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© 1996 The Journal of Bone and Joint Surgery, Inc. Use of the Hepatitis-B Vaccine and Infection with Hepatitis B and C among Orthopaedic Surgeons* , AND THE AMERICAN ACADEMY OF ORTHOPAEDIC SURGEONS SEROSURVEY STUDY COMMITTEE , ATLANTA, GEORGIAInvestigation performed by the National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta
We used a questionnaire, with a guarantee of anonymity to the respondents, and conducted serological testing of 3411 attendees at the 1991 Annual Meeting of The American Academy of Orthopaedic Surgeons to evaluate the prevalences of infection with the hepatitis-B and C viruses and the use of the hepatitis-B vaccine among orthopaedic surgeons. There was evidence of infection with hepatitis B in 410 (13 per cent) of 3239 participants who had reported having no non-occupational risk factors; 2103 (65 per cent) reported that they had been immunized with the hepatitis-B vaccine. Of 3262 participants who reported having no non-occupational risk factors and who were evaluated for infection with hepatitis C, twenty-seven (less than 1 per cent) tested positive for the antibody to the hepatitis-C virus. The prevalence of previous infection with hepatitis B increased with increasing age; four (3 per cent) of 136 surgeons who were twenty to twenty-nine years old had evidence of infection, whereas ninety-six (27 per cent) of 360 surgeons who were sixty years old or more had evidence of infection. The prevalence of infection with hepatitis C also increased with increasing age; none of 135 surgeons who were twenty to twenty-nine years old had evidence of infection, and five (1 per cent) of 360 surgeons who were sixty years old or more had evidence of the virus. The prevalence of vaccination decreased steadily with age: 123 (90 per cent) of 136 surgeons who were twenty to twenty-nine years old reported that they had received the hepatitis-B vaccine, whereas 127 (35 per cent) of 360 surgeons who were sixty years old or more reported that they had received the vaccine. The prevalence of infection with hepatitis B or hepatitis C was not associated with the measured indices of exposure to the blood of patients (the number of cutaneous or mucosal contacts with blood that had occurred within the previous month or the number of percutaneous injuries that had occurred within the previous month or year, as recalled by the participants). In conclusion, the prevalence of immunization with the hepatitis-B vaccine was high among the orthopaedic surgeons studied. Although the prevalence of infection with the hepatitis-C virus was several times greater in the current investigation than has been reported in studies of blood donors in the United States, infection with this virus was not associated with the indices of occupational exposure to blood measured in this study.
Infection with the hepatitis-B virus is an occupational risk for health-care workers. The risk of infection is three to five times greater for physicians, dentists, and other hospital workers than for the general population. In addition, the risk is related directly to the degree of exposure to the blood of patients through accidental puncture of the skin with a used needle, other percutaneous injuries, and contact of mucous membranes with the blood of patients11,12,15,18,30,31. Few large-scale studies of infection with hepatitis B have been conducted among health-care workers since 1982, the year that the hepatitis-B vaccine became available. The hepatitis-C virus is also a blood-borne pathogen and thus is transmitted through blood transfusions and accidental puncture of the skin with a used needle. Within the previous few years, serological tests have been developed to detect the antibody to the hepatitis-C virus. In two hospital-based studies in Japan21,26, the risk of transmission of the virus was estimated to be 3 per cent (three of 110) and 10 per cent (seven of sixty-eight) after an accidental puncture of the skin with a needle that had been used for a patient who had the antibody to the hepatitis-C virus. However, there have been few studies in which the prevalence of infection with hepatitis C in health-care workers has been evaluated. Because of the potential for substantial exposure to the blood of patients through accidental puncture with a needle and the frequent handling of sharp instruments and objects during operative procedures, orthopaedic surgeons are at risk for infection with the hepatitis-B virus and other blood-borne pathogens27,34. To determine the risk of infection with the hepatitis-B or C virus, and to evaluate the frequency of immunization with the hepatitis-B vaccine, we conducted a survey of orthopaedic surgeons attending the 1991 Annual Meeting of The American Academy of Orthopaedic Surgeons.
Study Population and Collection of Data Serum specimens were obtained from those who volunteered to participate, and each participant completed, anonymously, a self-administered questionnaire that included items regarding demographic characteristics; history with regard to clinical practice; immunization with the hepatitis-B vaccine; the number of cutaneous, percutaneous, and mucosal contacts with the blood of patients during operations within the previous month or year; and non-occupational risk factors for infection with blood-borne pathogens. Because the questionnaire had been designed primarily to determine risk factors for infection with the human immunodeficiency virus, non-occupational risk factors were defined as receipt of a blood transfusion at some time between 1978 and 1985, receipt of a clotting factor concentrate for hemophilia or another coagulation disorder at some time since 1977, male-to-male sexual contact at some time since 1977, intravenous drug abuse at some time since 1977, birth in Haiti or Central or East Africa, or sexual contact with someone who had any of these risk factors. Participants were not asked to indicate which risk factor or factors applied to them. To assess how representative the participants were of orthopaedic surgeons in general, we compared the demographic and clinical-practice characteristics of the participants with those of 10,411 orthopaedic surgeons who had responded to a questionnaire33 in November 1990. The questionnaire had been mailed to the 20,625 orthopaedic surgeons who were known by The American Academy of Orthopaedic Surgeons to be in training, in practice, or retired from practice in the United States or Canada.
Serological Testing Testing for the antibody to the hepatitis-C virus was done with a commercially available, first-generation enzyme immunoassay (Abbott Laboratories). When the test was positive, the serum was tested again with the enzyme immunoassay. Serum that was reactive on both immunoassays was tested with use of a supplemental neutralization assay for the antibody to the hepatitis-C virus (Abbott Laboratories). The sensitivity of the tests for the antibody to the hepatitis-C virus is approximately 90 per cent; data regarding the specificity of the test are limited7.
Analysis
We examined the relationships between hepatitis-B infection, hepatitis-B vaccination, and hepatitis-C infection and the demographic characteristics, the clinical-practice history, and the degree of exposure to the blood of patients. The two-tailed Fisher exact test and the chi-square test for trend were used to determine the significance of differences between proportions and to evaluate trends. Cochran-Mantel-Haenszel statistics were used to evaluate associations adjusted for age.
Characteristics of the Participants The characteristics of the participants were compared with those of the 10,411 orthopaedic surgeons who had responded to the questionnaire33 mailed in 1990. In the present study, the participants were younger, there were more participants in postgraduate training, and there were fewer retired orthopaedic surgeons. The participants in the two studies had a similar degree of exposure to blood-borne pathogens: the total number of years of training or practice, the average number of operative procedures that were performed per month, the number of cutaneous or mucosal contacts with the blood of patients that had occurred within the previous month, and the number of percutaneous injuries that had occurred within the previous month or year were similar for the two groups33.
Use of the Hepatitis-B Vaccine and Prevalence of Hepatitis-B Infection Over-all, of 3383 participants from whom there was sufficient serum for testing for the hepatitis-B markers and who reported their vaccination history, 465 (14 per cent) had evidence of infection with hepatitis B—that is, either they tested positive for the antibody to the hepatitis-B core antigen (418 participants) or they tested positive for the antibody to the hepatitis-B surface antigen and they had not received the vaccine (forty-seven participants). Participants who had not received the vaccine were more likely than those who had received it to test positive for the antibody to the hepatitis-B core antigen (odds ratio, 7.48; 95 per cent confidence interval, 5.91 to 9.48). All of the participants who tested positive for the antibody to the hepatitis-B core antigen also tested positive for the antibody to the hepatitis-B surface antigen, except for thirty-six participants, none of whom tested positive for the hepatitis-B surface antigen. Of the participants who were tested for hepatitis-B markers, 3347 reported whether or not they had non-occupational risk factors for infection with the human immunodeficiency virus. At least one non-occupational risk factor was reported by 108 participants (3 per cent); twenty-seven (25 per cent) of them had evidence of infection with hepatitis B, compared with 410 (13 per cent) of 3239 participants who reported having no non-occupational risk factors (odds ratio, 2.30; 95 per cent confidence interval, 1.43 to 3.67). The subsequent analyses for hepatitis-B infection and vaccination are restricted to 3239 participants who reported having no non-occupational risk factors. Age was an important determinant for both evidence of infection with and vaccination for hepatitis B. The prevalence of infection increased steadily with increasing age, from four (3 per cent) of 136 participants who were twenty to twenty-nine years old to ninety-six (27 per cent) of 360 participants who were sixty years old or more (p < 0.0001, chi-square test for trend). The rate of immunization with the hepatitis-B vaccine was inversely related to age. Over-all, 2103 (65 per cent) of the 3239 participants reported that they had received the vaccine and had no history of infection with hepatitis B. One hundred and twenty-three (90 per cent) of 136 participants who were twenty to twenty-nine years old reported that they had received the vaccine; this percentage decreased steadily to 127 (35 per cent) of 360 participants who were sixty years old or more (p < 0.0001, chi-square test for trend). Only nine participants (7 per cent) who were twenty to twenty-nine years old were susceptible to hepatitis-B infection, compared with 137 (38 per cent) who were sixty years old or more. Vaccinated participants who tested negative for the antibody to the hepatitis-B core antigen and had a low level of antibody to the hepatitis-B surface antigen tended to be older: the level was less than ten sample ratio units in 363 (36 per cent) of 1015 surgeons who were forty years old or more, compared with 165 (15 per cent) of 1088 surgeons who were less than forty years old (odds ratio, 3.11; 95 per cent confidence interval, 2.51 to 3.86). The prevalence of infection with hepatitis B was slightly lower in women (eleven [10 per cent] of 109) than in men (385 [13 per cent] of 3069) (odds ratio, 0.78; 95 per cent confidence interval, 0.39 to 1.52), but this difference was not significant with the numbers available. Although the rate of vaccination was higher for women than for men (Table I), there was no significant difference after the rates had been adjusted for age: sixty-eight (84 per cent) of eighty-one women who were less than forty years old and 1008 (83 per cent) of 1216 men in the same age-group had received the vaccine (odds ratio, 1.08; 95 per cent confidence interval, 0.57 to 2.09).
The occupational status and the number of years in clinical practice were also associated with both evidence of hepatitis-B infection and vaccination. The rate of vaccination was higher for participants who were in postgraduate training (internship, residency, or fellowship) than for those who were in full-time or part-time practice, administration, or retirement (p < 0.05, two-tailed Fisher exact test) (Table I). An increasing number of years of practice was associated with an increasing prevalence of infection and with a decreasing rate of vaccination (p < 0.05, chi-square test for trend, for both comparisons). Because the occupational status and the number of years of practice corresponded closely with age, it was not possible to assess the effects of these variables independently of age. After exclusion of the participants who reported having non-occupational risk factors and of those who were protected from infection because they had received the vaccine, the rates of hepatitis-B infection were examined by factors related to the degree of exposure to the blood of patients during operative procedures. For these 1136 participants, no significant association was found between the rate of infection with hepatitis B and the average number of operative procedures that were performed per month, the number of cutaneous or mucosal contacts with blood that had occurred within the previous month, or the number of percutaneous injuries that had occurred within the previous month or year (p > 0.05, Cochran-Mantel-Haenszel statistics, after adjusting for age) (Table II). With this sample size of 1136 participants who had not received the vaccine and 410 (36 per cent) who had evidence of infection, the study had an 80 per cent power to detect an approximate absolute difference of 8 per cent in the prevalence of infection.
Prevalence of Infection with the Hepatitis-C Virus For the participants who reported having no non-occupational risk factors, the prevalence of infection with hepatitis C was significantly associated with the age, the occupational status, and the number of years of practice (p < 0.05 for each comparison) (Table III). The prevalence of infection increased steadily with age, from none of 135 participants who were twenty to twenty-nine years old to five (1.4 per cent) of 360 participants who were sixty years old or more. Similarly, the prevalence increased with an increasing number of years of practice and was higher for participants who were in full-time clinical practice than for those who were in postgraduate training. The prevalences for men and women were similar.
No significant associations were found between the prevalence of infection with hepatitis C and the average number of operative procedures that were performed per month, the number of cutaneous or mucosal contacts with blood that had occurred within the previous month, or the number of percutaneous injuries that had occurred within the previous month or year (Table III). Furthermore, hepatitis-C infection was not associated with hepatitis-B infection. After exclusion of those who had serological evidence of immunity or who had reported that they had received the hepatitis-B vaccine, the prevalence of infection with hepatitis C was five (1.3 per cent) of 388 participants who had infection with hepatitis B, compared with ten (1.5 per cent) of 685 who were susceptible to infection with hepatitis B (odds ratio, 0.88; 95 per cent confidence interval, 0.23 to 2.85). With this sample size of 3262 participants and twenty-seven (0.8 per cent) who had evidence of infection with hepatitis C, the study had an 80 per cent power to detect approximately twofold differences.
The large percentage of participants in this study who reported that they had been immunized with the hepatitis-B vaccine is very encouraging. The frequency of vaccination was especially high (123 of 136 participants) for the orthopaedic surgeons who reported having no non-occupational risk factors and who were less than thirty years old. Nevertheless, of the 3239 participants who reported having no non-occupational risk factors, 727 (22 per cent) had not received the vaccine and were susceptible to infection with the hepatitis-B virus. The lower prevalence of immunization for the older orthopaedic surgeons indicates that more efforts are needed to encourage vaccination for this group. Few other data are available on the vaccination of surgeons. In a study in South Carolina and in a national survey conducted by mail in 1991, 115 (49 per cent) of 235 and 592 (54 per cent) of 1106 surgeons, respectively, had received the hepatitis-B vaccine5,24. A survey of 770 surgeons in training or practice affiliated with twenty-one hospitals in two major metropolitan areas demonstrated that 418 (54 per cent) had received the hepatitis-B vaccine28. To our knowledge, the present survey of orthopaedic surgeons is the largest study of vaccination of health-care workers to date, and it is one of the few in which serological testing was used to evaluate self-reports of vaccination. Approximately 25 per cent of the participants who reported that they had received the hepatitis-B vaccine tested negative for the antibody to the hepatitis-B core antigen and had a level of the antibody to the hepatitis-B surface antigen that was less than ten sample ratio units. This is not unexpected, given that in two studies involving a total of approximately 1200 people who had responded to the vaccine (that is, who had produced antibody to the hepatitis-B surface antigen at a level of more than 9.9 sample ratio units) 30 to 50 per cent of those tested did not have a detectable level of antibody seven years after the vaccination13,16. These studies showed, however, that when people respond to a vaccine with the production of antibody, and the level of the antibody decreases to the point at which it is no longer detectable, they are still protected from infection for at least nine years after the vaccination, and booster doses of vaccine are not routinely recommended8,14. In the current investigation, some participants who had received the vaccine and had a level of antibody to the hepatitis-B surface antigen that was less than ten sample ratio units probably had had no initial immune response to the vaccine. Immunogenicity studies of health-care workers and other groups have demonstrated that age is the most important factor affecting the immune response to the vaccine. For example, in a study in Louisiana4, an adequate level of the antibody was produced in 783 (93 per cent) of 839 health-care workers who were less than forty years old, compared with 771 (83 per cent) of 927 health-care workers who were forty years old or more. In our study, older surgeons were more likely to have a low level of the antibody to the hepatitis-B surface antigen; this may represent either a longer interval since they had received the vaccine or a higher rate of an initial non-response to the vaccine. We may have overestimated the percentage of orthopaedic surgeons who were protected from hepatitis-B infection as a result of vaccination if in fact the low level of the antibody to the hepatitis-B surface antigen was due to the lack of an immune response to the vaccine. In the current study, 465 (14 per cent) of 3383 participants had evidence of infection with hepatitis B, but none tested positive for the hepatitis-B surface antigen, a serological marker that indicates active infection. These findings are consistent with the results of studies conducted on surgeons during the 1970's and the early 1980's. In those studies, the prevalence of infection with hepatitis B ranged from 14 per cent (fifty-seven of 420 surgeons) to 28 per cent (fifty of 176 surgeons), depending on the subspecialty and the geographic area; the percentage of the surgeons who tested positive for the hepatitis-B surface antigen ranged from 0.8 per cent (one of 125) to 1.2 per cent (five of 420)11,12,15,30,31. A study of surgeons in the United States Army30, carried out between 1972 and 1974, demonstrated that eight (11 per cent) of seventy-five orthopaedic surgeons had serological evidence of previous or active infection with hepatitis B. In the current survey, the rate of infection with hepatitis B increased with increasing age and with an increasing number of years of practice. These associations have been observed in other studies of hepatitis-B infection in health-care workers28,32, and, as in this study, the independent effects of age and the number of years of practice could not be analyzed. No association was observed between infection with hepatitis B and the degree of exposure to the blood of patients. This finding is in contrast to the results of several other studies of health-care workers12,15. The reason why we did not find such an association may be that occupational exposure to blood is uniformly high among orthopaedic surgeons. In the studies in which the prevalence of hepatitis-B infection increased with greater degrees of exposure to blood, comparisons generally were made across specialties instead of within a specialty. For example, surgeons were compared with internists or laboratory technicians were compared with dietary personnel. Another possible reason for the lack of an association is that the indices measured in our survey may not have adequately reflected the occupational exposure that leads to hepatitis-B infection. The orthopaedic surgeons were asked to report the number of cutaneous and mucosal contacts with the blood of patients that had occurred within the previous month, the number of percutaneous injuries that had occurred within the previous month and year, and the average number of operative procedures that were performed per month. This information was acquired retrospectively and may not have been recalled or estimated accurately; it was not possible to assess independently the accuracy of the responses. Similar indices during an earlier period in a surgeon's career may be a more accurate indicator of exposure to blood; however, such information would be difficult to obtain and is subject to recall bias. In our serological survey, hepatitis-C infection was detected in twenty-seven (less than 1 per cent) of 3262 participants who had reported having no non-occupational risk factors for infection. This prevalence is consistent with those reported for surgeons in the United States and elsewhere, which have ranged from 0 (none of 199 surgeons) to 2 per cent (sixty of 3087 surgeons), as determined with use of a first or second-generation immunoassay or supplemental testing for the antibody to the hepatitis-C virus1,6,9,17,19,20,22,29,32. As was the case with hepatitis-B infection, the prevalence of hepatitis-C infection for orthopaedic surgeons was directly associated with age and the number of years of practice. It is difficult to determine whether the prevalence of infection with hepatitis C in the present study, and its association with age and the number of years of practice, are indicative of an occupational risk for health-care workers. First of all, the prevalence of infection with hepatitis C did not increase with an increase in the reported degree of exposure to blood. In addition, there are difficulties with the method with which exposure to blood was quantitated, as has already been discussed. With one exceptions26, previous studies addressing the association between hepatitis-C infection and the degree of exposure to blood in health-care workers also have not shown increasing rates of hepatitis-C infection with an increased exposure to blood. In the exceptional study, which involved a mixed group of hospital employees, an increased prevalence of infection with hepatitis C was found for individuals who had reported a history of frequent accidental punctures with used needless26. Perhaps the best index of lifetime occupational exposure to blood is serological evidence of infection with hepatitis B, and no association was found between hepatitis-B and hepatitis-C infection in our study. The reason for this lack of association is unclear. Our ability to detect an association may have been limited by the relatively small number of participants who had not received the hepatitis-B vaccine and who tested positive for the antibody to the hepatitis-C virus. Another difficulty is that currently available first and second-generation tests for the antibody to the hepatitis-C virus do not detect all cases of hepatitis-C infection. Also, there is evidence that after acute infection with hepatitis C the level of the antibody can decrease to the point at which it is undetectable2. We used the first-generation test for the antibody, which was the only test available at the time that the survey was conducted. The prevalence of infection with hepatitis C in our study is comparable with that in studies in which the second-generation assay was used17,19,32. The major difference between the first and second-generation tests is that the latter has a shorter window between acute infection and the detection of the antibody, but this difference is not relevant to a serological study of the prevalence of infection in asymptomatic people. The use of the second-generation test would not be expected to change the findings of the study, as the second-generation test detects infection in an additional 1.2 asymptomatic individuals per 1000 tested, compared with the first-generation test23. In one study, the level of antibody to the hepatitis-C virus that was determined with use of the first-generation test became undetectable at a rate of three per 100 person-years3. Because of the limitations in the sensitivity of the tests to detect the antibody to the hepatitis-C virus, the prevalence of infection in orthopaedic surgeons may be higher than the prevalence that we determined. Determining whether the prevalence of infection with the hepatitis-C virus indicates an occupational risk for health-care workers is also difficult because serological studies of hepatitis-C infection in health-care workers, including the present investigation, have been uncontrolled. In one study, the prevalence of infection with hepatitis C in dentists in New York City was twelve times greater than that in retrospectively age-matched blood donors from the same geographic area22. The prevalence of hepatitis-C infection in blood donors has been reported to range from 0.09 per cent (fourteen of 15,881 donors) to 0.36 per cent (twenty-two of 6118 donors), which is two to ninefold less than that observed in orthopaedic surgeons10,25. Blood donors may not be a proper group for comparison, however, as individuals who have risk factors (such as intravenous drug abuse) or a history of hepatitis are asked to refrain from donating blood. In addition, the age distribution of blood donors may differ from that of orthopaedic surgeons. Because of several potential limitations of the present serological survey, the over-all results must be interpreted with caution. The study involved orthopaedic surgeons who were attending an annual meeting of The American Academy of Orthopaedic Surgeons and who volunteered to participate. Some surgeons may have chosen or declined to participate because they knew their status of infection with hepatitis B or C. Therefore, the results of this survey may not be representative of all orthopaedic surgeons in the United States. In conclusion, approximately two-thirds of the orthopaedic surgeons who participated in this study had received the hepatitis-B vaccine, and the rate of vaccination was especially high for younger surgeons. Although the decreased use of the vaccine by the older participants highlights the need to encourage immunization for surgeons in this age-group, continued high rates of vaccination of younger surgeons will eventually result in protection from infection for nearly all surgeons. The prevalence of hepatitis-C infection in the participants in our study was several times greater than the prevalence in blood donors in the United States; this suggests a possible occupational risk. Controlled studies comparing health-care workers with appropriate groups may help to determine the risk of hepatitis-C infection for health-care workers. In addition, cohort studies of large groups of health-care workers may help to quantitate their risk of hepatitis-C infection more accurately; however, because of the over-all low rate of infection, such studies may be impractical.
NOTE: The authors thank Anthony Wright, Penny S. McKibben, Matthew Clarke, and Robert Holman, M.S., for their assistance in laboratory testing and data analysis, and Miriam J. Alter, Ph.D., and David M. Bell, M.D., for their helpful comments.
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.
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