Sports Dentistry

Possible disease transmission by contaminated mouthguards in two young football players

R. Thomas Glass, DDS, PhD n C. Rieger Wood, DDS n James W. Bullard, BA, MS n Robert S. Conrad, PhD

Previous studies have demonstrated that athletic mouthguards of exercise-induced asthma so severe that his inhaler could not worn by ice hockey and football players harbor large numbers of control the symptoms enough for him to resume play. This child’s bacteria, yeasts, and molds, some of which are either opportunistic mouthguard was contaminated with five different species of mold. or frank pathogens. This article details the clinical history of two The clinical implications of mouthguard contamination, possible junior high school football players. The first player had cellulitis avenues of disease transmission, and recommendations for of the leg after a non-break injury. The same unusual bacterium mouthguard care are discussed. was isolated from both the athletic mouthguard and abscess Received: March 26, 2007 cultures from the wound. The second patient suffered an attack Accepted: May 25, 2007

he vulnerability of teeth to biofims (Fig. 2). nated with Gram-negative bacteria trauma from contact sports These studies also demonstrated (especially Pseudomonas spp.) and T(such as football and ice hockey) that used mouthguards have sharp yeasts such as Candida spp. has underscored the protection and jagged edges capable of lacerat- Several articles further underscore provided to the dentition by athletic ing the oral tissues. This means the unique types of infectious dis- mouthguards.1-7 The ADA also has that the mouthguard microorgan- eases associated with athletes. One recommended mouthguards for isms have direct access to the rich article documented the problems all contact sports.8 Football and vascular system of the oral cavity; in that football players, wrestlers, and ice hockey players at all levels have addition, the acts of swallowing and fencers experienced with methicil- been the most compliant in wearing mouth-breathing during mouth- lin-resistant Staphylococcus aureus mouthguards, to the extent that guard wear provide microorganisms (MRSA).20 An equally disturbing failure to do so can result in a team with direct access to the gastrointes- article described life-threatening penalty.9-12 tinal and respiratory tracts. bacterial meningitis affecting two Recent studies of mouthguards Recent studies have compared New Jersey high school students retrieved from football and ice the spectrum of microorganisms whose only connection was that hockey players found that these found in mouthguards worn by they both played ice hockey for devices harbor a wide range of football and ice hockey players the same team.21 Daum and opportunistic or frank pathogenic to those found in mouthguards Herold pointed out that the MRSA bacteria as well as fungi, including worn by medical student volun- problem has increased 25-fold in both yeasts and molds.13,14 When teers.14 In general, medical student children, especially boys “with no these mouthguards were examined mouthguards had fewer potentially identified risks.”22 A 2002 study by scanning electron microscopy pathogenic microorganisms than involving football and ice hockey (SEM), the matrices were found to those worn by either football or ice players found S. aureus in 31% of be equally porous to dentures, as hockey players. the football players’ mouthguards reported in the literature (Fig. 1).15-19 Mouthguards worn by football and 47% of the ice hockey players’ Microorganisms were found both players had large quantities of soil mouthguards, compared to only on the surfaces and in the porosities microorganisms such as Bacillus 14% of the medical student mouth- of the used mouthguards; these cereus, Rhodotorula spp. (yeasts), guards.14 microorganisms often were incorpo- and molds. Ice hockey players’ Although opportunistic and rated into well-established, complex mouthguards were heavily contami- pathogenic microorganisms have

436 September/October 2007 General Dentistry www.agd.org Mycotic biofilm

10 µm 10 µm

Fig. 1. An example of a football mouthguard that has been boiled but Fig. 2. A mouthguard that has been both boiled and worn. Note the not worn. Note the large defects in the surface that would allow for complex biofilm on the surface that also can be seen penetrating into the microorganism penetration. (Original magnification: 1,000x.) mouthguard porosities. (Original magnification: 2,000x.)

24 hours

48 hours

36 hours

Fig. 3. The “boil and bite” mouthguard worn by a 13-year-old football Fig. 4. The left leg of the patient in Figure 3. Note the substantial swell- player. Note the rough posterior edges (arrows). ing over a period of 48 hours since the onset of symptoms (the numbers and black markings designate the swelling over that period of time).

been found in the mouthguards dered for testing on October 17 of the left tuberosity, and the gingiva of football and ice hockey players, that same year. The only significant associated with teeth No. 5, 15, actual clinical cases have not been dental finding was that the young and 18, which she attributed to the attributed to mouthguard wear. man had full maxillary and man- mouthguard wear. He continued to This article presents two cases of dibular orthodontic banding, which practice and wear his mouthguard probable transmission of disease by had been placed six months earlier. for another ten days. On October contaminated mouthguards. On October 4, approximately 15, his left leg became feverish, red, six weeks after contact drills began, and swollen (Fig. 4). Case report No. 1 the young man’s lower left leg was Within 24 hours, the patient’s leg A 13-year-old male football player injured when he was struck by an had swollen to approximately twice began the season practicing twice a opponent’s helmet. There was no its normal size and he was barely day, starting on August 20. Prior evidence of a visible bruise or lac- able to walk. He was taken to the to his first practice, he form-fitted eration. His mother noted that he emergency room of the local hospi- a “boil and bite” mouthguard (Fig. had ulcerations of his right buccal tal, where blood cultures were made 3) and wore it until it was surren- mucosa, the mucosa associated with and he was placed on IV antibiotics

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(ampicillin). When he failed to and the microorganism was found respond to antibiotic treatment and to be susceptible to bacitracin, the swelling continued to advance, erythromycin, tetracycline, and he was transferred to a large metro- (intermediately) to ciprofloxacin. It politan hospital. Upon his arrival at was resistant to oxacillin, penicillin the emergency room, he was placed G, gentamicin, and polymyxin B. on IV vancomycin. When the Considering the resistance pat- swelling continued to increase and terns of the isolated microorganisms disseminate, the IV antibiotic was and the clinical response in this case, changed to nafcillin, a beta-lactam the most probable agent producing commonly used against MRSA. the cellulitis was S. mucilaginosus. Over the next 24 hours, the swell- The most feasible transmission Fig. 5. The mouthguard of the patient in ing and cellulitis continued. At route would have been from the Figure 3. This mouthguard had been worn the same time, the lymph nodes in mouthguard into the vascular for approximately six weeks. Note the rough the left groin became tender and system via the mucosal ulcerations. and jagged edges over the entire mouthguard swollen. High levels of IV antibiot- The noninvasive injury of the leg surface. ics were administered, alternating could have increased the blood flow between vancomycin and nafcillin. in the region, allowing the vascular- On October 20, the wound was disseminated S. mucilaginosus to incised and drained. The gram stain invade the region of the injury and revealed Gram-positive cocci in short produce cellulitis. The microorganisms on the surfaces chains that were not further isolated and depths were cultured on blood or identified. However, a clinical Case report No. 2 agar, chocolate agar, and Sabourard diagnosis of MRSA was made solely This 13-year-old boy began his dextrose agar. The cultures revealed on the basis of Gram stain and football career in the first grade a variety of bacteria, including antibiotic response. The original and routinely wore a custom-made Bacillus spp., Corynebacterium spp., blood cultures also were negative. mouthguard from that time to the and Listeria spp. More importantly, Doppler examination of the left leg present. By the end of his first six isolates of Rhodotorula spp. and revealed no evidence that a deep season, he began to develop early five species of mold were isolated vein thrombosis was an etiology for symptoms of exercise-induced (Fig. 6). the cellulitis. The swelling slowly asthma (EIA). His pediatrician Given the variety of yeasts and subsided over the next two weeks. treated him with an oral bronchodi- molds found in the mouthguard On October 17, the mouth- lator inhaler. Over the next six years and the course of the subject’s EIA, guard (Fig. 3) was brought to the of football play, the subject’s EIA it is likely that the two are related Infectious Disease Laboratory at symptoms varied but overall became etiologically. While exercising Oklahoma State University Center progressively more intense. Midway vigorously on the field, the subject for Health Sciences (OSU-CHS). through the 2006 football season, presumably was aspirating yeasts Both the surfaces and depths of the subject had a severe asthma and mold spores into his respiratory the mouthguard were cultured attack during practice which his tract. There is a well-established using standard aseptic techniques. bronchodilator could not control connection between aspiration of While the cultures yielded isolated and he required additional medical yeasts and mold spores and the colonies of S. saprophyticus and S. attention. The subject’s father onset of asthma attacks in sensitized xylosus, the predominant bacteria brought the EIA to the attention individuals. If the insult of the were Gram-positive stomatococcus of his dentist, who asked to have yeasts and mold spores was suf- mucilaginosus and five isolates of the mouthguard cultured. Within ficient to cause EIA in this case, it Bacillus spp. In addition, six dif- two days of the most recent asthma probably would be refractory to the ferent isolates of the pink soil yeast attack, the mouthguard was brought type of topical inhalation therapy Rhodotorula and five species of to the Infectious Disease Laboratory that was attempted. Equally molds were identified. Antibiotic at OSU-CHS (Fig. 5). compelling is the finding that the sensitivity tests were performed on The mouthguard was processed subject also plays basketball but the Stomatococcus mucilaginosus using standard aseptic techniques. does not wear a mouthguard during

438 September/October 2007 General Dentistry www.agd.org both of the mouthguards in this report. A previous study of col- lege football players’ mouthguards also isolated a large number of Rhodotorula spp.14 It remains to be seen whether their presence in the mouthguards is mere coincidence or if they are active participants in a disease process such as EIA. These findings raise interesting Left Right clinical conundrums. The char- Fig. 6. Fungal cultures from the mouthguard in Figure 5. Note the quantity of yeasts and molds and acteristics of the microorganisms the variety of colonial morphologies that represent different species. isolated from the mouthguards enable them to disseminate systemi- cally and/or be aspirated into the respiratory tract. As a result, the immune system would be compro- practices or games and has had no (such as endocarditis) that ultimately mised and athletes would be more evidence of EIA to date while play- may lead to a cerebral mycotic susceptible to diseases such as those ing this sport. aneurysm.23-25 Other studies have demonstrated in these two cases. reported that Stomatococcus muci- The spectrum of microorganisms Discussion langinosis septicemia can be found in found in mouthguards raises the Two cases of serious disease were patients with chronic diseases and/or question as to whether the risk from present in otherwise healthy young compromised immune systems.26-30 wearing mouthguards is worth the athletes. In both of these otherwise The second case report is associ- tooth protection they provide. diverse clinical cases, the subjects ated with football but not basket- Finally, could these life- and/or played football and wore mouth- ball, suggesting that this athlete’s health-threatening conditions be guards that were contaminated condition does not strictly fulfill avoided by routine sanitization with microorganisms that could be the criteria for classic EIA. Current of the mouthguards or must the responsible for their illnesses. theories of EIA etiology are related mouthguards be discarded on a In the first case, an unusual and to changes in osmolarity of the regular basis? At the present time, seldom-seen opportunistic pathogen, bronchi and changes in the airway there are no acceptable decontam- Stomatococcus mucilaginosis, was temperature.31 However, most stud- ination methods available. The cultured from the mouthguard and ies indicate that molds may function major problem is that mouthguards, most likely was the agent cultured as allergens and therefore may be like dentures, are very porous. With from the pus of the wound. Given etiologic factors for EIA.32 Allen use, microorganisms invade these the antibiotic resistance pattern of noted in 2005 that bronchoconstric- porosities and thrive in the presence this subject’s microorganisms and tion had increased “among athletes of food and water from their host his clinical course of oral ulcerations, from school children to Olympians athlete. Unfortunately, as with these findings would support an to professionals.”33 A second article dentures, it is very difficult for sani- etiological association. Additional noted a similar increase in “asthma tizing solutions to penetrate these support for this assertion is found and bronchial hyperresponsiveness” pores. However, the biting actions in several studies that point out the that appeared to be more common athletes perform during mouthguard inconsistent antibiotic sensitivity among ice hockey players than in wear result in a systemic showering patterns of Stomatococcus mucilangi- “floor-ball players” or the Swiss of microorganisms throughout the nosis. Other reports highlight that population in general.34 oral cavity, esophagus, and trachea. Stomatococcus mucilaginosis is rarely As a possible example of molds or Based on the mouthguard studies to implicated as an etiological agent; yeasts causing EIA, the role of Rho- date, the authors recommend dis- however, it has been found in both dotorula spp. in the pathogenesis is posing of the mouthguards at least local cellulitis (cervical necrotizing intriguing, since this seldom-seen once a week. Another possibility is a fasciitis) and blood-borne diseases microorganism was isolated from single-use mouthguard. Regardless,

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it is imperative that dentists advise 2. Heintz W. Mouth protectors: A progress report. medical on dentures contaminated with known patients who are athletes concerning Bureau of Dental Health Education. J Am Dent microbial flora. An in vitro study. Quintessence Assoc 1968;77:632-636. Int 2004;35:194-199. the importance of proper mouth- 3. Fitted mouth guards afford key protection. J 19. Glass RT. Infection of dental implements and guard care. Am Dent Assoc 1972;84:531. appliances, part 2: The denture. Dent Today 4. Sane J. Comparison of maxillofacial and dental 2004;23:116-123. injuries in four contact team sports: American 20. Withers T. Staph infections rise among athletes. Summary football, bandy, basketball, and handball. Am J Available at: http://www.sfgate.com/cgi-bin The two cases presented in this Sports Med 1988;16:647-652. /article.cgi?f=/n/a/2006/11/25/sports article strongly implicate disease 5. McNutt T, Shannon SW, Wright JT, Feinstein RA. /s103621S23.DTL. Accessed June 2007. Oral trauma and adolescent athletes: A study of 21. Tsai J, Rosen D. Ramapo high athlete falls ill transmission by mouthguard wear. mouth protectors. Pediat Dent 1989;11:209- with meningitis. Available at: http://www While wearing a mouthguard to 213. .northjersey.com./page.php?qstr=eXJpcnk3Zjcx protect teeth is well-established and 6. Morrow R, Seals R Jr., Barnwell G Jr., Day E. Re- N2Y3dnFlZUVFeXkyJmZnYmVsN2Y3dnFlZUV port of a survey of oral injuries in male college FeXk3MDU4NDMx. Accessed January 2007. required in many sports, cases such and university athletes. Athletic Training 1991; 22. Purdy J. An enemy in our midst. Medicine on as those presented in this article 26:338-342. the Midway 2006;Summer:26-33. underscore the importance of proper 7. Labella CR, Smith BW, Sigurdsson A. Effect of 23. Lowry TR, Brennan JA. Stomatococcus muci- mouthguards on dental injuries and concus- langinosis infection leading to early cervical mouthguard hygiene. Previous sions in college basketball. Med Sci Sports necrotizing fasciitis. Otolaryngol Head Neck studies have shown that athletic Exerc 2002;34:41-44. Surg 2005;132:658-660. mouthguards can harbor a wide 8. Bureau of dental health education and bureau 24. Prag J, Kjoller E, Espersen F. Stomatococcus mu- of economic research and statistics. Mouth pro- cilaginosus endocarditis. Eur J Clin Microbiol range of opportunistic and frank tectors: 1962 and the future. J Am Dent Assoc 1985;4:422-424. pathogenic microorganisms. The 1963;66:539-543. 25. Perez-Vega C, Narvaez J, Calvo G, Castro-Bo- rough and jagged nature of worn 9. Moon DG, Mitchell DF. An evaluation of com- horquez FJ, Falgueras MT, Vilaseca-Momplet J. mercial protective mouthpieces for football Cerebral mycotic aneurysm complicating Sto- mouthguards allows for laceration players. J Am Dent Assoc 1961;62:568-572. matococcus mucilanginosis infective endocardi- of the oral tissues and for vascular 10. de Wet FA, Badenhorst M, Rossouw LM. Mouth- tis. Scand J Infect Dis 2002;34:863-866. dissemination of the microbes. The guards for rugby players at primary school level. 26. Poirier LP, Graudreau CL. Stomatococcus muci- J Dent Assoc S Afr 1981;36:249-253. laginosus catheter-associated infection with aspiration of the types of mold 11. Garon MW, Merkle A, Wright JT. Mouth protec- septicemia. J Clin Microbiol 1989;27:1125- found in mouthguards could be an tors and oral trauma: A study of adolescent 1126. important etiologic factor in the rise football players. J Am Dent Assoc 1986;112: 27. Ascher DP, Bash MC, Zbick C, White C. Sto- 663-665. matococcus mucilaginosus catheter-related in- of EIA seen in athletes. The authors 12. Berg R, Berkey DB, Tang JM, Altman DS, Londer- fection in an adolescent with osteosarcoma. recommend discarding mouthguards ee KA. Knowledge and attitudes of Arizona South Med J 1991;84:409-410. on at least a weekly basis. Because high-school coaches regarding oral-facial inju- 28. Relman DA, Ruoff K, Ferraro MJ. Stomatococ- ries and mouthguard use among athletes. J Am cus mucilanginosis endocarditis in the intrave- “boil and bite” mouthguards are so Dent Assoc 1998;129:1425-1432. nous drug abuser. J Infect Dis 1987;155: inexpensive, these might be consid- 13. Conrad R, Glass R, Bullard J. Microbial contami- 1080-1082. ered as single-use mouthguards. nation of hockey players’ protective mouth- 29. Weinblatt ME, Sahdev I, Berman M. Stomatococ- guards—An in vivo study. Abstract presented cus mucilanginosis infections in children with at: IADR 84th General Session Program Book; leukemia. Pediatr Infect Dis J 1990;9:678-679. Author information June 29, 2006; Brisbane, Australia. 30. Souillet G, Chomarat M, Barbe G, Balouck N, Dr. Glass is Professor of Forensic 14. Glass R, Bullard J, Conrad R. The contamination Ploton C, Philippe N. Stomatococcus mucilagi- of protective mouthguards: A characterization nosus meningitis in a child with leukemia. Clin Sciences, Pathology, and Dental of the microbiota found in football players’ pro- Infect Dis 1992;15:1045. Medicine and Adjunct Professor of tective mouthguards as compared to the oral 31. Storms WW. Review of exercise-induced asth- Microbiology, Oklahoma State Uni- microbiota found in first-year medical students. ma. Med Sci Sports Exerc 2003;35:1464-1470. Amer Dent Inst for Cont Educ J 2006; 93:23-38. 32. Breathing difficulties related to physical activity versity Center for Health Sciences in 15. Glass RT, Bullard JW, Hadley CS, Mix EW, Conrad for students with asthma: Exercise-induced Tulsa, where Dr. Conrad is a profes- RS. Partial spectrum of microorganisms found asthma. Available at: http://www.nhlbi.nih.gov sor of Microbiology and Chairman, in dentures and possible disease implications. J /health/prof/lung/asthma/exercise_induced.htm. Am Osteopath Assoc 2001;101:92-94. Accessed June 2007. Department of Biochemistry and 16. Glass RT, Goodson LB, Bullard JW, Conrad RS. 33. Allen TW. Return to play following exercise- Microbiology and Mr. Bullard is Comparison of the effectiveness of several den- induced bronchoconstriction. Clin J Sport Med Chief Laboratory Technician. Dr. ture-sanitizing systems: A clinical study. Com- 2005;15:421-425. pend Cont Educ Dent 2001;22:1093-1108. 34. Leuppi JD, Kuhn M, Comminot C, Reinhart WH. Wood is a general dentist in Tulsa. 17. Goodson L, Glass R, Bullard J, Conrad R. A sta- High prevalence of bronchial hyperresponsive- tistical comparison of denture sanitation using a ness and asthma in ice hockey players. Eur References commercially available denture cleaner with and Respir J 1998;12:13-16. 1. Stenger JM, Lawson EA, Wright JM, Ricketts J. without microwaving. Gen Dent 2003;51:148- Mouthguards: Protection against shock to the 152. Published with permission by the Academy of head, neck and teeth. J Am Dent Assoc 1964; 18. Glass RT, Bullard JW, Conrad RS, Blewett EL. General Dentistry. © Copyright 2007 by the Academy 69:273-281. Evaluation of the sanitization effectiveness of of General Dentistry. All rights reserved.

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