Exercise upregulates salivary amylase in humans (Review)

The secretion of salivary α-amylase is influenced by adrenergic regulation of the sympathetic nervous system and the hypothalamic-pituitary-adrenal axis; thus, exercise affects the levels of salivary α-amylase. Granger et al published a review in 2007 that focused attention on salivary α-amylase. In addition, a portable system for monitoring salivary α-amylase activity was launched in Japan at the end of 2005. The correlation between exercise and salivary α-amylase has since been extensively investigated. The present review summarizes relevant studies published in the English and Japanese literature after 2006. A search of the PubMed and CiNii databases identified 54 articles, from which 15 original articles were selected. The findings described in these publications indicate that exercise consistently increases mean salivary α-amylase activities and concentrations, particularly at an intensity of >70% VO2max in healthy young individuals. Thus, these studies have confirmed that salivary α-amylase levels markedly increase in response to physical stress. Salivary α-amylase levels may therefore serve as an effective indicator in the non-invasive assessment of physical stress.

1. Introduction 2. Materials and methods 3. Results and discussion

Introduction
Salivary α-amylase secretion is influenced by adrenergic regulation of the sympathetic nervous system and the hypothalamic-pituitary-adrenal axis (1). Therefore, exercise may affect salivary α-amylase levels.
Granger et al (1) published a review of biobehavioral studies of salivary α-amylase in 2007, suggesting that salivary α-amylase levels markedly increase in response to physical and psychological stress. Studies by Chatterton et al (2) and Kivlighan and Granger (3) identified that salivary α-amylase levels increased in response to exercise. Chatterton et al (2) compared levels of salivary α-amylase in males prior to and following exercise, a written examination or rest, and identified that aerobic exercise induced a three-fold mean increase in α-amylase levels. Kivlighan and Granger (3) observed that salivary α-amylase levels increased by an average of 156% in 42 members (21 females) of a collegiate crew team in response to an ergometer competition.
Following publication of the review by Granger et al (1), various groups investigated the correlation between exercise and salivary α-amylase. A portable system for monitoring salivary α-amylase activity was launched in Japan at the end of 2005 (4), which stimulated increased interest in the subject. Certain findings were only published in Japanese. The present review aims to summarize previous studies concerning the correlation between exercise and salivary α-amylase levels published in the English and Japanese literature.

Materials and methods
Information was collected from the PubMed (http://www.ncbi. nlm.nih.gov/pubmed/) and CiNii (http://ci.nii.ac.jp/) databases. The latter is a database maintained by the Japanese National Institute of Informatics (Tokyo, Japan), which comprises literature published by Japanese authors in academic journals or university memoirs and is listed in the database of the Japanese National Diet Library (Tokyo, Japan).
The search terms were ̔saliva̓, ̔amylase̓ and ̔exercise̓. Original studies published after 2006 concerning the effect of exercise on salivary α-amylase in healthy humans were selected according to the following exclusion criteria: published prior to 2006; the article was not original; the participants were not healthy; the study was intervention-based rather than exercise-based; salivary α-amylase levels/activity were not examined; the language was other than English or Japanese.
The PubMed search identified 42 studies. Fifteen reports were excluded as they were published prior to 2006. Thirteen studies were selected from the titles and abstracts of the remaining 27 publications, according to the aforementioned exclusion criteria. The CiNii search identified 12 studies. One was selected via the same procedure described for the PubMed search. Among the 42 publications obtained from PubMed, one review article by Papacosta and Nassis (5) cited 128 publications. According to the exclusion criteria, four articles were selected from the 10 listed among the references that described the correlation between salivary α-amylase and exercise in healthy humans. Three duplicated studies were excluded and the remaining 15 publications were selected (Fig. 1).
Data are presented as the mean ± SD unless otherwise specified. P<0.05 was considered to indicate a statistically significant difference.

Results and Discussion
Ten of the 15 publications observed significant increases in salivary α-amylase activity or levels in response to exercise, five identified no differences and no studies identified a reduction (Table I).
A simple comparison or meta-analysis was not applicable as the type, duration and intensity of exercise, and the characteristics of the study subjects differed markedly.
Eight studies defined exercise intensity as a ratio (%) of the maximum or peak oxygen uptake (VO 2 max and VO 2 peak, respectively) or peak power output of the study participants and four used ergometers (6-9) and treadmills (10-13) for exercise loading.
Ergometer exercise was consistently demonstrated to elevate salivary α-amylase activity. Bishop et al (6) noted an increase in salivary α-amylase activity following exercise at 70% VO 2 peak for 90 min in endurance-trained males (age 23±1 years; mean ± SEM). Allgrove et al (7,8) conducted two studies using a bicycle ergometer, one of which determined the effect of exercise in ten active males (age, 23±1 years; mean ± SEM) at intensities of 50% VO 2 max, 75% VO 2 max and at incremental loads to exhaustion. The duration was matched to the initial VO 2 max test. Levels of α-amylase activity increased in all three trials in response to exercise (7). The other study confirmed these results in 24 trained male participants (age, 23±5 years) who cycled for 2.5 h at 60% VO 2 max followed by 75% VO 2 max to exhaustion; the mean salivary α-amylase activity increased from 143±23 to 463±22 U/ml (8). Fortes et al (9) observed an increase (not significant) in salivary α-amylase activity during exercise at 55% peak power output at 33˚C, with ≤50% relative humidity; up to 3% of body mass was lost due to sweat in 13 participants (age 24±5 years). The control condition, with rehydration to offset fluid loss, was examined and the kinetics of salivary α-amylase activity were almost identical. The participants in these four studies of ergometer exercise were all healthy, with a mean age of ~23-24 years. The intensity of the exercise was low in the study of dehydration (9). Allgrove et al (7) showed that α-amylase activity increased at 50% VO 2 max and the study by Fortes et al indicated that the mean α-amylase activity increased at 55% peak power output, although not significantly (9). Thus, exercise on a bicycle ergometer at an intensity as low as 55% peak power output may elevate salivary α-amylase activity.
By contrast, treadmill running generated mixed results. Fortes and Whitham (10) observed that α-amylase activity was elevated following running on a treadmill for 30 min at 50% VO 2 max followed by 30 min at 70% VO 2 max, in six endurance-trained males (age, 21.8±1.9 years). Leicht et al (11) reported that α-amylase activity increased in 23 wheelchair athletes. However, subsequent publications did not confirm these results. According to Costa et al (12), salivary α-amylase activity increased, although not significantly, in 11 male endurance runners who ran at 75% VO 2 max for 2 h. The findings of Rosa et al (13) from a study of 10 active males who ran on treadmills at 70% VO 2 max for 1 h supported these results; the mean salivary α-amylase concentrations were increased but the increase was not statistically significant. Three of the four studies, with the exception of the study of wheelchair athletes, comprised small cohorts, which may account for this discrepancy.
Five studies demonstrated changes in salivary α-amylase in response to exercise without specifying the exercise intensity (14)(15)(16)(17)(18). In one of these studies, 12 Caucasian male national-level cyclists underwent a progressive test on a bicycle ergometer. The initial load was 50 W, which increased by 25 W every 2 min to exhaustion. The salivary α-amylase concentration increased in parallel with the increase in   (14). Galina et al (15) adopted the Bruce protocol test using treadmills. Twenty-one active males performed a single bout of exercise and a minimum of five stages of the Bruce protocol (19). Salivary α-amylase activity increased during the exercise and reached the greatest level following the highest completed stage achieved by each participant (15). Allgrove et al (16) examined responses in male athletes with spinal cord damage. Salivary α-amylase activity increased from 158±47 to 281±72 U/ml (SEM) following 1 h of self-paced handcycling time trials in nine physically active male wheelchair athletes. Ishiguro et al (17) observed changes in α-amylase activity among healthy elderly individuals (age 64.7±8.2 years) during a fitness program comprising a 10 min warm up, 30 min of exercise and a 10 min cool down. The exercise performed was light aerobic gymnastics with singing developed for the elderly and the warm up and cool down consisted of stretching. Salivary α-amylase activity were not affected by the program, as pre-exercise values compared with post-exercise values were 32.7±34.0 versus 36.3±34.9 U/ml, respectively. Yamaguchi et al (18) identified that levels of salivary α-amylase activity in 10 male university students (age 22.2±0.5 years) during a 20 min walk, in forest and urban environments, did not change. With the exception of light gymnastics for the elderly (17) and relaxed walking (18), physical exercise appears to increase salivary α-amylase activity and concentration (14)(15)(16).
Chiodo et al (20) and Diaz et al (21) investigated the effect of Taekwondo and swimming competitions, respectively. Sixteen taekwondo black belt athletes participated in an offi-cial youth competition consisting of three 2-min rounds with 1-min intervals. Salivary α-amylase activity was increased by 115% at the end of the competition compared with the pre-competition values (20). Diaz et al (21) compared the α-amylase concentrations in saliva during a national swimming competition with those two weeks following the event (the control day) in 11 professional swimmers. The α-amylase concentrations immediately prior to warming up for the race and 5 min after finishing were higher than those at the same time on the control day. Thus, psychological and physical stress were considered to contribute to the increase in α-amylase levels.
In conclusion, exercise has consistently been shown to increase mean salivary α-amylase activity and concentration in all studies examined in the present review, including those in which changes were not significant, with the exception of the 20-min forest walk (18). The effect tended to be more pronounced at exercise intensities >70% VO 2 max in healthy young individuals. Therefore, studies published following those reviewed by Granger et al (1) confirm the conclusion that salivary α-amylase levels markedly increase in response to physical stress. Therefore, α-amylase levels may be an effective non-invasive marker of physical stress. Data are presented as the mean ± SD unless otherwise specified. a Mean ± SEM. RH, relative humidity; VO 2 max, maximal oxygen consumption; VO 2 peak, peak oxygen consumption at high intensity workload; NS, not significant.