian Association for Exercise and Sports Science position statement on exercise and asthma. J Sci Med Sport. 2011;14(4):312–316.
3. Freeman AT, Hill D, Newell C, et al. Patient perceived barriers to exercise and their clinical associations in difficult asthma. Asthma Res Pract. 2020;6:5.
4. Mancuso CA, Sayles W, Robbins L, et al. Barriers and facilitators to healthy physical activity in asthma patients. J Asthma. 2006;43(2):137–143.
5. Cordova-Rivera L, Gibson PG, Gardiner PA, McDonald VM. A systematic review of associations of physical activity and sedentary time with asthma outcomes. J Allergy Clin Immunol Pract. 2018;6(6):1968–1981.e2.
6. Xu M, Lodge CJ, Lowe AJ, et al. Are adults with asthma less physically active? A systematic review and meta-analysis. J Asthma. 2021;58(11):1426–1443.
7. Cordova-Rivera L, Gibson PG, Gardiner PA, Powell H, McDonald VM. Physical activity and exercise capacity in severe asthma: key clinical associations. J Allergy Clin Immunol. 2018;6(3):814–822.
8. Bennie JA, De Cocker K, Teychenne MJ, Brown WJ, Biddle SJH. The epidemiology of aerobic physical activity and muscle-strengthening activity guideline adherence among 383,928 U.S. adults. Int J Behav Nutr Phys Act. 2019;16(1):34.
9. Zhao M, Veeranki SP, Magnussen CG, Xi B. Recommended physical activity and all cause and cause specific mortality in US adults: prospective cohort study. BMJ. 2020;370:m2031.
10. Xu M, Xu J, Yang X. Asthma and risk of cardiovascular disease or all-cause mortality: a meta-analysis. Ann Saudi Med. 2017;37(2):99–105.
11. Corbin C, Pangrazi R, Franks B. Definitions: health, fitness, and physical activity. Pres Counc Phys Fit Sports Res Dig. 2000;3(9):1–8.
12. Ruiz JR, Sui X, Lobelo F, et al. Association between muscular strength and mortality in men: prospective cohort study. BMJ. 2008;337:a439.
13. Karanth MS, Awad NT. Six minute walk test: a tool for predicting mortality in chronic pulmonary diseases. J Clin Diagn Res. 2017;11(4):OC34–OC38.
14. Carbone S, Kirkman DL, Garten RS, et al. Muscular strength and cardiovascular disease: an updated state-of-the-art narrative review. J Cardiopulm Rehabil Prev. 2020;40(5):302–309.
15. Steell L, Ho FK, Sillars A, et al. Dose-response associations of cardiorespiratory fitness with all-cause mortality and incidence and mortality of cancer and cardiovascular and respiratory diseases: the UK Biobank cohort study. Br J Sports Med. 2019;53(21):1371–1378.
16. De Oliveira JM, Spositon T, Cerci Neto A, Soares FMC, Pitta F, Furlanetto KC. Functional tests for adults with asthma: validity, reliability, minimal detectable change and feasibility. J Asthma. 2022;59(1):169–177.
17. Vancampfort D, Stubbs B, Firth J, Koyanagi A. Handgrip strength, chronic physical conditions and physical multimorbidity in middle-aged and older adults in six low- and middle income countries. Eur J Intern Med. 2019;61:96–102.
18. Ross R, Blair SN, Arena R, et al. Importance of assessing cardiorespiratory fitness in clinical practice: a case for fitness as a clinical vital sign: a scientific statement from the American Heart Association. Circulation. 2016;134(24):e653–e699.
19. Hansen ESH, Pitzner-Fabricius A, Toennesen LL, et al. Effect of aerobic exercise training on asthma in adults—a systematic review and meta-analysis. Eur Respir J. 2020;56(1):2000146.
20. Wu X, Gao S, Lian Y. Effects of continuous aerobic exercise on lung function and quality of life with asthma: a systematic review and meta-analysis. J Thorac Dis. 2020;12(9):4781–4795.
21. Mendes FAR, Goncalves RC, Nunes MPT, et al. Effects of aerobic training on psychosocial morbidity and symptoms in patients with asthma: a randomized clinical trial. Chest. 2010;138(2):331–337.
22. Bacon SL, Platts-Mills TA. Is it time for aerobic exercise to be included in asthma treatment guidelines? J Allergy Clin Immunol. 2020;8(9):2997–2998.
23. Dogra S, Patlan I, O'Neill C, Lewthwaite H. Recommendations for 24-hour movement behaviours in adults with asthma: a review of current guidelines. Int J Environ Res Public Health. 2020;17(5):1789.
24. Carson KV, Chandratilleke MG, Picot J, Brinn MP, Esterman AJ, Smith BJ. Physical training for asthma. Cochrane Database Syst Rev. 2013;(9):CD001116.
25. Joschtel B, Gomersall SR, Tweedy S, Petsky H, Chang AB, Trost SG. Effects of exercise training on physical and psychosocial health in children with chronic respiratory disease: a systematic review and meta-analysis. BMJ Open Sport Exerc Med. 2018;4(1):e000409.
26. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.
27. Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83(8):713–721.
28. Valkenborghs SR, Callister R, Visser MM, Nilsson M, van Vliet P. Interventions combined with task-specific training to improve upper limb motor recovery following stroke: a systematic review with meta-analyses. Phys Ther Rev. 2019;24(3–4):100–117.
29. Review Manager (RevMan) [computer program]. Version 5.4. Copenhagen, Denmark: The Nordic Cochrane Centre, The Cochrane Collaboration; 2014.
30. Higgins JP, Thomas J, Chandler J, et al. Cochrane Handbook for Systematic Reviews of Interventions. Chichester, England: John Wiley & Sons; 2019.
31. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–560.
32. Cohen J. Statistical Power Analysis for the Behavioral Sciences. New York, NY: Academic Press; 2013.
33. Shi J, Luo D, Weng H, et al. Optimally estimating the sample mean and standard deviation from the five-number summary. Res Synth Methods. 2020;11(5):641–654.
34. Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. http://www.math.hkbu.edu.hk/∼tongt/papers/median2mean.html. Accessed, 2020.
35. Afzelius-Frisk L, Grimby G, Lindholm N. Physical training in patients with asthma. Poumon Coeur. 1977;33(1):33–37.
36. Boyd A, Yang CT, Estell K, et al. Feasibility of exercising adults with asthma: a randomized pilot study. Allergy Asthma Clin Immunol. 2012;8(1):13.
37. Bundgaard A, Ingemann-Hansen T, Halkjaer-Kristensen J, Schmidt A, Bloch I, Andersen PK. Short-term physical training in bronchial asthma. Br J Dis Chest. 1983;77(2):147–152.
38. Coelho CM, Reboredo MM, Valle FM, et al. Effects of an unsupervised pedometer-based physical activity program on daily steps of adults with moderate to severe asthma: a randomized controlled trial. J Sports Sci. 2018;36(10):1186–1193.
39. Deniz S, Şahin H, Polat G, Erbaycu AE. In which the gain is more from pulmonary rehabilitation? Asthma or COPD? Turk Thorac J. 2019;20(3):160–167.
40. Farid R, Azad FJ, Atri AE, et al. Effect of aerobic exercise training on pulmonary function and tolerance of activity in asthmatic patients. Iran J Allergy Asthma Immunol. 2005;4(3):133–138.
41. França-Pinto A, Mendes FAR, de Carvalho-Pinto RM, et al. Aerobic training decreases bronchial hyperresponsiveness and systemic inflammation in patients with moderate or severe asthma: a randomised controlled trial. Thorax. 2015;70(8):732–739.
42. Freeman W, Nute MG, Williams C. The effect of endurance running training on asthmatic adults. Br J Sports Med. 1989;23(2):115–122.
43. Gonçalves R, Nunes M, Cukier A, Stelmach R, Martins M, Carvalho C. Effects of an aerobic physical training program on psychosocial characteristics, quality-of-life, symptoms and exhaled nitric oxide in individuals with moderate or severe persistent asthma. Brazilian J Phys Ther. 2008;12(2):127–135.
44. Haas F, Pasierski S, Levine N, et al. Effect of aerobic training on forced expiratory airflow in exercising asthmatic humans. J Appl Physiol. 1987;63(3):1230–1235.
45. Hallstrand TS, Bates PW, Schoene RB. Aerobic conditioning in mild asthma decreases the hyperpnea of exercise and improves exercise and ventilatory capacity. Chest. 2000;118(5):1460–1469.
46. Heba HA, Ashraf KA. Impact of a 12 weeks supervised exercise training program on pulmonary functions of patients with exercise induced asthma. Egyptian J Chest Dis Tuberculosis. 2013;62(1):33–37.
47. Mendes FAR, Franca-Pinto A, Martins MA, et al. Seasonal changes influence the improvement in asthma symptoms by exercise training in subjects with asthma. J Asthma. 2019;56(6):674–679.
48. Meyer A, Gunther S, Volmer T, Taube K, Baumann HJ. A 12-month, moderate-intensity exercise training program improves fitness and quality of life in adults with asthma: a controlled trial. BMC Pulm Med. 2015;15:56.
49. Miyamoto N, Senjyu H, Tanaka T, et al. Pulmonary rehabilitation improves exercise capacity and dyspnea in air pollution-related respiratory disease. Tohoku J Exp Med. 2014;232(1):1–8.
50. Peric R, Drobnic FM, Baker JS. Feasibility of individualized aerobic threshold-based exercise on ventilatory efficiency in sedentary adult asthma patients. Minerva Pneumologica. 2018;57(4):92–98.
51. Robinson DM, Egglestone DM, Hill PM, Rea HH, Richards GN, Robinson SM. Effects of a physical conditioning programme on asthmatic patients. N Z Med J. 1992;105(937):253–256.
52. Sahin H, Naz I. Comparing the effect of pulmonary rehabilitation in patients with uncontrolled and partially controlled asthma. J Asthma. 2019;56(1):87–94.
53. Scichilone N, Morici G, Zangla D, et al. Effects of exercise training on airway closure in asthmatics. J Appl Physiol. 2012;113(5):714–718.
54. Shaw I, Shaw BS, Brown GA. Role of diaphragmatic breathing and aerobic exercise in improving pulmonary function and maximal oxygen consumption in asthmatics. Sci Sports. 2010;25(3):139–145.
55. Toennesen LL, Meteran H, Hostrup M, et al. Effects of exercise and diet in nonobese asthma patients—a randomized controlled trial. J Allergy Clin Immunol. 2018;6(3):803–811.
56. Türk Y, Theel W, van Huisstede A, et al. Short-term and long-term effect of a high intensity pulmonary rehabilitation program in obese patients with asthma: a randomised controlled trial. Eur Respir J. 2020;56(1):1901820.
57. Turk Y, Van Huisstede A, Franssen FME, et al. Effect of an outpatient pulmonary rehabilitation program on exercise tolerance and asthma control in obese asthma patients. J Cardiopulm Rehabil Prev. 2017;37(3):214–222.
58. Turner S, Eastwood P, Cook A, Jenkins S. Improvements in symptoms and quality of life following exercise training in older adults with moderate/severe persistent asthma. Respiration. 2011;81(4):302–310.
59. Zampogna E, Paneroni M, Cherubino F, et al. Effectiveness of a pulmonary rehabilitation program on persistent asthma stratified for severity. Respir Care. 2019;64(12):1523–1530.
60. Candemir I, Ergun P, Kaymaz D. Efficacy of a multidisciplinary pulmonary rehabilitation outpatient program on exacerbations in overweight and obese patients with asthma. Wien Klin Wochenschr. 2017;129(19/20):655–664.
61. Cambach W, Chadwick-Straver R, Wagenaar R, Van Keimpema A, Kemper H. The effects of a community-based pulmonary rehabilitation programme on exercise tolerance and quality of life: a randomized controlled trial. Eur Respir J. 1997;10(1):104–113.
62. Dogra S, Jamnik V, Baker J. Self-directed exercise improves perceived measures of health in adults with partly controlled asthma. J Asthma. 2010;47(9):972–977.
63. Dogra S, Kuk J, Baker J, Jamnik V. Exercise is associated with improved asthma control in adults. Eur Respir J. 2011;37(2):318–323.
64. Emtner M, Finne M, Stalenheim G. A 3-year follow-up of asthmatic patients participating in a 10-week rehabilitation program with emphasis on physical training. Arch Phys Med Rehabil. 1998;79(5):539–544.
65. Emtner M, Finne M, Stålenheim G. High-intensity physical training in adults with asthma. A comparison between training on land and in water. Scand J Rehabil Med. 1998;30(4):201–209.
66. Emtner M, Hedin A. Adherence to and effects of physical activity on health in adults with asthma. Adv Physiotherapy. 2005;7(3):123–134.
67. Emtner M, Herala M, Stalenheim G. High-intensity physical training in adults with asthma: a 10-week rehabilitation program. Chest. 1996;109(2):323–330.
68. Freitas PD, Ferreira PG, Silva AG, et al. The role of exercise in a weight-loss program on clinical control in obese adults with asthma. A randomized controlled trial. Am J Respir Crit Care Med. 2017;195(1):32–42.
69. Freitas PD, Silva AG, Ferreira PG, et al. Exercise improves physical activity and comorbidities in obese adults with asthma. Med Sci Sports Exerc. 2018;52(7):1367–1376.
70. Hildenbrand K, Nordio S, Freson TS, Becker BE. Development of an aquatic exercise training protocol for the asthmatic population. Int J Aquatic Res Educ. 2010;4(3):7.
71. Hildenbrand K, Freson TS, Barbosa-Leiker C, Nordio S, Becker BE, Miller AJ. The impact of an aquatic exercise protocol on physiologic measures within an asthmatic population. Int J Aquatic Res Educ. 2011;5(4):5.
72. Mendes FAR, Almeida FM, Cukier A, et al. Effects of aerobic training on airway inflammation in asthmatic patients. Med Sci Sports Exercise. 2011;43(2):197–203.
73. Evaristo KB, Mendes FAR, Saccomani MG, et al. Effects of aerobic training versus breathing exercises on asthma control: a randomized trial. J Allergy Clin Immunol Pract. 2020;8(9):2989–2996.e4.
74. Hiles SA, Urroz PD, Gibson PG, Bogdanovs A, McDonald VM. A feasibility randomised controlled trial of Novel Activity Management in severe ASthma-Tailored Exercise (NAMASTE): yoga and mindfulness. BMC Pulm Med. 2021;21(1):71.
75. Lage SM, Pereira DAG, Corradi Magalhaes Nepomuceno AL, et al. Efficacy of inspiratory muscle training on inspiratory muscle function, functional capacity, and quality of life in patients with asthma: a randomized controlled trial. Clin Rehabil. 2021;35(6):870–881.
76. Majd S, Apps L, Chantrell S, et al. A feasibility study of a randomized controlled trial of asthma-tailored pulmonary rehabilitation compared with usual care in adults with severe asthma. J Allergy Clin Immunol Pract. 2020;8(10):3418–3427.
77. Rekha K, Doss DSS, Siddiue MA. Respiratory muscle training with theraband versus incentive spirometer among individuals with bronchial asthma. Int J Curr Pharmaceutical Res. 2020;12(3):117–120.
78. de Nijs SB, Krop EJM, Portengen L, et al. Effectiveness of pulmonary rehabilitation at high-altitude compared to sea-level in adults with severe refractory asthma. Respir Med. 2020;171:106123.
79. Global Initiative for Asthma. Global Strategy for Asthma Management and Prevention. Fontana, WI: Global Initiative for Asthma; 2018.
80. Norton K, Norton L, Sadgrove D. Position statement on physical activity and exercise intensity terminology. J Sci Med Sport. 2010;13(5):496–502.
81. Ekblom-Bak E, Ekblom B, Söderling J, et al. Sex- and age-specific associations between cardiorespiratory fitness, CVD morbidity and all-cause mortality in 266.109 adults. Prev Med. 2019;127:105799.
82. Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med. 2002;346(11):793–801.
83. Bohannon RW, Crouch R. Minimal clinically important difference for change in 6-minute walk test distance of adults with pathology: a systematic review. J Eval Clin Pract. 2017;23(2):377–381.
84. Huang L-H, Chen Y-J. The 6-minute walk test to assess exercise capacity of patients with chronic obstructive pulmonary disease. Eur Respir J. 2016;48(suppl 60):PA1385.
85. Bull FC, Al-Ansari SS, Biddle S, et al. World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br J Sports Med. 2020;54(24):1451–1462.
86. Blazer HJ, Jordan CL, Pederson JA, et al. Effects of time-of-day training preference on resistance-exercise performance. Res Q Exerc Sport. 2021;92(3):492–499.
87. Schoenfeld BJ, Grgic J, Ogborn D, Krieger JW. Strength and hypertrophy adaptations between low- vs. high-load resistance training: a systematic review and meta-analysis. J Strength Cond Res. 2017;31(12):3508–3523.
88. Colquhoun RJ, Gai CM, Aguilar D, et al. Training volume, not frequency, indicative of maximal strength adaptations to resistance training. J Strength Cond Res. 2018;32(5):1207–1213.
89. Suorsa KI, Cushing CC, Mullins AJ, et al. Adolescents and young adults with asthma and allergies: Physical activity, self-efficacy, social support, and subsequent psychosocial outcomes. Child Health Care. 2016;45(4):414–427.
90. Janssens T, Dupont L, Von Leupoldt A. Exercise fear-avoidance beliefs and self-reported physical activity in young adults with asthma and healthy controls. Eur Respir J. 2018;52(suppl 62):PA2479.
91. Chen S-Y, Sheu S, Chang C-S, Wang T-H, Huang M-S. The effects of the self-efficacy method on adult asthmatic patient self-care behavior. J Nurs Res. 2010;18(4):266–274.
92. Huang TT, Li YT, Wang CH. Individualized programme to promote self-care among older adults with asthma: randomized controlled trial. J Adv Nurs. 2009;65(2):348–358.
93. van der Palen J, Klein JJ, Zielhuis GA, van Herwaarden CL, Seydel ER. Behavioural effect of self-treatment guidelines in a self-management program for adults with asthma. Patient Educ Couns. 2001;43(2):161–169.
94. Hartmann-Boyce J, Gunnell J, Drake J, et al. Asthma and COVID-19: review of evidence on risks and management considerations [published online ahead of print September 3, 2020]. BMJ Evid Based Med. doi:10.1136/bmjebm-2020-111506.
95. Rogers NT, Waterlow NR, Brindle H, et al. Behavioral change towards reduced intensity physical activity is disproportionately prevalent among adults with serious health issues or self-perception of high risk during the UK COVID-19 lockdown. Front Public Health. 2020;8:575091.
96. Busse WW, Lemanske RF Jr, Gern JE. Role of viral respiratory infections in asthma and asthma exacerbations. Lancet. 2010;376(9743):826–834.
97. Chang S, Pierson E, Koh PW, et al. Mobility network models of COVID-19 explain inequities and inform reopening. Nature. 2021;589(7840):82–87.
98. Jang S, Han SH, Rhee J-Y. Cluster of coronavirus disease associated with fitness dance classes, South Korea. Emerg Infect Dis. 2020;26(8):1917–1920.
99. Epstein D, Korytny A, Isenberg Y, et al. Return to training in the COVID-19 era: the physiological effects of face masks during exercise. Scand J Med Sci Sports. 2021;31(1):70–75.
100. Weiler JM, Brannan JD, Randolph CC, et al. Exercise-induced bronchoconstriction update—2016. J Allergy Clin Immunol. 2016;138(5):1292–1295. e1236.
101. Scott HA, Gibson PG, Garg ML, et al. Dietary restriction and exercise improve airway inflammation and clinical outcomes in overweight and obese asthma: a randomized trial. Clin Exp Allergy. 2013;43(1):36–49.
102. Okoniewski W, Lu KD, Forno E. Weight loss for children and adults with obesity and asthma. A systematic review of randomized controlled trials. Ann Am Thorac Soc. 2019;16(5):613–625.
Keywords:

asthma; cardiorespiratory fitness; exercise; physical fitness

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