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High HCV+ Rates in China: Past Illegal Blood Donation in China Linked to Hepatitis C Virus Infection
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".....there will be an ongoing challenge to care for patients with HCV infection....Technical support and drugs are needed to assist these central Chinese provinces cope with the care and treatment needs of HCV patients.......The global hepatitis C virus (HCV) seroprevalence rate varies widely, from <1% in Hong Kong and Sweden to >14% in Egypt and Cameroon. An estimated 3.2% of persons in mainland China are infected with HCV.....Two Chinese studies published in 2004 showed that >70% of injection drug users (IDUs) in Sichuan and Guangxi Provinces were seropositive for HCV antibodies, compared with 60% of IDUs in the United States....in resource-limited developing countries, transmission of HCV by blood transfusion and the medical reuse of needles and syringes remain serious public-health problems...."
Journal of Infectious Diseases (IDSA), News Release
For Immediate Release: Oct. 20, 2005
Research in a rural province of central China has documented that illegal blood donation practices led to high hepatitis C virus (HCV) infection rates in blood and plasma donors during the 1980s and early 1990s, and that failure to screen for HCV in transfusion recipients increased their risk of infection as well, according to an article in the November 15 issue of The Journal of Infectious Diseases, now available online.
Some blood donation facilities in rural China illegally pooled blood and reinfused compatible red blood cells to permit more frequent donations. Although government action has markedly curtailed such practices since the late 1990s, blood collection and banking methods in such settings still need to be monitored and improved, the article noted.
Researchers from the United States and China, including Han-zhu Qian, MD, PhD, of the University of Alabama at Birmingham, conducted a survey in 2003 among a random sample of 538 adult residents from 12 former commercial plasma-donating villages in Shanxi Province. Structured questionnaires were administered and blood samples tested for HCV antibodies. HCV rates were 8% in all participants, 28% in former plasma/blood donors, and about 3% in non-donors. Selling blood or plasma was the strongest independent predictor for HCV-positive findings. Receiving a blood transfusion was also independently associated with HCV; villagers who received blood transfusion had about 8 times the risk of HCV infection than those who had no history of blood transfusion.
Among the 538 villagers, 22 percent had a history of selling blood or plasma; from village to village, the rates ranged from 9 percent to 49 percent. The most common reasons for the practice were a need for money and being talked into it by other people. Villagers began to sell blood as early as in 1973 and as late as 1998; the main reasons for stopping were improved economic status, concern about health effects of blood drawing, abnormal liver function tests or hepatitis, and shut-down of the illegal blood center.
The investigators concluded that unhygienic plasma donation and receipt of blood transfusion are strong risk factors for HCV infection in rural central China, and that improved blood collection and blood banking practices remain an urgent health priority. "Technical support and drugs are needed to assist these central Chinese provinces cope with the care and treatment needs of HCV patients," the investigators added.
In an accompanying editorial, Roger Y. Dodd, PhD, of the American Red Cross noted that the study is "a snapshot of past events and should not be taken to define the present circumstances." Nevertheless, it illustrates that "short cuts, shoddy practice, pursuit of the bottom line, and lack of oversight can have devastating outcomes, not only for patients but also for donors."
"Hepatitis C Virus Infection in Former Commercial Plasma/Blood Donors in Rural Shanxi Province, China: The China Integrated Programs for Research on AIDS"
The Journal of Infectious Diseases Nov 15, 2005;192:1694-1700
Han-zhu Qian,1,3 Zhongmin Yang,1 Xiaoming Shi,1 Jianhua Gao,2 Cuiling Xu,1 Lan Wang,1 Kai Zhou,1 Yan Cui,1 Xiwen Zheng,1 Zunyou Wu,1 Fan Lu,1 Shenghan Lai,4 Sten H. Vermund,3 Yiming Shao,1 and Ning Wang1
1National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, and 2Beijing Municipal Center for Disease Prevention and Control, Beijing, China; 3Schools of Public Health and Medicine, University of Alabama, Birmingham; 4Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
(See the editorial commentary by Dodd, below.)
Background. Unsafe practices during illegal plasma donation in the late 1980s and early 1990s spread bloodborne infections in central China.
Methods. We conducted a community-based epidemiological study to evaluate the HCV seroprevalence rate in residents of communities where illegal plasma-collection practices have been documented and to explore the risk factors associated with HCV seropositivity. A cross-sectional survey of a random sample of 538 adult residents of 12 villages in rural Shanxi Province, where there had been an illegal commercial plasma-collection center, was conducted in 2003. Structured questionnaires were administered, and blood samples were tested for hepatitis C virus (HCV) antibodies.
Results.
HCV seroprevalence rates were 8.2% in all subjects, 27.7% in former commercial plasma/blood donors, and 2.6% in nondonors.
Selling blood or plasma was the strongest independent predictor of HCV seropositivity (odds ratio [OR], 14.4 [95% confidence interval {CI}, 7.131.6]).
A history of blood transfusion was also independently associated with HCV seropositivity (OR, 8.3 [95% CI, 2.132.0]).
Plasma donors had a higher risk of being HCV seropositive than did whole-blood donors (OR, 7.6 [95% CI, 2.920.9]), and female donors had a lower risk than did male donors (OR, 0.32 [95% CI, 0.120.80]).
The strength of the association between selling blood and HCV seropositivity was weaker when plasma donors were excluded (OR, 8.0 vs. 14.4).
Conclusions.
Unsafe practices during illegal plasma donation led to a high risk of HCV seropositivity for donors during the 1980s and 1990s.
Failure to screen for HCV increased the risk of seropositivity for transfusion recipients during this same period.
China has taken steps to halt illegal plasma collection and to improve blood-banking methods.
However, there will be an ongoing challenge to care for patients with HCV infection, even as its incidence decreases.
DISCUSSION
This community-based cross-sectional study found high HCV seroprevalence rates in subjects in rural Shanxi Province, where there had been an illegal commercial plasma/blood-collection center. Of subjects 1859 years old, 8.2% were infected with HCV. In former plasma/blood donors, the HCV seroprevalence rate was 27.7%, whereas, in nondonors, the HCV seroprevalence rate was 2.6%, which is similar to that in the general population of China [2, 14]. Selling blood/plasma was the strongest predictor of being HCV seropositive; the risk in former plasma/blood donors was 14.4 times higher than that in nondonors, after adjustment for other confounding factors. In former donors, those who had donated plasma had 7.6 times the risk of being HCV seropositive than that in those who had donated whole blood only. Caution should be used when interpreting any association between HCV seropositivity and whole-blood donation, however. In the study villages, plasma donation is more stigmatized than whole-blood donation, because villagers associate plasma donation, during which erythrocytes are reinfused, with the risk of HIV infection. Therefore, some former plasma donors may have reported themselves as being former blood donors, thereby exhibiting the so-called social desirability bias [15]. It might be interesting to investigate how the 11 nondonors acquired HCV infection, because misclassification due to either inaccurate recall or the social desirability bias may play a role. Because only a small number of HCV infections were present in spouses, the statistical power of the study was inadequate to assess the association between donation and spouses' HCV status or other reasons associated with HCV seropositivity in the 11 nondonors.
Unlike the association between illegal private blood-collection centers and HIV infection that was found in a study published elsewhere [16], selling plasma and/or blood in official collection centers was significantly associated with HCV seropositivity in our univariate analysis but did not remain significant in our multivariate analysis. A possible explanation is that the unadjusted association is confounded by selling plasma; our subjects commonly sold plasma at both official and illegal commercial plasma-collection centers. Moreover, whether this reflects poor memory of the type of donation center that was visited nearly 10 years previously or whether there were also hygiene problems in government hospitals and official blood-collection centers is not known.
Exposure to contaminated blood or blood products is the major risk factor for HCV seropositivity; sexual transmission of HCV is far less efficient [17]. A prospective study reported that persons in long-term monogamous partnerships had a risk of 0%0.6%/year for HCV seroconversion, whereas persons with multiple partners or those at risk of acquiring sexually transmitted diseases had a risk of 0.4%1.8%/year [18]. The present study has shown that subjects with a history of blood transfusion had 8 times the risk of HCV seropositivity than that of those without a history of blood transfusion; this suggests the vital need for local blood banks to screen all blood products for HCV. Subjects with >1 lifetime sex partner also had a higher risk of HCV seropositivity than did those with 1 lifetime sex partner (P = .058). In the study villages, neither commercial sex work nor having multiple lifetime sex partners is common; only 5 subjects reported a history of commercial sex work, and only 30 reported having extramarital sex. Having multiple sequential spouses may increase the risk of acquiring sexually transmitted diseases (e.g., HIV or HCV infection) in this group, because some subjects reported that they remarried after their former spouses had died of blood donationrelated diseases, including AIDS. The present study had low statistical power to test the associations between HCV seropositivity and commercial sex work or multiple lifetime sex partners, so we categorized the number of lifetime sex partners as >1 (as is relevant for this low-risk population). Much larger sample sizes would be needed to confirm any independent association between multiple lifetime sex partners and HCV seropositivity and to clarify whether commercial sex work or spouse's HCV status is associated with HCV seropositivity in these communities.
Older age and lower level of education were associated with HCV seropositivity in the univariate analysis, but these associations were not significant in the multivariate analysis. These observations may be related to a cohort effect: former plasma/blood donors who sold plasma/blood in the early 1990s were >35 years old at the time of our 2003 survey, and they likely received less education than younger villagers; furthermore, they had a higher risk of HCV seropositivity because they had sold plasma/blood. It is likely that selling plasma or receiving a blood transfusion is the risk factor of importance, with age and education being associated with the exposure rather than the outcome per se. In those who reported selling plasma/blood, women had a lower risk of HCV seropositivity than did men. No biological mechanism has been reported to suggest that men are more vulnerable to HCV infection; this difference in the HCV seroprevalence rate between the sexes might imply that there are unmeasured risks for male former plasma/blood donorsfor example, more frequent donations among men. Residual confounding is still possible, even though we included a variable to dichotomize the frequency of donation (10 or <10 times), because the original questionnaire did not include donation frequency as a continuous variable. Another explanation for the sex difference is that women may be more likely to recover from HCV infection and subsequently lose anti-HCV reactivity, because of female sex hormones [19, 20].
Our community-based survey had a number of methodological strengths. We conducted a community census from which a random sample was drawn. The study was thoroughly explained to the subjects before the study and when individual informed consent was obtained, and the participation rate was high, even though subjects consented totally voluntarily. The majority of those who did not participate had temporarily out-migrated, and only 6.1% of villagers who were contacted refused to participate. Given China's extensive health-care networks that reach the village level, our experience suggests that good epidemiological studies can be undertaken even in rural China in collaboration with local public-health departments and community leaders.
The present study also had limitations. Because we did not perform HCV RNA testing or recombinant immunoblot testing, some samples that gave positive results for HCV antibodies by EIA may have actually given false-positive results. A complete virological and clinical work-up was not feasible. We did not successfully identify communities with high HIV seroprevalence rates (only 7 [1.3%] of 538 subjects were HIV seropositive), which made a study of risk factors for HIV-HCV coinfection impossible. We conducted our study 10 years after the possible HCV exposures had occurred, so death and out-migration may have altered our findings. HIV-related deaths may lead to an underestimation of HCV seroprevalence rates, because HCV shares a blood transmission route with HIV. Nonparticipants were younger than participants and were less likely to have been infected with HCV though plasma/blood donation; a majority of nonparticipants (81/120) were temporary out-migrants and may have been more likely than participants to engage in behaviors that put them at risk of HCV infection, such as illicit drug (e.g., heroin or marijuana) use or commercial sex work. Therefore, a lack of data regarding nonparticipants may have biased the estimates of HCV seroprevalence rates in either direction.
Unhygienic practices during plasma donation and receipt of blood transfusion are strong risk factors for HCV seropositivity in rural central China. Improved blood-collection and blood-banking practices are an urgent health priority. Technical support and drugs are needed to assist these central Chinese provinces in the treatment of patients with HCV infection.
Study context.
This epidemiological survey was conducted for planning purposes as part of a larger, ongoing projectthe China Integrated Programs for Research on AIDSled by the Chinese Center for Disease Control and Prevention. Our study estimated HCV seroprevalence rates and risk factors for HCV seropositivity in residents of communities in Shanxi Province in which illegal commercial plasma-collection centers had been present. The study protocol was approved by the Division of AIDS Prevention Science Review Committee of the National Institute of Allergy and Infectious Diseases and the institutional review boards of the Chinese National Center for AIDS/STD Prevention and Control and the University of Alabama, Birmingham. Written, informed consent was obtained from all subjects. The human-experimentation guidelines of the US Department of Health and Human Services and the National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, were followed in the conduct of the research.
Study site and subjects.
Shanxi Province is located in central China and, to the south, borders Henan Province, which had the most severe HIV epidemic caused by unhygienic practices during plasma collection. Of the 644 HIV infections reported during 19952003, 76% were associated with plasma/blood collection [13]. A township in the southern part of Shanxi Province was selected as the study site because an illegal commercial plasma-collection center had operated there in approximately 1995 and because local health officials had reported that many HIV-infected persons lived there. Twelve of 25 villages in the township were selected on the basis of their history of having illegal plasma-collection practices and the willingness of village leaders to collaborate. A roster of all residents of the study villages was obtained from local authorities. With the help of village leaders, this roster was updated to include new residents and exclude those who had died or had permanently moved out of the villages.
A roster of 660 adult villagers was selected randomly from a sampling of 9205 villagers. Inclusion criteria were as follows: (1) permanent residence, having lived in a target village continuously for at least 6 months; (2) 1859 years old; (3) able and willing to provide informed consent; (4) able and willing to provide contact information. The study was conducted in November and December 2003.
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