Exercise upregulates salivary amylase in humans (Review)
- Authors:
- Published online on: January 23, 2014 https://doi.org/10.3892/etm.2014.1497
- Pages: 773-777
Abstract
1. 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.
2. 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 ‘saliva’, ‘amylase’ and ‘exercise’. 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.
3. 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 (VO2max and VO2peak, 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% VO2peak 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% VO2max, 75% VO2max and at incremental loads to exhaustion. The duration was matched to the initial VO2max 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% VO2max followed by 75% VO2max 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% VO2max 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% VO2max followed by 30 min at 70% VO2max, 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% VO2max for 2 h. The findings of Rosa et al (13) from a study of 10 active males who ran on treadmills at 70% VO2max 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 (14–18). 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 load (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 (14–16).
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 official 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% VO2max 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.
Acknowledgements
This review was supported in part by the Ministry of Education, Culture, Sports, Science and Technology (MEXT)-Supported Program for the Strategic Research Foundation at Private Universities and a grant from the Research Project on Development of Agricultural Products and Foods with Health-promoting benefits (NARO), Japan.
References
Granger DA, Kivlighan KT, el-Sheikh M, Gordis EB and Stroud LR: Salivary alpha-amylase in biobehavioral research: recent developments and applications. Ann N Y Acad Sci. 1098:122–144. 2007. View Article : Google Scholar : PubMed/NCBI | |
Chatterton RT Jr, Vogelsong KM, Lu YC, Ellman AB and Hudgens GA: Salivary alpha-amylase as a measure of endogenous adrenergic activity. Clin Physiol. 16:433–448. 1996. View Article : Google Scholar : PubMed/NCBI | |
Kivlighan KT and Granger DA: Salivary alpha-amylase response to competition: relation to gender, previous experience, and attitudes. Psychoneuroendocrinology. 31:703–714. 2006. View Article : Google Scholar : PubMed/NCBI | |
Yamaguchi M, Hanawa N and Yoshida H: Evaluation of a novel monitor for the sympathetic nervous system using salivary amylase activity. Seitai-Ikougaku. 45:161–168. 2007.(in Japanese with English abstract). | |
Papacosta E and Nassis GP: Saliva as a tool for monitoring steroid, peptide and immune markers in sport and exercise science. J Sci Med Sport. 14:424–434. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bishop NC, Walker GJ, Scanlon GA, Richards S and Rogers E: Salivary IgA responses to prolonged intensive exercise following caffeine ingestion. Med Sci Sports Exerc. 38:513–519. 2006. View Article : Google Scholar : PubMed/NCBI | |
Allgrove JE, Gomes E, Hough J and Gleeson M: Effects of exercise intensity on salivary antimicrobial proteins and markers of stress in active men. J Sports Sci. 26:653–661. 2008. View Article : Google Scholar : PubMed/NCBI | |
Allgrove JE, Oliveira M and Gleeson M: Stimulating whole saliva affects the response of antimicrobial proteins to exercise. Scand J Med Sci Sports. March 19–2013.(Epub ahead of print). | |
Fortes MB, Diment BC, Di Felice U and Walsh NP: Dehydration decreases saliva antimicrobial proteins important for mucosal immunity. Appl Physiol Nutr Metab. 37:850–859. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fortes MB and Whitham M: Salivary Hsp72 does not track exercise stress and caffeine-stimulated plasma Hsp72 responses in humans. Cell Stress Chaperones. 16:345–352. 2011. View Article : Google Scholar : PubMed/NCBI | |
Leicht CA, Bishop NC and Goosey-Tolfrey VL: Mucosal immune responses to treadmill exercise in elite wheelchair athletes. Med Sci Sports Exerc. 43:1414–1421. 2011. View Article : Google Scholar : PubMed/NCBI | |
Costa RJ, Fortes MB, Richardson K, Bilzon JL and Walsh NP: The effects of postexercise feeding on saliva antimicrobial proteins. Int J Sport Nutr Exerc Metab. 22:184–191. 2012.PubMed/NCBI | |
Rosa L, Teixeira A, Lira F, Tufik S, Mello M and Santos R: Moderate acute exercise (70% VO2peak) induces TGF-β, α-amylase and IgA in saliva during recovery. Oral Dis. Feb 19–2013.(Epub ahead of print). | |
de Oliveira VN, Bessa A, Lamounier RP, et al: Changes in the salivary biomarkers induced by an effort test. Int J Sports Med. 6:377–381. 2010.PubMed/NCBI | |
Gallina S, Di Mauro M, D’Amico MA, D’Angelo E, Sablone A, Di Fonso A, Bascelli A, Izzicupo P and Di Baldassarre A: Salivary chromogranin A, but not α-amylase, correlates with cardiovascular parameters during high-intensity exercise. Clin Endocrinol (Oxf). 75:747–752. 2011. | |
Allgrove JE, Chapman M, Christides T and Smith PM: Immunoendocrine responses of male spinal cord injured athletes to 1-hour self-paced exercise: pilot study. J Rehabil Res Dev. 49:925–933. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ishiguro C, Ikuta M, Sugita A, Okada T, Kozasa Y, Numata Y, Higashino T and Mikouchi N: The effect of the health education initiative ‘Physical Exercise for Promotion of Health’ on people in the community. Nihon Sekijuji Toyota Kango Daigaku Kiyo [Bulletin of Japanese Red Cross Toyota University of Nursing]. 7:107–119. 2012.(In Japanese). | |
Yamaguchi M, Deguchi M and Miyazaki Y: The effects of exercise in forest and urban environments on sympathetic nervous activity of normal young adults. J Int Med Res. 34:152–159. 2006. View Article : Google Scholar : PubMed/NCBI | |
Bruce RA: Exercise testing of patients with coronary heart disease. Principles and normal standards for evaluation. Ann Clin Res. 3:323–332. 1971.PubMed/NCBI | |
Chiodo S, Tessitore A, Cortis C, et al: Stress-related hormonal and psychological changes to official youth Taekwondo competitions. Scand J Med Sci Sports. 21:111–119. 2011. View Article : Google Scholar : PubMed/NCBI | |
Diaz MM, Bocanegra OL, Teixeira RR, Soares SS and Espindola FS: Response of salivary markers of autonomic activity to elite competition. Int J Sports Med. 33:763–768. 2012. View Article : Google Scholar : PubMed/NCBI |