Influenza in children

Copyright © 2017 Wolters Kluwer Health, Inc. All rights reserved.
CURRENT
OPINION Influenza in children
Janienne Kondrich and Michele Rosenthal
Purpose of review
We review the current information and evidence available on the global burden of disease in the pediatric
population, clinical presentation and complications, testing, treatment, and immunization.
Recent findings
In addition to multiple other risk factors for influenza complications, children with neurologic and
neuromuscular disorders are significantly higher risk for serious complications. In practice, there is no lower
age limit for children with influenza who can be treated with oseltamivir. The quadrivalent live attenuated
influenza vaccine was not recommended for use during the 2016–2017 season due to poor effectiveness.
Summary
Influenza infection causes a significant burden of disease each year in the pediatric population worldwide.
Both healthy and chronically ill children can fall prey to complications either due to the virus itself or
secondary bacterial infection. Children within high-risk groups should be tested and treated with
neuraminidase inhibitors. Immunization against influenza is well tolerated and effective.
Keywords
influenza complications, influenza virus, neuraminidase inhibitors
INTRODUCTION
Influenza is a highly infectious virus that was
responsible for deadly pandemics throughout the
19th and 20th centuries and has caused millions of
deaths worldwide. The high rate of morbidity and
mortality in children and young adults during the
2009 H1N1 pandemic heightened our awareness of
influenza and its potential complications. In the
acute care setting, it can be challenging to ascertain
which of those patients with influenza-like illness
should be tested and treated. This article will review
the clinical presentations of influenza and risk fac-
tors for complications in the pediatric population, as
well as discuss current diagnostic testing options,
recommendations for testing and management, and
vaccine efficacy and safety.
BURDEN OF DISEASE
Although serious illness can occur in all ages, chil-
dren disproportionately bear the burden of influ-
enza infection. Rates of infection are consistently
highest in children [1,2], and each year approxi-
mately 870 000 children aged less than 5 years are
hospitalized worldwide due to influenza [3
&
]. A
meta-analysis by Nair et al. [4] estimated that
between 28 000 and 111 500 deaths in children aged
less than 5 years are attributable to influenza-related
causes, the vast majority of which occur in devel-
oping countries. In the United States, pediatric
death due to influenza became a nationally notifi-
able condition in late 2004. Since that time, the
number of reported influenza-associated deaths in
children per season has ranged from 37 to 171, with
the notable exception of 358 deaths during the 2009
pandemic [5
&
].
VIRAL TRANSMISSION
Human-to-human transmission of influenza occurs
via both large respiratory droplets and contact.
Large (>5 mm in diameter) droplets are formed when
an infected individual coughs, sneezes, or talks.
Most often these droplets are then inhaled by a
susceptible person or, less frequently, are spread
by contact, either from direct contact with an
infected person or indirectly via fomites [6,7]. The
Division of Pediatric Emergency Medicine,Weill Cornell Medical College,
New York Presbyterian Hospital, New York, New York, USA
Correspondence to Janienne Kondrich, MD, Division of Pediatric Emer-
gency Medicine, Weill Cornell Medical College, New York Presbyterian
Hospital, 525 East 68th Street, M130, New York, NY 10065, USA.
Tel: +1 212 746 0780; e-mail: jak7009@med.cornell.edu
Curr Opin Pediatr 2017, 29:297–302
DOI:10.1097/MOP.0000000000000495
1040-8703 Copyright ß 2017 Wolters Kluwer Health, Inc. All rights reserved. www.co-pediatrics.com
REVIEW

incubation period is between 1 and 4 days with peak
viral shedding occurring 2–3 days after illness onset
[8]. When compared with adults, both the viral load
and the duration of viral shedding are higher in
children [9].
CLINICAL PRESENTATION
Uncomplicated influenza characteristically begins
with the abrupt onset of fever, diffuse myalgia,
malaise, and headache, which is then rapidly fol-
lowed by development of nonproductive cough,
nasal congestion, rhinitis, and sore throat. Gastro-
intestinal symptoms are less commonly associated
with influenza but do occur for 10–30% of children.
In one study of children with laboratory-confirmed
influenza, fever was the most prominent sign,
followed closely by rhinitis and cough. Ninety-five
percent of children in this cohort presented as
febrile, with the highest fevers seen most often in
children aged younger than 3 years [10].
COMPLICATIONS
Although for most children influenza is a self-lim-
ited infection with resolution of symptoms after
about a week of illness, many pediatric patients
experience complications. Both previously healthy
and chronically ill children are potentially suscept-
ible to complications, which range from more minor
complications such as acute otitis media (AOM)
[10], to significant illness including respiratory fail-
ure and death [11,12].
Secondary bacterial infections frequently occur
and are most often due to Streptococcus pneumoniae
and Staphylococcus aureus [12,13]. AOM often
accompanies influenza infection, occurring in
approximately one-third of young children
[14,15]. Pneumonia is an important complication
from influenza and can lead to hospitalization,
respiratory failure, and death. The virus itself
increases susceptibility to pneumonia, typically
1 week after initial influenza infection [16]. In
one study, approximately of one-third of pediatric
patients with laboratory-confirmed influenza
developed complications, the most common of
which was pneumonia occurring in 22% of patients
[11]. Pneumonia secondary to methicillin-resistant
S. aureus in children and young adults has a rapid
clinical progression and a high fatality rate [17].
Nonrespiratory complications secondary to
influenza also occur. Acute myositis can follow both
influenza A and B virus infections. Affected patients
present with muscle pain and tenderness, most
commonly of the calves, and inability to ambulate,
at times leading to severe rhabdomyolysis, myoglo-
binuria, and acute kidney injury [2,18]. Although
rare in children, neurologic complications of influ-
enza are more common in children than adults and
include febrile seizures, transverse myelitis, ence-
phalopathy, and Guillain–Barre´ syndrome (GBS)
[2,19]. Myopericarditis due to influenza infection,
at times fulminant and subsequently fatal, has been
reported [20].
RISK FACTORS FOR COMPLICATED
INFLUENZA
Younger children and pediatric patients with certain
medical comorbidities are at a higher risk of com-
plications from influenza. According to the Centers
for Disease Control (CDC), children less than 5 years
of age, particularly those aged younger than 2 years,
are at higher risk. The risk of severe complications
from influenza is highest among children aged
less than 2 years who have much higher rates of
hospitalization for influenza-related complications
compared with older children [21]. Pediatric
patients with chronic pulmonary disease including
asthma, underlying hemodynamically significant
cardiac disease, neurologic or neurodevelopmental
conditions, sickle cell disease, and other hemo-
globinopathies, immunosuppression, HIV infec-
tion, morbid obesity, metabolic disease including
diabetes, who are pregnant or are within 2 weeks
post partum have also all been identified as being
higher risk [22,23
&&
]. Patients who are on long-term
aspirin therapy after Kawasaki disease or repair of
congenital heart disease who then contract influ-
enza infection are at risk for developing Reye’s
syndrome.
KEY POINTS
Influenza infection disproportionately affects infants and
young children.
Children under the age of 2 years or those children
with chronic pulmonary disease, underlying cardiac
disease, chronic renal dysfunction, neurologic or
neurodevelopmental conditions, immunosuppression,
morbid obesity, diabetes, on aspirin therapy, or who
are pregnant or have recently given birth are at higher
risk of influenza complications.
Patients at increased risk of complications, or others for
whom antiviral treatment is indicated who present with
symptoms consistent with influenza, including fever
alone, should be tested for influenza.
Oral oseltamivir, which may modestly reduce duration
of symptoms and decrease risk of mortality from
influenza, remains the treatment of choice.
Emergency and critical care medicine
298 www.co-pediatrics.com Volume 29 Number 3 June 2017

A systematic review and meta-analysis by Gill
et al. [24] in 2015 sought to further define which
children were at increased risk of influenza compli-
cations and found that prematurity, neurological
disorders, sickle cell disease, immunosuppression,
diabetes, and age younger than 2 years were all risk
factors for hospital admission, and that the presence
of more than one of these risk factors increased the
risk of hospital admission from 52 to 74%. In con-
trast to the CDC guidelines, this review did not find
obesity or asthma to be risk factors. Another pro-
spective study of influenza-like infections found
children with known neurologic or neuromuscular
conditions at substantially higher risk of compli-
cations [11].
DIAGNOSTIC TESTING
In the acute care setting, the prompt diagnosis of
influenza is key to guiding necessary workup and
treatment, yet clinical diagnosis can be challenging,
as the symptoms of influenza are nonspecific and
difficult to distinguish from other respiratory
viruses. Influenza testing methods range from quick
bedside tests to viral cultures that can take over a
week to result. Nasopharyngeal swabs and nasal
wash or aspirates are the preferred samples and
are ideally collected within 3–4 days of symptom
onset [25].
Rapid influenza diagnostic tests (RIDT) use anti-
gen detection and provide results in less than
15 min. RIDTs work effectively to diagnose influ-
enza as most have a specificity of greater than 97%.
However, most RIDTs used are only 50–70% sensi-
tive, making it difficult to exclude influenza due to a
large number of false negatives [9]. Of note, when
tested in children RIDTs had sensitivities closer to
the higher end of this range, likely due to the higher
viral loads and increased viral shedding in infants
and young children [9]. With such a large number of
false negatives of RIDTs, we recommend confirming
the results with another diagnostic test, and to limit
using RIDTs to individuals for whom the probably of
influenza infection is high [26,27]. To minimize
false results, it is recommended to send samples
for reverse-transcriptase PCR (RT-PCR) to confirm
results if the RIDT is positive and community influ-
enza activity is low, or for a negative RIDT, but
influenza activity in the community is high [27].
RT-PCR works by detecting viral RNA in the
samples. RT-PCR has replaced viral culture as
the gold standard for influenza diagnosis as it is
the most sensitive and specific test for influenza,
can differentiate between viral types and subtypes,
and can provide results within hours [25,27]. The
disadvantages to using RT-PCR and other molecular
assays are that they are not universally available,
are generally more expensive than other testing
modalities, and, depending on the capabilities of
the hospital in which the test is performed, may
provide results later than is necessary to inform
clinical management.
Increasing the diagnosis rate of influenza
benefits those with high-risk conditions who would
require treatment, or for admission cohorting [25].
Testing of any modality does not need to be sent on
those patients who do not meet treatment criteria.
However, proven influenza infection may in some
cases decrease unnecessary laboratory and radio-
logic studies [28].
TREATMENT
Two classes of antivirals are available for treatment
of influenza infection: the neuraminidase inhibitors
(NAIs) and the amantadanes. Of these two, only the
NAIs are consistently effective. The amantadanes,
amantadine and rimantadine, work specifically to
inhibit replication of influenza A and widespread
resistance among influenza A H3N2 and 2009 H1N1
virus strains has been reported [22]. Neither aman-
tadine nor rimantadine are recommended for use as
either treatment for or prophylaxis against influenza
infection.
The NAIs are active against both influenza A and
B. Less than 1% of circulating influenza strains have
exhibited resistance to the NAIs [5

]. The two NAIs
approved for treatment of children are oseltamivir
and zanamivir. Peramivir, another NAI, is currently
licensed for use in adults only. Laninamivir is a long-
acting NAI that is currently still investigational in
the United States but is approved for treatment and
prophylaxis of influenza in Japan [29].
Oseltamivir is available only in an oral formu-
lation and remains the treatment of choice. It has
been licensed by the Food and Drug Administration
(FDA) for treatment of influenza in children as
young as 2 weeks of age; however, oseltamivir can
be used in younger infants as well as the benefits of
treatment likely outweigh any risks [23

]. The
primary adverse effects of oseltamivir are nausea
and vomiting. Reports of neuropsychiatric symp-
toms in pediatric patients in Japan that were initially
thought to be adverse effects of the drug are now
believed to be secondary to the virus itself [23

,30].
Inhaled zanamivir can be difficult to administer,
particularly in younger children. It is approved by
the FDA for treatment of influenza in patients aged
7 years and older, and for prophylaxis in patients
aged 5 years and older. Zanamivir has been associ-
ated with bronchospasm and is not recommended
for use in patients with underlying respiratory
Influenza in children Kondrich and Rosenthal
1040-8703 Copyright ß 2017 Wolters Kluwer Health, Inc. All rights reserved. www.co-pediatrics.com 299

disease including asthma. Intravenous zanamivir,
currently only an investigational drug in the United
States, can be obtained for treatment of critically ill
patients on a compassionate-use basis, particularly
those who are immunocompromised or for whom
oral oseltamivir is not any option [23

].
Antiviral treatment should be offered to all
children with severe, complicated or progressive
respiratory illness due to confirmed or suspected
influenza infection. For severely ill patients, treat-
ment should not be delayed waiting for confirma-
tory lab results nor should immunization status or
time from onset of symptoms affect the decision to
treat. Children at high-risk of influenza compli-
cations should be treated when presenting with
influenza-like illness of any severity [23

]. Treat-
ment should also be considered in otherwise
healthy children with either clinically presumed
or testing confirmed influenza infection, particu-
larly those patients with contacts at home who
could not be immunized or whose underlying
medical condition puts them at risk for influenza
complications.
Treatment efficacy
There is some evidence that treatment with NAIs,
specifically oseltamivir, can result in shortened ill-
ness course and improve survival. For the greatest
benefit, treatment should be started as soon as
possible after symptom onset, ideally within 48 h.
Treatment of influenza with oseltamivir can reduce
duration of symptoms by 0.5–3.5 days [22,31], but
data on the effect of treatment with viral shedding
have been inconsistent [22]. Decreased mortality
has been seen in critically ill children with influenza
who were treated with NAIs, particularly when given
within the first 48 h of symptom onset as opposed to
later in the illness course [32].
POSTEXPOSURE PROPHYLAXIS
Oseltamivir and zanamivir are also effective when
given as chemoprophylaxis and are ideally started
within 48 h of exposure. Chemoprophylaxis is
recommended for the following children: those at
high risk of influenza complications but for whom
the influenza vaccine is contraindicated, for high
risk children who are exposed during the 2 weeks
after vaccination prior to achieving peak immunity,
for unimmunized children in institutional settings
for the purposes of control of an influenza outbreak,
as a supplement to immunocompromised children
at high risk who had been immunized, and for high-
risk children when circulating strains of influenza
virus in the community do not match the strains
within the vaccine. Chemoprophylaxis is not recom-
mended for children younger than 3 months [23

].
IMMUNIZATION
Influenza vaccines are developed each year based on
global monitoring and epidemiologic surveillance
regarding the anticipated circulating strains. For the
2016–2017 season, the trivalent vaccine contained
two influenza A viruses (H1N1 and H3N2) and one
influenza B virus. The quadrivalent vaccines
included these and an additional influenza B virus.
In the United States, the CDC recommends that
everyone 6 months of age and older receive immu-
nization against influenza with few exceptions.
Children aged younger than 9 years who are receiv-
ing the influenza vaccine for the first time or who
have received only one dose of vaccine per season
should receive two doses. As of fall of 2016, the CDC
recommended use of only the intramuscular influ-
enza vaccine (inactivated influenza vaccine or IIV3
or IIV4) or the recombinant influenza vaccine. The
live attenuated influenza vaccine (LAIV), a quadri-
valent vaccine administered intranasally, was not
used during the 2016–2017 season, stemming from
data demonstrating ineffectiveness or lower than
expected effectiveness over the previous three
seasons [33,34].
Vaccine efficacy
Vaccine efficacy depends on many factors, includ-
ing the age of the vaccine recipient and the match
between virus strains in the vaccine and those cir-
culating that season. The influenza vaccine prevents
illness from influenza and decreases the severity of
illness in those immunized persons who do contract
the virus [35]. There is a decreased risk of hospital-
ization and pediatric intensive care unit admission
from influenza in those who are immunized [36,37]
and pregnant women who are immunized against
influenza may reduce the risk of illness in their
babies by half, for as long as 4 months after birth
[37].
Vaccine safety
The most common reactions to the influenza
vaccine are local injection site reactions including
pain, erythema, swelling, induration, and ecchymo-
sis, along with systemic reactions of malaise, myal-
gia, headache, rigors, and fever. Immunization
reactions typically occur within 3 days of injection
and can last for up to 3 days. There was no difference
in rates or types or severity of reactions between
recipients of trivalent (IIV3) and quadrivalent (IIV4)
vaccines [38].

More serious reactions are rare, and beliefs that
the influenza vaccine is the cause of increased febrile
seizures, hospitalization, and death have recently
been dispelled. There is no independent increased
risk of febrile seizures with the administration of
IIV3 alone. However, when given with either pneu-
mococcal conjugate vaccine or DTaP vaccines, the
risk is somewhat increased [39]. Influenza vaccina-
tion also does not increase risk of hospitalization or
death: two recent studies proved no increased hos-
pitalization risk to nonasthma, nonimmunocom-
promised patients after LAIV, and a noncausal
relationship between deaths and vaccination within
30 days [33,40].
Two severe reactions that have been found to
have increased incidence following administration
of the influenza vaccine, and therefore have
received more attention and specific guidelines,
are GBS and anaphylaxis.
Guillain–Barre´ syndrome
The 1976 swine influenza vaccine was associated
with an increased frequency of GBS, estimated at
one additional case of GBS per 100 000 vaccinated
persons [33]. Since then, the incidence has not been
found to be nearly that high. The estimated risk for
GBS is slightly elevated at one additional case per 1
million vaccinated, with a greater risk for pandemic
vaccines [40]. Despite the elevated risk of GBS after
vaccination, it is still significantly lower than the
risk observed following influenza infection [41]. The
cumulative risk for GBS is expected to be greater
among those with a history of GBS; those known to
have GBS within the prior 6 weeks should not be
vaccinated [40].
Anaphylaxis
Anaphylaxis after influenza vaccination is rare. The
incidence of anaphylaxis after immunization is 1.31
cases per million vaccine doses in all ages [42]. The
influenza vaccine contains small amounts of egg
protein that has not been shown to cause significant
reactions in those with proven egg allergies [43]. The
current recommendation for egg-allergic patients is
for these patients to be immunized against influenza
despite a known allergy. The 30-min observation
period postvaccine administration has also been
lifted, with the exception of those with severe egg
allergies who should receive the vaccine in a medical
setting supervised by a trained healthcare provider.
CONCLUSION
The burden of influenza illness disproportionately
affects the pediatric population worldwide. Certain
children, either due to age or chronic medical con-
ditions, are at higher risk of influenza-associated
complications. We recommend that the children
within these high-risk groups be tested for influenza
using RT-PCR if available and then treated with
NAIs as soon as possible after symptom onset. We
also recommend treatment of all hospitalized and
severely ill children with suspected or laboratory-
confirmed influenza, regardless of illness duration
or immunization status as the potential benefits far
outweigh the risk.
Acknowledgements
None.
Financial support and sponsorship
None.
Conflicts of interest
There are no conflicts of interest.
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READING
Papers of particular interest, published within the annual period of review, have
been highlighted as:
of special interest
of outstanding interest
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