INTRODUCTION
Skin infections are common in contact sports, such as wrestling, football, and rugby. They can be directly transmitted between athletes through skin-to-skin contact or indirectly through contaminated equipment. Bacterial skin and soft tissue infections (SSTIs), dermatophyte infections (tinea gladiatorum), and herpes simplex viral infections (herpes gladiatorium) are the most common cutaneous infections reported in wrestlers. Although cutaneous bacteria, fungi, and viruses can be treated with standard antimicrobials, some strains are becoming more resistant to commonly prescribed medications. Recalcitrant infections contribute to a significant amount of time lost in practice and competition, pose greater risk of serious complications, and are associated with increased healthcare costs. This manuscript aims to discuss common sport-related dermatologic infections, the problem with the rise in resistance of Staphylococcus aureus and dermatophytes, and updated treatment recommendations. In addition, we will discuss monitoring and safety measures for cutaneous infections in wrestlers and other combat athletes.
BACTERIAL CUTANEOUS INFECTIONS: GENERAL CONSIDERATIONS
Staphylococcus aureus (S. aureus) is the most commonly transmitted bacterial skin infection in athletes and may present as folliculitis, furunculosis, impetigo, or cellulitis. β-lactam antibiotics, such as penicillin, methicillin, and cephalosporins, were traditionally the treatment of choice for these skin infections; however, the increased usage of these antibiotics contributed to strains of S. aureus developing resistance through acquisition of new genes that code for virulence factors or changing the structure of target sites for traditional therapy.
Poor response to initial treatment may suggest a more virulent infection, such as methicillin-resistant S. aureus (MRSA). MRSA is a bacterium that contributes to more than 50% of all S. aureus isolates in the United States.1 When MRSA infections are not optimally treated, the infection can spread more aggressively to the involved area, resulting in sequelae, such as sepsis or necrotizing fasciitis. These complications can lead to devastating outcomes, including limb loss or death.
Community-associated MRSA (CA-MRSA) outbreaks are implicated in 76% of all SSTIs.2 In athletes, rapid spread and the severity of clinical manifestations contribute to increased lost time from sport participation and hospitalization. From 1988 to 2004, 20% of lost practice time in National Collegiate Athletic Association (NCAA) wrestlers was due to cutaneous infection.3
Owing to the increased prevalence of MRSA and the distinct treatment requirements, it is important to perform routine cultures and sensitivities. Accurate identification ensures effective antibiotic selection. Culture samples can be taken from purulent cellulitis or fluid-filled infections. Skin biopsies may be taken from individuals with cellulitis without drainage or other nonpurulent infections; however, it is difficult to achieve a high enough yield from skin biopsies to identify the bacterial pathogen responsible for cellulitis and erysipelas infections.
CLINICAL PRESENTATION AND TREATMENT RECOMMENDATIONS
Impetigo is characterized by clusters of red pustules and honey-colored crusted erosions that often occur on the lower face and spread rapidly toward the torso and the upper extremities up to 48 hours after infection. About 70% of impetigo cases are classified as nonbullous lesions, while the remaining 30% consist of fluid-filled, bullous erosions.4S. aureus is responsible for nearly all bullous impetigo and approximately 80% of nonbullous impetigo.5 Group A beta-hemolytic Streptococci is responsible for a small percentage of nonbullous impetigo. Delayed or suboptimal treatment may precipitate rheumatic fever, acute poststreptococcal glomerulonephritis (PSGN), or staphylococcal scalded skin syndrome (SSSS).
First-line treatment (Table 1) for localized, nonbullous impetigo (Figure 1) traditionally includes a topical ointment such as mupirocin. Mupirocin (applied 3 times a day for 5 days) was traditionally effective against MRSA when the impetigo is limited to small clusters. However, Chaturvedi et al found mupirocin resistance rates of 18.3% to MRSA. Retapamulin 1% ointment (applied twice a day for 5 days) is a newer topical antibiotic that is effective against methicillin-sensitive S. aureus (MSSA) and streptococcus pyogenes, but not against MRSA.6 Premature discontinuation of topical medication can lead to resistance. Oral antibiotics are required when larger surface areas are involved. If the risk for MRSA is low or culture is negative for MRSA, then 250 to 500 mg dicloxacillin or cephalexin every 6 hours for 7 days is effective.7 In cases of bullous impetigo, oral antibiotics are required because fluid-filled blisters rupture easily, complicating a topical approach.
Summary of Recommended Guidelines for the Treatment of Cutaneous Sport Infections
| Skin Condition | Recommended Treatment | Organism Coverage | Special Considerations |
| Nonbullous impetigo | Mupirocin tid for 5 d* Retapamulin 1% bid for 5 d |
MSSA and S. pyogenes | 250–500 mg dicloxacillin or cephalexin qid for 7 d for nonbullous impetigo when larger surface areas are involved |
| Bullous impetigo | 250–500 mg dicloxacillin qid for 7 d or 250–500 mg cephalexin qid for 7 d |
MSSA and S. pyogenes | |
| Folliculitis and abscesses | Incision and drainage (I&D) 100 mg orally twice daily doxycycline for 5–7 days or 1 to 2 double-strength tablets twice daily trimethoprim–sulfamethoxazole (TMP-SMX) for 7–10 d |
MRSA | 250–500 mg dicloxacillin or cephalexin qid for 7 d if signs of systemic infection Adverse effects: GI, photosensitivity, renal toxicity |
| Erysipelas | 500 mg penicillin V potassium orally every 6 h or 875 mg amoxicillin orally every 12 h or 500 mg cephalexin orally every 6 h or 500 mg cefadroxil orally every 12 h |
β-hemolytic streptococci and MSSA |
C. difficile bacterial overgrowth black box warning for clindamycin TMP-SMX, amoxicillin plus doxycycline, or clindamycin therapy if MRSA coverage is indicated |
| Cellulitis | 500 mg dicloxacillin or cephalexin orally every 6 h or 500 mg cefadroxil orally every 12 h 450 mg tid TMP-SMX or clindamycin* TMP-SMX, amoxicillin plus doxycycline, or clindamycin* |
β-hemolytic streptococci and MSSA | |
|
Malassezia (Pityrosporum) folliculitis (MF) |
Ketoconazole cream daily for 2–4 wk 200 mg itraconazole twice daily for 1 wk 150 mg fluconazole once weekly for 2 to 6 wk |
Malassezia (Pityrosporum) Trichophyton tonsurans and other dermatophytes Molds and yeasts |
Can be exacerbated by antibiotics and steroids Itraconazole risk for rhabdomyolysis and liver damage |
*Additionally covers MRSA.
bid, twice a day; tid, 3 times a day; qid, 4 times a day.
Severe impetigo of the face.
Folliculitis (Figure 2) appears as small, red or white pustules within hair follicles on the scalp, underarms, and lower legs or thighs. Carbuncles or furuncles (hereafter, referred to as abscesses) present as a cluster of red or purple boils beneath the skin on the axilla, buttocks, or thighs. Incision and drainage (I&D) is the standard of care for all abscesses. I&D has a 80% success rate versus needle aspiration, which only has a 26% success rate.8 I&D may be contraindicated when fluid collections are too small, occur close to vasculature, or present in a sensitive body location.9 Oral antibiotics (dicloxacillin or cephalexin) may be prescribed if I&D is contraindicated or the patient shows symptoms of systemic infection, such as fever, hypotension, or sustained tachycardia.
Staphylococcal folliculitis.
If MRSA is confirmed or suspected, 100 mg of oral doxycycline twice daily for 5 to 7 days or 1 to 2 double-strength tablets twice daily trimethoprim-sulfamethoxazole (TMP-SMX) for 7 to 10 days is recommended. Both treatments have shown high efficacy rates against MRSA. A retrospective cohort study found that 95% of MRSA infections were susceptible to tetracyclines, such as doxycycline and minocycline.10 Similarly, TMP-SMX has shown complete clinical resolution in 73.9% patients with SSTIs caused by S. aureus in a prospective randomized trial.11 Tetracyclines and TMP-SMX are well tolerated, but their side effects may not be ideal for athletes. Gastrointestinal symptoms are common with doxycycline because patients often complain of stomach irritability and nausea if taken on an empty stomach. This could be exacerbated in athletes who are weight cycling or under a restrictive diet. In addition, photosensitivity reactions may also be a problem for athletes who practice outdoors. Adverse outcomes in TMP-SMX include renal toxicity, which should be considered in the setting of dehydration or weight loss for weight-class-based sports. It is important to consider adverse reactions caused by doxycycline and TMP-SMX and provide good counseling and monitoring in athletes.
Staphylococci or beta-hemolytic streptococci may also lead to nonpurulent, diffuse SSTIs in athletes, such as erysipelas and cellulitis (Figure 3). Erysipelas, caused by beta-hemolytic streptococci, involves the superficial layers of the dermis and presents as tender, erythematous rashes with raised edges, while cellulitis occurs in the deeper dermis and subcutaneous tissue, presenting as poorly demarcated, erythematous patches with associated edema and tenderness to palpation. Although cellulitis may be caused by S. aureus, mupirocin is not adequate for this deep infection. Oral antibiotics are required instead. The first-line treatment for isolated cellulitis is traditionally 5 to 6 days of oral β-lactam or cephalosporin antibiotic that covers β-hemolytic streptococci and MSSA. A systematic review by Kilburn et al12 determined that there is no difference between penicillin and cephalosporin or between different generations of cephalosporins in the treatment of cellulitis and erysipelas. Initial therapy that targets β-hemolytic streptococci and MSSA includes 500 mg dicloxacillin or cephalexin orally every 6 hours or 500 mg cefadroxil orally every 12 hours. If the patient is allergic to β-lactams, then TMP-SMX or clindamycin (450 mg tid) can be prescribed. Adverse effects of clindamycin include Clostridium difficile (C. difficile) bacterial overgrowth in the large intestine, which is a black box warning issued by the Food and Drug Administration. C. difficile is a leading cause of healthcare-associated infections, contributing to almost half a million infections annually and 29 000 deaths in 2011.13 Patient-specific factors that increase the risk of C. difficile include immunocompromisation, diabetes mellitus, and chronic kidney disease.14 Indications for MRSA coverage in erysipelas and cellulitis include systemic signs of toxicity or a medical history of MRSA infection. If there is an indication for MRSA coverage, then TMP-SMX, amoxicillin plus doxycycline, or clindamycin therapy can be initiated. Finally, empiric therapy for erysipelas that target β-hemolytic streptococci includes 500 mg penicillin V potassium orally every 6 hours, 875 mg amoxicillin orally every 12 hours, 500 mg cephalexin orally every 6 hours, or 500 mg cefadroxil orally every 12 hours. If infection is present in the lower extremity, elevation of the affected limb is recommended because associated edema can affect the penetration of antibiotics into the affected tissue. Associated lymphedema and venous insufficiency can also be treated with compression therapy.
Pseudomonal cellulitis.
DOSING
Therapeutic dosing may need to be adjusted in combat athletes who actively engage in weight cycling or rapid weight loss because they are prone to kidney dysfunction and potentially impaired drug metabolism. Wrestlers often aim to rapidly lose about 5% of their body weight for 5 to 7 days before competition.13 Weight loss may be achieved by increasing exercise and reducing energy intake. This results in dehydration, which increases the risk of acute kidney injury.15 In a study conducted by Trivic et al,16 rapid weight loss resulted in higher levels of blood urea nitrogen, uric acid, and serum creatinine. The study concluded that rapid weight loss combined with regular exercise leads to damaging effects on kidney function. In theory, athletes with impaired renal function may require decreased dosing requirements for renally-excreted antibiotics, including penicillin, cephalosporins, aminoglycosides, and tetracyclines (with the exception of doxycycline, which is metabolized by the liver). However, age and increased metabolic rate are 2 factors that seem to compensate for impaired renal clearance. At this time, there is no clear data to suggest that dosing should be altered in athletes engaging in weight cycling.
There are other factors that should be considered when creating a more nuanced approach for the athlete patient population. Fayock, et al address the adverse effects of oral antibiotics on athletes, such as the risk of QT prolongation, aortic dissection, nerve damage, and tendon injuries. Furthermore, Puccini et al propose that oral antibiotics have profound effects on athletes, such as muscle weakness, pain, fatigue, and Achilles tendon injuries because of increased production of reactive oxygen species (ROS) and impaired mitochondrial function. Although the biochemical and physiologic mechanisms of antibiotic use in athletes are outlined in the literature, research on dosing modifications remains limited.
FUNGAL CUTANEOUS INFECTIONS
In addition to bacterial cutaneous infections, fungal infections are common among combat athletes. Dermatophytes are the most common cause of cutaneous mycoses worldwide and infect keratinized tissue such as skin, hair, and nails. Trichophyton, Microsporum, and Epidermophyton are 3 genera of dermatophytes. Trichophyton tonsurans is the most common cause of dermatophyte outbreaks in wrestlers.17 From 1993 to 2004, dermatophytosis accounted for 22.1% of cutaneous infections in NCAA wrestlers and was recorded as the third-most-common type of cutaneous infection leading to lost practice time.3 Dermatophyte infections have been highly treatable with antifungal agents, such as terbinafine, itraconazole, fluconazole, and griseofulvin; however, there has recently been a growing rate of recalcitrant infections because of treatment failure or reinfection.18 Although some studies suggest that resistance to antifungals is responsible, other studies suggest that host immunologic response, steroid use, and environmental factors (ie heat, humidity, sweating) may also play a role in the rise of recalcitrant dermatophytosis.19 Therefore, the investigation of resistance mechanisms in dermatophytes is important to make appropriate changes to treatment recommendations.
Dermatophytes result in tinea infections, such as tinea pedis (athlete’s foot), tinea unguium (onychomycosis or fungal infection of the nail), tinea capitis (scalp and hair follicles), tinea barbae (skin and hair follicles in the beard area), and tinea corporis (anywhere else in the body). In wrestlers, dermatophyte lesions are most commonly found on points of contact between competitors, such as the trunk, head, neck, and upper extremities. Tinea capitis first appears as sharply demarcated, erythematous, scaly patches that spread outward. Weeks to months later, the erythema fades and the scaly patches result in alopecia with follicular plugs, showing a characteristic “black dot” appearance. Tinea corporis in the trunk, neck, arms, and legs is characterized by erythematous, scaly, sharply demarcated, annular papules or plaques with central clearing and raised borders. Infected patients may also experience local pruritus, erythema, and burning sensations. However, a study found that the typical appearance of tinea is often missed in wrestlers, as lesions may delay in presentation after routine skin checks or become abraded during competition.20 Diagnosis can be confirmed with a potassium hydroxide (KOH) preparation or fungal culture in infected individuals.
Malassezia (Pityrosporum) folliculitis (MF) is a fungal acneiform eruption that results from overgrowth of normal cutaneous yeast. It commonly presents as pruritic, monomorphic papules and pustules on the chest, back, posterior arms, and face. Altering normal cutaneous flora through immunosuppression and antibiotic use may lead to these eruptions. Fungal folliculitis is often misdiagnosed as common acne because it is commonly associated with acne; however, MF often persists for many years and does not resolve with typical acne medications. Pruritus is also a key characteristic that distinguishes MF from acne. MF is also often misdiagnosed as bacterial folliculitis, which is commonly treated with antibiotics or corticosteroids rather than antifungals. It is important to distinguish whether the source is fungal or bacterial because MF can be exacerbated through antibiotic or steroid use. Tinea incognito, also known as steroid-modified tinea, is a fungal skin infection that has been modified by the errant use of corticosteroids and calcineurin inhibitors.21 Superficial dermatophytosis can be exacerbated through the use of combination medications, such as Lotrisone (clotrimazole and betamethasone), because potent steroids may negate the effect of antifungal agents.21 It is suspected that topical corticosteroids may affect the ability of Langerhans cells in the epidermis to recognize antigen receptors, worsening tinea infections.19 Therefore, the use of combination fungal-steroid creams, corticosteroids, and calcineurin inhibitors should be avoided.
When suspecting a fungal infection, it is typically recommended to start a topical antifungal, such as ketoconazole cream daily for 2 to 4 weeks. If KOH or culture confirms a widespread dermatophyte infection, then terbinafine is recommended as a first-line oral antifungal treatment. If 250 mg/d terbinafine fails after 2 weeks, then 200 mg itraconazole twice daily can be considered for 1 week. This antifungal may have more severe adverse effects, such as rhabdomyolysis, so it should only be used if the athlete has a contraindication for terbinafine or fails first-line treatment. Other risk factors for rhabdomyolysis include physical exertion and heat exposure, so it is important to encourage athletes to take frequent breaks, rest in cooler areas, and vigorously hydrate to prevent adverse infections. In addition, athletes who are prescribed itraconazole should refrain from alcohol use. Itraconazole may also cause undesirable drug–drug interactions because it inhibits CYP3A4 substrates.
Many studies support that Trichophyton tonsurans and other dermatophytes have shown increasing resistance to terbinafine because of point mutations found in the gene for squalene epoxidase (SE), an enzyme that blocks the biosynthesis of ergosterol in the cell wall of fungi. However, 1 study conducted by Sardana et al suggests that the recent rise in antifungal failure may instead be affected by other factors, such as host immune response. Dermatophytes induce inflammatory cytokine production from keratinocytes through toll-like receptor 2 (TLR 2). This immune response involves Th2, which leads to persistence of infection, along with Th1 and Th17. In addition, lipase and phospholipase activity of Malassezia can damage the epithelial barrier and lead to chronic, low-grade inflammation in athletes. This mechanism suggests that resistance may not be the leading cause of treatment failure but rather the host–fungal interaction and immune response.
Recalcitrant fungal infections require a nuanced approach to antifungal selection in combat athletes to minimize lost practice time and decrease medical costs. Although Sardana et al did not find increased resistance to terbinafine in vitro, many clinical case studies highlight the shift from terbinafine to other antifungals, such as itraconazole and fluconazole.22 Recommended dosing for these antifungals are 200 mg itraconazole twice daily for 1 week or 150 mg fluconazole once weekly for 2 to 6 weeks. In addition, voriconazole has shown to be a good alternative for more severe infections, because it is highly effective and safe.23 When comparing the efficacy of voriconazole with that of itraconazole and itraconazole–isotretinoin combination in a clinical study, complete clearance was found in 83.3% of patients taking voriconazole, 53.3% taking itraconazole, and 70% taking the itraconazole–isotretinoin combination.24 In addition, the voriconazole group experienced a significantly lower recurrence rate. Because voriconazole can cause photosensitivity, it is especially important to use sunscreen in outdoor sports. Some dermatologists advise against the use of voriconazole because of its phototoxic effects.
Finally, it is important to check baseline liver enzymes in infected athletes because terbinafine and itraconazole can further elevate liver enzymes. However, it is important to distinguish whether the elevation in aminotransferases is due to liver impairment or exercise-related muscle damage. Strenuous exercise can lead to elevated aminotransferases without liver injury.25 Liver damage is likely to occur when cholestatic serum markers, such as alkaline phosphatase (ALP), are elevated.
If KOH testing or culture confirms that a mold or yeast is the causative agent, then it is recommended to prescribe an “azole,” such as oral fluconazole. Studies have shown increased efficacy of oral antifungals for the treatment of MF over topical antifungals; however, the combination of oral and topical antifungals has also shown good results.26
A variety of preventative actions can be done to decrease the risk of developing or prolonging the occurrence of infections in athletes involved in direct-contact sports, such as covering turf burns, refraining from shaving body hair, cleaning equipment with antiseptic cleansers, not sharing towels or other equipment with other athletes, showering before using communal whirlpools, and showering quickly after engaging in exercise.
CONCLUSIONS
Wrestlers experience a variety of bacterial and fungal infections that can rapidly spread to other athletes. When commonly prescribed medications fail to eradicate these infectious agents, infection can prolong, leading to worsening of disease, increased risk of spread to other athletes, and increased time off from sports. Owing to recent rises in virulence of methicillin-resistant Staphylococcus aureus (MRSA) and terbinafine-resistant Trichophyton tonsurans, changes to commonly recommended medications are necessary while considering the physiology of combat athletes. It is important for physicians to direct appropriate treatment depending on the causative agent to ensure quick recovery and reduced transmission rates between athletes so they can return to training.
References