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. 2020 Apr 24;99(17):e19832. doi: 10.1097/MD.0000000000019832

Overall prevalence of human parvovirus B19 among blood donors in mainland China

A PRISMA-compliant meta-analysis

Xin Li a,b, Zheng Lin c, Jiayan Liu a, Yuanyuan Tang d, Xiaohong Yuan a, Nainong Li a, Zhenxing Lin a, Yuanzhong Chen a,∗, Ailin Liu a,e,∗
Editor: Ahmet Emre Eskazan
PMCID: PMC7220778  PMID: 32332630

Supplemental Digital Content is available in the text

Keywords: blood donors, genotypes, human parvovirus B19, mainland China, meta-analysis, prevalence

Abstract

Background:

Human parvovirus B19 (B19V) infection exhibits a broad range of clinical outcomes. Blood transfusion is a common route of B19V transmission. However, information about the overall prevalence of B19V infection and B19V genotypes among blood donors in mainland China is lacking.

Methods:

This meta-analysis was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. A literature search for studies reporting the B19V prevalence among blood donors in mainland China from 2000 to 2018 was performed. The prevalence of B19V was estimated through a meta-analysis of the relevant literature. A comprehensive meta-analysis program was used for data processing and statistical analysis.

Results:

Twenty-one eligible articles were included, involving 48,923 participants assessed for B19V-DNA, 12,948 participants assessed for anti-B19V immunoglobulin M (IgM), and 8244 participants assessed for anti-B19V immunoglobulin G (IgG). The analysis revealed the pooled estimates of the prevalence rates of B19V-DNA, anti-B19V IgM, and anti-B19V IgG among blood donors to be 0.7% (95% confidence interval [CI] 0.2–2.4%), 2.7% (95% CI 1.7–4.3%), and 33.6% (95% CI 28.2–39.4%), respectively. Moreover, phylogenetic analyses indicated that 142 of 169 (84.0%) B19V isolates belonged to Genotype 1.

Conclusions:

The overall prevalence of B19V among blood donors is not high in mainland China, and most isolates belong to Genotype 1.

1. Introduction

In 1975, Australia virologist Cossart observed human parvovirus B19 (B19 V) particles under an electron microscope when screening serum samples from patients with hepatitis B.[1] Because the parvovirus virus-like particle was found in a sample marked as No. 19, Cossart named it the human parvovirus B19.[1] As the smallest and structurally most simple human virus, it is a small, non-enveloped DNA virus with a single-stranded linear DNA genome and measures only 20 to 25 nm in diameter.[2–6] B19V belongs to the genus Erythroparvovirus in the family Parvoviridae, and infection with B19V may have a broad range of clinical outcomes, including transient aplastic crisis (TAC), rash-fever illnesses, rheumatoid arthritis (RA), systemiclupus erythematosus (SLE), pure red cell aplasia (PRCA), hydrops fetalis, and fetal death, especially for patients with abnormal hematology or immunestatus.[7–16] B19V is transmitted mainly through the respiratory route, blood transfusions, organ/bone marrow transplantations, and mother-to-child transmission.[3,7,15,17–19] Recently, commonly used detection methods of B19V infection have included enzyme-linked immunosorbent assays (ELISA) for anti-B19V immunoglobulin G (IgG) and anti-B19V immunoglobulin M (IgM) antibodies and nucleic acid tests (NAT) for B19V-DNA.[20,21] In some countries, regulations or guidelines for screening and monitoring B19V have been proposed to ensure the safety of blood products as much as possible. Thus, information about the overall prevalence of B19V infection and B19V genotypes among blood donors in mainland China is lacking. To provide a reference for evaluating and developing appropriate strategies, we conducted a meta-analysis based on available data from mainland China between 2000 and 2018.

2. Methods

This work was performed and reported in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (Supplementary Table 1).[22] In addition, these analyses were based on previously published studies; therefore, no ethical approval was necessary for this study.

2.1. Literature search

Search strings were established by combining the following terms using Boolean operators: “parvovirus B19, human,” “blood donors,” and “China.” We searched for relevant studies published from 2000 to 2018 in the China National Knowledge Infrastructure (CNKI), PubMed, and Wanfang databases. To include as many relevant studies as possible, a search of the reference lists of published articles was also manually conducted.

2.2. Data selection and extraction

Two investigators independently and carefully screened the studies and extracted the relevant data in accordance with the inclusion and exclusion criteria. Any disagreement was resolved by discussion. The inclusion criteria were as follows: the literature selected must be related to the epidemiological investigation or genotype research of B19V and the subjects of the selected studies were blood donors in mainland China. The exclusion criteria were articles published in non-academic journals; dissertations, review papers, conference abstracts, or presentations; irrelevant research; and studies from regions of China outside the mainland (i.e., Hong Kong, Macao, and Taiwan).

2.3. Study quality evaluation

Researchers used a cross-sectional/prevalence study quality assessment tool recommended by the Agency for Healthcare Research and Quality (AHRQ) to determine the quality of the included studies.[23] This tool has been widely used to evaluate the quality of cross-sectional/prevalence studies.[24,25] The checklist consisted of 11 items. If the answer was “Yes,” the score of an item was recorded as“1”; otherwise, the score was recorded as “0.” The total score range was 0 to 11 for each study. The included studies were categorized as low, medium, or high quality according to a total score of 0 to 3, 4 to 7, or 8 to 11, respectively.

2.4. Statistical analysis

Comprehensive Meta-Analysis version 2.0 (CMA 2.0; Biostat Inc., Englewood, NJ) was used for data manipulation and statistical analyses. Conversion of the prevalence to the logit prevalence was performed as follows: logit p = ln (p/[1 − p]), where p is the prevalence and ln is the natural logarithm; the data distribution was normalized. The sampling variance of each logit prevalence, V(logit p), was equal to 1/(np) + 1/(n[1 – p]), with n representing the sample size. To facilitate the final interpretation, the logit p was back-transformed into the prevalence rate after the statistical analyses were conducted.[26] The prevalence estimates and their 95% confidence intervals (CIs) were determined based on fixed or random effects models, taking into consideration the heterogeneity among studies, which was calculated with the Q test (P < .10 represents statistically significant heterogeneity) and I2 test (values of 75%, 50%, and 25% were considered high, medium, and low levels of heterogeneity, respectively). Potential publication bias was examined using a funnel plot (logit prevalence vs standard error), Begg's test and Egger's test (P < .05 was considered indicative of statistically significant publication bias). The trim and fill method was also used to adjust the data for publication bias. Stratified analyses were performed by study locations, sex, and sample size of the included studies. Furthermore, the B19V genotypes of infected blood donors on the Chinese mainland were evaluated.

3. Results

3.1. Process of study selection

In total, 544 articles were initially retrieved from the PubMed (9), CNKI (469), and Wanfang (66) databases using the literature search strategy mentioned above. Based on the inclusion and exclusion criteria, 455 articles were excluded after abstract review, and another 5 articles were excluded after the full text was read. Twenty-one articles on B19V infection, including 11 articles examining B19V-DNA, 10 articles examining anti-B19V IgM, 12 articles examining anti-B19V IgG,[27–47] and 4 articles examining B19V genotypes, were eventually included in the present study.[45,48–50] The study selection process is shown in Fig. 1.

Figure 1.

Figure 1

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PRISMA flow diagram of the literature search process. PRISMA = Preferred Reporting Items for Systematic Reviews and Meta-Analyses.

3.2. Characteristics of the included studies

All 21 included studies of blood donors with B19V infection were cross-sectional; data from 11 provinces, 2 autonomous regions, and 1 municipality were included in these studies. The present analysis included 48,923 participants with NAT results, 12,948 with anti-B19V IgM results, and 8244 with anti-B19V IgG results. Most blood samples were from blood centers. The sample sizes for the NATs ranged from 110 to 10,452 (median 3957, interquartile range 450–8288), and the sample sizes of the selected studies using ELISAs ranged from 96 to 4500 (median 872, interquartile range 370–1098). In addition, 14 studies were categorized as moderate quality, and 7 were categorized as high quality, according to the checklist of Cross-sectional/Prevalence Study Quality (Supplementary Table 2). The overall quality of the included studies was moderate to high. Please see Table 1 for the relevant details of each study.

Table 1.

Summary of data from the included articles on B19V prevalence among blood donors in mainland China.

3.2.

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3.3. Prevalence of B19V infection among blood donors in mainland China

The overall prevalence of B19V-DNA was evaluated from the analysis of 11 studies.[28,29,31,32,34,36,38,40,43–45] Substantial heterogeneity was found among these studies (I2 = 98.2%, P < .001). Therefore, the pooled prevalence of B19V-DNA was estimated with a random effects model. The estimated prevalence of B19V-DNA was 0.7% (95% CI 0.2–2.4%), and the forest plot for the pooled estimate is illustrated in Fig. 2. Some degree of asymmetry was observed in the funnel plot (Supplementary Figure 1), and publication bias among the included studies was detected using Begg's test and Egger's test (PBegg's test = .10, and PEgger's test = .03). Thus, the trim and fill method was applied to adjust data for publication bias. The adjusted pooled prevalence of B19V-DNA was also 0.7% (95% CI 0.2–2.4%).

Figure 2.

Figure 2

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Forest plot of the meta-analysis of B19V-DNA prevalence among blood donors. B19V = Human parvovirus B19.

Similarly, the estimated prevalence rates of anti-B19V IgM and IgG were also calculated among the included studies.[27,30,33–35,37–39,41,42,44–47] As shown in Figs. 3 and 4 and Table 2, the estimates were 2.7% (95% CI 1.7–4.3%) and 33.6% (95% CI 28.2–39.4%), respectively. The funnel plots are also shown in Supplementary Figure 2 and 3.

Figure 3.

Figure 3

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Forest plot of the meta-analysis of the prevalence of anti-B19V IgM antibodies among blood donors. B19V = Human parvovirus B19.

Figure 4.

Figure 4

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Forest plot of the meta-analysis of the prevalence of anti-B19V IgG antibodies among blood donors. B19V = Human parvovirus B19.

Table 2.

Prevalence of B19V infection among blood donors in mainland China.

3.3.

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3.4. Stratified analysis of B19V-DNA screening data

Generally, mainland China can be divided into a south and north region according to geography. The study included 9 epidemiological studies of B19V-DNA in south China and 4 in north China.[28,29,31,32,34,38,40,43–45] In south China, the pooled prevalence of B19V-DNA was 0.4% (95% CI 0.1–1.6%), and the estimated prevalence of B19V-DNA was 2.5% (95% CI 0.4–15.7%) in north China. No significant statistical difference was found between the south and north regions of China (x2 = 2.26, P = .13).

Four studies investigated the association between sex and the prevalence of B19V-DNA among blood donors.[31,34,38,40] The prevalence of B19V-DNA among male donors was 1.0% (95% CI 0.1–6.6%), while that among female donors was 1.1% (95% CI 0.2–7.1%). No significant difference was observed in the prevalence of B19V-DNA between male and female donors (x2 = 0.005, P = .94).

Six studies had large sample sizes (>1000), and the estimate of B19V-DNA prevalence was 0.1% (95% CI 0–0.2%).[34,36,40,43–45] The other 5 studies had sample sizes of <1000, and the pooled estimate of B19V-DNA prevalence was 7.1% (95% CI 3.2–14.9%).[28,29,31,32,38] A statistically significant difference was observed between the 2 groups (x2 = 52.3, P < .001).

3.5. B19V-DNA genotypes among blood donors

Four included studies conducted phylogenetic analyses of NS1/VP1-unique regions to analyze the genotype of 169 B19V-DNA sequences from positive samples.[45,48–50] These phylogenetic analyses indicated that 2 B19V genotypes (Genotype 1 and Genotype 3) were present in mainland China, and none of the samples clustered with Genotype 2 sequences; 142 of 169 (84.0%) B19V isolates belonged to Genotype 1, and the remaining isolates belonged to Genotype 3.

4. Discussion

Although B19V infection generally does not result in serious health problems, it can cause serious complications in some high-risk groups, such as pregnant women, potential hematological malignancy patients, and patients with immunodeficiency. Since the beginning of this century, Germany, the Netherlands, and Poland have performed B19V NATs to screen blood donors.[21,51–53] In Germany, NATs for B19V DNA were introduced into blood donor screening programs in 2000. Blood products containing ≥105 IU/mL of B19V DNA are discarded, while minipools of blood products with <105 IU/mL of B19V DNA are released.[52] In the Netherlands, it has been proposed that “B19V-safe” cellular blood products be administered to the high-risk groups mentioned above. “B19-safe” cellular blood products are defined as those from a donor in which anti-B19V IgG antibodies have been detected in 2 separate blood samples taken at least 6 months apart.[53] B19V screening of blood products was subsequently expanded in some regions and countries. To reduce the risk of transmission via transfusion, relevant regulations in the European Pharmacopoeia were initiated to control the potential B19V burden in pooled virus-inactivated plasma and anti-D immunoglobulins in 2004.[21,54,55] The US Food and Drug Administration (FDA) also issued similar guidelines and standards that limit the level of B19V DNA in plasma derivatives to 104 IU/mL; however, no blood donor screening test for B19V has been licensed.[21,55–57] In 2008, Japan started to introduce B19V screening of all blood donations.[21,55,58] Published studies show that the prevalence rates of B19V infection among blood donors worldwide range from 0.7% to 7.5% for IgM and from 6.0% to 79.1% for IgG.[21,59–62] Generally, the B19V-DNA prevalence among blood donors is low, ranging from 0% to 1.3%.[21,34,63–65]

In mainland China, there are currently no specific strategies for monitoring and screening B19V in blood donations or products. Prevention and control strategies for transfusion-transmitted infections (TTIs) should be established based on epidemiological evidence. Considering the high cost of detecting and removing B19V, the overall prevalence in donors in mainland China needs to be elucidated to develop appropriate prevention strategies. Therefore, the B19V prevalence among blood donors was evaluated based on previous research in this area. Twenty-one articles on the prevalence of B19V infection in blood donors were identified. The pooled estimates of the prevalence rates were 0.7% for B19V-DNA, 2.7% for anti-B19V IgM, and 33.6% for anti-B19V IgG. Therefore, the present study found a low, non-endemic prevalence of B19V among blood donors in mainland China. Whether it is necessary to screen and monitor B19V in blood donation or products in mainland China needs further study; future studies should include strategy evaluations, cost-effectiveness, etc.

Moreover, stratified analysis suggested that no significant geographic difference in the prevalence of B19V-DNA existed, although the estimated prevalence of B19V-DNA in south China was lower than that in north China. There are several possible reasons for this, including large-scale population migration, economic development, and improved living and sanitary conditions. The prevalence of B19V-DNA was not significantly different between male and female donors, indicating that both male and female donors have the same susceptibility to B19V. Our work also determined that in studies with large sample sizes (>1000), the prevalence of B19V-DNA in blood donors was lower than that in studies with small sample sizes. The small-study effect is obvious in these small-sample studies. The possible impact of this effect on the results is an increased estimate of BV19 prevalence. Therefore, the use of large sample sizes is recommended for future B19V epidemiological studies of blood donors.

Phylogenetic analysis identified three main genotypes of B19V, including Genotype 1, which is prevalent worldwide, acting as the prototypical and most common B19V,[66,67] Genotype 2, which is sporadically found circulating in Europe and North America and is a rare genotype,[49,68–70] and Genotype 3, which appears to be principally endemic to Ghana and has also been found in Brazil, France, North India, and the United States.[49,71] This study showed that the majority of B19V isolates in mainland China belonged to Genotype 1, followed by Genotype 3, and Genotype 2 was not detected. It would be beneficial to understand the source, spread, and control of B19V in the Chinese mainland.

There are several limitations of this work. The included studies only involved 14 of the 31 provinces in mainland China (i.e., 11 provinces, 2 autonomous regions, and 1 municipality). Other areas of mainland China lacked epidemiological studies on B19V in blood donors. Further analyses such as stratified analysis and meta regression are needed to provide additional data support. Additionally, because some important information provided in the included studies was not detailed, the ability to evaluate the quality of the research was limited. Moreover, some studies were from different regions in the same province, such as Guangdong Province. Although these studies were independently performed by different research teams, B19V-positive donors might have been resampled due to population migration, design overlap, etc. Considering the population of about 1.3 billion and blood donation rate of 9‰ in mainland China, the population of blood donors in each province is large.[72] The chance of being resampled is probably low; therefore, such risks have little effect on the estimated prevalence of B19V. Finally, blood donors were not chosen randomly in the included studies. Thus, selection bias and confounding seem to be inevitable, especially in the small-sample size studies of B19V prevalence in which there may exist a small-sample effect. A small sample size means studies are susceptible to selection bias and confounding. However, given the poor representation of small-sample studies, we are still inclined to conclude that the pooled prevalence of B19V in blood donors is not high in mainland China. In addition, readers whose native language is not Chinese would find it difficult to use the original materials included because most of the studies were written in Chinese. However, we are confident in the results because the included studies were obtained from multiple sources, combining data from 48,923 samples subjected to NATs, 12,948 samples tested for anti-B19V IgM, and 8244 samples tested for anti-B19V IgG by ELISAs, which are large sample sizes.

In summary, this research provides comprehensive and objective data on the prevalence of BV19 in blood donors. The results indicate that the prevalence of B19V among blood donors in mainland China is not high, and most B19V isolates belong to Genotype 1.

Acknowledgments

The authors gratefully acknowledge all of the researchers whose articles were included in this meta-analysis.

Author contributions

Conceptualization: Xin Li, Ailin Liu, and Yuanzhong Chen.

Data curation: Xin Li, Zheng Lin, Jiayan Liu, and Yuanyuan Tang.

Formal analysis: Xin Li, Zheng Lin, and Xiaohong Yuan.

Funding acquisition: Yuanzhong Chen.

Investigation: Jiayan Liu, Yuanyuan Tang, and Xiaohong Yuan.

Methodology: Xin Li, Zheng Lin, and Zhenxing Lin.

Resources: Xin Li, Ailin Liu, and Nainong Li.

Visualization: Xin Li and Zheng Lin.

Supervision: Ailin Liu and Yuanyuan Tang.

Validation: Ailin Liu and Nainong Li.

Writing – original draft: Xin Li, Jiayan Liu, and Yuanyuan Tang.

Writing – review and editing: Xin Li, Ailin Liu, and Yuanzhong Chen.

Supplementary Material

Supplemental Digital Content

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Footnotes

Abbreviations: B19V = human parvovirus B19, CI = confidence interval, CNKI = China National Knowledge Infrastructure, ELISA = enzyme-linked immunosorbent assay, FDA = Food and Drug Administration, IgG = immunoglobulin G, IgM = immunoglobulin M, NAT = nucleic acid test, PRCA = pure red cell aplasia, RA = rheumatoid arthritis, SLE = systemiclupus erythematosus, TAC = transient aplastic crisis, TTI = transfusion-transmitted infection.

How to cite this article: Li X, Lin Z, Liu J, Tang Y, Yuan X, Li N, Lin Z, Chen Y, Liu A. Overall prevalence of human parvovirus B19 among blood donors in mainland China: A PRISMA-compliant meta-analysis. Medicine. 2020;99:17(e19832).

XL, ZL, JL, and YT have contributed equally to this work.

This study was supported by the National and Fujian Provincial Key Clinical Specialty Discipline Construction Program, P.R.C. and the Construction Project of Fujian Medical Center of Hematology (Min201704).

The authors have no conflicts of interest to disclose.

The description on the conflicts of interest and disclosure is accuracy.

Supplemental Digital Content is available for this article.

References

  • [1].Cossart YE, Field AM, Cant B, et al. Parvovirus-like particles in human sera. Lancet 1975;1:72–3. [DOI] [PubMed] [Google Scholar]
  • [2].Anderson MJ, Jones SE, Fisher-Hoch SP, et al. Human parvovirus, the cause of erythema infectiosum (fifth disease)? Lancet 1983;1:1378. [DOI] [PubMed] [Google Scholar]
  • [3].Brown KE. The expanding range of parvoviruses which infect humans. Rev Med Virol 2010;20:231–44. [DOI] [PubMed] [Google Scholar]
  • [4].Cotmore SF, Agbandje-McKenna M, Chiorini JA, et al. The family Parvoviridae. Arch Virol 2014;159:1239–47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [5].Lukashov VV, Goudsmit J. Evolutionary relationships among parvoviruses: virus-host coevolution among autonomous primate parvoviruses and links between adeno-associated and avian parvoviruses. J Virol 2001;75:2729–40. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [6].Young NS, Brown KE. Parvovirus B19. N Engl J Med 2004;350:586–97. [DOI] [PubMed] [Google Scholar]
  • [7].Anand A, Gray ES, Brown T, et al. Human parvovirus infection in pregnancy and hydrops fetalis. N Engl J Med 1987;316:183–6. [DOI] [PubMed] [Google Scholar]
  • [8].Erdman DD, Usher MJ, Tsou C, et al. Human parvovirus B19 specific IgG, IgA, and IgM antibodies and DNA in serum specimens from persons with erythema infectiosum. J Med Virol 1991;35:110–5. [DOI] [PubMed] [Google Scholar]
  • [9].Kerr JR. The role of parvovirus B19 in the pathogenesis of autoimmunity and autoimmune disease. J Clin Pathol 2016;69:279–91. [DOI] [PubMed] [Google Scholar]
  • [10].Kyeong KS, Won HS, Lee MY, et al. Clinical features of 10 fetuses with prenatally diagnosed parvovirus B19 infection and fetal hydrops. Fetal Pediatr Pathol 2015;34:49–56. [DOI] [PubMed] [Google Scholar]
  • [11].Lunardi C, Tinazzi E, Bason C, et al. Human parvovirus B19 infection and autoimmunity. Autoimmun Rev 2008;8:116–20. [DOI] [PubMed] [Google Scholar]
  • [12].Mouthon L, Guillevin L, Tellier Z. Intravenous immunoglobulins in autoimmune-or parvovirus B19-mediated pure red-cell aplasia. Autoimmun Rev 2005;4:264–9. [DOI] [PubMed] [Google Scholar]
  • [13].Page C, François C, Goëb V, et al. Human parvovirus B19 and autoimmune diseases. Review of the literature and pathophysiological hypotheses. J Clin Virol 2015;72:69–74. [DOI] [PubMed] [Google Scholar]
  • [14].Pattison JR, Jones SE, Hodgson J, et al. Parvovirus infections and hypoplastic crisis in sickle-cell anaemia. Lancet 1981;1:664–5. [DOI] [PubMed] [Google Scholar]
  • [15].Yamada H, Tairaku S, Morioka I, et al. Nationwide survey of mother-to-child infections in Japan. J Infect Chemother 2015;21:161–4. [DOI] [PubMed] [Google Scholar]
  • [16].Wawina TB, Tshiani OM, Ahuka SM, et al. Detection of human parvovirus B19 in serum samples from children under 5 years of age with rash-fever illnesses in the Democratic Republic of the Congo. Int J Infect Dis 2017;65:4–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [17].Heegaard ED, Brown KE. Human parvovirus B19. Clin Microbiol Rev 2002;15:485–505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [18].Jia J, Ma Y, Zhao X, et al. Prevalence of human parvovirus B19 in Chinese plasma pools for manufacturing plasma derivatives. Virol J 2015;12:162–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [19].Puccetti C, Contoli M, Bonvicini F, et al. Parvovirus B19 in pregnancy: possible consequences of vertical transmission. Prenat Diagn 2012;32:897–902. [DOI] [PubMed] [Google Scholar]
  • [20].Corcoran A, Doyle S. Advances in the biology, diagnosis and host-pathogen interactions of parvovirus B19. J Med Microbiol 2004;53(pt 6):459–75. [DOI] [PubMed] [Google Scholar]
  • [21].Marano G, Vaglio S, Pupella S, et al. Human Parvovirus B19 and blood product safety: a tale of twenty years of improvements. Blood Transfus 2015;13:184–96. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [22].Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [23]. Available at: https://www.ncbi.nlm.nih.gov/books/NBK35156. Accessed on June 15, 2019. [Google Scholar]
  • [24].Hu J, Dong Y, Chen X, et al. Prevalence of suicide attempts among Chinese adolescents: a meta-analysis of cross-sectional studies. Compr Psychiatry 2015;61:78–89. [DOI] [PubMed] [Google Scholar]
  • [25].Feng L, Li L, Liu W, et al. Prevalence of depression in myocardial infarction: a PRISMA-compliant meta-analysis. Medicine (Baltimore) 2019;98:e14596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [26].Lipsey ML, Wilson DB. Practical Meta-analysis. Thousand Oaks, CA: Sage; 2001. [Google Scholar]
  • [27].Li SQ, Yan YS, Chen R, et al. Serological investigation on human parvovirus B19 infections in Fujian. Strai J Prev Med 2000;6:1–2. (Chinese). [Google Scholar]
  • [28].Wang R, Wu MH, Xue M, et al. Analysis of screening parvovirus B19 among blood donors with PCR. Jiangsu Health Care 2002;4:14–5. (Chinese). [Google Scholar]
  • [29].Yang ZX, He HJ, Dai F, et al. Investigation on HPV B19 infection in 110 blood donors. J Huazhong Univ Sci Tech 2003;32:344–5. (Chinese). [Google Scholar]
  • [30].Wei Q, Li Y, Wang JW, et al. Prevalence of anti-human parvovirus B19 IgG antibody among blood donors in Jilin province. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 2006;20:60–2. (Chinese). [PubMed] [Google Scholar]
  • [31].Li BD, Xie SG, Ning Y. The status investigation of blood donors who infect the human parvovirus B19 in Linyi City. Med Lab Sci Clin 2010;21:58–60. (Chinese). [Google Scholar]
  • [32].Zhang NH, Du ZL, Zhao YH. Epidemiological investigation of the human parvovirus B19 among blood donators in Luxi region of Shandong. Mod Prev Med 2009;36:17–8. (Chinese). [Google Scholar]
  • [33].Zheng YR, Li ZP, Liang HJ, et al. Epidemiological study on HPV B19 and viral load among volunteer blood donors in Guangzhou. Chin J Blood Transf 2009;22:549–51. (Chinese). [Google Scholar]
  • [34].Ke L, He M, Li C, et al. The prevalence of human parvovirus B19 DNA and antibodies in blood donors from four Chinese blood centers. Transfusion 2011;51:1909–18. [DOI] [PubMed] [Google Scholar]
  • [35].Liang LL, Ye XZ, Zhou HQ, et al. Expression of structural protein VP1 of human parvovirus B19 and preliminary development of indirect ELISA for IgM. Chin J Biol 2012;25:345–56. (Chinese). [Google Scholar]
  • [36].Hou JF, Wang M, Ma QP. Determination of human parvovirus B19 DNA in source plasma and blood products. Chin J Biol 2012;25:1043–8. (Chinese). [Google Scholar]
  • [37].Ling HS, Chu XT, Zeng MX. Development of an indirect enzyme linked immunosorbent assay for detecting IgM antibodies of human parvovirus B19. Lab Med Clin 2014;11:583–5. 588 (Chinese). [Google Scholar]
  • [38].Liu YB, Liang WW, Yu HL, et al. Human parvovirus B19 infection in blood donors of Yao nationality. Chin J Blood Transf 2014;27:306–7. (Chinese). [Google Scholar]
  • [39].Bao HE, Yang BJ, Pan XY, et al. A survey of human parvovirus B19 prevalence among blood donors in the Three Gorges Region. J Clin Hematol 2015;28:289–91. (Chinese). [Google Scholar]
  • [40].Han T, Li C, Zhang Y, et al. The prevalence of hepatitis A virus and parvovirus B19 in source-plasma donors and whole blood donors in China. Transfus Med 2015;25:406–10. [DOI] [PubMed] [Google Scholar]
  • [41].Qin WW, Liao HM, Tan XX, et al. Study on the infection status of human parvovirus B19 among unpaid blood donors in Chongqing. Chongqing Med 2015;44:4968–71. (Chinese). [Google Scholar]
  • [42].Wang ZX, Zhou BB, Zhang N, Huang HY. Research on human parvovirus B19 infection among blood donors in Jining. J Pub Health Prev Med 2015;26:4–7. (Chinese). [Google Scholar]
  • [43].Zheng RB, Yu Y. Testing and analysis of human parvovirus B19 gene in blood products. China Med Pharm 2015;5:151–3. (Chinese). [Google Scholar]
  • [44].Zeng FX, He PD, Li YJ, et al. Investigation of the prevalence of human parvovirus B19 DNA in source plasma. Chin J Blood Transfusion 2015;28:162–5. (Chinese). [Google Scholar]
  • [45].Ou SH, Xie JZ, Zhang YL, et al. Prevalence of parvovirus B19 infection in Chinese Xiamen area blood donors. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2016;24:1572–6. (Chinese). [DOI] [PubMed] [Google Scholar]
  • [46].Yan JX, Wu WJ, Zhou JX, et al. Human parvovirus B19 detection in voluntary blood donors of Foshan City. Int J Lab Med 2016;37:1039–43. (Chinese). [Google Scholar]
  • [47].Zhang L, Cai C, Pan F, et al. Epidemiologic study of human parvovirus B19 infection in East China. J Med Virol 2016;88:1113–9. [DOI] [PubMed] [Google Scholar]
  • [48].He M, Gao L, Ke L, et al. Phylogenetic study of human parvovirus B19 distributed in China based on bayesian inference and maximum likelihood analysis. Chin J Blood Transfusion 2011;24:399–402. (Chinese). [Google Scholar]
  • [49].Jia J, Ma Y, Zhao X, et al. Existence of various human parvovirus B19 genotypes in Chinese plasma pools: genotype 1, genotype 3, putative intergenotypic recombinant variants and new genotypes. Virol J 2016;13:155–64. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [50].Wu Y, Geng YS, Wang JZ, et al. The prevalence and genotype of human parvovirus B19 in blood products. Chin J Microbiol Immunol 2009;29:1031–4. (Chinese). [Google Scholar]
  • [51].Grabarczyk P, Korzeniowska J, Liszewski G, et al. Parvovirus B19 DNA testing in Polish blood donors. Przegl Epidemiol 2012;66:7–12. [PubMed] [Google Scholar]
  • [52].Schmidt M, Themann A, Drexler C, et al. Blood donor screening for parvovirus B19 in Germany and Austria. Transfusion 2007;47:1775–82. [DOI] [PubMed] [Google Scholar]
  • [53].Groeneveld K, van der Noordaa J. Blood products and parvovirus B19. Neth J Med 2003;61:154–6. [PubMed] [Google Scholar]
  • [54].Council of Europe. European Pharmacopoeia. 6th ed.2008;Strasbourg: Council of Europe Publishing, Human plasma (pooled and treated for virus inactivation), monograph 1646. [Google Scholar]
  • [55].Ma YY, Jia JT, Zhang JG. Detection and significance of human parvovirus B19 in blood and blood products. J Clin Transfusion Lab Med 2016;18:201–4. (Chinese). [Google Scholar]
  • [56]. Food and Drug Administration. Guidance for Industry: Nucleic Acid Testing (NAT) to Reduce the Possible Risk of Parvovirus B19 Transmission by Plasma-Derived Products. Available at: https://www.fda.gov/media/72156/download. Accessed October 10, 2019. [Google Scholar]
  • [57]. American Association of Blood Banks. Human Parvovirus B19. Available at: http://www.aabb.org/tm/eid/Documents/107s.pdf. Accessed on October 10, 2019. [Google Scholar]
  • [58].Satake M, Hoshi Y, Taira R, et al. Symptomatic parvovirus B19 infection caused by blood component transfusion. Transfusion 2011;51:1887–95. [DOI] [PubMed] [Google Scholar]
  • [59].Ihara T, Furusyo N, Hayashi T, et al. A population-based epidemiological survey of human parvovirus B19 infection: a project of the Kyushu and Okinawa Population Study (KOPS). Arch Virol 2013;158:2465–72. [DOI] [PubMed] [Google Scholar]
  • [60].Kumar S, Gupta RM, Sen S, et al. Seroprevalence of human parvovirus B19 in healthy blood donors. Med J Armed Forces India 2013;69:268–72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [61].Manaresi E, Gallinella G, MorselliLabate AM, et al. Seroprevalence of IgG against conformational and linear capsid antigens of parvovirus B19 in Italian blood donors. Epidemiol Infect 2004;132:857–62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [62].O’Bryan TA, Wright WF. Parvovirus B19 and C-reactive protein in blood bank donors: implications for hygiene hypothesis research. Lupus 2010;19:1557–60. [DOI] [PubMed] [Google Scholar]
  • [63].Candotti D, Etiz N, Parsyan A, et al. Identification and characterization of persistent human erythrovirus infection in blood donor samples. J Virol 2004;78:12169–78. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [64].Obeid OE. Molecular and serological assessment of parvovirus B19 infections among sickle cell anemia patients. J Infect Dev Ctries 2011;5:535–9. [DOI] [PubMed] [Google Scholar]
  • [65].Slavov SN, Kashima S, Silva-Pinto AC, et al. Genotyping of Human parvovirus B19 among Brazilian patients with hemoglobinopathies. Can J Microbiol 2012;58:200–5. [DOI] [PubMed] [Google Scholar]
  • [66].Blümel J, Burger R, Drosten C, et al. Parvovirus B19 - revised. Transfus Med Hemother 2010;37:339–50. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [67].Hübschen JM, Mihneva Z, Mentis AF, et al. Phylogenetic analysis of human parvovirus b19 sequences from eleven different countries confirms the predominance of genotype 1 and suggests the spread of genotype 3b. J Clin Microbiol 2009;47:3735–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [68].Bock CT, Düchting A, Utta F, et al. Molecular phenotypes of human parvovirus B19 in patients with myocarditis. World J Cardiol 2014;6:183–95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [69].Corcioli F, Zakrzewska K, Rinieri A, et al. Tissue persistence of parvovirus B19 genotypes in asymptomatic persons. J Med Virol 2008;80:2005–11. [DOI] [PubMed] [Google Scholar]
  • [70].Grabarczyk P, Kalińska A, Kara M, et al. Identification and characterization of acute infection with parvovirus B19 genotype 2 in immunocompromised patients in Poland. J Med Virol 2011;83:142–9. [DOI] [PubMed] [Google Scholar]
  • [71].Candotti D, Danso K, Parsyan A, et al. Maternal-fetal transmission of human parvovirus B19 genotype 3. J Infect Dis 2006;194:608–11. [DOI] [PubMed] [Google Scholar]
  • [72].Shi L, Wang J, Liu Z, et al. Blood donor management in china. Transfus Med Hemother 2014;41:273–82. [DOI] [PMC free article] [PubMed] [Google Scholar]

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