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Asthma and Internalizing Behavior Problems in Adolescence: A Longitudinal Study

From the Schools of Population Health (R.A., J.M.N., G.M.W.) and Social Science (J.M.N.), The University of Queensland, Queensland, Australia; Mater Children’s Hospital, Queensland, Australia (M.O.C.); South Brisbane Child & Youth Mental Health Services, Queensland, Australia (W.B.); and the Department of Social Medicine, University of Bristol, Bristol, UK (D.A.L.).

Address correspondence and reprint requests to Rosa Alati, PhD, School of Population Health, University of Queensland, Public Health Building, Herston Rd., Herston, Queensland 4101, Australia. E-mail: r.alati{at}sph.edu.au; rosalati{at}ozemail.com.au

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX 1 APPENDIX 2 APPENDIX 3 NOTES REFERENCES

 
Objective: Clinical studies of asthmatic children have found an association between lung disease and internalizing behavior problems. The causal direction of this association is, however, unclear. This article examines the nature of the relationship between behavior and asthma problems in childhood and adolescence.

Methods: Data were analyzed on 5135 children from the Mater University Study of Pregnancy and its outcomes (MUSP), a large birth cohort of mothers and children started in Brisbane, Australia, in 1981. Lung disease was measured from maternal reports of asthma/bronchitis when the children were aged 5 and maternal reports of asthma symptoms when the children were aged 14. Symptoms of internalizing behaviors were obtained by maternal reports (Child Behavior Checklist) at 5 years and by maternal and children’s reports at 14 years (Child Behavior Checklist and Youth Self Report).

Results: Although there was no association between prevalence of asthma and externalizing symptoms, asthma and internalizing symptoms were significantly associated in cross-sectional analyses at 5 and 14 years. In prospective analyses, after excluding children with asthma at 5 years, internalizing symptoms at age 5 were not associated with the development of asthma symptoms at age 14. After excluding children with internalizing symptoms at 5 years, those who had asthma at 5 years had greater odds of developing internalizing symptoms at age 14.

Conclusion: Children who have asthma/bronchitis by the age of 5 are at greater risk of having internalizing behavior problems in adolescence.

Key Words: lung disease • asthma • behavior problems • adolescence • internalizing symptoms

Abbreviations: MUSP = Mater University Study of Pregnancy; FCV = first clinic visit; YSR = Youth Self Report; CBCL = Child Behavior Checklist; DSSI/SAD = Delusions-Symptoms-States-Inventory: State of Anxiety and Depression.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX 1 APPENDIX 2 APPENDIX 3 NOTES REFERENCES

 
The increase in the prevalence of asthma in Western populations has recently directed attention on a variety of comorbidities associated with its occurrence. In particular, there appears to be a relationship between mental health and lung disease across the whole age spectrum. National and international evidence points to a greater prevalence of anxiety and affective disorders among asthmatic adults (1–7). In Australia, adults with asthma are more than twice as likely to experience major depression (14.4%) compared with those with no asthma (5.7%) (6,7). In one study, the prevalence of "all depression" reached 22.1% in asthmatics as opposed to 16.7% in nonasthmatics (7).

Clinical studies suggest that there is also an association between lung disease and psychologic problems in childhood (8–16). Both male and female children with asthma experience a greater prevalence of emotional difficulties as compared with children with no asthma (8,9,15,16). Although there are some inconsistencies in the literature (12), a recent metaanalysis of 78 studies found that asthmatic children had increases in behavioral problems of approximately one half to two thirds of a standard deviation relative to comparison groups, with differences being more evident in the internalizing domain (9). The majority of these studies have measured "internalizing behavior" by using the withdrawn, anxiety/depression, and somatic complaints subscales of the Achenbach Child Behavior Checklist (CBCL (17,18)).

To date, the reason for the relationship between internalizing behavior and lung disease in childhood is uncertain, although some possible mechanisms underlying the association have been examined. Some evidence from clinical studies suggests that asthma and its management may trigger greater anxiety among asthmatic children (19). This is supported by findings suggesting that children who develop greater control and better management of asthma symptoms are less likely to show behavior problems (20). The family setting appears to be important in this process. Parental psychiatric disorders and/or marital conflict have been found to adversely affect the psychologic development of a child and his or her ability to cope with asthma and related medical compliance (13,21). These findings suggest that asthma may exacerbate behavior problems and that difficulties in managing children with asthma may be indirectly associated with these behavior problems (13).

On the other hand, a complex interactive relationship appears to exist among "emotions," "life stress," and lung disease (22). Children with asthma who experience "chronic stress" and "stressful life events" have been found to have a threefold increased risk of experiencing acute asthmatic attacks in the 2 weeks after the event (22). Experimental evidence also suggests that various emotions and types of stress have a different effect on respiratory resistance among asthmatic and nonasthmatic children (11). Seen from this perspective, "emotional stressors" may play a role in the causal pathway to the development of asthma or the worsening of its symptoms in childhood.

It is only in recent years that more attention has been given to the nature of the causal direction between behavioral problems and lung disease in childhood. It is not clear whether psychologic factors contribute to or exacerbate severe symptoms among children with asthma, whether early emotional difficulties have a causal role in the etiology of asthma, whether emotional and behavioral problems are the result of the asthma and its treatment, or whether other intervening or confounding factors explain the comorbidity (14). Prospective longitudinal studies are needed to clarify the direction of these associations and ascertain the causal processes involved.

To date, the longitudinal evidence in this area is short-term or drawn from clinical or at-risk populations (23,24) and the few population studies available suggest a complex picture. Evidence from the Epidemiology Catchment Area Study, for example, has found that adults receiving asthma treatment, but not those with untreated asthma, may be at increased risk of experiencing panic attacks (24). Among the participants of the Dunedin Study in New Zealand, experience with respiratory disturbance was found to contribute to panic disorder/agoraphobia in early adulthood, but not to other anxiety disorders (25).

This article explores the nature of the relationship between behavior and lung disease in childhood and adolescence in a large birth cohort study with follow-up phases when the children were aged 5 and 14. The association between behavior and lung disease (measured as reported symptoms of asthma and bronchitis) are examined in three ways. First, we examine the cross-sectional association between asthma and behavior, respectively, at 5 and 14 years. Second, we use the longitudinal nature of the study to examine the association of asthma duration on behavior to determine whether there is a dose-response with asthma duration such that those who have asthma symptoms at both ages 5 and 14 have the greatest risk of internalizing behavior problems at age 14. Finally, the direction of the relationship between asthma and behavior from 5 to 14 years of age is explored.

	METHODS

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The Mater University Study of Pregnancy (MUSP) is a prospective, longitudinal study of mothers and their children. Between 1981 and 1984, 8556 consecutive women attending their first obstetric visit at the Mater Misericordiae Hospital in Brisbane were invited to participate in the study and were followed up at 3 to 5 days, 6 months, 5 and 14 years after the birth. Some 7223 live singleton babies, for whom both maternal interviews and obstetric data were available at discharge from the hospital, constitute the MUSP birth cohort study. Of these, 52% (n = 3758) were males and 48% (n = 3465) were females.

Measures
Maternal Reports of Asthma/Bronchitis at 5 and 14 Years
Asthma symptoms were assessed at both 5 and 14 years through maternal reports. At 5 years, mothers were asked: "Has your child had any of these conditions or symptoms continuing longer than three months?" ("asthma," "bronchitis," and so on). Mothers could select from the following prompts: "No, not longer than 3 months," "Yes, but it limited activities very little," or "Yes, and it limited activities a lot." Because in clinical practice, diagnostic terms such as wheezy bronchitis, bronchiolitis, and asthma tended to be used interchangeably until the late 1980s (covering the early period of our study) (26), it is possible that mothers may have indicated that a child who would by today’s standards be diagnosed with asthma had bronchitis. For this reason, in our main analyses, symptoms of asthma and bronchitis were summed, so all those whose mothers indicated that they had either of these conditions were considered a case at age 5. The two symptoms overlapped: 51.5% (n = 50) children whose mothers reported symptoms of bronchitis also had symptoms of asthma reported. The answer were recoded into "no" (no = not longer than 3 months) and "yes" (yes = but it limited activities very little or yes = it limited activities a lot). We conducted sensitivity analyses in which only those children whose mothers indicated that they had symptoms of asthma were included as cases (those with symptoms of bronchitis were considered as noncases). In these analyses, none of the results were substantially different from those presented here.

At 14 years, mothers could select whether their child had experienced asthma by ticking "yes" or "no" to the following question: "Has your child had any of the following?" ("asthma," "diabetes," and so on). Bronchitis was not included in the list at age 14. Because this item did not contain a specific timeframe, we used an item from the CBCL ("Which best describes your child in the last 6 months?" "asthma") to confirm that the cases selected at 14 were new cases of asthma. Only 9.5% (n = 382) of mothers who indicated that their children had asthma reported that this had not occurred in the previous 6 months. We conducted sensitivity analyses in which we selected only those children whose mothers reported that they had asthma symptoms in the previous 6 months. Results did not differ substantially from those presented in this article.

Maternal and Child Reports of Internalizing Symptoms
Reports of child behavior were obtained at 5 and 14 years by using two modified subscales of the CBCL (18,27). The CBCL is a well-known scale that is widely used to assess symptoms of mental health/behavior difficulties among children. The checklist includes subscales assessing symptoms of externalizing, internalizing, and other problematic behaviors (18,27). Studies on the reliability and validity of the CBCL have been extensively summarized in the Achenbach manual (18). The internalizing and externalizing scales were used in this study. At age 5, the checklist was completed by the mother only. At age 14, the checklist was completed by the mother and, in addition, the Youth Self Report (YSR) of behavioral problems was completed by each child (17). In this analysis, we have used both CBCL and YSR at 14 years (17), because concerns have been raised about parents overreporting internalizing symptoms of behavior problems in asthmatic children (9).

At 5 years, a modified version of CBCL was administered to mothers (27), with response alternatives of 0 = "often," 1 = "sometimes," and 2 = "rarely/never." The scale "internalizing problems" at 5 years contained 10 items from the CBCL internalizing subscales of anxiety/depression and withdrawn (Appendix 1). The scale achieved a Cronbach’s alpha of 0.76 with an interitem mean correlation of 0.25. Items were summed and recoded into "normal" and "case" using the 10% cutoff to indicate "caseness."

At 14 years, the externalizing and internalizing behavior scales of the CBCL and YSR and the three subscales from which the "internalizing scale" is derived were used. The externalizing scales were constructed from the "aggression" and "delinquency" subscales and were made up of 32 (CBCL) and 31 items (YSR). The "internalizing scale" was constructed from the "withdrawn," "anxious/depressed," and "somatic complaints" scales, which were made up of 31 items for the children’s report (Appendix 2). The scales were categorized into two categories with a 10% cutoff for "cases." The externalizing scales achieved Cronbach’s alpha of 0.92 (CBCL) and 0.87 (YSR), whereas Cronbach alphas for the internalizing scales were 0.87 for the CBCL and 0.92 for the YSR. For seven of the nine questions in the "somatic complaints" scale, the phrase "without known medical cause" was omitted. Our scale, however, had reliability coefficients that were broadly comparable to those reported by Achenbach (17,18). Because one of the items in the "somatic complaints" scale ("rashes, skin problems") may be associated with asthma problems, we conducted sensitive analyses excluding this item from the scale. None of the results were substantially different than the one presented in this article.

Control Variables: Socioeconomic Status, Marital Satisfaction, and Maternal Mental Health
Available measures of socioeconomic status included maternal age and education at entry of the study (first antenatal visit) and family income at 5 years. Marital satisfaction was assessed at 5 years by using the Spanier Dyadic Adjustment Scale (DAS) (28) (see Appendix 3). The scale has been found to be a valid instrument in the Australian setting and has been used to assess marital satisfaction in different cohort studies (29,30) and achieved a Cronbach’s alpha of 0.86 in this study. The scale distribution was recoded into "good adjustment" and "conflict." Those who consistently answered the questions in a way that suggested they were dissatisfied or very dissatisfied were identified as having a relationship characterized by conflict (approximately 3% of mothers). The remaining was identified as having "good adjustment."

Maternal mental health status at 5 years were measured through the two seven-item Anxiety and Depression subscales of the Delusions-Symptoms-States-Inventory: State of Anxiety and Depression (DSSI/SAD) (31). The DSSI/SAD is a self-report measure for the detection of symptoms of depression and anxiety (31). It does not constitute a clinical diagnosis of depression and it shares with other self-report measures the disadvantage of not detecting less severe episodes (31,32). Cronbach’s alpha of 0.86 and 0.83 were obtained, respectively, for the depression and anxiety subscales. Symptoms of anxiety and/or depression were counted if the mothers said they had experienced each symptom "all the time," "most of the time," or "some of the time." We used a 10% cutoff in the analyses that follow.

Data Analysis
Associations between asthma and externalizing and internalizing symptoms at 5 and 14 years were examined by presenting frequencies in percentage of the sample and using the chi-squared test. To test the casual direction of each of the two conditions, multivariable logistic regressions analysis was conducted in which associations were consistently found. In the first causal model, we tested the possibility that internalizing symptoms of behavioral problems occurred first in the causal pathway of lung disease and mental health. To obtain a "clean" sample, all children whose mother reported long-term asthma and/or bronchitis at 5 years were excluded. The remaining males and females were categorized according to whether they had internalizing symptoms at 5 years. This variable was considered the "exposure" and asthma at 14 was treated as outcome in these analyses. In the second causal model, we hypothesized that early onset of lung disease may be a precursor of internalizing behaviors at 14 years. The "clean" sample, in this case, excluded those children with internalizing symptoms at 5 years. The remaining participants were categorized into those without and with asthma at 5 years, the "exposure" for the development of internalizing problems at 14 (outcome). Odds ratios were adjusted for those factors available in the dataset and which were considered to be potential confounding factors in these associations: socioeconomic status, marital satisfaction, and maternal mental health. Covariates were taken from measures at 5 years, except from maternal age and level of education, which were only available at the first clinic visit.

	RESULTS

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Of the 7223 original participants, there were 5106 mothers (70.7%) who provided information on both respiratory and behavior problems at 5 years (Table 1).

Asthma and Internalizing Behavior at 5 and 14 Years
For both males and females, there was a tendency for the prevalence of internalizing symptoms to be greater among those children with a report of asthma/bronchitis symptoms than those without (Table 1). At 14 years, 5135 (71.1%) participants provided information on both asthma prevalence and internalizing symptoms.

There were no associations between externalizing symptoms and prevalence of asthma. Like with the 5-year cross-sectional analyses, at age 14, the prevalence of internalizing problems was greater among those with reports of asthma for both males and females (Table 2).

Table 3 shows the association between duration of symptoms of asthma between 5 and 14 years and externalizing and internalizing behaviors. There was no association between externalizing symptoms and prevalence of asthma duration. For males, the prevalence of any internalizing problems increased with the duration of asthma symptoms such that those who had symptoms at both ages 5 and 14 had the highest prevalence; those with no symptoms at either age the lowest prevalence and those who had symptoms at just one age an intermediate prevalence.

From Internalizing Behaviors at 5 to Asthma at 14 Years
Table 4 shows the multivariable associations between internalizing behavior at age 5 and asthma at age 14 among those who were free of symptoms at age 5. These analyses are conducted only on the 1836 males and 1739 females with complete data on all variables included in any of the models. Internalizing symptoms at age 5 were not associated with the development of asthma symptoms at age 14.

From Asthma at 5 to Internalizing Behaviors at 14 Years
In the overall sample (table not presented), those who had asthma/bronchitis at 5 had greater odds of developing internalizing symptoms at 14. Adjusted odds ratios at 14 were 1.38 (95% confidence interval [CI], 0.86–2.03) for the YSR and 1.92 (95% CI, 1.28–2.88) for the CBCL.

Table 5 shows the multivariable associations of asthma/bronchitis at age 5 with internalizing behavior at age 14 among those who were free of internalizing behavior problems at age 5. These analyses are based on 1767 males and 1663 females who had complete data on all variables included in any model in the table. In the YSR, adjusted (baseline age and education, family income, marital status, relationship difficulties at 5) odds ratio of internalizing symptoms at 14 years associated with the presence of asthma/bronchitis at 5 was 1.85 for males and 1.10 for females. In the mothers’ CBCL reports, the adjusted odds ratios of internalizing behavior at age 14 comparing those with asthma/bronchitis at age 5 with those without was 2.12 for males and 1.90 for females. Therefore, based on mothers’ reports, the odds of internalizing behavior tended to be twice that for both females and males with asthma/bronchitis at age 5, whereas based on youth reports, there appeared to be little effects of these problems on internalizing symptoms in females. However, although results are presented by gender, there was no statistical evidence of a sex difference in the association between asthma and internalizing behavior problems in any analyses (p value for interaction with sex = .48 [YSR]; .92 [CBCL]). The associations between asthma and internalizing symptoms remained after adjustment for confounders (Table 5). Sensitivity analysis carried out on each of the three subscales of the internalizing scale (table not presented) suggested that the associations seemed to be primarily a consequence of somatic (adjusted odds ratios 2.24; 95% CI, 1.27–3.97 for the YSR) and anxiety/depression symptoms for males (adjusted odds ratios 2.49; 95% CI, 1.45–4.28 for the YSR) and somatic symptoms for females (2.59; 95% CI, 1.50–4.46 for the CBCL).

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX 1 APPENDIX 2 APPENDIX 3 NOTES REFERENCES

 
Results from this study are consistent with other studies in regard to an association between lung disease in childhood and adolescence and early signs of mental health problems in childhood (8–16). Our findings suggest that there is a greater prevalence of internalizing behavior problems among children and adolescents who have asthma compared with those who have no asthma (9,25). Those with symptoms at both 5 and 14 had the highest prevalence of internalizing symptoms.

Our study adds to the findings of previous work by examining the direction of the association between lung disease and internalizing symptoms to ascertain the temporal sequence of their association. When we examined whether internalizing symptoms at 5 years predicted asthma at 14 years, we found no association among those without asthma/bronchitis at 5 years. However, when we analyzed whether asthma/bronchitis predicted internalizing symptoms at 14, among those with no internalizing symptoms at 5 years, we found that asthmatic male children had an increased odds of developing internalizing symptoms. There was also a tendency in these prospective analyses for an increased odds of internalizing behavioral problems among females with a history of asthma, but these estimates in the YSR were imprecise and did not reach conventional (5%) levels of statistical significance. However, there was no evidence of a significant difference between the effect in males and females or between the effects between using the youth or maternal reports. Taken together, our results are consistent with lung disease being associated with increased odds of internalizing behaviors in both sexes. The causal pathways we examined suggest that asthma symptoms in childhood are more likely to predict emotional difficulties in adolescence than are early emotional difficulties to predict symptoms of asthma. This supports the need for internalizing behavior to be further explored in clinical studies of asthmatic children, because the association of asthma and internalizing problems is likely to be driven by the occurrence of asthma and not vice versa (12,24,25). Unlike others, we did not find that socioeconomic position, relationship difficulties, and maternal psychiatric disorders substantially confounded the association between asthma and internalizing behavior, with little attenuation in the effect with adjustment for these characteristics in our study (10,13,21). This may be the result of the fact that measures of socioeconomic status, marital satisfaction, and maternal mental health were only available at age 5 in our study and changes may occur in these domains over the course of 9 years. However, adjustment for these confounders did not substantially alter the nature of the association; therefore, even if further information was available on these factors between the ages of 5 and 14, it is unlikely that they would alter the study conclusion.

In interpreting the findings of this study, a number of limitations should be considered. First, the definition of asthma relied on maternal reports of the presence of asthma; these reports do not constitute a clinical diagnosis. A medical diagnosis of usually made over time and is based on history, physical examination, and respiratory function measures (33). This may have led to a misclassification of our cases. Despite this limitation, it is worth noting that the asthma prevalence in our sample is comparable to that reported in Australian children of that age by international studies on asthma conducted during the same timeframe of this data collection (34).

Also, our findings may be biased by attrition. Analysis of baseline data were carried out to examine differences in the sample among those lost or kept at follow up. Analysis of attrition at both 5 and 14 years shows that mothers lost to follow up were more likely to have lower family income and educational status at the first clinic visit, to have greater relationship difficulties, and poorer mental health. Our results would only be biased if the associations were absent or in the opposite direction among nonresponders.

Finally, two concerns have been raised about the interpretation of differences in the CBCL between healthy and chronically ill children. First, there is concern about the heavy reliance on maternal reports and the evidence that the presence of the illness itself affects the maternal report (9). In our study, for the main prospective analyses with behavioral outcomes at age 14, we have undertaken to address these issues by using both maternal and children’s self-reports at age 14 (children at age 5 are too young to self-report). Second, there are concerns about the items relating to the "somatic complaints" subscale (35). The issue here is that the somatic subscale aims to distinguish between physical symptoms that have a largely psychologic origin and those that have a largely physical origin. It is not clear that respondents are able to make this distinction or that this distinction reflects "real" differences that exist. In this study, any specific associations with the somatic subscale may be as a direct result of the physical nature of the asthmatic condition and/or its treatment or may reflect psychologic symptoms resulting from the condition. In any event, the internal reliability of the scale remains unaffected. The association that we also found in the prospective analyses between asthma/bronchitis at age 5 and depressive and anxiety symptoms at age 14 (in males) suggests that asthma may be causally related to future psychologic symptoms.

Despite these limitations, this study has the strength of being longitudinal in nature and one of the few studies to prospectively examine the direction of the asthma/internalizing symptoms relationship from childhood to adolescence, taking into account a number of important potential confounding factors. Our findings should then be seen as preliminary evidence and will need replications using other longitudinal data with clinical assessments of both asthma and symptoms of mental health problems and in addition large numbers with sufficient power to determine whether there is a true sex difference in any associations.

In conclusion, children who have symptoms of asthma and bronchitis by the time they are 5 years of age are at greatest risk of developing internalizing symptoms in adolescence. If these findings are replicated in other large prospective studies, clinicians should be encouraged to assess early symptoms of behavior in asthmatic children and provide referrals to appropriate services when necessary.

We are grateful to all participants in the study. We also acknowledge the contribution of the numerous research staff who helped collect the data over the years. Greg Shuttlewood, University of Queensland helped with data management for the study.

	APPENDIX 1

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX 1 APPENDIX 2 APPENDIX 3 NOTES REFERENCES

 

	APPENDIX 2

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX 1 APPENDIX 2 APPENDIX 3 NOTES REFERENCES

	APPENDIX 3

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX 1 APPENDIX 2 APPENDIX 3 NOTES REFERENCES

	NOTES

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX 1 APPENDIX 2 APPENDIX 3 NOTES REFERENCES

 

The core study is funded by the National Health and Medical Research Council of Australia (NHMRC). R. Alati is funded by an Australian NHMRC postdoctoral Public Health Fellowship. D. A. Lawlor is funded by a UK Department of Health Career Scientist Award. The views expressed in this publication are those of the authors and not necessarily those of any funding body.

DOI:10.1097/01.psy.0000161524.37575.42

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