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. 2024 Sep 11;6(5):298–303. doi: 10.1016/j.bsheal.2024.09.004

An outbreak of rhinovirus infection in a primary school in Shenyang City, China, in 2022

Yage Wang a, Jiayuan Liang b, Zhibo Xie a, Bing Wang c, Jinhua Song a, Baicheng Xia a, Huiling Wang a, Yao Zhang a, Ye Chen c, Ling Chen d, Shi Cong d, Yu Liu e, Aili Cui a, Yan Zhang a,⁎
PMCID: PMC11894958  PMID: 40078735

Highlights

  • •

    Rhinovirus (RV) can cause respiratory outbreaks in schools, hospitals and welfare institutions.

  • •

    Multiple types of RV can be detected in a respiratory outbreak.

  • •

    RV-A49 was the primary type in the current respiratory outbreak.

Keywords: Rhinoviruses (RV), Rhinoviruses-A49 type, Outbreak, Primary school, Respiratory tract infection

Abstract

Rhinovirus (RV) is a common pathogen that causes respiratory tract infection and can cause outbreaks in hospitals and welfare institutions. A cluster of respiratory diseases occurred in a primary school in Shenyang City, Liaoning Province, China, in 2022. In this outbreak, a total of 31 students had symptoms similar to those of upper respiratory tract infection, mainly cough and sore throat. Among them, 27 throat swabs were collected and identified for respiratory pathogens by TaqMan low-density array (TLDA), quantitative real-time polymerase chain reaction (PCR), reverse transcription-nested PCR and whole-genome sequencing. Out of the 27 specimens, 24 tested positive for RV, and 21 RV viral protein 1 sequences were obtained, of which 15 (71.43%) were identified as RV-A49, while 2 RV-A20 and 4 sequences from 2 specimens were RV-A30 coinfected with RV-C15. In addition, one whole-genome sequence (WGS) of RV-A49 was obtained, and three unique amino acid mutations were found compared to 23 WGS of RV-A49 from GenBank. In conclusion, this outbreak of upper respiratory tract infection is caused by RV, mainly RV-A49.

1. Introduction

Rhinovirus (RV) is a common pathogen that causes respiratory tract infections. The positive rates of RV in pneumonia and non-pneumonia patients were 24 % and 21 %, respectively, in a study of RV epidemiology among children [1]. Among infants under 1 year of age diagnosed with bronchiolitis, approximately 20 %–40 % are infected or co-infected with RV [2]. The clinical symptoms of RV infection are usually mild and primarily present as upper respiratory tract infection. The average incubation period is approximately 2 days, with a symptom duration of 7–14 days [3], [4]. Moreover, RV may also be associated with several lower respiratory tract infections, such as lung disease and severe bronchiolitis in infants and children, as well as fatal pneumonia in the elderly and immunocompromised individuals [5].

RV circulates throughout the year, with a high rate of positivity in summer in China [6]. RV is mostly transmitted in communities and mainly infects children and elderly individuals. There have also been reports of outbreaks of respiratory infections associated with RV in hospitals and welfare organizations, which could even cause death in severe cases [7], [8].

RV is a member of the genus Enterovirus in the family Picornaviridae and is a positive-sense, single-stranded ribonucleic acid (RNA) virus with approximately 7,200 base pairs in length. The viral genome contains 11 proteins, including four structural proteins (viral protein 1 to 4, VP1 to VP4) and seven non-structural proteins (2A, 2B, 2C, 3A, 3B, 3C, and 3D) [9]. RV were identified as A, B, and C based on their activity against antiviral compounds and differences between nucleotides [10], [11], [12]. The 5′ untranslated region of RV is highly conserved and can be used to identify RV in combination with other viruses, including other enteroviruses [13]. The VP1 region encodes an integral part of the viral capsid protein, which is used for the typing of RV species [14]. To date, 169 RV types have been identified for three species by the International Committee on Taxonomy of Viruses (ICTV) (https://ictv.global/report/chapter/picornaviridae/picornaviridae/enterovirus).

This study aimed to identify and analyze the pathogenesis of an outbreak of upper respiratory tract infection that occurred in a primary school in Shenyang City, Liaoning Province, China, from June 24th to July 2nd, 2022. An outbreak of upper respiratory tract infection caused by RV was reported, as well as the epidemiological investigation and pathogen identification methods of the outbreak, and genome-wide amino acid variation analysis was performed. This study helps to elucidate the epidemiological and etiological characteristics of RV and provides a reference for the identification, prevention and control of RV infection.

2. Methods

2.1. Epidemiological investigation and specimen collection

From June 24th to July 2nd, 2022, a cluster of respiratory tract infections with an unknown etiology occurred in a primary school in Yuhong District, Shenyang City, Liaoning Province, China. The infected population had a cough and sore throat as the primary clinical manifestations. The index case was reported on June 24th, with an increase in the number of cases on June 28th. The school promptly reported the outbreak to the local Centers for Disease Control and Prevention (CDC). Upon notification, the local CDC immediately initiated an investigation, conducted epidemiological surveys on students exhibiting symptoms such as fever, cough, sore throat, and runny nose on school, and collected epidemiological information and throat swab specimens. All specimens were transported to the Institute for Viral Disease Control and Prevention for further analysis in cold-packed sterile containers at a controlled low temperature of 4 °C.

2.2. Pathogen identification, type identification, and whole-genome sequencing

According to the manufacturer’s instructions, the total viral nucleic acid was extracted from the throat swab specimens using a Tianlong nucleic acid extraction kit (Tianlong Biotechnology, Xi'an, China). A TaqMan low-density array (TLDA) kit (Thermo Fisher Scientific Inc., Waltham, USA) was used to screen for human respiratory pathogens, including 16 viruses (adenovirus; human bocavirus; varicella zoster virus; Epstein-Barr virus; cytomegalovirus; human herpesvirus 6; influenza virus; parainfluenza virus; respiratory syncytial virus; human metapneumovirus; measles virus; coronavirus 229E, HKU1, NL63, OC43; Middle East respiratory syndrome coronavirus, severe acute respiratory syndrome coronavirus, and severe acute respiratory syndrome coronavirus 2; mumps virus; enterovirus; rhinovirus; and parechovirus), 9 bacteria (Bordetella; Bordetella holmesii; Bordetella pertussis; Haemophilus influenzae; Klebsiella pneumoniae; Legionella pneumophila; Moraxella catarrhalis; Staphylococcus aureus; and Streptococcus pneumoniae), and 3 other respiratory pathogens (Chlamydophila pneumoniae; Mycoplasma pneumoniae; and Pneumocystis jiroveci). The RV results were evaluated by quantitative real-time polymerase chain reaction (PCR) with a One Step PrimeScript™ RT-PCR Kit (Cat# RR064A; TaKaRa Biotechnology, Dalian, China) [13].

Nested reverse transcription-PCR (RT–PCR) was conducted with these three pairs of nested primers to amplify the VP1 sequence from RV-positive specimens using the PrimeScript™ One Step RT–PCR Kit Cat# RR057A (TaKaRa Biotechnology, Dalian, China). The reaction conditions and the purification and sequencing protocols were described previously [15].

A complementary deoxyribonucleic acid (cDNA) library was also constructed using the VAHTS® Universal V8 RNA-seq Library Prep Kit for MGI (Vazyme Biotech Co., Ltd., Lot# NRM605c, Nanjing, China). The library specimens were sent to the sequencing company MGI Tech Co., Ltd. for metagenome sequencing. The sequencing length was doubled to 150 bp, and the sequencing depth was above 5G.

2.3. Phylogenetic analysis

A sequencher (version 5.4.5; Gene Codes Corporation) was used to splice nucleotide sequences, and the full-length nucleotide sequence of the RV VP1 region was obtained by comparison with RV prototype strains recommended by the ICTV. MEGA (version 7.0; Mega Limited Auckland) software was used to align the RV VP1 sequences from this study and all the downloaded prototype strains of each RV type, as well as to calculate the pairwise nucleotide p-distance for each RV species [15]. BioEdit (version 7.1.3.0; LynnonBiosoft) software was used to analyze amino acid variation. CLC Genomic Workbench (version 22.0; CLC Bio) software was used to splice whole-genome sequences with Q20 and Q30 checks greater than 90 %.

3. Results

3.1. Epidemic situation

The index case of this outbreak involved a 7-year-old female student from Class 3, Grade 1. The case experienced rhinorrhea on the evening of June 24th and developed cough accompanied by fever on June 25th. Over the following three days, the number of cases with similar symptoms at school gradually increased, with seven new cases each on the 25th and 26th days, twelve new cases on the 27th day, and three new cases on the 28th day (Fig. 1). Schools were closed on June 29th, and the outbreak was judged to be over after four consecutive days without new cases until July 2nd.

Fig. 1.

Fig. 1

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Daily new cases of respiratory infections in a primary school in June in Shenyang City, Liaoning Province, China.

Thirty-one students were involved in the outbreak, and no teachers, staff, or parents were infected. The clinical manifestations of all 31 affected individuals were mainly respiratory tract infections, including cough in 17 cases (54.84 %), sore throat in 17 cases (54.84 %), runny nose in 15 cases (48.39 %), fever in 7 cases (22.58 %) and malaise in 13 cases (41.94 %). Among the 31 patients, 18 (58.06 %) were male, and 13 (41.94 %) were female. The median age was eight (7–12) years.

The spatial distribution of all 31 cases is shown in Table 1. There were 6 cases with the index case in Class 3, Grade 1, of which 1 case had malaise; 7 cases had Class 2, Grade 1, of which 2 had malaise; and 18 cases had Class 1, Grade 2, of which 10 had malaise (Table 1). All three classes are located on the west side of the first floor of the school’s academic building and are adjacent to each other.

Table 1.

Class distribution of 31 infected students in Shenyang City, Liaoning Province, China.

Class* Class size Number of infections in the class (%) Constituent ratio of infected individuals (%) Malaise (%)§
1.2 46 7 (15.22) 22.58 2 (28.57)
1.3† 46 6 (13.04) 19.35 1 (16.67)
2.1 52 18 (34.62) 58.07 10 (55.56)
Total 144 31 (21.53) 100.00 13 (41.94)
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*

: 1.2, 1.3 and 2.1 refer to Class 2, Class 3 of Grade 1, and Class 1 of Grade 2 in a primary school in Shenyang City, Liaoning Province, China, respectively.

†

: Class 3, Grade 1 is the class of the index case.

§

: Malaise refers to individuals without upper respiratory tract infection symptoms but with other symptoms such as weakness, sleepiness, inattention, etc. The ratio is the proportion of the malaise population in the total infected population of the class.

3.2. Etiological identification

Twenty-seven throat swabs were collected from 31 suspected patients. All specimens were subjected to respiratory pathogen screening using the TLDA assay kit. Among them, 19 specimens tested positive for RV, and all samples tested negative for other respiratory pathogens. A review of the results of 27 throat swabs using quantitative real-time PCR showed that 24 (88.89 %) throat swabs were RV positive, and the other 3 were RV negative.

3.3. Type identification

Twenty-one VP1 sequences were successfully amplified from 19 throat swabs from 24 RV-positive specimens, of which only RV-A sequences were amplified in 17 samples, and RV-A and RV-C sequences were amplified simultaneously in 2 samples. A total of 169 nucleotide sequences of different types of RV prototype strains were downloaded from GenBank, including 80 RV‐A sequences, 32 RV‐B sequences, and 57 RV‐C sequences. The phylogenetic tree was constructed based on the sequences of the above prototype strains and the 21 target VP1 sequences obtained in this outbreak, as shown in Fig. 2. The 21 VP1 sequences obtained in this study were classified into four types, A49 (15), A20 (2), A30 (2), and C15 (2), among which two patients were coinfected with RV-A30 and RV-C15.

Fig. 2.

Fig. 2

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Phylogenetic tree based on the RV-VP1 fragment constructed via the neighbor-joining method. The taxon names in red or black represent the sequences from this study or GenBank, respectively. The sequences linked with blue, violet, or orange branch lines were classified as RV-A, RV-B, or RV-C. Abbreviations: RV, rhinovirus; VP1, viral protein 1.

The genetic distance of the 15 RV-A49 VP1 sequences obtained in this study was 0 %–1.41 %, and the nucleotide and amino acid homology with those of the prototype strain (serial number: DQ473496) was 89.7 %–90.1 % and 95.0 %–96.1 %, respectively. Compared with those of the prototype strains RV-A20, RV-A30 and RV-C15, the nucleotide and amino acid homology of these strains were greater than 88.9 % and 94.2 %, respectively.

3.4. Whole-genome sequence analysis

A total of one RV-A49 whole-genome sequence, laboratory number SY20220284, was obtained by metagenomic sequencing. The nucleotide and amino acid homology of the SY20220284 whole-genome sequence and that of the prototype strain (sequence number: DQ473496) were 90.0 % and 96.8 %, respectively.

Through Basic Local Alignment Search Tool (BLAST) comparison, a total of 23 sequences with 90.08 %–97.97 % similarity to the whole genome of SY20220284 were downloaded from GenBank and are displayed in Supplementary Table 1. Among these sequences, MW587079 / Wuhan, China / 2016 [16] is the most similar to SY20220284, and the homology percentages of nucleotides and amino acids were 97.9 % and 99.7 %, respectively.

Compared with the above 23 RV-A49 whole-genome sequences, SY20220284 had three unique amino acid mutation sites, namely, the H591Q and S843P variants located in the picornavirus capsid protein (VP1) and the I1537V variant in the 3C cysteine protease (Supplementary Table 2). The H591Q amino acid variation was the common variation of the 15 RV-A49 sequences obtained on the VP1 protein in this study.

4. Discussion

From June 24th to July 2nd, 2022, a cluster outbreak of respiratory tract infections occurred in a primary school in Yuhong District, Shenyang City, Liaoning Province, China. The outbreak involved 31 students, and pathogenic identification of respiratory specimens revealed that the outbreak was caused by RV, and the spread of the outbreak was effectively under control through timely preventive and control measures. There were clinical symptoms similar to those of RV-associated respiratory infections in children in other studies [17], and the patients were all mildly ill with clinical symptoms of cough, sore throat, and runny nose.

The outbreak occurred in summer, which is the RV epidemic season. The incubation period of RV ranges from 0.8 to 4.5 days [4], and the number of new cases in this outbreak peaked on the third day after the first case, which is consistent with the incubation period after RV infection. The outbreak was confined to three adjacent classes and had some spatial clustering. The absence of infected individuals in other classes may have been due to measures implemented at the school, such as staggered meal times for students and ventilation in classrooms, which reduced the spread of RV.

Among children, the positive rate of RV gradually decreases with age [6], [18]. However, during this outbreak, more second-grade students than first-grade students were infected, and had milder clinical symptoms. This may be because the students in the upper grades were more immune and had less obvious symptoms after RV infection and did not take measures such as taking a leave or seeking medical attention, which triggered the spread of RV within the class as carriers. This is consistent with the presence of a certain percentage of asymptomatic infections among elderly individuals and children found in some studies [19], [20], [21], [22], suggesting that we should not only control and detect pathogens in symptomatic patients when an RV outbreak is detected but also monitor close contacts and those who may be involved in the outbreak to prevent more extraordinary transmission.

Unlike some respiratory virus outbreaks, such as the B3 genotype measles outbreak in Italy in 2017 and the BA9 genotype respiratory syncytial virus infection outbreak in Shenyang, China, in 2021, both of which were caused by one genotype [23], [24], RV outbreaks can be caused by single or multiple types at the same time. For example, RV outbreaks in orphanages in Vietnam in 2007 and in veteran care homes in Canada in 2013 were caused by a mix of RV-A and RV-C types [25], [26], while the RV outbreak in a psychiatric ward in a hospital in China’s Taiwan, in 2020 was caused by RV-A21[27]. Multiple RV types were detected in this outbreak in an elementary school in Shenyang City, with RV-A49 as the primary type, mixed with RV-A20, RV-A30, and RV-C15. The detection of multiple RV types in an RV outbreak may be due to the widespread prevalence of RV in the population and the large number of types, with low cross-protection between RV types [28]. However, due to the lack of testing for asymptomatic individuals in the study, it is impossible to determine whether RV-A20, RV-A30, and RV-C15 were part of a regular epidemic or an outbreak. Therefore, the outbreak is attributed primarily to RV-A49. This further underscores the importance of testing both symptomatic and asymptomatic individuals during disease outbreaks for more comprehensive pathogen tracing.

In addition to causing upper respiratory tract infections, RV can cause pneumonia. For example, in a study of community-acquired pneumonia cases in China in 2017–2019, a total of 81 RV types were identified, of which RV-A12, RV-A49, RV-B52, RV-C2, etc., were the common types [29]. RV-A49 was detected in cases of pneumonia and acute respiratory infection in Wuhan in 2016–2017, and its MW587079 sequence was most similar to the whole-genome sequence of SY20220284 obtained in this study [16]. These results indicate that RV-A49 can be detected in patients with pneumonia, acute respiratory tract infection, and upper respiratory tract infection. In addition, RV can even cause outbreaks of pneumonia cases with fatalities [25], [30]. In this investigation, RV-A49 was found to be the main type, and continuous monitoring of the prevalence of RV-A49 and other dominant types in China is needed.

VP1, an RV capsid protein, is the leading site of IgG1 and IgA antibody recognition, and its mutation may affect the immune evasion ability of RV [31]. The sequence of RV-A49 (SY20220284) identified in this study has three unique amino acid variants compared to the 23 whole-genome sequences of RV-A49 from BLAST, including the H591Q and S843P variants located in the VP1 region, with the H591Q variant being the common variant site in the VP1 region for the 15 RV-A49 in this study. The effects of these unique amino acid variants on the transmissibility and virulence of RV need to be further investigated.

In conclusion, this study reports an outbreak of upper respiratory tract infections caused by RV in a primary school in Shenyang City, Liaoning Province, China in 2022, with the primary type being RV-A49. This RV outbreak reminds us that we should strengthen the surveillance of RV, improve the detection methods for RV to identify RV infections in a timely and accurate manner, and understand the RV’s molecular epidemiology and pathogenetic characteristics to provide support for RV vaccine research and development, disease prevention and control. We also remind schools and other institutions where high-risk populations gather to perform their daily disinfection and sterilization work and adopt measures such as staggered meal times and open windows and ventilation to reduce the possibility of virus transmission during the peak season of respiratory virus epidemics.

Ethics statement

This study was approved by the Ethical Review Committee of the National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention. Written informed consent for the use of clinical specimens was obtained from all patients involved in this study or their guardians. This study did not involve human experimentation; the only human material used in this study was throat swab specimens collected from suspected respiratory infections cases during an outbreak in Shenyang City, Liaoning Province, China, from June to July 2022.

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2022YFC2704904).

Conflict of interest statement

The authors declare that there are no conflicts of interest.

Author contributions

Yage Wang: Writing – original draft, Investigation, Formal analysis. Jiayuan Liang: Resources, Investigation. Zhibo Xie: Writing – original draft, Validation. Bing Wang: Resources, Investigation. Jinhua Song: Writing – review & editing. Baicheng Xia: Methodology, Validation. Huiling Wang: Writing – review & editing. Yao Zhang: Validation, Formal analysis. Ye Chen: Investigation. Ling Chen: Validation. Shi Cong: Validation. Yu Liu: Investigation. Aili Cui: Funding acquisition. Yan Zhang: Conceptualization, Resources, Writing – review & editing, Supervision.

Footnotes

Supplementary data to this article can be found online at https://doi.org/10.1016/j.bsheal.2024.09.004.

Supplementary data

The following are the Supplementary data to this article:

Supplementary Data 1
mmc1.docx (15.4KB, docx)

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