JADA Continuing Education
Methicillin-Resistant Staphylococcus aureus
A Primer for Dentists
R. Monina Klevens, DDS, MPH,
Rachel J. Gorwitz, MD, MPH and
Amy S. Collins, BS, BSN, MPH
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ABSTRACT
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Background and Overview. In 2005 in the United States, an estimated 94,370 new, invasive infections and 18,650 deaths were associated with methicillin-resistant Staphylococcus aureus (MRSA); most of these infections were in people with exposures in health care settings. MRSA also has emerged as a community-based pathogen, causing primarily skin infections that are not life-threatening, but occasionally causing more severe and invasive infections. The authors describe the history of MRSA; identify populations at greatest risk of experiencing MRSA colonization and infection; compare characteristics of MRSA infections occurring in health care and community settings; and summarize strategies, based on U.S. Centers for Disease Control and Prevention recommendations and the literature, to prevent transmission of MRSA in dental offices.
Conclusions and Clinical Implications. Standard infection control precautions should be enforced strictly in all ambulatory care settings, including dental offices, to prevent facility-based transmission of MRSA and other infectious agents.
Key Words: Methicillin-resistant Staphylococcus aureus; MRSA; Standard Precautions; Contact Precautions; dental office; infection controlAbbreviations: CDC: Centers for Disease Control and Prevention • EPA: U.S. Environmental Protection Agency • MDROs: Multidrug-resistant organisms • MRSA: Methicillin-resistant Staphylococcus aureus • NNIS: National Nosocomial Infections Surveillance • PFGE: Pulsed-field gel electrophoresis • PFTs: Pulsed-field types • PPE: Personal protective equipment • VRSA: Vancomycin-resistant Staphylococcus aureus
Staphylococcus aureus is a gram-positive coccus that frequently colonizes the nose and skin of healthy people, and it can cause a variety of localized and invasive syndromes, ranging from superficial skin infections to life-threatening pneumonia and bloodstream infections.1 Methicillin-resistant S. aureus (MRSA) refers to S. aureus that is resistant to all currently available β-lactam antimicrobial agents, including antistaphylococcal penicillins (methicillin, oxacillin, nafcillin) and cephalosporins. The objective of this article is to provide dental care professionals with basic, evidence-based knowledge about MRSA to inform their actions in preventing the pathogen’s transmission during clinical care and in supporting prevention in the community.
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HISTORY OF METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS
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S. aureus infections have plagued humans since Biblical times.2 The first therapeutic use of penicillin for a S. aureus infection in 1940 was followed quickly by the appearance of the first penicillin-resistant strains of S. aureus.3 Methicillin was introduced in 1960 to treat penicillin-resistant S. aureus infections and was followed in 1961 by the development of MRSA in the United Kingdom.4,5 In 1968, the first outbreak of health care–associated MRSA was reported in a U.S. hospital.6 In response to outbreaks of infectious diseases in health care settings, the U.S. Centers for Disease Control and Prevention (CDC) and volunteer hospitals developed the National Nosocomial Infections Surveillance (NNIS) system in 1970. The system’s goal was monitoring the incidence of health care–associated (nosocomial) infections and their risk factors and pathogens. Across time, data from NNIS have shown an important increase in the proportion of S. aureus infections caused by MRSA, from 2 percent in 1975 to 29 percent in 19917 to 64 percent in 2003 (in participating intensive care units).8 However, a recent analysis of data from the National Healthcare Safety Network indicated a decline in the rate of MRSA bloodstream infections associated with central venous catheters through 2007.9
MRSA emerged as a significant public health problem in the community in the late 1990s. In 1997, four previously healthy children, with no established MRSA risk factors, died in Minnesota and North Dakota as a result of systemic MRSA infections.10 For the next several years, public health personnel in multiple states investigated outbreaks of MRSA infections of the skin and soft tissue among diverse community populations, including American Indians,11 sports teams,12 correctional facility inmates13 and child-care attendees6,14—all groups with typically little or no previous contact with the health care system. Concerns about outbreaks in the community encouraged the CDC to conduct coordinated surveillance activities in the United States.
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CHARACTERISTICS OF METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS IN HEALTH CARE AND COMMUNITY SETTINGS
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To date, certain characteristics have differentiated MRSA in health care and community settings (Table 1
). These characteristics include the populations affected, predominant clinical syndromes and genetic and phenotypic characteristics of the isolates, such as strain types, antimicrobial susceptibility patterns and presence of genes coding for various toxins or virulence factors. These genetic differences suggest that MRSA strains associated with community transmission originated in the community, where community strains of methicillin-susceptible S. aureus acquired genes conferring methicillin resistance. Across time, distinctions between MRSA in community and health care settings have begun to blur, as MRSA strains considered to be of community origin have entered health care settings15 and acquired new resistance elements.16
Population affected and clinical presentation.
In general, patients in health care settings, especially acute care hospitals, are more vulnerable to all infections because of age, underlying disease, treatments that alter immune response or invasive medical procedures that interrupt normal skin barriers.17 Health care–associated MRSA infections most commonly manifest as surgical site infections, pneumonia or bloodstream infections, and they require treatment with systemic antimicrobial agents. In the community, outbreaks of MRSA infections have been reported in settings in which people are crowded, have frequent skin-to-skin contact, have compromised skin (cuts and abrasions), lack adequate hygiene practices and share personal items. About 77 percent of community-associated MRSA infections are localized in the skin in the form of pustules, boils or abscesses18 (Figure) and typically can be treated in outpatient settings, often without antibiotics.19 However, less frequently, community strains of MRSA can lead to severe infections20 and potentially to invasive disease that can be fatal.21
Antimicrobial susceptibility patterns.
In general, the MRSA strains most frequently associated with infections in health care settings are resistant to multiple classes of antimicrobial agents in addition to β-lactam agents. In contrast, MRSA strains in the community have been susceptible to most classes of antimicrobial agents other than β-lactams, macrolides and azalides (such as erythromycin and azithromycin).18 However, resistance to additional agents—including fluoroquinolones, tetracyclines and clindamycin—has been observed among community MRSA strains.16,18,20,22,23
Vancomycin remains an agent of choice for treatment of invasive MRSA infections. However, increased use of vancomycin has contributed to a rapid increase in the incidence of colonization and infection with vancomycin-resistant enterococci in U.S. hospitals.24 Coexistence of vancomycin-resistant enterococci and MRSA in the same host was shown to facilitate the transfer of vancomycin resistance to S. aureus.24 In 1995, the CDC’s Hospital (now Healthcare) Infection Control Practices Advisory Committee developed and released its Recommendations for Preventing the Spread of Vancomycin Resistance.25 As of 2006, seven clinical cases of vancomycin-resistant S. aureus (VRSA) had been reported in the United States.26 Antimicrobial treatment options exist for vancomycin-resistant S. aureus infections but are limited.
Molecular characterization.
The CDC has primarily used a type of genotyping known as pulsed-field gel electrophoresis (PFGE) for molecular typing of S. aureus strains.27 Using this information, the CDC developed a PFGE nomenclature scheme and created a database identifying major MRSA lineages present in the United States, referred to as "pulsed-field types" (PFTs).28 The PFTs primarily associated with transmission in health care settings are USA100, USA200 and USA500, and those primarily associated with community transmission are USA300, USA400, USA1000 and USA1100.28–31
USA300 has emerged as the major community MRSA PFT in most areas of the country.32 The spread of USA300 as a common cause of community-associated S. aureus infection suggests that it has unique virulence and transmissibility factors. The relative importance of various toxins and other genetic elements in the pathogenicity of USA300 is an area of ongoing investigation.33 At present, testing of MRSA isolates for identification of specific virulence factors to inform clinical management of disease in individual patients is not recommended.
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THE OCCURRENCE OF MRSA IN THE UNITED STATES
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Colonization.
Colonization refers to the presence of microorganisms growing and multiplying in or on a host without causing disease. Approximately 30 percent of people in the United States carry S. aureus in their noses (anterior nares).34 Skin and mucosal membranes normally function as barriers to prevent tissue invasion in colonized people; however, any activity that promotes breakdown in the skin and mucosal integrity (such as chronic skin infections, physical trauma or poor health) can promote infection. Colonized people are capable of transmitting S. aureus to other people with whom they have close contact, and people who have active infections such as purulent skin infections offer a greater risk of transmission.
In 2003 and 2004, results of a national survey of S. aureus and MRSA nasal colonization among noninstitutionalized people in the United States showed that 28.6 percent were colonized with S. aureus, but only 1.5 percent carried MRSA.34 This corresponds to an estimated 78.9 million and 4.1 million people colonized with S. aureus and MRSA, respectively, in the United States.34 MRSA colonization was most prevalent among people 60 years or older.35 Among MRSA-colonized people, 19.7 percent were colonized with PFTs USA300 or USA400; USA1000 and USA1100 were rarely identified. Investigators in some smaller studies focusing on patients seeking health care have identified higher rates of MRSA nasal colonization. For example, among pediatric patients making health maintenance visits to two clinics in Tennessee, MRSA nasal colonization increased from 0.8 percent in 2001 to 9.2 percent in 2004.36 In addition, 22 percent of children admitted to a children’s hospital in Dallas during one month in 2005 had nasal colonization with MRSA on admission,37 as did 7.3 percent of adolescent and adult patients admitted to a public urban hospital in Atlanta during a one-month period in 2003.38 Other populations with a higher occurrence of MRSA colonization than the general population include patients undergoing hemodialysis,39 residents of nursing homes40 and patients admitted to hospitals.41
MRSA colonization is a risk factor for development of Methicillin-resistant Staphylococcus aureus infections in both health care and community settings.
Investigators in a small number of studies have looked at MRSA colonization of the oral cavity. In a study of patients undergoing dialysis in a hospital who were screened for MRSA, 25 percent had MRSA recovered from specimens from the anterior nares and tongue.42 In a study in which researchers monitored three years of records from a regional oral microbiology laboratory, S. aureus was isolated in oral cavity specimens from 1,017 of the 5,005 specimens; of these, 50 specimens in 37 of 615 patients (6 percent) were MRSA.43 MRSA has been found in the oral cavity more frequently in people 70 years or older43 and, in another study of people with MRSA colonization, has been found in multiple body sites and on dentures.44 A risk factor for oral carriage of MRSA among older people in hospital-based long-term care is related to antibiotic use, low serum albumin levels and poor nutrition.45
MRSA colonization is a risk factor for development of MRSA infections in both health care and community settings. Results of a study in five hospitals showed that MRSA infection was about 10 times more frequent among patients who were colonized with MRSA at admission compared with those who were colonized with susceptible S. aureus.46 In the community, researchers followed a cohort of soldiers for eight to 10 weeks, during which 38 percent of those colonized with MRSA developed an infection and only 3 percent of those colonized with susceptible S. aureus developed a MRSA infection.47
Infection.
Administrative data captured in nationally representative ambulatory care surveys indicate that from 2001 through 2003, there were 11.6 million outpatient visits annually in the United States associated with skin and soft-tissue infections typical of S. aureus, such as abscess, cellulitis, impetigo, carbuncle and furuncle.48 This finding corresponded to an annual visit rate of 410.7 visits per 10,000 people. Rates of visits to hospital outpatient departments and emergency departments for these visits increased by 59 percent and 31 percent, respectively, from 1992 through 1994 and from 2001 through 2003, possibly reflecting the emergence of MRSA as a community pathogen.48 Visit rates for these infections were highest for children younger than 2 years and people 65 years or older and were higher in the South than in the Midwest and among patients receiving Medicare and Medicaid than among patients with private insurance or no insurance. Between the two periods examined, rates increased in metropolitan statistical areas in the South and decreased in the Midwest. Since the 1990s, MRSA has accounted for an increasing proportion of community-associated S. aureus infections in the United States.49 In a 2004 study of adult patients with purulent skin and soft-tissue infections presenting to emergency departments in 11 U.S. cities, MRSA accounted for 78 percent of S. aureus skin and soft-tissue infections and 59 percent of skin and soft-tissue infections overall.20 In the head and neck area, community-associated MRSA increased as a proportion of all S. aureus infections in one otolaryngology clinic from 21 percent in 2000 to 64 percent in 2004.50
Since 2003, the CDC has supported routine surveillance for invasive infections in nine sites participating in its Emerging Infections Program. A case of invasive infection is defined by the isolation of MRSA from a normally sterile body site (such as blood, cerebrospinal fluid or pleural fluid). During 2005, the estimated number of new invasive MRSA infections in the United States, stratified by age, was 94,370 (Table 2).21 Rates of invasive infection were highest among men, people 65 years and older and African-Americans. Approximately 85 percent of all invasive MRSA infections occurred in people with health care risk factors (such as a history of MRSA, hospitalization, surgery, dialysis or residence in a long-term care facility within the previous year, or presence of an invasive device at the time of evaluation). An estimated 18,650 people with invasive MRSA died in the United States in 2005.
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TABLE 2 Estimated number and incidence of invasive MRSA* infections and deaths per 100,000 people in the United States, by age group, Active Bacterial Core surveillance, 2005.
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TRANSMISSION OF MRSA
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In health care settings.
In health care settings, S. aureus most often is spread indirectly from patient to patient on the transiently contaminated hands of health care professionals. Colonized health care personnel and visitors also sometimes can serve as reservoirs for transmission. MRSA has been isolated from environmental surfaces in health care facilities,51 but contaminated environmental surfaces and objects likely play a relatively minor role in MRSA transmission.52 In a study of S. aureus in a dental school clinic, investigators isolated MRSA from samples collected from the emergency treatment area: dental chair push buttons, light handles, air-and-water syringes and a computer keyboard; they did not evaluate transmission from the environment to patients or staff members.53
There has been one documented transmission of MRSA from a British dental practitioner to patients.54 Two patients undergoing oral surgical procedures within three weeks of each other developed MRSA infections of the same type. The dentist was identified as the only staff member with the same type of MRSA isolated from his fingers and nares. Of note, the dentist may have been colonized during a recent hospitalization for emergency surgery at a time when the hospital surgical unit was dealing with an outbreak of MRSA. The dentist was treated, and infection control practices were instituted in his practice, including the routine use of gloves. After nine weeks, no further MRSA was detected.
In the community.
In the community, S. aureus, including MRSA, can be spread among people having close skin-to-skin contact with an infected person. Draining lesions are highly infectious and represent the most common source of transmission. Spread also may occur through indirect contact by touching objects (such as towels, sheets, wound dressings, clothes, workout areas or sports equipment) contaminated by the infected skin of a person with MRSA.
Frequent exposure to antimicrobial agents may facilitate acquisition of MRSA. For example, in a case-control study conducted during a large community outbreak of MRSA skin and soft-tissue infections in southwestern Alaska, case subjects received significantly more courses of antimicrobial agents for nonskin infections during the 12 months before the outbreak than did age-matched control subjects without skin and soft-tissue infections.11 In an outbreak of MRSA skin and soft-tissue infections among professional football players, the risk of infection was almost eight times higher among players who had received antimicrobial agents in the year preceding the outbreak than among those who had not. Furthermore, the number of antimicrobial prescriptions received in the year before the outbreak was 10 times higher among members of the team who experienced the outbreak than among people of the same age and sex in the general community.55
In outpatient dental offices, strict enforcement of Standard Precautions is considered adequate in most circumstances to prevent the transmission of methicillin-resistant Staphylococcus aureus.
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PREVENTING MRSA TRANSMISSION
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In health care settings.
The CDC’s Healthcare Infection Control Practices Advisory Committee56 developed measures to control the spread of multidrug-resistant organisms (MDROs) of epidemiologic importance, such as MRSA, in health care settings. Prevention of MRSA and other MDRO transmission in these settings requires a comprehensive strategy that includes administrative measures (such as systems support and provision of resources); education and training of health care personnel; judicious use of antimicrobial agents; use of what the CDC classifies as Standard Precautions for all patients; use of Contact Precautions in acute care hospitals for patients known to be infected or colonized with these organisms; and ongoing monitoring of trends through time to measure progress in prevention and control. If rates do not decline despite these measures, additional intensified interventions—such as use of active surveillance cultures to identify colonized patients and implementation of Contact Precautions (see below)—are recommended.
Standard Precautions.
Standard Precautions are recommended for use with all patients in all health care settings to protect health care personnel and patients from contact with microorganisms, regardless of whether the source is recognized.57 Standard Precautions are based on the assumption that every person potentially is infected or colonized with an organism that could be transmitted in a health care setting. These precautions include the following:
- – performance of hand hygiene before and after having direct contact with patients or when moving from a contaminated body site to a clean body site during patient care;
- – use of personal protective equipment—such as gloves, gowns, and mouth, nose, and eye protection—for anticipated contact with blood or other potentially infectious materials, mucous membranes, nonintact skin or potentially contaminated intact skin (such as that of a patient incontinent of stool or urine);
- – use of respiratory hygiene and cough etiquette;
- – placing patients who pose a risk for transmission to others (for example, those with uncontained secretions, excretions or wound drainage) in a single-patient room when available;
- – establishing policies and procedures for containing, transporting and handling patient-care equipment and devices that may be contaminated with blood or body fluids;
- – establishing policies and procedures for routine and targeted cleaning of environmental surfaces;
- – use of safe injection practices.
In ambulatory care settings, including outpatient dental offices, strict enforcement of Standard Precautions, including making sure that gloves and gowns are used for anticipated contact with uncontrolled secretions and other potentially infectious body fluids, is considered adequate in most circumstances to prevent the transmission of MRSA and other MDROs. For this reason, dentists do not need to determine patients’ MRSA status routinely by means of history-taking or surveillance cultures or testing.
Dental procedures routinely require contact with saliva, blood and intraoral mucous membranes, all of which are potentially infectious. Table 3 provides a summary of infection control practices such as hand hygiene58,59 and use of personal protective equipment60 that prevent transmission of infectious agents (including MRSA) in the dental office. Few studies have been conducted to determine whether any additional actions can improve prevention of MRSA in dental settings. Investigators in one such study described the elimination of MRSA from patients’ dentures by use of common denture-cleansing solutions.61 Researchers in another study found that the rate of bacteremia occurring within one hour after a tooth extraction can be reduced by means of a preoperative rinse with an oral chlorhexidine solution.62
Contact Precautions.
Contact Precautions are recommended in addition to Standard Precautions in acute care hospitals for patients known to be infected or colonized with an MDRO and for certain patients in ambulatory settings (such as those with uncontrolled wound drainage or other syndromes that represent increased risk of contact transmission).57 These additional measures include patient placement in single-patient rooms when available or grouping as roommates patients who are infected or colonized with the same pathogen, use of personal protective equipment (gown and gloves) on room entry, transporting and moving patients outside of the room in acute care hospitals only for medically necessary purposes, use of single-use or patient-dedicated noncritical patient-care equipment (such as blood pressure cuffs) and ensuring that rooms of patients subject to Contact Precautions are prioritized for frequent cleaning and disinfection. In outpatient settings, such as a dental clinic, Contact Precautions would be indicated only in a situation in which a patient had uncontained drainage of an infected wound.
In the community.
No S. aureus vaccines are available, although such products are being developed.63 Optimal strategies for prevention of MRSA in the community have yet to be determined; however, an emphasis on general hygiene and wound care is imperative. In community outbreak settings, transmission has been interrupted after implementation of multicomponent strategies focusing on increased awareness, prompt identification and appropriate management of new infections, education on wound care and containment, enhanced hygiene, restricting shared use of potentially contaminated items such as clothing and towels, regular cleaning of frequently touched environmental surfaces, and restricting infected people from participation in certain close-contact activities if wound drainage cannot be contained.55,64
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CONCLUSIONS
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This article briefly describes the history and epidemiology of MRSA in health care and community settings and summarizes recommended control strategies in these settings. Dentists’ implementation of appropriate infection control practices can prevent and control transmission of bacteria and viruses in their offices; MRSA is only one of these pathogens. Dentists also can help educate the public on how to prevent and manage MRSA in the community. In dental offices, the risk of transmission of MRSA is lower than in acute care hospitals, and Standard Precautions combined with other selected measures are recommended. In the community, dentists’ awareness of opportunities for direct contact and factors that facilitate MRSA transmission—such as crowding, physical contact and lack of hygiene—will facilitate their support of community prevention.
The CDC has developed resources for health care professionals, including dental health care workers, and for patients56–60,65,66; it is hoped that readers will find them helpful in the battle against MRSA.
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FOOTNOTES
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Dr. Klevens is a medical epidemiologist, Division of Viral Hepatitis, Centers for Disease Control and Prevention, 1600 Clifton Rd. (G-37), Atlanta, Ga. 30333, e-mail "rmk2{at}cdc.gov". Address reprint requests to Dr. Klevens.
Dr. Gorwitz is a medical epidemiologist, Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta.
Ms. Collins is an epidemiologist, Division of Oral Health, Centers for Disease Control and Prevention, Atlanta.
Disclosures. None of the authors reported any disclosures.
The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the U.S. Centers for Disease Control and Prevention, Atlanta.
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ABSTRACT
HISTORY OF METHICILLIN-RESISTANT...
