Patient-to-Patient Transmission of Hepatitis B Virus Associated with Oral Surger

April 4, 2007

The Journal of Infectious Diseases 2007;195:1311-1314

0022-1899/2007/19509-0012$15.00

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BRIEF REPORT

Patient-to-Patient Transmission of Hepatitis B Virus Associated with Oral

Surgery

T. Redd,1,a Joan Baumbach,4 Kohn,2 Omana Nainan,3 Marina

Khristova,3 and Ian 3

1Epidemic Intelligence Service and Divisions of 2Oral Health and 3Viral

Hepatitis, Centers for Disease Control and Prevention, Atlanta, Georgia;

4Office 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-to-patient

transmission of a bloodborne pathogen in a dental setting in the United

States.

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Received 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. T. Redd, Hepatitis and Liver

Disease Section, Indian Health Service Div. of Epidemiology and Disease

Prevention, 5300 Homestead Rd. NE, Albuquerque, NM 87110

(john.redd@...).

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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 transmission 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-to-patient 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; bioMérieux); 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 L of serum

by nested polymerase chain reaction, and a 1200-bp region of the HBV genome

(Pre-S1, Pre-S2, and S 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 non-Hispanic

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 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 >6 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

18-year-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.

Table 1. Hepatitis B virus (HBV) vaccination history and serologic

test results of 28 oral surgery patients, by surgeon, date, and time of

operation.

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

waist-height 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, 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 bloodborne

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 intermediate-level 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

standard 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, patient-to-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

cross-contamination. 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; Swenson,

for testing the HBsAg subtypes; Alan Deubner; L. Golobic; Chad B.

Smelser; and E. Cheek.

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