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\begin{document}

\title{Rhinoviruses restored while fighting the COVID-19 Pandemic in Guangzhou,
China}



\author[1]{Di Wu}%
\author[2]{Tiantian Wu}%
\author[1]{Qing Zeng}%
\author[1]{Yiyun Chen}%
\author[1]{Yanhui Liu}%
\author[1]{Jianyun Lu}%
\affil[1]{Guangzhou Center for Disease Control and Prevention}%
\affil[2]{Sun Yat-Sen University}%


\vspace{-1em}



  
  \date{May 23, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Background To analyze the epidemic characteristics of the human
rhinovirus (HRV) outbreaks in Guangzhou, China, in 2020. Method
Descriptive epidemiological methods were used to analysis the HRV
related outbreaks of Guangzhou, 2020. Results 17 outbreaks were reported
in 2020 during the COVID-19 pandemic in Guangzhou, a total of 465
patients (290 males and 175 females) were enrolled, with a median age of
10. 223(47.96\%) had been tested for HRV, 89 (39.91\%) of which were
positive. 344/465 (73.98\%) had fever, 138/465 (29.68\%) had runny nose,
139/465 (29.89\%) had sore throat, 86/465 (18.49\%) had cough, 41/465
(8.82\%) had headache, 37/465 (7.96\%) had sneeze. Patients at age of 13
to 15 had the highest rate of sore throat and runny nose, patients at
the age of 11 to 12 had the highest rate of sneeze, and patients at age
of 12 to 14 had the highest rate of positive rate. Patients tested
positive had a higher rate of fever (?2=11.271, P=0.001), cough
(?2=6.987, P=0.008), runny nose (?2=7.980, P=0.005) and sneeze
(?2=4.676, P=0.031). Conclusion The HRV was restored during the fighting
the COVID-19 Pandemic. The conventional COVID-19 control measures were
not effective enough in preventing rhinovirus. More appropriate control
measures should be used to control HRV.%
\end{abstract}%



\sloppy


\textbf{Rhinovirusesrestored while fighting the COVID-19 Pandemic in
Guangzhou, China}

Di Wu \textsuperscript{1}, Tiantian Wu \textsuperscript{2}, Qing
Zeng\textsuperscript{1}, Yiyun Chen \textsuperscript{1}, Yanhui
Liu\textsuperscript{1}, Jianyun Lu \textsuperscript{1, *}

\textsuperscript{1} \emph{Division of Infectious Diseases, Guangzhou
Center for Disease Control and Prevention, Guangzhou, 510440, PR China.}

\textsuperscript{2} \emph{Institute of Human Virology, Zhongshan School
of Medicine, and Key Laboratory of Tropical Disease Control of Ministry
of Education, Sun Yat-sen University, Guangzhou 510080, PR China.}

\emph{\textsuperscript{*}Correspondence:}

Jianyun Lu\emph{, MPH, Division of Infectious Diseases, Guangzhou Center
for Disease Control and Prevention, NO. 1, Qide Road, Guangzhou City,
510440, PR China.}

\emph{Email: 258506273@qq.com}

\textbf{Abstract}

\textbf{Background} To analyze the epidemic characteristics of the human
rhinovirus (HRV) outbreaks in Guangzhou, China, in 2020.

\textbf{Method} Descriptive epidemiological methods were used to
analysis the HRV related outbreaks of Guangzhou, 2020.

\textbf{Results} 17 outbreaks were reported in 2020 during the COVID-19
pandemic in Guangzhou, a total of 465 patients (290 males and 175
females) were enrolled, with a median age of 10. 223(47.96\%) had been
tested for HRV, 89 (39.91\%) of which were positive. 344/465 (73.98\%)
had fever, 138/465 (29.68\%) had runny nose, 139/465 (29.89\%) had sore
throat, 86/465 (18.49\%) had cough, 41/465 (8.82\%) had headache, 37/465
(7.96\%) had sneeze. Patients at age of 13 to 15 had the highest rate of
sore throat and runny nose, patients at the age of 11 to 12 had the
highest rate of sneeze, and patients at age of 12 to 14 had the highest
rate of positive rate. Patients tested positive had a higher rate of
fever (\selectlanguage{greek}\textbf{χ\textsuperscript{2}}\selectlanguage{english} =11.271, \emph{P} =0.001), cough
(\selectlanguage{greek}\textbf{χ\textsuperscript{2}}\selectlanguage{english} =6.987, \emph{P} =0.008), runny nose
(\selectlanguage{greek}\textbf{χ\textsuperscript{2}}\selectlanguage{english} =7.980, \emph{P} =0.005) and sneeze
(\selectlanguage{greek}\textbf{χ\textsuperscript{2}}\selectlanguage{english} =4.676, \emph{P} =0.031).

\textbf{Conclusion} The HRV was restored during the fighting the
COVID-19 Pandemic. The conventional COVID-19 control measures were not
effective enough in preventing rhinovirus. More appropriate control
measures should be used to control HRV.

\textbf{Key Words} : Human Rhinovirus (HRV); Outbreaks; Coronavirus
Disease 2019 (COVID-19); Severe Acute Respiratory Syndrome Coronavirus 2
(SARS-COV-2); Pandemic;

Human Rhinoviruses (HRV) are the most common pathogens of the ``common
cold'', and caused more than half of the ``common cold'' was caused by
HRV\textsuperscript{1}. HRV was designated as A, B and C groups, within
the genus \emph{Enterovirus} and the family\emph{Picornaviridae}
\textsuperscript{2}. The main symptoms of the ``cold'' caused by HRV
infection are low fever, cough, runny nose, etc., and was a self-limited
disease in most conditions\textsuperscript{3}. The Coronavirus Disease
2019 (COVID-19) pandemic has led to an unprecedented level of concern
about the fever cases. The most common strategy for the control of the
unexplained fever event during the COVID-19 pandemic was to test for the
nucleic acid of the severe acute respiratory syndrome coronavirus 2
(SARS-COV-2) and influenza virus, however, we detected and found both
SARS-COV-2 and influenza were negative, and proved to be HRV infection
finally. Studies have reported that interference among respiratory
viruses could affect the infection of the host at a large scale
population level\textsuperscript{4-6}, influenza virus was the most
observed and studied respiratory virus, Anchi Wu \emph{et al}
\textsuperscript{7} found that rhinovirus disrupted the 2019 influenza A
virus pandemic in Europe and indicated that the respiratory viral
interference can potentially affect the seasonal influenza epidemics and
ongoing COVID-19 pandemic. We analyzed the outbreaks of the HRV
infection in Guangzhou City during the fight against COVID-19 pandemic,
and enhanced the understanding of the prevention and control of
rhinovirus outbreaks, and thus provide a better evidence for the
interference of the respiratory virus during the COVID-19 pandemic, and
thus control the pandemic.

\textbf{1 Materials and methods}

\textbf{1.1 Data and Specimen Collection}

We collected all the information of the fever events of unknown cause
during the combatting against the COVID-19 pandemic in Guangzhou City,
China, 2020. Throat swabs or nasopharyngeal swabs were taken in all out
breaks of the fever events during the filed investigation, and were
tested in the laboratory of Guangzhou Center for Disease Control and
Prevention.

\textbf{1.2 Case Definition}

The cases enrolled in the study are the ones with one of these symptoms
since the first case and before the last case was reported: fever,
cough, runny nose, sneezing or sore throat. If there were more than 5
cases reported in 3 days in a class should be defined as an outbreak.

\textbf{1.3 Etiological Detection}

During the field investigation, throat swabs were collected from
patients who did not take antiviral drugs within 3 days of onset and met
the case definition. SARS-COV-2 and influenza nucleic acid was tested by
Real-time quantitative PCR (qPCR) within 6 hours after the samples were
collected, and NxTAG Respiratory Pathogen Panel (LOT: XK051C-1045,
Luminex, USA) was used to test for the respiratory poly-pathogen nucleic
acid. Influenza virus (subtype AH1, AH3), A (H1N1)pdm09, influenza B
virus, respiratory syncytial virus and parainfluenza virus (1, 2, 3, 4),
Bocavirus, Human metapneumovirus (HMPV), HRV, adenovirus, coronavirus
(OC43, 229E, HKU-1, NL63), legionella, mycoplasma pneumoniae (MP) and
chlamydia pneumonia (CP) was included. All testes were followed by the
manufacturers' instructions.

\textbf{1.4 Statistical analysis}

Excel 2016 was used to collected the basic information of the patients
in the outbreaks during the field investigation. Chi-square
(\selectlanguage{greek}χ\selectlanguage{english}\textsuperscript{2}) test was used to statistical analysis using SPSS
statistics (version 13.0), \emph{P} \textless{}0.05 was considered to be
significant.

\textbf{2 Results}

\textbf{2.1 General Information}

Guangzhou City is the capital city of Guangdong Province, China, with
18.6 million populations. We have detected 17 outbreaks of HRV in 2020,
a total of 465 cases have been reported, of which, 290 were male and 175
were female, with an average age of 11.9 and the median age was 10.

\textbf{2.2 Temporal and spatial epidemiology}

Of all the 17 outbreaks, 6 were reported in June, 3 were reported in
July, 5 were reported in September, 1 was reported in October, and 2
were reported in November. All outbreaks were reported in schools, 8 out
of 17 were reported in primary school, 6 were reported in vocational
education school, 2 were in kindergarten and 1 in middle school
(\textbf{Table 1} ).

\textbf{2.3 Etiological Detection}

Of all the 465 cases, 223(47.96\%) had been taken specimen and tested,
ALL negative for SARS-COV-2 and influenza, of which, 89 (39.91\%) were
tested positive for HRV without genotyping.

\textbf{2.5 ClinicalCharacteristics of the patients in the outbreaks}

We collected all the core health indicators of the enrolled patients,
such as age, sex, the temperature of the patients, and the symptoms of
the patients: cough, sore throat, muscle pain, headache, conjunctival
congestion, runny nose, sneeze, diarrhea and vomit.

We analyzed and found the average age of all the patients is 11.9\selectlanguage{ngerman}±5.9
years, and the median age is 10. A total of 290 males and 175 females
were enrolled, 344/465 (73.98\%) had a record of temperature over than
37.3 \selectlanguage{english}, 138/465 (29.68\%) had runny nose, 139/465 (29.89\%) had sore
throat, 86/465 (18.49\%) had cough, 41/465 (8.82\%) had headache, 37/465
(7.96\%) had sneeze, and we found the female patients had a higher rate
of have fever and more likely to be tested positive for the HRV test
(\textbf{Table 2} ). Notably, 7/465 (1.51\%) had muscle pain, 5/465
(1.08\%) had diarrhea, 1/465 (0.22\%) had conjunctival congestion, and
1/465 (0.22\%) had vomit.

We next analyzed the results by age group, and found the patients less
than 5 years old had the highest rate of have fever, and if the patients
had an elder age will have less rate of have fever, but the patients
over than 18 had the opposite trend. The patients at the age of 9 to 10
had the highest rate of have cough. Patients at the age of 13 to 15 had
the highest rate of sore throat and runny nose, patients at the age of
11 to 12 had the highest rate of sneeze, and patients at age of 12 to 14
had the highest rate of positive rate (\textbf{Table 3} ).

We next found that the tested patients had a statistical lower rate of
fever than that of the patients without test
(\selectlanguage{greek}\textbf{χ\textsuperscript{2}}\selectlanguage{english} =32.563, \emph{P} \textless{}0.001), that
might be due to our preference to take specimens of the cases with
symptoms such as fever during field investigations. The rest of the
clinical characteristics were no statistical difference between the
tested and not tested ones (\textbf{Table 4} ).

\textbf{2.6 Clinical Characteristics of virus infections}

We nest analyzed the clinical characteristics of the patients we tested,
and found that there was a higher rate of fever
(\selectlanguage{greek}\textbf{χ\textsuperscript{2}}\selectlanguage{english} =11.271, \emph{P} =0.001), cough
(\selectlanguage{greek}\textbf{χ\textsuperscript{2}}\selectlanguage{english} =6.987, \emph{P} =0.008), runny nose
(\selectlanguage{greek}\textbf{χ\textsuperscript{2}}\selectlanguage{english} =7.980, \emph{P} =0.005) and sneeze
(\selectlanguage{greek}\textbf{χ\textsuperscript{2}}\selectlanguage{english} =4.676, \emph{P} =0.031) in the positive
ones of the infected (\textbf{Table 5} ).

\textbf{3 Discussion}

The ``common cold'' was not generally concerned by the general public
for the mild symptoms, however, there were more than 250 virus serotypes
could led to the ``common cold'' symptoms, and human rhinovirus (HRV)
has long been known for the main pathogens of the ``common
cold''\textsuperscript{2,8}, Cui and colleagues\textsuperscript{9} have
reported that among the influenza like illness (ILI), 6.46\% of which
were tested positive for HRV, another study conducted by Lan
Zhao\emph{et al} \textsuperscript{10} reported that 11.28\% of the acute
respiratory viral infection were caused by HRV infection. Yuki
Furuse\emph{et al} \textsuperscript{11}. also found that rhinoviruses
were the most frequently detected pathogen (22.2\%) among the acute
respiratory infection (ARI) cases, the hospitalized population would
have a higher positive rate of HRV\textsuperscript{12}.

A study conducted by Dr. Luka and colleges\textsuperscript{13} in Kenya
had reported that the common cold caused by HRV was mainly detected
among school-going children or teenagers with a mild acute respiratory
symptoms. However, the HRV infected adults were had a relative higher
mortality and longer hospitalization than that of the patients infected
influenza viruses in the elderly population\textsuperscript{14}. Dr.
Park\textsuperscript{15} analyzed the etiological surveillance data of
respiratory viruses in South Korea from 2016 to 2019 and 2020, and found
that the enveloped respiratory viruses (human coronavirus, HCoV,
non-SARS-COV-2; human metapneumovirus, HMPV; influenza virus, IFV;
parainfluenza virus, PIV; respiratory syncytial virus, RSV) were
effectively controlled at the COVID-19 control measures in 2020, while
non-enveloped respiratory viruses (adenovirus, ADV; human rhinovirus,
HRV; human bocavirus, HBoV) were not effectively controlled during this
period, and among hospitalized cases, the proportion of hospitalizations
due to rhinovirus infection was significantly increased. A study
conducted by Dr. Zhang\textsuperscript{16} observed a sharp increase of
the positive rate of HRV in Beijing, China, and reasonably assumed to be
explained by the reopening of the primary and secondary schools of
Beijing. Another study\textsuperscript{17} conducted in Southampton, UK,
gave a theory that the HRV was mainly found in children and adolescents
whom were the major reservoir for HRV infection, social distancing and
face masks are not effective in preventing transmission of HRV, with
``\emph{Back-to-School Upper Respiratory Infection} ''
effect\textsuperscript{18}, the risk of HRV transmission surges after
schools reopening. On the other hand, Dr. Nancy
Leung\textsuperscript{19} conducted experiments and proved that there
was no significant difference in filtering or protection effect of HRV
between wearing a face mask or not, indicating that wearing masks cannot
effectively protect the population from the HRV infection.

Our previous studies\textsuperscript{20-22} have showed that when
combated with the COVID-19 pandemic, measures had been taken to stop the
transmission of the SARS-COV-2, and respiratory virus like influenza
virus, varicella, herpes zoster, rubella, measles, mumps virus were
observed all dramatically decreased during the fighting against COVID-19
pandemic, however, HRV was found remains prevalent in school
teenagers\textsuperscript{23}.

In our study, most of the outbreaks were reported the primary and
secondary schools of Guangzhou, China, which was agree with the Dr.
Martha's and Dr. Zhang' s study\textsuperscript{13,16}. 74\% of the
patients in our study were recorded had fever, 30\% of the patients had
sore throat and runny nose, 19\% of the patients had cough and 8\% of
the patients had sneeze, so the most typical symptom of HRV infection in
our study was fever. By sampling and testing, we found that patients
with the symptoms of fever, cough, runny nose and sneezing were more
likely to test positive for HRV in a HRV related outbreak. Study have
proved that HRV infection in youngsters would be symptomatic while in
adults often asymptomatic\textsuperscript{24}.

Diurnal temperature range (DTR) was reported to be one of the risk
factors of the common cold, which gives the answer to the trend of the
endemic of HRV in spring and winter of the year\textsuperscript{25}.
Obesity was another risk factor reported to rise the possibility of HRV
infection\textsuperscript{26}. While in our study, we did not collect
the DTR, height and weight data of the patients, which is a shortcoming
of this study.

In summary, this study gives a glimpse of the endemic of HRV in
Guangzhou, China, proved better evidence for the prevention and control
of respiratory viruses, and indicated that the conventional COVID-19
control measures, such as wearing face masks or social distancing, are
not effective enough in preventing rhinovirus, so new masks that filter
non-enveloped viruses, including HRV, should be considered as a possible
new approach to preventing HRV infection.

\textbf{Funding:} This work was supported by the Natural Science
Foundation of Guangdong Province (2019A1515011407), Medical Science and
Technology Project of Guangzhou (20201A011067,20211A011059), Guangdong
Medical Science and Technology Research Project (A2019379, A2020399,
B2021244).

\textbf{Conflicts of Interest:} No conflict of interest to declare by
all authors

\textbf{ORCID:} \emph{Di Wuhttps://orcid.org/0000-0003-2462-4232}

\textbf{Ethical Approval Statement:} The ethical approval or individual
consent was not applicable.

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