Elsevier

Infection, Genetics and Evolution

Volume 37, January 2016, Pages 143-149
Infection, Genetics and Evolution

Research paper
Human bocavirus in hospitalized children with acute gastroenteritis in Russia from 2010 to 2012

https://doi.org/10.1016/j.meegid.2015.11.015Get rights and content

Highlights

  • 5502 stool samples from children were assayed for the presence of bocavirus DNA.

  • The prevalence of bocavirus variants in Novosibirsk was HBoV2 > HBoV1 > HBoV4 > HBoV3.

  • The prevalent HBoV genetic variants changed with time.

  • Both HBoV1 and HBoV2 could cause gastroenteritis in children in Novosibirsk.

  • HBoV infection is prevalently recorded in children during their first year of life.

Abstract

Human bocavirus (HBoV) can cause respiratory diseases and is detectable in the stool samples of patients with gastroenteritis. To assess the prevalence of HBoV in children hospitalized with acute gastroenteritis in Novosibirsk, Russia, as well as its genetic diversity and the potential role in the etiology of gastroenteritis in this region, a total of 5502 stool samples from children hospitalized with gastroenteritis from 2010 to 2012, n = 5250, and healthy children, n = 252, were assayed for the presence of HBoV DNA by semi-nested PCR. The HBoV DNA was found in 1.2% of stool samples from children, with gastroenteritis varying from 0.5% in 2012 to 1.7% in 2011. The prevalence of HBoV in healthy children was 0.3%. HBoV strains were detected throughout the year with an increase in the fall–winter season. In 87% of cases, HBoV was detected in children before 1 year of age. All known HBoV genetic variants have been detected in Novosibirsk, although with different prevalences: HBoV2 > HBoV1 > HBoV4 > HBoV3. At the beginning of 2011, HBoV2 replaced HBoV1 as the most prevalent variant. The median age of children with detected HBoV1 was 8.3 months, and that with HBoV2 was 8.0 months. All HBoV-positive samples were assayed for the presence of the rotaviruses A and C, norovirus GII, astrovirus, enterovirus, adenovirus F, Salmonella spp., Campylobacter spp., Shigella spp., and EIEC. HBoV1 and HBoV2 as single agents were found in 45.8% and 60% samples, respectively, although this difference was not statistically significant. In the case of co-infections, HBoV was most frequently recorded with rotavirus A and norovirus GII. This study demonstrated that the detection rate of HBoV in stool samples from children with gastroenteritis was low, although both HBoV1 and HBoV2 could be found as the sole agents in children with gastroenteritis in Novosibirsk.

Introduction

Human bocavirus (HBoV), which belongs to the family Parvoviridae, was first discovered in the nasopharyngeal aspirate samples from children with upper and lower respiratory diseases in Sweden in 2005 (Allander et al., 2005). Since 2007, HBoV has been detected in stool samples from children with gastroenteritis (GE) (Albuquerque et al., 2007, Chieochansin et al., 2008, Lau et al., 2007, Lee et al., 2007, Vicente et al., 2007). From 2009 to 2010, genetically different HBoV variants were found in stool samples and designated as HBoV2–HBoV4 (Arthur et al., 2009, Kapoor et al., 2009, Kapoor et al., 2010), whereas the previously discovered virus was referred to as HBoV1 (Chow and Esper, 2009). Currently, a new taxonomy for the family Parvoviridae is proposed; according to this new system, HBoV1–HBoV4 along with gorilla bocavirus belongs to the genus Bocaparvovirus, in which HBoV1 and HBoV3 are members of the species Primate bocaparvovirus 1, whereas HBoV2 and HBoV4 belong to the species Primate bocaparvovirus 2 (Cotmore et al., 2014).

HBoVs have a small (18–26 nm) nonenveloped icosahedral virion (Gurda et al., 2010) with a linear single-stranded DNA. The genome is approximately 3.5-kb long (Schildgen et al., 2012) and contains three open reading frames (ORFs). ORF1 encodes two variants of the nonstructural multifunctional protein NS1, ORF2 (a unique feature of HBoV) encodes an additional nonstructural protein, a nuclear phosphoprotein NP1 (Gurda et al., 2010, Schildgen et al., 2012), ORF3 contains two overlapping genes, which encode two major structural proteins, VP1 and VP2 (Allander et al., 2005). The degree of identity of the HBoV amino acid sequences belonging to different genotypes is rather small, amounting to 70% to 80% (Kapoor et al., 2009, Kapoor et al., 2010). In particular, the degree of homology between the NS1, NP1, and VP1/VP2 amino acid sequences of HBoV1 and HBoV2 genotypes is 78%, 67%, and 80%, respectively. Due to high genetic divergence, HBoV2 has been subdivided into three variants: HBoV2a, HBoV2b, and HBoV2c (Kapoor et al., 2009, Kapoor et al., 2010). By this time, HBoV has been detected in stool samples from children with GE worldwide, including Europe (Albuquerque et al., 2007, Kapoor et al., 2009, Risku et al., 2012), Asia (Ahn et al., 2014, Alam et al., 2015, Cheng et al., 2011, Jin et al., 2011, Kapoor et al., 2009, Khamrin et al., 2012, Lau et al., 2007, Monavari et al., 2013, Nakanishi et al., 2009, Wang et al., 2011, Zhang et al., 2014), Americas (Campos et al., 2015, Chhabra et al., 2013, Kapoor et al., 2011, Levican et al., 2013, Proenca-Modena et al., 2013, Santos et al., 2010), Africa (Kapoor et al., 2010), and Australia (Arthur et al., 2009) and the prevalence of HBoV varies from 0.5% to 20% depending on the region. However, studies of HBoV in GE in Russia are limited and do not allow to assess its role in the GE etiology in this region (Babkin et al., 2013, Zhirakovskaia et al., 2013). The aim of this study was to assess the prevalence of HBoV in children hospitalized with acute GE and healthy children (controls) in Novosibirsk, Russia and to characterize the genetic diversity of the detected HBoV strains.

Section snippets

Patients and sample collections

A total of 5,250 stool samples were collected from children ≤ 5 years of age hospitalized with diarrhea in the Novosibirsk Municipal Children's Hospital No. 3 from February 2010 to December 2012. Most cases of GE from Novosibirsk city and adjacent rural areas are referred to this hospital. The ages of children with diarrhea ranged from 3 days to 60 months (mean age ± SD, 7.44 ± 7.63 months). The majority of patients (85.2%) were 1 to 12 months old. The ratio of boys to girls was 1.2:1. Stool samples were

HBoV detection

To assess the HBoV molecular epidemiology in Novosibirsk, Russia, a total of 5502 stool samples from young children hospitalized with acute GE (n = 5,250) and healthy children (n = 252) were assayed for the presence of HBoV DNA by semi-nested PCR using only three primers from a primer set described by Kapoor et al. (Kapoor et al., 2009). According the PrimerBlast the selected primers were specific to a conservative region of the NS1 gene of HBoV1–HBoV4 and gorilla bocavirus. The size of the PCR

Discussion

The clinical data accumulated since the discovery of HBoV demonstrate that HBoV1 is an agent that causes upper and lower respiratory diseases but is also detectable in stool samples of GE patients (Alam et al., 2015, Albuquerque et al., 2007, Campos et al., 2015, Chhabra et al., 2013, Jartti et al., 2012, Kapoor et al., 2010, Khamrin et al., 2012, Levican et al., 2013, Monavari et al., 2013, Nadji et al., 2010, Proenca-Modena et al., 2013, Risku et al., 2012, Santos et al., 2010, Vicente et

Disclosure

All authors declare that they have no conflict of interest related to this study.

Acknowledgments

This work was supported by the Russian Foundation for Basic Research (project no. 13-04-00554а) and Russian Ministry of Education and Science (project VI.55.1.1).

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