Authors: 1Marisella Villano, MS, CFT, CES and 2Frank Spaniol, PhD
Department of Kinesiology, Texas A & M University – Corpus Christi
Corresponding Author:
Marisella Villano, MS, CFT, CCES
Marisella Villano recently graduated with a Master’s degree in Kinesiology from Texas A & M – Corpus Christi and has previously earned a Master’s degree in Gerontology from Long Island University. Additionally, she is a certified fitness trainer and corrective exercise specialist and is the founder and owner of MARVIL FIT, an indoor cycling, fitness and personal training studio in the Hamptons.
Frank Spaniol, PhD is a professor of sport and exercise science and also the program coordinator in the Kinesiology department at Texas A & M University – Corpus Christi. His
research interests include: sport performance, strength and conditioning, visual skills training, and sport technology.
Abstract
Purpose: This systematic review investigated the effects of COVID-19 infection on athletic performance. Methods: Using guidelines for a systematic search review, a comprehensive literature review was conducted utilizing the computer databases Google Scholar, PubMed and the Mary and Jeff Bell Library at Texas A&M University-Corpus Christi. Results: Incidence of cardiac abnormalities is low among athletes with COVID-19 infection, but cardiopulmonary deficiencies like shortness of breath have been shown to affect aerobic capacity which can impair performance. A premature switch to anaerobic metabolism at higher intensities was observed during cardiopulmonary exercise testing (CPET). Increased exercise heart rate (HR) and blood pressure (BP) were also observed in some athletes during CPET. Finally, the effects of COVID-19 appear to be multisystemic as decrements were also observed in balance, sleep and high intensity performance. Conclusion: COVID-19 infection primarily affects the cardiorespiratory system, but other multisystemic disturbances to athletic performance may occur which can negatively affect performance. Applications to Sport: Athletes recovered from COVID-19 illness continue to experience shortness of breath which may decrease recoverability after high intensity exertions and increase fatigability during competition. Proper screening beginning with CPET and planned RTP protocols based on the individual needs of athletes are necessary for seamless return to sport and attainment of performance levels prior to infection.
Keywords
Return to play, cardiorespiratory, cardiopulmonary exercise test, cardiac magnetic resonance, heart rate, VO2max, aerobic threshold, anaerobic threshold, ventilation, ventilatory efficiency, ventilatory inefficiency, long covid
Introduction
The COVID-19 pandemic spared no one, including athletes, and became a significant worldwide problem that appeared to primarily cause respiratory and cardiovascular illness (29). While clinical manifestations of COVID-19 in athletes are generally mild, persisting symptoms like cough, fatigue and tachycardia are similar to individuals in the general public (25). Individuals affected with mild or moderate COVID-19 illness also have the possibility of experiencing persistent symptoms post infection called Long-Covid (LC) and asymptomatic infection can introduce symptoms once a person has recovered from the primary infection (32). Persistent symptoms lasting more than 28 days are defined as LC and generally include fatigue and shortness of breath (6, 34).
Aside from the common symptoms of COVID-19 which include cardiorespiratory and cardiovascular disturbances, multisystemic disturbances have been observed in the central and peripheral nervous systems, gastrointestinal system, hematological system, liver, skeletal muscle, and kidneys (11, 16, 29). Furthermore, post infection sequelae causing imbalances of the autonomic system have also been observed (15). To sum up, the virus responsible for COVID-19 attacks the immune system of its host and creates a systemic inflammatory response by activating a large number of cytokines, which induces inflammation and can affect multiple organ systems that could potentially contribute to their failure in severe cases (1).
Multiorgan damage by COVID-19 infection is caused by penetration of the virus through angiotensin-converting enzyme-2 (ACE2) receptors found on the surface of the cell (21). Further, large concentrations of ACE2 receptors are found in pulmonary and cardiac tissue, which may explain symptoms of shortness of breath and cardiac complications in recovered individuals (21). Additionally, COVID-19 complications have been observed to last longer than 30 days and up to 6 months (28). Even though the athletic population appears to develop mild to moderate COVID-19 infection, are not at high risk for severe illness and are quick to recover, they may experience lingering post infection sequelae from COVID-19 like myocarditis, exertional dyspnea, tachycardia, muscle pain, joint pain and fatigue (even with asymptomatic and mild infection) (9, 15, 25). Lastly, estimations of LC in athletes are between 3 and 17% (34).
First time symptoms of COVID-19 illness can occur once the primary infection has subsided (32). Because athletes exert demanding loads compared to the average population, understanding the long-term effects of COVID-19 is not only important to help maintain maximal performance levels, but should also be a concern for their safety (2, 6, 32). While athletes appear to fully recover after COVID-19 infection, cardiopulmonary exercise testing (CPET) post infection has aided medical professionals to uncover potentially detrimental symptomatology during exertional activities (5).
Fortunately, current research has demonstrated that the chance for cardiac abnormalities among athletes recovering from asymptomatic to moderate COVID-19 illness is very rare (3, 14, 16, 19). In a study by Maestrini et. al. (2023), 6% of the participants exhibited cardiac abnormalities post COVID-19 cardiovascular evaluations. Also, of 1597 athletes in Big Ten American Football Conference, 37 athletes (2.3%) exhibited clinical or subclinical signs of myocarditis (10). Of interest, some cardiac issues uncovered during CPET and cardiovascular testing while undergoing return to play (RTP) protocols after infection had no relationship to COVID-19 and appeared to result from preexisting conditions (3, 24, 32). This emphasizes the need for regular CPET (which has been used as a standard test to determine the cardiorespiratory and pulmonary health of individuals post infection) and cardiovascular screening for all athletes (3, 24, 32).
While most athletes will have mild or no symptoms during acute COVID-19 infection, 3-17% will be affected by continuing symptoms, like fatigue, that can have negative effects, to optimal performance (33). Unfortunately, the recommended forced rest of 14 days for elite and competitive athletes can be detrimental to power and maximal oxygen consumption (VO2 max), cardiac output and stroke volume (21). Information regarding the long-term effects of COVID-19 continues to evolve and only necessitates the importance of research and investigation, especially in athletes because their success relies on their physical capabilities (31). Additionally, little research is available on the consequences of any potential musculoskeletal cellular interruptions through the ACE2 receptors primarily occurring in pulmonary and cardiac tissue (31).
Although many athletes have a significantly reduced risk of severe COVID-19 illness, they are not immune to contracting the disease and its lingering effects (9,33). Further, compared to other acute respiratory viruses, the proportion of athletes who have not fully recovered from COVID-19 is significantly higher (34). The purpose of this review is to evaluate the effects of COVID-19 infection on the performance of athletes.
List of Abbreviations
Cardiopulmonary Exercise Test (CPET), Cardiovascular Magnetic Resonance (CMR), Heart Rate (HR), Maximal Heart Rate (MHR), Ventilation (VE), Ventilatory Efficiency (VEf), Ventilatory Inefficiency (ViE), Long Covid (LC), Maximal Oxygen Consumption (VO2max), peak oxygen uptake (VO2 peak), Beats Per Minute (bpm), Blood Lactate (BL), Oxygen (O2), Carbon Dioxide (CO2), Repetition Maximum (RM), Respiratory Compensation Point (RC), Ventilatory Aerobic Threshold (VAT), Beat per Minute (BPM), VE/CO2 Slope (pulmonary ventilation to CO2 production), Partial Pressure of CO2 (PETCO2), Forced Expiratory Volume in the First Second (FEV1), Second Forced Expiratory Volume (FEV2)
Methods
Using guidelines for a systematic search review, a comprehensive literature review was conducted from January 2020 to November 2023 using the computer databases Google Scholar, PubMed and the Mary and Jeff Bell Library at Texas A&M University-Corpus Christi. Several search terms were used and include; covid and athlete; covid infection and athlete and performance and CPET; covid infection and athletes and power and performance and VO2max and cardiorespiratory; covid infection and CPET and anaerobic and athlete; covid infection and athletes and power and performance and VO2max and cardiorespiratory; covid infection and athletes and power and performance and VO2max and cardiopulmonary and sport. Larger search terms to narrow results were necessary when using Google Scholar as the use of two search terms like covid infection and athlete resulted in over 22,000 results. All search titles were carefully filtered to include athletic performance inferences and COVID-19 infection.
Once searches were filtered, article content was reviewed to determine relevance of the investigation as mentioned above. Research journal articles were selected along with 2 case studies due to lack of information in this newly emerged topic. 947 articles were retrieved using Google Scholar with search terms covid infection and athletes and power and performance and VO2max and cardiopulmonary and sport. Of the 947 articles, 10 were relevant to the research parameters. A second search on Google Scholar was conducted using the search terms covid infection and CPET and anaerobic and athlete with 899 results. Of the 889 resulting articles, 17 were relevant to the research parameters. Two separate searches were conducted in PubMed for the terms (1) covid infection and athlete and performance and CPET and (2) COVID infection and athlete and performance and CPET and anaerobic. The first search resulted in 122 outcomes with 18 relevant articles and the second search resulted in 7 outcomes with 5 relevant items. Larger search terms were used because using only the terms covid infection and athlete together resulted in almost 3,000 results. Lastly, the Mary and Jeff Bell Library was used in the review search using fewer search terms since using the larger terms resulted in an extreme narrowing of results. The search terms COVID and athlete were used and resulted in 237 articles. Using the option to include the search terms in the subject heading, the search was further narrowed to 88 where 7 of these search outcomes were selected based on the criteria. 6 articles were extracted from the final selection of articles that did not meet the search requirements and all results were compared for duplicates. In total, 32 articles were retrieved from the search. Additionally, a few articles were extracted from the articles obtained in the search for further investigation of research evidence.
Babity et al. (2022) observed a 10% decrease in VO2max in athletes recovered from COVID-19 infection when comparing their CPET values before illness. Also, post infection CPET times were longer among athletes recovered from COVID-19 infection (p=.003). Further, increased heart rate (HR) was observed in athletes previously infected with COVID-19 during testing. However, once adjustments for age were calculated, no statistically significant changes were evident. Additionally, 13% of elite athletes who participated in the study had asymptomatic infections and a small group appeared to have cardiac irregularities. Despite these differences, no difference was observed between COVID-19 athletes and the control group in ventilation (VE,) carbon dioxide (CO2) removal, blood lactate (BL) levels and percentage of time spent during the anaerobic phase. Vollrath et al. (2022) observed that athletes recovered from COVID-19 infection with persistent symptoms had lower ventilatory efficiency (VEf) than athletes who were symptom free and may indicate a slow recuperation of VEf for symptomatic individuals. Three months later, these persistent symptoms experienced by the athletes were reduced but still present in about 60% of the subjects.
Ventilatory inefficiency (ViE) was observed in competitive athletes that tested positive for COVID-19 by Komici et al. (2023) but was not observed to limit their exercise capacity. These athletes were tested after an RTP program of about 2 weeks. When comparing post infection sequelae, a study by Rinaldo et al. (2021), observed that nonathletic individuals exhibited similar symptoms at rest and at work whereas athletes did not appear to express symptomatology at rest. The exercise decrements observed between both groups in CPET included early AT, early termination of testing, lower peak oxygen (O2) pulse, lower work and a decreased slope relationship between O2 uptake and rate of work. Decreased capacity of exercise was not observed in athletes by Komici et al. 2021, however a trend was observed in the decrease of forced expiratory volume in the first second (FEV1) among the recovered athletes.
Similarly, Keller et al. also observed 4% lower peak values of VO2max in athletes recuperated from COVID-19 (p=.01) when compared to athletes who did not contract the virus. Along with reduced VO2max, Keller et al. (2023) observed an increased chance for exercise hypertension during CPET testing within this group which can be indicative of intolerance to exercise. Additionally, the authors noted that incidences of shortness of breath and chest pain were more prevalent with older athletes in the study group. Reduced peak oxygen uptake (VO2 peak) and increased BP among athletes recovered from COVID-19 illness were observed during CPET, but not at rest.
CPET values among COVID-19 recovered athletes with mild to moderate illness reached AT faster (p=.05) and also had lower measurements for minute ventilation (Ve) than the control group in an investigation by Anastasio et al. (2022). However, differences in maintaining CPET parameters between the two groups were not significant. Additionally, differences at maximal effort only differed by HR, with the COVID-19 group demonstrating higher HR values, but performance during testing was not altered. Finally, one month post COVID-19 infection athletes demonstrate a premature shift to anaerobic metabolism when compared to the control group.
Significant differences were not observed by Babity et al. (2022) when analyzing CPET values of elite athletes before and 3 months after COVID-19 infection. It is important to note that athletes in this study also underwent post COVID-19 retraining protocols where significant increases were observed in average exercise times (p=.003), time to achieve VO2max, respiration rate (p=.008), and HR achieved at AT (p=.004). Also, findings during examination uncovered arrhythmias or hypertension in asymptomatic athletes, and additional non-COVID-19 related to cardiac abnormalities. Moreover, Parpa & Michaelides (2022) observed significantly lower VO2max (p=.01) and decreased VO2max (p=.05) in 21 soccer players recovered from COVID-19. Significantly higher HR at ventilatory threshold (VT) (p=.01) and respiratory compensation point (RC) (p=.01) were also detected. Lastly, decreases in running speed during testing were only observed at VO2max (p=.05) and lower running times (p=.01) were observed.
In a study by Milovancev et al. (2021) of professional volleyball players recovered from COVID-19 infection with about 20 days of retraining, CPET values appeared to show fairly normal pulmonary function. After analyzing data from other studies of healthy athletes, the authors observed lower VO2max and second ventilatory threshold (VT2) in the participants of their study but contributed the deficits to detraining. Lastly, no cardiac disturbances were detected during testing. Similarly, testing results of athletes recovered from COVID-19 showed no statistically significant difference before and after COVID-19 in a study by Taralov et al. (2021) regardless of continued fatigue symptomatology. Due to the study’s small sample size, the authors looked at individual results and were able to see that one participant’s total CPET time was 30 seconds shorter post infection from 18 minutes to 17:30 minutes. Further, AT was reached earlier after acute infection. Additionally, maximal heart rates (MHR) were similar during testing before and after infection which suggests that the similar effort post infection resulted in decreased testing capacity. Another test subject had differing recovery HR 2 minutes into recovery from 141 beats per minute (bpm) before COVID-19 infection to 156 bpm after COVID-19 infection, which is an indication of diminished recovery capacity.
Wezenbeek et al. (2023) showed decreased aerobic performance after COVID-19 infection in elite soccer players about 2 months post infection. Statistically significant higher (MHR) percentages were observed 6 minutes into a Yo-Yo Intermittent Recovery Test (YYIR) (p=.006). When compared to non-infected team members, the MHR percentages were 6-11% greater in the players recovered from COVID-19. After a retest 4-5 months post recovery, these decreases dissipated to normal values. Lastly, the authors also investigated the effects of the viral infection on jumping, strength and sprinting capabilities and no significant differences were observed before and after infection.
A comparative study by Stavrou et al. (2023) between athletes that tested positive for COVID-19 and healthy athletes which never contracted COVID-19 demonstrated statistically significant differences during CPET even with non-significant differences in testing performance. First, the post-COVID-19 group had lower HR at maximal exertions than their healthy counterparts, 191.6 ±7.8 bpm and 196.6 ± 8.6 bpm respectively (p=.041). Mean arterial pressures were similar between both groups. Also, O2 consumption showed no significant difference between the groups. Second, BL levels in the post- COVID -19 group were significantly higher at rest (p=.001), during CPET and during recovery than the healthy group. Third, both groups achieved similar VO2max values, but the post-COVID-19 group did have greater exertional symptoms like increased VE. Fourth, increases in VE were observed in post-COVID-19 group even with non-significant performance differences in CPET between the two groups. Lastly, the post-COVID-19 group also had greater sleep disturbances based on study questionnaires (p=.001). Interestingly, no significant differences in O2 consumption were present between the groups, yet VE was higher at greater workloads in the post-COVID-19 group.
Another comparative study by Śliż et al. (2021) with endurance athletes before and after COVID-19 noted significant changes in CPET parameters after illness. These changes include aggravations to VO2 at AT (p=.00001), VO2 at RC (p=.00001), HR to RC (p=.00011) and VO2max (p=.00011). Additionally, lowered VO2max and early accumulation of lactate were observed during CPET.
Similar findings to ViE and decreased aerobic capacity in elite and highly trained recovered athletes were observed by Brito et al. (2023) with CPET 6-22 weeks after onset of illness. Further, statistically significant decrements were observed in both symptomatic and asymptomatic participants recovered from COVID-19 illness. Additionally, over 50% of all test subjects exhibited significant dysfunctional breathing (p=.023) and over 60% presented significant evidence of ViE (p=.001). Also, a statistically significant percentage of abnormalities were more prevalent among symptomatic individuals, specifically VE/CO2 slope (p<.001), PETCO2 rest (p=.007) and PETCO2 max (p=.008). Statistically significantly higher abnormalities of expiratory air flow/tidal volume were apparent with asymptomatic individuals (p=.012). Lastly, no changes in running economy were apparent in either group. Bruzzese et al. (2021) also noted statistically significant changes to oxygen uptake at second ventilatory threshold (VO2VT2) (p=.28), MHR (p=.04) and respiratory exchange ratio (RER) (p=.02).
In a case study by Barker-Davies et al. (2023) an elite runner recovering from COVID-19 experienced reduced work capacity and O2 uptake at AT 5 months after infection and occurred more rapidly than a previous CPET conducted 15 months earlier. Also, a decrease in workload by 27 watts (W) and a reduction of O2 uptake by 13% was also observed. When reviewing calorimetry, a 21% decrease in fat metabolism was observed and may explain the early onset to AT. Despite the decrements in performance, the absolute values of the CPET fell within normal range but the athlete complained of fatigue and difficulty generating power.
An investigation by Rajpal et al. (2021) which focused on cardiovascular magnetic resonance imaging (CMR) found incidence of current myocarditis or prior injury to the myocardium in almost 50% of 26 athletes recovered from COVID-19 (22). In another investigation by Maestrini et al. (2023), 2% of cardiac abnormalities were observed in 219 asymptomatic or mildly symptomatic athletes by Maestrini et al. (2023). Moreover, 3.3% of study participants demonstrated cardiac disturbances that included pericarditis and myopericarditis by Cavigli and colleagues. Juhász et al. (2023) also provided evidence that about 3% of recovered athletes had evidence of myocarditis or pericardial effusion. The authors also mentioned that persistent symptoms of COVID-19, like fatigue and chest pain, were factors that restricted players from RTP. Further, the disturbances seemed to be prevalent only among female athletes who had mild symptomatic COVID-19 infection. Additionally, these cardiac disturbances were determined during CPET testing and ECG monitoring. Biomarkers for cardiac disturbances, arrhythmias and structural abnormalities in the heart were also very low in the study by Sridi-Cheniti et al. (2022). Lastly, Cavigli et al. (2021) also observed that no athletes with asymptomatic COVID-19 infection demonstrated any cardiac complications.
Conversely, all athletes participating in an investigation by Fikenzer et al., (2021) had fluid accumulation in the pericardium (pericardial effusion) and magnetic resonance imaging (MRI) with high T1- and T2- values had a reduced maximal load, maximal O2 uptake, a higher HR at comparable exertion, and a significantly reduced O2 pulse when compared to previous testing. The changes to cardiac muscle in HR and O2 pulse were visible at moderate intensities, while the cardiopulmonary effects became apparent during higher intensities. Additionally, the respiratory minute volume which is used as a constraint of pulmonary function was considerably reduced. Malek and colleagues noted that 28 Olympic athletes recovered from COVID-19 infection did not appear to have any acute myocarditis findings after MRI testing. However, 5 of the subjects did show cardiac abnormalities. These individuals were all able to fully recover and RTP safely. Lastly, a case study by Nedeljkovic et al. (2021) observing native CMR images of an athlete recovered from asymptomatic COVID-19 infection demonstrated no signs of inflammation to the cardiac tissue. However, after contrast application, the indication of focal myocarditis became apparent where the athlete was advised to cease training for 3 months. Further, this individual continued to present with signs of myocarditis and decreased functional ability at a 3 month follow up visit.
Individuals like National Football League player Myles Garrett, National Basketball Association player Jayson Tatum and Major League Baseball player Yoan Moncada all experienced symptoms of fatigability (33). Because of this, Walker et al. (2023) compared the mean Pro Football Focus (PFF) game scores before and after a COVID-19 infection in players to examine performance. When analyzed by position before and after infection, statistically significant decreases in the numbers of snaps per game were observed in Defensive Backs (p=.03) and statistically significant decreases were further observed for mean scores in Defensive Linemen (p=.03). Additionally, similar findings were observed by Savicevic et al. (2021) in professional soccer players that were recovered from COVID-19 infection and completed RTP protocols where players demonstrated a decrease occurrence of high intensity accelerations and decelerations in game performance (p=.04).
Neuromuscular disturbances affecting balance may be another complication arising from COVID-19 as observed by Fernández-Rodríguez et al. (2023) which evaluated six handball players 1 month post infection and demonstrated degradation to static balance. Mild sleep disturbances were observed to affect 31% of individuals testing positive for COVID-19 by Śliż et al. (2023) and the sleep disturbances appear to influenced endurance athletes while performing CPET. Endurance athletes that experienced decreased sleep times experienced significant parameter changes in breath rate, pulmonary VE and BL concentration at AT. The study further observed several CPET correlations in athletes with sleep disturbances and performance and include (1) disturbances in HR and RC, (2) higher pulmonary VE at AT, (3) maximum power output and maximal HR and (4) individual habit which including methods to cope with sleep disturbances. Of interest, Vollrath et al. (2022) observed that sleep disturbances increased during the course of their investigation. Lastly, the authors further described that the most persistent symptoms observed in athletes included insomnia, fatigue and neurocognitive disorders, which can cause impairments to memory, learning and decision making.
Probing the influence of COVID-19 strains on athletic performance, Stojmenovic et. al. (2023) demonstrated that athletes infected with the Omicron variant, the latest virus strain, had higher VO2 max when compared to athletes infected with the older variants, Wuhan and Delta. Athletes affected by the Omicron variant had better VE and higher O2/HR values when compared to the two previous strains, Wuhan and Delta. Further, O2 transport to skeletal muscle was also greater with the Omicron variant. No statistical difference was observed with MHR at the completion of CPET and during the 3-minute recovery. Of further interest, the early transition of aerobic to anaerobic metabolism, which has been observed in several studies with the Wuhan and Delta variants, was not present for the Omicron variant (29).
Stojmenovic et. al. and colleagues further observed values of HR at ventilatory anaerobic threshold (VAT) and RC that were much higher in the athletes who contracted the Omicron strain versus the groups of athletes which contracted the Wuhan or Delta strain (p=.01). Additionally, higher HR values at the VAT were observed with the Wuhan and Delta variants when compared to the Omicron variant (p=.001). The RER at lower intensities was greater among the Wuhan and Delta group (p=.001) which demonstrates a greater dependence toward carbohydrate as a fuel rather than fat and further indicating an inability to utilize O2 for energy production. The efficiency of O2 delivery was the greatest for athletes with the Omicron variant. Moreover, VEf, although within normal limits for all three strains, was the best for individuals recovered from Omicron which further highlights more effective O2 transport to the skeletal muscle. Also, this study demonstrated meaningful decreases in aerobic capacity for all COVID-19 strains. Deng et al. (2023) investigated the neuromuscular performance of the upper body and mental health in a group of vaccinated kayakers recovered from the Omicron variant. No decrements were evident in 1RM bench press about 22 days post infection. Mental health appeared to be intact.
In an investigation by Jafarnezhadgero et al. (2022) recreational female runners that were hospitalized for COVID-19 were able to maintain steady state running with similar HR as the control group but ran at slower paces than the control group (p=.0001). Further, running test in COVID-19 recovered female runners terminated early (p=.0001). Also, these individuals had longer foot contact time (p=.002), peak propulsion forces (p=.0004) and reductions in loading rate (p=.04). Another study by Toresdahl and colleagues explored a potential link to COVID-19 infection and increased chances for injury in recovered runners due to systemic inflammation. While the investigation relied on self-reported questionaries, the outcome presented finding that about 20% of 1947 study participants, which included both males and females, experienced injury after a positive COVID-19 infection that prevented them from running for at least one week.
Juhász, et al. (2023) also noted that females, when compared to men, were more likely to suffer from short term prolonged symptoms of COVID-19 infection (34% vs. 19%, p = 0.005). However, females conveyed information through study surveys which indicated that they were able to regain peak form and maximal training strength faster than their male counterparts (3 vs. 4 weeks, p = 0.01). Further, LC was statistically significant with age groups in the study, with older age groups experiencing LC and severe symptoms more than their younger counterparts (p= .02%).
Gattoni et al. (2022) noted significantly lower performance outcomes among soccer players recovered from COVID-19 infection (p<.01). Additionally, no cardiopulmonary or cardiovascular abnormalities were present among test subjects. Also, while no statistical significance was observed for cardiopulmonary abnormalities, individual impairments were noted.
Of 26 elite athletes and 20 physically trained individuals (average age 30) participating in a study by Brito and authors, 65% of them continued to have persisting symptoms approximately 2-3 weeks after COVID-19 diagnosis, with the most frequent symptom being dyspnea (or shortness of breath). Additionally, participants with symptomatic illness showed statistically significant impairment to minute ventilation/CO2 production (VE/VCO2) slope (p < 0.001), partial pressure of CO2 (PETCO2) rest (p = 0.007), and PETCO2 max (p = 0.009) when compared to asymptomatic individuals. However, expiratory air flow/tidal volume occurred more often among asymptomatic individuals (p = 0.012). Lastly, impairments during CPET did not differ between symptomatic and asymptomatic individuals.
Discussion
With increased research regarding the influence of COVID-19 infection to athletic performance, new information is emerging, and prior implications of significant cardiac involvement have been quelled. The concern for myocarditis and sport related cardiac complications lies in fears of sudden cardiac death due to high intensity workloads, but these complications in athletes who are typically healthy and young with asymptomatic or mild symptoms COVID-19 infection are low, yet the risk does exist (7, 23). Occurrences of myocarditis, pericarditis, intolerance to exercise, fatigue and shortness of breath in athletes presented the need for more regular medical examinations and screening post infection not only to conserve athletic capabilities, but to also prevent the possibility of sudden cardiac death (SCD) (29). Further, some of the cardiac issues uncovered with CPET and cardiovascular testing with RTP protocol may have been preexisting conditions in athletes which had no relationship to COVID-19 (3). For this reason alone, CPET testing and cardiovascular screening is recommended for all athletes (3). To complicate matters, changes to the heart muscle can occur in athletes due to adaptations resulting from exercise quantity and intensities that are necessary to maintain athletic performance and may make testing athletes at resting conditions to be counterproductive (22, 32).
Cardiac abnormality involvement in athletes recovered from COVID-19 is inconsistent (18). Clinical cardiac events in elite and high-level athletes after mild or asymptomatic infection are very low even after resuming high-level training (27). Because of the low prevalence of cardiac complications associated with COVID-19 infection, the use of resonance CMR has been suggested to be reserved as a screening tool for athletes that may be at risk for cardiovascular abnormalities, although cardiac screening in athletes was suggested to be performed at least once to help detect underlying heart abnormalities (3, 17).
COVID-19 seems to affect the cardiorespiratory system more than the cardiovascular system (19). Several studies have observed an early switch to anaerobic metabolism during CPET. The greater recruitment of anaerobic metabolism at a specific workload can help to explain the inability of athletes to develop a significant power output during exertion, most probably due to fatiguability (4). Further, a study by Ajaz et al., observed decreased cellular respiration in hospitalized COVID-19 patients when the glucose pathway for energy was blocked. Additionally, Stavrou et al. (2023) also emphasized this to be a deficiency in the aerobic pathway for energy production as ventilation increased during physical exertion. Keller and colleagues suggested that the limitations to performance are directly related to delivery of O2 to muscles tissue rather than occurring from cardiac complications. Also, Jafarnezhadgero et al. (2022) determined that decreased performance during running tests were caused by deficits in O2 transport rather than fatigue, and they did not affect running mechanics in the study participants which recovered from COVID-19. Finally, these ideas are further supported by Wezenbeek and colleagues, who believe that COVID-19 infection can cause disruption to capillary blood flow, thus limiting the uptake of O2.
Of interest, a study by Ajaz et al. (2021) observed decreased cellular respiration in hospitalized COVID-19 patients when the glucose pathway for energy was blocked. Additionally, cellular respiration in the healthy control group and a separate group with various chest infections not related to COVID-19 did not exhibit any augmentation to cellular respiration. Also, in all three groups, no changes were present when other energy pathways with glutamine and long chain fatty acids were blocked. Further, Ajaz and authors believe the dependency on glucose may explain the early shift from aerobic to anaerobic metabolism observed in some athletes post COVID-19 infection. Moreover, the authors consider that mitochondrial dysfunction from COVID-19 infection is responsible for the preference of cells to utilize the process of glycolysis for cellular respiration and energy production. Lastly, greater metabolism of carbohydrates may have more negative implications in female athletes since females are more reliant on fat metabolism than men (4).
Although testing parameters in a study by Taralov et al. (2021) demonstrated no statistical significance in CPET and blood testing before and after COVID-19 infection in athletes, many continued to complain of persisting fatigue for several months. By examining the individual differences among the small sample group, the authors were able to detect small changes in performance. For example, a 30 second shorter CPET time post infection with time with similar MHR and intensity values before infection may be indicative of fatigue. Additionally, another test subject exhibited higher recovery HR parameters post infection which can be indicative of a reduced capacity for recovery. Further, AT was reached earlier after acute infection. Taralov and authors further emphasized that these findings can be significant during competition. While these changes seem small when comparing test results, these small differences can make large differences during competition by increasing fatigability and decreased recovery capacity that can have a negative impact to performance.
Recovery from persistent COVID-19 infection sequelae can take several months. Parpa & Michaelides (2022) concluded that 2 months of recovery post infection may not be sufficient for athletes, especially since some symptoms are not detectable at rest. Subsequently, post COVID-19 infection can cause reduced VO2 peak during exercise testing and increases in blood pressure during exercise despite presenting normal findings at rest reinforces the need for return to play testing in athletes (14). Additionally, even mild illness in athletes who have non-significant differences in VO2max when compared to non-infected individuals will experience aerobic burdens, which will display strains in performance and respiration (28). Lastly, the authors recommended that factors like VT, RC and HR and running speed should be observed during VO2max and respiratory threshold (RT).
One of the primary reasons for performance decrement may be due to detraining from COVID-19 infection and the necessary forced rest (19). Declines in VO2max with detraining have been observed in as little as 12 days and are caused by decreased stroke volume and arteriovenous gas exchange due to decreased volume of plasma from decreased exercise exertion (19). In addition, decreases in mitochondrial density have been observed after three weeks of exercise with no changes in muscle capillarization (19). Finally, cessation of exercise in 42-85 days has been noted to change the oxidative capacity of intermediate type IIa muscle fibers toward type IIb muscle fibers (19).
Moreover, an increase in VE/VCO2 slope is suggestive of intolerance to exercise along with cardiovascular or cardiopulmonary disease (15). Komici et al., (2023) did not believe that deconditioning was associated with ViE from their ventilatory parameters because the slope of VE/VCO2 appeared similar within all groups of athletes recovered from COVID-19 in their study. However, a perceived inverse correlation among ventilatory efficiency slope (VCO2/VE) maximum and ventilatory equivalents for O2 (VO2/VE) maximum among test subjects was suggestive of a perfusion mismatching in ventilation which is indicative to ViE (15). While the mechanisms involved in their ViE were not clearly understood, an inverse relation was observed between maximum volume of CO2 during ventilatory exchange and the volume of max O2 during ventilatory exchange and may have implications to a mismatching of O2 (24). Moreover, cardiorespiratory deficits have been attributed to muscle deconditioning in patients, not athletes, when decreased ventilatory response and early AT was observed in post COVID-19 patients (24). Athletes recovered from COVID-19 infection may demonstrate shortness of breath but can also have reduced pulmonary capacity and cardiac symptoms only detectable during sub-maximal conditions which can result in reduced physical capacity (10,15, 25). Moreover, increases in HR at VT and RC may be a response in the cardiovascular system resulting from hypoxemia, which has been observed as a mismatching of gas exchange in several studies (21). To conclude, understanding how to assist athletes with regaining pre-COVID-19 infection performance is not only important for a safe return to play, but for performance too.
Sleep is important for the body to function properly, and can affect attitude, breathing, pulmonary VE, memory impairment, stress tolerance, BL concentrations, glycogen recovery, metabolic processes and immune function (26). In addition, reaction times, accuracy, perceptual abilities, skill performance, strength, power, endurance and overall athletic performance can be affected by sleep disturbances and may not allow adequate recovery from physical exertion (26, 28). Finally, lack of sleep and decreased ability for recovery may increase injury risk because of slower reaction times and decreased perceptual abilities (28).
Also, Jafarnezhadgero et al. (2022) suggested that COVID-19 infection may also alter rates of perceived exertion which can possibly affect running biomechanics. Further, Toresdahl et al. (2022) observed a potential cellular musculoskeletal deterioration from systemic inflammation of COVID-19 in a group of endurance runners. Since this investigation used only questionnaires, more research is necessary to confirm if the outcomes were a result of cellular musculoskeletal deterioration or if they were a result of deconditioning due to forced rest associated with illness which could be responsible for developing muscle weakness or neuromuscular control.
With the emergence of COVID-19 strains, understanding the symptomatology before and after disease is important for the determination of athletic integrity among individuals in sports (28). Fortunately, the emergence of new COVID-19 variants appears to have diluted pathologies or symptomatologies (8, 29). However, the authors emphasized that all athletes affected with the COVID-19 variants exhibited decreased collected values in VO2max. Stojmenovic and authors examined the effects of COVID-19 virus variants when compared to healthy athletes which never tested positive for COVID-19. Furthermore, testing was conducted during the athletic season where athletic capacity should be optimal. Additionally, Stojmenovic et. al. (2023) observed an adequate supply of O2 to the muscle in all three groups during testing and speculate an inefficiency with mitochondrial or cellular respiration caused by COVID-19 infection. Finally, Bruzzese and colleagues noted that although significant performance differences during CPET were observed in athletes pre and post COVID-19 infection, significant work intensities were attained.
Static balance is a skill for all sports and may help increase strength, power and speed (9). Fernández-Rodríguez and colleagues suggested that decrements to static balance may be due to the neurological impairment of sensory processing that may occur with COVID-19 infection. Moreover, sensory processing in sports is important for the cognitive control of decision making, planning of movement, organization of movement, thought planning and actual execution of performance (9). Lastly, other reasons for balance decrement can include mental health issues like depression, anxiety, inability to make decisions, fatigue and lack of sleep, cardiorespiratory impairments, or simply the forced break after infection with limited physical activity (9).
Bruzzese et al. (2023) suggested that a decrease in volume of O2 at second forced expiratory volume (FEV2) in evaluated athletes was a result of detraining from forced rest and isolation due to a positive COVID-19 diagnosis. Additionally, a case study by Barker-Davies et al. (2023) suggested that deconditioning due to imposed rest was a potential reason that might explain performance decrements. However, the individuals observed presented with normal stroke volume and cardiac output and values did not decrease as they would in a deconditioned individual. The authors further hypothesized that decreases in performance may also be a result of mitochondrial dysfunction, which has been observed with COVID-19 infection. Mitochondrial dysfunction is the result of the cells possessing an increased dependence of glucose rather than fat metabolism (4). Further, the authors explain that after calorimetry data review, the larger ratio of the metabolism of anaerobic to aerobic pathways may be another possible explanation for perceived decreases in power output. Finally, women appear to be more dependent on fat metabolism than men, thus reductions in aerobic pathways will probably have a greater impact on women (4).
Unfortunately, RTP for some athletes may not be an option because of persistent sequelae due to COVID-19 illness (12). Organizations like the National Strength and Conditioning Association and the Collegiate Strength and Conditioning Coaches Association Joint committee have recommended a gradual RTP which involves low intensity exercise once symptoms have subsided (12). From current studies, persisting sequalae among athletes post COVID-19 infection appear to resolve in 3-4 months and incidences of LC lasting more than three months was very low (3, 17, 23). Because the physical long-term health implications of COVID-19 to athletes are not fully understood and research is limited, an ambivalence for RTS protocols exists (11).
Currently, RTP protocols, which assist athletes to fully recover from illness, ranges from 1-4 weeks depending on severity of COVID-19 and generally have not included exercise stress (17, 25). Exercise should not be continued among symptomatic players that continue to experience persistent fever, dyspnea at rest, cough, chest pain, or palpitations, since high intensity exercise may increase inflammation and advance the rate of viral replication therefore negatively impacting immunity to exacerbate or even lengthen duration of illness (7, 19). Conversely, moderate exercise intensity has been noted to have positive effects on immunity (19).
Performance can be limiting as some athletes, specifically those with cardiac symptomatology, will require several months to clear symptoms and can lead to deconditioning, specifically to power and VO2max(5). Savicevic et al. (2021) noted absences resulting from COVID-19 infection ranged from 7-91 days and can have implications to detraining. Unfortunately, forced breaks in training due to COVID-19 illness may be the reason for decreases in mitochondrial functioning, which will decrease the oxidative capacity of the muscle and capabilities (12). Further, the lack of energy supply, coupled with possible decreases in oxygen transport, suggested to be a common consequence of COVID-19 infection, may contribute to fatigue during performances in sports (12). Additionally, voluntary skeletal muscle function and activation can also be compromised under circumstances of fatigue and can further precipitate early onset of fatigue and alter biomechanics of movement (12). However, the effects of detraining among elite athletes lasting less than 28 days have been observed to have non-significant effects on neuromuscular functioning (8).
Even with decrements in VO2max from COVID-19 infection, different sports have varying uses for aerobic capacity (21). For instance, sports like basketball and tennis rely primarily on anaerobic energy pathways, but rely on aerobic fitness for recovery, and resynthesis of phosphocreatine for the ATP-PC (21). Conversely, a sport like soccer will rely heavily on aerobic fitness with total distances covered by players in a game can range between 9-14 kilometers (21). Further, distance covered in a 90-minute soccer game is dependent on VO2max and lactate threshold and metabolite removal/recoverability (21). Additionally, with reference to team sports, Savicevic et al. stressed the fact that a decline in the performance of one team player could affect the performance of the entire team. Lastly, using CPET can be beneficial to observe athlete responses to high intensity demands and help distinguish between the effects of detraining or cardiorespiratory inefficiency from illness (21).
Conclusion
To conclude, COVID-19 infection does appear to affect athletes adversely and may last for several months. Although small, these differences could affect team success or individual success in sports. Additionally, some athletes recovered from acute COVID-19 infection continue to feel fatigued under physical exertions even when medical screening, physical fitness tests and power output results were within normal limits and may cause limitations during athletic performance. Individuals experiencing these symptoms of fatigue after a short-forced rest may be a result of viral infiltration resulting in mitochondrial dysfunction, while longer forced rest times may be contributed to deconditioning along with metabolic deficiencies. Fortunately, these issues appear to be reversible as observed with Babity et. al. (2022), where athletes were observes to have better CPET values post infection with a rigorous retraining protocol. Lastly, further research on decrements during competitive performance is necessary to fully understand the true effects of the virus infiltration among athletes since laboratory conditions cannot replicate the actual competitive environment.
Applications to Sport
Due to the complicated nature of COVID-19 and slow recovery associated with persistent fatigue which may be a result from a possible disconnect to pulmonary efficiency, capillary perfusion or mitochondrial function, screening for exertional stressors during athletic performance is highly recommended with CPET and spirometry. Further, the problematic physical circumstances of COVID-19 illness can prevent athletes from returning to sport at physically competitive levels. Individualized gradual RTP is recommended to acclimatize athletes to the high intensity demands of sports since small decrements to performance can produce negative consequential outcomes during play in competitive sports.
Limitations
There were several limitations to this review. First, many of the studies conducted had small sample sizes. Second, most of the testing was conducted with male athletes. Third, limited data was available from CPET and cardiac screening before infection among test subjects which did not allow for comparative investigations. Also, since COVID-19 is a relatively new epidemic and disease, limited data is available, especially among the athletic population and vaccinated individuals. Additionally, data varies with respect to recovery times and physical conditioning as some testing was conducted after RTP or during the competitive season. Lastly, very limited data investigating strength and power was available and is of interest since many decrements to performance were observed during high intensity exercises in a few investigations.
Acknowledgements
Special thanks to Drs. Frank Spaniol and Dr. Donald Melrose for all their support and advice.
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