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First Report of Human Salivirus/Klassevirus in Respiratory Specimens of a Child with Fatal Adenovirus Infection

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First Report of Human Salivirus/Klassevirus in Respiratory Specimens of a Child with Fatal Adenovirus Infection Virus Genes DOI 10.1007/s11262-016-1361-7 First report of human salivirus/klassevirus in respiratory specimens of a child with fatal adenovirus infection 1,3 2 1 1 1,4 Na Pei • Jiaosheng Zhang • Jinmin Ma • Liqiang Li • Meng Li • 1 1 1 1 1 1 Jiandong Li • Yisuo Sun • Jingkai Ji • Hui Jiang • Yong Hou • Fengping Xu • 1 2,5 2 1 2 Haorong Lu • Ruimu Zhang • Xuemei Wei • Xun Xu • Jikui Deng Received: 6 April 2016 / Accepted: 1 June 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Adenovirus is a leading cause of respiratory conducted on the samples from a nasopharyngeal swab of infection in children. Salivirus/klassevirus was first iden- the children with adenovirus infection. Sequences were tified as an etiologic agent of gastroenteritis and was never assembled using IDBA-ud (1.1.1); phylogenetic analysis reported in respiratory infection cases. The case being was performed using MEGA 5.2. RT-PCR and quantitative discussed here caught our attention because, although it is a PCR were performed to verify the existence of the virus in common respiratory infection, it was fatal, while similar the samples. A nearly full genome of this new virus strain cases were mild. In order to find potential causes in the was obtained with 7633 nt encoding a polyprotein of 2331 fatal case, we describe the clinical diagnosis and treatment, aa. Meanwhile, it was detected specifically in the the sequencing analysis of the salivirus/klassevirus, and the nasopharyngeal swab by RT-PCR. Further, homology co-infectious adenovirus. Metagenomics sequencing was analysis indicated that the virus has a closer relationship with Salivirus A strain in Shanghai (GU245894). Our study reports the first case of Human salivirus/klassevirus in Edited by Paul Schnitzler. respiratory specimens of a child with fatal adenovirus infection in Shenzhen, China. The finding and investigation Na Pei, Jinmin Ma and Jiaosheng Zhang have contributed equally to of the virus will provide more useful information for the this study. clinical diagnosis of unexplained lethal infection and Electronic supplementary material The online version of this expand our knowledge of the new family, salivirus/klas- article (doi:10.1007/s11262-016-1361-7) contains supplementary sevirus in picornavirus. material, which is available to authorized users. & Jinmin Ma Yisuo Sun [email protected] [email protected] & Xun Xu Jingkai Ji [email protected] [email protected] & Jikui Deng Hui Jiang [email protected] [email protected] Na Pei Yong Hou [email protected] [email protected] Jiaosheng Zhang Fengping Xu [email protected] [email protected] Liqiang Li Haorong Lu [email protected] [email protected] Meng Li Ruimu Zhang [email protected] [email protected] Jiandong Li Xuemei Wei [email protected] [email protected] 123 Virus Genes Keywords Salivirus/klassevirus Á Picornavirus Á samples using Qiagen RNeasykit (Qiagen, Inc., Germany) Sequencing Á Respiratory infection Á Adenovirus following the standard library construction process required for the next sequencing platform, Ion Proton (Life Inc., New York, USA) for metagenomics sequencing. RT- Introduction PCR was performed to verify the existence of the virus in both the nasopharyngeal and the blood samples of the fatal Respiratory infection is a tremendous burden on humans. case. A quantitative PCR approach was used on the More specifically, it is a primary cause of death in children nasopharyngeal swab. The cDNA swab product of the first under 5 years old. Viral infections are the primary cause PCR with gel extraction was gradient diluted from 10-1, behind respiratory infections in children after bacterial 10-2,to10-7 to establish a standard (Fig. 1), and then real- infections. The most common respiratory viruses include time PCR was performed. respiratory syncytial virus (RSV), influenza virus, and adenovirus. Data analysis Picornaviruses are non-enveloped viruses with a single- stranded positive-sense RNA genome that encodes a single For genome assembly, we used the IDBA-ud (1.1.1) to polyprotein [1]. It consists of 29 genera, six of which were assemble the data and then filtered the redundant sequen- identified as potentially infectious to humans (Enterovirus, ces. Contigs were blasted against the reference genome and Hepatovirus, Parechovirus, Kobuvirus, Cosavirus, and co-linearity analysis was made. Fourteen contigs were Cardiovirus). Salivirus/klassevirus belong to the genus finally obtained, and specific primers were designed to fill Salivirus, which is associated with human gastroenteritis the gaps to obtain the complete genome of Salivirus. [2]. Homology and Phylogenetic analysis was also performed Next-generation sequencing hastened the discovery of between the partial gene of the new genome and the ref- the new virus [3]. A sequence-based method [4] was used erence based on amino acid similarity. For the adenovirus to dig the potential pathogen, which decreased the time and sequences in the fatal case and the control sample, we used labor involved. More importantly, however, this study an in-house, reference-based method. First, non-human provides useful information for clinical diagnosis in cases reads were mapped to the adenoviridae reference database. of unexplained lethal infection [5]. These were constructed first to obtain the adeno-associated In our analysis, we describe the first known case of reads and to select a candidate reference genome. Second, salivirus/klassevirus in the respiratory specimens of a child the candidate reference genome was reduced with the infected with adenovirus and present the sequencing anal- threshold of sequence identity greater than 90 %. All the ysis of the salivirus/klassevirus and the co-infectious ade- adeno-associated reads were mapped to the reduced refer- novirus, with PCR verification and quantification of the ence genome. Third, we calculated entropy based on the salivirus/klassevirus. mapping result. Mapped reference positions with sequence depths greater than 0.5 were used as the consensus base. Methods 32 Sample source and verification 30 28 One nasopharyngeal swab and a blood sample were col- 26 24 lected from the fatal case. Additional nasopharyngeal 22 swabs from another non-fatal case of adenovirus pneu- 20 18 monia were collected for parallel analysis. All clinical Ct diagnosis and treatment were processed in accordance with 16 14 the hospital standards. Total RNA was extracted from the \ [ 12 5 10 8 1 BGI-Shenzhen, Shenzhen 518083, China 6 2 Shenzhen Children’s Hospital, Shenzhen 518038, China 024 3 Shenzhen Key Laboratory of Transomics Biotechnologies, Log DNA (fg/ul) BGI-Shenzhen, Shenzhen 518083, China Fig. 1 Relationship between tenfold serially diluted DNA and C 4 Qingdao University, Qingdao 266071, Shandong, China t value. A linear range was observed for DNA concentrations from 5 Shantou University, Shantou 515000, China 0.075 ng/ul to 0.75 fg/ul 123 Virus Genes Unknown bases were noted as ‘‘N.’’ The reduced reference, designed on the contigs, and sanger sequencing was used to which had the longest length and coverage rate, was the fill the gaps. The nearly full genome of this virus strain was final sequence. 7633 nt encoding a polyprotein of 2331 aa. The genome of the salivirus/klassevirus has been submitted to GenBank under accession no. KT182636 (Supplement 3). Results To verify the existence of this novel salivirus/klasse- virus (Salivirus A SZ1), we have designed several pairs of Clinical diagnosis and treatment specific primers based on the polyprotein regions. RT-PCR was performed to verify the existence of the virus in both In July 2013, a previously healthy 7-month-old boy was the nasopharyngeal and the blood samples of the fatal case. admitted to Shenzhen Children’s Hospital because of a All regions were detected specifically in the nasopharyn- persistent cough of 3 days duration, with wheezing and a geal swab by RT-PCR. Blood samples of the fatal case fever of 40.2 °C (104.36 °F). On the day of admission, he were also analyzed to determine whether viremia was had mild cyanosis around his mouth, shortness of breath, present; however, the PCR result was negative. Quantita- and fine crackles and wheezing rale over both lungs could tive PCR was then performed using the nasopharyngeal be heard. The white blood cell (WBC) count was swab. A linear range was observed for DNA concentrations 24.1 9 109/L; neutrophilic granulocyte count was from 0.075 ng/ul to 0.75 fg/ul, Ct values were observed 18.75 9 109/L, and C-reactive protein level was 51.9 mg/ with R2 = 0.98, and the copy number of the virus was L. A chest radiograph showed an exudative lesion over the 1.53 9 104 copies/ul in the swab (Figs. 1, 2). right lung. Further homology analysis between the genome with all Bacterial cultures from blood and deep tracheal aspirate of the salivirus/klassevirus genomes from NCBI based on were negative. A virus test was performed using direct the 3D gene of the genome indicated a closer relationship. immunofluorescence antigen detection. Adenovirus was The new genome is closest to the Salivirus A strain in positive in both the nasopharyngeal swab, and a bron- Shanghai (GU245894). A phylogenetic relationship choalveolar lavage fluid (BALF) procedure was performed between the new genome and selected species from the to detect any other respiratory tract viruses present, picornavirus genus based on amino acid similarity of VP1 including influenza A, influenza B, parainfluenza I, genes was also established (Fig. 3). parainfluenza II, parainfluenza III, and RSV; the results The adenovirus sequences were also analyzed in the were negative. Results were also negative for the following fatal case and the control case using an in-house reference- infectious disease testing: HIV antibody/antigen screen, based method. The results indicated that both the fatal case syphilis enzyme immunoassay, serum IgM for mycoplasma and the control case had a more coverage of the Human pneumonia, nasopharyngeal swab and BALF PCRs for adenovirus 7, which is one of the most prevalent aden- mycoplasma pneumonia and tubercle bacillus (TB).
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