Abstract
The coronavirus disease 2019 (COVID-19) can lead to serious health conditions thus vaccination is crucial, especially for elite athletes to avoid severe/prolonged symptoms after the coronavirus infection, which can significantly influence their sports performance. Yet, only a few studies examined immunization reactions after vaccination in elite athletes, and none in young athletes. Thus, we aimed to examine the prevalence and severity of any reactions after the Pfizer-BioNTech COVID-19 vaccine in young elite athletes. Local and systemic reactions were assessed two to three days after first vaccination in adolescent elite athletes. 15 different reactions, more local than systemic reactions, were reported. The most prevalent local reaction was injection site pain, and nearly 20% of the adolescents reported severe pain. In the case of systemic reactions, half of the adolescents reported mild/moderate fatigue, and one-third experienced mild/moderate muscle pain and/or headache. The most prevalent co-occurrence was between injection site pain, pain in extremity, fatigue and muscle pain. Young elite athletes tended to feel more pain and sensation, partly due to the fact that the systemic circulation of their skeletal muscle allows an advanced spread of the vaccine, causing stronger immune reactions. The network of the reported reactions may provide a clue for understanding the connections of local and systemic reactions. These findings show that the profile of post-vaccine reactions in young elite athletes can differ from that of the general population, which could be important for the timing of vaccination, the planning of pre/post-vaccination protocol, and for returning to normal training intensity.
Introduction
The coronavirus disease 2019 (COVID-19) pandemic is an ongoing global pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The outbreak of the coronavirus pandemic at the end of 2019 called for the rapid development of a new type of vaccine (Pfizer/BioNTech [BNT162b2] COVID-19 vaccine, P/B) based on mRNA packed in a PEGylated liposomes [1]. It was introduced as an emergency use authorization due to the rapid development of the pandemic and thus the traditional approval process could not be followed [2, 3]. Therefore, its efficacy and normal or adverse reactions had not been completely assessed among a wide range of populations.
In Hungary, community transmission of SARS-CoV-2 was first documented in March 2020, yet the first wave of the COVID-19 epidemic was suppressed very rapidly due to an effective government response [4, 5]. Subsequent waves of the COVID-19 epidemic in Hungary were more severe in terms of both morbidity and mortality [6]. The Hungarian vaccination campaign was started in 2021 with five different vaccines, including the BNT162b2 (Pfizer/BioNTech) COVID-19 vaccine, during the third wave of the COVID-19 pandemic. Initially, the older adults at risk for increased mortality were immunized [7]. Later, the protection of younger age groups also became important to reduce viral circulation in the overall population. The risk of infection in closed communities of young people, such as in team sports communities, increased significantly, so vaccinating them quickly became a priority. The preauthorization trials of the P/B vaccine demonstrated its efficacy and favourable safety profile in teens aged 12 to 17 as well [7, 8].
Previous studies had shown that there are immunization reactions to various vaccines such as chickenpox virus, influenza virus, tuberculosis, etc., thus one can assume that this might be the case with COVID-19 vaccines, as well. It is important to note that most of these reactions or “adverse” events can be the normal signs of the immune system building up protection. The most common symptoms of vaccine reactions are local reactions such as pain, redness and swelling at the injection site. Occasionally, there is an injection-site nodule which may last for many weeks, but no treatment is needed [9]. Furthermore, there are also systemic reactions, such as low-grade fever, tiredness, mild headache, muscle pain and nausea, which start within 24 h of the shot and last for a few days.
In the case of the Pfizer/BioNTech COVID-19 vaccine, one per 1,000 vaccinated adolescents reported adverse events during the study period of December 14, 2020 to July 16, 2021, based on the Vaccine Adverse Event Reporting System [10]. Of these, “90.7% were for non-serious adverse events and 9.3% were for serious adverse events including myocarditis”18 and anaphylaxis [11–14]. The incidence of post-vaccine myocarditis is low, estimated 0.3–5.0 cases per 100,000 vaccinated individuals. The clinical presentation was generally mild with a complete recovery [15–18]. Although myocarditis is a rare adverse event after mRNA vaccination, it has a crucial impact on athletic individuals in their safe return to sports participation [19]. Similarly to the findings of the Phase 3 clinical trial [8]; the most common non-serious adverse events were dizziness, syncope, nausea, headache, and fever.
Vaccination as a method of prevention is always a crucial point in the healthcare of elite athletes because of their global travelling and mass congregation, which increase the risk of viral transfer. The effects of any infection and vaccination can be more serious for an athlete than for the average population, and even mild adverse events and brief interruptions to training also influence their sports performance [20]. The risk and severity of any adverse after vaccination events can be reduced by the appropriate vaccine and vaccination technique as well as the timing of vaccination [21].
Until now, only a few studies have examined the adverse reactions after COVID-19 vaccination in elite athletes, none in young athletes. Hull, Wootten & Ranson [22, 23] followed 127 Olympic and Paralympic sports athletes (mean age 27.5 years, SD = 4.9) for 10 days after the Pfizer-BioNTech vaccination. The elite athletes reported few significant adverse reactions with only minor if any effects on training and sports participation. Batatinha et al. [24] reported minimal effects of COVID-19 vaccination on the metabolic and physiological responses to various intensities of exercise in physically active healthy people (mean age 29 years, SD = 5.4).
The COVID-19 vaccination is crucial for elite athletes. The SARS-CoV-2 infection and prolonged symptoms after the infection can significantly delay the return to sports activities. Around one in four elite athletes were not fully able to return to sport a month after the onset of infection [22, 23]. Yet, few if any studies investigated the COVID-19 vaccination in young elite athletes. Although it can be assumed that in the population of athletes reactogenicity is the same as in the general population, young elite athletes can have different side-effects profiles. Thus, we aimed to examine the prevalence and severity of any reactions after the first Pfizer-BioNTech vaccine in young elite athletes, whose intense cardiac workloads can be a risk factor.
Materials and methods
Study sample and procedure
The present study involved adolescent soccer players of the Hungarian Puskás Akadémia Football Club (PAFC, N = 39). Training load was 10–13 h of training per week and one match on weekends. All participants received the first dose Pfizer-BioNTech COVID-19 vaccine (Comirnaty) in their upper arm between July and September, 2022. There was no training session on the day of the vaccination, and the vaccination was timed so that there would be no matches in the following four days. If there was any symptom after vaccination, training was not allowed until full recovery. Local and systemic reactions were assessed two to three days after the vaccination.
Post-vaccine reactions
For assessing post-vaccine reactions, we used a self-completed questionnaire including the most frequently reported reactions in vaccine clinical trials [8, 25, 26]. The athletes had the option to report any further reactions. The athletes indicated the presence and severity of the reactions.
Local reactions included injection site pain, pain in extremity (arm), injection site redness, injection site swelling, and swollen lymph nodes. Systemic reactions included fatigue, muscle pain, headache, chills, joint pain, malaise, nausea, abdominal discomfort, vomiting, fever, diarrhoea and rash, itching, urticaria.
The severity of reactions was measured on a 0 to 4 scale, where 0: no reaction, 1: mild reaction (does not interfere with activity), 2: moderate reaction (some interference with activity), 3: severe reaction (prevents daily activity), and Grade 4: emergency room visit or hospitalization for any reaction [27].
Statistical analysis
To describe the data, descriptive analysis and the distribution of relative frequencies were used. Data were presented as mean ± SD or frequency and proportion. Gender differences were tested by robust independent samples t-tests with Hedges' g effect size. The level of significance was set a priori at 0.05. Statistical analysis and visualization were conducted using IBM SPSS Statistics for Windows, Version 25.0 (IBM Corp. Released 2017. Armonk, NY: IBM Corp) and jamovi (Version 2.2.2, The jamovi project 2021., retrieved from https://www.jamovi.org), as well as the qgraph package (version 1.6.9.) in R [28].
Results
A total of 39 adolescent soccer players participated in the present study. The majority of players were adolescent boys (87.2%, n = 34), with a mean age of 14.4 (SD = 1.3, min–max = 12–17), while the girls (12.8%, n = 5) were on the mean age of 15.0 (SD = 0.7, min–max = 14–16).
Local and systemic post-vaccine reactions
The adolescent athletes reported 15 different reactions. They experienced a mean of four reactions (SD = 3.2, min–max = 0–13) simultaneously (Fig. 1A). Six athletes reported no reactions (one girl and five boys). There was no statistically significant gender difference in the number of the reported reactions (t(37) = 1.728, P = 0.119, g = 0.54), but boys reported relatively more reactions (M = 4.1, SD = 3.3) than girls (M = 2.4, SD = 1.8).
Frequency distribution of the number of reported post-vaccine reactions in adolescent athletes, (A) local reactions; (B) systemic reactions; (C) total of reactions
Notes. Violin plots with density curves and box plots. The horizontal line is the median of the number of reactions. Individual data points are represented by jittered points.
Citation: SPRINT – Sports Research International 1, 1; 10.1556/1020.2023.10001
In sum, nearly half of the reported reactions were local (54.3%) and half were systemic (45.7%). Girls reported relatively fewer systemic (35.4%) and more local reactions (64.6%) than boys (systemic: 47.1%, local: 52.9%).
The prevalence of the five local reactions was 37.6 ± 18.5% (mean 1.9 of five reactions, SD = 0.9), whereas the prevalence of the ten systemic reactions was 27.3 ± 24.1% (mean 2.7 of ten reactions, SD = 2.4) (Fig. 1B and C). No gender difference was found in the prevalence of local reactions (t(31) = 0.288, P = 0.788, g = 0.15; girls: 35 ± 19.1%, boys: 37.9 ± 18.8%), whereas there was a gender difference in the prevalence of systemic reactions: boys showed a higher prevalence (29.3 ± 24.9%) than girls (12.5 ± 9.6%) (t(31) = 2.525, P = 0.030, g = 0.70).
Local post-vaccine reactions – prevalence, severity and co-occurrence
Of the five local reactions, namely, injection site pain, pain in extremity, injection site redness, injection site swelling and swollen lymph nodes, the most prevalent was the injection site pain (82.1%, n = 32). One-third of the adolescent athletes rated this pain to be mild/moderate and nearly 20% reported severe pain. The second most prevalent reaction experienced by nearly 40% of the adolescents (41%, n = 16) was the pain in extremity; most adolescents showed mild pain. In most cases, the injection site pain and swelling, as well as pain in the extremity occurred at the same time (Fig. 2). No Grade 4 local reactions were reported. In sum, the severity of the local reactions (M = 1.6, SD = 0.6) showed a gender difference (t(31) = 2.869, P = 0.016, g = 0.87). Boys rated local reactions with a higher level of severity (M = 1.7, SD = 0.6) than girls (M = 1.2, SD = 0.2).
Prevalence, severity and co-occurrence of local post-vaccine reactions in anatomical order
Citation: SPRINT – Sports Research International 1, 1; 10.1556/1020.2023.10001
Systemic post-vaccine reactions – prevalence, severity and co-occurrence
Of the ten systemic reactions, namely, fatigue, muscle pain, headache, chills, joint pain, malaise, nausea, abdominal discomfort, fever and diarrhoea, more than half of the adolescents (53.8%, n = 21) reported mild/moderate fatigue. Muscle pain (43.6%, n = 17) and headache (30.8%, n = 12) were also prevalent with mild/moderate severity. Girls reported fewer systemic reactions than boys; girls experienced “only” fatigue, headache and muscle pain. In most cases, fatigue, muscle pain, headache and chills occurred at the same time (Fig. 3). No Grade 4 systemic reactions were reported. In sum, the severity of the systemic reactions (M = 1.3, SD = 0.4) showed non-significant gender difference (t(17) = 0.834, P = 0.453, g = 0.26). Boys rated the severity of the systemic reactions at a mean of 1.3 (SD = 0.4), and girls rated it at a mean of 1.2 (SD = 0.3).
Prevalence, severity and co-occurrence of systemic post-vaccine reactions in spreading order
Citation: SPRINT – Sports Research International 1, 1; 10.1556/1020.2023.10001
Network of the co-occurrence among post-vaccine reactions
Examining the co-occurrence among post-vaccine reactions, of the reported 15 reactions, two local and five systemic reactions occurred at the same time with a prevalence above 10% (Fig. 4). The most prevalent co-occurrence was found between injection site pain, pain in extremity, fatigue and muscle pain.
The figure illustrates a network of local and systemic reactions reported by adolescent football players. The width and the colour of the lines indicate the frequency of co-occurrence (≥15 in red, ≥10 in blue, <10 in green)
Citation: SPRINT – Sports Research International 1, 1; 10.1556/1020.2023.10001
Discussion
In line with the results of previous studies on the younger population [4, 8, 25, 26]. we found that adolescent athletes also reported more local reactions than systemic ones after the first dose of Pfizer-BioNTech COVID-19 vaccine. At the same time, the levels of severity of injection site pain and pain in extremity were more severe compared to the reported severity in the general adolescent population. Furthermore, examining systemic reactions, fatigue and headache were more prevalent and more severe in adolescent athletes than in the general adolescent population. It is of note that there were some subtle different reactions after the first vaccination in female versus male athletes, which warrants further investigations.
The effects of exercise before and after the first vaccination are controversial with all vaccines, not only with the COVID-19 vaccines. Several studies have reported an increased antibody response to vaccination when exercise was performed near the time of immunization [29, 30] but some studies found no benefit of exercise [31, 32] or only in special populations, such as active people [33]. Exercise performed after vaccination is still in question. Hallam et al. [34] showed an increased antibody response after the first dose of the Pfizer-BioNTech vaccine without an increase in adverse events, when light-to-moderate intensity exercise was performed after vaccination. At the same time, it is generally recommended to avoid strenuous exercise 48 h post-vaccination [35], particularly for adolescents and younger persons. For athletes, a temporary reduction in training load in the first 48–72 h post-vaccine injection is recommended, particularly after the second dose [36].
The present study was designed to assess the immunization reactions in elite athletes. The reactions were classified as local and systemic (remote) according to anatomical locations. As the figures show, primarily local reactions were observed, but there were a few systemic changes as well. The subjective component cannot be completely excluded, however. It is of note that these young athletes tended to feel more pain and sensation, partly due to the fact that the systemic circulation of their skeletal muscle allows an advanced spread of the vaccine, causing stronger immune reactions. The network of the reported reactions may provide a clue for understanding the underlying mechanisms regarding the connections of local and systemic reactions (Fig. 4). Developing such networks may help to reveal a consequential relationship in a larger cohort and design vaccination time and mode in age, race and gender-specific manner.
An important finding of the present study is that we did not observe myocarditis, a rare adverse event, which has been observed after vaccination with mRNA vaccines in post-authorization monitoring, with the highest risk after the second dose, particularly in adolescents and young men [37–40]. This finding would help to promote the encouragement, adherence, and compliance of young athletes to vaccinations.
Strengths and limitations
The number of participants was not high enough (especially for girls) to be able to draw generalized conclusions. However, this group of athletes was homogeneous in their age and the intensity of training. In addition, the relatively low number of major reactions could be since the study was conducted after the first dose of vaccination. The reason for this was to exclude those who experience major adverse effects from the second vaccination, as it has been shown that after the second jab more serious reactions can occur in the adolescent population [15, 17, 26]. Another limitation is the lack of reliable information about the COVID-19 infection prior the vaccination. It is of note that this study was performed in healthy young athletes; thus, our findings cannot be directly translated to older healthy populations or to people with cardiovascular diseases, where more serious reactions can occur [41].
Conclusions
The results of the present study support the notion that young athletes (females and males), can be safely immunized against COVID-19 with the Pfizer/BioNTech vaccine. Nevertheless, it is important that in young athletes not only the efficacy of vaccines need to be known, but also the profile of reactions, which can differ from those of the general population. In the case of the Pfizer/BioNTech COVID-19 vaccine, knowing the immunization reactions profile of elite athletes, which could vary in different types of sport, could be crucial for the timing and mode of vaccination, for the planning of pre- and post-vaccination protocol, as well as for the return to normal training intensity.
Author contributions
Conceptualization, A.K.; methodology. A.K and J.T.; analysis, J.T.; writing—original draft preparation, J.T. and A.K; writing—review and editing, A.K.; visualization, J.T.; supervision, A.K. All authors have read and agreed to the published version of the manuscript.
Funding
Ministry for Innovation and Technology, Hungary, National Research, Development and Innovation Fund (NRDI) TKP2020-NKA-17, TKP2021-EGA-37, OTKA K 132596, (A.K.) Hungarian Academy of Sciences Post-Covid 2021-34. (A.K. and J.T.) NRDI, ÚNKP-22-4, New National Excellence Program (J.T.)
Institutional review board statement
The study was conducted in accordance with the Declaration of Helsinki and approved by the Ferenc Puskás Football Academy. This research was approved by the Ethical Committee of the Medical Research Council (TUKEB), Hungary, under Semmelweis University Regional and Institutional Committee of Science and Research ethics, ethical permission No. SE RKEB 118/2022.
Informed consent statement
Informed consent was obtained from all subjects involved in the study.
Data availability statement
The data presented in this study are available on request from the corresponding author.
Conflicts of interest
The authors declare no conflict of interest.
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