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\begin{document}

\title{Viral epidemiology and SARS-CoV-2 coinfections with other respiratory
viruses during the first COVID-19 wave in Paris, France}



\author[1]{Donia BOUZID}%
\author[1]{Quentin Le hingrat}%
\author[1]{Christophe Choquet}%
\author[1]{odile Laurent}%
\author[1]{Xavier Lescure}%
\author[1]{Jean François Timsit}%
\author[1]{Nadhira Houhou Fidouh}%
\author[1]{Enrique Casalino}%
\author[1]{Jean Christophe Lucet}%
\author[1]{Diane Descamps}%
\author[1]{Benoit Visseaux}%
\affil[1]{APHP}%


\vspace{-1em}



  
  \date{May 27, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Abstract: Objectives: Our work assessed the prevalence of co-infections
in patients with SARS-CoV-2. Methods: All patients hospitalized in a
Parisian hospital during the first wave of COVID-19 were tested by mPCR
if they presented ILI symptoms. Results: A total of 806 patients (21\%)
were positive for SARS-CoV-2, 755 (20\%) were positive for other
respiratory viruses. Among the SARS-CoV-2 positive patients, 49 (6\%)
had viral co-infections. They presented similar age, symptoms, except
for fever (p=0.013) and headaches (p=0.048), than single SARS-CoV-2
infections. Conclusions: SARS-CoV-2 infected patients presenting viral
co-infections had similar clinical characteristics and prognosis than
patients solely infected with SARS-CoV-2.%
\end{abstract}%



\sloppy


\textbf{Viral epidemiology and SARS-CoV-2 coinfections with other
respiratory viruses during the first COVID-19 wave in Paris, France}

\selectlanguage{ngerman}\emph{Quentin Le Hingrat *\textsuperscript{,1,2}, Donia Bouzid
*\textsuperscript{,1,3}, Christophe Choquet \textsuperscript{3}, Odile
Laurent \textsuperscript{3}, François-Xavier
Lescure\textsuperscript{1,4}, Jean-François
Timsit\textsuperscript{1,5},Nadhira Houhou-Fidouh \textsuperscript{2},
Enrique Casalino \textsuperscript{1,3}, Jean-Christophe
Lucet\textsuperscript{1,6}, Diane Descamps \textsuperscript{1,2}, Benoit
Visseaux \textsuperscript{1,2}}

*Equally contributed to this work

\textsuperscript{1} Université de Paris, INSERM, IAME, F-75006 Paris,
France

\textsuperscript{2} AP-HP Nord, Virology Department, Bichat-Claude
Bernard University Hospital, Paris, France

\textsuperscript{3} AP-HP Nord, Emergency Department, Bichat-Claude
Bernard University Hospital, Paris, France

\textsuperscript{4} AP-HP Nord, Infectious Diseases Department,
Bichat-Claude Bernard University Hospital, Paris, France

\textsuperscript{5} AP-HP Nord, Medical and Infectious Diseases
Intensive Care Unit, Bichat-Claude Bernard University Hospital, Paris,
France

\textsuperscript{6} AP-HP Nord, Infection Control Unit, Bichat-Claude
Bernard University Hospital, Paris, France

\textbf{Abstract:}

\textbf{Objectives:} Our work assessed the prevalence of co-infections
in patients with SARS-CoV-2.

\textbf{Methods:} All patients hospitalized in a Parisian hospital
during the first wave of COVID-19 were tested by mPCR if they presented
ILI symptoms.

\textbf{Results:} A total of 806 patients (21\%) were positive for
SARS-CoV-2, 755 (20\%) were positive for other respiratory viruses.
Among the SARS-CoV-2 positive patients, 49 (6\%) had viral
co-infections. They presented similar age, symptoms, except for fever
(p=0.013) and headaches (p=0.048), than single SARS-CoV-2 infections.

\textbf{Conclusions:} ~SARS-CoV-2 infected patients presenting viral
co-infections had similar clinical characteristics and prognosis than
patients solely infected with SARS-CoV-2.

\textbf{Key words:} SARS-CoV-2, viral co-infection, syndromic testing,
respiratory viruses

\textbf{Words count:}

\emph{Introduction}

As of December 2020, COVID-19 has been responsible for more than 63
million infections and over 1.5 million deaths worldwide {[}1{]}. The
common symptoms of COVID-19 are fever, cough, dyspnea, fatigue, myalgia,
and diarrhea. Most of these symptoms are also falling within the
definition of influenza-like illness {[}2,3{]}. In France, SARS-CoV-2
first wave struck from late February to the end of April, coinciding
with the very end of the winter-associated viruses' epidemic this year
and raising the question of potential viral co-infections with
SARS-CoV-2 and their impact.

A few studies reported cases of SARS-CoV2 co-infection with other
respiratory viruses, and a meta-analysis estimated the prevalence of
those viral co-infections to 3\% {[}4--7{]}. However, none of the
included studies has used systematic wide range PCR methods. Moreover,
there is no data on the impact of SARS-CoV-2 viral co-infection on
disease severity and clinical outcomes.

Here, we take advantage of the systematic multiplex PCR (mPCR) testing
of patients hospitalized for respiratory tract infection during the
first SARS-CoV-2 epidemic wave to assess the cocirculation of all
respiratory viruses with SARS-CoV-2, the number of SARS-CoV-2 viral
co-infections, and the clinical features of such co-infections.

\emph{Methods}

All adult patients hospitalized in a COVID-19 first-line hospital in
Paris, France, from January 25th, 2020 to April 30th, 2020 were
included. All patients were tested by systematic mPCR testing if they
presented Influenza-like illness (ILI) symptoms, according to the eCDC
definition, and required hospitalization. The two mPCR assays used
during the study period, the QIAstat-Dx SARS-CoV-2 respiratory panel,
Qiagen {[}8{]}, and the BioFire FilmArray RP2+, BioMérieux {[}9{]} allow
for detecting a wide range of viral and atypical bacterial respiratory
targets, including influenza A and B, parainfluenza virus,
rhinoviruses/enteroviruses, RSV, metapneumovirus, adenovirus, human
coronaviruses (229E, HKU1, OC43, and NL63), Mycoplasma pneumoniae, and
Bordetella pertussis. According to the French national definition, a
specific SARS-CoV-2 RT-PCR for at-risk patients was performed, starting
from March 10th, 2020, when systematic testing for SARS-CoV-2 infection
began. During this period, three SARS-CoV-2 RT-PCR assays were used: the
WHO recommended in-house RT-PCR assay, the RealStar® SARS-CoV-2 RT-PCR
kit (Altona, Germany), and the Cobas® SARS-CoV-2 assay (Roche
Diagnostics, USA). All these assays provided similar performance and
limit of detection {[}10,11{]}. Demographic, clinical, and biological
features were prospectively collected in the Emergency Department (ED)
and retrospectively from the other units. Baseline characteristics
within each group were summarized using appropriate descriptive
statistics. The statistical analysis was performed using Stata15. The
research was approved by the local ethic committee N° CER-2020-6.

\emph{Results}

3768 patients were included during the study period, 1906 from the ED
and 1862 other inpatients. Overall, 806 (21\%), 755 (20\%), and 28 (1\%)
samples were positive for SARS-CoV-2, any other respiratory viruses, or
atypical bacteria, respectively. The SARS-CoV-2 wave struck from
February to April with a peak incidence between mid-March and
early-April. At this time, rhinoviruses, human coronaviruses,
adenoviruses, or parainfluenza viruses were still circulating, but most
of the seasonal respiratory virus epidemic was already gone, especially
influenza (cf Figure 1). Among the 806 SARS-CoV-2-positive patients, 42
(5\%), 7 (1\%), and 6 (1\%) also presented one, two other viruses and
atypical bacteria, respectively, and 61 (8\%) non-SARS-CoV-2 patients
positive by mPCR showed viral co-infections. Most frequently associated
viruses were rhinoviruses (17), common human coronaviruses (15),
adenoviruses (7), parainfluenza (5), metapneumoviruses (4), influenza
(4), and RSV (2) and other pathogens (7). The temporal distribution of
pathogens is depicted below (Figure). When comparing ED patients with
SARS-CoV-2 either alone (n= 249) or associated (n=33) , they presented
similar age, symptoms, vital signs measurements, or comorbidities,
except for fever (p=0.013) and headaches (p=0.048). Among those
co-infected patients, 0 (0\%) were hospitalized in ICU at day 1 versus
64/249 (26\%) patients with only a SARS-CoV2 infection, p=0.78. 5 (2\%)
among the co-infected patients died during hospitalization, and 49
(20\%) with only a SARS-CoV2 infection, p=0.78.

\emph{Discussion}

This work highlights that 6\% of SARS-CoV-2-infected patient presented
with viral co-infection at our adult ED. This proportion is higher than
previously reported for SARS-CoV-2 {[}6{]} but at a level similar to the
other respiratory viruses{[}12{]}. This high prevalence of viral
co-infections was observed, despite the limited circulation of other
respiratory viruses due to lockdown, curfew, and being in the tail of
the season of respiratory viruses {[}7{]}. Rhinoviruses, adenoviruses,
and other coronaviruses were the most frequently detected viruses with
SARS-CoV-2. Adenoviruses and rhinoviruses have already been reported,
outside the scope of SARS-CoV-2, as being more frequently involved in
viral co-infection, contrary to influenza viruses {[}13{]}.

In our population, only 6 patients with SARS-CoV-2 were also infected
with atypical bacteria. Co-infections can lead to viral interference,
one virus limiting or suppressing the replication of the second virus,
or to an enhancement of disease severity compared to mono-infection
{[}14{]}. In our cohort, patients presenting with viral co-infections
with SARS-CoV-2 had similar clinical pictures, except for headache and
fever, and prognosis than patients solely infected with SARS-CoV-2.

Our study presents several strengths and limitations. It showed a
relatively large number of SARS-CoV-2 co-infections compared to previous
works {[}4--7{]} and linked virological data with detailed clinical
data. Syndromic mPCR testing was performed on all patients presenting
with ILI during the study period. Thus patients recruited in this
observational study are not skewed towards more severe patients and
represent all adult patients hospitalised for ILI. However, our study is
monocentric, and the SARS-CoV-2 epidemic flared in Ile-de-France when
the incidence of most respiratory viruses was waning. Prevalence of
viral co-infections with SARS-CoV-2 might be higher in settings with an
active circulation of respiratory viruses and/or once social distancing
will be over. We also cannot rule out that some specific co-infections
might have a deleterious impact, notably SARS-CoV-2/influenza, as only 4
were detected during our study period. Higher severity of
SARS-CoV-2/influenza A H1N1pdm2009 has recently been described in golden
Syrian hamsters when the two viruses were simultaneously inoculated
{[}15{]}. We also did not retrieve data on the other pneumonia diagnosis
related to \emph{pneumococcus} or \emph{staphylococcus} . Thus, although
we found that SARS-CoV-2 viral co-infections were rare during the first
epidemic wave and did not differ either by their clinical presentation
or their outcome from SARS-CoV-2 mono-infections, this reassuring
finding must be confirmed in the upcoming months.

\textbf{Words count:} 1013

\textbf{References}

{[}1{]} WHO. World Health Organization. Coronavirus disease 2019
(COVID-19) situation report -- 96 n.d.

{[}2{]} Docherty AB, Harrison EM, Green CA, Hardwick HE, Pius R, Norman
L, et al. Features of 20 133 UK patients in hospital with covid-19 using
the ISARIC WHO Clinical Characterisation Protocol: prospective
observational cohort study. BMJ 2020;369.
https://doi.org/10.1136/bmj.m1985.

{[}3{]} Bouzid D, Mulahert J, hingrat QL, Laurent odile, Duval X,
Lescure X, et al. Characteristics associated with COVID-19 or other
respiratory viruses' infections at a single-center Emergency Department.
Preprints; 2020. https://doi.org/10.22541/au.160091431.15743661.

{[}4{]} Lai C-C, Wang C-Y, Hsueh P-R. Co-infections among patients with
COVID-19: The need for combination therapy with non-anti-SARS-CoV-2
agents? J Microbiol Immunol Infect 2020;53:505--12.
https://doi.org/10.1016/j.jmii.2020.05.013.

{[}5{]} Kim D, Quinn J, Pinsky B, Shah NH, Brown I. Rates of
Co-infection Between SARS-CoV-2 and Other Respiratory Pathogens. JAMA
2020. https://doi.org/10.1001/jama.2020.6266.

{[}6{]} Lansbury L, Lim B, Baskaran V, Lim WS. Co-infections in people
with COVID-19: a systematic review and meta-analysis. J Infect
2020;81:266--75. https://doi.org/10.1016/j.jinf.2020.05.046.

{[}7{]} Nowak MD, Sordillo EM, Gitman MR, Paniz Mondolfi AE. Coinfection
in SARS-CoV-2 infected patients: Where are influenza virus and
rhinovirus/enterovirus? J Med Virol 2020;92:1699--700.
https://doi.org/10.1002/jmv.25953.

{[}8{]} Visseaux B, Le Hingrat Q, Collin G, Bouzid D, Lebourgeois S, Le
Pluart D, et al. Evaluation of the QIAstat-Dx Respiratory SARS-CoV-2
Panel, the first rapid multiplex PCR commercial assay for SARS-CoV-2
detection. J Clin Microbiol 2020. https://doi.org/10.1128/JCM.00630-20.

{[}9{]} Leber AL, Everhart K, Daly JA, Hopper A, Harrington A,
Schreckenberger P, et al. Multicenter Evaluation of BioFire FilmArray
Respiratory Panel 2 for Detection of Viruses and Bacteria in
Nasopharyngeal Swab Samples. J Clin Microbiol 2018;56.
https://doi.org/10.1128/JCM.01945-17.

{[}10{]} Visseaux B, Le Hingrat Q, Collin G, Ferré V, Storto A, Ichou H,
et al. Evaluation of the RealStar® SARS-CoV-2 RT-PCR kit RUO
performances and limit of detection. Journal of Clinical Virology
2020;129:104520. https://doi.org/10.1016/j.jcv.2020.104520.

{[}11{]} Wirden M, Feghoul L, Bertine M, Nere M-L, Le Hingrat Q, Abdi B,
et al. Multicenter comparison of the Cobas 6800 system with the RealStar
RT-PCR kit for the detection of SARS-CoV-2. J Clin Virol
2020;130:104573. https://doi.org/10.1016/j.jcv.2020.104573.

{[}12{]} Visseaux B, Burdet C, Voiriot G, Lescure F-X, Chougar T,
Brugière O, et al. Prevalence of respiratory viruses among adults, by
season, age, respiratory tract region and type of medical unit in Paris,
France, from 2011 to 2016. PLoS One 2017;12.
https://doi.org/10.1371/journal.pone.0180888.

{[}13{]} Mandelia Y, Procop GW, Richter SS, Worley S, Liu W, Esper F.
Dynamics and predisposition of respiratory viral co-infections in
children and adults. Clinical Microbiology and Infection 2020;0.
https://doi.org/10.1016/j.cmi.2020.05.042.

{[}14{]} RECOVERY Collaborative Group, Horby P, Lim WS, Emberson JR,
Mafham M, Bell JL, et al. Dexamethasone in Hospitalized Patients with
Covid-19 - Preliminary Report. N Engl J Med 2020.
https://doi.org/10.1056/NEJMoa2021436.

{[}15{]} Zhang AJ, Lee AC-Y, Chan JF-W, Liu F, Li C, Chen Y, et al.
Co-infection by severe acute respiratory syndrome coronavirus 2 and
influenza A(H1N1)pdm09 virus enhances the severity of pneumonia in
golden Syrian hamsters. Clin Infect Dis 2020.
https://doi.org/10.1093/cid/ciaa1747.

\textbf{Acknowledgments}

\emph{ED influenza management study group:}

Luisa COLOSI, Romain HELLMANN, Thomas PAVLOVSKY, Daniel Aiham GHAZALI,
Maéva RENOUX, Laure FALQUE-PIERROTIN, Élise DUPEYRAT, Camille RAVAUT,
Parfait KOUADIO, Laurent PEREIRA, Romain NGUYEN, Stéphanie ANTONIOL
POSTIC, Anne Sophie CHAULET, Vittiaroat ING, Philippe KENWAY, Swanie
GIGOT, Karine GAUFFRIAUD, Kadir KALKA, Philippe MOUJAOUI, Lorène RADOU,
Richard CLERY, Michèle MACAUX.

\emph{The virology laboratory team:}

Houria ICHOU, Florence DAMOND, Vincent MACKIEWICZ, Charlotte
CHARPENTIER, Valentine Marie FERRE, Manuella Mireille ONAMBELE GUINDI,
Lucile LARROUY.

\textbf{Conflict of interest:}

None

\textbf{Funding}

This study was not funded.

\textbf{Transparency Declarations}

DB and BV have received funds for speaking at symposia organized on
behalf of Qiagen and has also received funds for research from Qiagen.

\textbf{Previous publication:}

None

\textbf{Figure 1. Temporal distribution of SARS-CoV-2 and other
respiratory viruses during the study period.}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}\selectlanguage{english}
\begin{longtable}[]{@{}llll@{}}
\toprule
\begin{minipage}[b]{0.24\columnwidth}\raggedright\strut
\strut
\end{minipage} & \begin{minipage}[b]{0.24\columnwidth}\raggedright\strut
\textbf{SARS-CoV-2 only} \textbf{(n=249)}\strut
\end{minipage} & \begin{minipage}[b]{0.24\columnwidth}\raggedright\strut
\textbf{SARS-CoV-2 coinfection with another respiratory virus
(n=33)}\strut
\end{minipage} & \begin{minipage}[b]{0.24\columnwidth}\raggedright\strut
\textbf{P-value}\strut
\end{minipage}\tabularnewline
\midrule
\endhead
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Age (Median, IQR)}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
59 (49-73)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
58 (45-69)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.26\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Male gender}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
175 (70\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
24 (73\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.84\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Fever}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
202~(81\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
21 (64\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.037\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Dyspnea}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
137 (55\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
16 (48\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.57\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Expectoration}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
10 (5\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
2 (10\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.6\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Cough}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
184 (74\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
22 (67\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.4\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Myalgia}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
74 (30\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
10 (30\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
1\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Headache}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
36 (14\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
10 (30\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.04\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Symptoms duration, median (IQR)}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
4 {[}3-7{]}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
3 {[}2-7{]}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.26\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{ICU admission, day 1}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
64 (26\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0 (0\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textless{}0.001\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{ICU admission, day 14}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
31 (15\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
3 (9\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.27\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
\textbf{Hospital mortality}\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
49 (20\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
5 (15\%)\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
0.48\strut
\end{minipage}\tabularnewline
\bottomrule
\end{longtable}

\textbf{Table 1. Main clinical characteristics of patients presenting a
SARS-CoV-2 infection with or without any other respiratory viruses
coinfection.}

\selectlanguage{english}
\FloatBarrier
\end{document}

