key: cord-0856770-mp5g8sye
authors: Zhang, Junfeng; Cao, JiaJia; Ye, Qing
title: Nonpharmaceutical interventions against the COVID‐19 pandemic significantly decreased the spread of enterovirus in children
date: 2022-05-03
journal: J Med Virol
DOI: 10.1002/jmv.27806
sha: bdfb7b1ab272f86fa015ceefc19d7cf6251648b8
doc_id: 856770
cord_uid: mp5g8sye

Precise prevention and control measures have been adopted to impede the transmission of coronavirus disease 2019 (COVID‐19) in China. This study was performed to investigate the effect of protective measures on gastrointestinal infection in children during the COVID‐19 pandemic. The data on the rotavirus and adenovirus antigen tests were collected in outpatient children due to gastroenteritis from January 1, 2019 to December 31, 2020, at the Children's Hospital of Zhejiang University School of Medicine. According to age and month distribution, the positive number and rate of rotavirus and adenovirus in 2020 were compared with 2019. A 3.8‐fold and 4‐fold reduction in the number of rotavirus‐ and adenovirus‐positive patients in 2020 were found, respectively. The overall positive rate of rotavirus and adenovirus infection was drastically decreased in 2020 (rotavirus 2020: 18.18% vs. 2019: 9.75%, p < 0.001; adenovirus 2020: 3.13% vs. 2019: 1.58%, p < 0.001). The proportions of rotavirus and adenovirus in all age groups in 2020 decreased compared with those in 2019. The highest frequency of rotavirus infection occurred among children aged 1–3 years both in 2019 and 2020 (2019: 27.95% vs. 2020: 17.19%, p < 0.001), while adenovirus infection was detected in children aged 3–5 years, which had the highest percent positivity (2019: 8.19% vs. 2020: 4.46%; p < 0.001). An obvious peak prevalence of rotavirus incidence was found during December–April, and the percent positivity of rotavirus significantly decreased in 2020 (December 2019: 24.26% vs. 2020: 8.44%, p < 0.001; January 2019: 40.67% vs. 2020: 38.18%, p < 0.05; February 2019: 40.73% vs. 2020: 15.04%, p < 0.001; March 2019: 31.47% vs. 2020: 7.88%, p < 0.001; April 2019: 15.52% vs. 2020: 4.78%, p < 0.001). The positive rate of adenovirus distributed throughout 2019 was 1.91%–4.86%, while the percent positivity during 2020 in the same period was much lower (0.00%–3.58%). Our results confirmed that the preventive and control measures adopted during the COVID‐19 pandemic and the collateral benefit of these interventions have significantly decreased the transmission of rotavirus or adenovirus.

Coronavirus disease 2019 has spread in most countries, leading to enormous challenges to global healthcare and tremendously impacting everyone's lives. Since the outbreak of the pandemic, precise prevention and control measures, including early isolation and treated infected people, close contact tracing and quarantine, minimizing public gathering activities and closing of schools, and strengthening disinfection in places with large population flows are to been implemented for different regions and at different levels. In addition, personal protection measures such as respiratory etiquette, mask-wearing, hand hygiene, environmental sanitation, physical distancing, and travel restriction were strictly maintained all year round in China. 1 These measures curb the spread of COVID-19 and effectively control the transmission of other infectious diseases that are prevalent every winter, such as respiratory, influenza, and mycoplasma infections. [2] [3] [4] However, few studies have focused on the influence of the incidence rate of gastrointestinal-related viruses before and after the COVID-19 pandemic.

Gastrointestinal infectious diseases are among the most common life-threatening etiologies, especially in pediatric patients. 5 Viral infections generally cause gastroenteritis, and rotaviruses and adenoviruses are thought to be the major pathogens, 6 which are usually transmitted through the fecal-oral route. It is a tremendous burden. Approximately 1.5 million doctor visits yearly are associated with gastroenteritis. 7 The treatment of rotavirus gastroenteritis expends 365 million dollars each year in China. 8 Therefore, this retrospective study aimed to investigate whether the prevalence of rotavirus and adenovirus among children with gastroenteritis infection has changed under continual prevention and control strategies during the COVID-19 pandemic and to provide support for finding better protection strategies.

Data from outpatients with gastroenteritis at the Children's Hospital of Zhejiang University School of Medicine from January 2019 to December 2020 were collected. The specimen number of detection for rotavirus and adenovirus and the positive cases were analyzed in the present study. Gastroenteritis is diagnosed on clinical grounds. Its leading manifestations are sudden loosening of stool consistency and increased stool frequency to more than three times per day (or more than two times per day beyond the patient's usual frequency), sometimes accompanied by vomiting or fever. 9 Metabolic disturbances, intestinal obstruction, appendicitis, and other infectious diseases, such as pneumonia and meningitis, are the main elements of the differential diagnosis. None of the patients received any medications or medical tests before they visited our hospital, and patients over 18 years old or diagnosed with chronic diarrhea were excluded from the study. All subjects were divided into five age groups: under 6 months, 6 months-1 year, 1-3 years, 3-5 years, and older than 5 years. The positive rates of rotavirus and adenovirus were also compared by month.

Stool samples (1 g or 1 ml for children with diarrhea) were collected in a sterile screw-capped plastic container. Approximately 50 mg of stool sample was mixed with 1 ml of sample extraction solution and then used for detection. Rotavirus A and human adenovirus antigen were detected by a latex agglutination test using a commercial kit (b) if the control line was observed blue and the adenovirus test line was observed red, the sample was determined to be adenovirus positive. In our previous study, using quantitative real-time polymerase chain reaction (qRT-PCR) as the gold standard, the sensitivity and specificity of the latex agglutination test for detecting rotavirus A were 81.03% and 97.44%, respectively, and the sensitivity and specificity of the latex agglutination test for detecting human adenovirus were 76.27% and 94.19%, respectively. 10 

Statistical analyses were performed using SPSS 22.0 software. Categorical variables were analyzed by the χ 2 test or Fisher's exact test, and a two-sided p value less than 0.05 was considered statistically significant.

From January 2019 to December 2020, a total of 42 789 specimens were tested in our hospital due to gastroenteritis infection, including Among them, 25 152 were male, and 17 637 were female, with a male to female ratio of 1.43:1. However, a difference in sex between patients in 2019 and 2020 was not observed. In the five age groups, most patients were aged 1-3 years (4904, 34.97%) in 2020, which was roughly the same as that in 2019 (13 388, 46.54%) ( Table 1) . The overall positive rates of rotavirus and adenovirus involved in this study in 2020 were significantly lower than those in 2019 (χ 2 = 513.530, p < 0.001; χ 2 = 88.825, p < 0.001) ( Table 1 ). 

The positivity detection rate of rotavirus and adenovirus in 2019 and 2020 according to age was shown in Figure 2 . 18, 20 Interestingly, under Zhejiang's prevention and control measures that 

The authors declare no conflicts of interest.

The data that support the findings of this study are available from the corresponding author upon reasonable request. All requests should be submitted to the corresponding author for consideration.

All procedures performed in our study were in accordance with the guidelines of the Ethical Committee in our hospital and with the 1964

Helsinki Declaration and its later amendments. Committee approved this study of the Children's Hospital, Zhejiang University School of Medicine (approval no. 2022-IRB-072), and informed consent was taken from all patients.

Qing Ye http://orcid.org/0000-0002-5614-2695

Rapid and sustained containment of covid-19 is achievable and worthwhile: implications for pandemic response

Trends in respiratory virus circulation following COVID-19-targeted nonpharmaceutical interventions in Germany

Impact of nonpharmaceutical interventions targeted at COVID-19 pandemic on influenza burden: a systematic review

Effect of COVID-19 on childhood Mycoplasma pneumoniae infection in Chengdu

Prevalence, risk factors and seasonal variations of different Enteropathogens in Lebanese hospitalized children with acute gastroenteritis

Frequency of rotavirus and adenovirus gastroenteritis among children in

Managing acute gastroenteritis among children: oral rehydration, maintenance, and nutritional therapy

Burden of rotavirus gastroenteritis and distribution of rotavirus strains in Asia: a systematic review

Acute infectious gastroenteritis in infancy and childhood

Evaluation of a commercial latex agglutination test for detecting rotavirus A and human adenovirus in children's stool specimens

Epidemiological changes of common respiratory viruses in children during the COVID-19 pandemic

Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in sub-Saharan Africa: a randomised, doubleblind, placebo-controlled trial

Rotavirus diarrhea among children in Taiz, Yemen: prevalence-risk factors and detection of genotypes

Human rotavirus G9 and G3 as major cause of diarrhea in hospitalized children

Epidemiology of human astroviruses among children younger than 5 years: prospective hospital-based sentinel surveillance in South Africa

Prevalence and clinical profile of rotavirus A infection among diarrhoeal children and phylogenetic analysis with vaccine strains in Chengdu, West China

Prevalence and genotypes of group A rotavirus among outpatient children under five years old with diarrhea in Beijing, China

Prevalence and genotype distribution of group A rotavirus circulating in Shanxi Province, China during

Molecular epidemiology of group A rotavirus in outpatient diarrhea infants and children in Chongqing, China

Prevalence of rotavirus and rapid changes in circulating rotavirus strains among children with acute diarrhea in China

Prevalence of astrovirus, adenovirus, and sapovirus infections among Iranian children with acute gastroenteritis

Prevalence, risk factors, and clinical characteristics of rotavirus and adenovirus among Lebanese hospitalized children with acute gastroenteritis

Epidemiological aspects of rotavirus and adenovirus in hospitalized children with diarrhea: a 5-year survey in Beijing

Genetic diversity of group A rotavirus in acute gastroenteritis outpatients in Shanghai from

Epidemiology and clinical characteristics of respiratory infections due to adenovirus in children

Epidemiology and burden of rotavirus infection among children in Hangzhou

Medium-to long-term impact of rotavirus vaccination on hospital care in Belgium: a 7-year follow-up of the rotavirus Belgium Impact Study (RotaBIS)

Rotavirus: to the gut and beyond

Systemic features of rotavirus infection

Rotavirus infection beyond the gut

Risk factors for intussusception in infants in Vietnam and Australia: adenovirus implicated, but not rotavirus

Adenovirus: an increasingly important pathogen in paediatric bone marrow transplant patients

Nonpharmaceutical interventions against the COVID-19 pandemic significantly decreased the spread of enterovirus in children