Vaccinations among athletes: evidence and recommendations

KEYWORDS:

• Vaccination
• elite athletes
• open window
• immunization strategies
• Olympic Games

The last Olympic Summer Games, that took place in Brazil during August 2016, kept worldwide attention not only because the Olympic Games is the most important sporting event but also for the risks of infection related to the location, both for athletes and for visitors. For the first time in the Internet era, the Olympic official website provided a specific webpage with general information on vaccines recommended for travelers.

The risk of sporadic cases of communicable diseases among athletes and their team or the spread of an epidemic was a possible scenario at the Olympic Games probably because the Zika virus outbreak in South America resulted in a growing emphasis on the potential public health risks for athletes and travelers so that some experts declared that the ‘Rio’s Olympics are a risk to global health’ [1].

In this context, the interest in infectious diseases increased the attention of international sport and health authorities on vaccinations, on what are the most important ways to prevent infectious diseases. Before the beginning of the Games, the World Health Organization created a webpage containing health advice for travelers to the 2016 Summer Olympic and Paralympic Games with specific information on vaccines [http://www.who.int/ith/updates/20160621/en/]; this was a very important effort, considering that in the London 2012 Summer Olympic Games, only general public health measures were reported in the WHO website.

These experiences seemed to suggest that the fear of infections is a very good way to highlight the importance of prevention: also during the 2010 Winter Games, the H1N1 pandemic encouraged official recommendations on vaccination for athletes attending sporting events [2].

In scientific literature the theme of vaccinations of athletes is not largely studied and over the last 30 years only 18 papers are available in PubMed using the following key words: ‘vaccine and athletes’, ‘vaccine and sport’, ‘vaccination and athletes’, ‘vaccination and sport’ [1–18]. We considered only articles in English in which the main topic (or the only topic) was related to immunization strategies or concerns for athletes. If we limit our research to the last 10 years, we can find nine articles. Overall, only four papers [5,6,8,9] (two in the last 10 years) could be classified as research articles, the others belong to expert opinion and narrative reviews.

The prevention of vaccine preventable diseases among athletes can be examined according to three points of view: their major risk of infection due to environmental factors; their need to fulfill the training schedule; the issue of ‘sport immunology’ or ‘exercise immunology’, defined as the study of acute and chronic effects of various exercise workloads on the immune system and immunological surveillance against pathogens [19]. These emerging issues must be read in the view of epidemiological changes related to the immunization strategies.

The determinants of increased infectious diseases transmission among athletes are related to the sport activities areas (in particular for indoor sports), to the frequent use of collective structures (for example: hotels, restaurants) and to international travels and permanence related to sport challenges.

Athletes stay in crowded places (e.g. locker rooms, sport meetings) with a great number of persons and in particular for indoor sports (wrestling, gymnastics, etc.), close contact between athletes is common, with increased risk of airborne infection [20]. During international competitions, athletes are hosted in villages where they share the same services and in these settings there is a high risk of outbreak onset (e.g. food-born infection): for example, in 2016, the Rio Olympic Village hosted 17,950 athletes and technical staff in 3604 flats [21]. In this location, there is also an increased risk of promiscuity and sexual transmission of disease. Elite athletes travel a lot to join national and international events and thus they are prone to acquire infections not prevalent in their home countries; this is the example of Zika virus in Brazil and of ticks infestation in Austria during 2008 European Football Championship [3].

Athletes need to be healthy as getting sick can compromise their competitive performances. Moreover, infections have a different significance in competitive sports. For elite athletes even mild diseases, that would never cause absenteeism in the general population, are relevant for their individual performance and because team coaches tend to leave them on the bench in case of infection [4]. A diarrhea or an upper respiratory infection is not a serious problem for a healthy young adult, but it can be very serious for an international athlete the day before the World Cup Final: due to this apparently mild disease, he could miss or fail the most important appointment in his life, e.g. McIntyre described an outbreak of influenza during the XV Winter Olympic Games held in Calgary in February 1988. In the Olympic village 1700 athletes representing 57 countries were housed and the outbreak compromised the performances and the winning chances of so many of them [17].

Intense exercise (either acute or chronic) alters the functions and quantity of both innate and acquired immune system’s circulating cells (e.g. neutrophils, monocytes and NK cells). The reason for the observed decrease in the acquired immune response during intense physical exercise seems to be related to an increased release and circulation of stress hormones (cortisol and catecholamines) and to the cytokines-mediated alteration of the balance pro-/anti-inflammatory activity [19]. This alteration of the immune response following intense training and competitions is called the ‘open window’ and it is responsible for a higher risk of infection in athletes when exposed to microorganisms [3,16].

This window could cause an increase in susceptibility to upper respiratory tract diseases (and in this group we can find several vaccine preventable diseases, such as influenza or pertussis). Many studies have indicated a decrease in the immune function in response to exercise. In particular, a study carried out in 2011 among elite male taekwondo athletes showed that mucosal immunity is modulated by exercise and because of the ‘open window’ of impaired immunity during the precompetition period, the incidence of upper respiratory tract infections was significantly increased after the competition [22].

These immunological concerns must be considered when the vaccination schedule is planned because vaccine administration during the ‘open window’ phase could be associated with a suboptimal immune response and reduced vaccine efficacy [14].

All these themes must be reviewed considering the actual scenario of the vaccine preventable diseases epidemiology, dramatically changed by vaccination strategies (e.g. the international strategy for the measles and rubella eradication and the universal mass strategy for varicella). International efforts for measles elimination achieved the goal of measles control but suboptimal coverage in some areas (such as Europe) and are associated with a reduction of virus circulation, a lack of immunity among young adults and an increase in the median age of infection. In the past all young adults, including athletes, could be considered immune against measles because >90% of the population acquired the infection during the first 10 years of life, instead actually sport club medical staffs have to consider the circumstance that some athletes could be susceptible to measles. The screening of measles immunization status of the athletes is strongly recommended to prevent sporadic cases or clusters of measles among team members; in particular, we have to consider that there is an increasing risk of complications related to measles infection among young adults. In some countries, where universal mass vaccination programs for varicella were activated, similar considerations must be extended also to varicella.

According to the current evidence, it is recommended that elite athletes receive all vaccinations recommended for general population, according to their age. In case of international travels, the risk of vaccine-preventable diseases endemic in the visited country must be considered; finally, some authors suggested additional immunization activities, e.g. for food-borne illness (hepatitis A, typhoid fever) or for influenza (not currently recommended for healthy young adults).

Signorelli et al., in a paper published in 2011, evaluated the increased risks for infectious diseases transmission due the particular exposures and the periodical decrease of the immune system (the so called ‘open window’) and suggested specific guidelines for immunization practices: a check for the standard immunizations of childhood and adolescence, the routine immunizations (seasonal flu and decennial booster doses for tetanus and diphtheria) and the management of particular circumstances in case of epidemics or intercontinental tournaments [15].

For lack of official recommendations from the International Olympic Committee, some authors (sport and public health physicians) reported that athletes should undergo the recommended immunization for the general population. Strong and particular recommendations have been formulated for tetanus, in particular for athletes who have potential contacts with soils contaminated with C. tetani and who are at risks of lesions (e.g. horse racing, cross-country) and hepatitis B, above all in sports with possible contact to blood and body fluid such as football, boxing and hockey [3,4]. In addition, athletes should be the of annual influenza immunization campaigns because of the sharing of overcrowded environments and the advantages of a healthy status for their performances; it is favorable to clarify that in several countries, annual flu vaccination is recommended only for oldest persons or subjects affected by chronic diseases and not for young adults, such as athletes [3]. Yellow fever, meningococcal, hepatitis A and typhoid fever vaccines are recommended only in case of international travels, that could be very frequent for elite athletes who attended international or world challenges; in particular, in the last decades, several international challenges have been located in developing countries (e.g. 2016 Olimpic Games in Brazil or the 2015 Summer Universiade in North Korea) where there is the risk of the circulation of pathogen eliminated in developed countries.

Gärtner and Meyer [4] underlined that the risks of adverse events following immunization are aggravated in athletes for immunological factors as it is for the risk due to infection, and they recommended several risk-benefits evaluations before the vaccination, but their observations did not seem to be based on rigorous data.

Similarly, in 2014 Brito affirmed that the general vaccination guidelines may not always be appropriate for elite athletes, because vaccines and their side effects may impair sports performance or even disturb an athlete’s physiology, but also in this case his considerations are based only on an expert opinion and are not related to experimental observations [16].

This controversy introduces the future of this debate. We need a more rigorous approach to studying the topic of vaccination of elite athletes, based on the availability of current epidemiological data and observational studies. According to this data, research will be able to evaluate the opportunity and the ethical justification of clinical trials that will document if an ad hoc vaccination schedule will be useful for this subgroup of population.

To carry out these studies, an alliance between vaccinologists, the medical staff of sport clubs and sport federations must be built.

The aim of athletes’ immunization is not the eradication of the infections but the protection of an at risk subgroup of the population. For this reason, it is important to correctly select the best vaccines and the best timing for immunization practices and this choice must be evidence-based. Data on immunogenicity and cost-effectiveness of vaccination, with a specific focus on athletes, should be quickly available for stakeholders (Sport Federations, Clubs, Medical Staffs).

Moreover general data about vaccination coverage among athletes are not available, but a survey conducted in 2014 showed that only one in six high school senior athletes received the recommended tetanus, meningococcal and influenza immunizations and a lower proportion of females, only one in 28, received all the recommended HPV vaccines [18]. This seems to be getting to the heart of the problem: as in the general population, athletes may not receive recommended vaccinations. Efforts of public health authorities and medical staff must be spent trying to get athletes vaccinated at least with the routinely recommended vaccines. Finally, athletes are the heroes of new generations that recently seemed prone to refuse vaccines; vaccinologists have to gain the alliance with athletes in order to promote the immunization practices and this would be of great importance in this era of vaccination crisis.

Athletes’ vaccination must become part of the international vaccination programs in order to improve vaccination coverages in communities through their exemplar role. To achieve the goal of a high vaccination acceptance of athletes, vaccination must be offered to all staff members: coaches, referees, trainers. There is good evidence, in reference to health care workers, that the leader opinion and the general attitude of the group are able to increase the vaccination acceptance.

Declaration of interest

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties.

Additional information

Funding

The manuscript was not funded.