Introduction

A recent review has highlighted the paucity of both clinical and laboratory data on the role of S. aureus in the oral cavity in both health or disease.1 Some oral infections are caused at least in part by S. aureus, for example, angular cheilitis,2 parotitis3 and staphylococcal mucositis.4 Furthermore there is now a growing body of evidence to suggest that staphylococci can be frequently isolated from the oral cavity of particular patient groups such as children,5 the elderly4 and some groups with systemic disease, such as the terminally ill,6 rheumatoid arthritis7 and patients with haematological malignancies.8

The aim of this study was to identify the rate of S. aureus isolation from specimens submitted to a regional diagnostic oral microbiology laboratory over the period 1998–2000.

Materials and methods

A hand search was conducted of laboratory work sheets compiled during 1998–2000.

Reports were searched for the isolation of S. aureus from specimens submitted to a regional oral microbiology diagnostic laboratory. The specimens most commonly submitted to the unit normally comprise dento-alveolar aspirates and swabs, oral mucosal swabs and oral rinses. Data were collected from the request form submitted by the clinician and the accompanying laboratory work sheet. The patient age, referring clinical unit, clinical presentation, specimen type and sensitivity to methicillin were recorded for each patient.

Results

The isolation rate of S. aureus over the 3-year period is shown in Table 1. For the period 1998–2000, there were 5,005 specimens submitted to the laboratory. S. aureus was isolated from 1,017 specimens, of which 967 (95%) were sensitive to methicillin (MSSA) and 50 (5%) were resistant to methicillin (MRSA). The 1,017 specimens were provided from 615 patients. MRSA was isolated from 37 (6%) of these patients.

Table 1 Number of MSSA and MRSA isolates per year
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There was an increasing incidence of S. aureus with age (Table 2) particularly in the >70 years age group. The most common specimen type (Tables 3a and 3b) from which MSSA was isolated was an oral rinse (38%) whilst for MRSA isolates this was a tongue swab (28%). Of interest was the recovery of S. aureus from six dento-alveolar abscess infections and one case of localised alveolar osteitis (dry socket). All of these isolates were sensitive to methicillin. S. aureus accounted for a small number of salivary gland infections from the parotid (n=3) and submandibular gland (n=1). The clinical condition most commonly reported for MSSA isolates (Table 4) was angular cheilitis (22%). A large proportion of both MSSA (25%) and MRSA (16%) were associated with erythema, swelling, painful or burning of the oral mucosa. Patients from which the MSSA isolates were recovered were most commonly (55%) seen in the oral medicine clinic at the dental hospital. Patients with MRSA were more commonly seen in primary care settings such as nursing homes, hospices and general dental practice (51%).

Table 2 Age distribution of patients with MRSA and MSSA
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Table 3 Details of specimen types containing MSSA
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Table 4 Details of specimen types containing MRSA
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Discussion

This study highlights the potential role of S. aureus in a number of oral diseases. However, it is difficult from this retrospective study to ascribe a pathogenic role to the S. aureus isolates, which may have been colonising rather than infecting the oral cavity. S. aureus infection is commonly associated with angular cheilitis and the findings of this study have confirmed those of earlier workers, suggesting a S. aureus isolation rate of 63% from angular cheilitis.2

Of interest was the isolation of S. aureus from a small number of acute dento-alveolar infections, such as a dental abscess. The acute dento-alveolar abscess is more usually associated with strict anaerobes and S. anginosus group streptococci.

There was a trend to increased recovery of S. aureus isolates from more elderly patients in contrast to previous work9 which found no age related trend for the recovery of S. aureus from a healthy population. It is unclear whether this reflects changes in the oral flora associated with increasing age, medication, increased incidence of prosthetic oral devices or referral patterns. The presence of prosthetic devices within the oral cavity, such as acrylic dentures, may encourage the carriage of staphylococci.10 In studies of denture wearing patients, carriage rates of S. aureus have varied from 23–48%.11,12

In a study of 110 patients attending a dental hospital with a range of oral diseases there was an observed prevalence of S.aureus in saliva of 21% and from gingival swabs of 11%.13 Salivary carriage of S. aureus in a cohort of patients with reduced salivary flow rates attending an oral medicine clinic was found in 41% of patients with a range of concentrations from 3.7×101 – 5.2×103 cfu ml−1.14

The case for S. aureus in the aetiology of oral dysaesthesia and mucositis is complicated by the diversity of the normal oral flora and by healthy carriage of S. aureus in some patient groups. However, the high rates of recovery of S. aureus from patients presenting with symptoms from the oral mucosa ranging from pain, burning, erythema and swelling, suggests that clinicians should address the possibility of this agent playing a role in oral mucosal disease. Isolates of S. aureus are capable of producing a wide range of exotoxins which has been noted in oral isolates. A study of staphylococcal carriage in children attending a paedodontic department found that 19% of the S. aureus isolates produced exfoilotive toxin and 40% produced enterotoxin.5

Of concern was the small but significant number of MRSA isolates recovered from oral specimens. This may reflect the increasing reservoir of community MRSA, for example, 17% of nursing homes in one locality.15 The prevention of horizontal transmission of MRSA has become increasingly more important as the prevalence of this pathogen increases. Oral carriage of MRSA may serve as a reservoir for recolonisation of other body sites or for cross-infection to other patients or healthcare workers. At least two cases have been reported of cross infection from a general dental practitioner to patients.16 The practitioner had probably been colonised whilst a patient in hospital. Nursing homes are another important source of colonisation and infection and two cases of acute parotitis caused by MRSA in elderly patients have been described.17 Within the oral cavity MRSA may preferentially colonise denture surfaces. One group of workers12 found 10% of unselected denture wearing patients carrying MRSA on their dentures which proved difficult to eradicate using conventional denture cleaning agents. In a subsequent study, eradication of the long term carriage of MRSA from denture wearing patients was successful only after heat sterilising or remaking the dentures that had become persistently colonised by MRSA.18 More recently, 19% of an elderly institutionalised veteran population were shown to be colonised by MRSA in the oral cavity, compared with a prevalence of 20% in the nares. Interestingly 4% of subjects were culture positive for oral MRSA without evidence of nasal carriage.18

In conclusion this study suggests that oral carriage of S. aureus may be more common than previously recognised and the data collected suggests a reappraisal of the role of S. aureus in the health and disease of the oral cavity.

Table 5 Clinical details from which MRSA and MSSA were recovered
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