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Household Transmission of 2009 Influenza A (H1N1) Virus after a School-Based Outbreak in New York City, April–May 2009

  1. Anne Marie France1,3,
  2. Michael Jackson1,2,
  3. Stephanie Schrag2,
  4. Michael Lynch2,
  5. Christopher Zimmerman3,
  6. Matthew Biggerstaff2 and
  7. James Hadler3
  1. 1Epidemic Intelligence Service, Office of Workforce and Career Development, Atlanta, Georgia
  2. 2National Center For Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia
  3. 3New York City Department of Health and Mental Hygiene, New York, New York
  1. Reprints or correspondence: Dr France, US Public Health Service, Bureau of Communicable Disease, New York City Dept of Health and Mental Hygiene, 125 Worth St, Room 214a, CN 22a, New York, NY 10013 (afrance{at}health.nyc.gov).
 
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Abstract

In April 2009, an outbreak due to infection with the 2009 pandemic influenza A (H1N1) virus (pH1N1) was investigated in a New York City high school. We surveyed household contacts of ill students to characterize the extent of transmission within households, identify contact groups at highest risk for illness, and assess the potential for preventing household transmission. Influenza-like illness (ILI) was reported by 79 of 702 household contacts (11.3% attack rate). Multivariate analysis showed that older age was protective: for each increasing year of age, the risk of ILI was reduced 5%. Additional protective factors included antiviral prophylaxis and having had a household discussion about influenza. Providing care for the index case patient and watching television with the index case patient were risk factors among parents and siblings, respectively. Fifty percent of cases occurred within 3 days of onset of illness in the student. These factors have implications for mitigating the impact of pH1N1 transmission.

An influenza outbreak due to the 2009 pandemic influenza A (H1N1) virus (pH1N1) was identified in a New York City high school (school A) <1 week after the first identification of this virus in 2 children in California [1, 2] and concurrent with the first media reports of influenza outbreaks in Mexico. This first known introduction of pH1N1 into New York City was the largest cluster identified at the time in the United States [3]. The timing and magnitude of this outbreak presented a unique opportunity to characterize dynamics of transmission of the pH1N1 virus.

The school outbreak was identified on 23 April 2009, when the New York City Department of Health and Mental Hygiene (NYC DOHMH) was contacted by the school nurse at school A, who reported that ∼100 students had presented to her with fever ⩽102.7F° (⩾39.3⩽C) and complaints of headache, sore throat, dizziness, and shortness of breath. School A, a parochial school, has an enrollment of ∼2700 students in grades 9–12. The NYC DOHMH immediately launched an investigation, which revealed that ∼33% of students reported symptoms consistent with influenza infection [4]. The pH1N1 virus was confirmed by real-time reverse-transcription polymerase chain reaction at the national Centers for Disease Control and Prevention (CDC) in 7 of 9 specimens collected from students on 24 April 2009. The week before the investigation, the school had been on spring break; pH1N1 was probably introduced into the school population by students who had traveled to Mexico during this time [3]. Transmission in the school was rapid, with the peak of cases occurring on 23 April, the fourth day after school resumed (Figure 1).

Figure 1.
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Figure 1.

Epidemic curve and household transmission investigation timeline for outbreak of novel H1N1 influenza A in school A. ILI, influenza-like illness.

Once pH1N1 was confirmed, the school closed from 27 April to 1 May 2009. Written information posted on the school Internet site advised those who were sick to stay home for ∼7 days after onset of fever, limit contact with others to the extent possible, and avoid close contact.

Understanding household transmission is particularly important, because symptomatic persons told to go home from school or work often put household contacts at risk. We conducted an investigation of pH1N1 transmission within households of ill students from school A to characterize the extent of transmission within households, identify contact groups at highest risk for illness, and assess the potential for preventing household transmission.

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Methods

Study population. Index case patients were students of school A who either reported symptoms consistent with influenza-like illness (ILI) with onset dates between 22 and 25 April or had laboratory-confirmed influenza with onset between 22 and 30 April. ILI was defined as a fever (measured or subjective) with cough or sore throat. Patients with ILI were identified based on a student survey done in school A as part of the outbreak investigation. The illness-onset period of 22–25 April was chosen on the basis of the peak of the school's epidemic curve (Figure 1) to increase the probability that ILI in these cases resulted from pH1N1 infection. A total of 568 index case patients were identified, and their household contacts were invited to participate in a household transmission survey. Household contacts were defined as all persons who spent ⩾2 nights per week in the household.

Survey. The survey was divided into general and individual-level sections. The general section included household-level questions (eg, number of persons and number of rooms in the household) and collective actions taken in response to news of the pH1N1 outbreak at school A. Individual-level questions included the presence of ILI symptoms, their onset and duration, use of antivirals, duration and type of contact with the index case patient, and receipt of the 2008–2009 seasonal influenza vaccine. Survey instructions directed the primary caregiver in the household to complete the survey for each member of the household, consulting with household members as needed.

The survey was implemented as an Internet-based survey, using the mrInterview platform (SPSS). Households were contacted by US Postal Service mail; a letter introducing the survey and addressed by name to the student's parents or guardians included the URL for a password-protected site and a unique household identification number and password to access the survey. Letters were mailed on Wednesday, 6 May; the online survey was available 7–27 May. Households that had not responded by Monday, 12 May, were contacted by telephone with a reminder to complete the survey online and offered the option to complete the survey by telephone interview. On 14 May, reminder letters were sent to all households. Both telephone and mail follow-up communication described incentives in the form of a raffle for retail gift cards, donated by the CDC Foundation. During this time frame, a convenience sample of 30 of the households participating in the study as part of a related laboratory investigation completed the same survey as a self-administered survey on paper. The NYC DOHMH and CDC determined that the survey constituted a public health response that did not require institutional review board authorization.

Analyses. The primary outcome of interest was ILI in a household contact. We calculated the secondary attack rate (SAR) as the percentage of household contacts reporting ILI. We calculated the interval between infections (serial interval) as the number of days between the reported onset of symptoms in the household contact and the reported onset date for that household's index case patient. Antiviral prophylaxis was defined as self-reported prophylaxis with oseltamivir phosphate or zanamivir, with the first date of prophylaxis ⩾1 day before onset of illness if the person became ill.

To determine factors associated with ILI among contacts, we performed a bivariate analysis with ILI as the outcome. Predictor variables included epidemiologic characteristics of the household, index case patient, and household contacts. Stratified analyses of selected variables were performed to assess possible interaction. Variables associated with ILI in a bivariate analysis, with differences considered statistically significant at P ⩽ .10, were considered in a multivariate analysis. For continuous variables, the Box-Tidwell test was used to assess the assumption of linearity [5, 6]. Both bivariate and multivariate analyses accounted for household correlations, using SAS PROC SURVEYFREQ and SAS PROC SURVEYLOGISTIC procedures (SAS Institute), respectively, to adjust variance estimates. Analyses were conducted by using SAS software (version 9.1.3). Because the prevalence of ILI was high (>10%), we used the formula recommended by Zhang and Yu [7] to transform odds ratio estimates from multivariate modeling to risk ratio estimates.

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Results

Response. Of 568 households invited to participate in the household transmission survey, 322 (57%) responded: 30 (9%) on paper, 165 (51%) online, and 127 (39%) by telephone. These 322 households included responses for 1365 individual household members. For the subset of 538 households in which the ill student had responded to the original school A outbreak investigation survey [4], we compared characteristics of respondents to the household transmission survey (n = 322) with those of nonrespondents (n = 216). Households with an index case patient in 9th–11th grade were significantly more likely to respond than households with an index case patient in 12th grade (59% vs 45%; P = .04). No difference was observed with regard to sex, chronic health problems in the index case patient, number of persons in the household, or reported ILI among household contacts.

Responses from 58 households were excluded from the analysis for the following reasons: the index case patient was not a student at school A (4 households); the index case patient's symptoms did not meet the ILI case definition (47 households); a case of ILI in the household had an earlier onset date than that of the index case patient (4 households); or inconsistent or invalid responses (3 households) were provided, giving an age for the index case patient that was implausible for a high- school student. Additionally, 42 households had ⩾1 household contact other than the index case patient who was either a student or staff member at school A; because of the potential for nonhousehold exposure to ill students from school A, these households were excluded from the analysis. After exclusions, the study included 222 index case patients and 702 household contacts.

Home, index case patient, and household contact characteristics. Households ranged in size from 2 to 8 persons (median, 4 persons). The number of rooms in the household, excluding bathrooms, kitchen, and closets, ranged from 2 to 15 (median, 6 rooms); the number of rooms per person ranged from 0.33 to 5 (median, 1.4).

Index case patients ranged in age from 14 to 19 years (median, 16 years); 136 (61%) patients were female. Antivirals were taken for treatment by 58 (26%) of 222 index case patients; 51 took oseltamivir, 6 took zanamivir, and 1 took both. The time between onset of symptoms and initiation of antiviral therapy among index case patients ranged from 0 to 10 days, with a median of 2 days. In 41 (71%) of index case patients who took antivirals for treatment, therapy was initiated within 2 days of illness onset. The duration of illness ranged from 1 to 15 days (median, 5 days) and did not differ between index patients who took antivirals for treatment and those who did not.

Household contacts ranged in age from <1 year to 91 years, with a bimodal distribution peaking at 15 and 51 years and a median of 45 years; 369 (53%) were female. Fifty (7%) reported taking antiviral prophylaxis with either oseltamivir (n = 46) or zanamivir (n = 4). A total of 315 (45%) reported having taken care of the index case patient. Of these, 209 (66%) were mothers; 75 (24%), fathers; 11 (3%), other children in the household; 13 (4%), other related adults; and 7 (2%), adult siblings.

SAR results. Overall, 79 of 702 household contacts reported ILI, for an SAR of 11.3% (95% confidence interval, 8.8–13.7). One household-level factor was significantly associated with SAR in bivariate analysis: having had a household discussion about how to prevent transmission (risk ratio, 0.60; 95% confidence interval, 0.36–0.97) (Table 1). Individual-level risk factors significantly associated with SARs in bivariate analysis included age, sex, and relationship to the index case patient (Table 2). The association between age and SAR was pronounced, with the highest SAR (30.8%) among household contacts aged 0–4 years and the lowest (2.1%) among those aged ⩾55 years. Compared with other household contacts, mothers and siblings had the highest SARs. Whereas a borderline significant 67% decreased risk for ILI was observed with use of antiviral prophylaxis among household contacts, no difference was observed in SARs with receipt of the 2008–2009 influenza vaccine (Table 2).

Table 1.
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Table 1.

Household-level Characteristics and Occurrence of Secondary Cases of Influenza-like Illness (ILI) among Household Contacts of Index Case Patients from School A

Table 2.
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Table 2.

Secondary Attack Rate (SAR) and Risk Ratio (RR) of Association with Influenza-like Illness (ILI), by Characteristics of Household Contacts

A higher SAR was observed among household contacts who slept in the same room or watched television with the index case patient, with larger differences in SAR associated with these activities among select groups (Table 3). SARs also increased with increased hours per day spent in the same house as an index case patient (P = .001, by Cochran-Armitage trend test). Taking care of the index case patient was associated with a higher SAR among parents but not among siblings or other relatives. Sharing personal items (eg, cups or utensils) and towels did not increase the risk of infection significantly.

Table 3.
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Table 3.

Secondary Attack Rate (SAR) and Risk Ratio (RR) for Association with Influenza-like Illness (ILI), by Items Shared with Index Case Patient

After adjustment for the other variables included in the multivariate analysis, older age and having had a household discussion about preventing transmission remained significantly associated with decreased risk for ILI (Table 4). For each year of age, the risk of ILI was reduced 5% (Figure 2). In families in which a household discussion occurred, the risk to individual contacts was reduced 40%. Additionally, the protective effect associated with antiviral prophylaxis became statistically significant, with a 68% reduction of risk for those who had taken prophylaxis. Groups with a higher risk for ILI included parents who had provided care to the index case patient, care providers who slept in the same room as the index case patient, and siblings who had watched television or played video games with the index case patient. The amount of time spent in the same house as the index case patient was not associated with ILI.

Table 4.
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Table 4.

Unadjusted and Adjusted Risk Ratio (RR) Estimates for Characteristics Associated with Reported Influenza-like Illness among Household Contacts of Index Case Patients from School A

Figure 2.
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Figure 2.

Risk ratio for influenza-like illness (ILI) by age after adjustment for other factors in a multivariate model (risk ratio, 0.95; 95% confidence interval, 0.92–0.98).

Among the 62 households with ⩾1 secondary case, 13 (21%) had 2 secondary cases and 1 (2%) had 3. The only factor among households with secondary cases that predicted having >1 was higher mean household size (5.2 residents vs 4.3 residents; P = .02, by the Student t test).

Serial interval. Serial interval times ranged from 0 to 23 days (median, 3 days) (Figure 3); 87% of cases occurred ⩽7 days after the index case patient. Contacts with onset occurring >7 days after onset of illness in the index student (referred to as late cases) were more likely to be school aged (5–18 years) than contacts with onset within 2 days of the index student (8 of 11 [73%] vs 8 of 29 [28%]; P = .009). We considered the impact of excluding late cases and observed similar results with and without such exclusion.

Figure 3.
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Figure 3.

Distribution of serial interval times among 77 household contacts reporting symptoms consistent with influenza-like illness (ILI). A serial interval of 0 days indicates onset of illness in the household contact within 24 h of onset in the index case patient; the date of symptom onset was missing for 2 of 79 household contacts reporting ILI.

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Discussion

We provide one of the first characterizations of the transmission of pH1N1 infection within households. The overall SAR of 11.3%, the median serial interval of 3 days, and the factors associated with increased and decreased risk for infection all have implications for mitigating the impact of the continuing pandemic.

Because the time between onset of illness in the index case and secondary patients was short, with almost all household transmission completed in ⩽1 week, any strategy to reduce household transmission should be implemented quickly and even then might be insufficient to prevent ⩽50% of potential cases. The serial interval we observed is consistent with an estimate based on seasonal influenza transmission during the 2007 season in Hong Kong [8] but longer than a recent estimate of 1–2 days based on historic data from an institutional outbreak during the 1918 influenza pandemic [9].

The overall SAR among household contacts was substantially lower than the SARs observed among students in the school A outbreak (11.3% of household contacts, compared with >30% of school A students). However, this overall SAR reflects the differences in the risk of infection associated with both age and antiviral use; in siblings of the index case patient who did not receive antiviral prophylaxis, the SAR was similar to that seen among students in the school A outbreak. Thus, pH1N1 transmission in the household is more efficient than the 11.3% overall rate indicates.

Investigations of household transmission of seasonal influenza have revealed overall SARs of 5%–24% [10–12]. Although the overall SARs we observed are within this range, direct comparison is not possible for a number of reasons, including differences in case definitions, potential for transmission from outside the household, interventions to reduce transmission, and characteristics of the households investigated. The most suitable comparison might be with the results of an analysis of 4 family studies, which estimated the SAR for seasonal influenza, in the absence of antiviral prophylaxis, to be 15% after taking community transmission into account [13].

Both nonmodifiable and modifiable risk factors were key predictors of secondary ILI among household contacts. The risk of ILI was most strongly age related. This effect remained significant after adjustment for factors associated with transmission. This indicates that the pattern observed in the crude analysis did not result purely from increased opportunity for transmission among younger age groups. This relationship is consistent with findings from surveillance for pH1N1 hospitalizations and deaths during the spring 2009 outbreak, demonstrating a disproportionate burden of disease among younger age groups [14], and findings from a laboratory investigation indicating an inverse association between age and presence of cross-reactive antibody to pH1N1 [15]. Although age is not modifiable, pH1N1 vaccination strategies identify children and young adults aged 6 months to 24 years as an initial target group for vaccination efforts [14]. Because >50% of the secondary cases in this investigation were among household contacts aged 0–24 years, reducing susceptibility among this population at high risk might dramatically reduce overall SARs.

Taking care of an index adolescent was associated with a higher risk for ILI among parents but not among other house hold contacts. Among caretakers, those who slept in the same room with the index case patient were at higher risk. Although caretaking itself might not be a modifiable risk factor, modifiable behaviors associated with caretaking (eg, not sleeping in the same room with the index case patient) indicate that there are ways to reduce the risk for illness among this group. Additional study is needed to determine what precautions could be taken to minimize this added risk. Meanwhile, sleeping in the same room should continue to be discouraged; if it is necessary, antiviral prophylaxis should be considered for the caretakers, particularly those with risk factors for influenza complications [16].

The most important modifiable risk factors for transmission were antiviral prophylaxis and whether the family had had a discussion about how to avoid contracting influenza. After adjustment for other factors, antiviral prophylaxis reduced the risk for ILI by 68% among household contacts who took it. This is similar to the protective effect of antivirals against seasonal influenza in randomized controlled trials in which oseltamivir and zanamivir reduced the risk for laboratory-confirmed seasonal influenza among household contacts by 89% and 72%, respectively [12, 17]. Recent reports of oseltamivirresistant novel H1N1 infection [18, 19] underscore the need to consider this protective effect in light of the potential for adverse outcomes of chemoprophylaxis. CDC recommendations regarding use of antivirals during the 2009 H1N1 pandemic, as updated on 7 December 2009, advise that the use of antiviral medications for postexposure chemoprophylaxis should be reserved for persons at higher risk for influenza- related complications who have had contact with someone likely to have been infected with influenza; additionally, early treatment was emphasized as an alternative to chemoprophylaxis after suspected exposure [16]. Although smaller in magnitude, the protective effect associated with having had a household discussion about how to avoid contracting pH1N1 infection is important, because it indicates that behavioral changes can be effective in decreasing the risk for secondary illness within a household. We do not know what type of behavior changes might have occurred in households that had such a discussion, but it is plausible that these households more carefully observed the recommendations sent to all school A households by the health department. We did not ask about hand hygiene or routine covering of coughs and sneezes; however, both measures were included in the recommendations to school A households and are known to decrease the risk for colds and influenza [20].

Watching television or playing video games with the index case patient was common among both siblings and parents (reported by 61% and 62%, respectively) and slightly less common with other relatives (42%). This activity was associated with an increased risk of acquiring infection among siblings but not among parents and other relatives. Siblings might interact more closely with one another while watching television than do adults. We did not distinguish between television and video games, and it is likely that video games were most commonly played between siblings and the index case patient. Hand-held video game controllers and joysticks, which are often passed back and forth, could act as fomites for transmission—the influenza virus has been reported to survive 24–48 h on hard, nonporous surfaces (eg, plastic) [–].

We did not find any increased individual risk of ILI based on the number of persons in the household, household density, or how serious the primary caretaker perceived pH1N1 to be. The lack of effect of the number of persons in the household is consistent with our observation of the distribution of serial interval times: secondary cases occurred quickly, and the distribution indicates that multiple generations of transmission within a household were uncommon. Finally, we did not observe any association between secondary ILI and receipt of the 2008–2009 seasonal influenza vaccine. This is consistent with findings in serologic studies demonstrating that vaccination with recent (2005–2009) seasonal influenza vaccines is unlikely to provide protection against novel H1N1 virus [15].

Our study has certain limitations. First, because ILI was used as a proxy of pH1N1 infection, some misclassification might have occurred. Second, though transmission among the general community was low during the time of this investigation (NYC DOHMH; unpublished data, 2009), some secondary outbreaks occurred at schools attended by siblings of students at school A. Therefore, certain secondary cases in our analysis might be attributable to community transmission. Third, this study is limited by the modest response rate and use of 3 different data collection methods. We do not know how SARs might have differed among nonparticipating households. Finally, this investigation assessed household transmission only from index case patients of high school age and only in households with a single index case patient. Different factors might be important in household transmission from persons of other ages or in households with multiple simultaneously affected students.

In summary, transmission of ILI from high school-age students occurred in 11.3% of household contacts, with much higher rates in certain groups depending on age or the degree of interaction with the index case patient. The SAR, serial interval, and protective effect of antiviral prophylaxis we observed are similar to those observed in investigations of seasonal influenza.

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Acknowledgments

We are grateful to Marci Layton, MD, and the Swine Flu Investigation Team at the NYC DOHMH; Betsy Gunnels, PhD, in the EIS Field Activities Branch (CDC); the CDC staff volunteers in the call center of the CDC Emergency Operations Center; Elizabeth Cavallaro, Catherine Dentinger, Doug Esposito, Christopher Gregory, Brian Harcourt, Rebecca Noe, Tamara Pilishvili, Jennifer Rosen, and the New York City H1N1 Epi-Aid field investigation team; and the CDC Foundation.

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Footnotes

  • Potential conflicts of interest: none reported.

  • Financial support: New York City Department of Health and Mental Hygiene; Centers for Disease Control and Prevention. Presented in part: 137th Annual Meeting of the American Public Health Association, Philadelphia, 7-11 November 2009.

  • The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

  • Received November 4, 2009.
  • Accepted December 18, 2009.
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  1. J Infect Dis. (2010) 201 (7): 984-992. doi: 10.1086/651145
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