Acute and chronic effects of exercise on markers of mucosal immunity.

Decreased secretion rate of salivary markers of mucosal immunity, and in particular salivary immunoglobulin A (s-IgA), have been implicated as risk factors for subsequent episodes of respiratory infection in athletes. IgA is the predominant Ig in mucosal secretions and acts with innate mucosal defences to provide the 'first line of defence' against pathogens and antigens presented at the mucosa. As well as summarising the evidence concerning the effects of acute exercise and longer-term intensive training on these markers of mucosal immunity, this review explores the factors that impact upon salivary responses to exercise, such as method of saliva collection, stimulation of saliva collection and the method of reporting s-IgA data. The influence of adequate hydration and nutritional supplementation during exercise as well as exercising in extreme environmental conditions on salivary responses is also explored. Finally, the possible mechanisms underlying the acute and longer-term of effects of exercise on salivary responses are examined, with particular emphasis on the potential role of the sympathetic nervous system and the expression and mobilisation of the polymeric Ig receptor.

[1]  G A Hudgens,et al.  Salivary alpha-amylase as a measure of endogenous adrenergic activity. , 1996, Clinical physiology.

[2]  K. Zeman,et al.  Immunological status of competitive cyclists before and after the training season. , 1994, International journal of sports medicine.

[3]  Jamie R. Blackwell,et al.  Salivary IgA response to prolonged exercise in a cold environment in trained cyclists. , 2002, Medicine and science in sports and exercise.

[4]  D. Jenkins,et al.  Decreased salivary immunoglobulins after intense interval exercise before and after training. , 1993, Medicine and science in sports and exercise.

[5]  H. Northoff,et al.  INFLUENCE OF ECHINACIN (EC31) TREATMENT ON THE EXERCISE-INDUCED IMMUNE RESPONSE IN ATHLETES , 1998 .

[6]  L. Dimitriou,et al.  Circadian effects on the acute responses of salivary cortisol and IgA in well trained swimmers , 2002, British journal of sports medicine.

[7]  G. Carpenter,et al.  Immunoglobulin a Secretion into Saliva During Dual Sympathetic and Parasympathetic Nerve Stimulation of Rat Submandibular Glands , 2000, Experimental physiology.

[8]  G. Carpenter,et al.  Regulation of salivary gland function by autonomic nerves , 2007, Autonomic Neuroscience.

[9]  H. Engels,et al.  Mucosal IgA and URTI in American college football players: a year longitudinal study. , 2005, Medicine and science in sports and exercise.

[10]  T Akimoto,et al.  Effects of 12 months of exercise training on salivary secretory IgA levels in elderly subjects , 2003, British journal of sports medicine.

[11]  L. Strazdins,et al.  Impact of saliva collection methods on sIgA and cortisol assays and acceptability to participants. , 2005, Journal of immunological methods.

[12]  E. Mylona,et al.  s-IgA response in females following a single bout of moderate intensity exercise in cold and thermoneutral environments. , 2002, International journal of sports medicine.

[13]  W. Kraemer,et al.  Strength, workload, anaerobic intensity and the immune response to resistance exercise in women. , 2003, Acta physiologica Scandinavica.

[14]  A. Cripps,et al.  The effect on immunity of long‐term intensive training in elite swimmers , 1995, Clinical and experimental immunology.

[15]  I. Jonsdottir,et al.  Neuropeptides and their interaction with exercise and immune function , 2000 .

[16]  M. Chennaoui,et al.  Intense training: mucosal immunity and incidence of respiratory infections , 2004, European Journal of Applied Physiology.

[17]  T. Housh,et al.  The Effect of Exercise at Various Temperatures on Salivary Levels of Immunoglobulin A , 1991, International journal of sports medicine.

[18]  S. Humphrey,et al.  A review of saliva: normal composition, flow, and function. , 2001, The Journal of prosthetic dentistry.

[19]  L. Yel Selective IgA Deficiency , 1975, The Lancet.

[20]  M. Lamm Current concepts in mucosal immunity. IV. How epithelial transport of IgA antibodies relates to host defense , 1998 .

[21]  P. Robson,et al.  The effects of high-intensity intermittent exercise on saliva IgA, total protein and alpha-amylase. , 1999, Journal of sports sciences.

[22]  W. K. Prusaczyk,et al.  Effects of caffeine on muscle glycogen utilization and the neuroendocrine axis during exercise. , 2000, The Journal of clinical endocrinology and metabolism.

[23]  E. Veerman,et al.  Neuroendocrine regulation of salivary IgA synthesis and secretion: implications for oral health , 2004, Biological chemistry.

[24]  D. Jenkins,et al.  Tennis, incidence of URTI and salivary IgA. , 2003, International journal of sports medicine.

[25]  J. Duarte,et al.  The impact of soccer training on the immune system. , 1998, The Journal of sports medicine and physical fitness.

[26]  M. Gleeson,et al.  The effects of carbohydrate supplementation during repeated bouts of prolonged exercise on saliva flow rate and immunoglobulin A , 2005, Journal of sports sciences.

[27]  C. Hardy,et al.  The influence of sympathetic activity and isoprenaline on the secretion of amylase from the human parotid gland. , 1974, Archives of oral biology.

[28]  C. Cunningham-Rundles Selective IgA deficiency. , 1988, Journal of pediatric gastroenterology and nutrition.

[29]  R. E. Noble Salivary alpha-amylase and lysozyme levels: a non-invasive technique for measuring parotid vs submandibular/sublingual gland activity. , 2000, Journal of oral science.

[30]  David B Pyne,et al.  Epstein-Barr virus reactivation and upper-respiratory illness in elite swimmers. , 2002, Medicine and science in sports and exercise.

[31]  Margarita Pérez,et al.  Saliva Composition and Exercise , 1998, Sports medicine.

[32]  J. Morrow,et al.  Influence of vitamin C supplementation on oxidative and salivary IgA changes following an ultramarathon , 2003, European Journal of Applied Physiology.

[33]  B. Barrett Medicinal properties of Echinacea: a critical review. , 2003, Phytomedicine : international journal of phytotherapy and phytopharmacology.

[34]  G. Carpenter,et al.  Salivary secretion of immunoglobulin A by submandibular glands in response to autonomimetic infusions in anaesthetised rats , 2003, Journal of Neuroimmunology.

[35]  D. Nieman Exercise, Infection, and Immunity , 1994, International journal of sports medicine.

[36]  P. Drummond,et al.  The effect of moderate aerobic exercise and relaxation on secretory immunoglobulin A. , 2001, International journal of sports medicine.

[37]  R. Rossen,et al.  The proteins in nasal secretion. II. A longitudinal study of IgA and neutralizing antibody levels in nasal washings from men infected with influenza virus. , 1970, JAMA.

[38]  P. Robach,et al.  Living high–training low altitude training: effects on mucosal immunity , 2005, European Journal of Applied Physiology.

[39]  J. Krieger,et al.  Chronic glutamine supplementation increases nasal but not salivary IgA during 9 days of interval training. , 2004, Journal of applied physiology.

[40]  A. Cripps,et al.  Immune status and respiratory illness for elite swimmers during a 12-week training cycle. , 2000, International journal of sports medicine.

[41]  G. Proctor,et al.  Chewing Stimulates Secretion of Human Salivary Secretory Immunoglobulin A , 2001, Journal of dental research.

[42]  G. Carpenter,et al.  Secretion of IgA by rat parotid and submandibular cells in response to autonomimetic stimulation in vitro. , 2004, International immunopharmacology.

[43]  Maree Gleeson,et al.  Exercise effects on mucosal immunity , 2000 .

[44]  M. Lamm IV. How epithelial transport of IgA antibodies relates to host defense. , 1998, American journal of physiology. Gastrointestinal and liver physiology.

[45]  D A Henson,et al.  Physical activity and immune function in elderly women. , 1993, Medicine and science in sports and exercise.

[46]  D. Nieman,et al.  Immune response to a 30-minute walk. , 2005, Medicine and science in sports and exercise.

[47]  E. Bateman,et al.  Ultramarathon running and upper respiratory tract infections. An epidemiological survey. , 1983, South African medical journal = Suid-Afrikaanse tydskrif vir geneeskunde.

[48]  P. Freedson,et al.  Moderate to vigorous physical activity and risk of upper-respiratory tract infection. , 2002, Medicine and science in sports and exercise.

[49]  Y. Takaesu,et al.  Oral health status related to subgingival bacterial flora and sex hormones in saliva during pregnancy. , 1994, The Bulletin of Tokyo Dental College.

[50]  T. Reilly,et al.  Salivary IgA response to intermittent and continuous exercise. , 2006, International journal of sports medicine.

[51]  F. Greer,et al.  Comparison of caffeine and theophylline ingestion: exercise metabolism and endurance. , 2000, Journal of applied physiology.

[52]  J. R. Garrett,et al.  Nerve‐Evoked Secretion of Immunoglobulin a in Relation to other Proteins by Parotid Glands in Anaesthetized Rat , 2000, Experimental physiology.

[53]  J. Davis,et al.  Effects of mode and carbohydrate on the granulocyte and monocyte response to intensive, prolonged exercise. , 1998, Journal of applied physiology.

[54]  C. White,et al.  Evaluation of echinacea for the prevention and treatment of the common cold: a meta-analysis , 2007, The Lancet Infectious Diseases.

[55]  B. Sonies,et al.  Xerostomia: evaluation of a symptom with increasing significance. , 1985, Journal of the American Dental Association.

[56]  J. Jemmott,et al.  Academic stress, social support, and secretory immunoglobulin A. , 1988, Journal of personality and social psychology.

[57]  T. Housh,et al.  The effect of exercise intensity and duration on salivary immunoglobulin A , 2004, European Journal of Applied Physiology and Occupational Physiology.

[58]  M. Gleeson,et al.  Carbohydrate and fluid intake affect the saliva flow rate and IgA response to cycling. , 2000, Medicine and science in sports and exercise.

[59]  David C. Nieman,et al.  Saliva immunoglobulins in elite women rowers , 2000, European Journal of Applied Physiology.

[60]  J. Davis,et al.  Change in salivary IgA following a competitive marathon race. , 2002, International journal of sports medicine.

[61]  B. Pedersen,et al.  Effect of glutamine and protein supplementation on exercise-induced decreases in salivary IgA. , 2001, Journal of applied physiology.

[62]  N. Bishop,et al.  Effect of prolonged exercise and carbohydrate on total neutrophil elastase content. , 2003, Medicine and science in sports and exercise.

[63]  F. Hucklebridge,et al.  The relationship between salivary secretory immunoglobulin A and cortisol: neuroendocrine response to awakening and the diurnal cycle. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[64]  T. Graham,et al.  Caffeine, coffee and ephedrine: impact on exercise performance and metabolism. , 2001, Canadian journal of applied physiology = Revue canadienne de physiologie appliquee.

[65]  D B Pyne,et al.  Mucosal immunity, respiratory illness, and competitive performance in elite swimmers. , 2001, Medicine and science in sports and exercise.

[66]  Jamie R. Blackwell,et al.  Salivary IgA response to prolonged exercise in a hot environment in trained cyclists , 2005, European Journal of Applied Physiology.

[67]  P. Klentrou,et al.  Effect of moderate exercise on salivary immunoglobulin A and infection risk in humans , 2002, European Journal of Applied Physiology.

[68]  D. Pyne,et al.  Antimicrobial peptides and proteins, exercise and innate mucosal immunity , 2006, FEMS immunology and medical microbiology.

[69]  M. Gleeson,et al.  The effect of single and repeated bouts of prolonged cycling and circadian variation on saliva flow rate, immunoglobulin A and alpha-amylase responses. , 2004, Journal of sports sciences.

[70]  D B Pyne,et al.  Salivary IgA levels and infection risk in elite swimmers. , 1999, Medicine and science in sports and exercise.

[71]  J. Carins,et al.  Salivary immunoglobulin-A as a marker of stress during strenuous physical training. , 2002, Aviation, space, and environmental medicine.

[72]  D. Nieman,et al.  Is infection risk linked to exercise workload? , 2000, Medicine and science in sports and exercise.

[73]  M. Taubman,et al.  Minor salivary glands as a major source of secretory immunoglobin A in the human oral cavity , 1975, Science.

[74]  J. Bilzon,et al.  The influence of an arduous military training program on immune function and upper respiratory tract infection incidence. , 2006, Military medicine.

[75]  T. Reilly,et al.  The effects of single and repeated bouts of soccer-specific exercise on salivary IgA. , 2007, Archives of oral biology.

[76]  Arie V Nieuw Amerongen,et al.  Stress and secretory immunity. , 2002, International review of neurobiology.

[77]  H. Engels,et al.  Echinacea purpurea and mucosal immunity. , 2007, International journal of sports medicine.

[78]  C. Christensen,et al.  A Comparison of Whole Mouth Resting and Stimulated Salivary Measurement Procedures , 1982, Journal of dental research.

[79]  G. J. Walker,et al.  Salivary IgA responses to prolonged intensive exercise following caffeine ingestion. , 2006, Medicine and science in sports and exercise.

[80]  R. Fielding,et al.  Effects of prior exercise on eccentric exercise-induced neutrophilia and enzyme release. , 2000, Medicine and science in sports and exercise.

[81]  Gerald A. Hudgens,et al.  Salivary α‐amylase as a measure of endogenous adrenergic activity , 1996 .

[82]  F. Scannapieco,et al.  Emergence in Human Dental Plaque and Host Distribution of Amylase-binding Streptococci , 1994, Journal of dental research.

[83]  G. J. Walker,et al.  Lymphocyte responses to influenza and tetanus toxoid in vitro following intensive exercise and carbohydrate ingestion on consecutive days. , 2005, Journal of applied physiology.

[84]  J. Morrow,et al.  Immune and oxidative changes during and following the Western States Endurance Run. , 2003, International journal of sports medicine.

[85]  G. Carpenter,et al.  The influence of nerves on the secretion of immunoglobulin A into submandibular saliva in rats , 1998, The Journal of physiology.

[86]  P. Brandtzaeg,et al.  The J Chain Is Essential for Polymeric Ig Receptor-Mediated Epithelial Transport of IgA1 , 2001, The Journal of Immunology.

[87]  J. Bilzon,et al.  Salivary immunoglobulin A response at rest and after exercise following a 48 h period of fluid and/or energy restriction , 2007, British Journal of Nutrition.

[88]  K. Lamb,et al.  The effects of a high carbohydrate diet on cortisol and salivary immunoglobulin A (s-IgA) during a period of increase exercise workload amongst Olympic and Ironman triathletes. , 2005, International journal of sports medicine.

[89]  K. Kaibara,et al.  Blood lactoferrin release induced by running exercise in normal volunteers: antibacterial activity. , 2004, Clinica chimica acta; international journal of clinical chemistry.

[90]  K. Aizawa,et al.  A rat model of saliva secretory immunoglobulin: a suppression caused by intense exercise , 2008, Scandinavian journal of medicine & science in sports.

[91]  N P Walsh,et al.  The Effect of Exercising to Exhaustion at Different Intensities on Saliva Immunoglobulin A, Protein and Electrolyte Secretion , 1998, International journal of sports medicine.

[92]  T. Tomasi,et al.  Decreased secretory immunoglobulins following intense endurance exercise , 1989 .

[93]  A. van As,et al.  The effect of exercise on secretory and natural immunity. , 1987, Advances in experimental medicine and biology.

[94]  Herbert Benson,et al.  ACADEMIC STRESS, POWER MOTIVATION, AND DECREASE IN SECRETION RATE OF SALIVARY SECRETORY IMMUNOGLOBULIN A , 1983, The Lancet.

[95]  J. Davis,et al.  Carbohydrate Supplementation and the Lymphocyte Proliferative Response to Long Endurance Running , 1998, International journal of sports medicine.

[96]  T. Tomasi,et al.  Immune parameters in athletes before and after strenuous exercise , 1982, Journal of Clinical Immunology.

[97]  I. Jonsdottir Special feature for the Olympics: effects of exercise on the immune system: neuropeptides and their interaction with exercise and immune function. , 2000, Immunology and cell biology.