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Ann Thorac Surg 1999;68:2267-2272
© 1999 The Society of Thoracic Surgeons


Original Articles

Decreasing occupational risk related to blood-borne viruses in cardiovascular surgery in Paris, France

Yu-Hung Kuo, MD, PhDa, Jean-Noël Fabiani, MDb, Ali Si Mohamed, PharmDa, Jean Paul A. Couetil, MDb, Michel Lévy, PhDa,b, Laurent Gutmann, MD, PhDa, Alain F. Carpentier, MD, PhDb, Laurent Bélec, MD, PhDa

a Laboratoire de Virologie, Hôpital Broussais, Paris, France
b Service de Chirurgie Cardiovasculaire, Hôpital Broussais, Paris, France

Address reprint requests to Dr Bélec, Laboratoire de Virologie, Hôpital Broussais, 96 rue Didot, 75674 Paris Cedex 14, France


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Surgeons face the risk of patient-to-physician transmission of blood-borne viruses. This risk is related to the seroprevalence of the viruses in the patient population.

Methods. The seroprevalence of the human immunodeficiency virus, hepatitis B virus, and hepatitis C virus were determined in cardiovascular patients at Hôpital Broussais in Paris, France, over a 5-year period (1994 to 1998).

Results. Hepatitis C virus is the most prevalent virus in the patient population, whereas human immunodeficiency virus is the least frequent. The seroprevalence of hepatitis C virus and human immunodeficiency virus has decreased over time, whereas hepatitis B virus has remained constant. We apply the seroprevalence data to a mathematical model to estimate the occupational risk of seroconversion faced by surgeons over the length of their career. Our results show that the principal risk faced by the surgeon arises from hepatitis B virus and hepatitis C virus. The decreasing seroprevalence of the hepatitis C virus has resulted in a decrease in the occupational risk.

Conclusions. The probability of becoming infected with a blood-borne virus over the career of the surgeon is notable. The greatest occupational risk to the surgeon is from the hepatitis viruses and not HIV.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Patient-to-physician transmission of disease is an occupational risk that is accepted as an inherent part of every-day life for the medical professional. The occupational risk associated with blood-borne pathogens is particularly prominent for the surgeon. Surgeons have been shown to have a four- to eightfold higher incidence of exposure to patient blood compared with internists [1]. The risk of exposure is greater with increasing volume of blood loss and prolonged length of procedure [2]. Surgical subspecialties including cardiovascular, orthopedic, neurologic, and obstetrical and gynecologic surgery, in which these factors play a prominent role, have the highest rates of exposure among surgeons [3].

Surveys have shown that the possibility of becoming infected with the human immunodeficiency virus (HIV) is a concern for a large majority of surgeons [46]. While it has always been considered part of the ethical duty of the surgeon to treat all patients, including those infected with HIV, a significant fraction of physicians report in anonymous surveys that the patient’s HIV status would either influence their decision to operate, or that they would choose not to operate on any HIV-positive patient [4, 7, 8]. Although HIV is at the forefront of discussions on occupational blood-borne pathogens, its rate of infectivity is actually rather low [2]. Hepatitis B virus (HBV) is the blood-borne virus that is most frequently involved in patient-to-surgeon transmission. The rate of seroconversion with HBV is possibly as high as 30% after percutaneous exposure to blood from a chronically infected patient [9]. Surgeons are known to have a greater rate of hepatitis B infection than other health care workers [2, 10]. Before HBV vaccination, it was estimated that up to 40% of surgeons would seroconvert for HBV during their career [11]. Finally, hepatitis C virus (HCV) also poses a risk for surgeons, with a seroconversion rate from percutaneous exposure to HCV-infected blood estimated at 4% to 10% [6, 12].

Many surgeons report that they would alter their surgical techniques and practice if a patient was demonstrated to harbor such viruses [7, 1316]. This attitude is also reflected by the large number of surgeons who support preoperative testing of all surgical patients [4, 7, 16]. Hôpital Broussais in Paris, France, is one of the principal cardiovascular units for the French public medical system. Screening for blood-borne viruses is requested of all surgical candidates at this hospital, with the aim of reducing the risk to the surgeon. We analyze the seroprevalence of the three blood-borne viruses, HIV, HBV, and HCV, in patients presenting between 1994 and 1998. The seroprevalence data are applied to an actuarial model to estimate the lifetime occupational risk of infection to cardiovascular surgeons who perform procedures on this population of patients.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Patient population and serologic testing
Surgical candidates seaking treatment at the cardiovascular department of Hôpital Broussais in Paris between May 1994 and December 1998 were tested for HIV, HBV, and HCV after obtaining informed written consent.

Screening for HIV was done by assaying for p24 antigen and for antibodies of the immunoglobulin (Ig)G and IgM isotypes to HIV using the Vidas Duo Test (BioMerieux, Marcy-l’Etoile, France). Sera reactive for HIV by screening test was further confirmed by Western blot (New Lav Blot I; Sanofi-Diagnostics Pasteur, Marnes-la-Coquette, France) using a second blood sample. Screening for hepatitis B surface (HBs) antigen and IgG to HCV was performed using the IMX System (Abbott Laboratories, Abbott Park, Chicago, IL).

Mathematical approach and statistical analysis
The occupation risk of infection by blood-borne viruses can be estimated using an actuarial model. The probability of infection by a given pathogen i from a single percutaneous exposure ai(pi,ri) can be defined by the following expression, where pi is defined as the prevalence of infection and ri is the estimated rate of infection per exposure:

The cumulative risk of infection by a given pathogen for a given year of practice Ri(ai,n) is then defined as follows, where n equals the average number of exposures a surgeon suffers per year:

The cumulative occupational probability of infection with a given pathogen Li(ai,n,d) would thus be defined, if d is the number of years in which a physician practices, by:

Substituting for the probability of infection, ai:

The number of years (Ei(ai,T,n) in which an individual would have to practice in order to have a probability T of being infected with a pathogen can be calculated by rearranging equation (I) to obtain the expression:

Finally, the probability A of infection by any one of the multiple potential blood-borne pathogens a surgeon faces over his career would then be defined by the sum of the probabilities for each given pathogen:

A can be substituted for ai in equations I and II above.

Statistical analysis
Quantitative results were expressed as mean ± standard error for the mean. Trends in blood-borne virus prevalence over time was calculated using simple linear regression. All results were analyzed with Statview 4.5 (Abacus Concepts Inc, Cupertino, CA). A p value less than 0.05 was set as the cutoff for statistical significance.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Seroprevalence of HIV, HBV, and HCV
A total of 7,218 patients (age 60.0 ± 0.61 years, range 1 to 97 years; male/female ratio: 66.4/33.6) consented to screening for HIV, HBV, and HCV. The demographic characteristics of the patient population screened each month was analyzed at 6-month intervals for age and distribution of gender; no significant difference was found among the months analyzed (not shown), attesting to the homogeneity of the study population over time.

The mean monthly frequency of positive tests for each of the blood-borne viral pathogens per year is shown in Table 1. HIV was the least frequent virus, with a mean monthly seroprevalence of 0.26% ± 0.12%. The peak frequency of HIV was 1.47%, observed in February 1995. The total number of cases of HIV presenting never exceeded two, and the majority of the months during this period (39 of 56 months) demonstrated no cases of HIV. Positive tests for HBV occurred with a greater frequency. The mean monthly seroprevalence of HBV was 1.03% ± 0.98% (range 0% to 4.55%). The peak number of cases seen in 1 month was five, with 17 of 56 months having no HBV-positive tests. HCV was the most frequent virus found in our patient population. The mean monthly seroprevalence of HCV was 4.15% ± 2.23% (range 0% to 10.65%). In 2 of the 56 months, there were no patients positive for HCV.


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Table 1. Monthly Seroprevalences of HIV, HBV, and HCV in Cardiovascular Patients at Hôpital Broussais (Paris) From 1994 to 1998

 
To evaluate the trend in blood-borne viruses over the 56-month period, the frequency of positive tests were plotted against time and subjected to linear regression (Fig 1). The frequency of HBV has remained constant over the period of study (r2 = 0.001, p = 0.84). In contrast, the pattern for HCV demonstrates a progressive decrease in seroprevalence over the time period of the study (r2 = 0.231, p = 0.0002). A similar, but weaker, downward trend is also shown for HIV by linear regression (r2 = 0.071; p = 0.047).



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Fig 1. Seroprevalences of HIV, HBV, and HCV in cardiovascular surgical patients at Hôpital Broussais from 1994 to 1998. The seroprevalence is expressed as a percentage of the number of patients presenting for that given month. The line is the result of linear regression fitting, and the associated p value of the fit is shown.

 
Calculated estimates of occupation risk
To estimate the cumulative occupational risk of infection by HIV, HBV, and HCV, the annual seroprevalence data from 1998 was used to estimate pi in the previously described actuarial model (HIV = 0.0021, HBV = 0.0093, HCV = 0.033). The probabilities ri of seroconversion from a single percutaneous injury for HIV, HBV, and HCV were estimated to be 0.3%, 30% and 4%, respectively [2, 9, 17].

Table 2 shows the cumulative occupational probability of infection by each individual blood-borne viruses as a function of career length for differing frequencies of percutaneous injuries per annum. The risk of seroconversion from HIV based on our data is extremely low, remaining below 1% at 30 years, even with an extreme injury rate of 15 per year. By comparison, the risk of infection by HBV and HCV is up to two orders of magnitude greater over the estimated 30-year career of the surgeon. Although HCV is more frequent in our population than HBV by approximately three- to fourfold in 1998, the risk of HCV infection is lower than that of HBV. This is due to the approximately 10-fold greater rate of infectivity for HBV as compared with HCV. Figure 2 shows the probability of becoming infected by any one of the three blood-borne viruses over the career of the surgeon. The overall probability is dominated by the high degree of risk associated with HBV.


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Table 2. Cumulative Occupational Risk of Infection With HIV, HBV, and HCV According to Equation I' of the Acturial Model

 


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Fig 2. Calculated occupational risk of infection by HIV, HBV, or HCV blood-borne viruses as a function of career length for surgeons at Hôpital Broussais. The probability of infection is estimated using equations I and II, and is expressed as percent chance out of 100. Each individual curve shows the risk for a given number of percutaneous injuries per annum.

 
Vaccination against HBV has been demonstrated to be up to 96% effective in reducing the transmission of HBV [18, 19]. The effects of vaccination on the probability of becoming infected by HBV or by any one of the three blood-borne viruses is plotted in Table 3. It is evident from comparison of Tables 2 and 3 that vaccination causes a significant reduction in the lifetime probability of seroconversion for HBV, and consequently diminishes the cumulative lifetime probability of infection by any one of the blood-borne viruses.


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Table 3. Effects of the Vaccine Against HBV on the Cumulative Risk of HBV Seroconversion According to Equation I' of the Actuarial Model

 
Table 4 compares the career occupational risk for a surgeon averaging two percutaneous exposures to patient bodily fluids per year. Assuming a constant rate of injury, the risk of occupational seroconversion for HCV has diminished approximately twofold over the 5 years of our study. While the risk of infection by HIV was already below 1% in 1994, the decreasing seroprevalence of this virus has further reduced to risk faced by the surgeon by two- to threefold. However, calculation of the risk posed by all potential infectious blood-borne viruses shows a much smaller decrease in occupational risk due to the high rate of infectivity by HBV, the only virus that has not shown a reduced seroprevalence over the 56-month period.


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Table 4. Comparisons of the Cumulative Career Occupational Risk of Infection by Blood-Borne Viruses Between 1993 and 1998 With n = 2 Percutaneous Injuries Per Annum, According to Equation I' of the Actuarial Model

 

    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
When considering the subject of occupation risk of infection from blood-borne viruses, HIV is the leading pathogen on the minds of most surgeons. However, screening of surgical candidates at the cardiovascular service of Hôpital Broussais demonstrates that in this population, the hepatitis viruses HBV and HCV occur at a markedly greater frequency than HIV. Although the frequency of HCV, the leading cause of non-A, non-B hepatitis, has decreased between 1994 and 1998, it is still the most prevalent blood-borne virus. This points to HCV as a major pathogen for both cardiovascular patients and their surgeons. The seroprevalences of HBs antigen and of HIV-specific antibodies in our patient population is higher than the general adult population of France, as estimated from voluntary blood donors [20]. The prevalence of HCV antibodies in our cardiovascular population was about sixfold that of the general adult population in Paris in 1994 and threefold in 1998 [21]. Although our study was not designed to evaluate factors influencing the seroprevalence of blood-borne viruses, we can hypothesize that the decreasing seroprevalence of HCV and HIV may be the result of preventive measures introduced to minimize transmission of blood-borne viruses. Public health measures include increased public awareness of routes of transmission via public service announcements and programs such as needle exchange for intravenous drug users. Measures to decrease iatrogenic transmission were also implemented in France in the last 5 years [22].

Our actuarial model shows that the principal source of occupational risk to surgeons is not HIV, but the hepatitis viruses. Studies have estimated the risk of HIV seroconversion after a single percutaneous exposure to be at approximately 0.3% [2]. The risk to the surgeon of HIV transmission from this patient population is less than 1% over a 30-year career, even with an extreme percutaneous injury rate of 15 per year. This is consistent with data from worldwide surveys of HIV seroconversion in health care workers. As of 1997, there has only been 1 documented case and 14 possible cases of surgeons seroconverting from occupational exposure to HIV [23]. This represents 1.1% and 8.2% of the worldwide documented and possible cases, respectively. Factors associated with seroconversion after percutaneous injury are larger volumes of blood, deeper penetration, and possibly higher titers of HIV virus. Most surgical injuries are not affiliated with transmission of high volumes of blood, as they are with solid instruments and not hollow-bore needles. While the surgeon needs to be aware of the occupational risk from HIV, the hepatitis viruses present a greater risk of morbidity and mortality. Based on our model, equation II, for an unvaccinated surgeon who sustains an average of five percutaneous injuries a year, he would need to work for 22,004 years to have a 50% chance of seroconversion for HIV. In contrast, he would need to work for 49 years to have a 50% probability of HBV seroconversion and 105 years for HCV seroconversion.

The risk of infection by blood-borne virus is dependent on three factors: (1) the prevalence of the infectious agent; (2) the probability of infection from exposure; and (3) the frequency of exposure. The decreasing prevalence of HCV in our patient population would indicate that the risk to cardiovascular surgeons operating on this population has diminished between 1994 and 1998. Although decreasing the seroprevalence of blood-borne viruses will lessen the risk faced by the operating surgeon, this is dependent on the development of public health measures, including screening, vaccination, treatment, and control of transmission, that are for the most part beyond the control of the surgeon. While most surgeons express concern about blood-borne viruses, surveys have shown that the majority of surgeons continue to put themselves at risk for the patient’s benefit [8]. The physician can reduce the seroprevalence in his patient population by refusing to operate on patients who are positive for the viruses, but this is considered ethically unacceptable. Thus, it is important to consider methods to influence the other factors affecting occupational risk.

The rate of exposure to bodily fluids is one variable that surgeons can directly influence. The onset of the AIDS epidemic led to the recommendation of universal precautions in treatment of all patients where there is the potential for exposure to bodily fluids. Changes in operative techniques including "no-touch" passing of instruments, use of instrumentation to hold all sharps, minimizing the use of hands in body cavities with limited visualization, and sewing away from the surgeon have been proposed to further reduce the percutaneous injury rate [11, 24]. While the use of double gloves instead of single gloves will not prevent percutaneous exposure, it has been demonstrated to decrease the frequency of cutaneous exposure from glove failure [3]. The use of double gloves also decreases the volume of patient blood inoculum when percutaneous injury does occur with suturing needles [25]. Implementation of these procedures has affected the rate of physician exposure to bodily fluids. Studies by Lowenfels and associates show that the rate of percutaneous injuries has diminished between the years 1988 and 1993, from a mean of 5.5 yearly injuries to 2.1 [26, 27]. Increasing consciousness about occupational risk as well as education about protective measures may further decrease the rate of exposure.

Surveys reveal that a significant number of surgeons would like to screen all preoperative patients for HIV before surgery [7, 15, 16]. In fact, over 95% of cardiovascular surgeons supported systematic preoperative testing [4, 28]. They argue that screening all patients would decrease the probability of exposure, as surgical practice would be altered for patients known to be an infectious risk. There are, however, a number of problems with systematic screening. Testing of patients is dependent on patient consent, and illicit testing or refusal to treat patients who refuse consent is considered unethical. Not all clinical situations, and in particular emergent ones, permit testing before surgery. Finally, the strongest argument against systematic testing is that knowledge of patient HIV risk has not been shown to decrease the rate of percutaneous injury [3]. The best surgical practice in light of these arguments is for the surgeon to assume all patients are infectious and to use all means available to minimize exposure.

The third factor affecting occupational risk, the infectivity of the pathogen, is one that the surgeon can partially control. While HBV does not have the inevitable fatal course of HIV, it is a major source of morbidity and mortality. Coupled with the high rate of infectivity, it represents the greatest threat to the operating surgeon. The risk of HBV infection can be lessened by vaccination. HBV vaccination results in protective levels of antibodies in 88% to 95% of recipients, reducing the rate of transmission from 30% to 4% [19, 29]. Studies have shown that among younger surgeons, the message about HBV vaccination is starting to make an impact [6]. Continued efforts to increase the rate of vaccination can further diminish the economic and health impact of HBV.

While similar vaccination has not been developed for HIV, some progress has been made with postexposure prophylaxis (PEP). Centers for Disease Control guidelines have been established for health care workers exposed to HIV. The decision to recommend PEP is based on stratification of risk based on the type of exposure and the patient’s HIV status or HIV risk factors if serum status is unknown. Case control studies of monotherapy PEP with zidovudine have shown that PEP can reduce the odds of seroconversion from percutaneous exposure by 80% [30]. There are also multi-drug PEP regimens that are available for exposure to patients who are not treatment naive and may harbor resistant strains.

This leaves HCV as the only blood-borne virus whose infectivity has not been diminished. There are currently no vaccines available against HCV, and PEP with immune globulin has not been shown to be effective in reducing seroconversion [31]. In light of this, our data demonstrating a diminishing seroprevalence of HCV are encouraging. Nonetheless, reducing the frequency of exposure to bodily fluids is still the best defense the surgeon has.

In summary, we show that in the patient population presenting to our cardiovascular service: (1) HCV is the most prevalent blood-borne virus; (2) HIV is very infrequently found; (3) the seroprevalences of HCV and HIV have been decreasing over the past 5 years; (4) the probability of becoming infected with a blood-borne over the career of the surgeon is notable; (5) the greatest occupational risk to the surgeon is from the hepatitis viruses and not HIV; and (6) vaccination against HBV can greatly reduce the risk faced by the surgeon.


    Acknowledgments
 
We thank the staff of the laboratory of virology at Hôpital Broussais who performed the analysis of patient sera.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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Accepted for publication July 15, 1999.




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