BRIEF REPORT
Patient-to-Patient Transmission of Hepatitis B Virus Associated with Oral Surgery John T. Redd,1,a Joan Baumbach,4 William Kohn,2 Omana Nainan,3 Marina Khristova,3 and Ian Williams3 1
Epidemic Intelligence Service and Divisions of 2Oral Health and 3Viral Hepatitis, Centers for Disease Control and Prevention, Atlanta, Georgia; 4 Office of Epidemiology, New Mexico Department of Health, Santa Fe (See the editorial commentaries by Hecht et al., on pages 1239–41, and Allos and Schaffner, on pages 1245–7; and the major article by Blick et al., on pages 1250–9.)
We used molecular epidemiologic techniques to document patient-to-patient transmission of hepatitis B virus (HBV) between 2 outpatient oral surgery patients operated on 161 min apart. Serological testing of 25 (93%) of 27 patients operated on after the source patient revealed that 19 (76%) of 25 were previously immune to HBV; no additional cases were identified. We found no deficiencies in infection control practices. Transmission may have been limited by the high prevalence (64%) of patients vaccinated against HBV. To our knowledge, this is the first documented case of patient-topatient transmission of a bloodborne pathogen in a dental setting in the United States. Hepatitis B virus (HBV) is a bloodborne virus of major concern in dental infection control. Dental health care personnel (DHCP) are at occupational risk of HBV infection [1–4], but infections have declined dramatically over the past 2 decades because of DHCP vaccination and adherence to standard infection control precautions [1–6]. No cases of dentist-to-patient HBV transReceived 20 April 2006; accepted 15 June 2006; electronically published 21 March 2007. Potential conflicts of interest: none reported. The use of trade names is for informational purposes only and does not constitute endorsement by the Centers for Disease Control and Prevention. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention. This article is dedicated to the memory of Dr. Omana Nainan. a Present affiliation: Prevention Branch, Division of Viral Hepatitis, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia. Reprints or correspondence: Dr. John T. Redd, Hepatitis and Liver Disease Section, Indian Health Service Div. of Epidemiology and Disease Prevention, 5300 Homestead Rd. NE, Albuquerque, NM 87110 (
[email protected]). The Journal of Infectious Diseases 2007; 195:1311–4 2007 by the Infectious Diseases Society of America. All rights reserved. 0022-1899/2007/19509-0012$15.00 DOI: 10.1086/513435
mission have been reported since 1987 (Centers for Disease Control and Prevention [CDC], unpublished data). There has been no description in the medical literature of patient-topatient transmission of a bloodborne pathogen, including HBV, in a dental setting; however, transmission may go unrecognized because many patients with acute infection are asymptomatic. Patients and methods. The State A Department of Health (DOH) was notified of a case of acute hepatitis B on 1 April 2002. The index patient was a 60-year-old woman who became symptomatic on 11 February 2002. The DOH found none of the traditional hepatitis B risk factors during routine case investigation, but she reported having oral surgery on 10 October 2001. An epidemiologic investigation was therefore begun. The index patient was interviewed in April 2002 using a standard CDC blood and body fluid exposure questionnaire. To determine whether there were additional infections, we identified patients who were seen at the same oral surgery center from Monday through Friday of the week of the index patient’s surgery. We excluded patients who were seen for standard dental visits in the separate, nonsurgery section of the building. Our list was compared with the confidential State A DOH Hepatitis B Registry. Patients were first contacted by the oral surgeons and advised to expect a call from the DOH. Patients who could not be contacted by telephone were sent up to 2 registered letters. We reviewed employee health records, performed HBV serologic tests on all employees with direct patient contact, and conducted an on-site office assessment. We defined cases of current or past HBV infection and HBV vaccination according to standard interpretations of HBV serologic markers [7]. Samples were tested for antibodies to hepatitis C virus (Ortho HCV ELISA 3.0; Ortho-Clinical Diagnostics); antibodies to HIV-1 (Vironostika HIV-1 MicroELISA System; bioMe´rieux); and markers of HBV infection, including total antibody to hepatitis B core antigen (anti-HBc; ETI-AB-COREK PLUS; DiaSorin), IgM anti-HBc (ETI-CORE-IgMK PLUS; DiaSorin), hepatitis B surface antigen (HBsAg; HBsAg EIA 2.0; Bio-Rad), hepatitis B surface antibody (anti-HBs; ETI-AB-AUK PLUS; DiaSorin), hepatitis B e antigen (HBeAg; ETI-EBK PLUS; DiaSorin), hepatitis B e antibody (anti-HBe; ETI-AB-EBK PLUS; DiaSorin), and HBV DNA concentration (HBV ASR; Abbott Molecular). Samples from HBsAg-positive patients were analyzed for HBsAg subtype by enzyme immunoassay [8]. HBV DNA was extracted from 50 mL of serum by nested polymerase chain reaction, and a ∼1200-bp region of the HBV genome (Pre-S1, Pre-S2, and S BRIEF REPORT • JID 2007:195 (1 May) • 1311
region [nt 2800–703]) was examined to determine the genetic relatedness of HBsAg-positive samples [9, 10]. Results. The index patient was a 60-year-old white nonHispanic woman with no history of hepatitis B vaccination. She became symptomatic on 11 February 2002 with pain and swelling of multiple large and small joints, extremity swelling, anterior shin lesions, and fatigue. She had not been sexually active for many years. In the 6 months before symptom onset, she had no occupational blood exposures, intravenous drug use, blood or blood product transfusions, household contact with someone with hepatitis B, or history of hemodialysis. She recovered from her HBV infection. She had 7 teeth extracted on Wednesday, 10 October 2001. The uncomplicated operation lasted from 10:50 a.m. until 11:16 a.m. Surgeon A operated with 3 assistants: one scrubbed in, one controlled the patient’s head and monitored anesthesia, and one did multiple tasks in the operative suite and clean area. A cross-match of the DOH Hepatitis B Registry found an HBV-infected patient who had oral surgery in the same operative suite on the same morning as the index patient. She was a 36-year-old woman with a complicated medical history, including hepatitis B since at least 1999. She had 3 teeth extracted under intravenous general anesthesia, with oxygen delivered through a reusable rubber nasal mask. Her uncomplicated surgery started at 8:09 a.m. and lasted until 8:51 a.m. Three patients were treated after her and before the index patient, all in the same operative suite. Surgeon A performed all the operations with the same 3 assistants in the same configuration. Both source and index patients received intravenous methohexital, diazepam, dexamethasone, fentanyl, and droperidol. The source patient also received intravenous succinylcholine and intramuscular methylprednisolone acetate. Both received local lidocaine and nasal oxygen. Medications were kept in multidose vials in a separate medication room. Serum from the index patient was tested on 12 February 2002 and showed an aspartate aminotransferase (AST) level of 311 U/L, an alanine aminotransferase (ALT) level of 533 U/L, an alkaline phosphatase level of 200 U/L, a total bilirubin level of 0.3 mg/dL, positive HBsAg, positive IgM anti-HBc, and negative total antibody to hepatitis A virus. Tests on 22 February 2002 showed an AST level of 994 U/L, an ALT level of 1674 U/L, negative anti-HBs, positive HBeAg, and negative anti-HBe. We obtained medical records on the source patient. Serologic testing on 1 February 2002 showed positive HBsAg, negative anti-HBs, positive total anti-HBc, and equivocal IgM anti-HBc. Testing done during our investigation on 3 September 2002 showed the same results as those from 1 February 2002; our results also showed positive HBeAg and negative anti-HBe with an HBV DNA concentration of 3,210,000 IU/mL. These results
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indicate that the source patient had chronic hepatitis B with a high viral load when she had oral surgery. HBsAg from both the index patient (12 February 2002) and the source patient (1 February 2002) was genotype A/subtype adw2. DNA sequencing showed that the isolates were identical in the region examined. Forty-eight other patients had operations during the same week (Monday–Friday) as the index patient. After finding the source patient, we contacted the 27 patients (including the index patient) whose procedures occurred after the source patient’s. Their mean age was 31 years (range, 15–67 years), with 16 (59%) aged !25 years; 15 (56%) were male; and 25 (93%) agreed to DOH testing. The DOH collected blood samples a mean of 257 days (range, 231–357 days) after oral surgery. Of the 25 patients tested, 16 (64%) had receipt of 3 doses of hepatitis B vaccine documented from vaccination records (table 1). Immunization status varied by age: 14 (93%) of the 15 patients aged !25 years had documentation of receipt of 3 doses of hepatitis B vaccine, compared with 2 (20%) of the 10 patients aged ⭓25 years (P ! .001 ). Three (12%) had a positive total anti-HBc with a negative IgM anti-HBc, reflecting infection 16 months in the past. The first, a 67-year-old man, had a distant history of multiple sex partners in the 1950s when in the military. The second, a 53-year-old woman, grew up in Southeast Asia, where hepatitis B is endemic. The third, an 18year-old man, had a medical record-documented history of 3 doses of hepatitis B vaccine in March, May, and October of 1995. Additional testing showed positive anti-HBs, negative HBsAg, negative anti-HBe, and negative HBeAg. No patients were positive for antibodies to hepatitis C virus (HCV) or HIV. The oral surgery center was in a detached, single-story building owned and run by 2 oral surgeons, who were the only surgeons who operated there. It contained 2 entirely separate operating suites. They were located across the hall from a recovery area containing standard gurneys with plastic-covered mattresses, a clean area for storing medications, and a waistheight clean bench with a standard sink. The surgeons used autoclavable surgical hand pieces, with the nondetachable components of the system covered by disposable plastic barriers that were changed between patients. Anesthesia equipment and monitors were covered with plastic barriers. Reusable rubber nasal masks for nitrous oxide and oxygen delivery were cleaned with a disinfectant soap-and-water solution and then disinfected according to manufacturer’s instructions with Birex spray (Biotrol International). Surgical instruments were manually scrubbed after use with a soap-and-bleach solution, rinsed with water, and allowed to dry before being loaded into standard autoclave packaging and sterilized in a Midmark M11 UltraClave autoclave (Midmark). Instruments were removed from their sterile packaging, laid out on surgical trays, covered,
Table 1. Hepatitis B virus (HBV) vaccination history and serologic test results of 28 oral surgery patients, by surgeon, date, and time of operation. Surgeon B
Surgeon A
Date, time Wednesday, 10 October 2001 b 8:00 8:30 9:30 10:00 10:30c 11:00 Thursday, 11 October 2001 7:45 8:00 8:30 9:00 9:30 10:00 10:30 11:00 Friday, 12 October 2001 8:00 8:30 9:00 9:30 10:00 10:30 11:00 11:15
History History of HBV IgM of HBV IgM vaccinationa Anti-HBs Anti-HBc anti-HBc HBsAg vaccinationa Anti-HBs Anti-HBc anti-HBc HBsAg No No Yes Yes No Yes
⫺ ⫺ + + ⫺ +
⫺ ⫺ ⫺ + ⫺
Refusedd Yes No Yes Yes Yes No No
+ ⫺ + + + ⫺ ⫺
⫺ ⫺ ⫺ + ⫺ ⫺ +
+ ⫺ ⫺ ⫺ + ⫺
+
⫺
⫺
⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺
Yes Yes Yes Yes Refusedd No
+ + + +
⫺ ⫺ ⫺ ⫺
⫺ ⫺ ⫺ ⫺
⫺
⫺
⫺
Yes Yes Yes Yes No No Yes No
+ + Equivocal + ⫺ ⫺ + ⫺
⫺ ⫺ ⫺ ⫺ ⫺ + ⫺ ⫺
⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺
⫺
NOTE. Anti-HBc, total HB anti-core antibody; anti-HBs, HB surface antibody; HBsAg, HB surface antigen; IgM anti-HBc, HB anti-core IgM antibody. a b c d
Confirmed receipt of 3 doses of HBV vaccine. Source patient. Index patient. Refused evaluation by Department of Health.
and held in a clean storage area for short periods before being placed in the operating suite immediately before procedures. Of 15 employees with direct patient care responsibilities, 14 (93.3%) had a documented 3-dose hepatitis B immunization series. No employee had serologic evidence of HBV infection. All staff members were full-time employees who were familiar with standard operating procedures. No employee recalled any unusual events on 10 October 2001. We observed multiple regularly scheduled surgical procedures on 26 September 2002. The office was modern and clean, with anesthesia, operation, cleaning, autoclave, and infection control practices that follow the standard for offices of this type. Medications were drawn up before surgery in a clean medication room. There was strict 1-way flow of needles after medications had been drawn up in the clean area, and no reuse of needles. The practice maintains an up-to-date log of controlled-substance multidose vials. Standard precautions for preventing transmission of blood-
borne pathogens were followed, including appropriate surgical hand antisepsis. Gloves, gowns, and masks were changed between patients. Plastic barriers covered most high-touch surfaces (including the patient’s chair), and light handles were covered with aluminum foil. Barriers were changed between patients. All covered (and many uncovered) surfaces were sprayed between patients with a hospital-grade intermediatelevel disinfectant according to the manufacturer’s instructions. All patients in a single morning were operated on with fresh instruments and with no instruments in common. Autoclave logs showed no autoclave problems. Discussion. HBV is a hardy virus that can persist in dried blood on surfaces for a week or more; infectious HBV can be present on surfaces even in the absence of visible blood [10, 11]. Despite these viral characteristics, frequent blood loss during oral surgery, and a challenging operation field that frequently leads to surfaces being contaminated with blood, HBV transmission in a dental setting is rare, particularly since stan-
BRIEF REPORT • JID 2007:195 (1 May) • 1313
dard precautions and routine vaccinations for dental workers were adopted. Using molecular techniques, we documented for the first time in the United States, to our knowledge, patientto-patient transmission of HBV in an oral surgery office despite no evidence of a breakdown in procedures. We can only speculate about the mechanism of transmission; cross-contamination from an environmental surface is one possibility. Theoretically, many surfaces (including clothing and plastic barriers) in the operation suite and the recovery area could have been contaminated with blood. Despite good standard operating procedures, some areas could have been missed during clean-up after the source patient, with subsequent crosscontamination. When tested by us, the source patient was HBeAg positive with a high viral load. We paid particular attention to the possibility of transmission due to contamination of multidose vials because of prior iatrogenic HBV and HCV transmission in this manner [12–15]. The index and source patients received 4 intravenous medicines and local lidocaine in common. However, the office’s physical layout, strict 1-way flow of needles from the clean area, careful record keeping for controlled-substance multidose vials, and lack of observed improper procedures suggest that this was not a likely mode of transmission. We found a high rate of prior vaccination (64%) among the patients operated on after the source patient, including 3 of the 5 patients who had surgery after the source patient on the same day, which may have limited the magnitude of HBV transmission and also prevented us from identifying the specific mechanism of transmission. Hepatitis B infection is not an indication for dental infection control measures other than standard bloodborne pathogen precautions. Although transmission such as we describe appears to be rare, this case reinforces the value of universal hepatitis B childhood vaccination (recommended since 1991 in the United States) and meticulous maintenance of bloodborne pathogen infection control for all patients in dental settings [4].
Acknowledgments We thank the oral surgeons involved in this outbreak, for their assistance; Wendi Kuhnert, for managing laboratory samples; Paul Swenson, for testing
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the HBsAg subtypes; Alan Deubner; John L. Golobic; Chad B. Smelser; and James E. Cheek.
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E R R AT U M
In the 1 May issue of the Journal, in the report by Redd et al. (Redd JT, Baumbach J, Kohn W, et al. Patient-to-patient transmission of hepatitis B virus associated with oral surgery. J Infect Dis 2007; 195:1311–4), there is an error in the penultimate paragraph of the Results section: the last sentence should
The Journal of Infectious Diseases 2007; 195:1874 2007 by the Infectious Diseases Society of America. All rights reserved. 0022-1899/2007/19512-0022$15.00 DOI: 10.1086/518669
1874 • JID 2007:195 (15 June) • ERRATUM
read as ⬙All uncovered (and many covered) surfaces were sprayed between patients with a hospital-grade intermediatelevel disinfectant according to the manufacturer’s instructions.⬙ The authors regret this error.
