Summary
Background
Illegal commercial plasma and blood donation activities in the late 1980s and early 1990s caused a large number of hepatitis C virus (HCV) infections in rural areas of China.
Methods
A cross-sectional survey was carried out in 2008, in which all residents in a former blood donation village in rural Hebei Province were invited for a questionnaire interview and testing for HCV antibodies. Questionnaires were administered to collect information about their personal status and commercial blood donation history, and HCV antibodies were tested by enzyme immunoassay.
Results
Of 520 villagers who participated in the interviews, 236 (45.4%) reported a history of selling whole blood or plasma. HCV seropositivity was confirmed in 148/520 (28.5%) interviewees and 101/236 (42.8%) former commercial plasma and blood donors. Selling plasma was the strongest independent predictor of HCV seropositivity (p = 0.0037). Past history of an operation was also independently associated with HCV infection (p = 0.0270).
Conclusions
Unsafe practices during illegal plasma donation led to a high risk of HCV seropositivity for donors during the late 1980s and early 1990s. Many infected people suffered chronic hepatitis from that time onwards and urgently needed treatment and care.
Keywords
1. Introduction
Hepatitis C virus (HCV) infection occurs worldwide. It is a major cause of chronic liver disease and the most common indication for liver transplantation.
1
, 2
Although the prevalence varies broadly among geographic areas, it is estimated that there are 170 million HCV chronic carriers globally and the prevalence rates range between about 0.1% in countries such as Iceland and Norway to 18.1% in Egypt.3
In China, a nationwide study conducted in 1992 revealed that HCV prevalence was 3.2% in China overall and 3.1% in rural China.4
Other smaller studies have reported HCV prevalence rates of 0–3% in rural populations from various Chinese provinces.- Xia G.L.
- Liu C.B.
- Cao H.L.
- Bi S.L.
- Zhan M.Y.
- Su C.A.
- et al.
Prevalence of hepatitis B and C virus infections in the general Chinese population. Results from a nationwide cross-sectional seroepidemiologic study of hepatitis A, B, C, D, and E virus infections in China, 1992.
Int Hepatol Commun. 1996; 5: 62-73
5
, 6
, 7
HCV is most frequently transmitted by percutaneous exposure to infected blood or blood-derived body fluids, such as through transfusion of contaminated blood or blood products, nonsterile medical injections, or injecting drug use.
8
In China, illegal commercial plasma and blood collection activities were very common in the late 1980s and early 1990s before the national blood donation law was enacted. These illegal blood donations caused serious blood-borne HCV infections in some rural areas. The first recognized outbreak of HCV infection among plasma donors occurred in the late 1980s.9
Since then, cross-sectional studies have investigated HCV infection among former plasma or blood donors, in whom prevalence rates have varied from 9.6% to 72.8%.10
, 11
, 12
, 13
, 14
In the present study, we performed a cross-sectional survey to investigate the prevalence and risk factors among residents in a former commercial blood donation village in Central China, where farming is the predominant occupation. The data derived could be used to provide basic information for the management and treatment of HCV carriers in order to reduce the transmission of HCV after blood donation.
2. Methods
2.1 Participants and samples
A register of all residents of the study village was obtained from the local authorities during the preparatory study. Next, all the local residents of this village aged 1–91 years were invited to participate in the investigation during 2005–2006. The field study was conducted in the village clinic or village committee office. Standardized questionnaire-based interviews sought demographic, medical, and behavioral data, including plasma/blood donation history. Ten milliliters of venous blood was collected in a vacutainer containing sodium heparin for HCV antibody testing. The samples were stored at room temperature and transferred within 3 h to a field station for processing. Aliquots of plasma were stored at −40 °C until they were sent on dry ice to the Chinese Center for Disease Control and Prevention in Beijing. The study protocol was approved by the Institute of the Chinese Academy of Medical Sciences.
2.2 Laboratory assays
We tested the plasma specimens for HCV antibody by HCV version 3.0 enzyme immunoassay (EIA) (Ortho Diagnostics, Raritan, NJ, USA) in accordance with the manufacturer's instructions. Samples that were positive by HCV EIA were confirmed by HCV version 3.0 RIBA (Ortho Diagnostics).
2.3 Statistical analysis
A Chi-square test was used to calculate and compare the prevalence of viral infections among participants with different sociodemographic characteristics. Multivariate logistic regression analyses were undertaken to compare factors associated with HCV infection among all participants. The 95% confidence interval (CI) of the prevalence was calculated based on normal approximation to binomial distribution when that approximation held. All statistical analyses were done using SAS software version 8.0.
3. Results
3.1 Participation rate and sociodemographics of participants
Of the 1109 villagers, 520 individuals participated in the interviews, contributed blood samples for HCV testing, and were thereby included in the analysis. The proportions of male and female participants were almost equal and their age distribution was 1–91 years. The mean age of the male participants was 45.11 ± 19.32 years and for the female participants was 45.24 ± 17.46 years. Non-participation was mainly because of out-migration of the villagers for a temporary job. All participants were of Han majority ethnicity.
3.2 Commercial plasma/blood donation history
Of the 520 participants, 236 (45.4%) had a history of selling plasma or blood in the village, where there had been an illegal commercial plasma collection center. The other 284 villagers had never sold plasma or blood. Among the donors, 117 individuals had sold only blood and five had sold only plasma. The remaining 114 had sold both blood and plasma, and accounted for 48.3% of all donors.
3.3 HCV seroprevalence and risk factors for HCV seropositivity
3.3.1 Seroprevalence of anti-HCV in all subjects stratified by sex, age, education, and blood donation experience
HCV infection was detected in 148 (28.5%) of the 520 villagers; 70 were males and 78 were females. The prevalence did not differ meaningfully by sex (Chi-square = 0.3094, p = 0.5780), however the trend Chi-square test revealed that HCV seropositivity varied with age. The peak HCV seropositivity occurred in the 50–59 years age group.
Our results indicated that there was a significant difference between educated and illiterate villagers with regard to HCV infection, but we found no difference with respect to the level of education attained by those who had been educated (primary school, middle school, or high school level); this proved that HCV seropositivity had no relationship with educational experience.
Of the villagers who had sold blood or plasma, 101 were infected, whereas only 47 of those who had never sold blood or plasma were seropositive. HCV seroprevalence in donors was 2.6 times higher than in the villagers who had not sold blood or plasma. All of the results are shown in Table 1.
Table 1Seroprevalence of anti-HCV in all subjects stratified by sex, age, education, and blood donation experience
| Parameters | Number | HCV seropositivity, n (%) | Chi-square value | p-Value |
|---|---|---|---|---|
| Sex | 0.3094 | 0.578 | ||
| Male | 256 | 70 (27.3) | ||
| Female | 264 | 78 (29.5) | ||
| Age groups, years | 21.5842 | <0.0001 | ||
| 1–19 | 49 | 4 (8.2) | ||
| 20–29 | 64 | 9 (14.1) | ||
| 30–39 | 60 | 9 (15.0) | ||
| 40–49 | 129 | 43 (33.3) | ||
| 50–59 | 110 | 54 (49.1) | ||
| 60 or older | 108 | 29 (26.9) | ||
| Education | 4.341 | 0.0372 | ||
| Educated | 380 | 95 (25.0) | ||
| Illiterate | 140 | 53 (37.9) | ||
| Educational experience | 0.5789 | 0.7487 | ||
| Illiterate | 140 | 53 (37.9) | ||
| Primary school | 175 | 43 (24.6) | ||
| Middle school | 165 | 42 (25.5) | ||
| High school | 40 | 10 (25.0) | ||
| Donation | 43.611 | <0.0001 | ||
| Donors | 236 | 101 (42.8) | ||
| Non-donors | 284 | 47 (16.5) |
HCV, hepatitis C virus.
3.3.2 HCV seroprevalence in donors of blood and plasma
HCV seroprevalence was higher in the donors who had sold both blood and plasma than in those who had only sold blood. However, there was no significant difference in HCV infection between the donors who had sold both blood and plasma and those who had only sold plasma. The villagers who had only sold plasma were more likely to have become HCV-seropositive than those who had only sold blood. The results are shown in Table 2.
Table 2HCV seroprevalence in donors of blood and plasma
| Type of donation | HCV antibody | HCV seropositivity (%) | Chi-square value | p-Value | |
|---|---|---|---|---|---|
| Positive | Negative | ||||
| Non-donors | 47 | 237 | 16.5 | 0.715 | 0.3978 |
| Blood donation only | 18 | 99 | 15.4 | ||
| Blood donation only | 18 | 99 | 15.4 | 0.0037 | |
| Plasma donation only | 4 | 1 | 80.0 | ||
| Plasma donation only | 4 | 1 | 80.0 | 0.26 | 0.6101 |
| Both donation | 79 | 35 | 69.3 | ||
| Non-donors | 47 | 237 | 16.5 | 104.62 | <0.0001 |
| Both donation | 79 | 35 | 69.3 | ||
HCV, hepatitis C virus.
a p-Value calculated directly by Fisher's bilateral exact probability test.
3.3.3 HCV seroprevalence according to route of blood exposure
Univariate analysis demonstrated that surgery was a greater risk factor for HCV infection than receiving a blood transfusion, acupuncture, dental extraction, or sharing a razor or toothbrush. The results are shown in Table 3.
Table 3HCV seroprevalence according to route of blood exposure
| Risk factors | HCV antibody | Total | HCV seropositivity (%) | Chi-square value | p-Value | |
|---|---|---|---|---|---|---|
| Positive | Negative | |||||
| Blood transfusion | 0.3393 | |||||
| Yes | 2 | 3 | 5 | 40.0 | ||
| No | 146 | 369 | 515 | 28.3 | ||
| Operation | 4.8936 | 0.027 | ||||
| Yes | 30 | 47 | 77 | 39.0 | ||
| No | 118 | 325 | 443 | 26.6 | ||
| Acupuncture | 0.046 | 0.8301 | ||||
| Yes | 7 | 16 | 23 | 30.4 | ||
| No | 141 | 356 | 497 | 28.4 | ||
| Dental extraction | 0.7906 | 0.3739 | ||||
| Yes | 20 | 40 | 60 | 33.3 | ||
| No | 128 | 332 | 460 | 27.8 | ||
| Razor share | 0.1833 | 0.6685 | ||||
| Yes | 3 | 4 | 7 | 42.9 | ||
| No | 145 | 368 | 513 | 28.3 | ||
| Teeth-brush share | 0.4383 | |||||
| Yes | 1 | 2 | 3 | 33.3 | ||
| No | 147 | 370 | 517 | 28.4 | ||
HCV, hepatitis C virus.
a p-Value calculated directly by Fisher's bilateral exact probability test.
3.3.4 Multivariate logistic regression analysis of risk factors
Multivariate logistic regression analysis suggested that plasma donation (odds ratio (OR) 33.200, 95% CI 1.284–858.446; p = 0.035) and whole blood donation (OR 34.626, 95% CI 2.167–553.272; p = 0.012) were highly associated with HCV seropositivity. The results are shown in Table 4.
Table 4Multivariate logistic regression analysis of risk factors
| Variable | p-Value | OR | 95% CI |
|---|---|---|---|
| Age | 0.024 | 0.816 | 0.683–0.974 |
| Plasma donation | 0.035 | 33.200 | 1.284–858.446 |
| Plasma and blood donation | 0.012 | 34.626 | 2.167–553.272 |
| Operation | 0.394 | 1.363 | 0.669–2.777 |
OR, odds ratio; 95% CI, 95% confidence interval.
4. Discussion
According to the national survey of HCV infection, the average seroprevalence was 3.2%,
4
which means that >40 million Chinese people were HCV-seropositive. Another epidemiological investigation has indicated that HCV is highly prevalent in former illegal blood and plasma donors and that prevalence could be up to 8.2% in that population.- Xia G.L.
- Liu C.B.
- Cao H.L.
- Bi S.L.
- Zhan M.Y.
- Su C.A.
- et al.
Prevalence of hepatitis B and C virus infections in the general Chinese population. Results from a nationwide cross-sectional seroepidemiologic study of hepatitis A, B, C, D, and E virus infections in China, 1992.
Int Hepatol Commun. 1996; 5: 62-73
15
In the present study, 520 residents were selected from a former blood donation village in Dazhang, Zhao County, Hebei Province. We found that HCV seroprevalence was 28.5% in all villagers and 42.8% in former commercial plasma/blood donors, prevalences that are higher than the previously reported average.15
The increased risk of HCV infection was mainly as a result of the illegal commercial plasma and blood collection activities in selected rural areas. In particular, the practice of pooling blood and reinfusing red blood cells into donors of the same blood types caused the rapid spread of HCV infection.9
There was no difference in HCV seropositivity according to sex, which suggests a similar sensitivity to HCV infection between men and women. Chi-square tests revealed that HCV seropositivity increased with age and reached a peak in the 50–59 years age group. In contrast, HCV seroprevalence was lower in those aged ≥60 years than in the 50–59 years age group, because participation in commercial blood donation mostly involved adults and adolescents at that time. This study was performed more than 10 years after the ban on illegal commercial blood donation, and most of the donors were aged >40 years. This could explain why the 50–59 years age group had a relatively higher HCV seropositivity.
Although HCV is transmitted mainly through blood-to-blood contact and intravenous drug use is currently the dominant route of transmission in developed countries, in China as a developing country, nosocomial transmission of HCV is not an uncommon route of infection and may be greatly underestimated. That is why surgery was found to be the most important HCV risk factor in our study by univariate analysis.
In both male and female subjects, selling plasma, older age, and surgery appeared to be associated with HCV infection. In the multivariate analyses to identify risk factors, selling plasma (OR 33.200; p = 0.035) and whole blood (OR 34.626; p = 0.012) were independently associated with HCV seropositivity.
However, HCV seropositivity was 16.5% in those who had never sold blood or plasma, which is clearly higher than the average HCV seroprevalence in the Chinese population. This phenomenon was probably caused by other unusual routes of HCV transmission, such as mucosal exposure, sexual transmission, and perinatal exposure (mother to child).
16
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, 18
For example, the spouse of an HCV carrier was much more likely to be infected, and the child of an HCV-infected mother was also at higher risk.In summary, HCV is now common in this selected rural Chinese community and the public health impact of the high prevalence of HCV infection may be substantial. HCV is an important cause of end-stage liver disease and hepatocellular carcinoma, and it can act synergistically with hepatitis B virus infection,
19
which is endemic in China. Future studies should examine the prevalence of blood-borne viruses in other parts of China, how these viruses are transmitted, and the resulting health effects. Efforts to halt the transmission of HCV and other blood-borne viruses in rural China should be a top public health priority.Acknowledgements
This work was supported by a grant from the Major Science and Technology Project for Infectious Disease. The authors express their sincere thanks to all members of the epidemic prevention station of Zhengding County for their support during the collection of samples.
Conflict of interest: The authors declare that they have no competing interests.
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Article info
Publication history
Published online: July 16, 2012
Accepted:
May 23,
2012
Received:
May 23,
2012
Corresponding Editor: William Cameron, Ottawa, CanadaIdentification
Copyright
© 2012 International Society for Infectious Diseases. Published by Elsevier Inc.
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