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1 Department of Molecular Pathology, Institute of Pathology, University Hospital of Tübingen, 72076 Tübingen, Germany
2 Department of Parasitology, Institute of Tropical Medicine, University of Tübingen, Germany
3 Medical Research Unit, Albert Schweitzer Hospital, Lambarene, Gabon
4 Tran Hung Dao Hospital, Hanoi, Vietnam
5 Department of Pediatric Oncology, Children's Hospital, University of Tübingen, Germany
6 354 Hospital, Hanoi, Vietnam
7 Department of Medicine, Victorian Infectious Diseases Service, Centre for Clinical Research Excellence, Royal Melbourne Hospital, The University of Melbourne, Australia
Correspondence
C.-Thomas Bock
thomas.bock{at}med.uni-tuebingen.de
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the nucleotide sequences of B19 samples determined in this study are DQ357064 (V147) and DQ357065 (V115).
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Parvoviruses are non-enveloped and are amongst the smallest DNA-containing viruses that are capable of infecting mammalian cells (Heegaard & Brown, 2002). B19 has a diverse spectrum of clinical manifestations, including erythema infectiosum, hydrops fetalis, aplastic anaemia (Anderson et al., 1983; Young & Brown, 2004), arthritis (Takahashi et al., 1998; Moore, 2000), myocarditis (Bültmann et al., 2003; Bock et al., 2005; Tschöpe et al., 2005; Bock, 2006), vasculitic syndromes (Finkel et al., 1994; Dingli et al., 2000), neurological disorders (Barah et al., 2001) and hepatic inflammation (Naides et al., 1996; Yoto et al., 1996; Hillingsø et al., 1998; Karetnyi et al., 1999; He et al., 2003).
The genome of B19 consists of a linear, single-stranded DNA molecule of about 5600 nt (Morinet, 1992; Zhi et al., 2004), which contains three open reading frames encoding the non-structural protein NS1 (77 kDa) and the two structural proteins VP1 (84 kDa) and VP2 (58 kDa) (Cotmore et al., 1986). Genetic diversity among B19 strains has been shown to be very low, with <1–2 % nucleotide divergence of the full-length sequences. Partial sequence data from different coding regions of the viral genome have confirmed a slightly higher degree of variability with a larger number of strains from distinct epidemiological settings and geographical areas (Erdman et al., 1996). However, some B19 strains obtained from patients with persistent infection show a higher degree of variability, particularly in the VP1-unique (VP1u) region, demonstrating 4 and 8 % divergence at the DNA and protein levels, respectively (Hemauer et al., 1996; Gallinella et al., 2003). Fukada et al. (2000) reported four putative subtypes of B19 based on the amino acid substitutions of 10 isolates in Japan. Their study indicated that a total of 122 mutation sites in a 4145 nt fragment were found in 11 isolates, including the previously published B19-au strain, of which 24 were accompanied by amino acid substitution (Fukada et al., 2000).
Currently, three distinct genotypes of B19 have been identified by >10 % nucleotide divergence (Servant et al., 2002). Genotype 1 is thought to be the most common genotype worldwide, whereas genotype 2 has been reported in patients from several European countries, the United States and Brazil (Nguyen et al., 2002; Liefeldt et al., 2005; Sanabani et al., 2006). Genotype 3 has been detected in patients from France and Brazil, as well as in blood-donor samples from Ghana (Servant et al., 2002; Candotti et al., 2004; Sanabani et al., 2006).
In this study, we have investigated the distribution of B19 genotypes in individuals from Vietnam. Phylogenetic analysis of the subgenomic NS1/VP1u region and the coding NS1, VP1 and VP2 regions demonstrated that two genotypes of B19 (1 and 2) were detected in this cohort, with a predominance of genotype 1. Additionally, we have shown that genotype 1 can be classified into at least two subgroups.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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, 2004; Toan et al., 2006). From these, 49 randomly selected B19-positive serum samples were analysed further by DNA sequencing. Additionally, 64 healthy Vietnamese individuals were included as controls. Patients were enrolled at Tran Hung Dao Hospital, Bach Mai Hospital, 103 Military University Hospital, Hanoi, Vietnam, in 2000 and 2002.
PCR.
The detection of B19 DNA by nested PCR (nPCR) using primers specific for the VP1/VP2 coding sequence has been described previously (Bültmann et al., 2003). All samples testing positive for B19 were confirmed in duplicate with a second PCR, which was different from the first PCR in order to exclude contamination, using B19 primers (P5F and P5R for the first PCR and n-P5F and n-P5R for nPCR; Table 1) specific for the subgenomic NS1/VP1u region from nt 2355 to 2690 (numbering according to GenBank accession no. AF162273
[GenBank]
). Sample processing (DNA extraction, template preparation, spinning and aliquotting, mastermix preparation) and PCR amplication were done in separate laboratory rooms that were all certified for molecular diagnostics and especially for PCR, using standard precautions to prevent assay contamination.
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). The specificity and sensitivity of the B19 qPCR were determined by using the WHO international standard for B19 DNA (NIBSC Code 99/800; http://www.who.int/bloodproducts/publications/IFU_00-928.pdf) and B19-negative control plasmids. In order to standardize the qPCR, increasing dilutions of B19 plasmid DNA (3.5x104–3.5x101 genomes per qPCR) were included to demonstrate the sensitivity of the qPCR. All samples were analysed in duplicate.
DNA sequence analysis.
DNA fragments spanning the coding NS1/VP1/VP2 region ranging from nt 602 to 5014 (4413 nt; numbering according to GenBank accession no. AF162273
[GenBank]
) were amplified by nPCR using primer pairs as indicated in Table 1
for six B19 DNA-positive samples. To obtain the entire sequence, the first PCR was carried out for 35 cycles (94 °C for 30 s, 48 °C for 30 s, 72 °C for 45 s), and 40 cycles (94 °C for 30 s, 50 °C for 30 s, 72 °C for 45 s) were used for nPCR. The sequencing reaction was performed with 1–5 µl purified PCR product with 2 µl BigDye Terminator cycle sequencing mix (Perkin Elmer) and 15 pmol primers (Table 1). The PCR products were sequenced twice using the forward and reverse primers described in Table 1. The n-P5F and n-P5R specific primers (Table 1) were used for sequencing of a fragment of the NS1/VP1u region from nt 2355 to 2690 (numbering according to GenBank accession no. AF162273
[GenBank]
) for 49 B19 DNA-positive samples. The DNA sequences were analysed on an ABI Prism Genetic Analyser 3100C (Applied Biosystems). All samples were analysed in duplicate.
B19 genotype analysis.
B19 sequences were aligned by using CLUSTAL_W (Thompson et al., 1994) and BLAST (National Center for Biotechnology Information; http://www.ncbi.nlm.nih.gov/blast/blast.cgi). The reliability of alignment was additionally checked by using the BioEdit program (Department of Microbiology, North Carolina State University, Raleigh, NC, USA; http://www.mbio.ncsu.edu/BioEdit/bioedit.html). Genetic distances were calculated by using the Kimura two-parameter method (Kimura, 1980) and phylogenetic trees were constructed by the neighbour-joining method (Saitou & Nei, 1987). The results of phylogenetic trees were visualized by using TreeView v. 1.6.6 (http://taxonomy.zoology.gla.ac.uk/rod/treeview.html). Prototype B19 sequences from GenBank were used as reference sequences (GenBank accession numbers were as follows: genotype 1, AB030694
[GenBank]
, AF113323
[GenBank]
, AF162273
[GenBank]
, M13178
[GenBank]
, DQ225148
[GenBank]
, DQ225149
[GenBank]
, DQ225150
[GenBank]
and DQ225151
[GenBank]
; genotype 2, AY064476
[GenBank]
, AY044266
[GenBank]
, AY661663
[GenBank]
and AY661664
[GenBank]
; genotype 3, AX003421
[GenBank]
and AY083234
[GenBank]
).
Statistical analysis.
Statistical analysis was performed by using the 
2 test (available at www.stata.com) and the non-parametric Mann–Whitney U test or Kruskall–Wallis test using STATVIEW, version 4.57 (available at www.statview.com).
Ethical approval.
The study was approval by the Institutional Review Board of Hanoi University of Medicine, Hanoi, Vietnam, and the Institutional Review Board of the Tran Hung Dao Hospital, Hanoi, Vietnam.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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]. The calculated viral loads from qPCR demonstrated viral titres of B19 DNA in the samples of patients ranging from 102 to 104 B19 copies ml–1. Sequence analyses of partial NS1/VP1u amplicons revealed nucleotide variations of the B19 sequences when compared with each other, thereby excluding cross-contamination of patient samples with B19. There was no significant difference in the B19 viral load in serum across the different HBV-infected groups (P>0.05; data not shown). B19 DNA-positive patients were tested for B19 antibodies. Anti-B19-IgG(+)IgM(–) were identified in 78.4 %, anti-B19-IgG(+)IgM(+) in 4.5 % and anti-B19-IgG(–)IgM(+) in 9.1 % of B19 DNA-positive patients, representing persistent, recent or reactivated and acute B19 infection, respectively (Toan et al., 2006).
Distribution of B19 genotypes in the Vietnamese population
Three genotypes (1, 2 and 3) of B19 have been identified (Servant et al., 2002). B19 genotype 1 seems to be the most common genotype worldwide. In order to analyse the distribution of B19 genotypes in Vietnamese patients with HBV infections, we randomly analysed 49 B19 DNA-positive samples identified from the 399 HBV-infected patients. Sequencing analysis of the subgenomic NS1/VP1u region showed that both genotypes 1 and 2 of B19 were present in Vietnamese patients. However, B19 genotype 1 was more frequent than genotype 2 [47 of 49 (96 %) vs 2 of 49 (4 %)], whilst B19 genotype 3 was not detected in this population (Fig. 1).
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). To confirm two major branches within genotype 1, the 4413 nt sequence of the coding NS1/VP1/VP2 region (nt 602–5014) of B19 was analysed for two B19 sequences from Vietnam. For sequencing, the 4413 nt sequence was divided into 10 overlapping sections (Table 1). The 10 overlapping parts of the sequences were linked with each other to give the sequence of 4413 nt, which covers the complete NS1, VP1 and VP2 regions of the B19 genome. Molecular genetic analysis based on the coding NS1/VP1/VP2 region of two B19 strains (V147 and V115) from Vietnam and 11 reference sequences from GenBank revealed the existence of two major groups within genotype 1 (Fig. 2a). Similar clusters were also observed by analyses of the single NS1, VP1 and VP2 regions (Fig. 2b, c and d, respectively). From these results, we propose two subgroups within B19 genotype 1: subgroup A (B19-1A) for isolates reported previously and infrequently in this study, and subgroup B (B19-1B) for strains predominantly detectable in Vietnam.
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). In accordance with these results, analysis of the single regions of the NS1, VP1 and VP2 genes showed that the nucleotide divergence between B19-1B (V147 and V115) and B19-1A (GenBank accession numbers M13178
[GenBank]
, AF113323
[GenBank]
and DQ225148
[GenBank]
–DQ225151
[GenBank]
) was >5 % (6 %, NS1; 5–6 %, VP1 and VP2). However, the nucleotide difference between B19-1B and genotypes 2 and 3 was >10 % (15–16 %, NS1; 10–11 %, VP1; 13 %, VP2) and 12 % (17 %, NS1; 13 %, VP1; 14–15 %, VP2), respectively (Table 3). The above results, together with the nucleotide divergences in the coding NS1/VP1/VP2 region (nt 602–5014) and the region NS1, VP1 and VP2 genes, support the concept that B19-1A and B19-1B belong to genotype 1 and that they can be considered as separate subgroups within this genotype.
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; Fig. 3a, b). The mean percentage of amino acid variations between B19-1B (V147 and V115) and B19-1A (B19-au, M13178
[GenBank]
) was >2 %: 4–5 % (NS1), 2–3 % (VP1) and 2–3 % (VP2) (Table 3; Fig. 3a, b). As compared with the B19-A6 variant (genotype 2, GenBank accession no. AY064476
[GenBank]
), the B19-1B (V147 and V115) amino acid sequence difference was 8–9, 5–6 and 4 %. Additionally, amino acid divergence between B19-1B (V147 and V115) and the B19 V9 variant (genotype 3, GenBank accession no. AX003421
[GenBank]
) was >3 %: 8–9 % (NS1), 5 % (VP1) and 3–4 % (VP2) (Table 3; Fig. 3a, b). The NS1 region contains highly conserved motifs found in a variety of parvoviruses (Bergoin & Tijssen, 1998). These include the replication-initiator motifs I and II (aa 79–147; Sukhumsirichart et al., 2006) and the NTP-binding and helicase domains A, B, B' and C (aa 320–416; Walker et al., 1997). The alignment of our B19-1B strains failed to reveal point mutations within these regions, with the exception of the B19 strain V147, which demonstrated a tryptophan to glycine substitution at aa 325 (W325G; Fig. 3a). Also, analysis of the VP1u region, which contains a highly conserved domain representing the B19 phospholipase A2-like activity region (vPLA2) spanning aa 130–195 (Dorsch et al., 2002), showed no mutations (Fig. 3b). With the exception of strain V147, which demonstrated a glutamine to histidine substitution at aa 595 (Q195H; Fig. 3b), sequence analysis of the receptor-binding site of B19, which is located in the VP1/2 region (aa 577–677; globoside-binding motif) of B19-1B, also failed to reveal any mutations.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Genotype 1 seems to be the most common genotype worldwide, whereas genotype 2 is found rarely, in several European countries, including Finland (Hokynar et al., 2002) and Germany (Liefeldt et al., 2005), in the USA (Nguyen et al., 2002) and in Brazil (Sanabani et al., 2006). In contrast, detection of genotype 3 of B19 has been mainly limited to France (Servant et al., 2002), Ghana (Candotti et al., 2004) and Brazil (Sanabani et al., 2006). In this study, we have determined the distribution and genetic characterization of B19 genotypes from 49 B19-infected Vietnamese patients with HBV co-infection. By using phylogenetic analysis, we identified both B19 genotypes 1 and 2, but not genotype 3, in this population. In accordance with previous studies (Servant et al., 2002; Candotti et al., 2004), we found that B19 genotype 1 was predominantly observed in Vietnam. Interestingly, B19 genotype 2 was also found in Vietnamese patients with HBV infections (4 %).
Previous studies have indicated that B19 sequences show a low degree of genetic diversity among B19 strains (<2 %), but a higher degree of variability among viral strains from distinct epidemiological settings and geographical areas (Erdman et al., 1996). In this study, we have analysed 49 sequences of the B19 NS1/VP1u region and combined the sequence results with recently published human B19 sequences, with results indicating that 37 B19 sequences from Vietnam were more diverse than others within genotype 1 and that they clustered in two different branches of genotype 1. Phylogenetic analysis of the coding NS1/VP1/VP2 region and the single NS1, VP1 and VP2 genes revealed the existence of two major subgroups within genotype 1 (Fig. 2a–d). Additionally, the mean percentage of nucleotide divergence between two subgroups within genotype 1 of B19 was 5–6 % and intragenotypic differences in each subgroup were <2 %. Therefore, genotype 1 of B19 detected in our study can be classified into at least two subgroups, which we designated B19-1A and B19-1B. Interestingly, B19-1B was found predominantly in Vietnamese patients, whilst B19-1A was frequent in recently published B19 sequences and also in patients from Vietnam. Fukada et al. (2000) showed four subtypes (A–D) of B19 based on the amino acid substitutions of 10 B19 isolates in Japan. Their report showed that, in the 4145 nt studied, 122 mutation sites were found in these B19 isolates, of which 24 were accompanied by amino acid substitution.
The coding regions of the NS1, VP1 and VP2 genes for the proteins of B19-1B (V147 and V115) present no insertions, deletions or additional stop codons (Fig. 3). The gene encoding the NS1 protein turned out to be more divergent than the genes encoding the capsid proteins VP1 and VP2. As expected, at the protein level, the NS1 region was most divergent, whilst the major capsid protein VP2 showed differences of 2 and 3 % compared with the prototype B19-au (GenBank accession no. M13178
[GenBank]
). Analysis of the NS1 region, which contains highly conserved functional motifs, of the VP1u region with its vPLA2 activity and of the VP2 region with its globoside-binding motif revealed no mutations. However, the V147 strain did show mutations W325G in the NS1 and Q195H in the VP1 regions (Fig. 3b). Previous studies have suggested that mutations at these positions have no functional significance (Walker et al., 1997; Sukhumsirichart et al., 2006).
In summary, our study is the first to show the distribution of B19 genotypes in Vietnamese patients with HBV infections and also demonstrates that two of three genotypes of B19 are detectable in this cohort, with predominance of genotype 1. Furthermore, we have shown the existence of at least two subgroups within genotype 1 of B19, designated B19-1A and B19-1B, with B19-1B predominating in Vietnamese patients with HBV infections. Conserved amino acid sequences between each subgroup were identified. Further studies are needed in order to evaluate the biological significance of the new subgroups of B19 genotype 1.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 16 March 2006;
accepted 21 June 2006.
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