© 2014 John Wiley & Sons A/S.
Scand J Med Sci Sports 2014: ••: ••–•• doi: 10.1111/sms.12266
Published by John Wiley & Sons Ltd
Effect of endurance training on dental erosion, caries, and saliva C. Frese1, F. Frese2, S. Kuhlmann1, D. Saure3, D. Reljic2, H. J. Staehle1, D. Wolff1 1
Department of Conservative Dentistry, School of Dental Medicine, University Hospital Heidelberg, Heidelberg, Germany, Department of Sports Medicine, Medical Clinic, University Hospital Heidelberg, Heidelberg, Germany, 3Institute of Medical Biometry and Informatics, Ruprecht Karls University, Heidelberg, Germany Corresponding author: Cornelia Frese, DDS, Department of Conservative Dentistry, Dental School, University Hospital Heidelberg, Im Neuenheimer Feld 400, 69120 Heidelberg, Germany. Tel: +49 6221 5639889, Fax: +49 6221 565074, E-mail: [email protected]
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Accepted for publication 9 May 2014
The aim of this investigation was to give insights into the impact of endurance training on oral health, with regard to tooth erosion, caries, and salivary parameters. The study included 35 triathletes and 35 non-exercising controls. The clinical investigation comprised oral examination, assessment of oral status with special regard to caries and erosion, saliva testing during inactivity, and a self-administered questionnaire about eating, drinking, and oral hygiene behavior. In addition, athletes were asked about their training habits and intake of beverages and sports nutrition. For saliva assessment during exercise, a subsample of n = 15 athletes volunteered in an incremental running field test (IRFT). Athletes showed an
increased risk for dental erosion (P = 0.001). No differences were observed with regard to caries prevalence and salivary parameters measured during inactivity between athletes and controls. Among athletes, a significant correlation was found between caries prevalence and the cumulative weekly training time (r = 0.347, P = 0.04). In athletes after IRFT and at maximum workload, saliva flow rates decreased (P = 0.001 stimulated; P = 0.01 unstimulated) and saliva pH increased significantly (P = 0.003). Higher risk for dental erosions, exercisedependent caries risk, and load-dependent changes in saliva parameters point out the need for risk-adapted preventive dental concepts in the field of sports dentistry.
Today, endurance sports have become increasingly popular among amateurs. Because of their unique training and nutritional habits, it is likely that they are at different risk levels for oral health compared with average non-exercising people. Special attention should be paid on oral diseases such as erosive tooth wear and dental caries, as well as on the changes in salivary parameters. However, their special needs with regard to dental care and oral hygiene education have not yet been considered appropriately in dental research. And although one may presume that athletes might have more precise physical (and oral) perception than nonexercising people, a recent study showed that 302 athletes participating in the London 2012 Olympic Games displayed poor oral health with comparably high prevalence of dental erosions, caries, and periodontitis (Needleman et al., 2013). Data on exercise-dependent alterations of salivary parameters with special regard to the impact on dental erosions and caries are rare (Horswill et al., 2006; Phillips et al., 2011; Mulic et al., 2012). Investigations showed that a great number of athletes presented signs of tooth erosion. There is also evidence that the performance of exercise decreased salivary flow rates and
salivary pH increased or decreased dependent on the beverages consumed by the athletes. A decreased salivary pH might be associated with tooth wear (Horswill et al., 2006; Mulic et al., 2012). Comprehensive information is available on exercisedependent changes of salivary components (e.g., proteins and hormones), as well as on stimulated and unstimulated flow rates (Ljungberg et al., 1997; Blannin et al., 1998; Horswill et al., 2006; Gatti & De Palo, 2011; Zauber et al., 2012; Allgrove et al., 2013). It was shown that, for example, exercise significantly affects up- and down-regulation of steroid hormone levels (cortisol, testosterone, and dehydroepiandrosterone). The defined interrelation of salivary and plasma steroid hormone levels observed during exercise can be used as a diagnostic tool for the assessment of training conditions (Gatti & De Palo, 2011). In endurance sports, sport drinks, gels, energy bars, etc. are widely used for substitution and supplementation of electrolytes and carbohydrates before, during, and after exercise (Kenefick & Cheuvront, 2012). During endurance exercise, a fluid and electrolyte deficit because of water and sweat loss may affect exercise performance (Maughan & Shirreffs, 2010). With regard
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Frese et al. to oral health, it is common knowledge that frequent consumption of carbohydrates leads to pH drops in the oral environment causing tooth demineralization and subsequent caries lesion development (Gustafsson et al., 1954). The consumption of acidic beverages may cause a low-pH environment hereby being the cause of tooth wear in the form of dental erosions. The negative effect of acidic and high-carbohydrate nutrition might be aggravated by an attenuated saliva flow rate during exercise causing a dry mouth (Blannin et al., 1998; Phillips et al., 2011) Several investigations evaluated the relationship between sport drinks and tooth erosion (Mathew et al., 2002; Coombes, 2005; Wongkhantee et al., 2006; El Aidi et al., 2011; Min et al., 2011; Li et al., 2012; Lussi et al., 2012) revealing controversial results for the assessment of athletes’ risks for erosive tooth wear. Thus, the purpose of the present study was to compare a group of individuals practicing endurance sports (triathlon training) with a group of matched, non-exercising individuals in a standardized clinical setup to determine the potential impact of endurance training on oral health. It was hypothesized that endurance training could affect oral health with special regard to dental erosion, caries, and salivary parameters. Materials and methods This clinical trial was conducted at the Department of Conservative Dentistry, University Hospital Heidelberg. After obtaining approval from the local ethics committee (Medical Faculty of the University of Heidelberg S-324/2012), the study was registered at the German Clinical Trials Registry Platform (DRKS00004951) that is linked to the International Clinical Trials Registry Platform of the World Health Organization. Thirty-five athletes from sport clubs around Heidelberg who perform 5 or more hours of triathlon training per week participated in the investigation. The study was officially announced in the sport clubs and athletes willing to participate were invited for study appointments. The control group was recruited from consecutive first-time patients visiting the Department for Conservative Dentistry of the University Hospital Heidelberg. Within the study setting, this was the less biased cohort closest to representative that we were able to include. Non-exercising control patients were (n = 35) matched according to the variables, gender, age, and socioeconomic status.
Inclusion and exclusion criteria The inclusion criteria of test group were participants (a) are older than 18 years; (b) gave written informed consent; (c) declare to perform a cumulative weekly training of 5 or more hours; (d) practice endurance sports such as running and non-weightbearing sports, such as cycling and swimming (disciplines are combined in an individual ratio within triathlon training); and (e) are in good general health and not restricted in practicing oral hygiene. The inclusion criteria for the controls were participants (a) are older than 18 years; (b) gave written informed consent; (c) are not practicing any endurance sports; (d) declare that if performing sports, it is clearly less than 5 h per week; and (e) are in good general health and not restricted in practicing oral hygiene. The
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exclusion criteria for test and controls were participants (a) are pregnant or nursing; (b) take part or took part in another clinical study during the last 30 days; (c) took antibiotics during the last 30 days; and (d) are dental students or dental staff members.
Questionnaire Both the test and control groups completed a self-administered questionnaire with regard to the participants’ age, gender, height, body weight, and oral hygiene regime. Athletes were asked about their cumulative weekly training time (separated into running, swimming, and cycling) and years of sports activity. Type of beverage (water, sports drink, nothing) and sports nutrition (carbohydrate gels, bars) were specified. Frequency, total amount of drinking (mL per hour) and nutrition during training was recorded.
Oral assessment Two calibrated examiners performed the standardized clinical examination on clean and dry teeth. It was not feasible to blind examiners with regard to test and controls, since the appearance of athletes (figure, muscular mass, and clothes) was obvious to the investigators. It was decided to check ambiguous intraoral findings mutually to find consensus for both examiners. The study protocol included anamnesis in written form, intraoral inspection, standardized photographs, and a saliva test (see below). The prevalence and severity of dental erosions were assessed by the four-level Basic Erosive Wear Examination (BEWE). Scores 0 to 3 are depicted in Fig. 1(a–d). The most severely affected surface of each sextant was recorded and the cumulative score sum was calculated and transferred into an individual risk level (Table 1; Bartlett et al., 2008). Intraoral examination was done using a dental operating light, plain mirrors, and diagnostic probes. For assessment of caries prevalence, the DMFT (Decayed Missing Filled Teeth) and DMFS (Decayed Missing Filled Surfaces) indices were calculated (Klein et al., 1938).
Saliva assessment during inactivity For standardization of the saliva assessment test and control, participants (n = 35, each) were asked to omit tooth brushing, drinking, eating, chewing gums/lozenges, and smoking 45 min prior to the saliva assessment. A commercially available test kit was used (Saliva Check Buffer, GC EUROPE, Leuven, Belgium). Paper pH strips were used for the determination of saliva pH with a drop of unstimulated saliva. The stimulated quantity was determined by collecting saliva while chewing a piece of wax for 5 min. The diagnostic value of the collection of stimulated samples is representative for the level of activation of the salivary glands by an external stimulus such as chewing or drinking. Unstimulated samples are intended to represent the secretory capacity of salivary glands without any external stimuli. Stimulated salivary flow rates below 0.7 mL per min are considered as lowered (Holbrook et al., 2009). The buffering capacity was determined by using the manufacturer’s test pad strips, color chart, and 12-point rating scale (0–5, very low buffering capacity; 6–9, low buffering capacity; 10–12, normal/high buffering capacity). Expenditure of time for the test averages to 15 min.
Saliva assessment during exercise A subsample of 15 athletes volunteered for saliva assessment during an incremental running field test (IRFT). Athletes were asked to omit hard exercise for a minimum of 3 days prior to the
Endurance sports and oral health (a)
(b)
(c)
(d)
Fig. 1. Clinical photographs of the BEWE score 0–3. (a) BEWE score 0: intact surface contour, morphological signs of fissures, and pits are clearly visible; (b) BEWE score 1: initial loss of enamel and surface contour, smooth surface, and partial loss of fissures and pits; (c) BEWE score 2: moderate loss of enamel and surface contour, arrow is marking shallow concavities where dentine is visible, morphological loss of cusps, fissures, and pits; (d) BEWE score 3: distinct loss of enamel and dentine, complete loss of surface contour, dentine is visible, complete loss of cusps, fissures, and pits. Table 1. Basic Erosive Wear Examination (BEWE) with four levels grading the most severely affected tooth surfaces in each sextant (according to Bartlett et al., 2008)
BEWE score in each sextant
Clinical symptoms
0 1 2*
No erosive tooth wear Initial loss of surface texture Distinct defect, hard tissue loss < 50% of the surface area Hard tissue loss ≥ 50% of the surface area
3* Cumulative BEWE score† (sum of all sextants)
Risk level
≤2 3–8 9–13 ≥ 14
No risk for dental erosion Low risk for dental erosion Medium risk for dental erosion High risk for dental erosion
*In scores 2 and 3, dentine can be involved. † Cumulative assessment of all sextants allows for individual risk assessment.
IRFT. The IRFT was performed on a 400 m outdoor field track (synthetic surface) with a distance stage of 1200 m. Cones were placed on the track every 100 m as reference. The test starts at 8 km/h and increases every 1200 m distance stage by 2 km/h until
exhaustion. The running pace is controlled by a timing audio cue (beep), which determines the running speed marked by the cones. The test ended when the subject no longer maintained the required speed dictated by the audio beep. The complete saliva assessment (see above “Saliva assessment during inactivity”) was carried out 5 min prior to and 5 min after the IRFT. Athletes were asked to omit drinking and eating as long as the saliva assessment during exercise was performed. To monitor saliva flow rate during the IRFT, a quick saliva assessment was carried out at minimum (8 km/h) and maximum workload. It comprised assessment of unstimulated saliva flow for 1 min during the break between the steps of the IRFT. Unstimulated saliva was collected in a plastic container and weighed on a highly sensitive balance (Sartorius research, type R 300S; Sartorius AG, Göttingen, Germany) before and immediately after collection to assess saliva volume (mg). The saliva density was assumed to be 1.0 g/mL (Allgrove et al., 2013). Saliva pH and buffering capacity were measured 5 min before IRFT, at minimum and maximum workload (only pH) and 5 min post-exhaustion.
The pH of swimming pools Athletes trained in three different indoor swimming pools around Heidelberg. We determined the pH of the swimming pools by means of a pH-meter (MA 235 pH/ion Analyzer, Mettler Toledo International Inc., Greifensee, Switzerland). They were at pH of 6.8, 6.8, and 7.0.
Statistical analysis The data were analyzed using descriptive statistics evaluating means and standard deviations. Pairwise comparisons between
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Frese et al. Table 2. Clinical data and questionnaire information from test and controls, descriptive statistics multiple comparisons are displayed
Label
Age (years) Size (cm) Body weight (kg) Body mass index (BMI) BEWE score maxilla BEWE score mandible BEWE score cumulative DMFT DMFS Saliva pH at rest Stimulated saliva flow rate at rest (mL per min) Frequency of tooth brushing per day
Test (n = 35)
Control (n = 35)
P value
Mean
SD
Mean
SD
36.8 178.0 73.2 22.9 4.8 4.8 9.6 9.4 25.5 6.8 1.8 2.1
7.2 8.1 13.3 2.7 1.4 1.2 2.3 5.3 18.7 0.5 0.7 0.4
36.1 181.0 83.5 25.2 3.5 3.8 7.3 8.6 23.2 6.7 1.8 2.0
7.6 9.4 18.4 4.3 0.9 0.9 1.5 5.3 18.7 0.5 0.7 0.4
0.69 0.16 0.01 0.01 < 0.0001 0.0004 0.001 0.51 0.61 0.71 0.72 0.76
BEWE, Basic Erosive Wear Examination; DMFS, Decayed Missing Filled Surfaces, DMFT, Decayed Missing Filled Teeth; SD, standard deviation.
test and control groups were made using t-test or U-test procedures and categorical data were compared using the χ2 test. A multivariate regression model was performed, to determine influential dental erosion parameters. In the test and control groups, correlations were assessed for the variables BEWE, DMFT, DMFS, and saliva pH by means of the Spearman correlation coefficient (r). Two-sided P values < 0.05 were considered statistically significant. Because of the exploratory nature of the study, no adjustment was made for multiple testing. The data were processed using the SAS statistical package (Version 9.2, SAS Institute Inc., Cary, North Carolina, USA) and R 2.15.2 (www .r-project.org).
Results General data Of the 35 athletes, 24 were male. The mean age of the athletes was 36.8 ± 7.2 years (range 21–48 years). The mean age of controls was 36.1 ± 7.6 years (range 23–52 years). Athletes showed a significantly lower body weight (P = 0.01) and a lower body mass index (BMI; P = 0.01) than controls (Table 2).
Fig. 2. Scatterplot of Spearman correlation in the test group showing positive correlation of DMFT vs cumulative weekly training time (h) (r = 0.347, P = 0.04). The slope of the regression line is m = 0.24. An increase of endurance training of 1 h/ week raises the DMFT in value 0.24.
Caries and dental erosion Athletes mean cumulative BEWE score of 9.6 ± 2.3 was significantly higher than that of controls (7.3 ± 1.5, P = 0.001). The athletes cumulative BEWE score of 9.6 represents a medium risk level for dental erosion whereas the nonathletes score of 7.3 represents a low risk level (see Table 1 and Fig. 1(a–d); Bartlett et al., 2008). Athletes and controls showed similar caries prevalence of 9.4 vs 8.6 decayed, missing or filled teeth (P = 0.51). In the group of athletes, a significant correlation was found between the DMFT and the cumulative weekly training time. An increase of endurance training of 1 h/week raises the DMFT in value 0.24. (r = 0.347, P = 0.04, Fig. 2). Multivariate logistic regression analysis in the test group showed that neither the kind of beverage consumed during exercise [P = 0.542, odds ratio (OR): 1.651, 95% confidence interval (CI; 0.329,
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8.274)], nor the years of sports activity [P = 0.574, OR: 0.962, 95% CI (0.840, 1.101)] or the total amount of drinking during exercise [P = 0.233, OR: 1.002, 95% CI *(0.999, 1.006)] (mL per hour) had a significant impact on the severity of dental erosion at the medium risk level (cumulative BEWE score 9–13, Table 1). Questionnaire Athletes perform a cumulative weekly training of 9.5 ± 3.7 h per week, including 3.2 ± 1.3 h of running, 4.5 ± 2.7 h of cycling and 1.8 ± 1.3 h of swimming. 45.7% consumed sports drinks, 51.4% water, and 2.9% no drinks during exercise. The mean total amount of drinking was 592.9 ± 279.0 mL per hour (range 0.0– 1500.0 mL per hour). The consumption of sports
Endurance sports and oral health nutrition (gels and bars) was reported by 74% of the athletes. Subgroup analysis yielded no significant influence of sports nutrition intake on DMFT (P = 0.48), DMFS (P = 0.23), and dental erosion, BEWE (P = 0.35).
(a)
Saliva assessment during inactivity The mean stimulated saliva flow rate was equally high in both groups (1.8 ± 0.7 mL per min). Saliva pH yielded similar neutral values in both groups (6.8 ± 0.5 athletes, 6.7 ± 0.6 controls) (Table 2).
(b)
Saliva assessment during exercise The mean duration time of the IRFT was 36:26 ± 5:02 min. Stimulated saliva flow rate was significantly lower after than 5 min before IRFT (P = 0.001, Fig. 3a). Also, unstimulated saliva flow rate decreased from minimum workload (8 km/h) to maximum workload significantly (P = 0.01; Fig. 3b). Saliva pH increased throughout the IRFT and the pH at maximum workload was significantly higher than 5 min before the IRFT (P = 0.003). Five minutes post-exhaustion, the pH decreased toward the starting value (Fig. 4). Buffering capacity measured 5 min before exercise and 5 min postexhaustion was normal/high, respectively (P = 0.54, Table 3).
Fig. 3. (a) Mean change of stimulated saliva flow rate (mL/min) measured 5 min before exercise and 5 min post-exhaustion during IRFT (n = 15); P = 0.001. (b) Mean change of unstimulated saliva flow rate (mL/min) from minimum to maximum workload during IRFT (n = 15); P = 0.01.
Fig. 4. Saliva pH during IRFT (mean ± SD); **P = 0.003.
Table 3. Saliva and physiological parameters during IRFT [mean ± standard deviation (SD)]
Buffering capacity (0 to 12 rating scale) Heart rate (beats/min) Lactate (mmol/L)
5 min before exercise
Minimum workload
Maximum workload
5 min post-exhaustion
P values
10.33 (1.74)
–
–
10.07 (1.61)
0.54
–
125 (14) 1.18 (0.38)
184 (14) 8.31 (2.40)
0.94 (0.22)
108 (32) 8.01 (2.59)
– –
The buffering capacity was determined by a 12-point rating scale: 0–5, very low buffering capacity; 6–9, low buffering capacity; 10–12, normal/high buffering capacity. IRFT, incremental running field test.
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Frese et al. Discussion In the present study, a group of triathletes were compared with a matched control group evaluating caries risk, erosion, and salivary parameters. This study showed that, although positive effects of endurance training relating to body weight and BMI are observed, the oral health of individuals practicing endurance sports might be affected by an increased risk for dental erosion. There are several investigations on the association of sports exercise and dental erosion (Mathew et al., 2002; Sirimaharaj et al., 2002; Venables et al., 2005; Lussi & Jaeggi, 2008; Bryant et al., 2011; Phillips et al., 2011). In a recent case-controlled study investigating participants who worked out at a fitness center (Mulic et al., 2012), it was shown that a majority of those physically active young adults had erosive lesions. Furthermore, it was shown that participants with reduced stimulated salivary flow rate after exercise revealed significantly more erosive wear indicating that hard exercise and decreased stimulated salivary flow rates might be associated herewith. Evaluating athletes’ caries, one exploratory study from New Zealand provides preliminary results. Elite triathletes responded to a questionnaire, and 10 randomly selected subjects underwent clinical oral investigation (Bryant et al., 2011). A high caries risk for elite triathletes was revealed. However, with special regard to endurance sports, there are no comprehensive clinical studies assessing its impact on oral health with special regard to diseases of the dental hard tissue and saliva. During inactivity, no differences in stimulated saliva flow rates and pH were observed between athletes and controls. Yet, a significant exercise-dependent shift of parameters revealed a decrease in stimulated and unstimulated saliva flow rates and an increase in saliva pH at maximum workload (Figs. 3(a–b) and 4). Notably, the absolute values of stimulated saliva before [1.8 (0.7) mL/min] and after IRFT [1.1 (0.4) mL/min] are above and within physiological range, respectively. The reasons for the significant decrease from before to after the IRFT are due to an increase in sympathetic activity and a repression of the cholinergic parasympathetic innervation causing a significant vasoconstriction in salivary glands (Proctor & Carpenter, 2007). Fluid and electrolyte deficit as a consequence to water and sweat loss might add to the effect (Mulic et al., 2012; Allgrove et al., 2013). The significant increase of saliva pH at exhaustion, however, suggests a compensatory reaction in order to balance prior deficit of saliva (Fig. 4). These alterations in saliva flow rates are in line with previous investigations (Mulic et al., 2012; Allgrove et al., 2013). Interestingly, in different participants, Mulic et al. showed not only a decrease, but also an increase in stimulated and unstimulated saliva flow rates. This was also seen in our subsample where three participants
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showed an increase of unstimulated saliva flow rate from minimum to maximum workload (Fig. 3(b)). During exercise, the composition of saliva is altered leading to an increase of proteins such as immunoglobulins and metabolites with antioxidant functions (Ljungberg et al., 1997; Blannin et al., 1998; Zauber et al., 2012). Therefore, it might be assumed that with regard to its protective function of dental hard tissue, saliva might have an impaired function during exercise. At this point, it seems necessary to point out the function of the so-called acquired enamel pellicle (AEP), which is a saliva-based layer of glycoproteins covering tooth surfaces in the oral cavity. It was suggested that it has an erosion-inhibiting potential, thus playing a role in preventing dental erosions (Wetton et al., 2006; Cheaib & Lussi, 2011). The higher prevalence of dental erosion in athletes indicates that the alterations of saliva composition during and because of endurance training might account for a defective AEP formation resulting in restricted or completely deficient protective function (Hara et al., 2006). Thus, it might be possible that during intense exercise, even water with neutral pH, as a beverage or in a swimming pool, might have detrimental effects on sound tooth structure. Two main explanatory concepts for the higher prevalence of dental erosion are discussed: first the impact of low-pH sports nutrition and drinks; and second, the altered salivary parameters during and because of high-impact exercise. Commercially available sports drinks have a pH ranging from 3.2 to 3.7, and a buffering capacity of 43.0–56.5 (mmol/OH- per L to pH 7; Lussi et al., 2012). A consumption of 1 L per hour or 1 g per min has been shown to help maintain the blood glucose levels and exercise performance (Kenefick & Cheuvront, 2012). The frequent consumption of sports drinks by 55.3–91.3% of athletes has been reported (Mathew et al., 2002; Sirimaharaj et al., 2002; Bryant et al., 2011). A recent meta-analysis, however, found no association between sports drinks and dental erosion (Li et al., 2012). Accordingly, we could not identify any of the parameters investigated here [type of beverage, years of sports activity, total amount of drinking (mL per hour)] to have significant influence on the severity of dental erosions at the medium risk level. In the present investigation, the caries prevalence of athletes and controls was similar. Although this is deviant from other studies (Bryant et al., 2011; Needleman et al., 2013), our study notably included a matched control group allowing for comparison with a representative cohort. Even though caries prevalence was not different from controls, a positive correlation between cumulative weekly training time and caries prevalence in athletes was seen (P = 0.04, Fig. 2). The subgroup analysis of the positive and negative reports on carbohydrate consumption (sports gels, bars) in athletes yielded no significant influence on caries prevalence. Our results emphasize, that rather the duration of
Endurance sports and oral health physical exercise, which is understandably associated with an increased frequency of nutritional intake (Maughan & Shirreffs, 2010; Phillips et al., 2011), had a significant impact on caries prevalence. Critical considerations on weaknesses and limitations of the study yield the following: even though an acceptable number of test and controls were included, an explanatory analysis of data was not possible. In contrast to caries assessment, which is an elementary and robust method in dentistry, the assessment of dental erosions using the BEWE might be biased by diagnostic uncertainties. We have tried to address this problem by involving two calibrated examiners to gain increased reliability. The BEWE is, to date, the scientifically most recommended scoring system for dental erosions (Olley et al., 2013). We see the inclusion of a matched control group as strength of our investigation. Furthermore, the saliva testing protocol was fundamentally enhanced on the basis of critical aspects existing in prior investigations such as eating and drinking prior to saliva assessment or during exercise performance when saliva samples were collected (Horswill et al., 2006; Mulic et al., 2012; Allgrove et al., 2013). In conclusion, the data from the present investigation strengthens the association between sports exercise and dental erosion. Endurance training influenced saliva flow rate and pH during exercise. An association of endurance sports and poor oral health in the form of high caries prevalence was not seen in this cohort. Longer
cumulative weekly training time, however, was associated with higher caries prevalence. Perspectives Based on these findings, it can be suggested that endurance training has detrimental effects on oral health. They are enhanced by kind, frequency and amount of nutritional intake during exercise. Further research is needed to understand the role of saliva and its impact on oral health during exercise. Additionally, there is a need for exercise-adjusted oral hygiene regimes and nutritional modifications in the field of sports dentistry. Key words: Caries risk, physical endurance, saliva, tooth erosion.
Acknowledgements We would like to thank all the athletes who participated in this study. We thank Prof. B. Friedmann-Bette, Department of Sports Medicine, Medical Clinic, University Hospital Heidelberg for providing her expertise. We thank Tanja Krüger, Hye-Min Hong, Maria Inceoglu, Simona Schick from the Department of Conservative Dentistry, University Hospital Heidelberg for personal support during the incremental running field test. We would also like to thank GC EUROPE, Leuven, Belgium, and the GABA International AG, Therwil Switzerland for providing saliva test kits and gifts for study participants.
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Scand J Med Sci Sports 2014: ••: ••–•• doi: 10.1111/sms.12266
Published by John Wiley & Sons Ltd
Effect of endurance training on dental erosion, caries, and saliva C. Frese1, F. Frese2, S. Kuhlmann1, D. Saure3, D. Reljic2, H. J. Staehle1, D. Wolff1 1
Department of Conservative Dentistry, School of Dental Medicine, University Hospital Heidelberg, Heidelberg, Germany, Department of Sports Medicine, Medical Clinic, University Hospital Heidelberg, Heidelberg, Germany, 3Institute of Medical Biometry and Informatics, Ruprecht Karls University, Heidelberg, Germany Corresponding author: Cornelia Frese, DDS, Department of Conservative Dentistry, Dental School, University Hospital Heidelberg, Im Neuenheimer Feld 400, 69120 Heidelberg, Germany. Tel: +49 6221 5639889, Fax: +49 6221 565074, E-mail: [email protected]
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Accepted for publication 9 May 2014
The aim of this investigation was to give insights into the impact of endurance training on oral health, with regard to tooth erosion, caries, and salivary parameters. The study included 35 triathletes and 35 non-exercising controls. The clinical investigation comprised oral examination, assessment of oral status with special regard to caries and erosion, saliva testing during inactivity, and a self-administered questionnaire about eating, drinking, and oral hygiene behavior. In addition, athletes were asked about their training habits and intake of beverages and sports nutrition. For saliva assessment during exercise, a subsample of n = 15 athletes volunteered in an incremental running field test (IRFT). Athletes showed an
increased risk for dental erosion (P = 0.001). No differences were observed with regard to caries prevalence and salivary parameters measured during inactivity between athletes and controls. Among athletes, a significant correlation was found between caries prevalence and the cumulative weekly training time (r = 0.347, P = 0.04). In athletes after IRFT and at maximum workload, saliva flow rates decreased (P = 0.001 stimulated; P = 0.01 unstimulated) and saliva pH increased significantly (P = 0.003). Higher risk for dental erosions, exercisedependent caries risk, and load-dependent changes in saliva parameters point out the need for risk-adapted preventive dental concepts in the field of sports dentistry.
Today, endurance sports have become increasingly popular among amateurs. Because of their unique training and nutritional habits, it is likely that they are at different risk levels for oral health compared with average non-exercising people. Special attention should be paid on oral diseases such as erosive tooth wear and dental caries, as well as on the changes in salivary parameters. However, their special needs with regard to dental care and oral hygiene education have not yet been considered appropriately in dental research. And although one may presume that athletes might have more precise physical (and oral) perception than nonexercising people, a recent study showed that 302 athletes participating in the London 2012 Olympic Games displayed poor oral health with comparably high prevalence of dental erosions, caries, and periodontitis (Needleman et al., 2013). Data on exercise-dependent alterations of salivary parameters with special regard to the impact on dental erosions and caries are rare (Horswill et al., 2006; Phillips et al., 2011; Mulic et al., 2012). Investigations showed that a great number of athletes presented signs of tooth erosion. There is also evidence that the performance of exercise decreased salivary flow rates and
salivary pH increased or decreased dependent on the beverages consumed by the athletes. A decreased salivary pH might be associated with tooth wear (Horswill et al., 2006; Mulic et al., 2012). Comprehensive information is available on exercisedependent changes of salivary components (e.g., proteins and hormones), as well as on stimulated and unstimulated flow rates (Ljungberg et al., 1997; Blannin et al., 1998; Horswill et al., 2006; Gatti & De Palo, 2011; Zauber et al., 2012; Allgrove et al., 2013). It was shown that, for example, exercise significantly affects up- and down-regulation of steroid hormone levels (cortisol, testosterone, and dehydroepiandrosterone). The defined interrelation of salivary and plasma steroid hormone levels observed during exercise can be used as a diagnostic tool for the assessment of training conditions (Gatti & De Palo, 2011). In endurance sports, sport drinks, gels, energy bars, etc. are widely used for substitution and supplementation of electrolytes and carbohydrates before, during, and after exercise (Kenefick & Cheuvront, 2012). During endurance exercise, a fluid and electrolyte deficit because of water and sweat loss may affect exercise performance (Maughan & Shirreffs, 2010). With regard
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Frese et al. to oral health, it is common knowledge that frequent consumption of carbohydrates leads to pH drops in the oral environment causing tooth demineralization and subsequent caries lesion development (Gustafsson et al., 1954). The consumption of acidic beverages may cause a low-pH environment hereby being the cause of tooth wear in the form of dental erosions. The negative effect of acidic and high-carbohydrate nutrition might be aggravated by an attenuated saliva flow rate during exercise causing a dry mouth (Blannin et al., 1998; Phillips et al., 2011) Several investigations evaluated the relationship between sport drinks and tooth erosion (Mathew et al., 2002; Coombes, 2005; Wongkhantee et al., 2006; El Aidi et al., 2011; Min et al., 2011; Li et al., 2012; Lussi et al., 2012) revealing controversial results for the assessment of athletes’ risks for erosive tooth wear. Thus, the purpose of the present study was to compare a group of individuals practicing endurance sports (triathlon training) with a group of matched, non-exercising individuals in a standardized clinical setup to determine the potential impact of endurance training on oral health. It was hypothesized that endurance training could affect oral health with special regard to dental erosion, caries, and salivary parameters. Materials and methods This clinical trial was conducted at the Department of Conservative Dentistry, University Hospital Heidelberg. After obtaining approval from the local ethics committee (Medical Faculty of the University of Heidelberg S-324/2012), the study was registered at the German Clinical Trials Registry Platform (DRKS00004951) that is linked to the International Clinical Trials Registry Platform of the World Health Organization. Thirty-five athletes from sport clubs around Heidelberg who perform 5 or more hours of triathlon training per week participated in the investigation. The study was officially announced in the sport clubs and athletes willing to participate were invited for study appointments. The control group was recruited from consecutive first-time patients visiting the Department for Conservative Dentistry of the University Hospital Heidelberg. Within the study setting, this was the less biased cohort closest to representative that we were able to include. Non-exercising control patients were (n = 35) matched according to the variables, gender, age, and socioeconomic status.
Inclusion and exclusion criteria The inclusion criteria of test group were participants (a) are older than 18 years; (b) gave written informed consent; (c) declare to perform a cumulative weekly training of 5 or more hours; (d) practice endurance sports such as running and non-weightbearing sports, such as cycling and swimming (disciplines are combined in an individual ratio within triathlon training); and (e) are in good general health and not restricted in practicing oral hygiene. The inclusion criteria for the controls were participants (a) are older than 18 years; (b) gave written informed consent; (c) are not practicing any endurance sports; (d) declare that if performing sports, it is clearly less than 5 h per week; and (e) are in good general health and not restricted in practicing oral hygiene. The
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exclusion criteria for test and controls were participants (a) are pregnant or nursing; (b) take part or took part in another clinical study during the last 30 days; (c) took antibiotics during the last 30 days; and (d) are dental students or dental staff members.
Questionnaire Both the test and control groups completed a self-administered questionnaire with regard to the participants’ age, gender, height, body weight, and oral hygiene regime. Athletes were asked about their cumulative weekly training time (separated into running, swimming, and cycling) and years of sports activity. Type of beverage (water, sports drink, nothing) and sports nutrition (carbohydrate gels, bars) were specified. Frequency, total amount of drinking (mL per hour) and nutrition during training was recorded.
Oral assessment Two calibrated examiners performed the standardized clinical examination on clean and dry teeth. It was not feasible to blind examiners with regard to test and controls, since the appearance of athletes (figure, muscular mass, and clothes) was obvious to the investigators. It was decided to check ambiguous intraoral findings mutually to find consensus for both examiners. The study protocol included anamnesis in written form, intraoral inspection, standardized photographs, and a saliva test (see below). The prevalence and severity of dental erosions were assessed by the four-level Basic Erosive Wear Examination (BEWE). Scores 0 to 3 are depicted in Fig. 1(a–d). The most severely affected surface of each sextant was recorded and the cumulative score sum was calculated and transferred into an individual risk level (Table 1; Bartlett et al., 2008). Intraoral examination was done using a dental operating light, plain mirrors, and diagnostic probes. For assessment of caries prevalence, the DMFT (Decayed Missing Filled Teeth) and DMFS (Decayed Missing Filled Surfaces) indices were calculated (Klein et al., 1938).
Saliva assessment during inactivity For standardization of the saliva assessment test and control, participants (n = 35, each) were asked to omit tooth brushing, drinking, eating, chewing gums/lozenges, and smoking 45 min prior to the saliva assessment. A commercially available test kit was used (Saliva Check Buffer, GC EUROPE, Leuven, Belgium). Paper pH strips were used for the determination of saliva pH with a drop of unstimulated saliva. The stimulated quantity was determined by collecting saliva while chewing a piece of wax for 5 min. The diagnostic value of the collection of stimulated samples is representative for the level of activation of the salivary glands by an external stimulus such as chewing or drinking. Unstimulated samples are intended to represent the secretory capacity of salivary glands without any external stimuli. Stimulated salivary flow rates below 0.7 mL per min are considered as lowered (Holbrook et al., 2009). The buffering capacity was determined by using the manufacturer’s test pad strips, color chart, and 12-point rating scale (0–5, very low buffering capacity; 6–9, low buffering capacity; 10–12, normal/high buffering capacity). Expenditure of time for the test averages to 15 min.
Saliva assessment during exercise A subsample of 15 athletes volunteered for saliva assessment during an incremental running field test (IRFT). Athletes were asked to omit hard exercise for a minimum of 3 days prior to the
Endurance sports and oral health (a)
(b)
(c)
(d)
Fig. 1. Clinical photographs of the BEWE score 0–3. (a) BEWE score 0: intact surface contour, morphological signs of fissures, and pits are clearly visible; (b) BEWE score 1: initial loss of enamel and surface contour, smooth surface, and partial loss of fissures and pits; (c) BEWE score 2: moderate loss of enamel and surface contour, arrow is marking shallow concavities where dentine is visible, morphological loss of cusps, fissures, and pits; (d) BEWE score 3: distinct loss of enamel and dentine, complete loss of surface contour, dentine is visible, complete loss of cusps, fissures, and pits. Table 1. Basic Erosive Wear Examination (BEWE) with four levels grading the most severely affected tooth surfaces in each sextant (according to Bartlett et al., 2008)
BEWE score in each sextant
Clinical symptoms
0 1 2*
No erosive tooth wear Initial loss of surface texture Distinct defect, hard tissue loss < 50% of the surface area Hard tissue loss ≥ 50% of the surface area
3* Cumulative BEWE score† (sum of all sextants)
Risk level
≤2 3–8 9–13 ≥ 14
No risk for dental erosion Low risk for dental erosion Medium risk for dental erosion High risk for dental erosion
*In scores 2 and 3, dentine can be involved. † Cumulative assessment of all sextants allows for individual risk assessment.
IRFT. The IRFT was performed on a 400 m outdoor field track (synthetic surface) with a distance stage of 1200 m. Cones were placed on the track every 100 m as reference. The test starts at 8 km/h and increases every 1200 m distance stage by 2 km/h until
exhaustion. The running pace is controlled by a timing audio cue (beep), which determines the running speed marked by the cones. The test ended when the subject no longer maintained the required speed dictated by the audio beep. The complete saliva assessment (see above “Saliva assessment during inactivity”) was carried out 5 min prior to and 5 min after the IRFT. Athletes were asked to omit drinking and eating as long as the saliva assessment during exercise was performed. To monitor saliva flow rate during the IRFT, a quick saliva assessment was carried out at minimum (8 km/h) and maximum workload. It comprised assessment of unstimulated saliva flow for 1 min during the break between the steps of the IRFT. Unstimulated saliva was collected in a plastic container and weighed on a highly sensitive balance (Sartorius research, type R 300S; Sartorius AG, Göttingen, Germany) before and immediately after collection to assess saliva volume (mg). The saliva density was assumed to be 1.0 g/mL (Allgrove et al., 2013). Saliva pH and buffering capacity were measured 5 min before IRFT, at minimum and maximum workload (only pH) and 5 min post-exhaustion.
The pH of swimming pools Athletes trained in three different indoor swimming pools around Heidelberg. We determined the pH of the swimming pools by means of a pH-meter (MA 235 pH/ion Analyzer, Mettler Toledo International Inc., Greifensee, Switzerland). They were at pH of 6.8, 6.8, and 7.0.
Statistical analysis The data were analyzed using descriptive statistics evaluating means and standard deviations. Pairwise comparisons between
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Frese et al. Table 2. Clinical data and questionnaire information from test and controls, descriptive statistics multiple comparisons are displayed
Label
Age (years) Size (cm) Body weight (kg) Body mass index (BMI) BEWE score maxilla BEWE score mandible BEWE score cumulative DMFT DMFS Saliva pH at rest Stimulated saliva flow rate at rest (mL per min) Frequency of tooth brushing per day
Test (n = 35)
Control (n = 35)
P value
Mean
SD
Mean
SD
36.8 178.0 73.2 22.9 4.8 4.8 9.6 9.4 25.5 6.8 1.8 2.1
7.2 8.1 13.3 2.7 1.4 1.2 2.3 5.3 18.7 0.5 0.7 0.4
36.1 181.0 83.5 25.2 3.5 3.8 7.3 8.6 23.2 6.7 1.8 2.0
7.6 9.4 18.4 4.3 0.9 0.9 1.5 5.3 18.7 0.5 0.7 0.4
0.69 0.16 0.01 0.01 < 0.0001 0.0004 0.001 0.51 0.61 0.71 0.72 0.76
BEWE, Basic Erosive Wear Examination; DMFS, Decayed Missing Filled Surfaces, DMFT, Decayed Missing Filled Teeth; SD, standard deviation.
test and control groups were made using t-test or U-test procedures and categorical data were compared using the χ2 test. A multivariate regression model was performed, to determine influential dental erosion parameters. In the test and control groups, correlations were assessed for the variables BEWE, DMFT, DMFS, and saliva pH by means of the Spearman correlation coefficient (r). Two-sided P values < 0.05 were considered statistically significant. Because of the exploratory nature of the study, no adjustment was made for multiple testing. The data were processed using the SAS statistical package (Version 9.2, SAS Institute Inc., Cary, North Carolina, USA) and R 2.15.2 (www .r-project.org).
Results General data Of the 35 athletes, 24 were male. The mean age of the athletes was 36.8 ± 7.2 years (range 21–48 years). The mean age of controls was 36.1 ± 7.6 years (range 23–52 years). Athletes showed a significantly lower body weight (P = 0.01) and a lower body mass index (BMI; P = 0.01) than controls (Table 2).
Fig. 2. Scatterplot of Spearman correlation in the test group showing positive correlation of DMFT vs cumulative weekly training time (h) (r = 0.347, P = 0.04). The slope of the regression line is m = 0.24. An increase of endurance training of 1 h/ week raises the DMFT in value 0.24.
Caries and dental erosion Athletes mean cumulative BEWE score of 9.6 ± 2.3 was significantly higher than that of controls (7.3 ± 1.5, P = 0.001). The athletes cumulative BEWE score of 9.6 represents a medium risk level for dental erosion whereas the nonathletes score of 7.3 represents a low risk level (see Table 1 and Fig. 1(a–d); Bartlett et al., 2008). Athletes and controls showed similar caries prevalence of 9.4 vs 8.6 decayed, missing or filled teeth (P = 0.51). In the group of athletes, a significant correlation was found between the DMFT and the cumulative weekly training time. An increase of endurance training of 1 h/week raises the DMFT in value 0.24. (r = 0.347, P = 0.04, Fig. 2). Multivariate logistic regression analysis in the test group showed that neither the kind of beverage consumed during exercise [P = 0.542, odds ratio (OR): 1.651, 95% confidence interval (CI; 0.329,
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8.274)], nor the years of sports activity [P = 0.574, OR: 0.962, 95% CI (0.840, 1.101)] or the total amount of drinking during exercise [P = 0.233, OR: 1.002, 95% CI *(0.999, 1.006)] (mL per hour) had a significant impact on the severity of dental erosion at the medium risk level (cumulative BEWE score 9–13, Table 1). Questionnaire Athletes perform a cumulative weekly training of 9.5 ± 3.7 h per week, including 3.2 ± 1.3 h of running, 4.5 ± 2.7 h of cycling and 1.8 ± 1.3 h of swimming. 45.7% consumed sports drinks, 51.4% water, and 2.9% no drinks during exercise. The mean total amount of drinking was 592.9 ± 279.0 mL per hour (range 0.0– 1500.0 mL per hour). The consumption of sports
Endurance sports and oral health nutrition (gels and bars) was reported by 74% of the athletes. Subgroup analysis yielded no significant influence of sports nutrition intake on DMFT (P = 0.48), DMFS (P = 0.23), and dental erosion, BEWE (P = 0.35).
(a)
Saliva assessment during inactivity The mean stimulated saliva flow rate was equally high in both groups (1.8 ± 0.7 mL per min). Saliva pH yielded similar neutral values in both groups (6.8 ± 0.5 athletes, 6.7 ± 0.6 controls) (Table 2).
(b)
Saliva assessment during exercise The mean duration time of the IRFT was 36:26 ± 5:02 min. Stimulated saliva flow rate was significantly lower after than 5 min before IRFT (P = 0.001, Fig. 3a). Also, unstimulated saliva flow rate decreased from minimum workload (8 km/h) to maximum workload significantly (P = 0.01; Fig. 3b). Saliva pH increased throughout the IRFT and the pH at maximum workload was significantly higher than 5 min before the IRFT (P = 0.003). Five minutes post-exhaustion, the pH decreased toward the starting value (Fig. 4). Buffering capacity measured 5 min before exercise and 5 min postexhaustion was normal/high, respectively (P = 0.54, Table 3).
Fig. 3. (a) Mean change of stimulated saliva flow rate (mL/min) measured 5 min before exercise and 5 min post-exhaustion during IRFT (n = 15); P = 0.001. (b) Mean change of unstimulated saliva flow rate (mL/min) from minimum to maximum workload during IRFT (n = 15); P = 0.01.
Fig. 4. Saliva pH during IRFT (mean ± SD); **P = 0.003.
Table 3. Saliva and physiological parameters during IRFT [mean ± standard deviation (SD)]
Buffering capacity (0 to 12 rating scale) Heart rate (beats/min) Lactate (mmol/L)
5 min before exercise
Minimum workload
Maximum workload
5 min post-exhaustion
P values
10.33 (1.74)
–
–
10.07 (1.61)
0.54
–
125 (14) 1.18 (0.38)
184 (14) 8.31 (2.40)
0.94 (0.22)
108 (32) 8.01 (2.59)
– –
The buffering capacity was determined by a 12-point rating scale: 0–5, very low buffering capacity; 6–9, low buffering capacity; 10–12, normal/high buffering capacity. IRFT, incremental running field test.
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Frese et al. Discussion In the present study, a group of triathletes were compared with a matched control group evaluating caries risk, erosion, and salivary parameters. This study showed that, although positive effects of endurance training relating to body weight and BMI are observed, the oral health of individuals practicing endurance sports might be affected by an increased risk for dental erosion. There are several investigations on the association of sports exercise and dental erosion (Mathew et al., 2002; Sirimaharaj et al., 2002; Venables et al., 2005; Lussi & Jaeggi, 2008; Bryant et al., 2011; Phillips et al., 2011). In a recent case-controlled study investigating participants who worked out at a fitness center (Mulic et al., 2012), it was shown that a majority of those physically active young adults had erosive lesions. Furthermore, it was shown that participants with reduced stimulated salivary flow rate after exercise revealed significantly more erosive wear indicating that hard exercise and decreased stimulated salivary flow rates might be associated herewith. Evaluating athletes’ caries, one exploratory study from New Zealand provides preliminary results. Elite triathletes responded to a questionnaire, and 10 randomly selected subjects underwent clinical oral investigation (Bryant et al., 2011). A high caries risk for elite triathletes was revealed. However, with special regard to endurance sports, there are no comprehensive clinical studies assessing its impact on oral health with special regard to diseases of the dental hard tissue and saliva. During inactivity, no differences in stimulated saliva flow rates and pH were observed between athletes and controls. Yet, a significant exercise-dependent shift of parameters revealed a decrease in stimulated and unstimulated saliva flow rates and an increase in saliva pH at maximum workload (Figs. 3(a–b) and 4). Notably, the absolute values of stimulated saliva before [1.8 (0.7) mL/min] and after IRFT [1.1 (0.4) mL/min] are above and within physiological range, respectively. The reasons for the significant decrease from before to after the IRFT are due to an increase in sympathetic activity and a repression of the cholinergic parasympathetic innervation causing a significant vasoconstriction in salivary glands (Proctor & Carpenter, 2007). Fluid and electrolyte deficit as a consequence to water and sweat loss might add to the effect (Mulic et al., 2012; Allgrove et al., 2013). The significant increase of saliva pH at exhaustion, however, suggests a compensatory reaction in order to balance prior deficit of saliva (Fig. 4). These alterations in saliva flow rates are in line with previous investigations (Mulic et al., 2012; Allgrove et al., 2013). Interestingly, in different participants, Mulic et al. showed not only a decrease, but also an increase in stimulated and unstimulated saliva flow rates. This was also seen in our subsample where three participants
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showed an increase of unstimulated saliva flow rate from minimum to maximum workload (Fig. 3(b)). During exercise, the composition of saliva is altered leading to an increase of proteins such as immunoglobulins and metabolites with antioxidant functions (Ljungberg et al., 1997; Blannin et al., 1998; Zauber et al., 2012). Therefore, it might be assumed that with regard to its protective function of dental hard tissue, saliva might have an impaired function during exercise. At this point, it seems necessary to point out the function of the so-called acquired enamel pellicle (AEP), which is a saliva-based layer of glycoproteins covering tooth surfaces in the oral cavity. It was suggested that it has an erosion-inhibiting potential, thus playing a role in preventing dental erosions (Wetton et al., 2006; Cheaib & Lussi, 2011). The higher prevalence of dental erosion in athletes indicates that the alterations of saliva composition during and because of endurance training might account for a defective AEP formation resulting in restricted or completely deficient protective function (Hara et al., 2006). Thus, it might be possible that during intense exercise, even water with neutral pH, as a beverage or in a swimming pool, might have detrimental effects on sound tooth structure. Two main explanatory concepts for the higher prevalence of dental erosion are discussed: first the impact of low-pH sports nutrition and drinks; and second, the altered salivary parameters during and because of high-impact exercise. Commercially available sports drinks have a pH ranging from 3.2 to 3.7, and a buffering capacity of 43.0–56.5 (mmol/OH- per L to pH 7; Lussi et al., 2012). A consumption of 1 L per hour or 1 g per min has been shown to help maintain the blood glucose levels and exercise performance (Kenefick & Cheuvront, 2012). The frequent consumption of sports drinks by 55.3–91.3% of athletes has been reported (Mathew et al., 2002; Sirimaharaj et al., 2002; Bryant et al., 2011). A recent meta-analysis, however, found no association between sports drinks and dental erosion (Li et al., 2012). Accordingly, we could not identify any of the parameters investigated here [type of beverage, years of sports activity, total amount of drinking (mL per hour)] to have significant influence on the severity of dental erosions at the medium risk level. In the present investigation, the caries prevalence of athletes and controls was similar. Although this is deviant from other studies (Bryant et al., 2011; Needleman et al., 2013), our study notably included a matched control group allowing for comparison with a representative cohort. Even though caries prevalence was not different from controls, a positive correlation between cumulative weekly training time and caries prevalence in athletes was seen (P = 0.04, Fig. 2). The subgroup analysis of the positive and negative reports on carbohydrate consumption (sports gels, bars) in athletes yielded no significant influence on caries prevalence. Our results emphasize, that rather the duration of
Endurance sports and oral health physical exercise, which is understandably associated with an increased frequency of nutritional intake (Maughan & Shirreffs, 2010; Phillips et al., 2011), had a significant impact on caries prevalence. Critical considerations on weaknesses and limitations of the study yield the following: even though an acceptable number of test and controls were included, an explanatory analysis of data was not possible. In contrast to caries assessment, which is an elementary and robust method in dentistry, the assessment of dental erosions using the BEWE might be biased by diagnostic uncertainties. We have tried to address this problem by involving two calibrated examiners to gain increased reliability. The BEWE is, to date, the scientifically most recommended scoring system for dental erosions (Olley et al., 2013). We see the inclusion of a matched control group as strength of our investigation. Furthermore, the saliva testing protocol was fundamentally enhanced on the basis of critical aspects existing in prior investigations such as eating and drinking prior to saliva assessment or during exercise performance when saliva samples were collected (Horswill et al., 2006; Mulic et al., 2012; Allgrove et al., 2013). In conclusion, the data from the present investigation strengthens the association between sports exercise and dental erosion. Endurance training influenced saliva flow rate and pH during exercise. An association of endurance sports and poor oral health in the form of high caries prevalence was not seen in this cohort. Longer
cumulative weekly training time, however, was associated with higher caries prevalence. Perspectives Based on these findings, it can be suggested that endurance training has detrimental effects on oral health. They are enhanced by kind, frequency and amount of nutritional intake during exercise. Further research is needed to understand the role of saliva and its impact on oral health during exercise. Additionally, there is a need for exercise-adjusted oral hygiene regimes and nutritional modifications in the field of sports dentistry. Key words: Caries risk, physical endurance, saliva, tooth erosion.
Acknowledgements We would like to thank all the athletes who participated in this study. We thank Prof. B. Friedmann-Bette, Department of Sports Medicine, Medical Clinic, University Hospital Heidelberg for providing her expertise. We thank Tanja Krüger, Hye-Min Hong, Maria Inceoglu, Simona Schick from the Department of Conservative Dentistry, University Hospital Heidelberg for personal support during the incremental running field test. We would also like to thank GC EUROPE, Leuven, Belgium, and the GABA International AG, Therwil Switzerland for providing saliva test kits and gifts for study participants.
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