International Olympic Committee (IOC) consensus statement on ... - British Journal of Sports Medicine
Key points
Acute illnesses account for up to ~50% of all medical consultations at major sporting events, with ~50% of all acute illnesses involving the respiratory system.
Acute respiratory infections (ARinf) account for most of the acute respiratory illnesses in athletes and are caused primarily by viruses.
ARinf involve predominantly the upper airways and two clinical syndromes (ie, acute viral rhinitis/rhinosinusitis with or without systemic symptoms) are responsible for most ARinf in athletes.
Sport and Exercise Medicine clinicians can implement a practical clinical approach to the diagnosis, management, return-to-sport decision making and prevention of ARinf in athletes.
Introduction
The International Olympic Committee (IOC) Medical and Scientific Commission identified 'protection of the health of athletes' as an important focus involving prevention,1 management and safe return to sport (RTS) after acute illness in athletes. Management and prevention of acute illness in athletes forms a significant component of the work of Sport and Exercise Medicine (SEM) clinicians at international single-sport2–9 and multisport events such as the Olympics,10–14 Paralympic Games15–17 and Youth Olympics.18 19 Approximately 50% of all medical consultations at these events relate to acute illness in athletes, with the respiratory system consistently the most common organ system affected.4 7 8 11 12 20 21 Acute respiratory illness (ARill) can occur as a result of multiple causes, which can be broadly classified as non-infective or infective. In most studies to date,22 acute respiratory infections (ARinf) in athletes were diagnosed by history and clinical assessment without laboratory confirmation of an infection, or identification of a specific pathogen and are 'suspected' ARinf.4 7 8 10 12
The aim of this consensus statement is to provide the SEM clinician with an overview and practical clinical approach to ARinf in athletes. This document forms part 1 of a three-part series, with part 2 focusing on non-infective ARill in athletes23 and part 3 on SARS-CoV-2 infection in athletes.24 The specific focus of part 1 is to review clinically relevant aspects of ARinf in athletes. The first section of this manuscript proposes a set of definitions and classifications of ARinf in athletes to standardise future data collection and reporting. The remainder of this IOC consensus examines a wide range of clinical considerations related to ARinf in athletes: epidemiology, risk factors, pathology/pathophysiology, clinical presentation and diagnosis, management, prevention, medical considerations and risks of illness during exercise, effects of illness on exercise/sports performance and RTS decisions.
The work of this consensus group started in September 2019, before the COVID-19 pandemic. As the pandemic emerged in 2020, the work of IOC consensus group was expanded with the formation of subgroup 7, which was tasked to focus on SARS-CoV-2 infection in the athlete. The focus of this part 1 of the consensus was on all ARinf in athletes, but as new data on SARS-CoV-2 infection in athletes emerged from March 2020, several research findings that are generally applicable to ARinf were identified, and these are included in this part 1 consensus. As indicated, the specific work of subgroup 7 forms a separate IOC consensus on SARS-CoV-2 infection in athletes (part 3).
Methods
The process to generate this consensus statement involved several steps: (1) to identify SEM experts in the field, nomination forms (detailing key publications in the field, clinical experience and professional motivations) were widely distributed by the IOC Medical Commission and Scientific Department to all contacts in the IOC Research Centres for Prevention of Injury and Protection of Athlete Health, National Olympic Committee medical staff in past Olympic Games, and participants of past meetings and conferences such as the IOC World Conference on Prevention of Injury and Illness in Sport and IOC advanced team physician courses; (2) nominations were considered, and members then invited as either 'core' or 'corresponding' members ('core' members coordinated the preparation of specific consensus sections and 'core' and 'corresponding' members were involved with reviewing literature, collating data and conducting systematic and narrative reviews in six focus areas), the final 'core' group included representation from a former Olympic athlete (CM); (3) various areas of ARill were originally identified including ARinf and non-infective ARill such as acute asthma and related conditions, causes of nasal obstruction, and acute nasal/vocal cord dysfunction presenting as ARill; (4) each subgroup held online meetings to discuss broad content and formulate a systematic (with or without meta-analyses) or narrative review(s), and data from these reviews were incorporated into the main consensus documents; (5) the draft sections of the consensus documents were allocated to 'core' members. Initial draft sections of the consensus statements were reviewed internally before further discussion and finalisation of the consensus document at a meeting conducted in Lausanne, Switzerland on 11 to 12 October 2021. Final edits were completed in a 3-month period after the meeting, prior to submission of the manuscript.
Terminology, definitions and classification of ARinf in athletes
ARill in athletes, and specifically ARinf, can be categorised based on an anatomical and pathological classification. For the purposes of this consensus document, terminology and anatomical/pathological classifications of ARill and ARinf were agreed on by the consensus group early in the process and finalised after an online meeting in January 2021. Non-infective ARill was defined as an illness not caused by infection from a specific pathogen, by clinical diagnosis or laboratory investigation(s). There are several conditions that cause non-infective ARill and these are comprehensively reviewed in part 2 of the IOC Consensus statement on ARill in athletes.23
Anatomical classification of ARinf in athletes
Due to the structural and functional connection between upper and lower airways, there is a pathological continuum in many conditions causing ARill including allergy, asthma, infection and other inflammatory conditions related to pollution and chemical exposure.25 26 However, the terms 'upper' or 'lower' respiratory tract disease are still used commonly when referring to both non-infective and infective causes of ARill. In this context, 'upper' ARinf refers to symptoms, signs, and pathological features of infective conditions above and including the larynx (nose, sinuses, pharynx, larynx), while 'lower' ARinf refers to symptoms, signs, and pathological features of infective conditions below the level of the larynx (trachea, bronchi, lungs and pleura). The consensus group adopted use of the term 'predominantly' for upper or lower ARinf, based on the main clinical (cluster of upper or lower symptoms, signs) or pathological features involving the 'upper' or 'lower' airways.
Pathological classification of ARinf in athletes
Historically, in many studies reporting on ARill in athletes,22 the pathology could not be attributed specifically to an infection or a non-infective cause, and/or these details were not specified explicitly in the study design or methods section. When analysing data from these studies, the consensus group defined the ARill as an 'undiagnosed' ARill. In studies where an infection was reported, the infection was often not confirmed and/or the specific viral, bacteriological, or other pathogens causing the infection were not identified. In these cases, the consensus group classified the ARinf as 'suspected' rather than 'confirmed'. For the purposes of this consensus statement, the following broad classification, and methods to diagnose ARinf used in studies to date, were agreed on and applied for this document (table 1). This table, featuring the methods to diagnose and classify ARinf, is adapted from two systematic reviews conducted by specific subgroups.22 27
Classification and methods to diagnose acute respiratory infection (ARinf) in athletes (adapted from Derman et al 22)
A 'suspected' ARinf was defined as ARill presenting with general symptoms and/or physical signs suggestive of an ARinf, but where the specific pathogen causing an infection was not confirmed by laboratory testing. In published studies of ARinf in athletes, the following methods were used to classify 'suspected' ARinf: (1) self-reported symptoms, coupled with an algorithm that was validated for the diagnosis of ARinf. The validated questionnaires included the Wisconsin Upper Respiratory Symptom Survey-21,28 the Jackson Cold Scale,29 or other questionnaires where the severity of the symptoms was scored to provide a quantitative assessment,30 31 (2) a review of self-reported symptoms of an ARinf by a physician, but without clinical or laboratory evaluation, or (3) clinical diagnosis of an ARinf by a physician, based on history and clinical examination.
A 'confirmed' ARinf was defined as an ARinf diagnosed by a physician with laboratory evidence confirming an infection. A 'confirmed' ARinf could then be further classified as either: (1) a confirmed ARinf but where the specific pathogen was not identified or (2) a confirmed ARinf where a specific pathogen (predominantly viral and less commonly bacterial) was identified by polymerase chain reaction (PCR) testing on specimens, culture of an organism from specimens, or serology (eg, rise in antibody titres) (table 1).
Pathology and pathophysiology of ARinf in athletes
Pathogens causing ARinf
ARinfs are mostly caused by different viruses, occasionally by bacteria, and rarely by other pathogens (eg, fungal).32 In the general population, a viral aetiology accounts for >80% of all upper ARinf.33–35 At least 10 different respiratory viruses species with hundreds of subtypes cause most ARinf in the general population (table 2), but there are many subtypes and serotypes.34 Clinically non-significant bacterial colonisation can also be combined with viral pathogen identification, as has been shown in 5% to 10% of adults with upper ARinf.35
More common pathogens (viral, bacterial) causing acute respiratory infection in the general population32 34
The specific pathogens causing ARinf in athletes have not been studied extensively, but the same pathogens cause ARinf in athletes as in the general adult population. Prior to the COVID-19 pandemic, rhinoviruses, non-SARS coronaviruses, influenza viruses and RS-viruses were identified as the most frequent pathogens causing ARinf in athletes, but only in a few studies.36–41 Since December 2019, the predominant pathogen causing ARinf in the general population was the novel coronavirus, SARS-CoV-2.
As in the general population, pathogens cannot be detected in all athletes presenting with symptoms of ARinf. Early studies conducted in Australia36 38 reported viral aetiology in one-third of athletes with symptoms of respiratory infection. In contrast, more recent studies from Finland showed a higher detection rate of viral causes (77%) in athletes with symptoms of ARinf.39 40 This higher detection rate, which is similar to reports in the general adult population, may be explained by several factors including: expected viral epidemics of winter season, winter sport disciplines, and methodological variations. In more recent studies four different multiplex PCR panels were used to identify pathogens.32 42 43 These studies indicate that athletes presenting with mild symptoms of respiratory infection are likely to have a viral aetiology. However, more prospective studies in larger athlete populations with a longer surveillance and follow-up time are needed. Bacterial causes of ARinf in athletes are described but are uncommon.44 As in the general population, the cause of ARinf in athletes has also been dominated by SARS-CoV-2 infection since December 2019.45–49
Pathophysiology of ARinf
Respiratory pathogens circulate commonly in all age groups by an efficient person-to-person transmission. The transmission pathways are dependent on the pathogen and include aerosol, droplet, as well as direct or indirect contact transmission.50 A detailed discussion of the pathophysiology of respiratory tract infection by viral and bacterial pathogens is beyond the scope of this consensus, and has been reviewed elsewhere.51 52 In general, on entry of the respiratory tract, viruses invade the respiratory epithelium, gain entry to the cells, elicit an inflammatory response, replicate, cause cellular death, and subsequently shed and transmit via respiratory secretions.51 53 Bacteria, such as those causing acute pharyngitis, attach to and, in the case of group A beta-haemolytic streptococcus, invade the mucosa of the respiratory tract, elicit an inflammatory response, cause cell death and may form an adherent exudate.51
The pathophysiological mechanisms responsible for the common general symptoms of ARinf are related to a non-specific acute phase response, as well as local tissue injury by the pathogen. In the early stages of the infection, the non-specific acute phase response results in the systemic release of several cytokines, which collectively are an important component of the host defence mechanism.52 Acute phase reactants (APR) are a heterogeneous group of plasma proteins that increase or decrease in concentration in response to inflammatory stimuli, including acute infection. APR such as C reactive protein (CRP) and procalcitonin (PCT) can be measured in the laboratory and are useful markers of inflammation associated with ARinf. Their response is proportional to the severity of the inflammatory stimulus of the ARinf.54 In most ARinf, inflammatory mediators such as prostaglandin and bradykinin are responsible for local symptoms (rhinorrhoea and nasal congestion), while cytokines are responsible for systemic symptoms (fever, chills, headache, myalgia).52 The clinical relevance of the acute phase response is that symptoms of ARinf caused by acute phase inflammatory mediators are non-specific and common to infections caused by different pathogens. As a result, symptoms of ARinf are generally non-specific and cannot be used to diagnose the underlying pathogen causing an ARinf. However, these symptoms (type, duration and severity) are related to the magnitude of the inflammatory response and can indicate the severity of the ARinf.54
Incubation period and infectiousness are two pathophysiological features of ARinf that have specific clinical relevance to the SEM clinician. The incubation period (defined as the time from pathogen exposure to onset of signs and symptoms) is pathogen-dependent, and varies from 1 to 14 days (eg, rhinovirus=1–3 days; adenovirus=7–13 days and SARS-CoV-2=2–14 days).33 55 56 Knowledge of the incubation period is important for the SEM clinician because it informs clinical decision making when controlling viral epidemics within teams.39 40
Until recently, viral shedding time was used to determine the duration of infectiousness, but this concept is changing due to the increased knowledge of SARS-CoV-2. Shedding time of respiratory viruses can range from a few days up to weeks, but the time of infectiousness during the detection of viral agent is often not known.57 The risk of viral transmission is highest during the first 3–4 days of the infection and in the case of SARS-CoV-2, up to 48 hours before the onset of symptoms. Infectiousness is an important determinant in decision making on the duration of quarantining infected athletes, and when an athlete can return to team practice, locker rooms and shared transportation.
Potential complications in other organ/organ systems, other than the upper respiratory tract, that can be associated with an ARinf
Although the majority of ARinf only result in pathology within the upper respiratory tract, there are potential regional systemic and complications in other organs/organ systems caused by respiratory viral pathogens causing ARinf (online supplemental table S1). The risk and type of complications vary according to the host and the pathogen.
Supplemental material
A systematic review of potential multiorgan complications of ARinf in athletes was commissioned and then undertaken by a subgroup of the IOC Consensus group. This review identified too few studies to analyse, therefore, data in this area are currently very limited. Although apparently very rare, particularly in younger populations, potential complications are of clinical relevance to athletes with ARinf because they can indicate more extensive or severe disease. This aspect was highlighted by studies during the recent COVID-19 pandemic indicating that, for example, reported cardiovascular complications such as myocarditis/pericarditis that can occur in athletes with SARS-CoV-2 infection. Initial studies, with small sample sizes in selected athletic cohorts, showed a high prevalence of myocarditis/pericarditis after SARS-CoV-2 infection,58 59 but in several larger studies this complication was found to be rare (<3% or less).60–62 Thus, although potential complications of ARinf affecting multiple organ systems are rare, the SEM clinician should consider these complications as they may predispose athletes to an increased risk of adverse medical events during return to full training and competition.
Incidence of ARinf in athletes
A systematic review and meta-analysis undertaken by a subgroup of the IOC Consensus group determined the incidence per 1000 athlete days of ARill, and specifically ARinf, in athletes.22 This review included subanalyses based on the anatomical and pathological classification of ARill, and specifically ARinf in athletes. Data included athletes at any level of performance (elite/non-elite), aged 15–65 years. Analysis was done from data in 124 original research articles (n=128 360 athletes) published between January 1990 and July 2020.
Incidence of ARinf in athletes
The incidence of ARinf by pathological and anatomical classification and by method of diagnosis is summarised in figure 1.
The incidence (per 1000 athlete days; 95% CIs) of acute respiratory infection (ARinf) by pathological and anatomical classification and by method of diagnosis (adapted from Derman et al 22).
The overall pooled incidence of all ARinf (both suspected and confirmed) in athletes was 4.9 per 1000 athlete days,22 and the incidence was twofold higher for predominantly upper ARinf (5.9 per 1000 athlete days) versus general (defined as combined upper and lower ARinf) ARinf (2.8 per 1000 athlete days). There was a higher incidence of ARinf in athletes with confirmed ARinf (pathogen identification) compared with all other categories of suspected ARinf. Studies in athletes with confirmed ARinf (pathogen identification)39 40 were conducted in a selected cohort of elite athletes during international winter sport competition and used a different more sensitive definition of ARinf (any symptom or viral pathogen that was detected). Although the incidence of ARinf was higher in these studies, there were wide 95% CIs, and this estimate was not significantly different from the incidence of ARinf in other studies.22 A higher incidence of ARinf in non-elite athletes (8.7 per 1000 athlete days) compared with elite athletes (4.2 per 1000 athlete days) was reported in the recent review. However, in a winter sport team setting, a seven-fold higher incidence of ARinf was evident in a group of elite athletes compared with age-matched controls exercising less than 6 hours per week and a control group of non-athletes.39 The study was conducted during a winter viral epidemic where athletes were asked to report even mild respiratory symptoms, which may explain the difference in findings.
Clinical point/s: How common are acute respiratory infections (ARinf) in athletes?
The general incidence of ARinf in athletes equates to ~1.8 ARinf per athlete per year (in comparison to ~2.3 in the general population).
There is a high incidence of predominantly upper ARinf.
Elite athletes have a lower incidence of ARinf than non-elite athletes.
The incidence of suspected ARinf is similar across methods of diagnosis, indicating that Sport and Exercise Medicine clinicians can confidently use validated questionnaires and checklists to screen athletes for suspected ARinf.
There appears to be a higher incidence of confirmed ARinf with pathogen identification compared with suspected ARinf, but this outcome requires confirmation in future studies with larger cohorts.
Risk factors associated with ARinf in athletes
A comprehensive review of the risk factors and biomarkers for both suspected and confirmed ARinf (n=24 studies) has been published by an IOC consensus subgroup.63 This review included 48 studies (19 390 athletes) and the majority (71%) of studies were self-reported ARill in athletes. Sub-analyses included the pathological classification of ARinf and methods used to diagnose suspected ARinf. A summary of risk factors with a strong positive association to a high incidence of confirmed ARinf or suspected ARinf is presented below.
Clinical point/s: What are the risk factors associated with acute respiratory infections (ARinf) in athletes? (strong positive associations)
Endurance sports versus other sports.
Winter vs other seasons.
Training variables (high intensity training, increased training load, training monotony, lack of tapering).
Training at altitude.
Competition periods.
Travel (during and following long-haul international travel).
Vitamin D deficiency.
While other possible risk factors for ARinf were identified in this review, conflicting evidence limited conclusions to be drawn, and further research is warranted.
Clinical presentation and diagnosis of ARinf in athletes
Introduction
Athletes with ARill who present with typical respiratory symptoms are traditionally categorised according to the predominant anatomical area affected: upper respiratory tract, lower respiratory tract/regional symptoms and systemic (whole body) symptoms. There is considerable overlap between symptoms of non-infective ARill and ARinf, but discrete symptoms and symptom clusters are more typical of ARinf than non-infective ARill (online supplemental table S2). Associated systemic symptoms, or other symptoms of multiorgan involvement, can also indicate ARinf rather than a non-infective cause of ARill (online supplemental table S2).
The clinical presentation of an ARinf is highly variable, and is influenced by several pathogen and host factors,64 and ranges in severity from mildly symptomatic to life-threatening and death.34 Explanations for the non-specific clinical presentation of ARinf include: (1) overlapping of some symptoms and clinical signs of ARinf and non-infective ARill, (2) the same pathogen can cause variable clinical presentations of ARinf in a group of athletes, (3) different pathogens can cause a similar ARinf clinical syndrome in the same athlete,34 and (4) many symptoms are the result of a non-specific acute phase response, which are common to all infections.52 Therefore, an ARinf caused by a specific pathogen cannot be diagnosed by typical symptoms and clinical signs (clinical syndrome) alone, and laboratory tests are required for formal identification.
Asymptomatic ARinf in athletes
Several pathogens can infect athletes, but the athlete may remain asymptomatic.64 For example, in a review of adult human influenza volunteer challenge studies in the general population, 30% of influenza virus infections were asymptomatic.65 In one study among athletes during the Nordic Ski World Championships, viral infections were asymptomatic in 8% of athletes of Team Finland, 19% of staff members and 22% of controls.39 Data from recent studies during the COVID-19 pandemic indicate that about 20% to 30% of SARS-CoV-2 infections in athletes are asymptomatic. Asymptomatic infections are important in the SEM context because: (1) there may be a risk, although likely to be very small, of adverse medical events during exercise, (2) the potential negative effect of asymptomatic ARinf on exercise/sports performance in athletes is unclear, but again is likely to be low and (3) there is a potential risk of transmission within teams and sports events.40 The importance of asymptomatic ARinf in transmission chains has been highlighted by the COVID-19 pandemic.
Clinical syndromes of ARinf
A clinical syndrome is defined as a combination of symptoms and signs (sometimes also referred to as a clinical phenotype) that together represent a disease process. Defining and diagnosing the clinical syndrome of ARinf, plotting the time course by monitoring the progress of the symptoms and signs, and knowing the pathogen, are all important in guiding the SEM clinician in management of athletes with ARinf. These parameters are relevant to identify potential detrimental effects of ARinf on exercise and sports performance and mitigate the risk of medical complications when resuming exercise training.
Symptomatic ARinf typically presents with mild, non-specific localised upper respiratory tract symptoms such as sore throat, sneezing, rhinorrhoea and nasal congestion/stuffiness.34 Cough and hoarseness are variable, and can indicate either upper or lower respiratory tract involvement. Primary symptoms can emerge initially or develop after several days.34 Both pathogen and host dependent symptoms of ARinf typically peak within 2–3 days after onset, are self-limited and resolve by 7–10 days in adults, both in the general population34 and in athletes.27 The duration of ARinf symptoms can be used as an indicator of severity of ARinf. Indicators of a more severe infection are: (1) regional symptoms (headache), (2) systemic symptoms (malaise, fever, myalgia and fatigue), (3) prolonged symptoms (lasting >7 days), (4) symptoms that increase rather than decrease in severity over time, (5) the development of new symptoms over time and (6) specific symptoms associated with multiorgan (non-respiratory) involvement.
Classification of clinical syndromes of ARinf
Clinical syndromes of ARinf can be based on a broad anatomical classification (predominantly upper or lower respiratory tract) and underlying pathology. Although this scenario is rapidly changing, most SEM clinicians do not yet have routine access to laboratory testing methods to identify specific pathogens causing ARinf to guide their clinical decision making. In this IOC consensus, we propose a classification of the clinical syndromes of ARinf in athletes, which has been adapted from Treanor.34 This classification is also based on a clinical presentation of an ARinf predominantly affecting the upper or the lower respiratory tract.
Clinical point/s: Classification of clinical syndromes of acute respiratory infections (ARinf) in athletes
Diagnosing the clinical syndromes of ARinf in athletes
Clinical diagnosis of a suspected ARinf (history and clinical examination)
Awareness of the current epidemics and a careful history of symptomatology with a clinical examination is recommended to identify the clinical syndromes of an ARinf. The case definition for each clinical syndrome as well as the broad clinical features of each clinical syndrome are summarised in table 3.
Case definitions and clinical features of acute respiratory infections (ARinf) clinical syndromes in athletes
Special investigations to confirm the diagnosis of an ARinf (no pathogen identified)
APRs are a heterogeneous group of plasma proteins that increase or decrease in concentration in response to inflammatory stimuli, including acute infections. There are several clinically important APR's and their potential diagnostic value has been reviewed.54 66 Non-diagnostic specific markers of infection that the SEM clinician can consider as diagnostic markers are erythrocyte sedimentation rate (ESR), CRP and PCT. CRP is a better measure of the acute-phase response, more sensitive than ESR, and the preferred marker of infection. The clinical relevance of CRP is that, in response to ARinf, CRP concentration begins to rise after 12 to 24 hours and peaks within 2–3 days (50–100 mg/L). Extremely high increases in CRP (>500 mg/L) are more common in bacterial infections and severe systemic infections.54 Therefore, measurement of CRP concentration in an athlete with suspected ARinf can be useful to confirm the presence of an infection.
PCT is less commonly measured but can be a useful differential biomarker for bacterial (vs viral) ARinf. PCT has been used in the early identification of bacterial lower ARinf, and to stratify patients with a higher risk of complications.54 Finally, a full blood count (FBC) and differential white cell count can also be of value to distinguish non-infective ARill from ARinf in an athlete.54
Special investigations to identify the causative pathogen in ARinf
There are several methods to detect the pathogens causing the ARinf by collecting a nasopharyngeal mucosal sample with a flocked nasal swab, obtaining a sputum sample, or taking a blood sample for antibody testing.67 Viral and bacterial culture remains the 'gold standard' for pathogen identification. For viral diagnostics, the traditional diagnostic method of culture has, in the last two decades, largely been superseded by PCR tests.68 Antigen tests have proven to be useful in virus detection and control during the COVID-19 pandemic.69 However, antigen tests are not able to detect all respiratory viruses, and their sensitivity in adults may be as low as 30%.70 71 The commercial multiplex respiratory PCR tests are particularly useful as they can detect the genetic material (nucleic acids) of up to 16–18 respiratory viruses concurrently from a single mucus sample.72–74 Additionally bacterial targets such as Streptococcus pneumoniae, Mycoplasma pneumoniae, Chlamydia pneumoniae, Haemophilus influenzae are also included in some commercial PCR kits.75 76 It is important to note that a positive PCR test does not necessarily reflect active virus replication, and associations between viral load and infectiousness remain unclear.33 77 Sensitive and specific molecular test platforms, as well as fast, automated molecular point-of-care tests are becoming increasingly applicable for clinical use in SEM at international competitions such as the Olympic and Paralympic Games.39 40 78 The need for routine expensive comprehensive pathogen identification of ARinf is debatable as a specific therapeutic intervention is only available for influenza. However, the COVID-19 pandemic highlighted the importance of early recognition of symptoms, and early and precise viral pathogen identification so that athletes can be isolated quickly and quarantined to prevent spread of infection.39 40
Special investigations to assess for regional and systemic involvement (multiorgan involvement) of ARinf
In suspected cases of more severe and complicated ARinf, a range of special investigations can be considered to confirm the diagnosis of multiorgan involvement. The choice of special investigations will depend on the suspected involvement of the organ system/s involved. Some of the more common special investigations that the SEM clinician can consider in cases of moderate to severe ARinf in athletes are listed (online supplemental table S4). The consensus group recommends that confirmation of the diagnosis, determination of ARinf severity as well as management of regional and multiorgan complications, are best conducted in conjunction with specialist clinician colleagues.
Determining the severity of ARinf in athletes
There is substantial variability in the severity of illness when the same pathogen causes ARinf in multiple athletes, or when different pathogens cause ARinf in one athlete. The severity of an ARinf in athletes is dependent on numerous factors including the pathogen and host characteristics, which may be genetic or acquired. The following host (athlete) characteristics may predispose an individual to a more severe ARinf; older age, male sex, obesity and comorbidities (immune system dysfunction, immunosuppression, use of immune suppressive medications (eg, Transplant Games), hypertension, cardiovascular disease, cancer, chronic lung disease including asthma, diabetes mellitus) and Para athletes with spinal cord lesions and those of high needs. The risk of more severe ARinf is also related to vaccination status and exposure to a higher pathogen (viral) load.
Determination of what is considered a 'more severe' ARinf is derived from studies in the general population, particularly during the COVID-19 pandemic. In the general population, the definition of the 'severity' of an ARinf is based on parameters such as the presence or absence of severe symptoms (severe dyspnoea at rest), extremely low oxygen saturation, hospital admission, high care or intensive care unit admission, presence of respiratory distress requiring mechanical ventilation or death.79 However, most athletes with ARinf do not have extremely low oxygen saturation, do not require hospitalisation, and would be classified with an ARinf of mild to moderate severity. Currently, there are no validated tools, algorithms or scoring systems to differentiate severity of ARinf in athletes, who fall into the majority 'mild to moderate severity' category.
For the SEM clinician, it is important to assess the severity of ARinf in athletes in this 'mild to moderate' category of ARinf because this can: (1) influence the risk of medical complications during exercise after infection, which then guide clinical decision making in RTS following an ARinf, and (2) determine potential detrimental effects on exercise and sports performance post-infection. This IOC consensus group, by expert opinion, suggests that several parameters on clinical presentation (history and findings on clinical examination), as well as results of special investigations, can be useful indicators to stratify the severity of an ARinf in an athlete (table 4). We suggest that this clinical approach can be used in the initial assessment of athletes with ARinf and can form the basis of RTS decision making. However, we recognise that validation of these indicators has not been established fully, and further research is needed.
Indicators of the severity of an upper ARinf in athletes (history, physical examination and results of special investigations)
Principles of management of ARinf in athletes
The two most common clinical syndromes of ARinf that an SEM clinician will manage routinely are the 'predominantly' upper ARinf syndromes of: (1) acute rhinitis/rhinosinusitis/rhinopharyngitis ('common cold', 'coryza', 'viral upper respiratory infection') and (2) acute rhinitis/rhinosinusitis/rhinopharyngitis with systemic symptoms/signs ('influenza-like', 'influenza' syndrome). In this section, we focus on the principles of management of these two clinical syndromes. Other clinical syndromes of upper ARinf (acute laryngitis and tracheobronchitis) are less common and lower ARinf syndromes in athletes are rare.
There are seven main principles of management of ARinf that SEM clinicians can consider.
Clinical point/s: Seven principles of management of acute respiratory infections (ARinf) that Sport and Exercise Medicine clinicians can consider
General non-pharmacological treatment to support recovery and the immune response.
Nutritional, immune or probiotic supplementation.
Pharmacological treatment of symptoms.
Antiviral agents (for specific cases).
Antibacterial agents (for specific cases).
Management of the athlete with suspected multiorgan involvement or other complications (if present).
Decisions to allow an athlete with an ARinf to return-to-sport, including the initial decision to resume training (return-to-participation), and the subsequent decision to return to full exercise/sport performance.
These principles will be briefly reviewed, but a detailed summary, including the specific treatment, the advice/administration dose, as well as evidence of the effect of the treatment and potential side effects unique to upper ARinf in athletes, is presented in table 5.
A summary of the principles treatment of upper acute respiratory infection (ARinf) in athletes
General treatment to support recovery and the normal immune response
Rest/training reduction/restriction
In an athlete presenting with ARinf, one of the first management decisions the SEM clinician will make is whether rest, training reduction or restriction of training is required during the acute phase of the ARinf. The following recommendations are based on the severity classification of the upper ARinf (table 4). In mild/moderate ARinf, normal daily activity is generally allowed. In most cases symptoms of ARinf resolve within 1–3 days, but it is advisable to perform a daily checklist before either starting or resuming exercise training (checklist 1: table 6).
Checklists before starting or resuming exercise training in an athlete with acute respiratory infection (ARinf)
In general, once localised symptoms have either resolved or are very mild, and if there are no items flagged in the checklist, the athlete can be advised to perform an exercise challenge test (self-administered field test by the athlete/coach/support staff or a laboratory test). In severe ARinf, bed rest is recommended until regional and systemic symptoms have resolved, and there is no evidence of active multiorgan involvement, after which normal daily activity is allowed. For severe ARinf, the athlete is advised to consult an SEM clinician who will perform a checklist before giving advice of resuming exercise training (checklist 2: table 6). Based on the outcome of the checklist, a decision can be made to conduct an exercise challenge test.
General nutrition
It is well known that general nutritional status influences both their susceptibility to infection and response to infection.80 81 Thus, adequate energy availability as well as micro-and macronutrient intake are important for immune health in athletes with ARinf.80–82
Hydration
Maintenance of fluid intake during an ARinf is important to ensure that mucous membranes remain moist, to their defensive function and alleviate acute symptoms.82 However, there is no evidence to support increasing fluid intake beyond the maintenance of normal hydration.
Nasal saline irrigation
Nasal saline irrigation may relieve symptoms of ARinf, but data are limited.
Nutritional/immune supplements and/or probiotics
The use of specific nutritional or immune supplements as well as probiotics for athletes with ARinf is common and has a high cultural influence and community support. In general, scientific evidence to support the widespread use of these agents is lacking (table 5). Some studies report that nutritional supplements have some benefit in reducing the duration of symptoms or the recovery time of ARinf and these include zinc,83 84 Vitamin C and Vitamin D but only in vitamin deficient athletes. Although supplementation with herbal medicines is popular there is only low level evidence that some may be beneficial (table 5) including BNO1016, cineole and andrographis paniculata SHA-10 extract, pelargonium sidoides extract85 86 and Echinacea.87 Probiotics may help reduce the number of and the mean duration of upper ARinf,88 but the quality of the evidence is low. In summary, evidence for these therapies is generally of low quality, remains mixed and further studies are required.
Pharmacological treatment of symptoms
Treatment of symptoms is an important component of the clinical care of athletes with ARinf. Rhinorrhoea may impair athletes' well-being and physical performance and swollen mucous membranes in the nasopharynx may give rise to obstruction and predispose athletes to secondary otitis media and/or sinusitis. There are several options for pharmacological treatment of symptoms of ARinf in athletes including analgesics, non-steroidal anti-inflammatory drugs (NSAIDs), mucolytics, corticosteroids, decongestants, antitussive agents, antihistamines, and combination drugs. Options for the pharmacological treatment of symptoms, and evidence for using these medications during the acute phase of upper ARinf, is summarised in table 5.
These treatments are frequently available as over-the-counter drugs in most countries, and therefore, are not well controlled by SEM clinicians and may cause side effects in athletes and can lead to doping violations. For example, NSAID's can lead to gastric side effects, may increase risk of bleeding, can have renal side effects, and by masking symptoms can lead to a false positive perception of the clinical status of an athlete.
Antiviral agents
Antiviral treatment is available only for influenza viruses. SEM clinicians should be aware of the prevailing viral epidemics and can confirm influenza virus infection by PCR when suspected. In cases of confirmed influenza infection, antiviral treatment with oseltamivir or zanamivir should be started soon after the onset of the symptoms,89 but side effects of these drugs must be considered (table 5). If an athlete has been in close contact with influenza virus, prophylaxis treatment can be considered. Point-of-care-testing enables prophylaxis with oseltamivir for those predisposed to influenza virus infections, for example, living in same household or travelling in the same flight or carpool (https://www.cdc.gov/). Isolation of infected team members should be initiated after the onset of symptom/s and continued for 3–4 days, that is, the most infectious period.90