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Article

Preterm Birth and Inhaled Corticosteroid Use in 6- to 19-Year-Olds: A Swedish National Cohort Study

Hartmut Vogt, Karolina Lindström, Lennart Bråbäck and Anders Hjern
Pediatrics June 2011, 127 (6) 1052-1059; DOI: https://doi.org/10.1542/peds.2010-3083
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Abstract

OBJECTIVE: Preterm birth is associated with respiratory morbidity later in life, including asthma. Previous studies have mainly focused on asthma in early childhood in children born extremely preterm. In this study, we examined the risk of asthma in a national cohort of schoolchildren grouped according to degree of immaturity expressed as completed gestational weeks at birth.

METHODS: This was a register study in a Swedish national cohort of 1 100 826 children 6 to 19 years old. Retrieval of at least 1 prescription of inhaled corticosteroids (ICS) during 2006 was used as the main indicator for asthma. Logistic regression was used to test hypotheses, with adjustment for multiple socioeconomic and perinatal indicators.

RESULTS: Degree of immaturity, expressed as completed gestational weeks at birth, had an inverse dose-response relationship with ICS use. Compared with children born between 39 and 41 weeks' gestation, the odds ratio for ICS use increased with the degree of prematurity, from 1.10 (95% confidence interval: 1.08–1.13) for children born in weeks 37 to 38, to 2.28 (95% confidence interval: 1.96–2.64) for children born in weeks 23 to 28, after adjustment for confounders. The increase in ICS use with decreasing gestational age at delivery was similar in boys and girls, and declined with older age.

CONCLUSION: Preterm birth increased the risk of ICS use in these 6- to 19-year-olds by degree of immaturity, from extremely preterm to early term birth.

WHAT'S KNOWN ON THIS SUBJECT:

Preterm birth is associated with respiratory morbidity later in life, including asthma. Previous studies have mainly focused on asthma in early childhood in children born extremely preterm.

WHAT THIS STUDY ADDS:

Moderate preterm (33–36 weeks' gestation) and early term (37–38 weeks' gestation) births are associated with increased risk of asthma medication at 6 to 19 years of age. Gestational age per se seems to be the most important factor responsible for this effect.

Preterm birth, defined as a gestational age of <37 completed weeks at delivery, is associated with increased respiratory morbidity later in life.1 Preterm children are born with underdeveloped lungs, decreased number of alveoli, and impaired respiratory function.2 These findings contribute to an increased risk of asthma and bronchitis, especially during infancy.1 Respiratory disease is particularly common among preterm children who develop bronchopulmonary dysplasia.3

It has been suggested that morbidity in adult life might already be determined in utero.4,5 Many different factors during infancy may account for the development of asthma,6 and there is a strong association between pre- and perinatal events and hospital admission because of bronchitis and asthma during infancy.7 An increased risk for asthma can persist throughout adulthood,8 but few studies have examined how the effect of early exposures changes beyond early childhood.

Potential causal pathways between prenatal factors, preterm birth, and asthma are rather complex, as discussed in the review by Jaakkola et al.1 Various prenatal factors may result in preterm birth and, in turn, an increased risk for asthma. A prenatal factor—for example, maternal smoking—might also be a common determinant for both preterm birth and asthma. It can also be difficult to disentangle the effects of pre- and postnatal maternal smoking.

Most studies examining the potential effect of preterm delivery on respiratory morbidity have concentrated on extremely preterm infants. Only 2 previous studies have assessed the effects on asthma of moderately preterm (34–36 weeks' gestation)9 or early term (36–38 weeks' gestation)10 births in children up to the age of 6 years. To our knowledge, no previous study has assessed the effects of late preterm birth on asthma or asthma medication after 6 years of age. There are some studies that have evaluated the development of airway function in general up to early adulthood, but they focus mainly on very premature born children or a small number of individuals.11,12

The aim of the present study was to examine the potential effect of gestational age on inhaled corticosteroids (ICS) use as a proxy for asthma in children ages 6 to 19 years. We also investigated the importance of the degree of immaturity by using all weeks of gestation (23–45 weeks) in this study.

METHODS

This national cohort study was based on Swedish national registers held by the National Board of Health and Welfare and Statistics (Sweden). All Swedish residents are assigned a unique 10-digit identification number at birth (ie, the personal identification number). We built a database using the personal identification number to link information from different registers. The study was approved by the regional ethics committee in Stockholm.

Study Population

The study population was created from the 1 142 806 children born in Sweden between 1987 and 2000 according to the Swedish Medical Birth Register. All infants fulfilled the criteria of being offspring of 2 Swedish parents according to the Swedish Multi-Generation Register and residents in Sweden on December 31, 2005, according to the Register of the Total Population. Offspring of foreign parents were excluded because of the influence of ethnicity on asthma prevalence in Sweden.13

From this population, we excluded 33 183 children who had at least 1 malformation reported at birth by the attending pediatrician. However, minor malformations (undescended testicles, preauricular appendage, and congenital nevus) and hip dislocation were considered insignificant and were not excluded.

A total of 8797 children with a registered birth weight for gestational age >3 SDs or less than −6 SDs, according to the growth chart developed by Marsál et al,14 were excluded as probable coding errors,15 leaving 1 100 826 individuals to be included in the study population.

The register variables used in the study are described in Table 1.

View this table:
TABLE 1

Register Variables in the Study

Asthma

The Swedish Prescribed Drug Register contains data with unique patient identifiers for all drugs prescribed and dispensed to the entire population of Sweden (>9 million inhabitants) since July 2005. The purchase of at least 1 prescription of a drug with an Anatomical Therapeutic Chemical (ATC) code of R03AK or R03BA during the calendar year 2006, according to this register, was used to create the variable “inhaled corticosteroids.” The purchase of at least 1 prescription of a drug with an ATC code starting with R03 (comprising not only ICS but also β agonists and all other drugs for asthma) during the calendar year 2006, according to this register, was used to create the variable “any asthma medication.”

There were considerable regional differences in the purchase of asthma medications (Table 2), supposedly reflecting regional differences in prevalence of asthma as well as differences in access to and prescription patterns in care. A 4-category county variable with different levels of retrieval of prescribed ICS was created to adjust the analysis to these regional differences: 5.0% to 5.7%, 4.6% to 4.9%, 4.0% to 4.5% and 3.5% to 3.9%.

View this table:
TABLE 2

Prevalence of Asthma Medication According to Sociodemographic and Parental Asthma Indicators

Statistical Analysis

Logistic regression was used to calculate odds ratios (ORs) with 95% confidence intervals (CIs) as estimates of effects, with ICS as defined here as the outcome variable.

Four models were used to investigate the effects of preterm birth on ICS. Age was entered as a continuous variable in all models according to the age profile of ICS use. Because this age profile differed between boys and girls, decreasing with older age in boys and increasing with older age in girls, we included an interaction term of age * gender in all models. Model 1 was adjusted for age and gender only. In model 2, we added county of residence, maternal education, social assistance, maternal and paternal asthma medication, and maternal smoking during pregnancy as confounders. Thus, we considered model 2 as the fully adjusted model. We investigated potential mediating variables by adding the potential perinatal mediators small for gestational age (SGA), chorioamnionitis, multiple birth, asphyxia, and cesarean delivery to model 3 and hospital admission because of respiratory syncytial virus (RSV) infection to model 4.

Multiplicative interactions for ICS of gender, age, and maternal education with gestational age in 3 categories (weeks 23–32, weeks 33–36, and weeks 37–41) were investigated in model 1. Maternal education was dichotomized with ≤12 years of schooling as yes.

Statistical analysis was performed using PASW statistics 18 for Windows Release 18.0.1 (SPSS Inc, Chicago, IL).

RESULTS

In all, 7.39% of the boys and 6.45% of the girls had purchased any asthma medication in 2006. Corresponding rates for ICS were 4.89% and 3.78%, respectively. The distribution of asthma medication in relation to sociodemographic characteristics and parental asthma medication is shown in Table 2. Table 3 presents gestational age categories grouped according to sociodemographic characteristics and parental asthma medication.

View this table:
TABLE 3

Gestational Age Grouped According to Sociodemographic Indicators and Parental Asthma Medication; Values Are Given as Percentages

ICS medication grouped according to perinatal and child morbidity indicators is summarized in Table 4. The prevalence of ICS use declined by increasing age in males; in contrast, it increased slightly by age in females born at term. Increasing gestational age was related to a decreasing prevalence of ICS use in both genders (P for trend, <.001), with similar effect sizes for boys and girls of preterm birth on ICS in interaction analyses (P = .21 to .38).

View this table:
TABLE 4

Perinatal and Child Morbidity Indicators and Inhaled Cortisone Medication; Values Are Given as Percentages

Table 5 presents the adjusted ORs for ICS use after multivariate analyses. All models included terms for the interaction between age and gender. The ORs for ICS use were higher in all categories of gestational age <39 weeks compared with term infants and increased with degree of immaturity. Adjusting the analysis for confounding variables (county of residence, maternal education, parental asthma medication, and maternal smoking during pregnancy) had only marginal effects on these estimates. The ORs were slightly attenuated in model 3 after addition of perinatal mediators (SGA, chorioamnionitis, multiple birth, asphyxia, and cesarean delivery). The effects of the preterm birth categories on ICS use in Table 5 were similar in boys and girls.

View this table:
Table 5

Logistic Regression of Gestational Age and Inhaled Cortisone Use

The introduction of cesarean delivery contributed to the attenuation of the ORs for gestational age in model 3. The OR for cesarean delivery was 1.13 (95% CI: 1.09–1.16) in model 3 and 1.20 (95% CI: 1.17–1.23) after removal of gestational age from the model. The addition of SGA and chorioamnionitis in model 3 did not affect the ORs for gestational age. The ORs for SGA in models with and without gestational age were 1.06 (95% CI: 1.00–1.12) and 1.16 (95% CI: 1.10–1.22), respectively. Corresponding ORs for chorioamnionitis were 1.03 (95% CI: 0.83–1.26) and 1.32 (95% CI: 1.09–1.61), respectively.

Children of all gestational ages who had been hospitalized for RSV infection had an increased rate of ICS medication (Table 4). The addition of RSV hospitalization to the logistic regression analysis, however, did not affect the ORs for gestational age in the analysis presented in Table 5.

The effect of extreme and very preterm birth (weeks 23–32), as well as moderately preterm birth (weeks 33–36), was attenuated by increasing age in boys as well as girls (P < .001 in interaction analyses for each gender separately). The effects were very similar in offspring of mothers with ≥13 years of schooling compared with those with fewer years of education (P = .27 to .40).

DISCUSSION

In this study in a national cohort of >1 million 6- to 19-year-olds, we found that the risk of ICS use, as a proxy for asthma, increased with degree of immaturity at birth as defined by gestational age. An effect of immaturity on ICS use was present also in early and moderately term births, and the effect was similar in boys and girls. This effect decreased with older age but was only marginally attenuated when multiple indicators of potential perinatal, hereditary, and socioeconomic confounders were adjusted for in the analysis.

The multivariate analysis indicates that immaturity per se seems to be the most important factor responsible for the effect of preterm birth on ICS use later in life. Lung development is a continuous process that starts in utero and continues into childhood. Every week of maturation is important for the development of the lung. A shortened pulmonary development because of preterm delivery results in different structural and functional deficits of the lung such as low lung volumes, decreased airway stability, and increased airway resistance.16 It is reasonable to believe that these functional and structural changes of the airway also play an important role in the increased risk for asthma medication later in life.

This study demonstrates a close relationship between preterm birth and asthma medication in schoolchildren and adolescents, but this association was attenuated by increasing age, which suggests a fading effect on asthma with older age. This is consistent with the meta-analysis by Jaakkola et al1 that showed stronger effects of prematurity in younger populations.

Moderately preterm birth is known to be associated with an increased neonatal respiratory morbidity.17 However, long-term consequences have seldom been investigated, and previous investigations have shown inconsistent results.8,–,10,18,–,20 In our study, moderately preterm birth was associated with a 20% to 30% increased risk of ICS medication use, something which has been suggested but not convincingly demonstrated before.

Our study had a sufficiently large population to make it possible to detect an increased risk of asthma medication up to the age of 15 to 19 years also in subjects born at 37 to 38 weeks' gestation. The risk increase for early term birth was only 10%. On the population level, however, this small risk increase accounts for almost 2% of all cases because of the large proportion of the population exposed to this risk factor (20%), whereas the extremely preterm group accounted for only 0.2% of all cases of ICS use.

Cesarean delivery is a well-known risk factor for asthma.21 In our study, cesarean delivery was associated with a 20% increased risk of asthma medication. However, some of the effect was related to immaturity at birth because the OR was reduced after adjustment for gestational age. This finding has important implications for the timing of cesarean deliveries in obstetric care, because unnecessary early deliveries should be avoided to prevent the increased risk for asthma later in life.

Chorioamnionitis is a major cause of preterm delivery but has also been described as an independent risk factor for wheeze22 and physician-diagnosed asthma23 in early childhood. We did not find that chorioamnionitis contributed to an increased risk of asthma medication after adjustment for gestational age. The focus on school-aged children in this study, however, does not exclude potential effects on ICS use in younger children. The crude nature of the indicator for chorioamnionitis used in this study, which can only be expected to detect quite severe infections with clinical relevance in the perinatal period, also needs to be considered.

Low birth weight and gestational age are closely correlated. SGA did not contribute to an increased risk of asthma medication after adjustment for prematurity in the present study, consistent with another cohort study from Alaska.24 In contrast, recent twin studies strongly suggest that birth weight has effects on asthma25,26 independent of familial and genetic factors.27 A previous Finnish study of 16-year-old twins demonstrated an increasing risk of asthma with increasing ponderal index whereas birth weight and gestational age did not have any independent effects.28 The etiology of SGA in multiple pregnancies has some specific risk factors, with different degrees of twin transfusion syndrome being a fairly common cause; this may suggest that these findings are not necessarily relevant for singletons. However, an association between fetal growth restriction and development of asthma independent of gestational age could be more easily detected in studies of twin pairs.

Hospital admissions for respiratory illness due to RSV infections were associated with a twofold increased risk of asthma medication in school-aged children in this study. Preterm children have an increased risk for hospitalization for RSV infections.29 In this study, as well as in an US cohort study,10 however, hospital admissions for RSV infections did not affect the association between gestational age and medication for asthma, indicating that the association between preterm birth and asthma medication is not mediated by an increased susceptibility to respiratory infections.

An association of socioeconomic disadvantage to asthma (Table 2) as well as to preterm birth (Table 3) was demonstrated in this study. Adjusting the multivariate analysis in Table 5 to our 2 socioeconomic indicators maternal education and social assistance, however, resulted in marginal effects only, indicating that socioeconomic confounding was not a major issue in this study.

This study does not comprise any markers of atopic sensitization. It is unlikely, however, that the association between gestational age and ICS use is related to allergy. Previous studies indicate rather that prematurity is associated with a decreased risk of allergic sensitization,18 allergic rhinitis,8 and eczema.30,31

The strength of this study is the large population with data regarding potential confounders, risk factors, and outcome collected independently from each other and without involving the study subjects, thus minimizing various types of bias (eg, selection, recall). Moreover, our study provides an analysis of practically the entire Swedish population between 6 and 19 years of age in 2006, which makes us confident that our results reflect a representative sample for these age groups in Sweden. It is reasonable to believe that our findings could be generalized to other similar populations. We were able to adjust our analysis for a large number of potential confounders (Table 1), such as perinatal and sociodemographic confounders, maternal smoking habits, and family history of asthma, but cannot exclude the possibility of other confounders linking preterm birth with asthma, considering the complex etiology of preterm birth as well as asthma. A limitation of the cross-sectional design of this study is the possibility that an increased survival rate of extremely preterm infants in more recent birth cohorts might bias the age pattern of this category of preterm birth for ICS use by increasing the ORs more for younger compared with older children in the cohort.

There is no gold standard for the diagnosis of asthma.32 The prevalence of asthma in Swedish schoolchildren and young adults during the last decades has been estimated to be between 5% and 11%.33 The prevalence rates of physician-diagnosed asthma in 2 large cohorts in northern Sweden correlate in similar age groups fairly well with the prevalence rates of ICS used as a proxy for asthma in our survey.34,35

Prescription of asthma medication as a proxy for asthma has certain limitations.36 This study is based on the use of ICS because several other antiasthmatic drugs are sometimes prescribed for purposes other than asthma. ICS are used by a substantial number of individuals with active disease37 and are more likely to represent clinically significant disease.34 We have not included children younger than 6 years of age because of diagnostic problems and the risk of overtreatment with ICS in this age group.38

Economic resources of the parents could influence the use of asthma medication39 and contribute to an underdiagnosis of asthma related to a low socioeconomic status. Sweden has a reimbursement system for prescription medicines, however, which means that patients only pay a rather low maximum amount per year for the medicines. We also adjusted for various socioeconomic determinants in our analyses, but this did not affect the association between gestational age and asthma medication. A more serious methodologic concern in this study is probably the regional variation of our outcome measure—purchase of asthma medication. The Swedish health care system provides better access to care in urban areas compared with rural areas. We cannot completely exclude the possibility of bias through regional patterns of access to care that overlap with regional rates of preterm birth and asthma prevalence. The marginal effect in our study when we did adjust for the county variation, however, seems to indicate that such bias was minor.

CONCLUSIONS

This population-based cohort study found an association between degree of immaturity, as expressed by gestational age, and medication for asthma among 6- to 19-year-olds in Sweden, independent of socioeconomic confounders, perinatal mediators, and RSV infections in infancy. We showed that even infants born at early term have a higher risk for asthma medication use as a proxy for asthma later in life compared with children born at term (ie, every gestational week is important for the risk for developing asthma).

ACKNOWLEDGMENTS

Dr Bråbäck was supported by the Umeå SIMSAM Node (Microdata research on childhood for lifelong health and welfare) financed by the Swedish Research Council. Drs Lindström and Hjern were supported by The Swedish Council for Working Life and Social Research (Stockholm, Sweden). Dr Vogt was supported by The Swedish Asthma and Allergy Association (Stockholm, Sweden).

Footnotes

    • Accepted February 1, 2011.
  • Address correspondence to Hartmut Vogt, MD, Department of Clinical and Experimental Medicine, Division of Pediatrics, Faculty of Health Sciences, Linköping University, SE-581 85 Linköping, Sweden. E-mail: hartmut.vogt{at}liu.se

  • All authors made substantial contributions to the study conception and design, acquisition of data, or analysis and interpretation of data. They also all assisted in drafting the article or revising it critically for important intellectual content. All authors gave final approval of the version to be published.

  • FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

  • ICS =
    inhaled corticosteroids •
    ATC =
    Anatomical Therapeutic Chemical •
    OR =
    odds ratio •
    CI =
    confidence interval •
    SGA =
    small for gestational age •
    RSV =
    respiratory syncytial virus

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Pediatrics
Vol. 127, Issue 6
1 Jun 2011
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Preterm Birth and Inhaled Corticosteroid Use in 6- to 19-Year-Olds: A Swedish National Cohort Study
Hartmut Vogt, Karolina Lindström, Lennart Bråbäck, Anders Hjern
Pediatrics Jun 2011, 127 (6) 1052-1059; DOI: 10.1542/peds.2010-3083
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