Effects of high-intensity endurance exercise on epidermal barriers against microbial invasion.

Author:Eda, Nobuhiko
Position:Research article - Report
 
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Introduction

The peak condition of an athlete can be seriously hampered by injuries and infections that occur before a competitive event. Infections are particularly common among athletes because of chronic immunosuppression in response to intensive physical training and major competitions (Shephard et al., 1991). An athlete's skin is often macerated from sweating, a condition which provides a fertile breeding environment for microorganisms, while trauma inherent to sporting activities can damage the cutaneous barrier allowing microorganisms to infiltrate deeper layers (Adams, 2008). It is therefore possible that skin infections in susceptible athletes might negatively influence physical condition and performance.

Staphylococcal skin infections occur in various contact sports such as football, basketball, rugby, hockey, and wrestling (Adams, 2002). Staphylococci are classified as Staphylococcus aureus (S. aureus) or coagulase-negative Staphylococcus. In a study of 110 football players and 8 athlete trainers, 67 (57%) were positive for S. aureus, of which 8 (12%) developed staphylococcal skin infections (Fontanilla et al., 2010). Previous studies on football players (Bartlett et al., 1982) and basketball players (Sosin et al., 1989) have reported an increase in S. aureus on the skin after both training sessions and games. Skin to skin contact between athletes and contact with sports equipment was considered a major cause of increasing the spread of S. aureus (Pollard, 1966). Staphylococcus epidermidis (S. epidermidis) is the most frequently isolated bacterium of coagulase-negative Staphylococcus and normally inhabits the skin as nonpathogenic resident (Vuong and Otto, 2002). Moreover, S. epidermidis might have a beneficial role on the skin surface by producing its own antimicrobial peptides (Cogen et al., 2010) and enhancing the expression of human antimicrobial peptides from keratinocytes (Dinulos et al., 2003). On the other hand, S. epidermidis attaches more tightly to the surface of epithelial cells than S. aureus (Kume and Fukushima, 1994) and forms biofilms which is considered to be the main virulence factor (Raad et al., 1998). In clinical practice, S. epidermidis can cause skin infections, such as folliculitis and sycosis vulgaris, in compromised hosts and patients with the damaged cutaneous barrier (Katayama et al., 2009). Intensive exercise-induced immunosuppression might promote infectious skin disease, therefore, athletes are habitually at risk for skin infections, which are important causes of temporary disability (Pecci et al., 2009). Moreover, it is possible that skin infections negatively affect athlete performance. Therefore, countermeasures against infectious disease on the skin are significant for maintaining conditions in athletes.

The epidermis barrier functions as an immunological, biochemical, and physical barrier against pathogen invasion. Secretory immunoglobulin A (SIgA), one type of immune barrier, is found on the skin in sweat from eccrine glands (Okada et al., 1988). Mucosal SIgA works as the first line of defense for the human body against pathogenic microbial invasion (Lamm et al., 1995). Previous studies have shown that S. aureus opsonized with mucosal SIgA is significantly ingested by polymorphonuclear leucocytes (Gorter et al., 1987) and that the number of S. aureus is lower around sweat ducts (Goto et al., 1995). Therefore, it is possible that skin-SIgA works similarly as the first line of defense against pathogenic microbial invasion on the skin surface. A previous study of patients in Brazil with IgA deficiency reported that mucosal infections of the skin and the respiratory and gastrointestinal tracts occurred in 80 of 126 (63.5%) patients (Jacob et al., 2008). Therefore, skin-SIgA might be a useful indicator for estimating athlete skin condition. The previous study on salivary SIgA secretion has shown a transient decrease following high-intensity endurance exercise (Mackinnon et al., 1993). However, no study has investigated the effects of exercise on skin-SIgA.

Defensin, which is an antimicrobial peptide, provides a biochemical barrier and exhibits anti-pathogenic activity (Ganz, 1999). Defensin exerts an antimicrobial effect by breaking the hydrophobic core of the lipid bilayer on microbes (Oren et al., 1999; Schaller et al., 2000). Human [beta]-defensin 2 (HBD-2) expression is induced by the stimulation of bacterial bodies such as staphylococci, Candida, and Pseudomonas aeruginosa in keratinocytes (Dinulos et al., 2003), and tumor necrosis factor (TNF)-[alpha] and interleukin (IL)-1 in keratinocytes (Liu et al., 2002) and respiratory epithelial cells (Harder et al., 2000). In a previous study on salivary HBD-2, high-intensity endurance exercise increased HBD-2 expression transiently (Usui et al., 2011).

The stratum corneum serves as a physical barrier against percutaneous penetration of chemicals and microbes (Madison, 2003). It is known that the moisture content of the stratum corneum is a useful measure of barrier function (Proksch et al., 2008). The previous study reported that the low water content of the stratum corneum in patients with atopic dermatitis is related to a clinical condition (Loden et al., 1992).

We have previously investigated skin SIgA concentration and the number of staphylococci before and after exercise and reported a skin SIgA decrease and staphylococci increase (submitted). However, our previous study only determined the alteration of skin SIgA and staphylococci before and after exercise, and no study has investigated the time course of epidermal barriers after exercise. In this study, we examine skin SIgA, staphylococci, HBD-2, and moisture content of the stratum corneum after 60 min and 120 min of exercise. Elucidating this relationship will contribute to the development of conditioning programs which include prevention of skin infection for athletes.

The aim of this study therefore, was to determine the effect of high-intensity endurance exercise on epidermal barriers, primarily skin SIgA, HBD-2, and moisture content of the stratum corneum. We hypothesized that high-intensity exercise may decrease both skin SIgA secretion and moisture content of the stratum corneum while increasing skin HBD-2 expression.

Methods

Participants

Six healthy adult males (age, 22.3 [+ or -] 1.6 years; height, 1.77 [+ or -] 0.05 m; body mass, 69.4 [+ or -] 4.9 kg; body fat percentage, 17.4 [+ or -] 4.8%; and body mass index, 22.3 [+ or -] 2.0 kg-m-2) participated in the study. Participants were given a detailed explanation of risks, stress, and the potential benefits of the study before they signed an informed consent form. All participants had passed a complete medical examination within the preceding year. No participants had been treated with any drugs that are known to affect immune function. No participants reported allergies such as atopic dermatitis or recent infections (prior 3 months) in the determination. The study was approved by the Ethics Committee on Human Research of Waseda University. Experiments were conducted in accordance with the Declaration of Helsinki.

Protocol

Participants performed a bicycle-ergometer exercise test for 60 min from 18:30 to 19:30 in a laboratory at Waseda University. They then rested for the remainder of the assessment. Measurements were carried out in a climate-controlled room at 25 [degrees]C and 35% relative humidity at 18:30 (Before exercise; pre), 19:30 (After exercise; post), 20:30 (After 60 min of exercise; 60 min), and 21:30 (After 120 min of exercise; 120 min).

Exercise

Previously, power at 75%[HR.sub.max] (PWC75%[HR.sub.max]) was determined using a bicycle ergometer (75XLIII; Combi Wellness, Tokyo, Japan). After resting for 60 s, loading motion was progressively increased by 15 W x [min.sup.-1] until reaching 75%[HR.sub.max]. During exercise, the pedalling rate was maintained at 50 rpm. From 18:30 to 19:30 on the measurement day, participants pedalled a bike for 1 min at 50%[HR.sub.max] and for 59 min at 75%[HR.sub.max]...

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