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Article |

Children Hospitalized With 2009 Novel Influenza A(H1N1) in California FREE

Janice K. Louie, MD, MPH; Shilpa Gavali, MPH; Meileen Acosta, MPH; Michael C. Samuel, DrPH; Kathleen Winter, MPH; Cynthia Jean, MPH; Carol A. Glaser, MD, DVM; Bela T. Matyas, MD, MPH; Robert Schechter, MD, MPH; California Pandemic (H1N1) Working Group
[+] Author Affiliations

Author Affiliations: Division of Communicable Disease Control, California Department of Public Health, Richmond.


Arch Pediatr Adolesc Med. 2010;164(11):1023-1031. doi:10.1001/archpediatrics.2010.203.
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Objective  To describe clinical and epidemiologic features of 2009 novel influenza A(H1N1) in children.

Design  Analysis of data obtained from standardized report forms and medical records.

Setting  Statewide public health surveillance in California.

Participants  Three hundred forty-five children who were hospitalized with or died of 2009 novel influenza A(H1N1).

Main Exposure  Laboratory-confirmed 2009 novel influenza A(H1N1).

Main Outcome Measures  Hospitalization and death.

Results  From April 23 to August 11, 2009, 345 cases in children younger than 18 years were reported. The median age was 6 years. The hospitalization rate per 100 000 per 110 days was 3.5 (0.97 per 100 000 person-months), with rates highest in infants younger than 6 months (13.9 per 100 000 or 3.86 per 100 000 person-months). Two-thirds (230; 67%) had comorbidities. More than half (163 of 278; 59%) had pneumonia, 94 (27%) required intensive care, and 9 (3%) died; in 3 fatal cases (33%), children had secondary bacterial infections. More than two-thirds (221 of 319; 69%) received antiviral treatment, 44% (88 of 202) within 48 hours of symptom onset. In multivariate analysis, congenital heart disease (odds ratio [OR], 5.0; 95% confidence interval [CI], 1.9-13.5) and cerebral palsy/developmental delay (OR, 3.5; 95% CI, 1.7-7.4) were associated with increased likelihood of intensive care unit admission and/or death; likelihood was decreased in Hispanic (OR, 0.4; 95% CI, 0.2-0.8) and black (OR, 0.3; 95% CI, 0.1-1.0) children compared with white children.

Conclusions  More than one-quarter of children hospitalized with 2009 novel influenza A(H1N1) reported to the California Department of Public Health required intensive care and/or died. Regardless of rapid test results, when 2009 novel influenza A(H1N1) is circulating, clinicians should maintain a high suspicion in children with febrile respiratory illness and promptly treat those with underlying risk factors, especially infants.

Figures in this Article

Following the detection of the first cases of 2009 novel influenza A(H1N1) in California in April 2009, the virus has rapidly spread throughout the world.1,2 In the United States, observations suggest that most cases of 2009 novel influenza A(H1N1) are in children or young adults, with 40% of cases in children between the ages of 10 and 18 years; the attack rate in children aged 5 to 14 years (147 per 100 000) has been higher than that of adults 60 years and older (10.5 per 100 000).38

Data are still emerging on the impact of 2009 novel influenza A(H1N1) in children. Early in the pandemic, reviews of hospitalized cases from the United States and Canada found a high proportion of patients with chronic comorbidity, predominantly asthma, with 20% to 30% requiring intensive care.811 In these studies, the overall case-fatality proportions were low (about 1%); in contrast, fatality rates of children hospitalized with 2009 novel influenza A(H1N1) in Argentina were 10-fold higher than prior rates from seasonal influenza.12 In this report, we describe the first 345 children hospitalized with 2009 novel influenza A(H1N1) reported to the California Department of Public Health (CDPH) and analyze clinical and epidemiologic risk factors associated with severe illness and death.

Since April 23, 2009, CDPH and 61 local health jurisdictions have requested that clinicians report hospitalized or fatal cases of 2009 novel influenza A(H1N1) to their local health jurisdiction. A hospitalized case is defined as a person hospitalized for 24 hours or more with influenza-like symptoms (eg, fever plus cough, sore throat, or clinical suspicion for influenza infection) and a polymerase chain reaction test result indicative of 2009 novel influenza A(H1N1).13 Fatal cases had influenza-like symptoms, confirmation by polymerase chain reaction test results, and influenza listed in the death certificate as a cause of death. Cases were first reported by clinicians to local health jurisdictions and subsequently reported to CDPH using a standardized form. Data on height and weight, demographics, clinical presentation and course, comorbid conditions, and laboratory and radiographic findings were abstracted from medical records by local health jurisdiction or CDPH staff. A comorbid condition was considered to be any chronic medical condition recorded in the medical record, or in the case of obesity, height and weight data that indicated a body mass index (calculated as weight in kilograms divided by height in meters squared) in the 95th percentile or higher for age in persons older than 2 years.14 Secondary infection was defined by isolation of bacteria from a (1) sterile site or (2) lower respiratory tract specimen in conjunction with a new infiltrate on chest radiography.

Hospitalized children who required intensive care unit (ICU) admission and/or died were compared with hospitalized children who did not require ICU admission and/or die with respect to demographics, clinical characteristics, and underlying risk factors using bivariate analysis. Comorbid conditions were not treated as mutually exclusive; if a child had multiple comorbid conditions, each condition was included in the analysis. Individuals who did not have underlying medical conditions coded in the medical records were excluded in the bivariate analysis. In multivariate analysis, a “missing” category was created for all variables. Variables that were considered preexisting risk factors (eg, demographic data or comorbidities) that had a P value ≤.05 in the bivariate analysis were included in a multivariate logistic regression model using SAS 9.2 (SAS Institute, Cary, North Carolina); variables that were not considered preexisting risk factors (eg, clinical signs and symptoms, laboratory or radiographic findings, and events occurring during the hospital course) were not included in the model. Calculations of confidence intervals (CIs) for age-specific rates were conducted using the epitools package of R (http://cran.r-project.org/web/packages/epitools/index.html).

This activity was reviewed by the California Committee for the Protection of Human Subjects and deemed a public health response that did not require institutional review board approval (http://www.oshpd.ca.gov/Boards/CPHS/researchers.html).

DEMOGRAPHICS AND INCIDENCE RATES

Between April 23 and August 11, 2009, 345 of 1090 hospitalized and fatal 2009 novel influenza A(H1N1) cases (32%) reported in California were children younger than 18 years (Figure 1), including 68 infants (6%) younger than 12 months. The median age was 6 years (range, 1 week-17 years; with 30% younger than 2 years), and 59% were male. In the 297 children in whom data were available, the most common reported race/ethnicity was Hispanic (152; 51%), followed by non-Hispanic Asian/Pacific Islander (55; 19%) and non-Hispanic white (48; 16%) (Table 1). Nine children (3%) died. The rate of hospitalization and/or fatality was 3.5 per 100 000 population per 110 days of observation (or 0.97 per 100 000 person-months), ranging from 2.4 for 12- to 17-year-olds (0.67 per 100 000 person-months) to 13.9 for infants younger than 6 months (3.86 per 100 000 person-months) during the same period (Figure 2).

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Figure 1.

No. of hospitalized and/or fatal cases with 2009 novel influenza A(H1N1) in children aged 0 to 17 years in California by date of symptom onset, reported April 23 to August 11, 2009 (n = 335).

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Figure 2.

Rate of hospitalization and/or fatality by age group. *Per 110 days of observation.

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Table Graphic Jump LocationTable 1. Demographic Characteristics of Hospitalized and/or Fatal Pediatric Cases of 2009 Novel Influenza A(H1N1) in Children Aged 0 to 17 Years in California, Reported April 23 to August 11, 2009
CHRONIC COMORBID ILLNESSES

Comorbid conditions reported in 345 children (67%) are shown in Table 2. Two-hundred twelve (61%) had Advisory Committee on Immunization Practices (ACIP) risk factors for severe influenza15,16; the most common were chronic pulmonary disease (including asthma), underlying neurologic disorders (including cerebral palsy/developmental delay and seizure disorder), and immunosuppression. Of 80 children with asthma in which admitting diagnosis was recorded, 19 (24%) were admitted for asthma exacerbation. Ninety-four children (28%) had other conditions not currently considered by ACIP as risk factors, including gastrointestinal disorders and history of prematurity (birth at gestational age ≤36 weeks). In addition, body mass index data were available in 124 hospitalized children; 23 (19%) were obese. Only 19 infants (28%) younger than 1 year had underlying conditions, most commonly chronic lung disease associated with prematurity (9; 47%) or prematurity (8; 42%).

Table Graphic Jump LocationTable 2. Chronic Comorbid Conditions of Hospitalized and/or Fatal Pediatric Cases of 2009 Novel Influenza A(H1N1) in Children Aged 0 to 17 Years in California, Reported April 23 to August 11, 2009
SYMPTOMS, SIGNS, AND CLINICAL COURSE

The symptoms or signs present in the study subjects are shown in Table 3. The median time from symptom onset to hospitalization was 2 days (range, 0-21 days). The most frequent symptoms or signs reported included fever, cough, shortness of breath or increased work of breathing, nausea or vomiting, diarrhea, and muscle aches. Of 27 infants hospitalized younger than 2 months, 21 (78%) were admitted with fever to evaluate potential invasive bacterial infection (“rule out sepsis”).

Table Graphic Jump LocationTable 3. Symptoms and Clinical Course and Findings of Hospitalized and/or Fatal Pediatric Cases of 2009 Novel Influenza A(H1N1) in Children Aged 0 to 17 Years in California, Reported April 23 to August 11, 2009

Central nervous system manifestations observed in 30 children (8.7%) included seizures (n = 17), altered mental status/delirium (n = 18), or both (n = 12). Presentation with seizures (P = .01) or altered mental status (P < .001) was significantly associated with ICU admission or death (Table 3). Eleven of these 30 children (37%) had preexisting cerebral palsy/developmental delay or seizure disorder. Seventeen of these 30 children (57%) were hospitalized in the ICU. The median length of stay for these children with neurologic symptoms was 4 days (range, 1-24 days).

Two hundred twenty-one of 261 children (85%) tested had positive enzyme immunoassay or direct fluorescent assay results. Of 278 children with chest radiographs or computed tomography, 163 (59%) had infiltrates suggestive of pneumonia or acute respiratory distress syndrome. Ninety-four of the 345 children (27%) required intensive care, of whom 35 (37%) required mechanical ventilation. There was no difference in the median duration between onset of symptoms and hospitalization among ICU and/or fatal cases (2 days) as compared with non-ICU, nonfatal cases (2 days) (P value = .87). Fifteen patients (4%) had evidence of a secondary bacterial infection. The median length of stay for all hospitalized cases was 3 days (range, 1-73 days) (Table 3).

For 319 children for whom data were available, 221 (69%) received antiviral treatment; more children with ACIP risk factors than those without were treated (74% [145 of 196] vs 62% [76 of 123]; P = .03). Eighty-eight of 202 children (44%) with available data received antiviral treatment within 48 hours of symptom onset; this proportion was similar for those with and without ACIP risk factors (42% vs 46%; P = .66). Seventy-three children were seen by a primary care provider for influenza-like symptoms prior to hospitalization, including 53 (73%) within 48 hours after onset of symptoms. Thirty-eight (72%) of these 53 children had available data on antiviral treatment; 11 (29%) were treated within 48 hours of symptom onset. Of the 116 children hospitalized within 48 hours of onset of symptoms and for whom dates of antiviral treatment are known, 79 (69%) received antiviral treatment within 48 hours of symptom onset.

FATAL CASES

Nine children (3%) died; their median age was 5 years (range, 6 months-14 years). Two of these children were declared dead on arrival in the hospital emergency department and had not been evaluated as outpatients prior to death. In 8 fatal cases (89%), children had comorbid illness, including neurologic disorders (n = 5, including 4 with cerebral palsy/developmental delay), chronic pulmonary disease (n = 4), immunosuppression (n = 3), chronic heart disease (n = 3), prematurity (birth at ≤32 weeks) (n = 3), and gastrointestinal disorders (n = 2). Three of the deaths were in children younger than 2 years and therefore body mass index could not be calculated; of the 6 remaining children, body mass index data were available in 4, and 3 of these 4 (75%) were obese. The mean number of comorbid conditions among fatal cases was 3. The remaining fatal case was a child reported as previously healthy. Three (33%) had evidence of secondary bacterial infection with group A Streptococcus (n = 2) or Staphylococcus aureus (n = 1). Six children (67%) received antiviral treatment, but only 1 within 48 hours of symptom onset. In addition to 2009 novel influenza A(H1N1), other contributory causes of death listed for the fatal cases included pneumonia or acute respiratory distress syndrome (n = 5), sepsis, (n = 3) and scarlet fever (n = 1). The median length of stay for fatal cases was 22 days (range, 1-73 days).

BIVARIATE AND MULTIVARIATE ANALYSES

The demographic characteristics, comorbid conditions, and clinical characteristics identified in bivariate analyses as significantly associated with intensive care and/or death are shown in Table 1, Table 2, and Table 3, respectively. Hispanic (odds ratio [OR], 0.4; 95% CI, 0.2-0.8) and black (OR, 0.3; 95% CI, 0.1-1.0) children were less likely to require ICU admission and/or die. In bivariate analysis, the presence of either an ACIP-established risk factor (OR, 2.0; 95% CI, 1.2-3.4) or a non–ACIP established risk factor (OR, 2.1; 95% CI, 1.2-3.4) was associated with ICU admission and/or death. Among these, chronic lung disease of prematurity (OR, 4.1; 95% CI, 1.4-12.0), chronic cardiac disease (OR, 4.3; 95% CI, 1.9-9.5), chronic neurologic disease (OR, 2.8; 95% CI, 1.6-5.0), chronic gastrointestinal disorder (OR, 2.4; 95% CI, 1.3-4.5), and prematurity (birth at ≤32 weeks) (OR, 2.8; 95% CI, 1.1-6.9) were most strongly associated with ICU admission and/or death. An abnormal chest radiograph or computed tomography consistent with pneumonia (P = .009), presence of secondary bacterial infection (P < .001), and diagnosis of sepsis (P < .001) were all associated with ICU admission and/or death, while a positive rapid test result (P = .004) and early antiviral treatment (P = .01) were not. In a multivariate regression model that examined age, race/ethnicity, and chronic medical conditions, factors that were significantly associated with intensive care and/or death included congenital heart disease (OR, 5.0; 95% CI, 1.9-13.5) and cerebral palsy/developmental delay (OR, 3.5; 95% CI, 1.7-7.4). Hispanic (OR, 0.4; 95% CI, 0.2-0.8) and black (OR, 0.3; 95% CI, 0.1-0.9) race/ethnicity were associated with a decreased likelihood of intensive care and/or death (Table 4).

Table Graphic Jump LocationTable 4. Risk Factors Independently Associated With Being a Severe Case in a Multivariate Logistic Regression Analysis

We report on the first 345 children known to be hospitalized with and/or die of 2009 novel influenza A(H1N1) in California. Hospitalization rates in the first 110 days of the pandemic were comparable with seasonal influenza and were highest in young infants, although these rates may be an underestimate given limited availability of sensitive laboratory testing, among other reasons. Most children presented with acute respiratory illness. As with seasonal influenza,16 gastrointestinal symptoms were frequent in children infected with 2009 novel influenza A(H1N1). Similar to other reports,811 we found a high proportion of underlying medical conditions in hospitalized children but not infants, of whom more than 70% were previously healthy. More than one-quarter of cases required intensive care. The case-fatality proportion was low; 33% of fatal cases had a secondary bacterial infection detected. In multivariate analysis, congenital heart disease and cerebral palsy/developmental delay were associated with increased likelihood of ICU admission and/or death, while Hispanic and black children had a decreased likelihood. Most hospitalized children had multiple underlying medical conditions, which may explain why most of the clinically important conditions noted as significant in bivariate analysis were not retained in the multivariate analysis.

Infants younger than 6 months were most likely to be hospitalized. Similarly, 60% of hospitalized children in Argentina were younger than 1 year.12 Hospitalization rates per 100 000 population for 2009 novel influenza A(H1N1) in Chicago, Illinois, were 25 for children aged 0 to 4 years vs 11 for older children.4 This is also comparable with seasonal influenza, where children younger than 6 months have annual rates per 100 000 of 240 to 720, compared with 17 to 45 at ages 2 to 5 years and 8 to 41 at ages 5 to 17 years.1521 Increased hospitalization rates may in part reflect a lower threshold for clinicians to admit young infants for evaluation of febrile illness.

The proportion of 2009 novel influenza A(H1N1)–infected children with comorbid conditions hospitalized in California is similar to Montreal, Canada, and Toronto, Canada, where up to 80% of hospitalized children had underlying conditions.811 Nearly one-third of hospitalized children in our series had asthma (32%), a frequency similar to observations of others,811 and more than double the estimated prevalence of asthma (15.4%) in the California population younger than 18 years.22 Pediatric asthma is also associated with a higher rate of hospitalization for seasonal influenza.1619,23,24 One-quarter of children with a history of asthma were admitted for asthma exacerbation and fever; in such cases, clinicians should maintain high clinical suspicion and initiate prompt antiviral treatment while awaiting test results for 2009 novel influenza A(H1N1) infection.

Comorbidity was associated with increased likelihood of ICU admission and/or death, including novel associations with gastrointestinal disease (often coexistent with underlying neurologic disorders such as children with cerebral palsy receiving gastrostomy feedings) and prematurity (birth at ≤32 weeks) (which was often coexistent with chronic lung disease). We found that cerebral palsy/developmental delay and congenital heart disease were independently associated with ICU admission and/or death. In Toronto, 17% of children hospitalized for 2009 novel influenza A(H1N1) had a history of neurologic impairment.9 Of 36 pediatric fatalities due to 2009 novel influenza A(H1N1) reported to the Centers for Disease Control and Prevention, 92% with high-risk conditions had a neurodevelopmental diagnosis.25 Similarly, approximately 8% to 12% of children requiring intensive care or dying with seasonal influenza had an underlying cardiac condition.15,26,27 Children with either chronic cardiac or neuromuscular disease hospitalized with seasonal influenza are more likely to require intensive care, prolonged hospitalization, or mechanical ventilation.2730 The fragility of children with these conditions warrants prompt immunization before illness and empirical therapy if 2009 novel influenza A(H1N1) is suspected.

In our case series, neurologic manifestations, such as seizures and encephalopathy/altered mental status, were reported frequently. Although many of these children were admitted to the ICU, their length of stay was relatively short, and most recovered to their neurologic baseline at discharge. Similar frequencies of neurologic complications in 2009 novel influenza A(H1N1) have been reported from many countries.9,31,32,32 Although the mechanism is not well understood, seasonal influenza is also associated with seizures and encephalopathy and post–infectious encephalopathy.3133 In contrast to recent reports of novel influenza A(H1N1), in more than 50% of Japanese cases of encephalitis associated with seasonal influenza, patients had severe neurologic sequelae or died.33

We note an association with severe illness and race/ethnicity, with Hispanic and black children less likely to have 2009 novel influenza A(H1N1) requiring ICU admission and/or dying than other race/ethnicity groups. Early in the surveillance period, CDPH guidance recommended testing of persons traveling from Mexico, which may have accounted for a larger proportion of Hispanic individuals having been tested and hospitalized with less severe illness. Reasons why the proportion of black children was less likely to have a severe outcome are unclear, although the numbers in our series are small. Data on 2009 novel influenza A(H1N1)–associated hospitalizations and deaths and race/ethnicity in the United States are limited. In Chicago, hospitalization rates in children 14 years and younger were higher for non-Hispanic black, Asian/Pacific Islander, and Hispanic vs non-Hispanic white children.4 Further data are needed on whether there are racial and ethnic disparities in 2009 novel influenza A(H1N1) and the causes of such disparities.

In contrast to seasonal influenza, bacterial coinfection was infrequently reported in our series and may have been underdiagnosed because of infrequent testing, testing performed late in hospitalization, or the receipt of antibiotics prior to microbiological testing. Of note, the presence of secondary bacterial infection was significantly associated with admission to the ICU and/or death, with one-third of the fatal cases having secondary bacterial infections. When postmortem tissue has been evaluated using specific immunohistochemistry and polymerase chain reaction methods, higher (29%-43%) rates of secondary bacterial infection due to Streptococcus pneumoniae, S aureus, and group A Streptococcus have been identified.25,34 Studies of fatal pediatric cases due to seasonal influenza have also suggested high rates of bacterial coinfection.26,35

Possibly consistent with the known higher sensitivity of rapid tests for seasonal influenza in children, who may shed higher viral loads for prolonged periods compared with adults,15 sensitivity of rapid tests in our case series was 85%. However, other studies have demonstrated poor sensitivity of rapid tests for 2009 novel influenza A(H1N1) in both adults and children.3639 A negative rapid test result should not be the sole basis for excluding a diagnosis of 2009 novel influenza A(H1N1) when clinical suspicion is high. Almost 70% of cases received treatment with antiviral drugs, but often more than 48 hours after onset of symptoms, in contrast to recommendations that patients at high risk for severe disease with 2009 novel influenza A(H1N1) infection, including hospitalized patients, be treated with a neuraminidase inhibitor as soon as possible.40 In our case series, children with a positive rapid test result or who received early antiviral treatment were less likely to require ICU admission or die.

Our data are subject to several limitations. Data were extracted from nonstandardized medical records. Case ascertainment was based on passive reporting by clinicians, and underreporting may have occurred because of poor recognition, nonspecificity of influenza-like symptoms, and limited availability of confirmatory laboratory testing, leading to underestimation of rates of hospitalization. Likewise, clinicians may have been more inclined to suspect and test for 2009 novel influenza A(H1N1) in patients with complex comorbid conditions or more severe illness, to admit those children to an ICU for closer monitoring, and to report more severely ill cases to their local health jurisdiction, resulting in possible overestimation of the proportion of children admitted to the ICU. Finally, ascertainment of race/ethnicity data was higher in severe cases than nonsevere cases, possibly reflecting a bias in completeness of reporting data according to severity.

In conclusion, clinicians should be aware of when and what type of influenza and other respiratory viruses, including 2009 novel influenza A(H1N1), are circulating in their community. When 2009 novel influenza A(H1N1) activity is present, clinicians should maintain high suspicion for infection in pediatric patients presenting with febrile respiratory illness and initiate prompt treatment in infants and children with underlying risk factors regardless of rapid antigen test results. The epidemiology of severe pediatric 2009 novel influenza A(H1N1) in California supports national recommendations for targeting immunization, when vaccine supplies are scarce, to those caring for infants younger than 6 months, pregnant women who may convey immunity to infants younger than 6 months, children 6 to 59 months of age (especially those 6-18 months of age), and children with conditions associated with severe influenza.

Correspondence: Janice K. Louie, MD, MPH, California Department of Public Health, 850 Marina Bay Pkwy, Richmond, CA 94804 (janice.louie@cdph.ca.gov).

Accepted for Publication: May 6, 2010.

Author Contributions: Dr Louie had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Louie, Acosta, and Matyas. Acquisition of data: Louie, Gavali, Acosta, Samuel, Winter, and Jean. Analysis and interpretation of data: Louie, Gavali, Acosta, Samuel, Winter, Jean, Glaser, Matyas, and Schechter. Drafting of the manuscript: Louie, Gavali, Winter, Glaser, Matyas, and Schechter. Critical revision of the manuscript for important intellectual content: Louie, Gavali, Acosta, Samuel, Jean, Matyas, and Schechter. Statistical analysis: Gavali, Acosta, Samuel, Winter, and Schechter. Administrative, technical, and material support: Acosta, Jean, Glaser, and Matyas. Study supervision: Louie and Samuel.

Financial Disclosure: None reported.

Funding/Support: This work was supported by the CDPH.

Role of the Sponsor: Design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, and approval of the manuscript was fully sponsored by the CDPH.

Additional Contributions: All members of the California Pandemic (H1N1) Working Group work at local health departments or the CDPH and helped collect information on the reported cases. They also reviewed multiple versions of the manuscript. We are especially indebted to Christopher Anderson, BS, Jaynia Anderson, BS, Nina Huynh, BS, Daniel Zhuang, BA, Samuel Yang, BA, Melanie Stewart, BA, Tong Kong, BS, Maria Nevares, Erica Boston, BA, Sabrina Gilliam, MPH, Edward Powers, DVM, Huyen Cao, MD, David Schnurr, PhD, Sharon Messenger, PhD, Kathleen Harriman, PhD, Duc Vugia, MD, Jon Rosenberg, MD, John Talarico, DO, Carol Pertowski, MD, Douglas Hatch, MD, and Gilberto Chavez, MD, for their support and dedication. Thanks to the Centers for Disease Control and Prevention staff that support and advise us, including Tim Uyeki, MD, and Scott Harper, MD. Many thanks to all dedicated staff at the CDPH, epidemiologists and laboratorians alike, who contributed to surveillance and laboratory investigation of novel influenza A(H1N1) cases. In addition, while we cannot name them all, we gratefully acknowledge the contributions of the clinicians throughout California and all the staff at California local health departments who diligently worked to help acquire the epidemiological and clinical information and ensured that these cases were reported to CDPH.

Box Section Ref ID

California Pandemic (H1N1) Working Group

Faisal Aranki, MD, MPH, Fresno County Department of Public Health, Fresno, California; Elizabeth Bancroft, MD, County of Los Angeles Department of Public Health, Los Angeles, California; Carol Barney, PHN, MPH, Madera County Public Health Department, Madera, California; Paige Batson, Santa Barbara County Public Health Department, Santa Barbara, California; Janet Botta, San Luis Obispo County Health Agency, San Luis Obispo, California; Olivia Byron-Cooper, MPH, El Dorado County Health Services Department, Placerville, California; Ronald Chapman, MD, Solano County Public Health, Fairfield, California; Michele Cheung, MD, Orange County Health Care Agency, Santa Ana, California; Sara Cody, MD, Santa Clara County Public Health Department, San Jose, California; Andrew Deckert, MD, MPH, Shasta County Health and Human Services Agency, Redding, California; Elizabeth Falade, MD, MPH, San Benito County Health and Human Services Agency, Hollister, California; Susan Farley, BSN, Contra Costa Health Services, Martinez, California; Sharon Fortino, RN, BSN, PHN, Riverside County Department of Public Health, Riverside, California; Lynne Foster, RN, PHN, Yolo County Health Department, Woodland, California; Michele Ginsberg, MD, San Diego County Health and Human Services, San Diego, California; Barbara Gregory, RN, PHN, City of Berkeley Department of Health, Berkeley, California; Lucinda Hammond, MSPH, Sonoma County Department of Health Services, Santa Rosa, California; Jennifer Henn, PhD, Napa County Public Health, Napa, California; Lisa B. Hernandez, MD, MPH, Monterey County Health Department, Salinas, California; Richard Johnson, MD, MPH, Inyo County Health and Human Services, Bishop, California; Claudia Jonah, MD, Kern County Department of Public Health, Bakersfield, California; Jeremy Kempf, RN, BSN, Tulare County Health and Human Services Agency, Visalia, California; Paula Kriner, Imperial County Public Health Department, El Centro, California; Ann Lindsay, MD, Humboldt County Department of Health and Human Services, Eureka, California; Michael MacLean, MD, County of Kings Department of Public Health, Hanford, California; Fritzi Nelson, BSN, County of Santa Cruz Health Services Agency, Santa Cruz, California; Agnes Norman, RN, PHN, Sacramento County Department of Health and Human Services, Sacramento, California; Maxwell Ohikhuare, MD, San Bernardino Department of Public Health, San Bernardino, California; Erica Pan, MD, MPH, San Francisco Department of Public Health, San Francisco, California; Kelly Rose, MPH, Merced County Department of Public Health, Merced, California; Rosilyn Ryals, MD, Alameda County Public Health Department, Oakland, California; Erin Salce, MPH, Long Beach Department of Health and Human Services, Long Beach, California; Catherine S. Sallenave, MD, San Mateo County Health System, San Mateo, California; Fred Schwartz, MD, County of Marin, Department of Health and Human Services, San Rafael, California; Nirali Shah, MPH, San Joaquin County Public Health Services, Stockton, California; Mark Starr, DVM, Placer County Health and Human Services, Auburn, California; Karen M. Tait, MD, Lake County Department of Health Services, Lakeport, California; Burjessa E. Tighe, PHN, MSN, Butte County Public Health Department, Oroville, California; Marvin Trotter, MD, Mendocino County Public Health Department, Ukiah, California; Takashi Wada, MD, MPH, City of Pasadena Public Health Department, Pasadena, California; John A. Walker, MD, Stanislaus County Health Services Agency, Modesto, California.

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Miroballi  YBaird  JSZackai  S  et al.  Novel influenza A(H1N1) in a pediatric health care facility in New York City during the first wave of the 2009 pandemic. Arch Pediatr Adolesc Med 2010;164 (1) 24- 30
PubMed
Bettinger  JASauvé  LJScheifele  DW  et al.  Pandemic influenza in Canadian children: a summary of hospitalized pediatric cases. Vaccine 2010;28 (18) 3180- 3184
PubMed
Libster  RBugna  JCoviello  S  et al.  Pediatric hospitalizations associated with 2009 pandemic influenza A (H1N1) in Argentina. N Engl J Med 2010;362 (1) 45- 55
PubMed
Guevara  HSaguar  EEspinosa  APan  CSchnurr  D Implementation of a TAQMAN RT-PCR protocol for the typing (A,B) and subtyping (A/H1, A/H3, A/H5) of influenza at the Viral and Rickettsial Disease Laboratory.  Paper presented at: 125th Clinical Virology Symposium April 21, 2009 Daytona Beach, FL
 Defining childhood overweight and obesity. CDC Web site. http://www.cdc.gov/obesity/childhood/defining.html. Accessed January 24, 2010
Fiore  AEShay  DKBroder  K  et al. Centers for Disease Control and Prevention, Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recomm Rep 2009;58 (RR-8) 1- 52
PubMed
Harper  SABradley  JSEnglund  JA  et al. Expert Panel of the Infectious Diseases Society of America, Seasonal influenza in adults and children—diagnosis, treatment, chemoprophylaxis, and institutional outbreak management: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis 2009;48 (8) 1003- 1032
PubMed
O’Brien  MAUyeki  TMShay  DK  et al.  Incidence of outpatient visits and hospitalizations related to influenza in infants and young children. Pediatrics 2004;113 (3, pt 1) 585- 593
PubMed
Izurieta  HSThompson  WWKramarz  P  et al.  Influenza and the rates of hospitalization for respiratory disease among infants and young children. N Engl J Med 2000;342 (4) 232- 239
PubMed
Poehling  KAEdwards  KMWeinberg  GA  et al. New Vaccine Surveillance Network, New Vaccine Surveillance Network. The underrecognized burden of influenza in young children. N Engl J Med 2006;355 (1) 31- 40
PubMed
American Academy of Pediatrics Committee on Infectious Diseases, Prevention of influenza: recommendations for influenza immunization of children, 2007-2008. Pediatrics 2008;121 (4) e1016- e1031
PubMed
National Center for Immunization and Respiratory Diseases, CDC; Centers for Disease Control and Prevention (CDC), Use of influenza A (H1N1) 2009 monovalent vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recomm Rep 2009;58 (RR-10) 1- 8
PubMed
 California Health Interview Survey. CHIS 2007 Adult Public Use File. Release 1 [computer file].  Los Angeles UCLA Center for Health Policy Research2007;
Neuzil  KMWright  PFMitchel  EF  JrGriffin  MR The burden of influenza illness in children with asthma and other chronic medical conditions. J Pediatr 2000;137 (6) 856- 864
PubMed
Miller  EKGriffin  MREdwards  KM  et al. New Vaccine Surveillance Network, Influenza burden for children with asthma. Pediatrics 2008;121 (1) 1- 8
Centers for Disease Control and Prevention (CDC), Surveillance for pediatric deaths associated with 2009 pandemic influenza A (H1N1) virus infection—United States, April-August 2009. MMWR Morb Mortal Wkly Rep 2009;58 (34) 941- 947
PubMed
Bhat  NWright  JGBroder  KR  et al. Influenza Special Investigations Team, Influenza-associated deaths among children in the United States, 2003-2004. N Engl J Med 2005;353 (24) 2559- 2567
PubMed
Louie  JKSchechter  RHonarmand  S  et al.  Severe pediatric influenza in California, 2003-2005: implications for immunization recommendations. Pediatrics 2006;117 (4) e610- e618
PubMed
Keren  RZaoutis  TEBridges  CB  et al.  Neurological and neuromuscular disease as a risk factor for respiratory failure in children hospitalized with influenza infection. JAMA 2005;294 (17) 2188- 2194
PubMed
Quach  CPiché-Walker  LPlatt  RMoore  D Risk factors associated with severe influenza infections in childhood: implication for vaccine strategy. Pediatrics 2003;112 (3, pt 1) e197- e201
PubMed
Coffin  SEZaoutis  TERosenquist  AB  et al.  Incidence, complications, and risk factors for prolonged stay in children hospitalized with community-acquired influenza. Pediatrics 2007;119 (4) 740- 748
PubMed
Centers for Disease Control and Prevention (CDC), Neurologic complications associated with novel influenza A (H1N1) virus infection in children—Dallas, Texas, May 2009. MMWR Morb Mortal Wkly Rep 2009;58 (28) 773- 778
PubMed
Laumay  EOvetchkine  PSt-Jean  MCoic  LLamarre  VDesmarais  N  Novel influenza A [H1N1] related hospitalization in a pediatric tertiary care centre: who's at risk for severe disease? severe H1N1 cases in children. Paper presented at: 49th Interscience Conference on Antimicrobial Agents and Chemotherapy September 14, 2009 San Francisco, CA
Togashi  TMatsuzono  YNarita  MMorishima  T Influenza-associated acute encephalopathy in Japanese children in 1994-2002. Virus Res 2004;103 (1-2) 75- 78
PubMed
Centers for Disease Control and Prevention (CDC), Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1)—United States, May-August 2009. MMWR Morb Mortal Wkly Rep 2009;58 (38) 1071- 1074
PubMed
Finelli  LFiore  ADhara  R  et al.  Influenza-associated pediatric mortality in the United States: increase of Staphylococcus aureus coinfection. Pediatrics 2008;122 (4) 805- 811
PubMed
Centers for Disease Control and Prevention (CDC), Evaluation of rapid influenza diagnostic tests for detection of novel influenza A (H1N1) virus—United States, 2009. MMWR Morb Mortal Wkly Rep 2009;58 (30) 826- 829
PubMed
Vasoo  SStevens  JSingh  K Rapid antigen tests for diagnosis of pandemic (swine) influenza A/H1N1. Clin Infect Dis 2009;49 (7) 1090- 1093
PubMed
Hawkes  MRichardson  SEIpp  MSchuh  SAdachi  DTran  D Sensitivity of rapid influenza diagnostic testing for swine-origin 2009 A (H1N1) influenza virus in children [published online February 15, 2010]. Pediatrics 10.1542/peds.2009-2669
Cruz  ATDemmler-Harrison  GJCaviness  ACBuffone  GJRevell  PA Performance of a rapid influenza test in children during the H1N1 2009 influenza a outbreak. Pediatrics 2010;125 (3) e645- e650
PubMed
 WHO guidelines for pharmacological management of pandemic (H1N1) 2009 influenza and other influenza viruses. World Health Organization Web site. http://www.who.int/csr/resources/publications/swineflu/h1n1_use_antivirals_20090820/en/index.html. Accessed November 26, 2009

Figures

Place holder to copy figure label and caption
Figure 1.

No. of hospitalized and/or fatal cases with 2009 novel influenza A(H1N1) in children aged 0 to 17 years in California by date of symptom onset, reported April 23 to August 11, 2009 (n = 335).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Rate of hospitalization and/or fatality by age group. *Per 110 days of observation.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Demographic Characteristics of Hospitalized and/or Fatal Pediatric Cases of 2009 Novel Influenza A(H1N1) in Children Aged 0 to 17 Years in California, Reported April 23 to August 11, 2009
Table Graphic Jump LocationTable 2. Chronic Comorbid Conditions of Hospitalized and/or Fatal Pediatric Cases of 2009 Novel Influenza A(H1N1) in Children Aged 0 to 17 Years in California, Reported April 23 to August 11, 2009
Table Graphic Jump LocationTable 3. Symptoms and Clinical Course and Findings of Hospitalized and/or Fatal Pediatric Cases of 2009 Novel Influenza A(H1N1) in Children Aged 0 to 17 Years in California, Reported April 23 to August 11, 2009
Table Graphic Jump LocationTable 4. Risk Factors Independently Associated With Being a Severe Case in a Multivariate Logistic Regression Analysis

References

Centers for Disease Control and Prevention (CDC), Swine influenza A (H1N1) infection in two children—Southern California, March-April 2009. MMWR Morb Mortal Wkly Rep 2009;58 (15) 400- 402
PubMed
 Epidemic and pandemic alert and response, influenza A (H1N1) situation updates. World Health Organization Web site. http://www.who.int/csr/disease/swineflu/en/index.html. Accessed November 26, 2009
Dawood  FSJain  SFinelli  L  et al. Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team, Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 2009;360 (25) 2605- 2615
PubMed
Centers for Disease Control and Prevention (CDC), 2009 pandemic influenza A (H1N1) virus infections—Chicago, Illinois, April-July 2009. MMWR Morb Mortal Wkly Rep 2009;58 (33) 913- 918
PubMed
Centers for Disease Control and Prevention (CDC), Hospitalized patients with novel influenza A (H1N1) virus infection—California, April-May, 2009. MMWR Morb Mortal Wkly Rep 2009;58 (19) 536- 541
PubMed
Vaillant  LLa Ruche  GTarantola  ABarboza  PEpidemic Intelligence Team at InVS, Epidemiology of fatal cases associated with pandemic H1N1 influenza 2009. Euro Surveill 2009;14 (33) pii: 19309
PubMed
Louie  JKAcosta  MWinter  K  et al. California Pandemic (H1N1) Working Group, Factors associated with death or hospitalization due to pandemic 2009 influenza A(H1N1) infection in California. JAMA 2009;302 (17) 1896- 1902
PubMed
Jain  SKamimoto  LBramley  AM  et al. 2009 Pandemic Influenza A (H1N1) Virus Hospitalizations Investigation Team, Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med 2009;361 (20) 1935- 1944
PubMed
O’Riordan  SBarton  MYau  YRead  SEAllen  UTran  D Risk factors and outcomes among children admitted to hospital with pandemic H1N1 influenza. CMAJ 2010;182 (1) 39- 44
PubMed
Miroballi  YBaird  JSZackai  S  et al.  Novel influenza A(H1N1) in a pediatric health care facility in New York City during the first wave of the 2009 pandemic. Arch Pediatr Adolesc Med 2010;164 (1) 24- 30
PubMed
Bettinger  JASauvé  LJScheifele  DW  et al.  Pandemic influenza in Canadian children: a summary of hospitalized pediatric cases. Vaccine 2010;28 (18) 3180- 3184
PubMed
Libster  RBugna  JCoviello  S  et al.  Pediatric hospitalizations associated with 2009 pandemic influenza A (H1N1) in Argentina. N Engl J Med 2010;362 (1) 45- 55
PubMed
Guevara  HSaguar  EEspinosa  APan  CSchnurr  D Implementation of a TAQMAN RT-PCR protocol for the typing (A,B) and subtyping (A/H1, A/H3, A/H5) of influenza at the Viral and Rickettsial Disease Laboratory.  Paper presented at: 125th Clinical Virology Symposium April 21, 2009 Daytona Beach, FL
 Defining childhood overweight and obesity. CDC Web site. http://www.cdc.gov/obesity/childhood/defining.html. Accessed January 24, 2010
Fiore  AEShay  DKBroder  K  et al. Centers for Disease Control and Prevention, Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recomm Rep 2009;58 (RR-8) 1- 52
PubMed
Harper  SABradley  JSEnglund  JA  et al. Expert Panel of the Infectious Diseases Society of America, Seasonal influenza in adults and children—diagnosis, treatment, chemoprophylaxis, and institutional outbreak management: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis 2009;48 (8) 1003- 1032
PubMed
O’Brien  MAUyeki  TMShay  DK  et al.  Incidence of outpatient visits and hospitalizations related to influenza in infants and young children. Pediatrics 2004;113 (3, pt 1) 585- 593
PubMed
Izurieta  HSThompson  WWKramarz  P  et al.  Influenza and the rates of hospitalization for respiratory disease among infants and young children. N Engl J Med 2000;342 (4) 232- 239
PubMed
Poehling  KAEdwards  KMWeinberg  GA  et al. New Vaccine Surveillance Network, New Vaccine Surveillance Network. The underrecognized burden of influenza in young children. N Engl J Med 2006;355 (1) 31- 40
PubMed
American Academy of Pediatrics Committee on Infectious Diseases, Prevention of influenza: recommendations for influenza immunization of children, 2007-2008. Pediatrics 2008;121 (4) e1016- e1031
PubMed
National Center for Immunization and Respiratory Diseases, CDC; Centers for Disease Control and Prevention (CDC), Use of influenza A (H1N1) 2009 monovalent vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recomm Rep 2009;58 (RR-10) 1- 8
PubMed
 California Health Interview Survey. CHIS 2007 Adult Public Use File. Release 1 [computer file].  Los Angeles UCLA Center for Health Policy Research2007;
Neuzil  KMWright  PFMitchel  EF  JrGriffin  MR The burden of influenza illness in children with asthma and other chronic medical conditions. J Pediatr 2000;137 (6) 856- 864
PubMed
Miller  EKGriffin  MREdwards  KM  et al. New Vaccine Surveillance Network, Influenza burden for children with asthma. Pediatrics 2008;121 (1) 1- 8
Centers for Disease Control and Prevention (CDC), Surveillance for pediatric deaths associated with 2009 pandemic influenza A (H1N1) virus infection—United States, April-August 2009. MMWR Morb Mortal Wkly Rep 2009;58 (34) 941- 947
PubMed
Bhat  NWright  JGBroder  KR  et al. Influenza Special Investigations Team, Influenza-associated deaths among children in the United States, 2003-2004. N Engl J Med 2005;353 (24) 2559- 2567
PubMed
Louie  JKSchechter  RHonarmand  S  et al.  Severe pediatric influenza in California, 2003-2005: implications for immunization recommendations. Pediatrics 2006;117 (4) e610- e618
PubMed
Keren  RZaoutis  TEBridges  CB  et al.  Neurological and neuromuscular disease as a risk factor for respiratory failure in children hospitalized with influenza infection. JAMA 2005;294 (17) 2188- 2194
PubMed
Quach  CPiché-Walker  LPlatt  RMoore  D Risk factors associated with severe influenza infections in childhood: implication for vaccine strategy. Pediatrics 2003;112 (3, pt 1) e197- e201
PubMed
Coffin  SEZaoutis  TERosenquist  AB  et al.  Incidence, complications, and risk factors for prolonged stay in children hospitalized with community-acquired influenza. Pediatrics 2007;119 (4) 740- 748
PubMed
Centers for Disease Control and Prevention (CDC), Neurologic complications associated with novel influenza A (H1N1) virus infection in children—Dallas, Texas, May 2009. MMWR Morb Mortal Wkly Rep 2009;58 (28) 773- 778
PubMed
Laumay  EOvetchkine  PSt-Jean  MCoic  LLamarre  VDesmarais  N  Novel influenza A [H1N1] related hospitalization in a pediatric tertiary care centre: who's at risk for severe disease? severe H1N1 cases in children. Paper presented at: 49th Interscience Conference on Antimicrobial Agents and Chemotherapy September 14, 2009 San Francisco, CA
Togashi  TMatsuzono  YNarita  MMorishima  T Influenza-associated acute encephalopathy in Japanese children in 1994-2002. Virus Res 2004;103 (1-2) 75- 78
PubMed
Centers for Disease Control and Prevention (CDC), Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1)—United States, May-August 2009. MMWR Morb Mortal Wkly Rep 2009;58 (38) 1071- 1074
PubMed
Finelli  LFiore  ADhara  R  et al.  Influenza-associated pediatric mortality in the United States: increase of Staphylococcus aureus coinfection. Pediatrics 2008;122 (4) 805- 811
PubMed
Centers for Disease Control and Prevention (CDC), Evaluation of rapid influenza diagnostic tests for detection of novel influenza A (H1N1) virus—United States, 2009. MMWR Morb Mortal Wkly Rep 2009;58 (30) 826- 829
PubMed
Vasoo  SStevens  JSingh  K Rapid antigen tests for diagnosis of pandemic (swine) influenza A/H1N1. Clin Infect Dis 2009;49 (7) 1090- 1093
PubMed
Hawkes  MRichardson  SEIpp  MSchuh  SAdachi  DTran  D Sensitivity of rapid influenza diagnostic testing for swine-origin 2009 A (H1N1) influenza virus in children [published online February 15, 2010]. Pediatrics 10.1542/peds.2009-2669
Cruz  ATDemmler-Harrison  GJCaviness  ACBuffone  GJRevell  PA Performance of a rapid influenza test in children during the H1N1 2009 influenza a outbreak. Pediatrics 2010;125 (3) e645- e650
PubMed
 WHO guidelines for pharmacological management of pandemic (H1N1) 2009 influenza and other influenza viruses. World Health Organization Web site. http://www.who.int/csr/resources/publications/swineflu/h1n1_use_antivirals_20090820/en/index.html. Accessed November 26, 2009

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