PEDIATRICS Vol. 118 No. 4 October 2006, pp. 1439-1446 (doi:10.1542/10.1542/peds.2006-0373)
ARTICLE |
Population-Based Study of the Impact of Childcare Attendance on Hospitalizations for Acute Respiratory Infections
a Department of Epidemiology Research
c Bandim Health Project, Statens Serum Institut, Copenhagen, Denmark
b National Institute of Public Health, Copenhagen, Denmark
| ABSTRACT |
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OBJECTIVES. It is well known that children attending childcare have a higher risk of acute respiratory infections compared with children in home care; however, knowledge is sparse regarding how the excess risk of acute respiratory infection varies with age, time since enrollment, and other factors.
METHODS. A national register-based study of 138821 inpatient admissions to hospital for acute respiratory infection during 3982925 person-years of follow-up in Danish children aged 0 to 5 years. Data on child and family characteristics, childcare attendance, and hospitalizations were obtained from Danish registries. The outcome of the study was inpatient admissions to hospital for acute respiratory infection. Incidence rate ratios were estimated using Poisson regression.
RESULTS. In children <1 year of age, the first 6 months of enrollment in the first childcare facility were associated with a 69% higher incidence of hospitalizations for acute respiratory infection compared with children in home care. Similar figures for children aged 1, 2, and
3 years were 47%, 41%, and 8%, respectively. The incidence decreased after the first 6 months, and after
1 year in childcare the incidence was comparable with that of children in home care. Similar patterns were seen after second enrollment. For 0- to 2-year-old children living in households with no additional children <5 years, the excess incidence during the first 6 months of enrollment was 100% compared with 25% and 9% for children living with 1 and
2 additional children, respectively.
CONCLUSIONS. The increased risk of acute respiratory infection was most pronounced among 0- to 2-year-old children living with no other children during the first 6 months of enrollment. Our findings may suggest that it would be optimal to postpone enrollment into childcare until after 1 year of age.
Key Words: childcare acute respiratory infection morbidity epidemiology
Abbreviations: ARIacute respiratory infection DCRSDanish Civil Registration System DNPRDanish National Patient Registry ICDInternational Classification of Diseases URIupper respiratory infection LRIlower respiratory infection IRRincidence rate ratio CIconfidence interval
Previous studies have consistently found that children who are taken care of in a childcare facility away from their home have a higher risk of acute respiratory infections (ARIs) than children in home care.122 In some studies, age4,8,11,21,22 or type of facility1,2,8,12,1416 have been studied as modifying factors in the association between childcare attendance and the risk of ARIs. However, sample sizes of these studies have not allowed for safe conclusions, and many potential modifying factors have not yet been studied. Modifying factors are important to study to identify particularly vulnerable groups and focus on a possible intervention.
In the present study, we took advantage of a national central registration of enrollment into childcare facilities, child and family characteristics, and hospitalizations. Using this material, we were able to determine child and family characteristics at all times during the study period. Thus, we could obtain precise and reliable estimates of the impact of childcare attendance on hospitalizations for ARI and identify child- and family-related factors that might modify the association.
| MATERIALS |
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Study Population
The study was based on a cohort of all of the Danish children born in the period from January 1, 1989, to November 17, 2004, in a municipality with childcare registration at time of birth. The study population was identified in the Danish Civil Registration System (DCRS).23 The DCRS was established April 1, 1968, when all individuals alive and living in Denmark were assigned a unique person identification number. Since April 1, 1968, all newborns in Denmark have been assigned a unique person identification number. The number is also recorded in other Danish registers. From the DCRS, information was retrieved regarding date of birth of the child, maternal age at birth of the child, and gender of the child, and throughout follow-up, information was obtained on postal address, migration, and death of the child, as well as number of children <5 years of age in the household.
Childcare Attendance Data
The information from the DCRS was linked with information regarding enrollment into childcare facilities from 3 data sources. These sources cover all childcare attendance in 266 of the 271 Danish municipalities. For each enrollment, date of enrollment and date of withdrawal was retrieved. Children from the 266 eligible municipalities who did not figure in any of the 3 childcare enrollment registers were considered in home care. Registration of enrollment into childcare did not start at the same date in all of the municipalities. Therefore, the study period differed between municipalities. The first municipalities registered enrollment from January 1, 1989, whereas the last municipality started registering from January 1, 2004. Crèches and day care homes are facilities for children aged 6 months to 3 years. In crèches, an average of 11 teachers look after 41 children, whereas day care homes are attended by
5 children and run by 1 single child minder. Age-integrated facilities are attended by children aged 6 months to 6 years. On average, 11 teachers mind 73 children. Kindergartens are facilities for children aged 3 to 6 years where, on average, 8 teachers mind 56 children.
According to national guidelines,24 ill/infectious children should not attend childcare until they are well and no longer contagious. A child is well when able to participate in usual activities without special care.
Hospitalization Data
From the Danish National Patient Registry (DNPR),25 International Classification of Diseases (ICD) 8, or ICD-10 diagnoses were identified for children who had been hospitalized during the relevant follow-up period. The outcome of the study was defined as an inpatient admission to hospital for ARI as the main condition. Diagnoses used to define ARI in the period from 1989 to 1993 were 032, 033, 075, 381 to 383, 460 to 466, 470 to 486, 490, 500, 501, 503, 510, and 513 (ICD-8) and A36, A37, B27, H65 to H67, H70, J00 to J06, J10 to J22, J32, J35, J36, J45, J85, and J86 (ICD-10) in the period from 1994 to 2004. ARIs were subgrouped into upper respiratory infection (URI) and lower respiratory infection (LRI) as described in a previous publication.26
Statistical Methods
Impact of childcare attendance on ARI was evaluated by incidence rate ratio (IRR). IRRs with 95% confidence intervals (CI) were estimated by multiple log-linear quasi-Poisson regression of the number of cases with the logarithm of person-years at risk as offset. A quasi-Poisson regression model was used instead of a traditional Poisson regression model to take into account the overdispersion that potentially could be induced by the clustering of events within the same person, families, or childcare facilities. The quasi-Poisson regression model is based on a Poisson quasi-likelihood where the variance is allowed to be the mean multiplied by an overdispersion factor.27 The IRR estimates are the same as in the traditional Poisson regression model, but the CIs are slightly widened.
Person-years at risk were calculated from 1 week after birth, immigration, or date of first registration in one of the eligible municipalities, whichever came last. The first week after birth was not included, because infections in this period were considered to be because of perinatal complications. Children were considered at risk until the first of the following events: emigration, moving to an ineligible municipality, death, sixth birthday, or end of follow-up (November 17, 2004). Each admission to hospital of the same child during the follow-up period was counted as a new case of hospitalization with covariates according to the time of hospitalization. However, children were not considered at risk the first 14 days after a hospitalization, because hospitalizations in this period could be related to the preceding hospitalization. Thus, person-years and cases (ie, hospital admissions) from this period were not included in the analyses.
Time since enrollment in childcare (regardless of type) is a time-dependent variable categorized as follows: never in childcare and currently in home care, 0 to 5 months in the first enrollment, 6 to 11 months in the first enrollment, >12 months in the first enrollment, once in childcare and currently in home care, 0 to 5 months in the second enrollment, 6 to 11 months in the second enrollment, >12 months in the second enrollment, twice in childcare and currently in home care, or
3 times enrolled in childcare. The first category is referred to as home care. Type of (current) childcare is a time-dependent variable categorized as home care, crèche, kindergarten, age-integrated facility, or day care home. In an additional analysis, the group of children categorized as "once in childcare and currently in home care" was categorized as in childcare according to time since first enrollment to evaluate the potential effect of frail children being moved from childcare to home care. The variables year, season, county of residence, population per kilometer squared in the residence area, age of the child, number of additional children <5 years living in the household, and type of childcare were created as time-dependent variables. Variables were categorized as follows: age (quarter-year intervals at ages 02 years and half-year intervals at ages 35 years), gender (boy versus girl), maternal age when giving birth (<20, 2024, 2529, 3034, or
35 years), type of parenthood at time of birth (single versus shared), year (1-year intervals), population per kilometers squared in the residence area (
50, 51500, 5012000, 20014000, or >4000 km2), county (numbers 114), season (summer [June to August], fall [September to November], winter [December to February], or spring [March to May]), and additional children <5 years living in the home (0, 1, or
2).
By means of quasi-Poisson regression, all of the variables were tested and included as confounders if they changed the estimated IRRs of time since first enrollment presented in Table 1 by 5% or more. Effect modification was evaluated using models with a 2-way interaction term between relevant covariates. Estimation was performed by PROC GENMOD in SAS (SAS Institute Inc, Cary, NC) with Poisson error distribution, log link, and a dispersion factor estimated from Pearson statistics.28 Population-attributable risk for the scenario that no children attended childcare was estimated as 1
(pa/IRRa), with a as age groups 0, 1, 2, 3, 4, 5 years, pa as the observed proportion of ARI cases in childcare in age group a, and IRRa as the estimated IRR of ARI hospitalization at age a in children in childcare compared with children in home care adjusted for age, gender, season, year, mother's age when giving birth, number of additional children <5 years in the household, population per kilometer squared in the residence area, and type of parenthood at time of birth.29,30
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| RESULTS |
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During 3982925 person-years of follow-up, a total of 138821 inpatient hospitalizations for ARI occurred among 0- to 5-year-old children. The hospitalizations were distributed with 46750 (34%) among children <1 year old, 39186 (28%) among 1-year-olds, 19179 (14%) among 2-year-olds, 14398 (10%) among 3-year-olds, 11394 (8%) among 4-year-olds, and 7914 (6%) among 5-year-olds. Overall, 37% of the infections were LRIs, and 63% were URIs. Among the hospitalized children, 65% were admitted once, 20% were admitted 2 times, and 15% were admitted
3 times. During follow-up, 0.2% of the children died. The proportion of children leaving the cohort was 6% at <1 year old, 7% at age 1 year, and 7% at 2 years of age.
Childcare Attendance and Age
In Fig 1, the IRR of hospitalization for ARI is shown for children enrolled into childcare for the first time compared with children of the same age in home care. The excess risk of ARI associated with attendance to childcare was highest in the youngest children. At the age of 6 months, the IRR of children enrolled into childcare was 79% (95% CI: 71%88%) higher than in children in home care. At age 1 year, the excess risk of children enrolled into childcare had decreased to 44% (95% CI: 38%51%) compared with children in home care. For children in childcare aged
3 years, the risk of ARI was similar to that of children in home care.
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Time Since Enrollment and Age
Table 1 shows the IRR of ARI in children attending childcare compared with home care according to time since enrollment into first and second childcare and age for children aged 0, 1, 2, and
3 years. At first enrollment, the IRR of ARI was markedly increased within the first 6 months of attendance to childcare in children <3 years, with the youngest children being at highest risk. A trend of decreasing IRRs was seen with increasing time since first enrollment in children <3 years. After
12 months of enrollment, the risk was similar to that of children in home care. Children in childcare aged
3 years had a risk comparable with those in home care, regardless of time since first enrollment. With regard to time since second enrollment, IRRs were comparable with those of time since first enrollment. Stratifying by age at first and second enrollment rather than attained age in the analysis gave similar results.
Time Since Enrollment and Type of Respiratory Infection
Figure 2 shows the IRR of LRI and URI in 0- to 2-year-old children in childcare compared with home care as a function of time since first enrollment. The function for LRI and URI was comparable apart from the periods between 3 and 8 months and
21 months since first enrollment. After
21 months of enrollment, however, the risk of URI was similar to that of children in home care, whereas the risk of LRI was significantly lower. The pattern for time since second enrollment was similar to that of time since first enrollment (data not shown).
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Time Since Enrollment and Type of Childcare
In Fig 3, the IRR of ARI in 0- to 2-year-old children in childcare compared with home care is shown as a function of time since first enrollment in 3 different types of childcare facilities. For most times since first enrollment, the risk of ARI was highest in children attending crèche. Assuming constant differences, the excess relative risk was 9% (95% CI: 6%13%) higher in crèche compared with day care home and 8% (95% CI: 4%13%) higher in crèche compared with age-integrated facilities.
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Time Since Enrollment and Covariates
Table 2 shows the IRR of ARI in 0- to 2-year-old children in childcare compared with home care in 3 groups of time since first enrollment into childcare and in groups of selected covariates. As presented, the effect of time since enrollment was similar in girls and boys. Differences between seasons were seen, with children being at high risk during summer and autumn months at all of the times since first enrollment. With regard to maternal age when giving birth, children of mothers aged
24 and children of mothers aged
35 years were slightly more affected when enrolled into childcare during the first 6 months compared with the large group of children of mothers aged 25 to 34 years.
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Children living with no additional children <5 years in their household were markedly more affected by attendance to childcare compared with children living with children <5 years. The increased effect of childcare in children living with no other children <5 years was observed at all of the times since first enrollment into childcare. Furthermore, children living with other children <5 years had a lower risk of ARI compared with children in home care when enrolled for
12 months. Children in the least and most populated areas compared with children in other areas had slightly higher IRRs when enrolled into childcare at all of the times since first enrollment. Finally, children of mothers who were single when giving birth to the child were slightly more prone to be hospitalized for ARI when attending childcare compared with children of shared parenthoods.
Population-Attributable Risk
To estimate the percentage of ARI hospitalizations that could be prevented given a scenario where no children attended childcare, we calculated the population-attributable risk. If causal, we estimated that 11% of ARI hospitalizations could be prevented if none of the children in the cohort attended childcare.
Additional Analyses
In a previous study, we found a sevenfold increase in the rate of short-term hospitalizations in 0- to 1-year-olds in the period from 1980 to 2001 in Denmark.26 To study whether this had affected the above associations, we excluded all 1-day hospitalizations in a subanalysis. We found comparable results when including and excluding 1-day hospitalizations. In an additional analysis, we evaluated whether frail children being moved from childcare back to home care could have biased our results. In this alternative approach, the children who had been in childcare once but currently were in home care were categorized as in childcare (according to time since their first enrollment). The results from this alternative approach were almost identical to the above-reported results.
| DISCUSSION |
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The present study shows that attendance to childcare facilities was associated with an increased risk of ARI but only in children aged 0 to 2 years. The effect of attendance to childcare was strongly modified by time since enrollment and presence of additional children <5 years in the household and slightly modified by season, population density, and single motherhood.
The present study is based on register data. The DCRS contains very sensitive information and is, therefore, subject to various laws securing a very high data quality. Data regarding childcare attendance are collected routinely to organize the payment and distribution of places in childcare facilities in Denmark, which contributes to a high quality of data.31 We were, however, not able to differentiate children enrolled full-time from children enrolled part-time. In the DNPR, hospital admissions are classified according to ICD.32 Classifications in the DNPR shifted from the 8th revision to the 10th revision in 1994. This does not seem to have affected our results, because results before and after 1994 are comparable (data not shown). The validity and coverage of data regarding respiratory infections among children in the DNPR has not been evaluated. However, a Danish study33 has shown that 73.7% of all pediatric diagnoses in the DNPR are correct and, furthermore, that 13.7% have a reasonable alternative despite a wrong diagnosis. Altogether, 70.4% of infection diagnoses in the DNPR were correct. We have no reason to believe misclassification in the DNPR should vary according to type of childcare or time since enrollment.
Data from 5 municipalities were not included in the study. According to Danish standards, 2 of these municipalities were big, 2 were middle sized, and 1 was small. In the present study, we, therefore, have a slight underrepresentation of children from big municipalities. If missing data from the 5 municipalities should have an effect our results, a strong effect of big municipalities should be present in the association between childcare and infections. We find no reason to suspect that. By studying the impact of attendance to childcare through a population-based design, we included all Danish children. Thus, we reduced selection biases, which may have influenced the results of previous studies. Furthermore, we reduced information biases, because we were able to determine child and family characteristics at all of the times during the study period. This study was based on time-dependent variables denoting the obtained category of, for example, type of childcare and additional children <5 years in the household, whereas previous studies have been based on 1 or a few measurements of the exposure variables. In conclusion, we argue that the present study allows for conclusions of high internal and external validity.
Previously, the possible modifying effect of age on respiratory infections in childcare has been studied in small studies, with age divided in broad categories. In an American study of 575 children <5 years of age, Fleming et al4 found the excess risk of URI associated with attendance to childcare to be the same in children aged <36 months and
36 months. An American study of repeated ear infections based on 5818 children aged 0 to 5 years found the effect of childcare to be strongest in children aged 1 to 2 years.8 In support, a Finnish study of 2568 children aged 1 through 7 years found a decreasing excess risk of common cold and acute otitis media associated with attendance to childcare with increasing age. Only at ages 1 and 2 years was the excess risk significantly higher than among children in home care.11 A recent American study of 1188 children reported a significantly higher risk of URI associated with childcare in children aged <1.5 years but not in children aged 1.5 to 5 years.22 Finally, a recent Canadian study of 185 children aged 0 to 2 years found the same percentage of <3-month-old children with respiratory illness among children ever attending day care compared with never attending day care. At age
3 months, there was a significantly higher percentage of children with respiratory illness among childcare attendees than among nonattendees.21 The decreasing excess risk associated with childcare attendance with increasing age found in the present study, as well as by others, may be because of gradual immunologic maturation.
Only 1 study has previously investigated the effect of time since enrollment into childcare with regard to respiratory infections.9 This study of 2137 American children aged 6 weeks through 59 months found that children who had been enrolled <9 months were at significantly higher risk compared with children who had been enrolled >9 months. This was found to a similar degree in all 3 of the studied age groups (6 weeks to 17 months, 1835 months, and 3659 months). In the present study, however, we found a short-term increased risk when enrolled into childcare only in children aged 0 to 2 years.
Intriguingly, we observed that enrollment into first childcare facility for
12 months was associated with a decreased risk of ARI in children living with no other children <5 years, and enrollment for
18 months was associated with a lower risk of LRI. This could reflect a selection effect rather than a biological effect if the children most prone to respiratory infections were taken out of childcare over time, leaving the healthiest children in childcare and, thus, giving an artificially low IRR estimate for childcare after a long time of enrollment. However, this effect persisted after conducting an additional analysis of children aged 0 to 2 years in which children who once were in childcare were considered in childcare irrespective of whether they went back to home, eliminating the potential bias introduced by frail children being taken out of childcare. Thus, the lower IRR after a long time of enrollment into childcare is likely to reflect a biological phenomenon. To our knowledge, the present study is the first to show that increasing time since enrollment into first childcare can be associated with a protective effect against ARI and LRI in certain groups.
Regarding the type of childcare facility, we found attendance in crèche to be associated with a slightly higher risk of ARI compared with attendance in home day care. This has been found previously by others and is most often ascribed to crowding in the type of facility.3,4,8,12 Despite the same degree of crowding as in crèches, we found a slightly lower risk in age-integrated facilities. This may be caused by the fact that age-integrated facilities are a recent phenomenon in Denmark and that the facilities are, therefore, designed for childcare purposes, whereas older crèches are often housed in buildings made for purposes other than childcare.
By studying time since enrollment in different strata of covariates, we attempted to identify factors that might modify the impact of childcare and thereby identify vulnerable groups. The short-term increased risk of ARI was modified by some of the covariates, whereas it was not modified by others.
We found autumn and summer months to be associated with a higher excess risk of ARI when attending childcare compared with during winter months. This may be because of the fact that during winter months young children are generally at a high risk of ARI, and the effect of childcare becomes less important.
Children from households with no additional children <5 years of age were found to have a markedly increased risk of ARI when enrolled into childcare compared with children living with other children <5 years. We believe that this reflects less exposure to ARIs from surroundings before enrollment into childcare. Another explanation may be that women becoming first-time mothers in households with no additional children <5 years have not been exposed to infectious diseases to the same degree as multiparous women and, therefore, have not delivered the same degree of protective antibodies to her first child.
Children of mothers who were single when giving birth were more frequently hospitalized for ARIs than children from shared parenthoods (data not shown). This, however, does not explain why children of single mothers were more prone to ARIs than children from shared parenthoods when enrolled into childcare. We have no apparent explanation to this finding.
A recent Danish study34 found the male/female ratio of admissions because of respiratory tract infections in children aged 0 to <5 years to be 1.45 (95% CI: 1.421.48). In our material, we found similar gender differences (data not shown), but although boys were more prone to ARI than girls, attendance to childcare had a similar effect on boys and girls. This is in contrast with a previous finding by Marbury et al,12 who found childcare attendance to have a more negative impact on girls compared with boys.
As opposed to most previous studies, the outcome of the present study was hospitalizations for ARIs rather than self-reported or childcare teacher-reported ARI morbidity. As described, we found results comparable with those of previous studies regarding well-known risk factors for ARIs, such as young age, male gender, and day care attendance versus no day care attendance. This suggests that the new results presented in the present article are applicable not only to ARI hospitalizations but to nonhospital-demanding ARI morbidity as well. Because it is difficult to differentiate inflammatory from infectious respiratory diseases using a register-based material like DNPR with few clinical data, we used a broad definition of ARI, including hospitalizations for asthmatic bronchitis and asthma without specification. Asthmatic bronchitis and asthma without specification accounted for 0.8% and 8.2% of the total number of ARI hospitalizations, respectively.
In 2002, maternity/paternity leave was extended to a total of 52 weeks on benefit for parents in Denmark. Thus, it is made possible for parents to keep their child at home for a longer time, thereby delaying enrollment into childcare. This is well in line with our findings of the most vulnerable period during the first year of life. Subanalyses did not indicate that extension of the maternity/paternity leave in 2002 affected the percentage of Danish children attending childcare or the overall incidence of ARI. Because most countries do not have maternity/paternity leave as long as in Denmark, a more modifiable factor might be for parents to enroll their children in day care homes or age-integrated facilities in preference to crèches, although only minor differences were seen.
In the entire cohort of 0- to 5-year-old children, we estimated that 11% of all of the inpatient ARI hospitalizations were because of attendance to childcare if causal. This population attributable risk percent is concordant with a previous study of American 0- to 5-year-old children.9
| CONCLUSIONS |
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We found that children between 0 and 2 years had an excess risk of ARI when attending childcare. The excess risk of ARI decreased with increasing age. We found the risk of ARI to be highest within the first short period of enrollment. However, it increased again with a shift to a new childcare facility. Finally, children living with no other children <5 years had an increased risk of ARI when attending childcare. Our findings may suggest that it would be optimal to postpone enrollment into childcare until after 1 year of age.
| ACKNOWLEDGMENTS |
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The present study received support from the Health Insurance Foundation, the Egmont Foundation, the Danish Graduate School in Public Health Science, Rosalie Petersens Fond, Gangstedfonden, and the National Union of Nursery and Childcare Assistance.
| FOOTNOTES |
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Accepted May 24, 2006.
Address correspondence to Mads Kamper-Jørgensen, Department of Epidemiology Research, Statens Serum Institut, Artillerivej 5, 2300 Copenhagen S, Denmark. E-mail: mka{at}ssi.dk
The authors have indicated they have no financial relationships relevant to this article to disclose.
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