The Impact of Sport Training on Oral Health in Athletes

letes' oral health appears to be poor in numerous sport activities and different diseases can limit athletic skills, both during training and during competitions. Sport activities can be considered a risk factor, among athletes from different sports, for the onset of oral diseases, such as caries with an incidence between 15% and 70%, dental trauma 14–70%, dental erosion 36%, pericoronitis 5–39% and periodontal disease up to 15%. The numerous diseases are related to the variations that involve the ecological factors of the oral cavity such as salivary pH, ow rate, buffering capability, total bacterial count, cariogenic bacterial load and values of secretory Immunoglobulin A. The decrease in the production of S-IgA and the association with an important intraoral growth of pathogenic bacteria leads us to consider the training an “open window” for exposure to oral cavity diseases. Sports dentistry focuses attention on the prevention and treatment of oral pathologies and injuries. Oral health promotion strategies are needed in the sports environment. To prevent the onset of oral diseases, the sports dentist can recommend the use of a custom-made mouthguard, an oral device with a triple function that improves the health and performance of athletes. During training, the sports dentist must monitor the athletes and the sports examination protocol must be implemented

Oral health promotion strategies are needed in the sports environment. To prevent the onset of oral diseases, the sports dentist can recommend the use of a custom-made mouthguard, an oral device with a triple function that improves the health and performance of athletes. During training, the sports dentist must monitor the athletes and the sports examination protocol must be implemented with the inclusion of the clinical examination, quantitative and qualitative analysis of saliva and instructions on the use, cleansing and storage of the mouthguard. Keywords:saliva; oral microbiota; S-IgA; mouthguards; oral disease; sports dentistry 1. Introduction The growing diffusion of sports activities is focusing attention on the development of diseases correlated with the sporting performance, in addition to the health bene ts. The athlete should know the risks associated with carrying out sporting activities and direct more attention to the health status of his oral cavity since the alterations of the oral cavity contribute in a negative way to the health, well-being and physical performance of the athlete [1]. The main disorders of the oral cavity, correlated with the performance of various sports that have a signi cant impact on the quality of life of athletes, are represented by trauma, joint disorders, alterations and/or oral pathologies, such as caries, erosions, dental discolorations and periodontal disease. Moreover, the intense physical exercise at the start of competitions and throughout training time involves a reduction in salivary ow rate and in secretory IgA (S-IgA) load, resulting in a decrease in the host organism's defenses and, therefore, an increase in susceptibility to particular pathologies, such as upper respiratory tract infections (URTI) and, speci cally, pathologies of the oral cavity [2–5]. Therefore, during sport activities, the athletes must be monitored by sport dentists for changes affecting their oral cavity and the sports examination protocol must be imple- mented with the inclusion of clinical examination, quantitative and qualitative analyses of saliva and the instructions on the use, cleansing and storage of the mouthguard, which is a dental device used by athletes who need to wear oral protection during sports activities [6]. Dent. J.2021,9, 51.

their oral cavity and the sports examination protocol must be imple- mented with the inclusion of clinical examination, quantitative and qualitative analyses of saliva and the instructions on the use, cleansing and storage of the mouthguard, which is a dental device used by athletes who need to wear oral protection during sports activities [6]. Dent. J.2021,9, 51.

Dent. J.2021,9, 51 2 of 12 The rst purpose of the present review is to describe the main diseases affecting the athletes' oral cavity and the changes that occur in their oral ecosystem during sport training with and/or without use of mouthguard. The second objective is to delineate a program of prophylaxis and/or treatment for the diseases and oral changes reported. 2. The Oral Ecosystem and the Saliva Diagnostic Function The oral ecosystem is a moist environment that includes the various anatomical microniches of the oral cavity and the oral microbiome. Two important physiological uids, saliva and gingival crevicular uid, wet the oral ecosystems and provide water, nutrients, adherence and antimicrobial factors [7]. Different physiochemical factors characterize the habitat of the oral cavity, thus sup- porting the development and growth of different microbial communities. The oral microbiome includes a complex range of microorganisms, either present in saliva as organisms in the planktonic phase or, in the sessile phase, adhering to the oral surfaces as a dental plaque bio lm, namely 2000 taxa of bacteria, archaea and protozoa, fungi and viruses [7–9]. They are organized through a mechanism of mutual exchange of resources that give life to an ecosystem and, in most cases, they live in balance with each other and they bring signi cant bene ts to the host organism. The major oral diseases, such as tooth decay and periodontal disease, arise from imbalance or dysbiosis within the plaque bio lm [7–9]. The gingival uid is an exudate from plasma; it contains proteins, albumin, leukocytes, immunoglobulins and complement and is characterized by slow diffusion through the healthy gingiva which increases during in ammation [8]. Human saliva is a body uid secreted by the salivary glands, whose function is to maintain the integrity of the hard and soft tissues of the oral cavity and to wet the mucous membranes of the mouth, throat and larynx in order to maintain the homeostasis of the oral ecosystem [10,11]. Normally, the daily salivary ow is estimated to be between 0.5 and 2 L [10]; the temperature of the saliva is more or less 35–36

the integrity of the hard and soft tissues of the oral cavity and to wet the mucous membranes of the mouth, throat and larynx in order to maintain the homeostasis of the oral ecosystem [10,11]. Normally, the daily salivary ow is estimated to be between 0.5 and 2 L [10]; the temperature of the saliva is more or less 35–36 and the pH is 7 0.25, being saturated with calcium phosphates [11]. The buffer systems present in the saliva allow the maintenance of proper acid–base balance, swinging the pH values between 5.7 and 6.2 in the rest condition, to values of stimulated saliva of 8, depending on the habits of oral hygiene, food and the buffering action of saliva [12,13]. Saliva hosts a broad spectrum of proteins/peptides, nucleic acids, electrolytes, heavy metals, microorganisms, hormones, drugs and neurotransmitters that come from multiple local and systemic sources. Indeed, human saliva can be de ned as a “body mirror” because it can re ect the physiological and pathological conditions of the whole body, including the oral cavity [13–15]. Therefore, it can represent an important diagnostic and monitoring tool in many elds such as dentistry, allowing healthcare providers to assess athletes, health or disease status [16] (Figure). Differences between individuals in the microbiological composition of saliva can also be re ected in variations in the biochemical composition. However, several authors agree that changes in the oral microbiota accompany a number of dental diseases, given the complex composition of saliva and its importance for oral homeostasis. Moreover, considering that the methods of collection and the degree of stimulation of salivary ow can in uence the salivary composition, it is necessary to develop standard operating procedures for the collection of the sample itself and for the storage conditions [17]. Numerous valid reasons lead us to use saliva as a diagnostic uid to monitor the state of health and disease. Human saliva offers several advantages over other biological uids, such as serum, as it is readily available; quick and easy to collect, store and ship; low cost in suf cient quantities for the analysis; is not susceptible

storage conditions [17]. Numerous valid reasons lead us to use saliva as a diagnostic uid to monitor the state of health and disease. Human saliva offers several advantages over other biological uids, such as serum, as it is readily available; quick and easy to collect, store and ship; low cost in suf cient quantities for the analysis; is not susceptible to transformations; and is easy to handle for diagnostic procedures. The sampling is cost-ef cient and stress- free [15,16,18,19]. Saliva collection is less invasive and safer than venous sampling, which could expose patients and health care providers to infectious diseases such as HIV or hepatitis virus [20].

Dent. J.2021,9, 51 3 of 12Dent. J. 2021, 9, x FOR PEER REVIEW 3 of 13 Figure 1. Human saliva collected from an athlete for the research of the main biomarkers. Differences between individuals in the microbiological composition of saliva can also be reflected in variations in the biochemical composition. However, several authors agree that changes in the oral microbiota accompany a number of dental diseases, given the complex composition of saliva and its importance for oral homeostasis. Moreover, consid- ering that the methods of collection and the degree of stimulation of salivary flow can influence the salivary composition, it is necessary to develop standard operating proce- dures for the collection of the sample itself and for the storage conditions [17]. Numerous valid reasons lead us to use saliva as a diagnostic fluid to monitor the state of health and disease. Human saliva offers several advantages over other biological fluids, such as serum, as it is readily available; quick and easy to collect, store and ship; low cost in sufficient quantities for the analysis; is not susceptible to transformations; and is easy to handle for diagnostic procedures. The sampling is cost-efficient and stress-free [15,16,18,19]. Saliva collection is less invasive and safer than venous sampling, which could expose patients and health care providers to infectious diseases such as HIV or hep- atitis virus [20]. The use of saliva can be performed in the field of sports medicine and exercise to examine exercise-related endocrinological, immunological and microbiological status as well as to assess training loads and subsequently the risk of developing diseases [19]. For example, determining cortisol concentrations in sequentially collected saliva samples in response to circadian rhythms to assess exercise stress can diagnose and pre- vent overtraining syndrome (OTS) in athletes. Overtraining syndrome is an accumulation of training and/or non-training stress that causes a decrease in long-term performance capacity with or without signs and symptoms related to physiological and psychological maladjustment, in which the restoration of performance capacity requires several weeks or months [21]. Moreover, an evaluation of salivary immunoglobulins (S-IgA) and anti- microbial proteins (α-amylase, lysozyme, lactoferrin) allows one to

Overtraining syndrome is an accumulation of training and/or non-training stress that causes a decrease in long-term performance capacity with or without signs and symptoms related to physiological and psychological maladjustment, in which the restoration of performance capacity requires several weeks or months [21]. Moreover, an evaluation of salivary immunoglobulins (S-IgA) and anti- microbial proteins (α-amylase, lysozyme, lactoferrin) allows one to determine the effects of exercise on mucosal immunity. Decreases in S-IgA and antimicrobial protein concen- tration and/or secretion rate have been described in athletes during a training season, thus making the athlete more susceptible to upper respiratory tract infections [19]. Sport Figure 1.Human saliva collected from an athlete for the research of the main biomarkers. The use of saliva can be performed in the eld of sports medicine and exercise to examine exercise-related endocrinological, immunological and microbiological status as well as to assess training loads and subsequently the risk of developing diseases [19]. For example, determining cortisol concentrations in sequentially collected saliva sam- ples in response to circadian rhythms to assess exercise stress can diagnose and prevent overtraining syndrome (OTS) in athletes. Overtraining syndrome is an accumulation of training and/or non-training stress that causes a decrease in long-term performance ca- pacity with or without signs and symptoms related to physiological and psychological maladjustment, in which the restoration of performance capacity requires several weeks or months [21]. Moreover, an evaluation of salivary immunoglobulins (S-IgA) and antimi- crobial proteins ( -amylase, lysozyme, lactoferrin) allows one to determine the effects of exercise on mucosal immunity. Decreases in S-IgA and antimicrobial protein concentration and/or secretion rate have been described in athletes during a training season, thus making the athlete more susceptible to upper respiratory tract infections [19]. Sport activities allow athletes to have a more “health-associated” intestinal microbiota. It is characterized by a greater presence of bacterial species that promote health, greater microbial diversity, func- tional metabolic capacity and metabolites associated with microbes, which can modulate mucosal immunity and improve gastrointestinal barrier function [22]. Finamore et al. demonstrated a link between saliva and intestinal pro les in patients with in ammatory bowel diseases (IBD),

more “health-associated” intestinal microbiota. It is characterized by a greater presence of bacterial species that promote health, greater microbial diversity, func- tional metabolic capacity and metabolites associated with microbes, which can modulate mucosal immunity and improve gastrointestinal barrier function [22]. Finamore et al. demonstrated a link between saliva and intestinal pro les in patients with in ammatory bowel diseases (IBD), and this result suggests that, even in athletes, saliva sampling can also be used as a biomarker for gut disease in the oral–gut axis [23]. By analyzing the saliva, in particular the pH values, buffer capacity, ow rate and growth of cariogenic bacteria, it is possible to assess caries risk [24–26]. Further possibilities for diagnosing speci c oral and systemic diseases can also be obtained by saliva tests, such as the assessment of periodontal diseases and atherosclerosis by checking salivary in ammatory cytokines including IL-1 , IL-6, TNF- and prostaglandin E2; acute myocar- dial infarction by evaluating the concentration of C reactive protein (CRP); and pancreatic cancer by searching for the presence ofNeisseria elongateandStreptococcus mitis[25–27]. At the same time, as a diagnostic tool, saliva has some disadvantages. Among the limits to the wide use of saliva, the great variability of its normal composition, attributable to diurnal/circadian variations of some biomolecules contained therein, must be regarded.

Dent. J.2021,9, 51 4 of 12 Based on these variations, particular attention should be paid to the sampling procedure and the xing of the reference limits for the concentrations of the individual components. At the same time, the high variability in the composition of saliva can be exploited for the monitoring of various biorhythms (seasonal, close to 24 h, circadian, etc.) in order to study the physiological characteristics of the human body during sport activities [15,19,28]. Research based on the use of infrared spectroscopy technique, applied to detect circadian changes in the content of biological uids, including saliva, has shown that gender- and age-dependent differences have been reported for some physicochemical characteristics of human saliva [29]. Currently, all doctors, dentists and laboratories should favor the use of saliva follow- ing the example of the American National Institute of Dental and Craniofacial Research (ANIDCR) that, in 2002, removed all obstacles and approved these body uids as a diag- nostic tool for assessing health and disease status [25,26]. Thus, during the rst visit of the athletes, salivary tests must be performed. The stimulated saliva can be collected with salivettes (Sarstedt AG & Co, Nümbrecht, Germany), with the athletes chewing the cotton roll present in the salivette for 1 min (Figure). The collected saliva can be subjected to chairside or laboratory analysis, in order to obtain information on microbiological, immunological and other ecological factors [30].Dent. J. 2021, 9, x FOR PEER REVIEW 4 of 13 activities allow athletes to have a more “health-associated” intestinal microbiota. It is char- acterized by a greater presence of bacterial species that promote health, greater microbial diversity, functional metabolic capacity and metabolites associated with microbes, which can modulate mucosal immunity and improve gastrointestinal barrier function [22]. Finamore et al. demonstrated a link between saliva and intestinal profiles in patients with inflammatory bowel diseases (IBD), and this result suggests that, even in athletes, saliva sampling can also be used as a biomarker for gut disease in the oral–gut axis [23]. By analyzing the saliva, in particular the pH values, buffer capacity, flow rate and growth of cariogenic bacteria, it

al. demonstrated a link between saliva and intestinal profiles in patients with inflammatory bowel diseases (IBD), and this result suggests that, even in athletes, saliva sampling can also be used as a biomarker for gut disease in the oral–gut axis [23]. By analyzing the saliva, in particular the pH values, buffer capacity, flow rate and growth of cariogenic bacteria, it is possible to assess caries risk [24–26]. Further possibili- ties for diagnosing specific oral and systemic diseases can also be obtained by saliva tests, such as the assessment of periodontal diseases and atherosclerosis by checking salivary inflammatory cytokines including IL-1β, IL-6, TNF-α and prostaglandin E2; acute myo- cardial infarction by evaluating the concentration of C reactive protein (CRP); and pan- creatic cancer by searching for the presence of Neisseria elongate and Streptococcus mitis [25– 27]. At the same time, as a diagnostic tool, saliva has some disadvantages. Among the limits to the wide use of saliva, the great variability of its normal composition, attributable to diurnal/circadian variations of some biomolecules contained therein, must be regarded. Based on these variations, particular attention should be paid to the sampling procedure and the fixing of the reference limits for the concentrations of the individual components. At the same time, the high variability in the composition of saliva can be exploited for the monitoring of various biorhythms (seasonal, close to 24 h, circadian, etc.) in order to study the physiological characteristics of the human body during sport activities [15,19,28]. Research based on the use of infrared spectroscopy technique, applied to detect cir- cadian changes in the content of biological fluids, including saliva, has shown that gender- and age-dependent differences have been reported for some physicochemical character- istics of human saliva [29]. Currently, all doctors, dentists and laboratories should favor the use of saliva follow- ing the example of the American National Institute of Dental and Craniofacial Research (ANIDCR) that, in 2002, removed all obstacles and approved these body fluids as a diag- nostic tool for assessing health and disease status [25,26]. Thus, during the first visit of the athletes, salivary tests must be performed.

dentists and laboratories should favor the use of saliva follow- ing the example of the American National Institute of Dental and Craniofacial Research (ANIDCR) that, in 2002, removed all obstacles and approved these body fluids as a diag- nostic tool for assessing health and disease status [25,26]. Thus, during the first visit of the athletes, salivary tests must be performed. The stim- ulated saliva can be collected with salivettes (Sarstedt AG & Co, Nümbrecht, Germany), with the athletes chewing the cotton roll present in the salivette for 1 min (Figure 2). The collected saliva can be subjected to chairside or laboratory analysis, in order to obtain in- formation on microbiological, immunological and other ecological factors [30]. Figure 2. The collection of stimulated saliva with salivettes. Moreover, the dentist must motivate the patient and can improve his compliance by determining the status of oral health through the saliva analysis. The checks must be con- tinued during training, and must include new salivary tests for control of the variations in the oral ecological factors caused by sports activities and by use of the mouthguard. Figure 2.The collection of stimulated saliva with salivettes. Moreover, the dentist must motivate the patient and can improve his compliance by determining the status of oral health through the saliva analysis. The checks must be continued during training, and must include new salivary tests for control of the variations in the oral ecological factors caused by sports activities and by use of the mouthguard. Such attention to the starting situation and the changes that occur in the athletes' oral cavity is justi ed by the need to resort to all available forms of prevention in order to preserve the oral health of athletes, usually adolescents. 3. Sports and Oral Health The environment of the oral cavity is in uenced by lifestyle, hygiene and eating habits, the possible intake of drugs and the performance of sports activities. Thanks to numerous researches carried out by sports dentists over the years, knowledge about the factors that regulate the oral ecology, such as salivary pH and ow, microbial load and S-IgA levels

This review discusses the impact of sport training on oral health in athletes.