Indan Journal of Medical Research Indan Journal of Medical Research Indan Journal of Medical Research Indan Journal of Medical Research
  Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login  
  Home Print this page Email this page Small font sizeDefault font sizeIncrease font size Users Online: 364       

   Table of Contents      
REVIEW ARTICLE
Year : 2018  |  Volume : 147  |  Issue : 3  |  Page : 239-247

Genotypes of erythrovirus B19, their geographical distribution & circulation in cases with various clinical manifestations


1 Department of Microbiology, K.G. Medical University, Lucknow, India
2 Former Vice-Chancellor, K.G. Medical University, Lucknow, India

Date of Submission09-Nov-2016
Date of Web Publication18-Jun-2018

Correspondence Address:
Dr Amita Jain
Department of Microbiology, K.G. Medical University, Lucknow 226 003, Uttar Pradesh
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmr.IJMR_1816_16

Rights and Permissions
   Abstract 

Erythrovirus B19 (B19V) is one of the erythroviruses known to be pathogenic in humans. B19V is classified into three distinct genotypes; 1, 2 and 3, differing from each other by 2-13 per cent. Genotype 1 consists of the prototype B19V isolates, genotype 2 comprises the A6, LaLi and their related isolates while genotype 3 includes the V9- and V9-related isolates. The classification of genotype 1 into two subtypes (1A and 1B) and genotype 3 into two subtypes (3a and 3b) with an estimated nucleotide difference of about 5 per cent has been done. Predominance of genotype 1 across all the continents is seen followed by genotypes 2 and 3. There are no disease-specific genotypes. All the three genotypes have been found in symptomatic as well as asymptomatic individuals and have been reported from several countries across the world. The prevalence of genotype 2 in older populations and its absence from current circulation in Northern Europe has also been reported. The present review focuses on geographic distribution and association of genotypes of B19V with different clinical manifestations.

Keywords: B19V - B19V genotypes - erythroviruses - geographical distribution - parvovirus - parvovirus B19


How to cite this article:
Jain A, Kant R. Genotypes of erythrovirus B19, their geographical distribution & circulation in cases with various clinical manifestations. Indian J Med Res 2018;147:239-47

How to cite this URL:
Jain A, Kant R. Genotypes of erythrovirus B19, their geographical distribution & circulation in cases with various clinical manifestations. Indian J Med Res [serial online] 2018 [cited 2019 Jul 18];147:239-47. Available from: http://www.ijmr.org.in/text.asp?2018/147/3/239/234604


   Introduction Top


Erythrovirus B19 (B19V) is a rather recently discovered virus, which has been associated with a spectrum of diseases, including erythema infectiosum in children (fifth disease), acute or chronic arthropathy in adults, transient aplastic crisis in patients with chronic haemolytic anaemia, persistent anaemia in immunodeficient/immunocompromised patients, and foetal hydrops in pregnant women [1]. Many genotypes of B19V (genotypes 1-3) are circulating; however, a comprehensive review on their geographic distribution and their association with different clinical manifestation is lacking. Therefore, the present review was written with a focus on geographic distribution and association of genotypes of B19V with different clinical manifestations.

Members of the family Parvoviridae are among the smallest known DNA-containing viruses that infect mammalian cells (Parvum 'small'; Latin). The Parvoviridae family contains many viruses which are pathogenic to animals, and erythovirus B19 (B19V) is one of them. B19V is also one of the best-characterized members and is classified as a member of the Erythroparvovirus genus. Family Parvoviridae is divided into two subfamilies; Parvovirinae and Densovirinae. The Parvovirinae is further subdivided into eight genera, Protoparvovirus (previously known as Parvovirus), Dependoparvovirus, Erythroparvovirus, Bocaparvovirus, Amdoparvovirus, Aveparvovirus, Copiparvovirus and Tetraparvovirus. At least four different parvoviruses are known to infect humans: Parvovirus B19, human adeno-associated viruses (dependoparvoviruses), human bocaparvovirus (HBoV) and human Parv4 virus (a member of the newly created Tetraparvovirus genera)[2].

B19V was discovered in 1975, in the serum samples of normal human individuals, during evaluation of assays for hepatitis B surface antigen using panels of serum samples [3]. Sample 19 in panel B (hence B19) gave a 'false positive' result in relatively insensitive counter immunoelectrophoresis assay. The precipitin line under electron microscopy showed 23 nm particles resembling parvoviruses [3]. Association of B19V infection with human diseases was first time made in 1981[4], and was subsequently identified in several experimental and seroepidemiologic studies [5],[6]. B19V was identified as the causative agent of fifth disease (erythema infectiosum), common childhood exanthema and a polyarthralgia syndrome in adults [7],[8]; transient aplastic crisis in patients with underlying haemolysis [4]; and spontaneous abortion [9]. Role of B19V in liver manifestations and hepatitis is also known [10].

Although originally labelled as human parvovirus, the virus was officially recognized as a member of the family Parvoviridae in 1985, and the International Committee on Taxonomy of Viruses recommended the name B19V to avoid confusion with other viruses [2]. Parvovirus forms small icosahedral capsids of about 25 nm. The genome size of B19V is small, consisting of a single strand of DNA of approximately 5600 nucleotides, with identical 365 nucleotide long inverted terminal repeat sequences at each end [11].


   Genotypes of Human Erythrovirus Top


It was only about till three decades ago when researchers realized that genetic variations among parvoviruses exist. Since 2000, many B19V genotypic variants have been reported which vary extensively from the prototype B19V with respect to genomic sequence, exhibiting >13 per cent divergence versus the <2 per cent divergence in characteristic of previously characterized prototype B19V isolates [12],[13],[14],[15].

In the first effort of genotyping parvoviruses, the genome of 17 strains of the human parvovirus B19V was compared after restriction with eight endonucleases. All but four strains proved indistinguishable [16]. Following this study, another study from Japan used DNA fingerprinting to demonstrate that the strains of parvoviruses circulating during 1981 were different from the strains circulating during 1986-1987[17]. Based on further studies and phylogenetic analysis, the B19V was classified into three distinct genotypes [12],[13],[14]. Genotype 1 consists of all the prototype B19V isolates, A6, LaLi and their related isolates are included in genotype 2[18],[19],[20], and genotype 3 is composed of V9 and V9-related isolates [20],[21].

Further, phylogenetic analyses revealed two subgroups within both genotypes 1 and 3. The analysis of 13 nearly full-length genotype 3 sequences from Ghana, Europe and Brazil identified two genetically distinct clusters, following which the classification of genotype 3 into two subtypes (3a and 3b) was made [22]. Rate of evolutionary change in strains of B19V genotype 3 (2 × 10−4 nucleotide substitutions per site per year) was similar to that of other B19V genotypes. The estimated divergence time between 3a and 3b was 525 years. Subtype 3a was predominant in Ghana [22].

B19V genomes from Vietnam showed two major subgroups within genotype 1 (1A and 1B) with an estimated nucleotide difference of >5 per cent between each subgroup. The mean percentage of amino acid variation in NS1, VP1 and VP2 proteins, between both subgroups was >2 per cent [23].

Reported nucleotide and amino acid changes among various genotypes are summarized in [Table 1]. The most striking variation was observed within the promoter area (~20%). Within the NS1 gene, sequence divergence between genotypes 1, 2 and 3 was about 13 per cent at the nucleotide level. The two identical terminal repeats (ITRs) of approximately 365 nucleotides seen in B19V genotype 1 genome are imperfect palindromes and form hairpin loops. The terminal repeats of genotypes 2 and 3 have not been yet cloned and sequenced [15],[24],[25]. The sequence of a human erythrovirus, termed V9, was markedly distinct (>11% nucleotide divergence) from that of B19V [27]. One V9-related strain (D91.1) with 5.3 per cent divergence from V9 and 13.8-14.2 per cent divergence to prototype B19V sequences was reported [26]. A6, a new atypical parvovirus sequence, exhibited 88 per cent similarity to prototype B19V and 92 per cent similarity to V9, compared to >98 per cent similarity between earlier reported B19V strains [26]. K71, a new B19V genotype, is carried in human skin and differs from prototype B19V by 10.8 and 8.6 per cent within protein-coding regions and non-coding region (covering nucleotides 189-435 of the promoter region) respectively, while divergence from V9 variant was 26.5 and 17.2 per cent within protein-coding regions and non-coding region (covering nucleotides 189-435 of the promoter region), respectively [12]. The amino acid sequence of A6 and V9 variants in NS1 protein diverges from that of the B19 V prototype-encoded counterpart by 6.2 and 6.1 per cent, respectively [24],[25]. Within the open reading frame encoding the VP1/2 proteins, genotypes 2 and 3 differ from the prototype B19V by 9 and 12 per cent, respectively, at the nucleotide level. However, at the amino acid level the difference is much less, 1.1 and 1.4 per cent. Genotypes 2 and 3 differ from genotype 1 by 4.4 and 6.6 per cent, respectively in the VP1 unique region (uVP1). uVP1 gene containing the reported phospholipase 2 activities (amino acids 130-195) is highly conserved, and variation is mostly seen in the N termini [24],[25]. The capsid protein sequence is conserved between the different genotypes, in spite of differences in the DNA sequences, as there is enough evidence in serologic and cross-neutralization reactions [28],[29],[30].
Table 1: Nucleotide and amino acid variance among different genotypes of B19V

Click here to view



   Persistence of B19V in Human Tissues and Distribution of B19V Genotypes Top


Several studies have suggested that after primary infection, in both symptomatic and asymptomatic subjects [31],[32],[33] and in both immunocompromised and immunocompetent hosts [34] the erythroviral genomic DNA is detectable in tissues. The genotype 1 replicates restrictively in the erythroid progenitors of human bone marrow producing high viral load viraemia [11],[29]. In contrast, high virus-load viraemia of genotypes 2 and 3 has been identified only occasionally [13],[14],[30],[35]. Manning et al[34] discussed the persistence of B19 in human tissues in immunocompetent hosts. A study by Norja et al[36] done on a large number of human tissues including synovial, skin, tonsil and liver tissues and human serum samples concluded, “erythrovirus genome persistence in human tissues is ubiquitous and lifelong and represents an entity, named the Bioportfolio, which indicates that the newly discovered virus type 2 was actually 'older' in occurrence in Central and Northern Europe than the virus prototype and that the type 3 never attained wide circulation in the area during the 70 years observation period from the 1930s to the present day”. However, in north India, genotype 3 has been detected in cases of cardiomyopathy [37] and solid tumors [38]. This analysis signifies that the distribution of genotypes is geographically restricted and distribution may change with time. Manning et al[34] also maintained that B19V genotype 2 was more commonly seen in older study subjects, while B19V genotype 1 was commonly seen in younger subjects. Studies published from Germany, Italy and Finland, after 2007 demonstrated presence of all the three genotypes 1, 2 and 3, both in patients and asymptomatic controls. Genotype 2 was also demonstrated in blood and tissue biopsies [39],[40],[41],[42],[43]. One study from South Africa detected genotype 2 from serum of a child providing evidence for its circulation [44].

Only a single serotype of B19V is suggested as seen by 100 per cent cross-reactivity of antibodies among these three genotypes [45].


   Geographical Distribution of Circulating Genotypes in Various Countries Top


Many studies have reported genotypes of B19V in human infections. [Table 2] summarizes the studies with genotypic details of B19V. Studies are available from Europe, Asia, South America and Africa. Very limited or no data are available from North America and Australia. [Table 3] shows the number and frequencies of total strains which have been genotyped from each geographical area. Only those continents from where more than three studies were available, are included in analysis.
Table 2: Prevalence of B19V genotypes as reported by different studies

Click here to view
Table 3: Frequencies of human erythrovirus B19 genotypes in different continents

Click here to view


Europe

Genotype 1 was most frequently seen (61.64%), followed by genotype 2 (36.73%) and genotype 3 (1.62%) [Table 3]. In most of studies from Germany, done on cases of cardiomyopathy, either genotype 1 or genotype 2 was detected [39],[40],[43],[44], with occasional reports of genotypes 3[47]. Studies done on transplant recipients [41], patients with hepatitis [46] and dilated cardiomyopathy [47] from Germany, showed presence of all the three genotypes, although genotype 1 was predominant. Predominantly genotypes 1 and 2[49],[69] were reported from Italy with occasional reports of genotypes 3 from two asymptomatic individuals [48]. Of the six B19V positive transplant recipients, one was positive for active infection with genotype 1 and genotype 5 was either reactivation or re-infection of genotype 2[51] as reported from France. In a landmark study from France, where both prospective and retrospective samples collected during 1972-2001, were analyzed, mainly genotype 1 was detected. Genotype 3 was detected (~11%) in samples collected during 1999-2001[14]. In a single study from Poland, genotype 3 was not found [50]. Studies from the UK [34] and Finland [42] demonstrated only genotype 1. In a study from Bulgaria, genotype 2 was not demonstrated [52].

Asia

Studies are available from many countries including China, India, Russia, Korea, Vietnam and Iran; however, no large-scale studies on B19V genotypes are available. Based on the available data, genotype 1 is most commonly reported genotype (95.7%), while genotype 2 (1.4%) and genotype 3 (2.9%) have been occasionally reported [Table 3]. Studies done in Vietnam [53] reported that majority of strains were genotype 1 with occasional reports of genotype 2. Genotype 3 was not reported from any other countries in Asia, except India, from where only occasional reports are available; however, genotype 2 was never reported from India [58]. In studies done from Iran [59], China [55],[56], Russia [57], Korea [60] and Thailand [54] only genotype 1 was reported. In north India genotype 3 was detected in cases of cardiomyopathy [37], and solid tumors [38].

South America

Only one study from Brazil, which was published on cases with haematological disorders, reported a single strain of genotype 2[20]. Based on available reports, genotypes 1 and 3 are present in frequencies of 87.94 and 11.70 per cent, respectively [Table 3]. Some of the studies showed prevalence of both genotype 1 (commonly) and genotype 3 (rarely)[61],[65],[66], while other studies showed the prevalence of genotype 1 only [62],[64],[67].

Africa

Genotype 1 has been most frequently reported (66.4%), followed by genotype 3 (22.1%) and genotype 2 (11.5%) [Table 3]. In a study done on pregnant women, predominantly genotype 3 was reported with occasional prevalence of genotype 1[67], while another study reported all the three genotypes [44]. Genotype 3 was not reported in studies from Gabon [51] and Nigeria [68].

North America

In a study from the USA [70] done on cases of cardiomyopathy genotype 3 was not detected. Majority of the strains were genotype 1 with occasional presence of genotype 2. In another study 204 strains from the USA were genotyped retrospectively and all of them were genotype 1[14].


   Erythrovirus B19 Genotypes and Their Associations with Diseases Top


As shown in [Table 4], prevalence of each genotype among various clinical groups varied significantly. Since genotype 1 was the most commonly reported genotype, its predominance in most of the clinical situations was also noticed except in individuals with cardiac manifestations, where genotype 2 was predominantly reported [Table 4]. The site of virus detection (various tissues or blood) varied from study to study. All the three genotypes have been detected in different proportions from cases presenting with different clinical manifestations, for example, anaemia, aplastic crisis, erythema infectiosum, arthropathy and cardiomyopathy. All the three genotypes have been found in symptomatic as well as normal individuals [Table 4].
Table 4: Frequency of human erythrovirus B19 genotypes in various clinical conditions

Click here to view



   Conclusion Top


B19V is classified into three distinct genotypes 1, 2 and 3, differing from each other by 2-13 per cent. The classification of genotype 3 strains into two subtypes (3a and 3b) and genotype 1 into two subtypes (1A and 1B) has been made. Predominance of genotype 1 across all the continents is seen followed by genotypes 2 and 3. There are no disease-specific genotypes and association of genotypes with clinical manifestations has not yet been established. All the three genotypes have been found in symptomatic as well as asymptomatic individuals and have been reported from several countries across the world. The prevalence of genotype 2 in older populations and its absence from the current circulation in Northern Europe has been reported.

Financial support & sponsorship: None.

Conflicts of Interest: None.



 
   References Top

1.
Young NS, Brown KE. Parvovirus B19. N Engl J Med 2004; 350 : 586-97.  Back to cited text no. 1
[PUBMED]    
2.
Cotmore SF, Agbandje-McKenna M, Chiorini JA, Mukha DV, Pintel DJ, Qiu J, et al. The family parvoviridae. Arch Virol 2014; 159 : 1239-47.  Back to cited text no. 2
[PUBMED]    
3.
Cossart YE, Field AM, Cant B, Widdows D. Parvovirus-like particles in human sera. Lancet 1975; 1 : 72-3.  Back to cited text no. 3
[PUBMED]    
4.
Pattison JR, Jones SE, Hodgson J, Davis LR, White JM, Stroud CE, et al. Parvovirus infections and hypoplastic crisis in sickle-cell anaemia. Lancet 1981; 1 : 664-5.  Back to cited text no. 4
    
5.
Anderson MJ, Lewis E, Kidd IM, Hall SM, Cohen BJ. An outbreak of erythema infectiosum associated with human parvovirus infection. J Hyg (Lond) 1984; 93 : 85-93.  Back to cited text no. 5
[PUBMED]    
6.
Anderson MJ, Higgins PG, Davis LR, Willman JS, Jones SE, Kidd IM, et al. Experimental parvoviral infection in humans. J Infect Dis 1985; 152 : 257-65.  Back to cited text no. 6
[PUBMED]    
7.
Reid DM, Reid TM, Brown T, Rennie JA, Eastmond CJ. Human parvovirus-associated arthritis: A clinical and laboratory description. Lancet 1985; 1 : 422-5.  Back to cited text no. 7
[PUBMED]    
8.
White DG, Woolf AD, Mortimer PP, Cohen BJ, Blake DR, Bacon PA, et al. Human parvovirus arthropathy. Lancet 1985; 1 : 419-21.  Back to cited text no. 8
    
9.
Brown T, Anand A, Ritchie LD, Clewley JP, Reid TM. Intrauterine parvovirus infection associated with hydrops fetalis. Lancet 1984; 2 : 1033-4.  Back to cited text no. 9
[PUBMED]    
10.
Bihari C, Rastogi A, Saxena P, Rangegowda D, Chowdhury A, Gupta N, et al. Parvovirus b19 associated hepatitis. Hepat Res Treat 2013; 2013 : 472027.  Back to cited text no. 10
[PUBMED]    
11.
Ozawa K, Ayub J, Hao YS, Kurtzman G, Shimada T, Young N, et al. Novel transcription map for the B19 (human) pathogenic parvovirus. J Virol 1987; 61 : 2395-406.  Back to cited text no. 11
    
12.
Hokynar K, Brunstein J, Söderlund-Venermo M, Kiviluoto O, Partio EK, Konttinen Y, et al. Integrity and full coding sequence of B19 virus DNA persisting in human synovial tissue. J Gen Virol 2000; 81 : 1017-25.  Back to cited text no. 12
    
13.
Hokynar K, Söderlund-Venermo M, Pesonen M, Ranki A, Kiviluoto O, Partio EK, et al. A new parvovirus genotype persistent in human skin. Virology 2002; 302 : 224-8.  Back to cited text no. 13
    
14.
Servant A, Laperche S, Lallemand F, Marinho V, De Saint Maur G, Meritet JF, et al. Genetic diversity within human erythroviruses: Identification of three genotypes. J Virol 2002; 76 : 9124-34.  Back to cited text no. 14
[PUBMED]    
15.
Servant-Delmas A, Laperche S, Mercier M, Lefrère JJ. Genetic diversity of human erythroviruses. Pathol Biol (Paris) 2009; 57 : 167-74.  Back to cited text no. 15
    
16.
Morinet F, Tratschin JD, Perol Y, Siegl G. Comparison of 17 isolates of the human parvovirus B 19 by restriction enzyme analysis. Brief report. Arch Virol 1986; 90 : 165-72.  Back to cited text no. 16
[PUBMED]    
17.
Umene K, Nunoue T. The genome type of human parvovirus B19 strains isolated in Japan during 1981 differs from types detected in 1986 to 1987: A correlation between genome type and prevalence. J Gen Virol 1990; 71 (Pt 4) : 983-6.  Back to cited text no. 17
[PUBMED]    
18.
Blümel J, Eis-Hübinger AM, Stühler A, Bönsch C, Gessner M, Löwer J, et al. Characterization of parvovirus B19 genotype 2 in KU812Ep6 cells. J Virol 2005; 79 : 14197-206.  Back to cited text no. 18
    
19.
Norja P, Eis-Hübinger AM, Söderlund-Venermo M, Hedman K, Simmonds P. Rapid sequence change and geographical spread of human parvovirus B19: Comparison of B19 virus evolution in acute and persistent infections. J Virol 2008; 82 : 6427-33.  Back to cited text no. 19
    
20.
Sanabani S, Neto WK, Pereira J, Sabino EC. Sequence variability of human erythroviruses present in bone marrow of Brazilian patients with various parvovirus B19-related hematological symptoms. J Clin Microbiol 2006; 44 : 604-6.  Back to cited text no. 20
[PUBMED]    
21.
Candotti D, Etiz N, Parsyan A, Allain JP. Identification and characterization of persistent human erythrovirus infection in blood donor samples. J Virol 2004; 78 : 12169-78.  Back to cited text no. 21
[PUBMED]    
22.
Parsyan A, Szmaragd C, Allain JP, Candotti D. Identification and genetic diversity of two human parvovirus B19 genotype 3 subtypes. J Gen Virol 2007; 88 : 428-31.  Back to cited text no. 22
[PUBMED]    
23.
Toan NL, Duechting A, Kremsner PG, Song le H, Ebinger M, Aberle S, et al. Phylogenetic analysis of human parvovirus B19, indicating two subgroups of genotype 1 in Vietnamese patients. J Gen Virol 2006; 87 : 2941-9.  Back to cited text no. 23
[PUBMED]    
24.
Dorsch S, Liebisch G, Kaufmann B, von Landenberg P, Hoffmann JH, Drobnik W, et al. The VP1 unique region of parvovirus B19 and its constituent phospholipase A2-like activity. J Virol 2002; 76 : 2014-8.  Back to cited text no. 24
[PUBMED]    
25.
Zádori Z, Szelei J, Lacoste MC, Li Y, Gariépy S, Raymond P, et al. A viral phospholipase A2 is required for parvovirus infectivity. Dev Cell 2001; 1 : 291-302.  Back to cited text no. 25
    
26.
Nguyen QT, Wong S, Heegaard ED, Brown KE. Identification and characterization of a second novel human erythrovirus variant, A6. Virology 2002; 301 : 374-80.  Back to cited text no. 26
[PUBMED]    
27.
Nguyen QT, Sifer C, Schneider V, Bernaudin F, Auguste V, Garbarg-Chenon A, et al. Detection of an erythrovirus sequence distinct from B19 in a child with acute anaemia. Lancet 1998; 352 : 1524.  Back to cited text no. 27
    
28.
Corcoran A, Doyle S, Allain JP, Candotti D, Parsyan A. Evidence of serological cross-reactivity between genotype 1 and genotype 3 erythrovirus infections. J Virol 2005; 79 : 5238-9.  Back to cited text no. 28
[PUBMED]    
29.
Srivastava A, Lu L. Replication of B19 parvovirus in highly enriched hematopoietic progenitor cells from normal human bone marrow. J Virol 1988; 62 : 3059-63.  Back to cited text no. 29
[PUBMED]    
30.
Tolfvenstam T, Rudén U, Broliden K. Evaluation of serological assays for identification of parvovirus B19 immunoglobulin M. Clin Diagn Lab Immunol 1996; 3 : 147-50.  Back to cited text no. 30
    
31.
Cassinotti P, Burtonboy G, Fopp M, Siegl G. Evidence for persistence of human parvovirus B19 DNA in bone marrow. J Med Virol 1997; 53 : 229-32.  Back to cited text no. 31
[PUBMED]    
32.
Eis-Hübinger AM, Reber U, Abdul-Nour T, Glatzel U, Lauschke H, Pütz U, et al. Evidence for persistence of parvovirus B19 DNA in livers of adults. J Med Virol 2001; 65 : 395-401.  Back to cited text no. 32
    
33.
Söderlund M, von Essen R, Haapasaari J, Kiistala U, Kiviluoto O, Hedman K, et al. Persistence of parvovirus B19 DNA in synovial membranes of young patients with and without chronic arthropathy. Lancet 1997; 349 : 1063-5.  Back to cited text no. 33
    
34.
Manning A, Willey SJ, Bell JE, Simmonds P. Comparison of tissue distribution, persistence, and molecular epidemiology of parvovirus B19 and novel human parvoviruses PARV4 and human bocavirus. J Infect Dis 2007; 195 : 1345-52.  Back to cited text no. 34
[PUBMED]    
35.
Liefeldt L, Plentz A, Klempa B, Kershaw O, Endres AS, Raab U, et al. Recurrent high level parvovirus B19/genotype 2 viremia in a renal transplant recipient analyzed by real-time PCR for simultaneous detection of genotypes 1 to 3. J Med Virol 2005; 75 : 161-9.  Back to cited text no. 35
[PUBMED]    
36.
Norja P, Hokynar K, Aaltonen LM, Chen R, Ranki A, Partio EK, et al. Bioportfolio: Lifelong persistence of variant and prototypic erythrovirus DNA genomes in human tissue. Proc Natl Acad Sci U S A 2006; 103 : 7450-3.  Back to cited text no. 36
[PUBMED]    
37.
Jain P, Jain A, Khan DN, Kumar M. Human parvovirus B19 associated dilated cardiomyopathy. BMJ Case Rep 2013; 2013. pii: bcr2013010410.  Back to cited text no. 37
    
38.
Jain A, Jain P, Prakash S, Kumar A, Khan DN, Seth A, et al. Genotype 3b of human parvovirus B19 detected from hospitalized children with solid malignancies in a North Indian tertiary care hospital. J Med Virol 2016; 88 : 1922-9.  Back to cited text no. 38
[PUBMED]    
39.
Kuethe F, Lindner J, Matschke K, Wenzel JJ, Norja P, Ploetze K, et al. Prevalence of parvovirus B19 and human bocavirus DNA in the heart of patients with no evidence of dilated cardiomyopathy or myocarditis. Clin Infect Dis 2009; 49 : 1660-6.  Back to cited text no. 39
[PUBMED]    
40.
Kühl U, Lassner D, Pauschinger M, Gross UM, Seeberg B, Noutsias M, et al. Prevalence of erythrovirus genotypes in the myocardium of patients with dilated cardiomyopathy. J Med Virol 2008; 80 : 1243-51.  Back to cited text no. 40
    
41.
Plentz A, Würdinger M, Kudlich M, Modrow S. Low-level DNAemia of parvovirus B19 (genotypes 1-3) in adult transplant recipients is not associated with anaemia. J Clin Virol 2013; 58 : 443-8.  Back to cited text no. 41
    
42.
Rahiala J, Koskenvuo M, Norja P, Meriluoto M, Toppinen M, Lahtinen A, et al. Human parvoviruses B19, PARV4 and bocavirus in pediatric patients with allogeneic hematopoietic SCT. Bone Marrow Transplant 2013; 48 : 1308-12.  Back to cited text no. 42
[PUBMED]    
43.
Schenk T, Enders M, Pollak S, Hahn R, Huzly D. High prevalence of human parvovirus B19 DNA in myocardial autopsy samples from subjects without myocarditis or dilative cardiomyopathy. J Clin Microbiol 2009; 47 : 106-10.  Back to cited text no. 43
[PUBMED]    
44.
Corcoran C, Hardie D, Yeats J, Smuts H. Genetic variants of human parvovirus B19 in South Africa: Cocirculation of three genotypes and identification of a novel subtype of genotype 1. J Clin Microbiol 2010; 48 : 137-42.  Back to cited text no. 44
[PUBMED]    
45.
Ekman A, Hokynar K, Kakkola L, Kantola K, Hedman L, Bondén H, et al. Biological and immunological relations among human parvovirus B19 genotypes 1 to 3. J Virol 2007; 81 : 6927-35.  Back to cited text no. 45
    
46.
Schneider B, Höne A, Tolba RH, Fischer HP, Blümel J, Eis-Hübinger AM, et al. Simultaneous persistence of multiple genome variants of human parvovirus B19. J Gen Virol 2008; 89 : 164-76.  Back to cited text no. 46
    
47.
Ruppert V, Meyer T, Balbach A, Richter A, Müller HH, Maisch B, et al. Genotype-specific effects on left ventricular function in parvovirus B19-positive patients with dilated cardiomyopathy. J Med Virol 2011; 83 : 1818-25.  Back to cited text no. 47
    
48.
Corcioli F, Zakrzewska K, Rinieri A, Fanci R, Innocenti M, Civinini R, et al. Tissue persistence of parvovirus B19 genotypes in asymptomatic persons. J Med Virol 2008; 80 : 2005-11.  Back to cited text no. 48
[PUBMED]    
49.
Zakrzewska K, Corcioli F, Carlsen KM, Giuggioli D, Fanci R, Rinieri A, et al. Human parvovirus B19 (B19V) infection in systemic sclerosis patients. Intervirology 2009; 52 : 279-82.  Back to cited text no. 49
[PUBMED]    
50.
Grabarczyk P, Kalińska A, Kara M, Wieczorek R, Ejduk A, Sulkowska E, 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.  Back to cited text no. 50
    
51.
Porignaux R, Vuiblet V, Barbe C, Nguyen Y, Lavaud S, Toupance O, et al. Frequent occurrence of parvovirus B19 DNAemia in the first year after kidney transplantation. J Med Virol 2013; 85 : 1115-21.  Back to cited text no. 51
[PUBMED]    
52.
Toshev A, Ivanova S, Kovaleva V, Andonova L, Mihneva Z. Detection of human parvovirusB19 (HPVB19) in serum samples from fever-rash ill individuals during the rubella outbreak (2005) in Bulgaria. Biotechnol Biotechnol Equip 2014; 28 : 1103-7.  Back to cited text no. 52
[PUBMED]    
53.
Toan NL, Sy BT, Song le H, Luong HV, Binh NT, Binh VQ, et al. Co-infection of human parvovirus B19 with plasmodium falciparum contributes to malaria disease severity in Gabonese patients. BMC Infect Dis 2013; 13 : 375.  Back to cited text no. 53
[PUBMED]    
54.
Siritantikorn S, Kaewrawang S, Siritanaratkul N, Theamboonlers A, Poovorawan Y, Kantakamalakul W, et al. The prevalence and persistence of human parvovirus B19 infection in thalassemic patients. Asian Pac J Allergy Immunol 2007; 25 : 169-74.  Back to cited text no. 54
[PUBMED]    
55.
Ke L, He M, Li C, Liu Y, Gao L, Yao F, et al. The prevalence of human parvovirus B19 DNA and antibodies in blood donors from four Chinese blood centers. Transfusion 2011; 51 : 1909-18.  Back to cited text no. 55
[PUBMED]    
56.
He M, Zhu J, Yin H, Ke L, Gao L, Pan Z, et al. Human immunodeficiency virus/human parvovirus B19 co-infection in blood donors and AIDS patients in Sichuan, China. Blood Transfus 2012; 10 : 502-14.  Back to cited text no. 56
[PUBMED]    
57.
Lavrent'eva IN, Antipova AIu, Semenov AV, Bichurina MA. Genotyping of parvovirus B19 isolates circulating in Northwestern Federal district of Russia. Zh Mikrobiol Epidemiol Immunobiol 2013; 6 : 36-43.  Back to cited text no. 57
    
58.
Jain P, Jain A, Prakash S, Khan DN, Singh DD, Kumar A, et al. Prevalence and genotypic characterization of human parvovirus B19 in children with hemato-oncological disorders in North India. J Med Virol 2015; 87 : 303-9.  Back to cited text no. 58
[PUBMED]    
59.
Azadmanesh K, Mohraz M, Kazemimanesh M, Aghakhani A, Foroughi M, Banifazl M, et al. Frequency and genotype of human parvovirus B19 among Iranian patients infected with HIV. J Med Virol 2015; 87 : 1124-9.  Back to cited text no. 59
[PUBMED]    
60.
Koppelman MH, Rood IG, Fryer JF, Baylis SA, Cuypers HT. Parvovirus B19 genotypes 1 and 2 detection with real-time polymerase chain reaction assays. Vox Sang 2007; 93 : 208-15.  Back to cited text no. 60
[PUBMED]    
61.
Freitas RB, Melo FL, Oliveira DS, Romano CM, Freitas MR, Macêdo O, et al. Molecular characterization of human erythrovirus B19 strains obtained from patients with several clinical presentations in the Amazon region of Brazil. J Clin Virol 2008; 43 : 60-5.  Back to cited text no. 61
    
62.
Mendonça MC, Ferreira AM, Santos MG, Oviedo EC, Bello MS, Siqueira MM, et al. Genotyping of human parvovirus B19 in clinical samples from Brazil and Paraguay using heteroduplex mobility assay, single-stranded conformation polymorphism and nucleotide sequencing. Mem Inst Oswaldo Cruz 2011; 106 : 502-4.  Back to cited text no. 62
    
63.
Slavov SN, Kashima S, Silva-Pinto AC, Covas DT. Genotyping of human parvovirus B19 among Brazilian patients with hemoglobinopathies. Can J Microbiol 2012; 58 : 200-5.  Back to cited text no. 63
[PUBMED]    
64.
Slavov SN, Kashima S, Silva-Pinto AC, Amarilla AA, Aquino VH, Covas DT, et al. Molecular and clinical evaluation of the acute human parvovirus B19 infection: Comparison of two cases in children with sickle cell disease and discussion of the literature. Braz J Infect Dis 2013; 17 : 97-101.  Back to cited text no. 64
    
65.
da Costa AC, Bendit I, de Oliveira AC, Kallas EG, Sabino EC, Sanabani SS, et al. Investigation of human parvovirus B19 occurrence and genetic variability in different leukaemia entities. Clin Microbiol Infect 2013; 19 : E31-43.  Back to cited text no. 65
    
66.
Pereira RF, Garcia Rde C, Azevedo KM, Setúbal S, Siqueira MA, Oliveira SA, et al. Clinical features and laboratory findings of human parvovirus B19 in human immunodeficiency virus-infected patients. Mem Inst Oswaldo Cruz 2014; 109 : 168-73.  Back to cited text no. 66
    
67.
Candotti D, Danso K, Parsyan A, Dompreh A, Allain JP. Maternal-fetal transmission of human parvovirus B19 genotype 3. J Infect Dis 2006; 194 : 608-11.  Back to cited text no. 67
[PUBMED]    
68.
Opaleye OO, Fagbami AH, Lalremruata A, Kun JF. Prevalence and association of human parvovirus B19V with hepatitis B and C viruses in Nigeria. J Med Virol 2011; 83 : 710-6.  Back to cited text no. 68
[PUBMED]    
69.
Sidoti F, Fierro MT, Costa C, Ponti R, Bergallo M, Comessatti A, et al. Prevalence and significance of human parvovirus variants in skin from primary cutaneous T cell lymphomas, inflammatory dermatoses and healthy subjects. Arch Dermatol Res 2009; 301 : 647-52.  Back to cited text no. 69
[PUBMED]    
70.
Stewart GC, Lopez-Molina J, Gottumukkala RV, Rosner GF, Anello MS, Hecht JL, et al. Myocardial parvovirus B19 persistence clinical perspective. Circ Heart Fail 2011; 4 : 71-8.  Back to cited text no. 70
[PUBMED]    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

Top
 
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
    Abstract
   Introduction
    Genotypes of Hum...
    Persistence of B...
    Geographical Dis...
    Erythrovirus B19...
   Conclusion
    References
    Article Tables

 Article Access Statistics
    Viewed543    
    Printed1    
    Emailed0    
    PDF Downloaded201    
    Comments [Add]    

Recommend this journal