Hepatitis B vaccination of healthcare workers at the Princess Marina Hospital, Botswana

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1 International Health Advance Access published November 25, 2014 Int Health doi: /inthealth/ihu084 Hepatitis B vaccination of healthcare workers at the Princess Marina Hospital, Botswana Tichaona Machiya a, Rosemary J. Burnett b, *, Lucy Fernandes a, Guido François c, Antoon De Schryver c, Marc van Sprundel c and M. Jeffrey Mphahlele b ORIGINAL ARTICLE a Department of Public Health, University of Limpopo, Medunsa Campus, Pretoria, South Africa; b HIV and Hepatitis Research Unit, Department of Virology, PO Box 173, University of Limpopo/National Health Laboratory Service, Medunsa Campus, Pretoria, 0204, South Africa; c Department of Epidemiology and Social Medicine, University of Antwerpen, Belgium *Corresponding author: Tel: ; Fax: ; Rose.Burnett@ul.ac.za Received 29 May 2014; revised 8 August 2014; accepted 29 September 2014 Background: Batswana (i.e., the people of Botswana) healthcare workers (HCWs) are at high risk for occupational exposure to hepatitis B virus (HBV), thus the Botswana Ministry of Health recommends that HCWs should receive three doses of hepatitis B (HB) vaccine. However there are no data on HB vaccination uptake by Batswana HCWs. This study investigated knowledge of, and attitudes towards HB prevention and control, and predictors of HB vaccination uptake in HCWs at the Princess Marina Hospital during Methods: Self-administered questionnaires were distributed to doctors, nurses and laboratory workers (n¼200). Knowledge was measured using 14 questions; attitude was measured using a 5-point Likert scale and 9 statements. Data on vaccination status and demographics were collected. Results: Of the respondents, 17.2% (20/116) had good knowledge, and 97.4% (113/116) had positive attitudes. At least one dose of HB vaccine had been received by 50.9% (59/116), while 31.0% (36/116) had received all three doses. Profession was the only predictor of HB vaccination uptake, with being a laboratory worker (OR¼61.0) or a doctor (OR¼51.5) predicting HB vaccination uptake with at least one dose. Conclusion: This is the first study on HB vaccination of Batswana HCWs, and shows that HB vaccination uptake is suboptimal. Keywords: Botswana, Healthcare workers, Hepatitis B virus, Princess Marina Hospital, Vaccination Introduction Healthcare workers (HCWs) in Botswana are at high risk for occupational exposure to two important bloodborne viruses. First, a third of the country s adults and 31.8% of pregnant women aged years are living with HIV infection, 1 with 50 70% of hospital beds being occupied by patients with HIV. 2 Second, Botswana is also endemic for hepatitis B virus (HBV), the causative agent of hepatitis B (HB), a serious liver disease which results in considerable morbidity and mortality. 3 Early studies conducted before the HIV epidemic reported % HB surface antigen (HBsAg) prevalence, 4 6 which classifies Botswana as highly endemic for HBV (i.e., 8% HBsAg carriage 3 ). In addition, HIV infection is a risk factor for HBV infection, and symptomatic HIVpositive patients are often co-infected with actively replicating HBV. 7 Studies from Botswana have found HIV/HBV co-infection rates ranging from 5.3% in patients receiving antiretroviral treatment for HIV, 8 to 10.6% in therapy naïve patients. 9 However, HIV is a risk factor for occult HBV infections (the presence of HBV DNA in the absence of HBsAg), 7 and these studies relied on HBsAg testing to identify HBV infections. A study from neighbouring South Africa found that 40.6% of therapy naïve patients with AIDS were HBV DNA positive, indicating that these patients were infectious, and these included 100% of HBsAg-positive and 23% of HBsAg-negative patients. 7 It is thus likely that the reported HIV/HBV co-infection rates from Botswana are an underestimation of the true prevalence, with many of the co-infected patients testing HBsAg-negative but harbouring actively replicating HBV. This means that HCWs experiencing occupational exposures to blood/body fluids are currently at a greater risk for HBV infection than before the HIV epidemic in Botswana. HIV/AIDS is not yet a vaccine-preventable disease, but there is a highly effective and safe vaccine against HBV infection. In 2000 Botswana complied with the 1992 recommendations of WHO by introducing universal HB vaccination at birth, two and nine months, and by 2002 was already achieving 85% coverage. 10 The Botswana Ministry of Health has cited the high rate of HIV/ HBV co-infection in hospitalised patients as a central issue in its # The Author Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene. All rights reserved. For permissions, please journals.permissions@oup.com. 1of6

2 T. Machiya et al. guidelines for HB vaccination of HCWs, calling for the vaccination of all at-risk HCWs. 11 These guidelines state that free HB vaccination should be offered by training institutions to student HCWs before they come into contact with blood or body fluids. Furthermore, health facility employers are called upon to offer free HB vaccination to HCWs who are occupationally exposed to blood or body fluids. Also, post-vaccination testing for protective antibodies (anti-hbs) is recommended, although details of when this should be done, or what is considered to be a protective anti-hb level, are not included in the guidelines. 11 There are no data on HB vaccination of Batswana (i.e., the people of Botswana) HCWs, hence the need for this study, which aimed to investigate: knowledge about, and attitudes towards the prevention and control of HB; HB vaccination coverage; associations between knowledge/attitudes and vaccination uptake; and predictors of HB vaccination uptake, amongst nurses, doctors and laboratory workers at the Princess Marina Hospital in Gaborone, Botswana, during Methods Princess Marina Hospital is the largest (550 beds) of three government referral hospitals in Botswana, and is a teaching hospital of the University of Botswana, located in the capital city of Gaborone. 12 At the time of this study the sampling frame of at-risk HCWs consisted of 103 laboratory workers, 107 doctors, and 440 nurses. Using Epi Info version 5.1 (CDC, Atlanta, GA, USA), for the first two objectives (for which descriptive statistics were required) a sample size of 84 was calculated at 80% power and 95% confidence based on the assumption that at least 50% of HCWs would have received at least one dose of vaccine. The assumption of 50% was used as this gives the largest sample size for descriptive studies, thus increasing statistical power. For the last two objectives where probability testing was employed, a sample size of 175 was calculated at 80% power and 95% confidence, based on the following assumptions from the literature: 75.5% of respondents have knowledge about the HB vaccine; 13 acceptance of vaccination in those with poor knowledge is 70.6%; 14 and acceptance of vaccination amongst those with good knowledge is 90.7%. 14 The sample size was increased to 200 to accommodate a lower response rate. A cross-sectional design with stratified random sampling was used to ensure proportional representation of nurses, doctors and laboratory workers. Data were collected from informed consenting HCWs during October 2010, using an anonymous self-administered structured questionnaire with closed-ended questions (see Supplementary File 1 for the list of questions). Data were collected on demographics (age, sex, years working as a HCW) and profession. Knowledge was measured (K) using 14 questions, with possible K scores ranging from 0 to 14. Attitude was measured (A) using a 5-point Likert scale and 9 statements, with possible A scores ranging from 218 to +18. K and A scores were collapsed into categorical data: poor K ( 5), moderate K (6 to10), and good K (11 to 14); negative A (218 to 27), neutral A (26 to 6), and positive A (7 to 18). HB vaccination questions included: ever receiving a HB vaccine; number of doses; testing after vaccination; and results of testing. Associations between receiving at least one dose of HB vaccine and good versus moderate/poor K; and positive versus neutral/negative A, were measured using the x 2 test for independence. For this, K and A data were further collapsed into dichotomous data, and the ORs, 95% CIs around the ORs, and x 2 p-values were calculated. Possible predictors (knowledge, attitude, age, gender, profession, and years worked as a HCW) of HB vaccination uptake were investigated using binary logistic regression analysis. Results Response rate and demographics A total of 117 questionnaires were returned out of 200 distributed giving an overall response rate of 58.5% (117/200), with a 53.4% (79/148) response from nurses; 69.2% (18/26) from doctors; and 76.9% (20/26) from laboratory staff. One of the questionnaires completed by a nurse had to be discarded because none of the questions on HB vaccination were answered, leaving a total of 116 questionnaires for analysis. This sample represents 17.8% (116/650) of the total population at risk of HBV infection at Princess Marina Hospital. The demographics of respondents are summarised in Table 1. K and A scores K scores ranged from 3 to 13 (mean: 7.96; SD¼2.31). Overall 17.2% (20/116) of HCWs had good knowledge, including 11.5% (9/78) of nurses, 20% (4/20) of laboratory staff, and 38.9% (7/18) of doctors. A scores ranged from 1 to 18 (mean: 12.10; SD¼3.04). Overall 97.4% (113/116) of HCWs had a positive attitude, including 94.4% (17/18) of doctors, 97.4% (76/78) of nurses, and 100% (20/20) of laboratory staff. Positive attitudes are exemplified by agreeing or strongly agreeing with statements such as vaccination against HBV should be made available to all HCWs for free, and disagreeing or strongly disagreeing with statements such as I do not trust vaccinations. HB vaccination uptake and post-vaccination testing Details of HB vaccination doses received by participants are provided in Table 2. Of HCWs who had received at least one dose of the HB vaccine, 61.0% (36/59) received the complete three dose series, including 70.6% (12/17) of doctors, 68.4% (13/19) of laboratory staff and 47.8% (11/23) of nurses. Of those who had received three or more doses, 22.2% (8/36) had been tested for anti-hbs, and of these, 100% (8/8) were protected (i.e., had anti-hb titres 10 miu/ml). Of the protected HCWs, 37.5% (3/8) were doctors, 37.5% (3/8) were laboratory workers, and 25% (2/8) were nurses. Of all participants, 6.9% (8/116) knew that they were protected against HB. Associations between K/A and HB vaccination uptake; and predictors of vaccination uptake As shown in Table 3, there were no statistically significant associations found between K or A and being vaccinated with at least one dose of HB vaccine. In addition, of those with good K and poor/ moderate K, 65.0% (13/20) and 47.9% (46/96) respectively were vaccinated with at least one dose of HB vaccine. Logistic regression analysis found that profession was a predictor of vaccination status, with being a laboratory worker (OR 61.0; 95% CI ; 2of6

3 International Health Table 1. Participant demographics stratified by profession Profession Doctor (n¼18) Nurse (n¼78) Lab staff (n¼20) Total (n¼116) n % n % n % n % Sex Male Female Age No answer Range Mean Years as healthcare worker, or more Table 2. Hepatitis B vaccination doses stratified by profession Doses Profession Doctor (n¼18) Nurse (n¼78) Lab staff (n¼20) Total (n¼116) n % n % n % n % None At least one One Two Three or more Don t know Table 3. Associations between knowledge/attitude and hepatitis B (HB) vaccination status Vaccinated a Unvaccinated (n¼59) (n¼57) OR (95% CI) p-value n % n % Knowledge Good ( ) b Poor/moderate Attitude Positive ( ) c Negative/neutral a Received at least one dose of HB vaccine. b x 2 p-value. c Fishers exact test used as an expected cell value was,5. 3of6

4 T. Machiya et al. p¼0.0006) or a doctor (OR 51.5; 95% CI ; p¼0.0029) statistically significantly predicting uptake of at least one dose of HB vaccine. Discussion At the time of conducting this study, the Botswana Ministry of Health had already developed national guidelines recommending HB vaccination of HCWs, which were subsequently published in 2011, 11 and currently the HB vaccine (rdna) B.P. (Serum Institute of India Ltd, Pune, India) is being used at the Princess Marina Hospital. The results of this study show that these guidelines are timely and very necessary, given that only 31% (36/116) of the HCWs at the Princess Marina Hospital have received the full three dose series of the HB vaccine, and only 6.9% (8/116) knew that they were protected against HB. There are currently no other data from Botswana on HB vaccination uptake in HCWs with which to compare these results. However, an early study conducted in South Africa, which borders on Botswana, found that only 21.2% (83/392) of HCWs working in a Gauteng hospital could remember ever being vaccinated, 15 while a more recent study from Gauteng found that 67.9% (491/723) of HCWs had received at least one dose of HB vaccine, but only 19.9% (94/472) were fully vaccinated. 16 Thus the findings that only half of the Princess Marina Hospital HCWs started the HB vaccination series, and that only 31% (36/116) of all the HCWs were fully vaccinated with all three doses, are not unusual for southern Africa. The low level of knowledge about HB prevention and control in HCWs employed at the Princess Marina Hospital, with only 17.2% (20/116) having good knowledge, is also not unusual for this region, with an unpublished South African study reporting that only 1.9% (3/161) of doctors and nurses working in the Ekurhuleni Metro of Gauteng had good knowledge about HB. 17 However, the majority of the Ekurhuleni HCWs were over the age of 40 years, whereas in this study the majority were younger than 40. In contrast, an unpublished South African study on final year student nurses, where the majority were younger than 30 years, found that 87.4% (271/310) had good knowledge. 18 Thus it seems that younger HCWs may be more knowledgeable about HB prevention and control. This suggests that either more information about HB has been disseminated to HCWs in recent times, or that the older HCWs do not remember what they learned during their training years. Interestingly, both these South African studies support the Princess Marina Hospital finding that knowledge is not a predictor of vaccination uptake. However, an OR of 2 indicates that HCWs with good knowledge were twice as likely to have received HB vaccination than those with moderate or low knowledge. As discussed below under limitations of the study, the finding that this was not statistically significant may have resulted from the sample size being underpowered. So while there is clearly a need for more education of in-service HCWs, larger studies are needed to show if this will result in a higher uptake of HB vaccination. The finding that almost all HCWs at Princess Marina Hospital had a positive attitude towards the prevention and control of HB is also supported by the South African study on employed HCWs, 17 where 74.5% (120/161) had a positive attitude. However, in contrast to the Princess Marina Hospital study, a positive attitude was found to predict vaccination uptake in the South African study. It is not clear why, despite having a positive attitude, most HCWs at the Princess Marina Hospital were not fully vaccinated. However, at the time of this study (October 2010), the Princess Marina Hospital did not seem to have had a HB vaccination policy. Thus it could be that these HCWs would have accepted HB vaccination if there had been a policy offering free HB vaccination to all HCWs at that time. A South African study conducted in 2010 supports the Princess Marina Hospital finding that being a doctor is a statistically significant predictor of vaccination uptake. In that study, doctors were 3.2 times more likely to be vaccinated with at least one dose of HB vaccine than nurses. 16 Apart from the South African study and this Princess Marina Hospital study, profession as a predictor of HB vaccination uptake has not been studied in southern Africa, and while there are HB vaccination in HCW studies from sub-saharan Africa that have stratified vaccination uptake by profession, to the best of our knowledge none have used logistic regression analysis to identify predictors of HB vaccination uptake. However, a study from Nigeria found that nurses were more likely to complete the HB vaccination schedule than doctors. 13 These contrasting results suggest that it may thus not be profession per se that predicts HB vaccination uptake, but rather the norms and standards that apply to different healthcare professions in different countries. This suggestion is also supported by the finding that knowledge was not a predictor of vaccination uptake, so although more doctors than nurses in this study had good knowledge about HB prevention and control, this factor did not translate directly into higher uptake of vaccination. Directly after this study had been concluded, on 30 November 2010, the Princess Marina Hospital Infection Control Committee approved a protocol for HB vaccination and post-exposure prophylaxis for HCWs at risk of occupational exposure to HBV. 19 This protocol is much more comprehensive than the national guidelines, but contradicts the recommendation that pre-vaccination screening should not be performed. It states that all consenting HCWs performing high-risk procedures and those who are newly employed, should be screened for HBsAg, anti-hbs, and antibodies against HB core antigen (anti-hbc; a serological marker for exposure to natural infection). Thereafter, anti-hbs- and HBsAg-negative HCWs should receive three doses of HB vaccine, at 0, 1, and 6 months, while HBsAg-positive and /or anti-hbc-positive HCWs should seek expert medical advice for further management, and HCWs with anti-hbs titres 10 miu/ml should not be vaccinated. Anti-HBs screening 4 6 weeks post-vaccination is recommended, with non-responders (anti-hbs,10 miu/ml) being offered a second three dose series and subsequent postvaccination screening. Routine anti-hbs screening and boosters are recommended for responders, while non-responders to the second series of HB vaccinations are to be counselled about the need for post-exposure prophylaxis against HBV after occupational exposures. 19 Pre-vaccination screening as suggested by the Princess Marina Hospital protocol may seem cost-effective, since early studies have found that 70 80% of Batswana adults have been exposed to HBV, 4,5 thus many HCWs may be naturally protected. However, given the following, this does not seem to be the case: first, the HB vaccine is relatively inexpensive (in South Africa, it costs about R5 [US$ 0.47] per dose in the public sector, resulting in a cost of about R15 [US$ 1.41] per HCW) compared to the serological tests (about R109 [US$ 10.15] for each antibody/antigen 4of6

5 International Health tested in the South African public sector using National Health Laboratory Service tariffs, resulting in a cost of about R327 [US$ 30.45] per HCW if the Princess Marina Hospital pre-screening protocol is followed). Second, it is likely that most protected adults (i.e., those who mounted an anti-hbs response to natural infection with a titre 10mIU/ml) would have been exposed as children 20 and thus their anti-hbs titres may have waned to levels,10 miu/ml, so it would be deemed necessary that they should receive the HB vaccination series in any case. Third, these protected HCWs with pre-vaccination anti-hbs levels,10 miu/ml would undoubtedly mount an anamnestic response to the HB vaccine. 21 Thus it seems more cost-effective to first vaccinate all HCWs, and then test them afterwards, but only for anti-hbs, resulting in a total cost of about R124 (US$ 11.53) per HCW. Then only those who are non-responders need to be tested for HBsAg and anti-hbc, which would result in considerable cost savings. Finally, the issue of routine follow-up of known responders for anti-hbs testing and boosters may be challenged by some authors. It has been shown that once an individual has mounted a sufficient immune response to the HB vaccine (i.e. anti-hbs 10mIU/ml), there is no need for booster doses even when the anti-hbs titre drops below the protective level, since upon re-exposure they will mount an anamnestic response and avert infection. 21 However, it is also known that HIV-positive individuals lose their anti-hbs more quickly than HIV-negatives, and also often do not mount a good and sustained immune response to either natural HBV exposure, or exposure to the HB vaccine. 20 Given that 12% of 204 Princess Marina Hospital HCWs who volunteered for HIV testing between 2006 and 2007 were HIV-positive, 12 and that this may be an underestimation given the reluctance of HCWs to be tested for HIV, further studies should find out whether it is necessary to offer follow-up anti-hbs screening and boosters to Batswana HCWs. Study limitations The statistical power for the last two objectives of this study was weakened to some extent by the relatively poor response rate, especially amongst nurses, which also may have introduced volunteer bias, with non-respondents perhaps having lower knowledge about HB or lower HB vaccination uptake than respondents. However, the sample constitutes 17.8% of the total number of at-risk HCWs at Princess Marina Hospital, and stratified random sampling was used, thus this sample is representative. Globally, response rates from HCWs can be as low as 15%, and those with high response rates often employ follow-up of non-responders or incentives for participation. 22 Since responses were anonymous in this study, follow-up was not possible, and no incentives for participation were offered. There are no similar studies from Botswana for comparison, but some South African studies on HBV in HCWs have found response rates even lower than the 58.5% reported here. For example, a study on occupational exposures to HBV amongst doctors reported a response rate of 51.7%, 23 while the previously mentioned study from Ekurhuleni Metro in Gauteng reported a 42.2% response from nurses working in public hospitals, while the response from doctors working in private practice was only 21.8%. 17 The low response rate from nurses in this study on Princess Marina Hospital may be related to their workload, since it has been reported that this hospital operates at twice its capacity with a 47% nursing shortage. 24 More importantly, in the absence of published data from southern Africa at the time of data collection, the first assumption (on knowledge) for the sample size calculation was based on a study from Nigeria, 13 while the second and third assumptions (on uptake of vaccination in those with good and poor knowledge) were based on a study from Pakistan. 14 This led to a substantially smaller sample size than was needed for Botswana, given the findings of the current study, which needed a sample size of 512 for adequate statistical power for the last two objectives (associations with, and predictors of vaccination uptake). Thus the results for the last two objectives should be treated with caution, as it is possible that larger studies may find statistically significant associations where none have been identified here. On the other hand, the statistically significant results reported here should not be entirely disregarded. Although the confidence intervals for the ORs were wide they did not contain 1, and it is possible that larger studies will result in statistically significant findings with narrower confidence intervals. The intention of reporting these results here despite the lack of statistical power is to highlight that these issues need to be further investigated using larger sample sizes. Finally, information bias may have been a problem since participants had to recall details of vaccination doses they had received in the past. Conclusions This study is the first publication on HB vaccination of Batswana HCWs. It shows that HB vaccination uptake is suboptimal, especially amongst nurses. Given the high risk of occupational exposure to HBV faced by Batswana HCWs, the HB vaccination guidelines issued by the Botswana Ministry of Health in 2011 are welcomed, as is the policy developed by the Princess Marina Hospital Infection Control Committee at the end of In light of these developments, data on HB vaccination uptake and HBV serology in HCWs should become available, and this will allow for evidence-based decision making on the most cost effective screening and vaccination programme. It has been suggested that a two dose schedule would improve HB vaccination compliance, and there is evidence that a two dose schedule of some types of HB vaccine may provide adequate protection. 25 However, only 7.8% of the HCWs in this study had received two doses, thus using a vaccine that may be licensed in the future for a two dose schedule may not improve protection in this population. Finally, Botswana institutions training student HCWs clearly need to place more emphasis on HB prevention and control education, and should try to ensure that student HCWs are fully vaccinated before being exposed to patients. In addition to education, an investigation into the professional norms and standards that apply to the different HCW professions in Botswana may reveal what can be done to improve HB vaccination uptake amongst nurses. Authors contributions: RJB and TM conceived the study; TM, RJB, GF, ADS, MvS and MJM contributed to protocol development; TM conducted the research under the guidance of RJB; TM, RJB and LF analysed the data; all authors contributed to writing the manuscript. All authors have read and approved the final version of the manuscript. RJB is the guarantor. 5of6

6 T. Machiya et al. Acknowledgements: The authors thank the management of Princess Marina Hospital for allowing this study to be conducted, and also thank the HCWs of Princess Marina Hospital who participated in this study. Funding: Data collection was self-funded by TM; dissemination of results was funded by the Flemish Interuniversity Council Institutional University Cooperation between the University of Antwerp and Limpopo University. Competing interests: None declared. Ethical approval: This study was approved by the University of Limpopo s Medunsa Research Ethics Committee (MREC/H/11/2010:PG), and further ethics clearance was obtained from all relevant Botswana authorities. References 1 Kandala NB, Campbell EK, Rakgoasi SD et al. The geography of HIV/ AIDS prevalence rates in Botswana. HIV AIDS (Auckl) 2012;4: Nair PS. Age structural transition in Botswana in the context of HIV/ AIDS. 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