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. 2023 Apr 27;19(1):2206774. doi: 10.1080/21645515.2023.2206774

Prevalence of antibody to hepatitis B surface antigen among qualified blood donors in Nanjing, China

Yi-Hua Zhou a,*, Jinhong Yu b,*, Lu Zhou a, Biyun Xu c, Yudong Dai d, Haining Wang d, Wensan Zhou a,✉, Hong Zhao e,✉
PMCID: PMC10142315  PMID: 37103976

ABSTRACT

Universal infant hepatitis B vaccination has been implemented more than three decades. This study aimed to determine the prevalence of antibodies to hepatitis B surface antigen (anti-HBs) and to hepatitis B core antigen (anti-HBc) in qualified blood donors in Nanjing, China. Plasmas of 815 qualified blood donors, collected from February through May 2019, were measured for anti-HBs and anti-HBc by enzyme-linked immunosorbent assay. There were 449 (55.1%) male and 366 (44.9%) female blood donors, with a median age of 28.9 years (18–60). The seroprevalence of anti-HBs was 58.8%, with no significant difference in different genders and different age groups. The overall prevalence of anti-HBc was 7.0%, with an increasing trend with age, from 0% in 18–20 years old group to 17.9% in 51–60 years old group (χ2 = 46.7965, p < .0001). The prevalence of anti-HBc in donors born after the implementation of universal hepatitis B vaccination was significantly lower than that in donors born before (1.0% vs 15.5%; χ2 = 63.6033, p < .0001). Our data suggest that more than half of the blood donors in Nanjing are anti-HBs positive. Since a blood recipient usually receives more than one unit of red blood cells or plasma, passively acquired anti-HBs in blood recipients may neutralize hepatitis B virus potentially presented in blood donors with occult hepatitis B infection. In addition, the presence of anti-HBs and/or anti-HBc in blood donors may cause unique hepatitis B serological profile in blood recipients.

KEYWORDS: Qualified blood donors, prevalence, antibody to hepatitis B surface antigen, antibody to hepatitis B core antigen

Introduction

Hepatitis B virus (HBV) infection, usually defined by the presence of hepatitis B surface antigen (HBsAg) in serum or plasma, is a serious global health issue. Blood transfusion is one of the causes of HBV infection. Despite screening for HBsAg is performed as a mandatory routine practice of blood donations, HBV infection caused by blood transfusion still presents as a threat to blood safety due to occult HBV infection (OBI)1–3 or the presence of HBV without detectable HBsAg. It has been reported that the prevalence of OBI in blood donors was 0.06%–1.4%,4–8 indicating the potential HBV transmission to transfusion recipients. However, the incidence of HBV infection caused by blood transfusion was 0–0.02%,9–12 much lower than the prevalence of OBI in blood donors. These studies suggest that transfusion of blood collected from donors with OBI does not necessarily cause HBV infection. The reason for this phenomenon is unknown.

The World Health Organization recommended in 1991 that all countries implement universal hepatitis B vaccination in newborn infants to prevent and control HBV infection.13 China has integrated hepatitis B vaccination into the Expanded Program on Immunization (EPI) since 1992.14,15 As many blood donors are young adults who were born after the implementation of universal hepatitis B vaccination, it is likely that a considerable proportion of blood donors is positive for antibodies directed against HBsAg (anti-HBs). In addition, since a blood recipient usually receives more than one unit of red blood cells or plasma or even more than five units,16–19 the recipients may receive anti-HBs positive blood products, in which the anti-HBs can neutralize the virus potentially existed in blood collected from donors with OBI. However, anti-HBs positive rate in blood donors has been neglected and less studied. We searched PubMed with terms “blood donor” and “anti-HBs” for articles published in any language from inception to December 31, 2018, just before the present study was conceived, and identified 479 articles only. Further search in PubMed using the same terms from inception to April 4, 2023, identified 515 articles, with only 36 articles more since January 1, 2019. Moreover, most articles did not show the prevalence of anti-HBs, and a few articles just mentioned the anti-HBs prevalence in blood donors,8,20 but did not interpret the significance of anti-HBs in blood donors. In the present study, we investigated the positive rate of anti-HBs in qualified blood donors in Nanjing, China.

Subjects and methods

Blood donors

This was a cross-sectional survey to mainly estimate the prevalence of anti-HBs in qualified blood donors in Nanjing. Based on the blood donation regulations set up by the National Health Commission of the People’s Republic of China, healthy adults who have normal alanine aminotransferase and are negative for HBsAg, antibodies against hepatitis C virus, human immunodeficiency virus, and Treponema pallidum are qualified for blood donation. Previously, we revealed that the positive rate of anti-HBs in pregnant women between 2002 and 2004, aged 25.1 ± 3.2 year, was 36.8% in Jiangsu province.21 In addition, the reported positive rate of anti-HBs in subgroups of blood donors in China ranged from 27.1% to 55.6%.20,22 Therefore, we assumed that at least 35% of the qualified blood donors in Nanjing should be anti-HBs positive. Based on this positive rate, the participant size in this survey was 714, with a confidence of 95% and a relative error of 3.5%. We finally collected blood samples from 815 qualified volunteer donors at Nanjing Red Cross Blood Center from February through May 2019. The blood samples were not directly collected from the donors but collected from the tubing segments connected to the bags of the donors’ blood with fresh blades to avoid cross-contamination during sampling. They were 449 males and 366 females. The median age was 28.9 years (range, 18–60). Samples were stored at −30°C.

This study was approved by the Ethics Committees of Nanjing Drum Tower Hospital and Nanjing Second Hospital. Waiver of informed consent was approved by the Ethics Committee.

Detection of anti-HBs and antibody to hepatitis B core antigen

Commercially available qualitative enzyme linked immunosorbent assay (ELISA) kits (Kehua Biotech, Shanghai, China) were used to detect anti-HBs and antibody to hepatitis B core antigen (anti-HBc) in the plasma samples based on the manufacturer’s instructions. The ELISA for anti-HBs was based on double-antigen sandwich assay. Briefly, 50 μl plasma was added to each well of the HBsAg-coated microplate, followed by adding 50 μl horseradish peroxidase (HRP) conjugated HBsAg. After incubation at 37°C for 30 min, the plate was washed 5 times with phosphate buffered saline-tween-20 (PBS-T). Then, 100 μl tetramethylbenzidine solution was added. After incubation at room temperature for 10 min, the color development was stopped by adding 50 μl 2 M H2SO4. The optical density at 450 nm (OD450) was determined on a microplate reader (Thermo Scientific, Multiskan FC). Results for anti-HBs were shown as follows: cutoff value (COV) = mean OD450 of three negative controls (NC) × 2.1; when mean NC OD450 ≤ 0.05, it was calculated as 0.05; when OD of the sample ≥ COV, it was determined as positive.

The ELISA for testing anti-HBc was based on a competitive assay. Plasma was 25-fold diluted. Specifically, 48 μl PBS-T was added to each well of the hepatitis B core antigen coated microplate, followed by adding 2 μl plasma and 50 μl HRP conjugated anti-HBc to each well. For results, COV = mean value of three NC × 0.5; when OD of the sample < COV, it was determined as positive.

Statistical analysis

Comparison between groups was performed by chi-square or Cochran-Mantel-Haenszel tests. The trend analysis of classification variables was performed by Cochran-Armitage trend test. A p value less than .05 was considered statistically significant. All analyses were conducted using a statistical analysis system software, Version 9.4 (SAS Institute Inc. Cary, USA).

Results

Prevalence of anti-HBs and anti-HBc in qualified blood donors

The present study included 815 plasma samples from 815 blood donors, with 449 (55.1%) males. Overall, the positive rate of anti-HBs was 58.8% (479/815), with 431 (52.9%) positive for anti-HBs alone and 48 (5.9%) positive for both anti-HBs and anti-HBc. In addition, 9 (1.1%) donors showed positive for anti-HBc alone. Thus, the total positive rate of anti-HBc in these donors was 7.0% (57/815).

Positive rates of anti-HBs and anti-HBc in different age groups

As shown in Table 1, anti-HBs positive rate ranged from 53.6% to 62.9% in various age groups. The differences in anti-HBs positivity rates in different age groups had no statistical significance (χ2 = 0.9353, p = .3335). The anti-HBc prevalence tended to be increasing with age, from 0% in 18–20 years old group to 17.9% in 51–60 age group (χ2 = 46.7965, p < .0001). As hepatitis B vaccination has been integrated into EPI in China since 1992, we compared the positive rates of anti-HBs and anti-HBc between donors born before and on and after January 1, 1992. Table 2 shows that the anti-HBc positive rate in donors born before January 1, 1992, was significantly higher than that in donors born on and after January 1, 1992 (15.5% vs 1.0%; χ2 = 63.6033, p < .0001), and the donors born before January 1, 1992, had significantly higher rate of positive anti-HBs and anti-HBc than the donors born on and after January 1, 1992 (13.1% vs 0.8%; χ2 = 53.8626, p < .0001).

Table 1.

Positive rates of anti-HBs and anti-HBc in donors at different ages.

Age (years) No of donors No of anti-HBs+* (%) No of anti-HBc+§ (%)
18–20 181 97 (53.6) 0 (0)
21–30 362 221 (61.0) 13 (3.6)
31–40 128 72 (56.3) 21 (16.4)
41–50 105 66 (62.9) 16 (15.2)
51–60 39 23 (59.0) 7 (17.9)
Total 815 479 (58.8) 57 (7.0)
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The trend analysis in the prevalence of anti-HBs and anti-HBc in different age groups were determined by Cochran-Armitage trend test, respectively.

*χ2 = 0.9353, p = .3335; §χ2 = 46.7965, p < .0001.

Table 2.

Prevalence of anti-HBs and anti-HBc among blood donors born before January 1992 and born in and after January 1992.

Antibody status No of donors born before January1992, n = 335 No of donors born on and after January 1992, n = 480 Chi-square (χ2) test p
Anti-HBs+ (%) 193 (57.6) 286 (59.6) 0.3165 .5737
Anti-HBc+ (%) 52 (15.5) 5 (1.0) 63.6033 < .0001
Anti-HBs+ and anti-HBc+ (%) 44 (13.1) 4 (0.8) 53.8626 < .0001
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Positive rates of anti-HBs and anti-HBc in males and females

Table 3 shows that the anti-HBs positivity rate in male and female donors was 57.5% and 60.4%, respectively (χ2 = 0.7103, p = .3994). The anti-HBs positive rate among each age group had no statistically significant differences between male and female donors (χ2 = 0.6199, p = .4311). Similarly, the prevalence of anti-HBc among male and female donors was 7.1% and 6.8%, respectively (χ2 = 0.0272, p = .8689). And the anti-HBc positivity rate among each age group was not significantly different between male and female donors (χ2 = 0.1657, p = .6840).

Table 3.

Prevalence of anti-HBs and anti-HBc among male and female blood donors at different ages.

Age (years) Male
 Female
No of donors No of anti-HBs+* (%) No of anti-HBc+§ (%) No of donors No of anti-HBs+* (%) No of anti-HBc+§ (%)
18–20 101 52 (51.5) 0 (0.0) 80 45 (56.3) 0 (0.0)
21–30 206 122 (59.2) 10 (4.9) 156 99 (63.5) 3 (1.9)
31–40 70 40 (57.1) 12 (17.1) 58 32 (55.2) 9 (15.5)
41–50 45 27 (60.0) 5 (11.1) 60 39 (65.0) 11 (18.3)
51–60 27 17 (63.0) 5 (18.5) 12 6 (50.0) 2 (16.7)
Total 449 258 (57.5)† 32 (7.1) 366 221 (60.4)† 25 (6.8)
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Note: The differences in the prevalence of anti-HBs and anti-HBc between males and females in different age groups were determined by Cochran-Mantel-Haenszel test (*χ2 = 0.6199, p = .4311; §χ2 = 0.1657, p = .6840).

†Comparison of anti-HBs prevalence between the male and female donors (χ2 = 0.7103, p = .3994).

Comparison of anti-HBc prevalence between the male and female donors (χ2 = 0.0272, p = .8689).

Discussion

The present survey showed that the anti-HBs positive rate among blood donors in Nanjing was 58.8%, with no significant difference in different genders and different age groups. The results indicated that over half of the blood donors in Nanjing are immune to HBV and the blood recipients who are anti-HBs negative can be transient anti-HBs positive if they receive blood from these donors.

Usually, most blood donors are young adults at the age of 18–40 years.23,24 In the present study, 82.3% of the blood donors were at the age of 18 to 40 years. The overall prevalence (58.8%) of anti-HBs among the blood donors in our present survey is generally similar to the reported positive rates of 44.1% and 69.7% in Argentina and Vietnam, respectively,25,26 as well as the reported rate of in subgroups of blood donors in China.20,22,27 However, the anti-HBs positive rate is much higher than that reported in Middle East regions and African countries, as such 3.34%–5.6% in Saudi Arabia,23,28 2.5%–12.7% in Nigeria,29,30 and 15.9% in Alexandria, Egypt.31 The remarkable difference in the prevalence of anti-HBs between our study and other reports may be attributed to the different coverage of hepatitis B vaccination. In China, hepatitis B vaccination had been integrated into EPI since 1992, and a nation-wide catch-up vaccination campaign was implemented in children who were born between 1994 and 2001 and received no or incomplete hepatitis B vaccination.15 In addition, the difference in other characteristics, such as economic status, lifestyle in donors between China and other countries may be also associated with the difference in the prevalence of anti-HBs. However, it is infeasible to directly compare these characteristics in donors between China and other countries.

Individuals with negative HBsAg and positive anti-HBc, regardless of anti-HBs, are considered to have resolved previous HBV infection. The overall prevalence of anti-HBc in the present study was 7.0%, which is lower than the 20.6% reported in Bangladesh and the 14.2% in India,32,33 but much higher than the 0.71% in the Netherlands and 0.9%–1.6% in Switzerland.4,34 The big differences in the prevalence of anti-HBc among blood donors may be due to the different endemicity in different countries. Most of the European countries have low endemicity of HBV infection, generally around or less than 1%.35

China has incorporated hepatitis B vaccine into EPI since 1992.15 In the present study, anti-HBc prevalence (1.0%) in donors born on and after January 1, 1992, was significantly lower than that (15.5%) in donors born before 1992 (Table 2). This is the additional evidence that hepatitis B vaccination plays an important role in preventing HBV transmission and infection. On the other hand, difference in anti-HBs positive rates between these two groups had no statistical significance (Table 2). This may be attributed to the higher proportion of donors born before 1992 who acquired anti-HBs by resolving natural HBV infection, because they had much higher prevalence of anti-HBc (Table 2), the consequence of resolved HBV infection.

The findings in the present study have clinical implications in following aspects. First, since more than half of the blood donors are anti-HBs positive and a blood recipient may receive blood from two or more donors,16–19 it is possible that one of these donors is positive for anti-HBs. The anti-HBs can neutralize the virus if a recipient is transfused with blood from an OBI donor. Thus, HBV infection caused by blood transfusion may be reduced. This may explain that the reported incidence of OBI in blood donors is higher than the incidence of HBV infection caused by blood transfusion. Indeed, anti-HBs in fresh frozen plasma may neutralize the small number of infectious viruses.36 Second, anti-HBs negative blood recipients are likely to become transient anti-HBs positive after blood transfusion. Thus, an anti-HBs seroconversion does not necessarily indicate resolved HBV infection.37 Third, in the case of a blood recipient who is infected with HBV (HBsAg positive), transfusion of blood with positive anti-HBs may result in coexistence of HBsAg and anti-HBs, leading to unique hepatitis B serological profiles. Fourth, similar to those who are transfused with anti-HBs positive blood, those who are transfused with anti-HBc positive blood or both anti-HBs and anti-HBc positive blood may have seropositive for anti-HBc or for both anti-HBs and anti-HBc. Thus, passive transfer of anti-HBs and/or anti-HBc by blood transfusion should be kept in mind in the explanation of hepatitis B serological profiles.38–40

In conclusion, we showed that the positive rate of anti-HBs among blood donors in Nanjing was 58.8%. Since the global coverage with three doses of hepatitis B vaccine in infancy reached 82%–85% during 2016–2020,41 it is anticipatable that more blood donors will be anti-HBs positive in the near future, which would be helpful to prevent the potential HBV infection caused by transfusion of blood from donors with OBI.

Funding Statement

This study was supported by grants from the Health Commission of Nanjing City (ZKX20021, ZKX15045), Science and Technology Department of Jiangsu Province (BK20221169), Clinical Center for Infectious Disease of Nanjing City (ZKX2008), and Jiangsu Province Center for Innovation in Obstetrics and Gynecology (CXZX202229).

Disclosure statement

No potential conflict of interest was reported by the author(s).

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