Transmission of blood-borne pathogens in US dental health care settings

METHODS

In 2012, the authors (J.L.C., S.K.G., J.A.H.) began a literature review to identify published reports of confirmed transmissions of BBPs in US dental settings since 2003. We defined transmissions as those situations for which the results of the epidemiologic investigation confirmed or identified a strong epidemiologic and molecular link between cases; we defined cases as people with acute viral hepatitis who visited the same dental clinic as other people who had acute or chronic viral hepatitis infection.^11,12 We conducted literature searches using Ovid MEDLINE, Web of Science, Cochrane Library, and the National Guideline Clearinghouse. Search terms included “disease transmission,” “surveillance,” “dental,” “dentistry,” “oral health,” “infection control,” “infection prevention,” “blood-borne pathogens,” “hepatitis B virus” or “HBV,” “hepatitis C virus” or “HCV,” “human immunodeficiency virus” or “HIV,” “occupational exposure,” “breaches,” “health care-associated infections” or “HAIs,” and “compliance.” We limited searches to articles published in English from January 2003 through November 2015, and we excluded editorials, expert opinions, and general reviews.

In addition, we reviewed published summaries from CDC's Division of Viral Hepatitis, which is part of the National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, of suspected health care–associated hepatitis transmissions reported by state and local health departments from 1998 to 2014.^11,12 HBV and HCV infections are reportable conditions in all states. Surveil-lance case report forms for viral hepatitis infections request information about potential behavioral risks, such as sexual contact and injection drug use, a history of working in a health care setting, and a history of receiving medical and dental treatment during the likely exposure period. State and local health departments investigate patients who do not report behavioral risk factors to determine potential sources of transmission. Although it is not mandatory for health departments to report suspected health care–associated hepatitis cases to the CDC, health departments can request that the CDC provide consultation and laboratory assistance to complete these investigations.

RESULTS

By searching the literature and reviewing reports to the CDC of transmission events from 2003 to 2015, we identified 3 episodes of BBP transmission in US dental settings (Table 1^8-10). In 2 episodes,^8,10 investigators confirmed a single instance of patient-to-patient transmission of either HBV or HCV. Both single-transmission episodes of BBPs occurred in outpatient oral surgery practices. In a third episode,⁹ investigators identified acute HBV infection in 3 patients and 2 DHCP who were volunteers and not involved directly in the delivery of clinical care (Box 1³). We did not identify any transmissions of HIV among dental patients or DHCP during our search.

In 2002, a state health department conducted an epidemiologic investigation of a person who had an acute HBV infection (Table 1).⁸ This index patient (that is, the first case or instance of a patient who came to the attention of health authorities) had no identified risk of developing infection, but the patient reported having recently had oral surgery involving intravenous (IV) sedation and undergone the extraction of 7 teeth. A retrospective investigation of the treating oral surgery practice revealed that another patient (the source patient), who had been seen earlier on the same day as the index patient, was listed on the state's reportable disease registry for HBV. Documentation showed that at the time the source patient had 3 teeth extracted under IV general anesthesia, she also had chronic hepatitis B and had tested positive for hepatitis e antigen with a high viral load. The findings of molecular genetic testing confirmed the transmission of HBV between this source patient and the index patient. During the investigation, office staff members reported that they had followed standard infection prevention and control practices. All staff members had been vaccinated, and none of them had HBV. The investigators only could speculate that the virus had been spread via an environmental surface that remained contaminated with blood, despite the staff members’ reportedly good cleaning practices. Furthermore, the fact that a substantial prevalence of previous vaccination (64%) among the patients who were treated after the source patient may have limited the potential for additional HBV transmissions.

In 2013, another single transmission of a BBP—this time involving HCV—from 1 oral surgery patient to another occurred¹⁰ (Table 1). The case was initially reported to state public health officials as a potential health care–associated HCV infection when a regular blood donor screened positive for HCV infection during a routine blood donation. All of the patient's previous blood donations, including 1 that had occurred in April 2012, had tested negative for HCV. The patient did not report having any typical risk factors for HCV infection, but the patient had undergone oral surgical procedures during multiple dental appointments at a single dental practice within the 3 months before testing positive for HCV. Investigators found multiple lapses of infection prevention and control practices, including but not limited to having dental assistants on staff who did not have appropriate certification and who determined dosage and administered IV sedation medication, improper dating and storage of multidose medication vials, use of single-dose medication vials for more than 1 patient, and a lack of autoclave monitoring and maintenance. Molecular testing conducted by CDC staff members compared HCV specimens from the index patient with another clinic patient who was known to be infected with HCV and who had undergone an oral surgical procedure on the same day as the index patient. These test results showed close molecular identity, which indicated a likely transmission between the 2 patients. Although the investigators identified multiple lapses in infection prevention practices, they concluded that it was possible that DHCP may have reused needles, syringes, or both to enter medication vials and then subsequently used one of those medication vials when treating another patient.¹⁰ This unsafe injection practice, which contaminates the contents of the medication vial, has been associated with the transmission of BBPs in a variety of health care settings.^13,14 The investigators did not identify any other cases of blood-borne infections that could be linked definitively to transmission among patients at this oral surgery clinic.

In 2009, investigators from the local and state health departments identified an outbreak of 5 acute HBV infections at a 2-day portable dental clinic⁹ (Table 1). Set up in a gymnasium, the dental clinic was staffed by 750 volunteers, and more than 1,100 adults received dental treatment. The 5 acute HBV infections included 3 patients and 2 DHCP who were not involved directly with patient care. All 3 patients had undergone extractions; 1 of the patients also had received restorations and another patient also received a dental prophylaxis. None of the 3 patients shared a treatment provider. One of the cases involved a member of the DHCP team at the clinic whose role was to maintain the dental equipment. The DHCP reported that, while wearing gloves, he had handled a blood-contaminated air compressor. He also reported having had frequent episodes of nose-blowing and had wiped sweat from his brow without removing his gloves. He also reported that he had worked at a similar clinic 2 weeks previously. When working at that clinic, he did not wear a mask or protective eyewear, and, while handling a full suction container, he had been splashed in the face by blood-contaminated saliva. The second case involving DHCP was a person who had directed patients from triage to the treatment waiting area. This person did not report having had any contact with blood. None of the 5 people who had acute HBV infections had reported having any behavioral risk factors for HBV, such as a recent history of injection drug use or multiple sex partners. By reviewing the state's HBV registry, the case investigators revealed 3 possible source patients (that is, patients who had positive serologic tests for hepatitis B surface antigens before they had visited the portable dental clinic). Serologic specimens were not available from these patients to conduct viral sequencing or to make comparisons with the outbreak cases.

The results of the investigation⁹ revealed several breaches of infection prevention practices that could have resulted in the exposure of patients, staff, and environmental surfaces to HBV and other BBPs. For example, reports indicated that the outer surfaces of dental handpieces had been cleaned with disinfectant wipes but were returned to service without being heat-sterilized before being used on other patients, that used instruments had been sterilized unwrapped, and that some patients had been allowed to carry their partially used anesthetic cartridges in the metal dental cartridge syringes on a tray to other stations if the anesthetic might have been needed for later reuse. Patient treatment chairs and portable dental units were in close proximity, and DHCP performed oral surgical procedures in treatment areas lacking physical barriers, such as curtains.

In addition, the results of the investigation⁹ revealed that volunteers who were not involved in patient care did not receive training about BBPs, and no one had verified their histories of having received the hepatitis B vaccination, even though the volunteers could potentially be exposed to blood. It was assumed that the licensed dentists and dental students who volunteered already received the HBV vaccination and training in preventing the transmission of BBPs. The clinic did have a policy for needlestick reporting and follow-up; however, written policies including training in and oversight for infection prevention and control were lacking. Written information about individual patient procedures and providers was limited. Despite the identification of breaches related to infection prevention and control during the clinic, it was not possible to retrospectively link specific practices to the transmission of HBV in this outbreak. Laboratory results from the patients’ HBV gene sequences showed that all were genotype D and that a partial gene sequence was identical in all cases; this finding provides limited evidence that these 5 outbreak cases could have been exposed to blood from a common source.

DISCUSSION

Infection prevention recommendations are designed to prevent or reduce the potential for disease transmission from patient to DHCP, from DHCP to patient, and from patient to patient. Patient-to-patient transmission of BBP can occur when lapses in basic infection prevention practices allow patients who are infected with HBV or HCV to serve as an indirect source of pathogens for disease transmission to other patients. For example, in a dental setting, DHCP should appropriately clean, disinfect, or heat-sterilize instruments and equipment before using them on another patient.^3,21 In addition, DHCP should barrier-protect or clean and disinfect environmental surfaces, including the light handle, chair controls, computer mouse, or keyboard, between patients.^3,21 Paying strict attention to aseptic technique when handling and administering parenteral medications, such as IV or intramuscular injections, can prevent the contamination of supplies used for injections, including medication vials, containers, needles, syringes, and IV tubing.^3,15 Finally, because contaminated hands can cause health care–associated infections (HAIs), proper use of gloves and performing correct hand hygiene is critical.^3,16,21

HBV and HCV transmission as a result of unsafe injection practices is well documented in US health care settings.^11,12,17-19 As a result of these transmissions, recommendations for safe injection practices are now basic elements of standard precautions^15,20 (Box 2²¹). Investigators of the 2013 event concluded that the dental patient-to-patient transmission of HCV likely was caused by DHCP reentering medication vials with a syringe that already had been used for a patient who had a chronic HCV infection and then using the contents of those vials for an injection in another patient.¹⁰ CDC recommends using single-dose medication vials whenever possible; if HCP must use multidose medication vials, they should dedicate the use of the vials to a single patient whenever possible. HCP should enter medication containers (single-dose and multidose medication vials, ampules, and bags) with a new needle and a new syringe, even when obtaining additional doses for the same patient. In addition, if HCP bring a multidose medication vial into an immediate patient treatment area, they should dedicate the vial for single-patient use and discard it immediately after use.^15,20,22 CDC recommendations for safe injection practices (Box 2²¹) apply not only when DHCP use parenteral medications combined with fluid infusion systems, such as for patients undergoing conscious sedation, but also when DHCP administer local anesthetic, during which they should use needles and cartridges containing local anesthetics for 1 patient only and ensure that the dental cartridge syringe is cleaned and heat-sterilized between patients.³

HBV and HCV can persist on environmental surfaces and devices contaminated with blood. HBV is a hardy virus that has been demonstrated to survive in dried blood at room temperature on environmental surfaces for at least 1 week.²³ In studies related to infectivity, the investigators have found that HCV can survive in the environment for up to 6 weeks on dry surfaces,^24,25 although most HCV transmissions occur through percutaneous exposure.^11,12 Strict adherence to CDC infection prevention recommendations for cleaning and disinfecting environmental surfaces and for packaging and heat-sterilizing contaminated instruments is critical in preventing the transmission of BBPs.^26,27

In this review, we described 3 events involving the transmission of BBPs that occurred in the United States between 2001 and 2013.^8-10 To put these events in context, we offer some historical comparisons of reported transmissions of BBPs in dental settings and the implementation of infection prevention recommendations. Before 1987, 9 outbreaks of HBV occurred in dental settings (general practice and oral surgery); the number of patients infected with hepatitis ranged from 3 patients in 1 outbreak to 55 patients in another.²⁸ In each practice, the dentist or oral surgeon also was infected. In addition, the results of serologic surveys indicated that there were a number of asymptomatic cases, suggesting that more transmissions had occurred in some of these outbreaks than had been reported.²⁸ To our knowledge, since 1987, there have been no transmissions of HBV or HCV in dental settings that involved an infected dentist or oral surgeon.

The hepatitis B vaccine became commercially available in 1982. Between 1983 and 1992, there was a 74% increase (from 22% to 85%) in the frequency of self-reported vaccination among US dentists participating in health screenings sponsored by the American Dental Association (ADA).²⁹ Serologic evidence of past HBV infection among dentists declined from prevaccine levels of 14% in 1972 to 9% in 1992, likely reflecting increased immunization and use of standard precautions.²⁹ From 1993 to 2007, levels of HBV infection among dentists remained relatively unchanged (Steven Gruninger, MS, senior research fellow, Research and Laboratories, Science Institute, American Dental Association, Chicago, IL, written communication, September 2014).

The average (standard deviation) prevalence of HCV antibodies among US dentists participating in ADA health screenings from 2000 to 2005 (0.47% [0.15]) remained well below the level of the general population (1.3-1.6%), suggesting that dentists in the United States have a low occupational risk of developing HCV infection.³⁰ In our review, we found no evidence of transmission of a BBP, including HCV, between an infected dentist or oral surgeon and a patient.

Documented, occupationally acquired HIV infection among HCP is rare in the United States, with few confirmed cases since the late 1990s. Transmission of HIV to 6 patients of a dentist with AIDS remains the only reported transmission of HIV in a dental setting.^31,32

Transmission of BBPs is usually of greatest concern to DHCP because of their frequent direct or indirect contact with blood or blood-contaminated saliva. Other modes of transmission, such as inhalation of infectious microorganisms, also can result in HAIs. For example, separate episodes of transmission of Legionella infection and tuberculosis (TB), respectively, also were reported from 2003 to 2015.^33,34 In 2011, an 82-year-old woman in Italy was diagnosed with Legionnaires’ disease, caused by Legionella pneumophila, and died 2 days later.³³ The patient's only known risk of exposure for Legionella infection consisted of attending 2 dental appointments. All isolates obtained from the woman's bronchial aspirate were genetically identical to those obtained from dental unit waterline samples in her dentist's office. This incident reinforces the need to follow CDC recommendations for dental water quality.^3,21

In 2010, investigators found that a dental hygienist who developed active pulmonary TB likely transmitted Mycobacterium tuberculosis to another DHCP who worked in the same practice location.³⁴ The newly hired hygienist worked for several months in the dental practice while she was infectious because her TB symptoms originally were misdiagnosed. This report highlights the importance of implementing a written TB infection prevention and control plan that ensures baseline screening of new hires for active or latent TB that uses a 2-step tuberculin skin test or a single blood assay for M. tuberculosis.^3,35,36 In addition, DHCP should be trained to recognize the signs and symptoms suggestive of active TB disease.³⁶

Although the transmissions of HBV and HCV described in this report could not be definitively linked with a specific breach of infection prevention and control practices, investigators of HAIs that have occurred in other medical settings have determined that HAIs were caused by the failure of HCP to consistently practice recommended infection prevention measures and to sufficiently integrate these measures into the day-to-day management of program areas.¹⁵ It is reasonable to assume that HAIs found in dental settings may be caused by similar lapses in compliance. In dental and medical settings, noncompliance with established guidelines has led not only to HAIs but also to burdens on resources at the state and local levels, such as the use of dedicated personnel, investigation costs, patient notification, and testing of potentially exposed patients for BBP infection.^9,37

Our findings emphasize the importance that all DHCP, including those not involved directly in patient care but who may be exposed to infectious materials and those who use portable dental equipment, should adhere to recommended infection prevention practices. Adherence involves providing operational oversight of infection prevention practices by an infection prevention coordinator, having written infection prevention policies and procedures, training DHCP in procedures that are designed to prevent BBP transmission and infection and that are appropriate for assigned duties, ensuring that all staff members who may come into contact with blood or body fluids have received HBV vaccination, and emphasizing the use of standard precautions as the foundation for a successful infection prevention program.^3,7,9,15,38 Ongoing monitoring and routine evaluation of the infection prevention and control program are critical components for assessing compliance with recommended practices. Continuous review of the goals, activities, and practice policies should be followed by improvement activities that are realistic in expectation and, above all, effective. Table 2³ provides examples of methods for evaluating infection prevention and control programs.

Infection prevention recommendations should be available and easily understandable so that all DHCP can routinely implement the recommendations. To accomplish these goals, CDC has developed the Summary of Infection Prevention Practices in Dental Settings: Basic Expectations for Safe Care.²¹ This publication reflects existing evidence-based recommendations presented in CDC's Guidelines for Infection Control in Dental Health-Care Settings—2003³ and other selected CDC recommendations published since 2003.^15,27,39-44 It also emphasizes the elements of standard precautions and the basic infection prevention expectations for safe care in dental settings; this publication is meant to supplement existing recommendations, not replace them. It includes a companion checklist to be used in dental practice settings to assess infection prevention policies and procedures and the adequacy of their supplies for adhering to standard precautions. Users can modify this checklist to reflect individual practice policies and procedures. In addition, infection control coordinators can use the checklist to periodically evaluate compliance with correct infection prevention practices by means of observing DHCP when they are performing their duties. We anticipate that the Summary of Infection Prevention Practices in Dental Settings: Basic Expectations for Safe Care and checklist can supplement existing infection prevention guidelines from the CDC, provide the basis for training and educating DHCP, and ultimately ensure the safety of both dental patients and DHCP.

CONCLUSIONS

The results of our review of reported transmissions of BBPs since 2003 indicate that the transmission of BBPs in US dental settings is infrequent. This finding emphasizes the overall importance of adhering to dental infection prevention recommendations, including standard precautions, to prevent BBP transmission and the dramatic effects of vaccination against occupational HBV infection. The CDC Guidelines for Infection Control in Dental Health-Care Settings—2003³ remains the standard of care for the profession. Failure among DHCP to adhere to CDC infection prevention recommendations likely led to the disease transmissions identified in these reports. These transmissions highlight the need for improved understanding of the primary principles of infection prevention and control as well as the implementation of standard precautions among DHCP, including those who are not involved directly in patient care activities.