Literature DB >> 35666729

The incidence and severity of COVID-19 in adult professional soccer players in Russia.

Eduard Bezuglov1,2,3, Vladimir Khaitin4,5, Artemii Lazarev1,2,6, Evgeniy Achkasov1, Larisa Romanova7,8, Mikhail Butovskiy9, Vladimir Khokhlov10, Maxim Tsyplenko11, Alexander Linskiy12, Petr Chetverikov13, Magomedtagir Sugaipov14, Arseniy Petrov15, Oleg Talibov2,16, Zbigniew Waśkiewicz1,17.   

Abstract

There are little data on the incidence, and clinical course of COVID-19 among professional soccer players, and the studies examining putative complications of COVID-19 infections are probabilistic. On February 28, the WHO raised the COVID-19 threat assessment to its highest level. The COVID-19 outbreak became a significant challenge for world health. Around 30 million people got infected with COVID-19 since the beginning of this year. More than 900.000 decease. Thus, examining the incidence of COVID-19 and various aspects of its clinical course in a group of adult professional soccer players would be of great practical interest. The incidence, clinical practice, and severity of COVID-19 infection, as well as the duration of treatment and return to play was studied based on a survey of team physicians and medical records assessment in the group of adult professional soccer players representing the clubs of the Russian Premier-League (RPL) during the period of championship resumption from 01.04.2020 until 20.09.2020. COVID-19 infection was detected in 103 soccer players during COVID-19 screening. This number comprises 14.5% of all soccer players on the rosters of RPL soccer teams and is subjected to regular COVID-19 testing. The asymptomatic course was observed in 43.7% of cases (n = 45). These players were isolated, and their clinical condition was monitored closely. In 56.3% of patients (n = 58), fatigue, headache, fever, and anosmia were the most common symptoms. COVID-19 infection was commonly diagnosed among adult professional soccer players in Russia. However, most cases had a mild course and did not impair return to regular exercise. Only two players were hospitalized with lung lesions and returned to regular sports.

Entities:  

Mesh:

Year:  2022        PMID: 35666729      PMCID: PMC9170087          DOI: 10.1371/journal.pone.0265019

Source DB:  PubMed          Journal:  PLoS One        ISSN: 1932-6203            Impact factor:   3.752


Introduction

Although their efficacy and safety are dubious, various therapeutic approaches for COVID-19 treatment are utilized. There have been very few studies to date that have investigated the clinical course of COVID-19 infection and its impact on the performance of soccer players [1, 2]. COVID-19 complications such as pulmonary fibrosis cardiac and hepatic consequences are actively studied [3]. The course of COVID-19 infection and its impact on athletic performance has not been studied in professional athletes. Nearly all soccer events had been canceled in March 2020 due to the fast-spreading of the global COVID-19 pandemic. As a result, most soccer players had to stop training [4-6]. During May-June 2020, sports events were resumed in several countries. However, the events took place without fans in most cases. In all cases when the events were resumed, the organizing sports leagues developed strict prevention and control measures to minimize the risk of infection for the participants [1, 2, 7]. The critical elements of these measures are as follows: close monitoring of the infection rates by PCR- tests; individual face masks and gloves wearing; surface and skin disinfection; adherence to social distancing guidelines. Nevertheless, media reports covering new infection cases among soccer players illustrate that as efficient as they are, these prevention measures cannot completely rule out the possibility of COVID-19 spreading in such a large population as soccer players. However, there is presently limited data on incidence and clinical course among professional soccer players, and the studies examining putative complications of COVID-19 infections are probabilistic. This research aims to investigate the clinical course of COVID-19 infection and its impact on the performance of adult professional soccer players as one of the most significant practical importance in sports medicine at the moment.

Materials and methods

Incidence, clinical course, and severity of COVID-19 infection, as well as the duration of treatment and recovery before return to play, were studied based on a survey of team physicians and medical records assessment in the group of adult professional soccer players representing the Russian Premier-League (RPL) clubs during the period of championship resumption from 01.04.2020 until 20.09.2020. The data of 710 soccer players who were on the rosters of 16 RPL clubs and 2 National Football League teams (second-tier soccer league in Russia) were included in the analysis. In addition, the study included players who were in the teams’ applications for the season and who were regularly tested following the existing national sanitary regulations. According to the RPL COVID-19 regulation, each player registered for a soccer match must undergo COVID-19 screening by submitting a throat and nostrils swab for a PCR test 3 days before the first play and once weekly after that [6]. Swabs were performed only by specialists from laboratories certified by the Federal Service for surveillance on consumer rights protection "Rospotrebnadzor"—a central Russian governmental entity responsible for sanitary and epidemiological surveillance. Teams used different laboratories. However, all laboratories had state accreditation. Without this test, the special QR-code to access the event would not be issued. All positive test results were automatically submitted to a centralized database and revised in special reference laboratories. Test results were available within 24–48 hours in most cases. According to the Russian quarantine rules, all individuals who tested positive for COVID-19 have to be isolated for 14 days regardless of their clinical symptoms. The quarantine can be lifted only after receiving two negative PCR-test results performed within 24 hours. Medical records of athletes diagnosed with COVID-19 by a PCR test were studied. Disease course (symptomatic/asymptomatic), the frequency of pulmonary involvement, and the severity of pulmonary lesions were assessed. The prevalence of distinct clinical findings, the therapeutic approaches, the duration of treatment, and recovery before return to play were included in the analysis. The team physicians were interviewed by telephone using a questionnaire compiled in advance. An independent clinical pharmacologist validated the questionnaire. All necessary information was obtained from the team physicians and, in some situations, from the athletes themselves. They measured their temperature and oxygen saturation daily to monitor asymptomatic players during quarantine. Also, they had to report the onset of any of the symptoms that appeared: cough, shortness of breath, loss of smell or taste, sore throat, and headache. This often happened when they were outside the team (at home or in the room at the training base). In such situations, the player was immediately advised to isolate himself. An independent clinical pharmacologist assessed all the medical records. All radiographic findings were initially evaluated by radiologists experienced in characterizing lung lesions. In addition, all players underwent regular testing following the adopted sanitary regulations, making it possible to identify and timely isolate initially asymptomatic carriers. However, such measures were not taken in Russia concerning representatives of the general population. The database was created with Microsoft Excel software; statistical analysis was performed utilizing the IBM SPSS 23.0 (Armonk, USA). Continuous data were tested for normality of distribution with the Kolmogorov-Smirnov test. Normally distributed data were described with Mean (M) and standard deviation (SD). Median (Me) and quartiles were used in case of abnormal distribution). Percentage and absolute numbers were provided for categorical data. Mann-Whitney U-test was performed to compare the duration of treatment and recovery before return to play between athletes with and without pulmonary lesions. Spearman’s correlation was used for non-normal distributed data. Results were considered statistically significant at p < 0.05. The study was approved by the local ethics committee (Sechenov University, protocol № 30–20 from 21.10.2020). Players provided written informed consent to participate in the survey. They explained that their medical documentation only served scientific purposes, and their data would be protected.

Results

COVID-19 infection was detected in 103 soccer players in the course of COVID-19 screening (average age: 25,1 ± 4,3 years, height: 183,7 ± 6,3 cm, weight: 76,6 ± 7,0 kg, BMI: 22,7 ± 1,4). This number comprised 14.5% of all soccer players on the rosters and underwent regular PCR testing. Out of the 103 infected players defensive midfielders were most frequently infected (n = 42; 40.8%), followed by defenders (n = 30; 29.1%), strikers (n = 19; 18.4%) and goalkeepers (n = 12; 11.7%). The asymptomatic course was observed in 43.7% of cases (n = 45). These players were isolated, and their clinical condition was monitored closely. Clinical symptoms were observed in 56.3% of cases (n = 58), the most common symptoms being fatigue, headache, fever, and anosmia (Table 1).
Table 1

Сlinical symptoms in soccer players with COVID-19 infection.

SymptomFrequency in symptomatic soccer players
(%, n)
Fatigue72.4%, 42
Headache65.5%, 38
t ≥38°C44.8%, 26
(Anosmia/parosmia)41.3%, 24
Sore throat31%, 18
37°C<Т <38°C27.6%, 16
Cough15.5%, 9
Diarrhea8.6%, 5
Myalgia6.9%, 4
Dyspnea1.7%, 1
In all COVID19 PCR-positive cases lung CT scan was performed. Pulmonary lesions were detected in 36.2% (n = 21) of symptomatic soccer players. And in 23.3% (n = 24) of players with positive test results (in 3 cases, pulmonary lesions were revealed in asymptomatic players. In asymptomatic patients, "frosted glass opacities" extended less than 10% of the lung. There were no fundamental differences in the structure of these players’ radiological changes compared to the radiological data of football players with clinical symptoms. All three asymptomatic players underwent CT because of their willingness, which undoubtedly did not match the current clinical recommendations. In all 24 cases, pulmonary lesion size was derived from CT images. Less than 10% of lung parenchyma were involved in 70.9% (n = 17) of cases, 11–20% in 16.6% (n = 4), and 20–29% in 8.3% (n = 2) of cases. Lesions involving more than 30% of lung parenchyma were detected only once (4.2%; n = 1). Two players (20 and 36 years old) were hospitalized with lung lesions (26% and 32%). They did not use oxygen therapy during their hospital stay. Lesions were most commonly associated with the following symptoms: fatigue (76.2%, n = 16), headache (71.4%, n = 15), t ≥ 38°C (52.4%, n = 11). Medical records (n = 61) were available for assessment. Players were clustered by the drug received (Table 2).
Table 2

Drugs utilized for the treatment of COVID-19 infection.

DrugsPrevalence (%, n)
Antivirals (Umifenovir)85.2%, 52
Antibiotics (Azithromycin)83.6%, 51
Polivitamins59%, 36
Anticoagulants (Enoxaparin)26.2%, 16
Interferons (intranasal interferon-gamma)14.8%, 9
Anti-malaria agents (hydroxychloroquine)11.5%, 7
NSAIDs (COX-2 selective inhibitors)6.6%, 4
The average treatment duration of symptomatic soccer players without pulmonary manifestations of the disease was 14,4 ± 4,8 days, and 17,4 ± 3,5 days in those with pulmonary lesions (p = 0.0083). Pulmonary lesions were not identified as a risk factor contributing to a longer duration of treatment, which were defined as the time for the disappearance of all symptoms (logistic regression, p = 0.09) or delaying the resumption of training as a regular player in the respective soccer team (logistic regression, p = 0.17). The significant duration of players with and without pulmonary lesions was registered (p = 0.022, Mann-Whitney), and no significant difference has been observed in the course of recovery before return to play (period of return to regular training activity, which was defined as the period from the moment of diagnosis of the disease to the start of training specific to the sport) (p = 0.29, Mann-Whitney). Treatment duration was significantly longer in the players with pulmonary lesions. There were no complications that required oxygen support or pulmonary ventilation. Low-flow oxygen support was not used in any case. After recovery, before return to training, all players underwent a thorough medical examination which is mandatory in Russia according to the Ministry of Health’s particular order. Admission of any football players to participate in competitions and regular training occurs only after passing a mandatory medical examination, performed twice a year. This examination includes a routine physical examination, clinical blood and urine test, ECG (rest and stress-test), spirography, chest X-ray. During this medical examination, no cardiovascular, pulmonary and hematological abnormalities were detected in players who recovered from COVID-19 infection. Before return to play, the average recovery duration was 18.0 ± 5.0 days (median±IQR). The recovery period lasted 18.0 ± 8.0 days (non-normal distribution) in those who suffered COVID pneumonia and 18.0 ± 5.0 days (non-normal distribution) in those with no pulmonary manifestations. No significant correlation in COVID-pneumonia and the duration of the recovery period was detected (Mann-Whitney, p = 0.32). The number of clinical findings assessed the disease severity. In all cases, the COVID-19 disease was mild, and the treatment algorithm in every case was determined individually. The age and clinical findings distribution are non-normal; thus, Spearman’s rank correlation coefficient was utilized. There was no significant and robust correlation between the age and clinical findings (p = 0.1; R = 0.18). Almost all soccer players who had symptomatic COVID-19 disease had already participated in soccer events to the moment of study recruitment.

Discussion

We have demonstrated the predominance of asymptomatic forms of COVID-19 infection among professional soccer players continuously residing in Russia. There were no severe complications. Furthermore, COVID19did not impair return to training after convalescence. This is the first study to investigate the progression of COVID-19 in professional soccer players with a focus on clinical and radiological findings. Grant et al. performed a systematic review and a meta-analysis of 148 scientific papers, including a total of 24410 adult patients with COVID-19 disease (age >16 years, average age 49 years) from 9 countries. The most common symptoms described were fever– 78%, cough– 57%, and fatigue– 31%. In addition, the headache was observed in 13% of cases, hyposmia– 25%, and myalgia—17%. In contrast to our study, Grant et al. assessed all symptoms in patients with a positive test result. Thus, the symptomatic course of the disease was less commonly observed in our study, which is most probably due to the younger age and excellent health of the soccer players [8]. Bergheim et al. performed a retrospective study of 121 symptomatic COVID-19 patients from China (average age 45±15.6 years). Pulmonary lesions were observed in 78% of patients. In our study, only 20.4% of soccer players had pulmonary manifestations, probably due to timely diagnosis and early treatment [9]. Meyer et al. [7] demonstrated a relatively low incidence of SARS-CoV-2 infections among German soccer players. During the study period from May to July 2020 (9 weeks), eight players were tested positive in the first PCR-testing round before the resumption of training sessions. Two players were tested positive in the third round of PCR testing, and 22 remained seropositive throughout the whole season. The numbers reported in this study are much lower than ours. Several factors might explain the differences. When club training and competitive matches in Russia were resumed, the fans were allowed to enter the stadium, facilitating the spread of infection. According to the sanitary regulations, players could not intersect with the spectators in any way since they immediately got out of the bus into the "clean" zone, which was the under-stands room and the field and the locker rooms. All people (except players) who were in the "clean zone" could get there only by passing a negative PCR test within 72 hours before the start of the match. In contrast to Russia, viewers were not allowed at Bundesliga games [7]. Another factor influencing the frequency of COVID-19 infections among Russian soccer players could be the frequent flying, thus a large number of close contacts. Each team had at least 20 flights, lasting >2 hours during the study period. Although the teams used charter flights, the risk of infection was nevertheless high. During teams’ stay at the training grounds and from the bus to the "clean" zone, all the players must wear masks. But unfortunately, not all Teams lived separately at the hotels or training grounds, in connection with which the players often stayed overnight at home. However, a higher detection rate in Russian players could be due to meticulous PCR-testing done by the physicians’ staff once a week, which allowed them to detect infections early and promptly isolate and treat the tested positive players. An essential aspect of the professional athlete’s treatment is strict adherence to anti-doping regulations. If prohibited substance use is necessary for t an athlete has to apply for a Therapeutic Exemption (TUE) by the respective national anti-doping association. Considering that the uniform COVID-19 treatment method has not been established yet, in some cases, it could be problematic to receive a TUE from the WADA retroactively, e.g., after being treated (e.g., with dexamethasone [10]. However, the treatment protocols applied to soccer players did not require the use of forbidden substances such as systemic glucocorticoid use. The recovery period to enable the safe resumption of training is critically important for soccer players. It is assumed that COVID-19 itself, as well as various therapeutics to treat the infection, might cause adverse effects on organs, primarily on the cardio-respiratory system [11]. However, the side effects might be sub-clinical and not appear instantly [12]. The importance of health monitoring in athletes who recovered from COVID-19 was stressed in previous studies [13]. According to Russian regulations, all professional athletes must undergo compulsory thorough medical examination twice a year. Those athletes who are non-compliant with this requirement will not receive permission from the national sports federation to train and participate in competitions [14]. The presence of a mandatory additional examination before admitting an athlete to physical and sports activity will allow identifying various deviations in the health status of athletes after suffering from COVID. After full recovery, all soccer players who had COVID19 diagnosed passed this type of examination, and none of them was diagnosed with any pulmonary or cardiac pathologies or exercise intolerance. Furthermore, no athletes got advice to restrain from physical activity irrespective of its intensity. Thus, asymptomatic and symptomatic soccer players with mild pulmonary manifestations of the disease did not demonstrate any impairment in respiratory and cardiovascular function or Exercise intolerance in the short-term after recovery from COVID-19 infection. The long-term effects of COVID-19 should be the focus of future research. At the survey time, the predominant virus strain was a wild strain (Wuhan strain). Nowadays, the new dominant strain may be more virulent and aggressive (e.g., B.1.167.2). This aspect must be considered when reading the article since all the results were obtained in a specific period when a particular virus strain prevailed.

Limitations of research

The research design was a retrospective survey that implies possible bias (e.g., recall bias).

Conclusion

COVID-19 infection was commonly diagnosed among adult professional soccer players in Russia. However, most infections had a mild course and did not impair return to regular exercise. (XLSX) Click here for additional data file.

Transfer Alert

This paper was transferred from another journal. As a result, its full editorial history (including decision letters, peer reviews and author responses) may not be present. 20 Dec 2021
PONE-D-21-35577
The Incidence and Severity of COVID-19 in Adult Professional Soccer Players
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Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: Yes ********** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: This is a relevant article in the context of the pandemic, because football matches and sports were suspended for many months. Methodology is sound and design is appropriate to estimate incidence. Paper has policy implications also because it highlights the need for regular screening based on the high proportion of asymptomatic cases. Reviewer #2: Review summary of the article PONE-D-21-355 A. Summary of the research: �  The article has addressed incidence, clinical course, severity of infection, types of conservative management and recovery from COVID-19 infection among 710 professional soccer players over 18 league teams in Russia. �  It was mostly a study of secondary data analysis besides telephonic interview of team physicians and sometimes from athletes themselves. �  Among the players, 14.5% were detected to have COVID-19 infection through screening tests and of them, 56.3% were having varied types of symptoms and 36.2% had pulmonary lesions in their CT scan. �  For the purpose of treatment, antivirals, antibiotics, anticoagulants, interferons etc. were used. �  Average treatment duration was found as significantly higher among those with pulmonary lesions though there was no significant difference in time required to return to play ground. �  The authors have cited 14 different studies as reference and have aptly mentioned that there is paucity of research in this particular field till now. �  The main strength of the research lies in exploration of a much less visited area which carries its own significance as soccer players are country representatives and their management too is challenging in regard that none could be administered with systemic glucocorticoids in order largely to adhere to anti-doping regulations. �  One limitation as mentioned by the authors as recall bias. Otherwise as nowhere it has been mentioned how many league teams are there in Russia, existence of generalizability cannot be assessed. B. Examples and Evidences: 1. Major issues (according to the progress of manuscript) �  In the introduction part, it is necessary to mention problem of the extent and rationale of the study in the backdrop of the objectives of the study. �  In the current study introduction part has been started and ended mentioning few studies in this issue which can be omitted at least at the beginning part. �  Objectives of the present study needed to mention at the last paragraph of the introduction. �  In “materials and methods” it has been mentioned that team physicians were interviewed over telephone. Whether the interview guide was structured or not, if it was validated or not to be mentioned briefly. �  In result section, page no. 7, “admission of any of the ………..with gas analysis” to be discussed very briefly as it is supportive information to build the result but it is not study finding directly. �  In the discussion part result of the current study will not be repeated. �  In reference part, if no. of authors >3, et al. to be mentioned. 2. Minor issues: �  Introductory statement of the abstract part better to describe the problem statement in brief. �  Page no. 10, “according to Russian…………competition”, the relevance of this statement to the current study is not clear. �  The 2nd limitation, “predominant virus strain………” is questionable/need clarity as a study limitation. Reviewer #3: a good article , what would be valuable ,if author add a rational why this particular group could be at higher risk or as they may have a good life style the covid -19 condition may have les serious course among this group ********** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: Yes: Pillaveetil Sathyadas Indu Reviewer #2: Yes: Dr. Satabdi Mitra, Assistant Professor, Community Medicine, KPC Medical College and Hospital, West Bengal, India Reviewer #3: Yes: Dr.Noora Alkubaisi [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. 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Submitted filename: PONE-D-21-35577_reviewer 11.pdf Click here for additional data file. 31 Jan 2022 Reviewer 1 Thank you very much for your acceptance. Reviewer 2 Reviewer #1: This is a relevant article in the context of the pandemic, because football matches and sports were suspended for many months. Methodology is sound and design is appropriate to estimate incidence. Paper has policy implications also because it highlights the need for regular screening based on the high proportion of asymptomatic cases. Answer: good point, no comments. Reviewer #2: Review summary of the article PONE-D-21-355 A. Summary of the research: 1. Major issues (according to the progress of manuscript) �  In the introduction part, it is necessary to mention the extent and rationale of the study in the backdrop of the objectives of the study. Answer: agree, we put this in the text. �  In the current study introduction part has been started and ended mentioning few studies in this issue which can be omitted at least at the beginning part. Answer: agree, Various therapeutic approaches for COVID-19 treatment are utilized, although their efficacy and safety are dubious. �  Objectives of the present study needed to mention at the last paragraph of the introduction. Answer: agree, we put this in the text. The objective of this research is to investigate the clinical course of COVID-19 infection and its impact on the performance of adult professional soccer players as one of the biggest practical importance in sports medicine at the moment. �  In the result section, page no. 7, “admission of any of the ………..with gas analysis” to be discussed very briefly as it is supportive information to build the result but it is not study finding directly. Answer: agree, we did it shorter. Admission of any of the football players to participate in competitions and regular training occurs only after passing mandatory medical examination, which should be performed twice a year. This examination includes routine physical examination, clinical blood and urine test, ECG (rest and stress-test), spirography, chest X- ray. �  In the discussion part the result of the current study will not be repeated. Answer: agree, deleted. �  In reference part, if no. of authors >3, et al. to be mentioned. Answer: agree, done. 2. Minor issues: �  Introductory statement of the abstract part better to describe the problem statement in brief. Answer: agree, we have added. �  Page no. 10, “according to Russian…………competition”, the relevance of this statement to the current study is not clear. Answer: The presence of a mandatory additional examination before admitting an athlete to physical and sports activity will allow to identify various deviations in the health status of athletes after suffering from COVID. �  The 2nd limitation, “predominant virus strain………” is questionable/need clarity as a study limitation. Answer: agree, Sure, it is not a limitation of the research. But this aspect must be taken into account when reading the article, since all the results were obtained in a specific period of time when a specific strain of the virus prevailed. Submitted filename: Point-by-point Response to Reviewers.pdf Click here for additional data file. 21 Feb 2022 The Incidence and Severity of COVID-19 in Adult Professional Soccer Players PONE-D-21-35577R1 Dear  Prof  Zbigniew Waśkiewicz , We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Dr Gopal Ashish Sharma, MBBS, MD Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #2: All comments have been addressed ********** 2. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #2: Yes ********** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #2: Yes ********** 4. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #2: Yes ********** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #2: Yes ********** 6. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #2: The article is well written and has aptly addressed a very important issue in current context. All the issues identified have been discussed and modified appropriately. Writing style is also very good. ********** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #2: Yes: Dr Satabdi Mitra 27 May 2022 PONE-D-21-35577R1 The Incidence and Severity of COVID-19 in Adult Professional Soccer Players in Russia Dear Dr. Waśkiewicz: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. If we can help with anything else, please email us at plosone@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Gopal Ashish Sharma Academic Editor PLOS ONE
  11 in total

1.  Football cannot restart soon during the COVID-19 emergency! A critical perspective from the Italian experience and a call for action.

Authors:  Alessandro Corsini; Gian Nicola Bisciotti; Cristiano Eirale; Piero Volpi
Journal:  Br J Sports Med       Date:  2020-03-24       Impact factor: 13.800

2.  Cardiovascular Magnetic Resonance Findings in Competitive Athletes Recovering From COVID-19 Infection.

Authors:  Saurabh Rajpal; Matthew S Tong; James Borchers; Karolina M Zareba; Timothy P Obarski; Orlando P Simonetti; Curt J Daniels
Journal:  JAMA Cardiol       Date:  2021-01-01       Impact factor: 14.676

3.  The prevalence of symptoms in 24,410 adults infected by the novel coronavirus (SARS-CoV-2; COVID-19): A systematic review and meta-analysis of 148 studies from 9 countries.

Authors:  Michael C Grant; Luke Geoghegan; Marc Arbyn; Zakaria Mohammed; Luke McGuinness; Emily L Clarke; Ryckie G Wade
Journal:  PLoS One       Date:  2020-06-23       Impact factor: 3.240

4.  Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study.

Authors:  Nanshan Chen; Min Zhou; Xuan Dong; Jieming Qu; Fengyun Gong; Yang Han; Yang Qiu; Jingli Wang; Ying Liu; Yuan Wei; Jia'an Xia; Ting Yu; Xinxin Zhang; Li Zhang
Journal:  Lancet       Date:  2020-01-30       Impact factor: 79.321

5.  COVID-19 and the cardiovascular system: implications for risk assessment, diagnosis, and treatment options.

Authors:  Tomasz J Guzik; Saidi A Mohiddin; Anthony Dimarco; Vimal Patel; Kostas Savvatis; Federica M Marelli-Berg; Meena S Madhur; Maciej Tomaszewski; Pasquale Maffia; Fulvio D'Acquisto; Stuart A Nicklin; Ali J Marian; Ryszard Nosalski; Eleanor C Murray; Bartlomiej Guzik; Colin Berry; Rhian M Touyz; Reinhold Kreutz; Dao Wen Wang; David Bhella; Orlando Sagliocco; Filippo Crea; Emma C Thomson; Iain B McInnes
Journal:  Cardiovasc Res       Date:  2020-08-01       Impact factor: 10.787

6.  Resuming professional football (soccer) during the COVID-19 pandemic in a country with high infection rates: a prospective cohort study.

Authors:  Karim Chamari; Roald Bahr; Yorck Olaf Schumacher; Montassar Tabben; Khalid Hassoun; Asmaa Al Marwani; Ibrahim Al Hussein; Peter Coyle; Ahmed Khellil Abbassi; Hani Taleb Ballan; Abdulaziz Al-Kuwari
Journal:  Br J Sports Med       Date:  2021-02-15       Impact factor: 13.800

7.  Reopening elite sport during the COVID-19 pandemic: Experiences from a controlled return to elite football in Denmark.

Authors:  Lars Pedersen; Jens Lindberg; Rune Rasmussen Lind; Hanne Rasmusen
Journal:  Scand J Med Sci Sports       Date:  2021-01-21       Impact factor: 4.221

Review 8.  Emerging pharmacotherapies for COVID-19.

Authors:  Rachana Salvi; Panini Patankar
Journal:  Biomed Pharmacother       Date:  2020-05-14       Impact factor: 6.529

Review 9.  Cardiorespiratory considerations for return-to-play in elite athletes after COVID-19 infection: a practical guide for sport and exercise medicine physicians.

Authors:  Mathew G Wilson; James H Hull; John Rogers; Noel Pollock; Miranda Dodd; Jemma Haines; Sally Harris; Mike Loosemore; Aneil Malhotra; Guido Pieles; Anand Shah; Lesley Taylor; Aashish Vyas; Fares S Haddad; Sanjay Sharma
Journal:  Br J Sports Med       Date:  2020-09-02       Impact factor: 13.800

10.  Successful return to professional men's football (soccer) competition after the COVID-19 shutdown: a cohort study in the German Bundesliga.

Authors:  Tim Meyer; Dietrich Mack; Katrin Donde; Oliver Harzer; Werner Krutsch; Annika Rössler; Janine Kimpel; Dorothee von Laer; Barbara C Gärtner
Journal:  Br J Sports Med       Date:  2020-09-24       Impact factor: 13.800

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