Minireviews Open Access
Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Hepatol. Mar 27, 2015; 7(3): 488-497
Published online Mar 27, 2015. doi: 10.4254/wjh.v7.i3.488
Hepatitis B in healthcare workers: Transmission events and guidance for management
Jessica D Lewis, Costi D Sifri, Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, VA 22908, United States
Kyle B Enfield, Division of Pulmonary and Critical Care Medicine, Department of Medicine, University of Virginia Health System, Charlottesville, VA 22908, United States
Kyle B Enfield, Costi D Sifri, Office of Hospital Epidemiology/Infection Prevention and Control, University of Virginia Health System, Charlottesville, VA 22908, United States
Author contributions: All authors contributed to this manuscript.
Supported by National Institutes of Health Infectious Diseases Training Grant No. 5T32AI007046-37.
Conflict-of-interest: All authors report no conflicts of interest relevant to this article.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Costi D Sifri, MD, Division of Infectious Diseases and International Health, Office of Hospital Epidemiology/Infection Prevention and Control, University of Virginia Health System, PO Box 800473, Charlottesville, VA 22908, United States. csifri@virginia.edu
Telephone: +1-434-9240260 Fax:+1-434-9241225
Received: September 3, 2014
Peer-review started: September 3, 2014
First decision: November 19, 2014
Revised: November 22, 2014
Accepted: December 16, 2014
Article in press: December 16, 2014
Published online: March 27, 2015

Abstract

Hepatitis B virus (HBV) is the most efficiently transmissible of the bloodborne viruses that are important in healthcare settings. Healthcare workers (HCWs) are at risk for exposure to HBV from infected patients and, if infected, are similarly at risk of transmitting HBV to patients. Published cases of HBV transmission from HCW to patient are relatively rare, having decreased in frequency following the introduction of standard (universal) precautions, adoption of enhanced percutaneous injury precautions such as double-gloving in surgery, and routine HBV vaccination of HCWs. Here we review published cases of HCW-to-patient transmission of HBV, details of which have helped to guide the creation of formal guidelines for the management of HBV-infected HCWs. We also compare the published guidelines for the management of HBV-infected HCWs from various governing bodies, focusing on their differences with regard to vaccination requirements, viral load limits, frequency of monitoring, and restrictions on practice. Importantly, while there are differences among the recommendations from governing bodies, no guidelines uniformly restrict HBV-infected HCWs from performing invasive or exposure-prone procedures.

Key Words: Hepatitis B, Healthcare worker, Blood-borne pathogens, Transmission, Invasive procedures

Core tip: Reports of transmission of hepatitis B virus (HBV) from infected healthcare workers (HCWs) to patients have been rare but are highly instructive when they do occur. These events have helped instruct formal recommendations for the management of HBV-infected HCWs. However, guidelines from various governing bodies differ in their recommendations for the monitoring of infected HCWs, as well as in their restriction of the practice of invasive, exposure-prone procedures.



INTRODUCTION

Hepatitis B virus (HBV) is one of numerous blood-borne pathogens known to be transmissible in healthcare settings. HBV, among the blood-borne viruses including hepatitis C virus (HCV) and human immunodeficiency virus (HIV), is of particular importance because it is the most efficiently transmissible following percutaneous exposure. The incidence of transmission via needlestick injury in one study was approximately 2% with HBV e antigen (HBeAg)-negative blood and 19% with HBeAg-positive blood[1]. Thus, healthcare workers (HCWs) are at risk for exposure to HBV from infected patients, and correspondingly, HBV-infected HCWs may potentially transmit HBV to patients. Fortunately, reported instances of HCW-to-patient transmission of HBV have been rare and have substantially decreased in frequency over the past four decades. Here, we examine the limited data available on the prevalence of HBV infection in HCWs, review published cases of HCW-to-patient transmission of HBV, and evaluate the guidelines and recommendations for the management of HBV-infected HCWs with a particular focus on the variability of guidelines across geographic regions and governing bodies.

PREVALENCE OF HBV INFECTION IN HEALTHCARE WORKERS

Since the development of a vaccine to prevent acute HBV infection in the early 1980s, the incidence of acute HBV infection in the general population of the United States has sharply fallen. The Centers for Disease Control and Prevention (CDC) estimates that the incidence of new HBV infections had fallen 5-fold between 1980 and 2010, from 208000 to 38000 new infections per year[2].

Historically, HCWs shouldered the burden of HBV infection in the United States. A study conducted in the United States Army between 1972 and 1974 found a HBV seropositivity rate of 5.8% among officers involved in direct patient care, compared to a seropositivity rate of 2.8% in those in non-patient care-oriented positions[3]. A serologic study conducted in physicians between 1975 and 1976 found serologic evidence of prior HBV infection in 18% of subjects, with a higher rate among pathologists (27%) and surgeons (28%)[4]. Following the 1982 Advisory Committee on Immunization Practices (ACIP) recommendation for HBV vaccination for HCWs[5], studies continued to demonstrate that HCWs were at increased risk for HBV infection, although the rates of seropositivity steadily declined. A voluntary study of 943 HCWs at a large urban academic medical center conducted over 8 mo in 1991 demonstrated HBV core antigen (HBcAg) positivity in 6.2% of HCWs compared to 1.8% in the comparator group of local blood donors[6]. Though the current prevalence of HBV in HCWs is not known, it likely mirrors that of the general population, significantly decreasing following the introduction of routine infant vaccination, catch-up adolescent vaccination, and pre-employment vaccination for HCWs who may potentially be exposed to blood or bodily fluids.

REVIEW OF PUBLISHED CASES OF HEALTHCARE WORKER-TO-PATIENT TRANSMISSION OF HBV

Table 1 summarizes the published cases of HCW-to-patient transmission of HBV[7-39]. Confirmed transmissions are defined as cases where the HCW and patient(s) were epidemiologically linked and genetic relatedness of the viruses was confirmed through partial or complete DNA sequencing. Probable transmissions are defined as cases in which the subtype of HBV infecting the HCW and patient were identical in investigations of epidemiologically-linked HCW and patient HBV infections. Possible transmissions are defined as cases in which epidemiologic links were established, infected patients had no other risk factors for HBV acquisition but virologic subtyping data was not available to confirm transmission. It should be noted that, based on the availability of molecular technology at the time, chronologically earlier reports were limited in their ability to confirm transmission. Additionally, earlier reports often do not include the HBV viral burden of the transmitting HCW.

Table 1 Published cases of healthcare worker-to-patient transmission of hepatitis B virus.
Ref.YearLocationType of providerHBeAg statusViral loadHBV status known to providerHBV status known to institutionNo. of patients infectedBreach in infection control identified
[7]1969United StatesNurseNot doneNot doneNoNo11a (11 possible)None
[8]1969-1974United StatesOral surgeonPositiveNot doneNot specifiedNot specified55 (10 probable, 45 possible)HCW did not wear gloves
[9]1973-1977SwitzerlandGeneral practitionerPositiveNot doneYesNot specified41 (41 possible)None
[10]1974United StatesRespiratory therapistPositiveNot doneNoNo4 (4 probable)HCW did not wear gloves, had an exudative dermatitis on hands, and reused syringes when accessing indwelling arterial catheters
[11]1975United StatesOral surgeonNot doneNot doneNot specifiedNot specified43 (43 probable)None
[12]1976-1979United KingdomSurgical registrarPositiveNot doneNoNo9 (7 probable, 2 possible)None
[13]1977-1978United KingdomSurgical registrar, gynecologic surgeryPositiveNot doneNoNo8 (6 probable, 2 possible)None
[14]1978United StatesDentistPositiveNot doneYesNot specified6 (2 probable, 4 possible)HCW did not wear gloves
[15]1978NorwayCardiac surgeonPositiveNot doneNoNo5 (5 probable)None
[16]1978-1979United StatesOral surgeonPositiveNot doneNoNo12 (4 probable, 8 possible)HCW did not wear gloves and had a generalized eczematous dermatitis, including hand involvement
[17]1979-1980United StatesObstetrician-gynecologistPositiveNot doneYesYes4 (1 probable, 3 possible)HCW held needle in hand rather than a needle holder when suturing, noted several episodes of blood on hands after removing gloves
[18]1979-1981The NetherlandsCardiac surgeonNot reportedNot doneNot specifiedNot specified3 (3 probable)None
[18]1979-1981The NetherlandsPerfusion technicianPositiveNot doneNot specifiedNot specified11 (8 probable, 3 possible)Bleeding warts on HCW’s hands
[19]1980United StatesOral surgeonNot doneNot doneNot specifiedNot specified3 (3 probable)None
[20]1980-1983United KingdomPerfusion technicianPositiveNot doneYesNot specified6 (6 probable)HCW did not wear gloves, and had cuts and abrasions on hands
[20]1980-1983United KingdomSurgical registrarNot reportedNot doneNot specifiedNot specified5 (5 possible)None
[20]1980-1983United KingdomHouse officerNot reportedNot doneNot specifiedNot specified1 (1 possible)None
[21]1984United StatesObstetrician-gynecologistPositiveNot doneNot specifiedNot specified6 (6 probable)None
[22]1984-1985United StatesDentistPositiveNot doneNoNo24 (6 probable, 18 possible)HCW did not wear gloves
[23]1987United StatesGeneral surgeonPositiveNot doneYesNot specified5 (3 probable, 2 possible)None
[24]1987United KingdomObstetrician-gynecologistPositiveNot doneNoNo22 (6 probable, 16 possible)None
[25]1988United KingdomGeneral surgeonNegative1 × 107 copies/mLNoNo1 (1 confirmed)None
[25]1988United KingdomObstetrician-gynecologist, traineeNegative4.4 × 106 copies/mLNoNo3 (3 confirmed)None
[25]1988United KingdomObstetrician-gynecologist, traineeNegative5.5 × 106 copies/mLYesNot specified1 (1 confirmed)None
[25]1988United KingdomGeneral surgeon, urologist, clinical assistantNegative2.5 × 105 copies/mLNoNo1 (1 confirmed)None
[26]1988United KingdomCardiothoracic surgeon, traineePositiveNot doneNoNo17 (9 probable, 8 possible)None
[27]1991United KingdomSurgeonPositiveNot doneNoNo3 (3 possible)None
[28]1991CanadaOrthopedic surgeonPositiveNot doneYesYes2 (1 probable, 1 possible)None
[29]1991-1992United StatesThoracic surgeonPositive1 × 109 copies/mLYesNot specified19 (9 confirmed, 4 probable, 6 possible)None
[30]1991-1993United KingdomCardiothoracic surgeonPositiveNot doneYesNo20 (14 confirmed, 6 probable)None
[31]1991-1996CanadaElectroencephalogram technicianPositiveNot doneNoNo75 (4 confirmed, 71 possible)HCW did not wear gloves and used reusable subdermal EEG electrodes
[32]1993United KingdomGeneral surgeonPositiveNot doneNoNo2 (2 confirmed)None
[33]1993-1994United KingdomGeneral surgeon, traineePositiveNot doneNot specifiedNot specified11 (1 confirmed, 10 possible)None
[33]1994United KingdomGeneral surgeon, traineePositiveNot doneNot specifiedNot specified2 (2 possible)None
[33]1994United KingdomUrologist, traineePositiveNot doneNot specifiedNot specified1 (1 possible)None
[34]1995-1999The NetherlandsGeneral surgeonPositive5 × 109 GE/mLNoNo28 (8 confirmed, 20 possible)HCW noted glove perforations
[35]1996United KingdomOrthopedic surgeonNegative but anti-HB e positive (pre-core mutant)Not doneYesYes1 (1 confirmed)None
[36]1999United KingdomCardiothoracic surgeonNegative but anti-HB e positive (pre-core mutant)1.03 × 106 GE/mLYesYes2 (2 confirmed)None
[37]2001United KingdomGeneral surgeonNegative> 106 copies/mLNoNo3 (3 confirmed)None
[38]2009United StatesOrthopedic surgeonPositive> 17.9 million IU/mLNoNo8 (2 confirmed, 6 possible)None
[39]2010JapanObstetrician-gynecologistPositive1.6 × 109 copies/mLNoNo1 (1 confirmed)None

Summarizing published cases of HCW-to-patient transmission of HBV, recognized breaches in infection control practices were implicated in the transmission event in a notable minority of cases. Early reports of transmission occurred in association with dental procedures during which the dentist or oral surgeon did not wear gloves[8,14,16,22], which was not a standard recommended practice until the 1980s[40]. In addition, several early reports of HBV transmission occurred during surgical procedures where the surgeon did not routinely double-glove, which was not a standard recommended practice until the early 2000s[41,42]. It is also notable that transmission of HBV from infected HCWs in primary care or other specialties that do not perform exposure-prone procedures (EPPs) is exceedingly rare. When transmissions did occur with these providers, they were more likely to be associated with breaches in infection control practices, such as reuse of syringes for access of indwelling arterial catheters[10], reuse of subdermal electroencephalogram electrodes[31], or failure to wear gloves in the setting of a skin condition involving the hands of the provider[10,18,20]. Overall, in the 35 cases in which HBeAg testing results were available, the vast majority (77%) of transmissions occurred as a result of an HBeAg-positive HCW. The lowest measured viral load at which transmission occurred was 2.5 × 105 copies/mL, which notably occurred in a HCW with HBeAg-seronegative chronic HBV[25]. In another study that included six HBeAg-seronegative surgeons who had previously been implicated in HCW-to-patient transmission events, all were viremic and the lowest HBV DNA viral load measured was 4 × 104 copies/mL[43]. Accordingly, the authors suggest that this viral load may represent a lower limit above which HBV transmission during invasive procedures cannot be definitively ruled out[43]. However, confidence in this viral load has some limitations, as it was measured at least 3 mo after the transmission event occurred.

REVIEW OF GUIDELINES FOR MANAGEMENT OF HEPATITIS B VIRUS-INFECTED HEALTHCARE WORKERS

Guidelines for the management of HBV-infected HCWs are largely based on the anecdotal data gleaned from cases of HCW-to-patient transmission and attempt to ethically balance the risk of viral transmission to the patient with the right of the infected HCW to perform his/her work in a safe manner without loss of the right to confidentiality about his/her own health issues. Here we summarize the guidelines on the management of HBV-infected HCWs from various governing bodies worldwide. Table 2 summarizes the recommendations, allowing direct comparison of guidelines on key factors, including screening and vaccination for HBV in HCWs, monitoring recommendations for HBV-infected HCWs, and restrictions on practice for those HCWs if any. Although there are slight differences among guidelines, it is important to note that none universally prohibits the practice of invasive procedures by an HBV-infected HCW. Table 3 summarizes each governing body’s definition and categorization of EPPs where delineated.

Table 2 Guidelines for management of hepatitis B virus-infected healthcare workers.
CDCSHEAACSCanadaUKEuropeAustralia
ScreeningAll HCWs at risk for HBV infection should be testedNot addressed in guidelineAll surgeons should know their HBV statusMandatory for all HCWs who perform EPPsMandatory for all HCWs who perform EPPs, can be done post-vaccinationMandatory for all HCWs who perform EPPs, can be done post-vaccinationAnnual testing recommended for all HCWs who perform EPPs
VaccinationAll HCWs susceptible to HBV infection should be vaccinatedNot addressed in guidelineAll surgeons who are antibody negative should be vaccinatedMandatory for all HCWs who perform EPPsMandatory for all HCWs who perform EPPsRecommended for all HCWsRecommended for all HCWs
Post- vaccination serologyRecommendedNot addressed in guidelineRecommendedRecommendedRecommendedRecommendedNot addressed in guideline
Frequency of testing/ monitoringEvery 6 moEvery 6 moNot specifiedEvery 12 moEvery 12 mo, or every 3 mo while on antiviral therapyEvery 12 mo if HBeAg negative, every 3 mo if HBeAg positive or on antiviral therapyEvery 3 mo if on antiviral therapy, every 12 mo if cleared HBsAg
Viral load limit1000 IU/mL or 5000 GE/mL104 GE/mLNot specifiedNot specified103 GE/mL104 GE/mLUndetectable by PCR assay
HBeAgNot required to be negativeNot required to be negativeNot required to be negativeNot required to be negativeMust be negativeNot required to be negativeNot addressed in guideline
Restriction of practiceEPPs restricted if viral load greater than set thresholdCategory III procedures restricted if viral burden greater than or equal to 104 GE/mL or HBeAg positiveDetermined by expert panelDetermined by expert panelIf HBeAg positive or if viral load greater than 103 GE/mLIf viral load greater than 104 GE/mLIf HBV DNA level detectable
Definition of EPPsYesYesNoYesYesYesYes
Expert panel recommendedYesYesYes, if HBeAg positive or high viral loadYes, if HBsAg positiveNo, recommend monitoring by an occupational health physicianNoYes
Pre-emptive patient notificationNoNoNot specifiedNoNoOptional for HCWs with HBV DNA levels above the cut-off level in order to continue practicing EPPsNo
Table 3 Categories of exposure-prone procedures.
CDC
Category I. Procedures known or likely to pose an increased risk of percutaneous injury to a healthcare provider that have resulted in provider- to-patient transmission of HBV. These procedures are limited to major abdominal, cardiothoracic, and orthopedic surgery, repair of major traumatic injuries, abdominal and vaginal hysterectomy, caesarean section, vaginal deliveries, and major oral or maxillofacial surgery. Techniques that have been demonstrated to increase the risk for healthcare provider percutaneous injury and provider-to-patient blood exposure include: digital palpation of a needle tip in a body cavity and/or the simultaneous presence of a health care provider’s fingers and a needle or other sharp instrument or object in a poorly visualized or highly confined anatomic site
Category II. These procedures pose low or no risk for percutaneous injury to a HCW or, if a percutaneous injury occurs, it usually happens outside of a patient’s body and generally does not pose a risk for provider-to-patient blood exposure. These include: surgical and obstetrical/gynecologic procedures that do not involve the techniques listed for Category I, the use of needles or other sharp devices when the HCW’s hands are outside a body cavity, dental procedures other than major oral or maxillofacial surgery, insertion of tubes, endoscopic or bronchoscopic procedures, internal examination with a gloved hand that does not involve the use of sharp devices, and procedures that involve external physical touch
SHEA
Category I. Procedures with de minimis risk of bloodborne virus transmission: regular history-taking and/or physical or dental examinations; routine dental preventive procedures, diagnostic procedures, orthodontic procedures, prosthetic procedures, cosmetic procedures not requiring local anesthesia; routine rectal or vaginal examination; minor surface suturing; elective peripheral phlebotomy; lower gastrointestinal tract endoscopic examinations and procedures; hands-off supervision during surgical procedures and computer-aided remote or robotic surgical procedures; and psychiatric evaluations
Category II. Procedures for which bloodborne virus transmission is theoretically possible but unlikely: locally anesthetized ophthalmologic surgery; locally anesthetized operative, prosthetic, and endodontic dental procedures; periodontal scaling and root planing; minor oral surgical procedures; minor local procedures under local anesthesia; percutaneous cardiac procedures; percutaneous and other minor orthopedic procedures; subcutaneous pacemaker implantation; bronchoscopy; insertion and maintenance of epidural and spinal anesthesia lines; minor gynecological procedures; male urological procedures; upper gastrointestinal tract endoscopic procedures; minor vascular procedures; amputations; breast augmentation or reduction; minimum-exposure plastic surgical procedures; total and subtotal thyroidectomy and/or biopsy; endoscopic ear, nose, and throat surgery and simple ear and nasal procedures; ophthalmic surgery; assistance with an uncomplicated vaginal delivery; laparoscopic procedures; thorascopic procedures; nasal endoscopic procedures; routine arthroscopic procedures; plastic surgery; insertion of, maintenance of, and drug administration into arterial and central venous lines; endotracheal intubation and use of laryngeal mask; and obtainment and use of venous and arterial access devices that occur under complete antiseptic technique, using universal precautions, “no-sharp” technique, and newly gloved hands
Category III. Procedures for which there is definite risk of bloodborne virus transmission or that have been classified previously as “exposure-prone:” general surgery; general oral surgery; cardiothoracic surgery; open extensive head and neck surgery involving bones; neurosurgery, other intracranial procedures, and open-spine surgery; nonelective procedures performed in the emergency department; obstetrical/gynecological surgery; orthopedic procedures; extensive plastic surgery; transplantation surgery except skin and corneal transplantation; trauma surgery; interactions with patients in situations during which the risk of the patient biting the physician is significant; and any open surgical procedure with a duration of more than 3 h, probably necessitating glove change
ACS
Not provided
Canada
Procedures during which transmission of HBV, HCV, or HIV from a HCW to patients is most likely to occur and includes the following: (1) digital palpation of a needle tip in a body cavity or the simultaneous presence of the HCW’s fingers and a needle or other sharp instrument or object in a blind or highly confined anatomic site; (2) repair of major traumatic injuries; or (3) major cutting or removal of any oral or perioral tissue, including tooth structures, during which there is potential for the patient’s open tissues to be exposed to the blood of an injured HCW
UK
Exposure-prone procedures are those invasive procedures where there is a risk that injury to the worker may result in the exposure of the patient’s open tissues to the blood of the worker. These include procedures where the worker’s gloved hands may be in contact with sharp instruments, needle tips or sharp tissues inside a patient’s open body cavity, wound, or confined anatomical space where the hands or fingertips may not be completely visible at all times
Europe
Exposure-prone procedures are invasive procedures where there is potential for contact between the skin of the HCW and sharp surgical instruments, needles, or sharp tissues in body cavities or poorly visualized/confined body sites
Australia
Category 1: A procedure where the hands and fingertips of the HCW are visible and outside of the body most of the time and the possibility of injury to the worker’s gloved hands from sharp instruments and/or tissues is slight
Category 2: A procedure where the fingertips of the HCW may not be visible at all times but injury to the worker’s gloved hands from sharp instruments and/or tissues is unlikely. If injury occurs it is likely to be noticed and acted upon quickly to avoid the HCW’s blood contaminating a patient’s open tissues
Category 3: A procedure where the fingertips are out of sight for a significant part of the procedure, or during certain critical stages, and in which there is a distinct risk of injury to the worker’s gloved hands from sharp instruments and/or tissues. In such circumstances it is possible that exposure of the patient’s open tissues to the HCW’s blood may go unnoticed or would not be noticed immediately

The Society for Healthcare Epidemiology of America, in guidelines updated in 2010[44], recommends that HCWs with a positive HBeAg or circulating HBV burden of greater than or equal to 104 genome equivalents (GE) per mL of blood be prohibited from performing certain pre-defined high-risk (Category III) EPPs and use double-gloving for all invasive procedures, for all contact with mucous membranes or non-intact skin, and for all instances in patient care for which gloving is recommended otherwise[44]. For HCWs with a circulating HBV burden of less than 104 GE/mL of blood, it is suggested that providers may perform all Category I and II (minimal- and low-risk) and Category III (high-risk) procedures as long as they (1) have not transmitted HBV infection to patients; (2) obtain advice from an expert review panel; (3) undergo routine follow-up by occupational medicine including twice yearly viral testing to ensure that viral burden remains less than 104 GE/mL; (4) receive follow-up care by a personal physician who has expertise in the management of HBV infection and who may communicate with the expert review panel about the HCW’s clinical status; (5) consult with an expert about optimal infection control procedures and strictly adhere to them; and (6) agree to and sign a contract or letter from the expert review panel that characterizes their responsibilities[44].

CDC guidelines from 2012 recommend that all HCWs receive HBV vaccination followed by assessment of hepatitis B surface antibody (anti-HBs) status and, in the case of non-response to vaccination, revaccination[45]. If HCWs do not achieve protective levels of anti-HBs after a second three-dose series of HBV vaccine, they should be tested for HBV surface antigen (HBsAg) and HBV core antibody (anti-HBc) to determine if previously or chronically infected. Pre-vaccination serology is recommended for HCWs who were born to mothers from endemic countries, who are sexually active men who have sex with men, and/or who perform EPPs[45]. CDC guidelines for management of chronic HBV infection apply only to those HCWs who perform EPPs. They recommend that HBV-infected HCWs that perform EPPs may continue to do so if a low (less than 1000 IU/mL or 5000 GE/mL) or undetectable HBV viral load is documented every 6 mo. If the viral load is above the recommended threshold, performance of EPPs should be restricted until subsequent retesting occurs[45]. CDC also recommends that institutions have written policies and procedures in place for the management of HBV-infected HCWs, including the ability to form an expert review panel to assist with management of these providers[45].

In its most recent guidelines, updated in 2003, the American College of Surgeons (ACS) recommends that surgeons know their HBV immunization and antibody status[46]. Surgeons who do not have protective anti-HBs levels should be vaccinated, with follow-up documentation of seroconversion. Failure to seroconvert should prompt a second vaccination series. Surgeons with antibody to HBV should know their HBsAg status and, if positive, their HBeAg status. ACS recommends that surgeons who are HBeAg-positive or have high viral loads be guided by expert panels regarding their continuation of clinical practice. These guidelines do not specify what constitutes a high viral load, the viral load limit at which a surgeon’s practice should be restricted, or what procedures constitute EPPs[46].

Canadian guidelines, set forth by the Laboratory Centre for Disease Control of Health Canada in 1998, recommend mandatory HBV immunization of HCWs who perform EPPs with follow-up testing 4-8 wk later for anti-HBs response[47]. Those who are found to be non-responders on post-immunization testing should be screened for infection annually, with HBsAg and anti-HBc. HCWs who perform EPPs and test positive for HBsAg should undergo testing for HBeAg and if positive, should be referred to an expert panel and cease practice pending the panel’s recommendations. If HBeAg-negative, they may continue to practice but should still be referred to an expert panel. Provided that the HCW follows recommendations set forth by the expert panel, disclosure of HBV status to patients before an EPP is not recommended.

The United Kingdom Department of Health (UKDH) released guidelines for management of HBV-infected HCWs in 2000[48], with an update focusing on HBV-infected HCWs on antiviral therapy in 2007[49]. UKDH recommends that all HCWs who perform EPPs be immunized against HBV and be tested for anti-HBs response post-vaccination[50]. If there is failure to respond to one vaccination series, the HCW should be tested for HBsAg, and if negative, should be tested for anti-HBc to determine if they have had prior infection or are true vaccine non-responders[50]. The guidelines recommend that all HCWs who are HBsAg-positive be tested for HBeAg[48]. Those that are HBeAg-positive or those who are HBeAg-negative but with a HBV viral load greater than 103 GE/mL should be restricted from performing EPPs[48]. If HBeAg is negative and viral load is less than 103 GE/mL without antiviral treatment, annual monitoring should be conducted, and practice should not be restricted[48]. The 2007 guidelines, developed in response to advances in antiviral treatment for HBV infection, recommends that HCWs who are HBeAg-negative should be permitted to perform EPPs while on antiviral therapy as long as their viral load remains < 103 GE/mL on monitoring done every 3 mo, and their pretreatment viral load was < 105 GE/mL[49]. Though the UKDH guidelines do not recommend formation of an expert panel to guide management of HBV-infected HCWs, they do recommend the involvement of an occupational health physician[48].

The European Consensus group guidelines published in 2003 recommend HBV vaccination of all HCWs in contact with patients, blood, or other bodily fluids, with vaccine response tested one month post-vaccination[51]. Non-responders should undergo additional vaccine series and if they continue to fail to respond, an investigation into their HBV status is recommended based on their job functions. Specifically for HCWs who perform EPPs, the group recommends proof of anti-HBs response and if negative or unavailable, they should receive a booster dose of HBV vaccination, with vaccine response tested one month later. Non-responders should be investigated for HBV infection, with testing of HBsAg or anti-HBc, and only those who are HBsAg-negative should be permitted to proceed with EPPs. HCWs who are HBsAg-positive should have HBeAg tested and if HBeAg-negative, can proceed with performing EPPs if the HBV DNA level is less than 104 GE/mL. The HBV DNA level should be monitored annually. If HBeAg-positive, the HCW should not perform EPPs unless their viral load is below the designated cut-off and they are evaluated by an expert panel that has approved the performance of EPPs. In this case, it is recommended that the HBV viral load be monitored every 3 mo.

Finally, Australian guidelines from 2012[52] recommend that all HCWs be vaccinated against HBV and that all HCWs who perform EPPs be tested for HBV and other blood-borne pathogens annually. A HCW is not permitted to perform EPPs if HBV DNA is detectable by an approved polymerase chain reaction assay. If the HCW is HBsAg-positive and on antiviral therapy, they are permitted to perform EPPs as long as HBV DNA is undetectable via testing every 3 mo. If HBsAg becomes negative on two consecutive occasions, the HCW may perform EPPs but will require annual testing thereafter. The guidelines also recommend formation of an expert review panel to advise on the management of HBV-infected HCWs.

The majority of governing bodies recommend the formation of an expert review panel or committee to assist with management and monitoring of HCWs infected with HBV and other bloodborne viruses. Guidelines generally recommend the inclusion of individuals who have expertise in the infected HCW’s specialty and the procedures they perform, healthcare epidemiologists, infectious disease specialists, hepatologists, occupational medicine physicians, hospital administrators, human resources personnel, and the HCW’s primary physician. Other suggested panel members include a public health official if such issues are managed at the state level, legal counsel, and experts in ethics.

CONCLUSION

HBV infection among HCWs is of particular concern given its high transmissibility relative to other blood-borne viruses, including documented transmissions from infected HCW to patient. Fortunately, instances of HCW-to-patient transmission of HBV have been relatively rare and have substantially decreased in frequency over the past four decades, presumably due to more vigilant screening and vaccination of HCWs, the use of universal precautions and double-gloving during EPPs, and formal recommendations from governing bodies on the appropriate restrictions of practice of infected HCWs. Our review of the published cases of HCW-to-patient transmission of HBV provides historical data for these formal recommendations. Our review also highlights the differences between recommendations for management of HBV-infected HCWs by various governing bodies, though a common feature is that no governing body uniformly prohibits the practice of EPPs by an HBV-infected HCW. While HBV is highly transmissible through parenteral and mucous membrane exposures, the formal recommendations set forth by the various governing bodies discussed above have helped to codify the manner in which we manage HBV-infected HCWs, thus reducing the risk of transmission to patients while balancing the need to protect the private health information of HCWs and their ability to continue to perform the work for which they are trained to do.

Footnotes

P- Reviewer: Bozdayi AM, Yoo BC S- Editor: Ji FF L- Editor: A E- Editor: Wu HL

References
1.  Werner BG, Grady GF. Accidental hepatitis-B-surface-antigen-positive inoculations. Use of e antigen to estimate infectivity. Ann Intern Med. 1982;97:367-369.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 174]  [Cited by in F6Publishing: 180]  [Article Influence: 4.3]  [Reference Citation Analysis (0)]
2.  Centers for Disease Control and Prevention. Historical reported cases and estimates [accessed 2014 July 2].  Available from: http://www.cdc.gov/hepatitis/Statistics/IncidenceArchive.htm.  [PubMed]  [DOI]  [Cited in This Article: ]
3.  Segal HE, Llewellyn CH, Irwin G, Bancroft WH, Boe GP, Balaban DJ. Hepatitis B antigen and antibody in the U.S. Army: prevalence in health care personnel. Am J Public Health. 1976;66:667-671.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 20]  [Cited by in F6Publishing: 22]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
4.  Denes AE, Smith JL, Maynard JE, Doto IL, Berquist KR, Finkel AJ. Hepatitis B infection in physicians. Results of a nationwide seroepidemiologic survey. JAMA. 1978;239:210-212.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 29]  [Cited by in F6Publishing: 29]  [Article Influence: 0.6]  [Reference Citation Analysis (0)]
5.  Centers for Disease Control (CDC). Recommendation of the Immunization Practices Advisory Committee (ACIP). Inactivated hepatitis B virus vaccine. MMWR Morb Mortal Wkly Rep. 1982;31:317-322, 327-328.  [PubMed]  [DOI]  [Cited in This Article: ]
6.  Thomas DL, Factor SH, Kelen GD, Washington AS, Taylor E, Quinn TC. Viral hepatitis in health care personnel at The Johns Hopkins Hospital. The seroprevalence of and risk factors for hepatitis B virus and hepatitis C virus infection. Arch Intern Med. 1993;153:1705-1712.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 68]  [Cited by in F6Publishing: 71]  [Article Influence: 2.3]  [Reference Citation Analysis (0)]
7.  Garibaldi RA, Rasmussen CM, Holmes AW, Gregg MB. Hospital-acquired serum hepatitis. Report of an outbreak. JAMA. 1972;219:1577-1580.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 28]  [Cited by in F6Publishing: 28]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
8.  Rimland D, Parkin WE, Miller GB, Schrack WD. Hepatitis B outbreak traced to an oral surgeon. N Engl J Med. 1977;296:953-958.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 93]  [Cited by in F6Publishing: 96]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
9.  Grob PJ, Bischof B, Naeff F. Cluster of hepatitis B transmitted by a physician. Lancet. 1981;2:1218-1220.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 30]  [Cited by in F6Publishing: 30]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
10.  Snydman DR, Hindman SH, Wineland MD, Bryan JA, Maynard JE. Nosocomial viral hepatitis B. A cluster among staff with subsequent transmission to patients. Ann Intern Med. 1976;85:573-577.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 46]  [Cited by in F6Publishing: 44]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
11.  Goodwin D, Fannin SL, McCracken BB.  An oral surgeon-related hepatitis B outbreak. California: California Morbidity 1976; 14.  [PubMed]  [DOI]  [Cited in This Article: ]
12.  Acute hepatitis B following gynaecological surgery J Hosp Infect. 1987;9:34-38.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 9]  [Cited by in F6Publishing: 9]  [Article Influence: 0.2]  [Reference Citation Analysis (0)]
13.  Acute hepatitis B associated with gynaecological surgery Lancet. 1980;1:1-6.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 2]  [Article Influence: 0.0]  [Reference Citation Analysis (0)]
14.  Hadler SC, Sorley DL, Acree KH, Webster HM, Schable CA, Francis DP, Maynard JE. An outbreak of hepatitis B in a dental practice. Ann Intern Med. 1981;95:133-138.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 68]  [Cited by in F6Publishing: 67]  [Article Influence: 1.6]  [Reference Citation Analysis (0)]
15.  Haerem JW, Siebke JC, Ulstrup J, Geiran O, Helle I. HBsAG transmission from a cardiac surgeon incubating hepatitis B resulting in chronic antigenemia in four patients. Acta Med Scand. 1981;210:389-392.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 19]  [Cited by in F6Publishing: 21]  [Article Influence: 1.4]  [Reference Citation Analysis (0)]
16.  Reingold AL, Kane MA, Murphy BL, Checko P, Francis DP, Maynard JE. Transmission of hepatitis B by an oral surgeon. J Infect Dis. 1982;145:262-268.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 47]  [Cited by in F6Publishing: 49]  [Article Influence: 1.2]  [Reference Citation Analysis (0)]
17.  Carl M, Blakey DL, Francis DP, Maynard JE. Interruption of hepatitis B transmission by modification of a gynaecologist’s surgical technique. Lancet. 1982;1:731-733.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 32]  [Cited by in F6Publishing: 30]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
18.  Coutinho RA, Albrecht-van Lent P, Stoutjesdijk L, Meerburg-Snarenberg P, Couroucé-Pauty AM, van Dijk BA, Kloek J. Hepatitis B from doctors. Lancet. 1982;1:345-346.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 18]  [Cited by in F6Publishing: 18]  [Article Influence: 0.4]  [Reference Citation Analysis (0)]
19.  Goodman RA, Ahtone JL, Finton RJ. Hepatitis B transmission from dental personnel to patients: unfinished business. Ann Intern Med. 1982;96:119.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 15]  [Cited by in F6Publishing: 16]  [Article Influence: 0.4]  [Reference Citation Analysis (0)]
20.  Polakoff S. Acute hepatitis B in patients in Britain related to previous operations and dental treatment. Br Med J (Clin Res Ed). 1986;293:33-36.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 25]  [Cited by in F6Publishing: 28]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
21.  Lettau LA, Smith JD, Williams D, Lundquist WD, Cruz F, Sikes RK, Hadler SC. Transmission of hepatitis B with resultant restriction of surgical practice. JAMA. 1986;255:934-937.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 9]  [Cited by in F6Publishing: 9]  [Article Influence: 0.2]  [Reference Citation Analysis (0)]
22.  Shaw FE, Barrett CL, Hamm R, Peare RB, Coleman PJ, Hadler SC, Fields HA, Maynard JE. Lethal outbreak of hepatitis B in a dental practice. JAMA. 1986;255:3260-3264.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 45]  [Cited by in F6Publishing: 45]  [Article Influence: 1.2]  [Reference Citation Analysis (0)]
23.  Prendergast TJ, Teitelbaum S, Peck B. Transmission of hepatitis B by a surgeon. West J Med. 1991;154:353.  [PubMed]  [DOI]  [Cited in This Article: ]
24.  Welch J, Webster M, Tilzey AJ, Noah ND, Banatvala JE. Hepatitis B infections after gynaecological surgery. Lancet. 1989;1:205-207.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 50]  [Cited by in F6Publishing: 57]  [Article Influence: 1.6]  [Reference Citation Analysis (0)]
25.  Incident Investigation Teams and Others. Transmission of hepatitis B to patients from four infected surgeons without hepatitis B e antigen. N Engl J Med. 1997;336:178-184.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 99]  [Cited by in F6Publishing: 104]  [Article Influence: 3.9]  [Reference Citation Analysis (0)]
26.  Prentice MB, Flower AJ, Morgan GM, Nicholson KG, Rana B, Firmin RK, Mitchell CJ. Infection with hepatitis B virus after open heart surgery. BMJ. 1992;304:761-764.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 28]  [Cited by in F6Publishing: 29]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
27.  Surgeons who are hepatitis B carriers BMJ. 1991;303:184-185.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 2]  [Article Influence: 0.1]  [Reference Citation Analysis (0)]
28.  Johnston BL, MacDonald S, Lee S, LeBlanc JC, Gross M, Schlech WF, Chaudhary R, Langille D. Nosocomial hepatitis B associated with orthopedic surgery--Nova Scotia. Can Commun Dis Rep. 1992;18:89-90.  [PubMed]  [DOI]  [Cited in This Article: ]
29.  Harpaz R, Von Seidlein L, Averhoff FM, Tormey MP, Sinha SD, Kotsopoulou K, Lambert SB, Robertson BH, Cherry JD, Shapiro CN. Transmission of hepatitis B virus to multiple patients from a surgeon without evidence of inadequate infection control. N Engl J Med. 1996;334:549-554.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 157]  [Cited by in F6Publishing: 162]  [Article Influence: 5.8]  [Reference Citation Analysis (0)]
30.  Heptonstall J. Lessons from two linked clusters of acute hepatitis B in cardiothoracic surgery patients. Commun Dis Rep CDR Rev. 1996;6:R119-R125.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 1]  [Article Influence: 0.0]  [Reference Citation Analysis (0)]
31.  An outbreak of hepatitis B associated with reusable subdermal electroencephalogram electrodes. Hepatitis B Outbreak Investigation Team. CMAJ. 2000;162:1127-1131.  [PubMed]  [DOI]  [Cited in This Article: ]
32.  Mukerjee AK, Westmoreland D, Rees HG. Response to the discovery of two practising surgeons infected with hepatitis B. Commun Dis Rep CDR Rev. 1996;6:R126-R128.  [PubMed]  [DOI]  [Cited in This Article: ]
33.  Oliver SE, Woodhouse J, Hollyoak V. Lessons from patient notification exercises following the identification of hepatitis B e antigen positive surgeons in an English health region. Commun Dis Public Health. 1999;2:130-136.  [PubMed]  [DOI]  [Cited in This Article: ]
34.  Spijkerman IJ, van Doorn LJ, Janssen MH, Wijkmans CJ, Bilkert-Mooiman MA, Coutinho RA, Weers-Pothoff G. Transmission of hepatitis B virus from a surgeon to his patients during high-risk and low-risk surgical procedures during 4 years. Infect Control Hosp Epidemiol. 2002;23:306-312.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 40]  [Cited by in F6Publishing: 43]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
35.  Sundkvist T, Hamilton GR, Rimmer D, Evans BG, Teo CG. Fatal outcome of transmission of hepatitis B from an e antigen negative surgeon. Commun Dis Public Health. 1998;1:48-50.  [PubMed]  [DOI]  [Cited in This Article: ]
36.  Molyneaux P, Reid TM, Collacott I, McIntyre PG, Dillon JF, Laing RB. Acute hepatitis B in two patients transmitted from an e antigen negative cardiothoracic surgeon. Commun Dis Public Health. 2000;3:250-252.  [PubMed]  [DOI]  [Cited in This Article: ]
37.  Laurenson IF, Jones DG, Hallam NF, Saunders CJ, Fraser DM, Carman WF. Transmission of hepatitis B virus from a vaccinated healthcare worker. J Hosp Infect. 2007;66:393-394.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 11]  [Cited by in F6Publishing: 12]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
38.  Enfield KB, Sharapov U, Hall KK, Leiner J, Berg CL, Xia GL, Thompson ND, Ganova-Raeva L, Sifri CD. Transmission of hepatitis B virus from an orthopedic surgeon with a high viral load. Clin Infect Dis. 2013;56:218-224.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 10]  [Cited by in F6Publishing: 11]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
39.  Sugimoto S, Nagakubo S, Ito T, Tsunoda Y, Imamura S, Tamura T, Morohoshi Y, Koike Y, Fujita Y, Ito S. A case of acute hepatitis B related to previous gynecological surgery in Japan. J Infect Chemother. 2013;19:524-529.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 5]  [Cited by in F6Publishing: 5]  [Article Influence: 0.4]  [Reference Citation Analysis (0)]
40.  Centers for Disease Control (CDC). Update: universal precautions for prevention of transmission of human immunodeficiency virus, hepatitis B virus, and other bloodborne pathogens in health-care settings. MMWR Morb Mortal Wkly Rep. 1988;37:377-82, 387-8.  [PubMed]  [DOI]  [Cited in This Article: ]
41.  Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for prevention of surgical site infection, 1999. Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol. 1999;20:250-78; quiz 279-80.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2944]  [Cited by in F6Publishing: 2721]  [Article Influence: 108.8]  [Reference Citation Analysis (0)]
42.  Association of periOperative Registered Nurses. Recommended practices for prevention of transmissible infections in the perioperative practice setting. AORN J. 2007;85:383-396.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 2]  [Article Influence: 0.1]  [Reference Citation Analysis (0)]
43.  Corden S, Ballard AL, Ijaz S, Barbara JA, Gilbert N, Gilson RJ, Boxall EH, Tedder RS. HBV DNA levels and transmission of hepatitis B by health care workers. J Clin Virol. 2003;27:52-58.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 34]  [Cited by in F6Publishing: 35]  [Article Influence: 1.7]  [Reference Citation Analysis (0)]
44.  Henderson DK, Dembry L, Fishman NO, Grady C, Lundstrom T, Palmore TN, Sepkowitz KA, Weber DJ. SHEA guideline for management of healthcare workers who are infected with hepatitis B virus, hepatitis C virus, and/or human immunodeficiency virus. Infect Control Hosp Epidemiol. 2010;31:203-232.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 89]  [Cited by in F6Publishing: 97]  [Article Influence: 6.9]  [Reference Citation Analysis (0)]
45.  Centers for Disease Control and Prevention (CDC). Updated CDC recommendations for the management of hepatitis B virus-infected health-care providers and students. MMWR Recomm Rep. 2012;61:1-12.  [PubMed]  [DOI]  [Cited in This Article: ]
46.  Statement on the surgeon and hepatitis B infection. American College of Surgeons. Bull Am Coll Surg. 1995;80:33-35.  [PubMed]  [DOI]  [Cited in This Article: ]
47.  Division of Nosocomial and Occupational Infections, Bureau of Infectious Diseases, Laboratory Center for Disease Control, Health Protection Branch. Health Canada. Proceedings of the Consensus Conference on Infected Health Care Worker Risk for transmission of bloodborne pathogens. Can Commun Dis Rep. 1998;24 Suppl 4:i-iii, 1-25; i-iii, 1-28.  [PubMed]  [DOI]  [Cited in This Article: ]
48.  Department of Health. Hepatitis B Infected Health Care Workers: Guidance on Implementation of Health Service Circular 2000/020, 2000: 11.  Available from: http://webarchive.nationalarchives.gov.uk/20130107105354/http: /www.dh.gov.uk/en/Publicationsandstatistics/Publications/PublicationsPolicyAndGuidance/DH_4008156.  [PubMed]  [DOI]  [Cited in This Article: ]
49.  Department of Health. Hepatitis B infected healthcare workers and antiviral therapy, 2007.  Available from: http://webarchive.nationalarchives.gov.uk/20130107105354/http: /www.dh.gov.uk/en/Publicationsandstatistics/Publications/PublicationsPolicyAndGuidance/DH_073164.  [PubMed]  [DOI]  [Cited in This Article: ]
50.  Department of Health. Addendum to HSG(93)40: Protecting health care workers and patients from hepatitis B - EL (96) 77 , 1996.  Available from: http://webarchive.nationalarchives.gov.uk/ /www.dh.gov.uk/en/Publicationsandstatistics/Lettersandcirculars/Executiveletters/DH_4088385.  [PubMed]  [DOI]  [Cited in This Article: ]
51.  Gunson RN, Shouval D, Roggendorf M, Zaaijer H, Nicholas H, Holzmann H, de Schryver A, Reynders D, Connell J, Gerlich WH. Hepatitis B virus (HBV) and hepatitis C virus (HCV) infections in health care workers (HCWs): guidelines for prevention of transmission of HBV and HCV from HCW to patients. J Clin Virol. 2003;27:213-230.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 108]  [Cited by in F6Publishing: 114]  [Article Influence: 5.4]  [Reference Citation Analysis (0)]
52.  Australian Government Department of Health and Aging. Australian National Guidelines for the Management of Health Care Workers Known to be Infected with Blood-Borne Viruses, 2012.  Available from: http://www.health.gov.au/internet/main/publishing.nsf/Content/cda-cdna-bloodborne.htm.  [PubMed]  [DOI]  [Cited in This Article: ]