RESEARCH ARTICLE
Recovery of performance and persistent
symptoms in athletes after COVID-19
Shirin VollrathID1*, Daniel Alexander Bizjak1, Jule Zorn1, Lynn Matits1,2, Achim Jerg1,
Moritz Munk1, Sebastian Viktor Waldemar Schulz1, Johannes Kirsten1,
Jana SchellenbergID1, Ju¨rgen Michael SteinackerID1
1 Division of Sports and Rehabilitation Medicine, Department of Medicine, Ulm University Hospital, Ulm,
Germany, 2 Clinical & Biological Psychology, Institute of Psychology and Education, Ulm University, Ulm,
Germany
* shirin.vollrath@uniklinik-ulm.de
Abstract
Introduction
After the acute Sars-CoV-2-infection, some athletes suffer from persistent, performance-
impairing symptoms, although the course of the disease is often mild to moderate. The rela-
tion between cardiopulmonary performance and persistent symptoms after the acute period
is still unclear. In addition, information about the development of this relationship is lacking.
Objective
To assess the prevalence of persistent symptoms over time and their association with the
performance capability of athletes.
Methods
We conducted two cardiopulmonary exercise tests (CPET) in a three months interval with
60 athletes (age: 35.2±12.1 years, 56.7% male) after infection with Sars-CoV-2 (t0: study
inclusion; t1: three months post t0). At each examination, athletes were asked about their
persistent symptoms. To evaluate the change of Peak VO2/BM (Body Mass) between the
time before infection and the first examination, the VO2/BM (predVO2) before infection was
predicted based on anthropometric data and exercise history of the athletes. For data analy-
sis, athletes were grouped according to their symptom status (symptom-free, SF; persistent
symptoms, PS) and its progression from the first to the second examination 1) SF-SF, 2)
PS-SF and 3) PS-PS.
Results
Comparing the SF and PS groups at t0, significant differences for Max Power/BM, Max
Power/lbm (lean body mass), Peak VO2, Peak VO2/BM, Peak VO2/lbm, Peak VO2/HR,
Peak VE, Peak Vt and VE/VCO2-Slope were observed. Regarding the progression over
three months, an increase in Max Power/BM was shown in SF-SF and PS-SF (tendency).
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OPEN ACCESS
Citation: Vollrath S, Bizjak DA, Zorn J, Matits L,
Jerg A, Munk M, et al. (2022) Recovery of
performance and persistent symptoms in athletes
after COVID-19. PLoS ONE 17(12): e0277984.
https://doi.org/10.1371/journal.pone.0277984
Editor: Emiliano Cè, Universita degli Studi di
Milano, ITALY
Received: August 5, 2022
Accepted: November 7, 2022
Published: December 7, 2022
Copyright: © 2022 Vollrath et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the article and its Supporting information
files.
Funding: The Study was funded by the Federal
Institut of Sport Science of Germany. Project
Number: 070106/20-23 https://www.bisp.de/
SharedDocs/Kurzmeldungen/DE/Nachrichten/
2021/COVID19KohortenstudiePodcast.html Funder
did not play any role in the study design, data
collection and analysis, decision to publish, or
preparation of the manuscript.
Max Power/lbm increased in SF-SF and PS-PS (tendency). A decrease of VE/VCO2-Slope
in PS-PS was found.
Conclusion
COVID-19 led to a decline in performance that was greater in PS than in SF. Additionally,
PS had decreased ventilatory parameters compared to SF. Furthermore, an improvement
over time was observed in some CPET parameters and a partial recovery was observed
judging by the decrease in various symptoms.
Introduction
The long-term sequelae of COVID-19 are manifold and patients suffer from the symptoms for
up to 12 weeks after infection (Long-COVID) or even longer (Post-COVID) [1–3]. Not only
people who were hospitalized in the acute period, even people with a mild or moderate disease
course can suffer from Long-COVID [4]. Furthermore, athletes, who mostly do not have
comorbidities, can be seriously affected by COVID-19 [5, 6]. In addition, symptoms can also
occur for the first time after recovery from the infection [1], resulting in a lower performance
capability of patients and athletes [7–10].
The limitations reported by patients vary in severity and symptomatic expression [11, 12].
To exclude organic restrictions and / or to evaluate the performance capability of the cardio-
pulmonary and respiratory system, cardiopulmonary exercise testing (CPET) can be con-
ducted [13]. Previous research focused on various CPET variables like breathing reserve,
Respiratory Exchange Ratio, Peak VO2, Peak Heart Rate or PETCO2 [14–16]. CPET is already
recommended and used in Long-COVID and Post-COVID studies to assess the limitations in
the cardiopulmonary and respiratory system after COVID-19 [17–21]. To gain insights how
persistent symptoms develop over time, it is important to monitor patients who have previ-
ously been infected with Sars-CoV-2 over at least several months up to several years by mea-
suring objective performance parameters, like Peak VO2 or VE/VCO2-Slope over time [22].
Although the majority of athletes represent a healthy part of the general population, they
have an increased need for health monitoring because they expose their bodies to increased
loads during heavy exercise, training and competition. However, there is only limited knowl-
edge about the development of the performance and cardiopulmonary function of athletes
after a Sars-CoV-2 infection, especially when athletes suffer from persistent symptoms.
Therefore, this study aims to evaluate the athletes’ symptom state, cardiopulmonary func-
tion, and performance capacity after infection and three months later. Thus, the predicted
performance capacity before infection was compared with the performance capacity post-
infection. Furthermore, it was of interest whether athletes with persistent symptoms have
decreased cardiopulmonary function and performance. In addition, the relationship between
the predicted aerobic capacity and decreased infection-related performance was analyzed.
Finally, the development of the recovery process of athletes with and without persistent symp-
toms over three months was studied.
Material and methods
The study was conducted at the Division for Sports and Rehabilitation Medicine, Center of
Internal Medicine of the University Hospital in Ulm, Germany. All athletes were participants
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Competing interests: The authors have declared
that no competing interests exist.
Abbreviations: Bf, Breathing Frequency; BM, Body
Mass; CFS, Chronic Fatigue Syndrome; CoSmo-S,
COVID-19 in elite sports – A multicenter cohort
study; COVID-19, Corona Virus Disease 2019;
CPET, Cardiopulmonary Exercise Test; IC,
Inspiratory Capacity; lbm, Lean Body Mass; MVV,
Maximal Voluntary Volume; PETCO2, Partial End
tidal Carbon dioxide; predVO2, Prediction of
Volume Oxygen before infection; PS, Persistent
Symptoms Group; RER, Respiratory Exchange
Ratio; SF, Symptom-free Group; t0, Study
inclusion, first examination; t1, Three months post
t0, second examination; VE/VCO2-Slope, Ventilation
/ Volume Carbon dioxide Slope; VE, Ventilation;
VO2, Volume Oxygen; Vt/VC, Tidal Volume / Vital
capacity; Vt, Volume Tidal; VT1, Ventilatory
Threshold 1.
of the CoSmo-S study (COVID-19 in German Competitive Sports) [23]. The inclusion criteria
were 1) Age  18 years, 2) Sport at least three times per week (20 metabolic equivalents
(METs) / week), 3) confirmed Sars-CoV-2 infection but at least > 2 weeks after a positive
PCR-test. Further details of the inclusion / exclusion criteria and the study design can be
found in the study protocol by Niess et al. [23].
Ethical approval
All participating athletes took part voluntarily and gave informed consent prior to inclusion.
The study was performed in accordance with the Declaration of Helsinki. The study was
approved by the ethics committee of Ulm University (EK 408/20).
Investigation period
The period of investigation was between June 2020 and January 2022, but the examination of
study participants is still ongoing at the time of submission of this manuscript. All athletes
who had at least two examinations, in a three months interval, with CPET until January 2022
were included in this pilot evaluation.
Study population
In total, 60 persons were included (56.7% male). There were two time points of investigation:
The first one (t0) (4.1 ± 3.8 months after infection) was at the day of study inclusion; the sec-
ond one (t1) three months later (3.3 ± 0.5 months).
Examination of symptoms
At both examination dates, the athletes were asked about the presence of persistent symptoms
based on the international consensus criteria for myalgic encephalomyelitis / chronic fatigue
syndrome and medical history evaluation [24]. The symptoms were differentiated into eight
symptom categories (Fatigue and performance decrease, Sleeping disorders, Neurocognitive dis-
orders, Respiratory disorders, Autonomic disorders, Pain, Psychological-related items, Immuno-
logical disorders). The severity of the symptoms is not rated in this questionnaire. All
symptoms assigned to the different categories appeared for the first time after or during
COVID-19. Once a symptom was mentioned, it was documented as "present" in the respective
category and the participant was grouped into the category Persistent Symptoms (Group PS).
Athletes who reported no symptoms related to COVID-19 at t0 were assigned to the symptom-
free group (Group SF). The athletes could report multiple persistent symptoms. Thus, an ath-
lete could be listed in several symptom categories.
Examination of body composition
For measuring weight and body fat, a bio-impedance-scale (InBody 770, InBody Europe B.V.,
Eschborn, Germany) was used. Lean Body Mass (lbm) was calculated as follows: lbm (kg) =
weight (kg)–body fat (kg). Lean body mass was used to diminish differences by gender.
Prediction of peak oxygen consumption before infection
The VO2 Peak before infection (predVO2) was predicted by three different experts blinded to
all information except the kind of sport, training and performance data before infection from
an athletes-questionnaire, medical history and anthropometric data. They estimated the VO2
Peak (ml/min/kg/BM) in intervals with a width of 5 ml in the range from “ 15 ml” to “> 65
ml”.
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CPET
The physical performance was tested by a CPET, conducted with the breath-by-breath (Ergos-
tik, Geratherm Respiratory, Bad Kissingen, Germany). All examinations were conducted on a
cycling ergometer (Excalibur Sport, LODE B.V., Groningen, Netherlands). The ramp protocol
was chosen according to the estimated fitness level, age, sex and weight of the athletes so that
total exhaustion was reached in the desired time (8–12 min). The same protocol was chosen at
the second measuring point. All CPETs were evaluated by the same examiner. To set individ-
ual reference values like calculated MVV (maximal voluntary volume) and IC (inspiratory
capacity) for the athletes, a spirometry was conducted before CPET using the same device.
The following variables were measured: Max Power/BM (W/kg BM), Max Power/lbm (W/
kg lean body mass), Peak VO2 (l/min), Peak VO2/BM (ml/min/kg BM), Peak VO2/lbm (ml/
min/kg lean body mass), Peak Heart Rate (HR) (1/min), Peak VO2/HR (ml/beat), Peak Venti-
lation (VE) (l/min), Peak Tidal Volume (Vt) (l/breath), Peak Breathing frequency (Bf) (1/
min), Peak Tidal Volume / Vital capacity (Vt/VC) (%), Ventilation/Volume of CO2 –Slope
(VE/VCO2-Slope).
Change of performance over three months
To determine whether the CPET variables changed over three months, three subgroups,
depending on their symptom status were formed in terms of progression: At t0 persistent
symptoms and at t1 symptom-free ! PS-SF, both at t0 and t1 persistent symptoms ! PS-PS,
both at t0 and t1 symptom-free ! SF-SF.
Statistics
The statistical analysis was performed using IBM SPSS Statistics, version 28.0.0.0 (IBM
Deutschland GmbH, Ehningen, Germany). Graphs were created with R version 4.1.1 (R Core
Team, 2020).
To evaluate the correlation of the different experts who estimated the predVO2, a Spearman
rho test was conducted. PredVO2 was calculated from the mean of the estimated intervals of
each rater. To calculate the difference between predVO2 and Peak VO2/BM in SF and PS, a
sign-test was conducted. To evaluate whether a difference in predVO2 between SF and PS
exists a Mann-Whitney-U test was conducted.
To examine the differences in CPET parameters between the different symptom groups
(PS: atheltes with persistent symptoms, SF: symptom-free athletes), t-tests and Mann-Whit-
ney-U tests were calculated. To control for possible confounding variables (time since infec-
tion and age), robust linear regression models were conducted.
To evaluate whether there is a change of the CPET variables in each group over three
months, a paired two-tailed t-test as well as a paired Wilcoxon-test were used.
Cohen’s d was calculated as effect size of the differences between the variables.
Missing values were always excluded in pairs in the analyses.
The significance level for all tests was set at (p<0.05).
Results
Progression of symptoms
In total, 60 athletes were included. However, not all parameters could be used for the analysis
due to implausible values during measurement or missing values. These values have been
excluded from the analysis presented in this study. At the first examination (t0), 16 of the 60
athletes were symptom-free. At t1, 23 athletes were symptom-free, of which nine athletes
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previously had symptoms at t0. While 44 athletes reported suffering from at least one symptom
at t0, this number decreased to 37 athletes at t1. Fig 1 shows the number of athletes with or
without symptoms at the two examinations.
Symptom categories
Fig 2 shows the number of athletes at both measurement points who reported at least one
symptom in the corresponding symptom category. With the medical history and the Interna-
tional Consensus CFS questionnaire [24], athletes were asked about persistent symptoms after
COVID-19. It was possible to report symptoms for more than one category. The number of
athletes with symptoms in the categories Fatigue and performance decrease, Neurocognitive
disorders, Respiratory disorders, Autonomic disorders and Pain decreased over time. Contrary
to that, the number of athletes with symptoms in the categories sleeping disorders, psychologi-
cal-related items and immunological disorders increased over time.
Number of symptom categories
Among the athletes who had persistent symptoms at t0, the highest number of athletes (n = 11)
had symptoms that belonged to two symptom categories, closely followed by both four symp-
tom categories (n = 10) and one symptom category (n = 10). At t1, 11 athletes had symptoms
from one symptom category, and nine athletes had symptoms from three symptom categories.
The highest numbers of symptom categories were seven at t0 and eight at t1.
Prediction of peak oxygen consumption before infection
The results of predVO2 of the three different expert raters correlated significantly (p<0.001).
The correlation factor shows how well the raters correspond with each other: rsp = 0.800, rsp =
0.628 rsp = 0.537. Fig 3 shows the means of the intervals of predVO2 and Peak VO2/BM at t0
for symptom-free athletes and athletes with persistent symptoms. The prediction of predVO2
differed significantly between SF and PS (p = 0.015). In both groups, there were differences
between predVO2 and Peak VO2/BM (SF: p = 0.004, PS: p<0.001). In SF, the means of pre-
dVO2 and Peak VO2/BM were in the intervals “> 45ml  50ml” and “> 40ml  45ml”,
respectively. In PS, the means of predVO2 and Peak VO2/BM were in the intervals “>
40  45ml” and “> 30ml  35ml”, respectively. In 45 athletes, Peak VO2/BM was decreased at
least one interval (~5 ml/min/kg BM) compared to the value predicted for the time before the
infection. Of these, 19 athletes had a peak VO2/BM lower by more than 10 ml/min/kg BM
Fig 1. Development of symptom status. Symptom status of all 60 athletes at t0 (first examination date) and t1 (3.3 ± 0.5 months post first examination).
35 of 44 athletes, who had persistent symptoms at t0 still stated persistent symptoms at t1 (progression group PS-PS). Nine athletes became symptom-
free over three months (progression group PS-SF). 14 of the 16 athletes remained symptom-free over the observation period (SF-SF). Two athletes
developed symptoms over time. Data were collected with medical history and the International Consensus CFS questionnaire [24].
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compared to predVO2, and two athletes had a deficit of more than 25 ml/min/kg BM com-
pared to predVO2. Athletes who were symptom-free at t0 had a lower decrease of Peak VO2/
BM than athletes with persistent symptoms. In eleven athletes, predVO2 was one interval
lower or at the same interval as measured at t0.
CPET
Table 1 shows the anthropometric and CPET data of all athletes at t0. The 35.15 (±12.14) years
old population had a mean of 36.80ml (±10.53ml) maximal oxygen consumption and was able
to perform 3.66W (±1.12W) per kilogram body mass.
The descriptive data tables for PS and SF (S1 and S2 Tables) and for the progression groups
(S3 Table) can be found in the appendix. The mean exercising time of the CPET was 09:27
min (±01:50 min). In 80.3% of the conducted CPETs, a RER  1.15 (Respiratory Exchange
Ratio) was achieved (t0: 76.6%; t1: 85.0%).
Differences between symptom-free athletes and athletes with persistent
symptoms
Table 2 shows the anthropometric data for SF and PS at t0. Age (p = 0.044) and time since
infection (p = 0.004) were possible factors influencing the results of the Mann-Whitney-U test.
Fig 2. Course of symptom categories over investigation period. Number of athletes who stated at least one symptom in the eight symptom categories
at t0 (first examination date) and t1 (3.3 ± 0.5 months post first examination). Data of symptom categories were collected with medical history and the
International Consensus CFS questionnaire [24]. In total 44 athletes stated at least one symptom at t0 and 37 athletes at t1 (3.3 ± 0.5 months post first
examination). Athletes could state symptoms in multiple categories.
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Therefore, age and time since infection were considered as possible confounders in further
analyses. The detailed test statistic can be found in the appendix (S4 Table).
Fig 4 shows significant differences between PS and SF at t0. Significant differences were
found between Max Power/BM (dif = 25.17%, p = 0.001, d = 0.419), Max Power/lbm
Table 1. Anthropometric and CPET data of study population (N = 60) at t0 (first examination date). Values are
given as mean and standard deviation (SD).
Anthropometrics & CPET variables
N
Mean (±SD)
Age (years)
60
35.15 (±12.14)
Body Mass (kg)
60
74.78 (±15.11)
Height (cm)
60
175.75 (±9.05)
Body Mass Index (kg/m2)
60
24.03 (±3.61)
Lean Body Mass (kg)
58
59.12 (±11.59)
Max Power/BM (W/kg BM)
60
3.66 (±1.12)
Max Power/lbm (W/kg lbm)
58
4.59 (±12.14)
Peak VO2 (l/min)
56
2.74 (±0.87)
Peak VO2/BM (ml/min/kg BM)
56
36.80 (±10.53)
Peak VO2 /lbm (ml/min/ kg lbm)
55
46.04 (±9.77)
Peak HR (1/min)
52
171.69 (±14.87)
Peak VO2/HR (ml/beat)
50
15.58 (±4.64)
Peak VE (l/min)
60
106.48 (±35.16)
Peak Bf (1/min)
60
39.77 (±8.00)
Peak Vt (l/breath)
60
2.66 (±0.66)
Peak Vt/VC (%)
60
56.98 (±8.67)
VE/VCO2-Slope
60
25.83 (±4.45)
Abbreviations: Bf: Breathing frequency; lbm: Lean Body Mass; VE: Ventilation; VE/VCO2-Slope: Ventilation /
Volume Carbon dioxide Slope; VO2: Volume Oxygen; Vt: Volume Tidal; Vt/VC: Tidal Volume / Vital capacity
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Fig 3. Differences between predVO2 and Peak VO2/BM. Significant differences of means between the calculated
Peak VO2 (predVO2) and in PS and SF at t0 (first examination). In both groups the measured values were significantly
below the values predicted for the time before infection. p<0.01, p<0.001.
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(dif = 16.86%, p = 0.008, d = 0.347), Peak VO2 (dif = 23.17%, p = 0.004, d = 0.385), Peak VO2/
BM (dif = 24.63%, p<0.001, d = 0.476), Peak VO2 /lbm (dif = 16.32%, p = 0.005, d = 0.375)
(Peak VO2/HR (dif = 21.53%, p = 0.009, d = 0.371), Peak VE (dif = 20.43%, p = 0.021,
d = 0.299) and VE/VCO2-Slope (dif = -13.77%, p = 0.008, d = 0.340). When considering time
since infection as a confounder, a tendency was observed for the variable Peak Vt (p = 0.082).
Without consideration of any confounder (dif = 15.67%, p = 0.010, d = 0.331) or with consid-
eration of age (p = 0.012) there was a significant difference, respectively. Even with consider-
ation of time since infection or age, no differences were found for Peak HR, Peak Bf, and Peak
Vt/VC.
Table 2. Anthropometric data and test statistic for being a confounder in SF (symptom-free) and PS (persistent symptoms) at t0 (first examination date).
Group & Examination Time Point
SF at t0
PS at t0
Mean (±SD)
Mean (±SD)
U
p-value
Age (years)
30.06 (±9.21)
37.00 (±12.63)
2.016
0.044
Body Mass (kg)
73.49 (±11.38)
75.24 (±16.34)
0.117
0.907
Height (cm)
177.19 (±8.50)
175.23 (±9.28)
-0.494
0.621
Body Mass Index (kg/m2)
23.20 (±2.73)
24.33 (±3.87)
0.828
0.408
Lean Body Mass (kg) (N = 58)
63.12 (±10.3)
57.58 (±11.94)
-1.583
0.113
Time since infection (months)
2.44 (±3.08)
4.73 (±3.96)
2.880
0.004
U = test statistic of Mann-Whitney-U-Test, significance level p<0.05.
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Fig 4. Differences in CPET between SF and PS at study inclusion. SF (symptom-free) had significantly higher mean
values for (A) Max Power/BM, (B) Max Power/lbm, (C) Peak VO2, Peak VO2/BM, (E) Peak VO2/lbm, (F) Peak VO2/
HR, and (G) Peak VE at t0 (first examination date). PS (persistent symptoms) had higher mean value for (I) VE/VCO2-
Slope compared to SF at t0. (H) Without confounder, a significantly higher mean value of Peak Vt in SF could be
observed. p<0.05, p<0.01, p<0.001.
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Change of CPET parameters over three months per progression group
The variable Max Power/BM (Fig 5, Panel A) changed between both examinations in SF-SF
(dif = 4.05%, t(13) = -3.239, p = 0.006, d = -0.866). In PS-SF, a tendency (p<0.1) for the vari-
able Max Power/BM could be observed (dif = 4.39%, t(8) = -1.999, p = 0.081, d = -0.666).
These athletes were able to generate more power per kg BM at t1 than at t0.
In SF-SF, a significant difference between the two examination dates was shown for Max
Power/lbm (dif = 3.67%, t(13) = -2.847, p = 0.014, d = -0.761) (Fig 5, Panel B). For Max Power/
lbm in PS-PS a tendency was observed (dif = 1.94%, t(34) = 1.872, p = 0.061) (Fig 5, Panel B).
In PS-SF, this variable did not change. No other variables changed in SF-SF.
In PS-PS a difference for the variable VE/VCO2-Slope (dif = -5.98%, t(34) = 2.827,
p = 0.008, d = -0.478) was observed. The mean of this variable decreased over time (Fig 5,
Panel C). Variable VE/VCO2-Slope did not change in SF-SF and PS-SF.
Discussion
We hypothesized that athletes have a decreased performance after COVID-19 and the perfor-
mance decrease is related to persistent symptoms. In the follow-up examination, three months
later, we observed a decrease in symptoms and a partial recovery of performance.
Symptoms
Our study showed that at t0, 73.3% of athletes who were previously infected with Sars-CoV-2
still suffered from COVID-19-related symptoms, collected with a questionnaire based on the
international consensus criteria for myalgic encephalomyelitis / chronic fatigue syndrome.
Three categories were most frequently reported: fatigue and performance decrease, neurocog-
nitive disorders and sleeping disorders. Komici et al. [6] conducted a study with competitive
athletes in which they found that anosmia was the most common persistent symptom, whereas
results similar to ours were shown by Carfi et al. [25]. They observed that 12.6% of the patients
who had been hospitalized due to COVID-19 showed ongoing symptoms after 60.3 days since
onset of the first COVID-19 symptom. The most reported long-term symptom in their study
was fatigue, followed by dyspnea. Goe¨rtz et al. [26] also found persistent symptoms in hospital-
ized persons and in people with mild or moderate courses. The symptoms most frequently
observed by them are equivalent to those in the study by Carfi et al. [25]. Fatigue is also the
most reported symptom category in our study, but the second one is sleeping disorders or neu-
rocognitive disorders. These are functional impairments that may get more present over a
Fig 5. Change of CPET variables over three months. (A) Variable Max Power/BM had in SF-SF (symptom-free–
symptom free) significantly higher mean values at t1 (three months post first examination) than at t0 (first examination
date). (B) Variable Max Power/lbm had in SF-SF significantly higher mean values at t1 than at t0. (C) Variable VE/
VCO2-Slope had in PS-PS significantly lower mean values at t1 than at t0. p<0.05, p<0.01.
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longer period, for example, sleeping disorders increased in our study over time. A further rea-
son could be the different study population.
Goe¨rtz et al. [26] observed a decline in symptoms for hospitalized and non-hospitalized
patients over time. Their cohort was asked about symptoms during the acute infection and
about existing symptoms approximately 80 days after the onset of initial symptoms. These
patients reported a reduction in fatigue (95% vs. 87%) and dyspnea (90% vs. 71%). This is in
line with our results at the follow-up after three months where fewer athletes reported persis-
tent symptoms. In addition, in our study, the number of persistent symptoms per person also
declined in most of the cases. However, the symptoms in the categories of sleeping disorders,
psychological-related items and immunological disorders increased. The origins of mental ill-
ness after a Sars-CoV-2 infection can be manifold, e.g. neurotrophic factors or impaired learn-
ing and memory [27]. Raveendran et al. [28] showed that psychological-related items are
common for Long-COVID, which is in accordance with our results. This could be indicative
of a development of psychological items due to an ongoing inflammation in the brain or the
persistent low physical capability, which can negatively affect mental health [29]. A recent
review by Haller et al. [30] showed that persistent fatigue is a risk factor for a decreased life
quality and work capacity. Furthermore, they observed that pre-existing psychological disor-
ders also increase the risk for the Post-COVID syndrome [30]. Therefore, our results that psy-
chological disorders increased over time, could indicate that the life quality decreases with
persistent fatigue. Therefore, it seems necessary to monitor not only the performance capabil-
ity but also the mental well-being, for example with the EQ-5D questionnaire [31], and for
symptom collection, the International consensus CFS questionnaire could be used [24].
Prediction of peak oxygen consumption before infection
The results of the comparison between predVO2 and the measured VO2/BM show that
COVID-19 leads to a decrease in performance, regardless of whether or not persistent symp-
toms exist. However, the performance decline is smaller in symptom-free athletes than in ath-
letes with persistent symptoms. Furthermore, athletes with a higher estimated predVO2 are
less likely to suffer from persistent symptoms. This is consistent with the findings by Massey
et al. [32] who also found a lower prevalence of Long-Covid in athletes compared with the gen-
eral population.
Performance in CPET
19.7% of our conducted CPETs ended without objective total exhaustion (RER<1.15),
although all of our athletes reported subjective exhaustion at the end of the test. This suggests
that some individuals were unable to exhaust themselves due to unknown mechanisms.
Additionally, we found decreased Max Power/lbm, Peak VO2/lbm, Peak VO2, and Peak
VO2/HR, in athletes with symptoms compared to athletes without symptoms. This declined
performance capability stands in contrast to the results by Anastasio et al. [33], who could not
find differences in oxygen consumption at the maximum load between elite cross-country ath-
letes with a mild-moderate disease course and healthy peers. However, they found differences
at the ventilatory threshold 1 (VT1), which is an indicator of the aerobic capacity and thus it
has an impact on the general performance capability. This result is in line with the result of a
reduced Peak VO2/HR in our study because a reduced Peak VO2/HR can be, among others, an
indicator of a limited aerobic capacity. A difference to our study is the shorter average period
between infection and examination, the training status (all of their study participants com-
peted in national and international competitions) as well as the gender distribution (77%
male). As mentioned above, they only included mild-moderate COVID-19 courses and thus
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they excluded all patients who suffered from dyspnea. This could explain why no differences
were found for other ventilatory variables.
Our results are in accordance with the results by Skjørten et al. [34]. They also observed
decreased performance capability parameters, like peak oxygen uptake and oxygen pulse, three
months after the Sars-CoV-2 infection in hospitalized patients. In addition, reduced Peak VO2
was observed by Debeaumont et al. [22] in a CPET six months after infection, while Barbage-
lata et al. [35] focused on patients with and without Post-COVID-19 syndrome and also found
a lower Peak VO2 in patients with Post-COVID-19 syndrome. This result is in accordance
with our result with an above-average fit cohort: Athletes with persistent symptoms have a
lower Peak VO2/BM than athletes who are symptom-free. In contrast to this, Komici et al. [6]
could not find any significant differences in CPET between competitive athletes who were
either post-acute Sars-CoV-2 infection or who had not been infected. However, they did not
cluster in accordance to their persistent symptoms.
Ventilatory parameters of CPET
In our study, the ventilatory parameters Peak VE, Peak Vt and VE/VCO2-Slope differed signif-
icantly between PS and SF at t0. It was already shown that besides a reduced VO2 peak con-
sumption, patients with persistent dyspnea have a higher VE/VCO2-Slope and a higher
PETCO2 than symptom-free patients [14]. While Ladlow et al. [36] did not find an association
between reported symptoms by the patients and the perceived functional limitation and dysau-
tonomia, they found an association between dysautonomia and reduced work rate, VO2 peak
and VE/VCO2-Slope. Further studies also showed an increased VE/VCO2-Slope [37, 38]. A
high VE/VCO2-Slope could be a result of hyperventilation, a lung obstruction or reduced lung
perfusion [39]. However, the breathing frequency did not differ significantly between PS and
SF, but Peak Vt was lower in PS compared to SF. This could indicate that these athletes are not
able to inhale the same volume compared to athletes from SF. Decreased Peak Vt can be
caused by prolonged sedentary behavior due to persistent symptoms which limit activity dur-
ing daily life. Due to this circumstance, the auxiliary respiratory muscles can degenerate and
this could result in a less efficient and less powerful breathing technique [39]. However, the
ratio Peak Vt/VC was not significantly different between both groups. Therefore, further
research regarding a potential auxiliary respiratory muscle degeneration may be useful.
CPET variables of the three months follow-up
To be able to provide information on how performance develops over time, long-term moni-
toring is necessary. Recent published studies and recommendations also state the need for
long time monitoring [21, 40, 41]. Studies with long-term monitoring and repeated examina-
tions of patients and athletes are rare. In our monitoring study, we showed that there is an
improvement of the VE/VCO2-Slope and a tendency of improvement for Max Power/lbm for
athletes with persistent symptoms (PS-PS). A tendency of enhancement of Max Power/BM
was shown in PS-SF, and in SF-SF an improvement of Max Power/BM and Max Power/lbm.
The results for SF-SF could indicate that a larger amount of training, after isolation and protec-
tion of the body due to the infection, led to an improvement of the performance over time that
had been decreased due to acute illness. It can be assumed that athletes are more likely to
return to sport after an acute infection than people with a more sedentary lifestyle.
The observed decrease of VE/VCO2-Slope in PS-PS indicates that there is a slow regenera-
tion of the ventilatory efficiency, despite persistent symptoms. It is possible that there are still
persistent symptoms while the intensity of the symptoms declines. Although we did not assess
the intensity, this would be in accordance with the results by Rooney et al. [42], who showed
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that there is an ongoing but still incomplete regeneration occurring in a proportion of previ-
ously infected individuals. A change in the VE/VCO2-Slope can result from a change in venti-
lation. However, we did not see any significant differences in Peak VE, Peak Vt, or Peak Bf.
Therefore, we assume that the improved VE/VCO2-Slope is caused by a better lung perfusion.
Furthermore, the tendency of improvement in Max Power/lbm and the descriptive data
showed an improvement in the general performance capacity (Peak VO2, Peak VO2/BM,
VO2/HR), which may indicate a general recovery.
In PS-SF, a tendency of improvement for Max Power/BM was found. This is in accordance
with the results of PS-PS. The performance capacity increased slightly over time. Furthermore,
descriptive data showed slightly improved ventilatory parameters. Regarding the ventilatory
parameters, it is possible that the athletes declared being symptom-free at t1 because they
potentially felt better due to less restriction during ventilation.
Limitations
Nine of 60 athletes in the study met the criteria of the PS-SF group. This relatively low number
is a probable reason why no significant results could be shown here. However, a tendency
could be shown that might indicate that significant differences could be shown with a higher
number of athletes. One further limitation was that the intensity of the symptoms was not
asked. Furthermore, the partly unknown medical history and the athletes’ unknown behavior
between the examinations reduce the explanatory power of this study’s results. However, the
different training behavior between the two examination dates is difficult to control due to the
different duration of symptoms. Although the participants were selected according to the
inclusion criteria, a certain heterogeneity of the group could not be avoided.
Conclusion
The study showed that after COVID-19, 70.3% of athletes stated having symptoms in the ques-
tionnaire at the first examination and 61.7% had persistent symptoms at the second examination.
In both groups, the maximal oxygen uptake was decreased compared to predicted maximal oxy-
gen uptake before infection. Moreover, the reduction in VO2/BM in symptom-free athletes was
smaller than in athletes with persistent symptoms. Athletes with a higher maximal oxygen uptake
before infection were less likely to report persistent symptoms after a Sars-CoV-2 infection.
The study showed differences in ventilatory (VE, VE/VCO2-Slope) as well as in general per-
formance parameters (e.g. Max Power/BM, PeakVO2/BM and Peak HR/VO2) between symp-
tom-free athletes and athletes with persistent symptoms. Which area (respiratory, cardiac and/
or muscular) is restricted and how long the restrictions last seems to be individual. Neverthe-
less, the decrease of the respiratory equivalent for athletes with long-term symptoms indicate a
slow recovery of the respiratory tract. To explain the mechanism of this fact further studies are
needed. In further studies, possible correlations of symptom categories, and CPET parameters,
for example, Max Power/lbm, Peak VO2/kg or VE/VCO2-Slope should be investigated. Fur-
thermore, there is a need to investigate the reason for performance decline and long-lasting
symptoms and the reasons why a number of people suffer from persistent symptoms for such
a long period and other do not. To gain further insights into athletes’ recovery and the progres-
sion of persistent symptoms, a longer period of monitoring as well as a still higher number of
patients are needed.
Supporting information
S1 Table. Descriptive data of the CPET variables for SF (symptom-free) and PS (persistent
symptoms) at t0 (first examination date). Abbreviations: Bf: Breathing frequency; lbm: Lean
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Recovery of performance and persistent symptoms in athletes after COVID-19
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December 7, 2022
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Body Mass; VE: Ventilation; VE/VCO2-Slope: Ventilation / Volume Carbon dioxide Slope;
VO2: Volume Oxygen; Vt: Volume Tidal; Vt/VC: Tidal Volume / Vital capacity.
(DOCX)
S2 Table. Descriptive data of the CPET variables for SF (symptom-free) and PS (persistent
symptoms) at t1 (three months post first examination). Abbreviations: Bf: Breathing fre-
quency; lbm: Lean Body Mass; VE: Ventilation; VE/VCO2-Slope: Ventilation / Volume Car-
bon dioxide Slope; VO2: Volume Oxygen; Vt: Volume Tidal; Vt/VC: Tidal Volume / Vital
capacity.
(DOCX)
S3 Table. Descriptive data of the CPET variables for SF-SF (symptom-free—symptom
free), PS-PS (persistent symptoms—persistent symptoms) and PS-SF (persistent symp-
toms–symptom-free) at t0 (first examination date) and t1 (three months post first exami-
nation). Abbreviations: Bf: Breathing frequency; lbm: Lean Body Mass; VE: Ventilation; VE/
VCO2-Slope: Ventilation / Volume Carbon dioxide Slope; VO2: Volume Oxygen; Vt: Volume
Tidal; Vt/VC: Tidal Volume / Vital capacity.
(DOCX)
S4 Table. Test statistic for the Mann-Whitney-U test without confounder, considering
time since infection or considering age. for each test: df = 1Abbreviations: β: beta weight; Bf:
Breathing frequency; lbm: Lean Body Mass; tsi: time since infection; VE: Ventilation; VE/
VCO2-Slope: Ventilation / Volume Carbon dioxide Slope; VO2: Volume Oxygen; Vt: Volume
Tidal; Vt/VC: Tidal Volume / Vital capacity.
(DOCX)
Acknowledgments
The authors thank all medical assistance for the study support and contribution to the develop-
ment and achievement of this research and all patients who participated in this study.
All authors have seen and approved the proposed article.
Author Contributions
Conceptualization: Shirin Vollrath, Daniel Alexander Bizjak, Achim Jerg, Moritz Munk,
Johannes Kirsten.
Data curation: Shirin Vollrath, Lynn Matits.
Formal analysis: Shirin Vollrath, Johannes Kirsten.
Funding acquisition: Ju¨rgen Michael Steinacker.
Investigation: Shirin Vollrath, Jule Zorn.
Methodology: Shirin Vollrath.
Project administration: Achim Jerg.
Supervision: Ju¨rgen Michael Steinacker.
Validation: Ju¨rgen Michael Steinacker.
Visualization: Lynn Matits.
Writing – original draft: Shirin Vollrath.
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Recovery of performance and persistent symptoms in athletes after COVID-19
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Writing – review & editing: Shirin Vollrath, Daniel Alexander Bizjak, Jule Zorn, Moritz
Munk, Sebastian Viktor Waldemar Schulz, Johannes Kirsten, Jana Schellenberg, Ju¨rgen
Michael Steinacker.
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Recovery of performance and persistent symptoms in athletes after COVID-19.
Vollrath, Shirin,Bizjak, Daniel Alexander,Zorn, Jule,Matits, Lynn,Jerg, Achim,Munk, Moritz,Schulz, Sebastian Viktor Waldemar,Kirsten, Johannes,Schellenberg, Jana,Steinacker, Jürgen Michael