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Health care workers in Pearl River Delta Area of China are not vaccinated adequately against hepatitis B: a retrospective cohort study

BMC Infectious Diseases201515:542

https://doi.org/10.1186/s12879-015-1278-0

Received: 7 October 2014

Accepted: 11 November 2015

Published: 22 November 2015

Abstract

Backgrounds

Health-care workers’ (HCWs) exposure to bodily fluids puts them at risk of hepatitis B virus HBV infection. This study investigated HBV vaccination practices and outcomes in HCWs and assessed postvaccination seroprotection across HCWs in different departments.

Methods

A survey of HCWs in a Chinese public general hospital was carried out with a retrospective cohort of 1420 hospital HCWs (458 males and 962 females). HBV vaccination status (10-μg/dose used) was investigated in the cohort from vaccination records from the period of 1988 to 2008. Blood samples were collected and tested for hepatitis B surface antigen (HBsAg) and HBV antibodies (anti-HBs).

Results

The overall vaccination (complete course) and HBsAg carrier rates among HCWs were 40.42 % (574/1420) and 6.13 % (87/1420), respectively. Vaccination rates differed by department, with HCWs in internal medicine (39.5 %) and emergency (42.0 %) departments having particularly low rates. The natural infection rate was 7.53 % (107/1420) among HCWs. HCWs in the department of infectious diseases (vaccination rate, 57.8 %) had the highest rate of antibody produced by natural infection (88.2 %).

Conclusion

The vaccination rate was a disappointingly low among HCWs in Pearl River Delta Area of China. HCWs working in infectious diseases departments and technicians were at particularly likely to have been infected with HBV. A concerted effort is needed to bring vaccination rates up among Chinese HCWs in Pearl River Delta Area of southern China.

Keywords

  • Vaccination
  • Hepatitis B
  • Hospital
  • Immunity
  • Occupational risk

Background

Hepatitis B virus (HBV) infection is a major cause of acute and chronic liver disease worldwide [1]—including hepatitis, cirrhosis, and hepatocellular carcinoma—and is one of the ten most common causes of death worldwide [2]. Approximately 30 % of the world’s population have serologic evidence of prior HBV infection [3]. An estimated 400 million people are infected with HBV, including 350 million chronic cases, with at least 1 million dying each year from chronic liver disease [4]. Chronic HBV infection is endemic in Asia and Africa, with more than 75 % of the world’s chronic HBsAg carriers being of Asian or African origin [5, 6].

Vaccination of health care workers (HCWs) is particularly important given their risk of exposure to blood-borne viral infections, particularly HBV, hepatitis C virus (HCV), and HIV, and vaccine-preventable diseases [79]. These risks are further heightened in developing countries in endemic regions such as Africa and Asia, including China [10]. Although effective anti-HBV vaccines have been available for over 10 years, many HCWs remain non-immunized against HBV [11]. Indeed HCWs, including those at particular risk of HBV infection, have been reported to have inadequate participation in vaccination programs [12, 13]. Although HBV vaccination rates are not satisfactory among HCWs in many countries, there was a complete HBV vaccination coverage among Polish surgical nurses [14].

However, currently, little is known about Chinese HCWs knowledge of HBV risk. Therefore, the aim of the present study was to assess HCWs’ HBV infection, vaccination, and seroprotection rates. The specific objectives of this study were: (1) to determine the vaccination and anti-HBV antibody statuses of HCWs in the Liver Disease Center of Pearl River Delta Area of China in a public teaching general hospital; (2) to compare vaccination seroprotection across hospital departments; and (3) to assess the HBV infection rate among Pearl River Delta Area Chinese HCWs.

Methods

Study design and ethics statement

The present study consisted of the retrospective analysis of medical records (1988–2008), administration of a questionnaire, and analysis of immunological blood tests. The protocol was approved by the local medical ethics committee of Third Affiliated Hospital, Sun Yat-Sen University The study was performed according to the World Medical Association Declaration of Helsinki, and. Written informed consent was obtained from all individuals included in this study. Data were entered in duplicate into a computerized database and were analyzed anonymously.

Study population

1420 HCWs (458 males and 962 females) of our retrospective study were assembled by recruiting HCWs from the health examination center database (est. 1988). And 1420HCWs were recruited from the Liver Disease Center in Pearl River Delta Area of China (820HCWs), the People’s Hospital of Tianhe District, GuangZhou (390HCWs) and the TianHe Maternal and Child Health Hospital (210HCWs), respectively. All individuals whose data are in the database have provided written informed consent for future research and analysis of their data; nevertheless, all included subjects also provided written informed consent to participate in this study as well. All of the recruited HCWs had chosen previously to have their routine medical examinations done at the Liver Disease Center of Pearl River Delta Area of China in a public teaching general hospital; therefore the population is most closely representative of Pearl River Delta Area of China in particular. Their data were analyzed anonymously. Vaccination status was confirmed by routine medical examination reports.

The exclusion criteria were: detailed vaccination record lacking, declining to complete the survey questionnaire, and declining to provide written informed consent (see Fig. 1). The final cohort consisted of 1420HCWs had a mean age of 37.72 ± 13.37 years (only 1182 HCWs ages range, 24–51 years). By age band, there were 146 subjects ≤25 years old, 788 that were 26–39 years old, 394 that were 40–59 years old, and 92 that were ≥60 years old.
Figure 1
Fig. 1

A flow diagram of study participants

Data collection

Questionnaire and medical records analysis

HCWs were asked to complete a questionnaire that asked about their vaccination history, department of employment, job category, and demographics. Prior completion of an HBV vaccination course was determined conclusively by examining the participants’ medical records.

Medical examination

During their 2008 routine medical examination, all HCWs in this study were subjected to testing for HBV serology, including tests for hepatitis B surface antigen (HBsAg), hepatitis surface antigen antibodies (anti-HBs), and antibody to hepatitis core antigen antibody (anti-HBc) tests. The presence of HBsAg was interpreted as indicating an active HBV infection. The presence of anti-HBs (with anti-HBc positivity) and no prior vaccination was interpreted as indicating a history of HBV infection. The presence of anti-HBs (with anti-HBc positivity) and prior vaccination was interpreted as indicating history of HBV infection in vaccinated successfully individuals. The presence of anti-HBs, but not anti-HBc, and a history of vaccination was interpreted as indicating an effective vaccination and never having been infected with HBV. The presence of anti-HBs (without anti-HBc positivity) was interpreted as indicating history of vaccinated successfully individuals.

The presence of HBsAg, anti-HBs, and anti-HBc was determined by enzyme-linked immunosorbent assay (ELISA) with kits from Shanghai Industrial Division Biotechnology Limited (China). The assays were conducted in strict accordance with the kit manufacturer’s instructions. The simple, rapid ELISA for HBsAg used is the gold-standard method for the detection of HBsAg with high sensitivity and specificity (≥99.0 %) [15]. The anti-HB titer cutoff for positive response (development of protective titers) was ≥10 mIU/mL. Data from earlier years that were originally reported with other units were converted to mIU/mL. All ELISAs were carried out in duplicate.

Data analysis

Normality of datasets was determined using the Student’s t-Test. For normally distributed data, means and standard deviations (SDs) were calculated and frequency distributions across category bins were determined. For non-normally distributed data and ranges were calculated. We used the chi-square test to detect general associations. All tests were two-sided and p < .05 being regarded as significant. Data were analyzed using SAS statistics software.

Results

HBV infection status

Of the 1420 participants whose data were examined, 87 (6.13 %) were found to be positive for HBsAg and thus identified as being currently infected with HBV. As shown in Table 1, non-vaccinated HCWs were more likely to be HBsAg-positive (indicating an active infection), than were vaccinated HCWs. Table 2 revealed that of the 1420 participants, 7.53 % (107/182) had gained immunity through natural infection with HBV.
Table 1

Status of HBV vaccination in HCWs in Pearl River Delta Area of China (N = 1420)

Factor

Number

HBV vaccination status, N (%)

χ 2

P

Vaccinated

Not vaccinated

Sex

Male

458

140 (30.57 %)

33 (7.20 %)

0.4164

.5188

Female

962

278 (28.90 %)

73 (7.59 %)

  

Age band

<25 years

146

77 (52.7 %)

14 (7.1 %)

36.546

5.741E-08

25 ~ 39 years

788

403 (51.1 %)

106 (13.5 %)

  

40 ~ 59 years

394

92 (23.4 %)

62 (15.7 %)

  

≥60 years

92

2 (2.2 %)

0 (0.0 %)

  

HBsAg

Detected

87

8 (1.33 %)

79 (9.65 %)

71.583

2.659E-17

Not detected

1333

593 (98.66 %)

138 (90.35 %)

  

Anti-HBs level

<10 mIU/mL

644

285 (44.3 %)

75 (11.7 %)

11.772

0.00278

1–10 mIU/mL

326

133 (40.8 %)

31 (9.5 %)

  

Anti-HBc-total

Not detected

450

129 (28.7 %)

62 (13.8 %)

  

Positive

262

42 (6.99 %)

220 (26.86 %)

5.783

3.871E-5

Negative

1158

559 (93.01 %)

599 (73.14 %)

  

Department

Infectious diseases

106

61 (57.8 %)

17 (15.6 %)

20.660

0.0081

General medicine

367

145 (39.5 %)

71 (19.4 %)

  

Surgery

305

186 (60.9 %)

40 (13.1 %)

  

Ob/gyn

88

56 (63.6 %)

20 (22.7 %)

  

Pediatrics

56

33 (58.9 %)

8 (14.3 %)

  

Dentistry

44

22 (50.0 %)

9 (20.5 %)

  

Emergency

88

37 (42.0 %)

6 (6.8 %)

  

Nephrology

23

13 (56.5 %)

2 (8.7 %)

  

Other

343

48 (14.0 %)

9 (2.6 %)

  

Profession

Medical doctor

405

194 (47.9 %)

58 (14.3 %)

3.4387

0.4873

Dentist

18

14 (77.8 %)

4 (22.2 %)

  

Nurse

542

311 (57.4 %)

98 (18.1 %)

  

Technician

123

42 (34.1 %)

17 (13.8 %)

  

Other

332

51 (15.4 %)

9 (2.7 %)

  
Table 2

Protective antibody status in relation to exposure route through natural infection versus vaccination by hospital department of employment and profession

Factor

Number

Portion of group with detectable protective antibodies, ratio (%)

χ 2

P

Vaccinated

Infected naturally

N = 601

N = 107

Department

Infectious diseases

106

42/61 (68.8 %)

15/17 (88.2 %)

1.743656

.0406

General medicine

367

80/145 (55.2 %)

44/71 (62.0 %)

0.927921

.1767

Surgery

305

104/186 (55.9 %)

25/40 (62.5 %)

0.695803

.2433

Ob/gyn

88

34/56 (60.7 %)

5/20 (25.0 %)

−2.74299

.0030

Pediatrics

56

24/33 (72.7 %)

3/8 (37.5 %)

−1.82574

.0339

Dentistry

44

12/22 (54.5 %)

5/9 (55.6 %)

0.051297

.4795

Emergency

88

23/37 (62.2 %)

3/6 (50.0 %)

−0.56521

.2860

Nephrology

23

4/13 (30.8 %)

0/2 (0.0 %)

−1.09545

.1367

Other

343

33/48 (68.8 %)

7/9 (77.7 %)

0.322184

.3737

Profession

Doctor

405

151 (77.8 %)

27 (46.6 %)

−4.68522

2E-6

Dentist

18

8 (57.1 %)

1 (25.0 %)

−1.13389

.1284

Nurse

542

192 (61.7 %)

60 (61.2 %)

−0.09085

.4638

Technician

123

17 (40.5 %)

12 (70.6 %)

2.095346

.0181

Other

332

31 (60.8 %)

7 (77.78 %)

0.334633

.3690

 

vaccination coverage/Infected naturally rates

1420

42.32 %

7.53 %

−6.35622

2E-7

Status of hepatitis B vaccination

The overall rate of vaccination (10-μg dose HBV vaccine) among HCWs was 40.42 % (574/1420). Vaccination rates were similar between males and females (Table 1). Likelihood of vaccination differed across hospital departments (Table 1). HCWs in the obstetrics and gynecology (ob/gyn) and surgery departments had the highest rates of HBV vaccination (≥60 %), whereas HCWs in the internal medicine and emergency departments had the lowest vaccination rates (≤42 %). HCWs in younger age bands, particularly the ≤25 year-old group, were more likely to have been vaccinated than HCWs than older age bands (Table 1).

Immunity from vaccination versus natural infection

The vaccinated group was confirmed to more likely to be anti-HBs positive (i.e. protected) than the non-vaccinated group (Table 1). Of the 614 HCWs whose survey results and medical histories indicated a history of HBV vaccination, 485 (79.0 %) were found to be anti-HBs positive. The remaining 129 HCWs (21.0 %) had no protective anti-HBs despite their history of vaccination. Conversely, of the 187 HCWs who had not been vaccinated, 76 (40.6 %) were positive for anti-HBs, indicating prior exposure to the virus.

Overall, more HCWs in the present study gained seroprotection against HBV from prior infection than from vaccination. The presence of seroprotection being conferred by vaccination versus natural HBV exposure differed across departments and professions. As shown in Table 2, HCWs working in infectious diseases departments were the most likely to have gained immunity through prior exposure, as opposed to vaccination. Meanwhile, medical doctors were more likely than technicans and nurses to have gained protection through vaccination (Table 2).

Discussion

The present study demonstrated that HCWs in southern China, overall, had a disappointingly low rate of HBV vaccination (near 40 %). Furthermore, approximately one-fifth of vaccinated HCWs lacked serological evidence of protection. Vaccination rates differed in relation to HCWs’ department of employment and profession.

HBV can be transmitted by blood transfusion, injection [16], operation, dental treatment [12], needle stick injuries, and mother-to-child vertical transmission. Estimates of the rate of HBV infection of HCWs following a one-time needle prick with an HBV-exposed needle range widely from 6 to 30 % [3]. HCWs work long hours in high-demand environments and are exposed frequently to patients’ bodily fluids, including blood, secretions, and excretions. The potential risk of acquiring blood-borne viruses through needle stick injuries has led several authors to examine the prevention of such incidents [13, 17]. Many reports have indicated that the main and, probably, only effective mechanism of preventing HBV infection among HCWs is an effective vaccine, which has been in use for about two decades [18, 19]. In 1991, the World Health Organization recommended that all countries should implement an anti-HBV vaccine in their national vaccination program by 1997 [20, 21]. Given HCWs elevated risk of HBV infection, and the related risks of infected HCWs transmitting the virus to uninfected patients, the strength of occupational protection of HCWs by vaccination should be increased aggressively [22].

The HBsAg positive rate found for HCWs in Pearl River Delta Area of southern China in this study was lower than expected [23]. However HCWs working in infectious diseases departments and technicians were at particularly likely to have been infected with HBV. Some portion of people who receive HBV vaccine inoculation remain at risk of HBV infection. Prior work suggests that HBV vaccination efficacy is better in younger recipients [24]. Eight vaccinated HCWs in the present study were HBsAg-positive, indicating that they were harboring an active HBV infection despite having been inoculated; presumably, they did not produce sufficient (or any) protective antibodies in response to the vaccine. Hence, serum anti-HBs levels should be assayed postvaccination to confirm whether protection has been conferred. The presence of protective antibodies in some non-vaccinated HCWs was presumably due to prior natural exposure to the virus. Nevertheless, HCWs in the vaccinated group were less likely to have a current HBV infection (indicated by HBsAg positivity) than HCWs in the non-vaccinated group, indicating that HBV vaccination had been clinically meaningful, though it was not 100 % effective.

Interestingly, the rate of workers having serologically evident protection by natural infection versus vaccination was not uniform across departments. HCWs in the infectious diseases department had the highest rate of antibody produced by natural infection; indeed more HCWs working in infectious diseases departments were infected with HBV naturally than were vaccinated. It is expected that HCWs who work in infectious diseases departments, and thus work directly with hepatitis-infected patients and samples, have a high risk of HBV exposure. Hence, the low rates of vaccination among these HCWs indicate strongly that there is a need for greater awareness of transmission risk and for promotion of HCW vaccination.

The relatively higher rate of vaccination among ob/gyn HCWs observed in this study could be related to these HCWs having gained greater awareness of the HBV vaccine as a consequence of their involvement with infant immunization plans. The four HCWs working in hemodialysis departments (encompassed in “Other” in Table 2), an area of particularly high infection risk [23], were noteworthy for characteristically obtaining anti-HBs by way of vaccination, indicating that they have a particularly high awareness of their occupational need for protection. It is noteworthy that immunity source also differed in relation to profession. Technicians with anti-HBs antibodies obtained immunity mostly through natural infection, whereas medical doctors with anti-HBs antibodies obtained immunity more often through vaccination. The low vaccination protection rate of technicians is particularly concerning given their frequent exposure to patients’ bodily fluids [25].

It is our view that HCWs who have a reasonable expectation of being exposed to blood on the job should be offered the HBV vaccine as a matter of course. Furthermore, HCWs should be informed that vaccination is not always effective and serological testing should be performed to confirm vaccine effectiveness. HCWs should be counseled regarding what steps they should take to protect their health in cases of vaccine non-responsiveness.

This study has the limitation of being largely limited to enrollment of HCWs in Pearl River Delta Area of southern China. So the HCWs enrolled in the present study can represent Local area of the HCWs in the Pearl River Delta Area of China to a certain extent. This geographical limitation limits the generalizability of these findings. Additional studies involving HCWs in other regions are needed to determine whether the patterns of data observed here are common southern China, throughout China and Asia at large, and larger retrospective studies are needed to confirm the present results. There ere also the limitation of the publication delay due to the delay in preparing the manuscript and the submission.

Conclusion

HCWs are at an elevated risk of HBV infection due to their exposure to blood and other bodily fluids in the course of their work. Vaccination rates are disappointingly low among HCWs in southern China, with large portions of HCWs, especially HCWs working in infectious diseases departments, showing serological evidence of a natural infection history. HCWs should not only be more broadly encouraged to be vaccinated, they should be made aware that a single innoculation may not confer protection. When HCWs contract an HBV infection, they place coworkers and patients at risk of infection as well. Hence, HCWs should be vaccinated not only early, but also regularly [26]. HCWs with undetectable or low anti-HB levels in particular should receive booster vaccinations.

Abbreviations

HCW: 

Health-care workers

HBV: 

Hepatitis B viruses

HBsAg: 

Hepatitis B surface antigen

anti-HBs: 

Antibody to hepatitis surface antigen

anti-HBc: 

Antibody to hepatitis core antigen

ELISA: 

Enzyme-linked immunosorbent assay

Declarations

Acknowledgements

This study was supported by the Science and technology project of Guangdong Province (No. 2014A020212059), the Natural Science Fund of Guangdong province (No. 2015A030313172). and The Guangzhou science and technology project (2016) (Project host:Yu-Bao Zheng) entitled: "receptor interacting protein -3 (RIP3) in the early warning role of aggravation of  acute-on-chronic hepatitis B liver failure". the National Grand Program on Key Infectious Diseases (AIDS and viral hepatitis), China (No.2012ZX10002007). The authors thank all participants of this study and are grateful to staff members of the Department of Infectious Diseases at the third hospital of Sun Yat-sen University. This manuscript was edited by a professional native English editor at Medjaden Bioscience Limited.

Funding

This study was supported by the Science and technology project of Guangdong Province (No. 2014A020212059), the Natural Science Fund of Guangdong province (No. 2015A030313172). The Guangzhou science and technology project (2016) (Project host:Yu-Bao Zheng) entitled: "receptor interacting protein -3 (RIP3) in the early warning role of aggravation of  acute-on-chronic hepatitis B liver failure". and the National Grand Program on Key Infectious Diseases (AIDS and viral hepatitis), China (No.2012ZX10002007). Funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Infectious Diseases, The Third Affiliated Hospital, Sun Yat-sen University, Guangzhou, China
(2)
Key Laboratory of Tropical Disease Control (Sun Yat-Sen University), Ministry of Education, Guangzhou City, P.R. China

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Copyright

© Zheng et al. 2015

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