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S
UPPLEMENT
The Global State of Influenza in Children
Susanna Esposito, MD, Paola Marchisio, MD, and Nicola Principi, MD
Abstract:
Recent data concerning influenza-related hospitalizationrates, deaths, outpatient visits, and drug consumption in otherwisehealthy children have shown that childhood influenza is significantlymore important than once believed. In addition to its clinicalimportance, influenza in healthy children can have substantial so-cioeconomic consequences for children, whose everyday activitiesare disrupted and who lose a significant number of school days, and their household contacts, who are frequently affected by similar illnesses. An overall evaluation of these data show that influenza ininfants and children is a significant clinical and socioeconomic problem and that healthy children appear to be candidates for yearlyvaccinations. Global evaluation of the impact of influenza in pedi-atric patients indicates that influenza vaccination should be morewidely used than is usually recommended. All of the data regardinginfluenza vaccines indicate that the immunogenicity of the available preparations is good, and that they are safe, well-tolerated, and significantly effective in preventing influenza illness and its com- plications in both high-risk and otherwise healthy children. More-over, the economic data indicate that universal childhood influenzavaccination is a low-cost preventive intervention that provideshealth benefits during epidemic and pandemic periods, supporting anextensive use of vaccination in childhood.
Key Words:
influenza, influenza viruses, influenza vaccine,epidemiology, prevention, children(
 Pediatr Infect Dis J 
2008;27: S149–S153)
I
nfluenza is the most common cause of admission of chil-dren to the emergency department (ED) in many countriesduring winter months. Among children admitted to the ED atMilan University’s Institute of Pediatrics during the 2003– 2004 winter season with influenza-like illness (ILI) due toeither influenza, respiratory syncytial virus (RSV), humanmetapneumovirus, coronavirus, rhinovirus, or adenovirus,30% of illnesses were due to influenza virus (Fig. 1).
1
Ratesof ED admissions for children with a laboratory diagnosis of influenza in the first 5 years of life are high. A study amongapproximately 2700 Italian children aged 0–3 and 4–5 yearsfound the rate of ED admission for influenza in the 2001– 2002 season to be 17.4 and 12.9%, respectively.
2
During the2002–2003 season, the rate of admission for ages 0–3 and 4–5 years was 5.5 and 4.4%, respectively.Cardiopulmonary disorder-related admissions duringthe influenza season are high during the first 5 years of life,according to data from a U.S. Medicaid program.
3
The studyshowed that the average excess annual hospitalizations for cardiopulmonary conditions per 10,000 children during aninfluenza season were 104 for children aged 
6 months, 50for those 6 to
12 months, 19 for those 1 to
3 years, 9 for those 3 to
5 years, and 4 for those 5 to
15 years.Investigators also found that, in absence of high-risk condi-tions, the rate of hospital admission for influenza in the first2 years of life was even higher than that observed in adoles-cents and adults with chronic disorders. These findings showthat, in the first 2 years of life, even healthy children are athigher risk of hospitalization than children with illnesses for whom vaccination is specifically recommended. Still, the rateof hospitalization for influenza in children 2–4 years of age isalso relatively high.
4,5
Interplay of Influenza-Like Illnesses
A study of 3310 children revealed that there is a differentdistribution of influenza infection by age and influenza virusstrain (Fig. 2). There is not a significant difference in infectionrates of type A influenza virus across age groups. However, typeB influenza tends to infect school-age children (
5 years of age)more often than children younger than 5 years of age.
6
An overlap exists in the clinical presentation amongdifferent viral infections caused by influenza A and influenzaB as well as infections due to RSV, adenovirus, and other viruses (Table 1).
6,7
Determining the underlying cause of anILI in a child in the ED is complicated by this overlap.Predictably, the number of outpatient visits and courses of antibiotics are also high among children who are positive for ILI infections.
Influenza-Related Deaths and SeriousComplications
A U.S. study of the 153 influenza-related deaths occur-ring during the 2003 and 2004 influenza season in children
18 years of age and reported by state health departmentsrevealed that half of deaths were in previously healthy chil-dren.
8
Only 33% of deceased children had an underlyingdisorder thought to increase the risk of influenza-related complications. A number of the healthy children (63%) were
5 years of age. This study underscores the need to makeinfluenza vaccine coverage a priority.
Complications of Childhood Influenza
Complications of childhood influenza include nosocomialtransmission to hospitalized children with risk factors that makethem vulnerable and neurologic events. A study by Newland et
From the Institute of Pediatrics, University of Milan. Fondazione IRCCSOspedale Maggiore Policlinico, Mangiagalli e Regina Elena, Milan,Italy.
 Disclosure:
The authors report no conflicts of interest.Address for correspondence: Susanna Esposito, MD, Via Commenda 9,20122 Milano Italy. E-mail: susanna.esposito@unimi.it.Copyright © 2008 by Lippincott Williams & WilkinsISSN: 0891-3668/08/2711-0149DOI: 10.1097/INF.0b013e31818a542b
The Pediatric Infectious Disease Journal 
• Volume 27, Number 11, November 2008
S149
 
al showed that influenza in children between 6 and 23 months of age was a risk factor for neurologic complications, mainlyseizures.
9
Among the study’s 842 children who were hospital-ized with influenza, 72 had at least one neurologic complication(mostly seizures) related to influenza. The study also showed that independent risk factors for influenza-related neurologiccomplications were an age of 6–23 months and underlyingneurologic or neuromuscular disorders.
Cost of Influenza
The high cost of influenza is associated largely withtherapeutics, particularly antibiotics and antipyretics, and to a
FIGURE 1.
Distribution of respiratory viruses during the winter season of 2003–2004. Data adapted from Esposito S, Bosis S,Niesters HG, et al.
J Med Virol 
. 2006;78:1609–1615.
FIGURE 2.
Age distribution of swabs positive for influenza A and B in study children. Data adapted from Esposito S, Bosis S,Niesters HG, et al.
J Clin Microbiol 
. 2008;46:1337–1342.
TABLE 1.
Main Clinical Characteristics of Children With Infections Caused by a Single Virus (%)
HBoV(n
49)RSV(n
121)Flu(n
151) Adeno(n
70)Parainfl(n
21)Rhino(n
74)HCoV(n
36)hMPV(n
2)Upper ARI 85.7* 32.2 66.2 61.4 76.2 62.2 69.4 0Lower ARI 4.0 57.0* 23.2 5.8 0 57.0 13.9 100.0GI disease 10.2 9.1 4.0 25.7* 11.1 10.8 14.3 0Fever WS 0 1.7 6.6 1.4 5.6 2.7 9.5 0Exanthema 0 0 0 5.7 0 8.1 0 0
*P
0.05 vs. at least one of the other viral groups. Adapted from Esposito S, Bosis S, Niesters HG, et al.
J Clin Microbiol.
2008;46:1337–1342.
 Esposito et al 
The Pediatric Infectious Disease Journal 
• Volume 27, Number 11, November 2008
© 2008 Lippincott Williams & Wilkins
S150
 
lesser degree with diagnostics, room costs, and supplies.
7,10
Costs related to prevention include those to patients as well asthose absorbed by the healthcare system. These costs arelikely to be greater for management of influenza in children
6 months of age but are certainly a consideration in older children, regardless of the presence of high-risk conditions.
Socioeconomic Impact
Data from the United States and Europe reveal that thesocioeconomic burden of influenza on both children and their families is significant (Table 2). Data from the households of children with influenza reveal that outpatient and ED visits;antipyretic, antibiotic, and other medication use; and lost parental or sibling work days is high, even higher than thatobserved for RSV.
7,11
Reconsidering Strategies for Prevention
Given the healthcare burden of influenza in children,we have to reconsider our strategies for its prevention. Inkeeping with this, the World Health Organization (WHO) hasrecommended a vaccine for the 2008–2009 influenza seasonin the Northern Hemisphere that differs from the one recom-mended for the Southern Hemisphere by 1 viral type.
12,13
Specifically, the WHO recommends that influenza vac-cine for the 2008–2009 influenza season in the NorthernHemisphere contain the following constituents:an A/Brisbane/59/2007 (H1N1)-like virusan A/Brisbane/10/2007 (H3N2)-like virusa B/Florida/4/2006-like virusThe WHO recommends that vaccines used in theSouthern Hemisphere for the 2008–2009 season contain thefollowing constituents:an A/Solomon Islands/3/2006 (H1N1)-like virusan A/Brisbane/10/2007 (H3N2)-like virusa B/Florida/4/2006-like virusThe recommendation by the WHO for annual vaccina-tion is an attempt to provide an adequate overlap between thevaccine and the circulating viruses. Annual changes in influ-enza vaccine composition are necessary because circulatinginfluenza viruses in humans usually develop permanent anti-genic changes that require annual modification of the influ-enza vaccine formulation. Updates in influenza vaccine com- position should ensure the closest possible match between theinfluenza vaccine strains and the circulating influenza strains.Authorities worldwide recommend vaccination for allchildren
6 months of age who have chronic pulmonary,cardiovascular, renal, hepatic, metabolic, diabetic, or immu-nologic disorders or conditions that can compromise respira-tory function or increase the risk of aspiration.
14
Moreover,vaccination is recommended for pediatric patients aged 
6months who are receiving long-term aspirin therapy and areat risk for developing Reye syndrome.
14
Data on actual coverage in different countries show thatcompliance to these recommendations is low. Our study of the rate of influenza vaccination in Italian children at highrisk for influenza complications due to chronic illness during3 recent influenza seasons revealed that the rate of vaccina-tion was sorely inadequate (Fig. 3).
15
Of the 5286 study participants aged 
14 years who were seen in an ED oneither of 2 days between 1 January and 30 April 2003, 274(5.2%) were judged high-risk. Use of influenza vaccine had increased significantly by the final season (2000–2001, 5.1%;2001–2002, 12.9%; 2002–2003, 26.3%;
P
0.001). Lowestvaccination rates occurred in children with asthma or cardiacdisease. Our findings are consistent with data from other countries showing that the vaccination rate of high-risk chil-dren is 15–35%.Parents of unvaccinated high-risk children (n
202)gave the following reasons for lack of vaccination: lack of awareness, 173 (85.6%); inconvenience, 11 (5.5%); and con-cern about side effects, 18 (8.9%).
15
Parents of vaccinated high-risk children (n
72) gave the following reasons for having their children vaccinated: pediatrician’s recommenda-tion, 63 (87.5%); protection of parents, 6 (8.3%); protectionof family elders, 2 (2.8%); and previous serious influenza-likeillness, 1 (1.4%).
15
Our finding that most compliance to therecommendation for vaccination of high-risk children wasassociated with a pediatrician’s recommendation suggeststhat we should make certain that physicians who care for children with chronic disorders are informed about the epi-
TABLE 2.
Socioeconomic Impact of Infections Due tohMPV, RSV, Influenza on Households
hMPV
HouseholdsRSV
HouseholdsInfluenza
HouseholdsSimilar disease tothe study child16 (12.5%)* 24 (4.7%) 78 (9.7%)*Outpatient visits 16 (12.5%)
†
16 (3.2%) 78 (9.7%)
†
 Antipyretic use 14 (10.9%)* 18 (3.6%) 104 (12.9%)
†
 Antibiotic use 6 (4.7%) 11 (2.2%) 36 (4.5%)Hospitalization 0 0 3 (0.4%)Days lost from work(median, range)4 (2–10)* 2.5 (2–7) 4 (1–10)*Days lost from school(median, range)4 (3–15)* 2 (2–4) 5 (1–15)*
*
 P
0.05 and
†
 P
0.001 vs. RSV
households. Adapted from Principi N, Esposito S, Bosis S.
N Engl J Med.
2004;350:1788–1790.
FIGURE 3.
Influenza vaccination rates among 5286 Italianchildren. Data adapted from Esposito S, Marchisio P,Droghetti R, et al.
Vaccine 
. 2006;24:5251–5255.
The Pediatric Infectious Disease Journal 
• Volume 27, Number 11, November 2008
Influenza in Children
© 2008 Lippincott Williams & Wilkins
S151
of 00

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