Rating of Perceived Exertion Associated With Acute Symptoms in Athletes With Recent SARS-CoV-2 Infection: Athletes With Acute Respiratory InfEction (AWARE) VI Study

This was a cross-sectional, experimental study in a cohort of athletes. Data were collected in the COVID-19 Recovery Clinic (the clinic) research laboratory at the Sport, Exercise Medicine and Lifestyle Institute (SEMLI) in Pretoria, South Africa, between July 20, 2020, and July 20, 2021, during the first (ancestral virus) and second (predominantly β-variant) waves of the COVID-19 pandemic. This study forms part of the Athlete With Acute Respiratory InfEction (AWARE) international, multicenter research study. The Research Ethics Committee of the Faculty of Health Sciences at the University of Pretoria approved the umbrella AWARE study (REC number: 644/2020) as well as this specific study protocol (REC number: 771/2019).

Potential participants for this study were 72 male and female athletes (age = 18 to 65 years) who had a recent SARS-CoV-2 infection and completed at least 10 days of mandatory isolation. Throughout the data collection period for this study, an isolation period of 10 days remained consistent and was mandated by the national government. The SARS-CoV-2 infection was confirmed by either a polymerase chain reaction analysis on a nasopharyngeal or throat swab (n = 70) or a positive IgG antigen test for SARS-CoV-2 taken at the onset of illness (n = 2).¹⁰  At the start of the study, COVID-19 vaccines were not available. In 2021, vaccination became available in a phased rollout, initially only for higher-risk and older individuals. Thus, at the time of closure for participant inclusion for this study (May 2021), no participants were vaccinated.

An athlete was defined as someone who “consistently trains in any sport for a minimum of 3 hours per week, competing at varying levels from recreational to elite.” Sport disciplines were classified according to their dynamic exercise load, which is associated with the percentage of maximal oxygen uptake (VO₂max) and increased cardiac output.¹¹  Sports were classified according to their cardiovascular dynamic load as follows: low, less than 50% (n = 3); moderate, 50% to 75% (n = 19); and high, greater than 75% (n = 47) dynamic load.¹¹  From this classification, the different types of sport within this population were combined for analysis and assigned to a low-moderate dynamic load (<75%) group, including judo, gymnastics, CrossFit, rugby union and rugby, and a high dynamic load (>75%) group, including football, tennis, field hockey, netball, cycling, triathlon, swimming, and running (long distance).¹¹ 

All athletes provided written informed consent and were assessed by an SEM physician in the clinic before a submaximal exercise challenge test. The initial clinical assessment was conducted between 10 and 28 days postonset of symptoms and included a medical history, clinical assessment, and selected special investigations. All participants completed a previously described online medical questionnaire to provide history related to (1) demographics (age and sex); (2) sport (classification by dynamic load, level of sport, highest level of sport participation, and years of participation in sport); (3) history of comorbidities by organ system, including cardiovascular disease or risk factors; respiratory, nervous system, psychological, gastrointestinal, metabolic, renal or bladder, or immune or blood disorders; and history of cancer; (4) preinfection training variables (hours of training) in 0 to 7 days and 8 to 35 days before the onset of symptoms of acute SARS-CoV-2 infection; and (5) symptoms (number) during the acute phase of the infection that were selected from a list of a maximum of 23 symptoms in 3 anatomical regions (nose and throat, chest and neck, and whole body [systemic]).^12,13  After a clinical assessment, the SEM physician cleared all athletes of any contraindications to a submaximal exercise challenge test.

Before commencing exercise, resting measurements were recorded for each athlete. Height (cm) and weight (kg) were measured by a stadiometer (seca 213; Hammer Steindamm) and weight scale (seca 813; Hammer Steindamm), respectively. Heart rate (bpm) was measured by a 12-lead electrocardiogram (custo cardio 110 BT, custo med GmbH) recorded for 30 seconds.^14,15  Systolic blood pressure (mm Hg) was measured by a manual Welch Allyn sphygmomanometer, inflatable cuff, and professional stethoscope (Welch Allyn Inc).^14,16 

Participants completed a submaximal exercise challenge test to measure HR, SBP, and RPE responses to exercise. The modified Bruce treadmill protocol was selected for the submaximal exercise test.¹⁴  The rationale for the selection of this protocol was the consideration of recent SARS-CoV-2 infection and possible resultant exercise intolerance. The modified Bruce protocol allows a slow, gradual progression of exercise intensity (gradient and speed), increasing the likelihood of reaching a steady-state of exercise compared with the common selection of the Bruce protocol that has more aggressive increments in exercise intensity.¹⁷  Participants completed 5 stages of the modified Bruce protocol, starting at 2.3 metabolic equivalents (METs; eg, low-intensity activities of daily living) and ending at 10.1 METs (eg, vigorous jogging, cycling, or swimming),¹⁸  or the test was terminated at 85% HR maximum if this was reached before completion of the fifth stage. Heart rate and SBP were measured using the same apparatus as at rest every 3 minutes (toward the end of each stage), and contraindications to continuing exercise testing were monitored throughout the test by the applied exercise physiologist conducting the tests.¹⁴  The RPE was measured every 3 minutes (in the last 30 seconds of each stage) using a visual chart of the Borg scale ranging from 6 (no exertion) to 20 (maximum exertion).^18–20 

The following selected factors that may affect the response to exercise were explored.

Demographic variables included age (years), sex (male or female), and body mass index (BMI; kg/m²).

Sport variables included the type of sport (low-moderate or high dynamic load), level of sport (professional versus amateur), highest level of sports participation (international, national, provincial, and recreational), and athlete experience (years).

Athletes were grouped as those with and those without a history of pre-existing comorbidities.

Preinfection training variables were hours of training at 0 to 7 and 8 to 35 days before the onset of symptoms and detraining days (days between the onset of symptoms and return to training).

The number (out of a maximum of 23 symptoms) of nose and throat, chest and neck, and whole body symptoms as well as the total number of symptoms during the acute phase of the infection were explored.

Descriptive information was reported as n (%) for categorical variables and mean ± SD for numerical variables. The outcomes (HR, SBP, and RPE) at stage 5 were analyzed, as it represented the highest exercise intensity (10.1 METs) measured across the sample and most realistically represents the exercise intensity at which athletes would return to training. The significance of the factors related to the outcomes at stage 5 was assessed using a linear model, and least square means and standard errors (mean [SEs]) with the χ² statistical test (P values) were reported.

Linear mixed models with a random intercept and slope were used to investigate the relationship between the outcomes (HR, SBP, and RPE) and the baseline stage to stage 5. The SEs were reported at each stage with the estimated differences (SEs and 95% CIs) from one stage to the next, with P values indicating whether the increase at each stage was significant. For the RPE, the interaction of stage × number of total symptoms was analyzed and the results conveyed using a graph. For reporting results, a significance level of 1% was used.

The cohort consisted of 72 athletes (age = 24.2 ± 6.3 years old; 28 female, 39%; 44 male, 61%) who were assessed 17.5 ± 4.6 days postonset of the SARS-CoV-2 infection. Athletes were assessed between June 2020 and July 2021 in South Africa, and as such, none had been vaccinated for COVID-19 at the time of infection or assessment. Most athletes (n = 46; 64%) had not resumed training postonset of symptoms at the time of assessment, and for those who had resumed training, 18.0 ± 9.3 days passed between the onset of symptoms and the resumption of training.

All demographic variables, sport variables, history of comorbidities, preinfection training, and symptoms during the acute phase of the infection are presented in Table 1.

The HR, SBP, and RPE response to the exercise challenge from rest to the completion of stage 5 (10.1 METs) of the submaximal exercise test is reported in Table 2. A significant increase was found from rest (HR and SBP) through all 5 stages of exercise (HR, SBP, and RPE; P < .0001). The largest increase in HR (39.5 bpm) was from baseline to stage 1. The largest increase in SBP (14.5 mmHg) and RPE (2.3) was from stage 4 to stage 5.

Factors potentially associated with the HR response at stage 5 (10.1 METs) of the submaximal exercise test are reported in Table 3. Younger age was significantly associated with a higher HR (P = .0007) with an average decrease in HR of 12 bpm for every 10-year increase in age. All other demographic, sport, or training variables and symptoms during the acute phase of the infection were not associated with the HR response.

Factors potentially associated with the SBP response at stage 5 (10.1 METs) of the submaximal exercise test are reported in Table 4. Age, sex, all sport variables, comorbidities, preinfection training variables, and symptoms during the acute phase of infection were not significantly associated with the SBP response. The only demographic variable that was associated with higher SBP at stage 5 was a higher BMI (P = .009) with an average of 1.5 mmHg increase in SBP for every 1 kg/m² increase in BMI.

Factors potentially associated with the RPE response at stage 5 (10.1 METs) of the submaximal exercise test are reported in Table 5. Demographics, sport variables, history of comorbidities, and preinfection training variables were not significantly associated with the RPE response at stage 5. A greater number of whole-body symptoms (P = .006) and the total number of symptoms (P = .004) were significantly associated with a higher RPE at stage 5. For every increase of 4 total number of symptoms, the RPE increased by 0.7 (SE = 0.23).

The relationship between the RPE response from stage 1 to stage 5 and the total number of symptoms is depicted in the Figure. An increase was seen in the RPE with increasing stages as well as a steeper increase with an increasing number of symptoms (P = .024 for interaction).

This study aimed to describe the HR, SBP, and RPE response to exercise and investigate the factors associated with the HR, SBP, and RPE response to submaximal exercise in athletes with a recent SARS-CoV-2 infection. The main findings of this study are as follows: (1) HR, SBP, and RPE significantly increased from rest to stage 5 of the exercise test; (2) higher exercise HR was significantly associated with younger age; (3) SBP at stage 5 was not associated with any factor; and (4) the most significant clinical finding was that the RPE at stage 5 was significantly associated with symptoms during the acute phase of infection.

The first main finding of this study is an expected HR and SBP response^14,18,20  to an exercise challenge test in athletes less than 28 days post–SARS-CoV-2 infection. Previous researchers have not described the HR and SBP response throughout the exercise challenge test but did report findings of resting HR, peak HR, and peak SBP without abnormality or significant difference to controls.^21–23  Thus, our findings are in keeping with those in previous reports.⁹  For the clinician planning safe RTS in athletes after SARS-CoV-2 infection, this finding is reassuring because athletes returning to sport after SARS-CoV-2 infection may present unique clinical scenarios that can raise concern and uncertainty for the attending SEM physician, clinician, and athlete.⁵ 

A second main finding from our study is the association between a higher HR and younger age. This finding was expected and can be explained by the widely documented finding that maximum exercise HR decreases with age.²⁴  We also show that SBP was not associated with any variables that we explored. Changes in HR and SBP during recovery from SARS-CoV-2 infection require further investigation.

A third and novel aspect of our study was to measure the RPE during an exercise challenge test in athletes at 10 to 28 days post–SARS-CoV-2 infection. The RPE response to exercise post–SARS-CoV-2, or any other acute respiratory infection, has not previously been reported, and we cannot compare our findings to those of previous research studies. The RPE response during exercise can provide valuable insight about the multisystem response to exercise^18,20,25,26  and provides a recognized measure of effort and relative fatigue during exercise, indicating intensity and homeostatic disturbance.^18,20,25,26  The RPE is an integration of various symptoms from a number of organ systems including, but not limited to, working muscles, cardiovascular and pulmonary systems, joints, and those responsible for sweating, possible pain, and dizziness.^19,27  Of particular practical clinical value, measuring the RPE during exercise does not require any equipment and can be measured not only by the clinician but also by the athlete or coach.

The most significant finding of this study was the association between a higher RPE and a greater number of symptoms during the acute phase of the infection. Athletes with a greater number of acute symptoms reported a higher RPE during exercise at the same workload than those with fewer symptoms (an RPE of 13 that is “somewhat hard” versus an RPE of 11 that is “fairly light,” respectively). In previously published studies reporting exercise tests in athletes with a recent SARS-CoV-2 infection, HR and BP variables have been reported, but not the RPE.^21–23,28  We suggest that measuring the RPE can be a valuable practical clinical tool to assess the multiorgan response to exercise in the setting of athletes with recent acute respiratory infection. We recently showed that a greater number of total symptoms is associated with prolonged return to training post–SARS-CoV-2 infection in athletes.¹²  Prolonged symptoms beyond the acute phase of infection have been reported in athletes including fatigue, shortness of breath, and headache,^3,4,29  and the regression of cardiopulmonary endurance parameters as a consequence of detraining has been questioned.²⁹  Evidence suggests that a greater number of symptoms during the acute phase of the SARS-CoV-2 infection in nonathletes is associated with multiorgan involvement and prolonged recovery.³⁰  We therefore hypothesize that multiorgan system involvement could be the main mechanism responsible for the increased RPE response we observed in athletes with a greater number of acute symptoms. We also suggest that monitoring the RPE during exercise in the recovery from infection can be valuable to track progress, recovery, and RTS. We do acknowledge that although the RPE scale is subjective, it has advantages because it is validated, reliable, easy to understand, simple to use, and gives data that are easy to interpret.^19,20  Further studies are needed to (1) explore the relationship between a higher RPE during an exercise challenge test and prolonged RTS in athletes post–SARS-CoV-2 infection, (2) track changes in the RPE during the recovery from infection over time, (3) explore other possible reasons for the higher RPE in athletes with a greater number of acute symptoms, and (4) investigate if findings are applicable to an athletic population vaccinated against the SARS-CoV-2 infection.

The strengths of this study include its relatively larger sample size than that of similar studies, the assessment of athletes at 10 to 28 days post–SARS-CoV-2 infection, and the fact that the RPE was measured during the exercise challenge test. Limitations to the study include the nature of RPE measurement and the limited training data available. The RPE is a subjective measure that requires time for the athlete to understand and interpret the sensitivity of the scale. Furthermore, the significant association between the RPE and number of acute symptoms was observed at submaximal intensities of exercise with a maximum RPE of 13 (“somewhat hard”). However, it would be expected for athletes to exceed an RPE of 13 during training, which limits the generalizability of the results. Thus, it would be beneficial to understand the exercise response at higher intensities of exercise and higher RPE ratings. Available training data preinfection were limited, and additional variables such as intensity and type of training could have strengthened the covariate analysis.

In summary, in this study, we report the response to an exercise challenge test in athletes with a recent (<28 days postonset of symptoms) SARS-CoV-2 infection. Based on the results of this study, we confirm the value of performing an exercise challenge test postacute respiratory infection, which is the recommendation from recently published International Olympic Committee consensus guidelines.⁸  We also suggest that the RPE be documented during exercise, in addition to other parameters that include HR and SBP. Symptoms during exercise also need to be monitored during follow-up exercise challenges as new exertional symptoms can be unmasked as training progresses.²⁹