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Psychosomatics 45:93-99, April 2004
© 2004 The Academy of Psychosomatic Medicine

Special Article

Comorbidity of Asthma and Anxiety and Depression in Puerto Rican Children

Alexander N. Ortega, Ph.D., Elizabeth L. McQuaid, Ph.D., Glorisa Canino, Ph.D., Renee D. Goodwin, Ph.D., and Gregory K. Fritz, M.D.

Presented in part at a conference on Critical Research Issues in Latino Mental Health, Princeton, N.J., Nov. 9, 2002. Received July 30, 2002; revision received May 7, 2003; accepted May 17, 2003. From the Division of Health Behavior and Health Promotion, Ohio State University School of Public Health; the Department of Psychiatry and Human Behavior, Rhode Island Hospital, Brown University Medical School, Providence, R.I.; the Behavioral Sciences Research Institute, University of Puerto Rico Medical Sciences Campus, San Juan, Puerto Rico; and the Department of Epidemiology, Mailman School of Public Health, Columbia University, New York. Address reprint requests to Dr. Ortega, Ohio State University School of Public Health, B-209 Starling Loving Hall, 320 West 10th Ave., Columbus, OH 43210; aortega{at}sph.osu.edu (e-mail).


  ABSTRACT

 
TOP
 ABSTRACT
INTRODUCTION
 METHOD
 RESULTS
 DISCUSSION
 REFERENCES
 
Studies have reported that childhood asthma is associated with internalizing disorders, but most of these studies have used global measures of depressive and anxiety symptoms. The Diagnostic Interview Schedule for Children was administered to a group of 1,891 youth ages 4 to 17 and their caregivers in Puerto Rico to determine DSM-IV symptoms and diagnoses. Asthma diagnosis and having had an asthma attack were assessed by parental report. A diagnosis of asthma was associated with having any depressive disorder and one symptom of separation anxiety. An asthma attack was associated with any depressive disorder and any anxiety disorder and, more specifically, with separation anxiety disorder, major depressive disorder, and symptoms of depression, separation anxiety, and generalized anxiety. Possible explanations for the findings are discussed.


  INTRODUCTION

 
TOP
 ABSTRACT
 INTRODUCTION
METHOD
 RESULTS
 DISCUSSION
 REFERENCES
 
Asthma is the most prevalent chronic condition among children in the United States. Statistics show that asthma has a particularly high prevalence in Latino and black children.1–3 Recent data have demonstrated that Puerto Rican island children have a significantly higher prevalence of asthma, relative to other groups of children.4,5 Moreover, studies have consistently shown that Puerto Rican children, both on the U.S. mainland and in Puerto Rico, have an especially high prevalence of parental-reported asthma diagnoses, relative to other minority children.4,6,7 The burden of asthma is also substantial in this population. For example, a recent U.S. mainland study of children with asthma in managed Medicaid found that Latino children had scores similar to those of white children on the American Academy of Pediatrics Children's Health Survey for Asthma, but Latino children had more school days missed and, more important, scored worse on the parent's global assessment for severity.8 Among the Latino children in the Medicaid sample, Puerto Rican children had worse Academy of Pediatrics asthma emotional and activity scores.8 Thus, research focusing on Puerto Rican children is critical, given the disproportionate burden of asthma in this population.

Over the past few decades, several studies have suggested that childhood asthma is related to higher rates of symptoms of depression and anxiety.9 Clinically based studies have documented associations between childhood asthma and internalizing symptoms.4,10–14 A recent meta-analysis using 26 different studies demonstrated a modest but consistent association between asthma and global internalizing symptoms in children.15 Results from a large U.S. multisite epidemiological study of childhood psychiatric disorders indicated that childhood asthma was specifically associated with anxiety disorder,4 and those results were supported by a French study of children.16

Despite the consistency of results to date, previous studies of childhood asthma and psychiatric disorders have been limited in a variety of ways. Specifically, with the exception of one study,4 previous findings have used clinically based samples. Additionally, some studies have used samples of children with only mild to moderate asthma17 or samples that had large proportions of children with severe asthma.14 Therefore, it is unclear whether the associations between internalizing symptoms and asthma are generalizable to youth in the community. Furthermore, many studies have used behavioral scales that do not sufficiently differentiate between symptoms of anxiety and depression and do not assess specific psychiatric disorders.13,15,18 Since psychiatric diagnoses are a key indicator of clinical significance and treatment need, this information is critical from both a clinical and epidemiological perspective.

The present study examines the relationships between asthma and specific anxiety and depressive disorders using a comprehensive structured diagnostic instrument based on the DSM-IV.19 In our previous work, parental reports of psychiatric disorders and asthma were examined in a probability sample of 1,891 children from the U.S. Commonwealth of Puerto Rico.5 In the current study, we extend the previous analyses by examining the relationships between parental reports of asthma diagnoses and attacks and the symptom levels of the internalizing disorders of anxiety and depression. These associations are examined in an attempt to provide greater clarity on the specific relationships between asthma and psychiatric symptoms.


  METHOD

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
RESULTS
 DISCUSSION
 REFERENCES
 
Approval of the study protocol was obtained by the institutional review board of the University of Puerto Rico, Medical Sciences Campus. Assent was obtained from the children, ages 6 to 10. Children 11 years and older were asked to sign their consent on the parent/primary caretaker consent form.

The methods used in this study have been fully described in a separate report.5 In brief, the study involves a two-wave survey of two separate samples of children, a sample of children from the community and a sample of children who had used mental health services. In this article, we present data from the community sample. The community sample is an island-wide household probability sample of children ages 4 to 17 years (in 1998) living in the U.S. Commonwealth of Puerto Rico. After enumerating 6,857 households, 2,102 were found eligible, and of these, 1,891 children and caregivers were interviewed, resulting in a 90.4% response rate.

Measures
Survey information was collected through direct interview with children and adolescents and their primary caregivers (over 90% of the caregivers were mothers). Descriptor variables included maternal education (less than high school, high school or equivalent, or at least some college), yearly family income (<$12,000, $12,000–$25,000, and >=$25,001), and zone of residence (urban or rural).

The Diagnostic Interview Schedule for Children was administered to both the children and the caregivers. A previous report investigated parental reports of asthma and parental reports of psychiatric disorders with the Diagnostic Interview Schedule for Children.5 In this study, we present not only the rates of disorders in the last year but also associated symptoms by using a composite measure of youth and primary caregiver reports. The Diagnostic Interview Schedule for Children, a reliable, respondent-based instrument that is widely used in epidemiological surveys and clinical settings, provides diagnostic data on both psychiatric disorders and symptoms.20,21 The Diagnostic Interview Schedule for Children is the only diagnostic instrument based on the standard psychiatric nosology that has been translated into Spanish by an international team of Hispanic bilingual investigators.22 The Spanish version of the Diagnostic Interview Schedule for Children used in the current study has been shown to have good test-retest reliability for most disorders.20

The anxiety disorders from the Diagnostic Interview Schedule for Children DSM-IV examined included panic disorder, separation anxiety disorder, social phobia, posttraumatic stress disorder (PTSD), and generalized anxiety disorder. The Diagnostic Interview Schedule for Children DSM-IV depressive disorders examined were major depressive disorder and dysthymic disorder. Two global diagnostic categories, one for anxiety and another for depression, were developed. These categories were constructed by collapsing all specific diagnoses with common clinical characteristics, e.g., major depressive episode and dysthymia, into the category of "any depressive disorder" and the previous specific anxiety disorders into the category of "any anxiety disorder." All relevant depressive symptoms of the key disorders were assessed (e.g., depressed or irritable mood, anhedonia). Because the literature indicates that broad anxiety symptoms and issues of parent-child interaction might be most relevant for this population, we chose only to investigate symptoms of separation anxiety (e.g., distress when separated) and generalized anxiety disorder (e.g., restlessness or feeling "on the edge"). Asthma indicators included parental reports of an asthma diagnosis made by a physician and parental reports of the child ever having an asthma attack.

Data Analysis
All analyses were weighted to account for the stratified feature of the sampling design.5 To account for the sampling weights, all analyses were conducted using SUDAAN software.23 SUDAAN allows for the estimates and variances to be calculated with adjustment for complicated sampling designs. Chi-square analyses were conducted to determine the general associations between having had an asthma diagnosis and ever having had an asthma attack and the psychiatric disorders and symptoms just listed. Frequencies are reported, along with weighted percentages. Testing for statistical significance was at the alpha 0.05 level.


  RESULTS

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
 RESULTS
DISCUSSION
 REFERENCES
 
Six hundred twelve (32%) subjects had parental reports of an asthma diagnosis, and 416 (22%) had a lifetime report of asthma attack. For the demographic variables, no associations were found for parental reports of asthma diagnosis. Two associations were found for parental reports of asthma attacks. Family income and zone of residence were associated with having had an asthma attack. Of the children who had histories of asthma attacks, 81% resided in urban areas, and 19% resided in rural areas. The urbanicity finding is consistent with studies from several European countries that have consistently found lower rates of atopy among youth living in rural rather than nonrural environments.24,25 Furthermore, of those subjects who had parental reports of asthma attacks, 39% lived in families with annual incomes of <$12,000, 29% with incomes of $12,000 to $25,000, and 32% with incomes >=$25,001.

We ran chi-square analyses to determine the relationships between having a parental report of child asthma diagnosis and specific and higher-rank anxiety and depressive disorders, and separation anxiety disorder and generalized anxiety disorder symptoms. A larger percentage of children with parental reports of an asthma diagnosis had any depressive disorder (5.6%) than those who did not have a diagnosis (2.4%) ({chi}2=4.04, df=1, p=0.04). No other significant associations were found for any of the other disorders examined. Although we did not find any associations for the depressive symptoms or for separation anxiety disorder, we found that "physical symptoms when separated" was associated with parental reports of child asthma diagnosis (21%) versus (15%) for those without a diagnosis ({chi}2=5.13, df=1, p=0.02).

Table 1 shows the results for the relationships between lifetime asthma attacks and anxiety and depressive disorders, and symptoms of generalized anxiety disorder and separation anxiety disorder. Our results show that children with a history of asthma attacks, compared with children who had never experienced these attacks, had higher prevalence rates of any depressive and any anxiety disorder, as well as major depressive disorder and separation anxiety disorder. When we analyzed the symptoms associated with major depressive disorder and dysthymic disorder, we found that compared with children who had never had an asthma attack, those who had attacks were more likely to have a depressed or irritable mood, diminished interest, fatigue, or loss of energy, weight gain or loss, and problems concentrating. Children with a history of asthma attacks also were more likely to have physical symptoms when separated and tended to refuse to sleep alone, relative to the children with no such history. For the generalized anxiety symptoms, there were more children who had difficulty concentrating and fatigue in the group that had ever had an asthma attack versus the group that had never had an asthma attack.


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TABLE 1. Relation Between Asthma Attacks and Affective and Anxiety Disorders and Symptoms in Puerto Rican Children




  DISCUSSION

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
 RESULTS
 DISCUSSION
REFERENCES
 
Many studies, including our previous work, have focused on associations between psychiatric disorders and asthma. To our knowledge, the current study is the first to examine the relationships between parental reports of asthma diagnosis and attacks and specific internalizing symptoms of anxiety and depression, as well as childhood DSM-IV diagnoses of anxiety and depressive disorders in a population-based epidemiological sample. Parental reports of asthma were associated with having any depressive disorder and with some symptoms of separation anxiety. Parental reports of child asthma attacks were linked with both depressive and anxiety disorders and some symptoms of generalized anxiety disorder and separation anxiety disorder.

These findings are consistent with previous clinical studies. For instance, Slattery et al.26 reported an association between parent-reported atopic disorders and separation anxiety disorder among youth in a clinical sample. The lack of association between social phobia and asthma in this sample, however, is somewhat inconsistent with previous reports from Kagan et al.27 and Bell et al.,28 who have documented associations between atopy and behavioral inhibition in clinical and community samples of youth. Although behavioral inhibition is linked to internalizing symptoms and disorders, the two are not synonymous, which may explain the difference in findings. Furthermore, the current study measured parental reports of asthma, not the more global index of atopy, which may account for some difference in the findings.

To date, there has been more evidence suggesting an association between asthma and anxiety disorders, compared with depressive disorders, among youth.4,16 The associations between specific anxiety disorders and asthma, however, have been largely uninvestigated because of the dependence of previous studies on clinical, high-risk samples and the use of instruments that do not sufficiently distinguish DSM-IV disorders. Our analyses suggest that parental reports of an asthma diagnosis are associated with having a depressive disorder and that having had an asthma attack is associated with separation anxiety, in addition to depression and internalizing symptoms. While the associations between asthma and panic disorder were not significant, associations between asthma and a greater risk of panic attacks have been shown among youth and among adults in the community.29 It is possible that the low base rate of cases of panic disorder contributed to the lack of an observed effect in this sample.

Why would children with a lifetime history of asthma attacks be more likely to have symptoms of separation anxiety, such as physical distress when separated, than children with no history of asthma attacks? One explanation may come from previous clinical notions of the relationship between asthma and separation anxiety that posit that parent-child attachment is related to respiratory problems.30–32 It is possible that having had an asthma attack changes children's comfort threshold for being away from their parents. It could also be that for children with severe asthma, the fear of being hospitalized could contribute to more severe symptoms of separation anxiety disorder.

The lack of significant associations between asthma and PTSD should be noted, since high rates of asthma were found in a clinical study of adolescent inpatients with PTSD33 and an association has been found between other respiratory illnesses and PTSD, early childhood abuse, and the comorbidity of respiratory illness and internalizing disorders in adults in the community.34 It is likely that the lack of a relationship in this sample was due to the low prevalence of posttraumatic stress. It is also possible that the association does not appear until later in life since it has been observed in older samples.

Some researchers have speculated that there may be some confusion among clinicians, parents, and researchers over differentiating childhood psychiatric and physiological symptoms, such as breathlessness.5 Such confusion could contribute to possible confounding and bias in the observation of asthma and anxiety. The symptoms (e.g., dyspnea) of asthma, panic attack, and separation anxiety are similar, thus making disease classification by symptom reporting difficult. It may also be that there are communication problems between parents and providers over the asthma diagnosis. For example, a study of Philadelphia schoolchildren found that minority children were more likely to be diagnosed with asthma than white children, despite the children sharing similar symptom profiles.35,36

Findings from the current study suggest that the mechanisms explaining asthma and mental illness are multiple and likely complex. Children may fear the exacerbation of asthma symptoms, causing them to be anxious and fearful of separation from attachment figures. They may also experience distress by internalizing the burden of asthma.14,32,37 Some researchers have raised suggestions that the association between asthma and psychiatric disorders is modified by the severity of asthma,5,38,39 which may explain the association between asthma attacks and anxiety and depressive disorders and symptoms. However, some studies have also observed psychiatric disorders in children with low to mild asthma.5,40 Alternatively, it may be that there are cross-cultural differences in the interpretation of the phrase "asthma attack" ("un ataque de asma" in Spanish). An attack may be perceived as a severe exacerbation. The mental health literature has also documented a condition that appears to be culturally bound to Caribbean Latinos—in particular, Puerto Ricans—called "ataques de nervios."41–45 This syndrome has been defined as an idiom of distress, which is commonly reported with symptoms of screaming uncontrollably, attacks of crying, trembling, and feelings of being out of control.19 Although "ataques de nervios" have not been documented in children and adolescents to date, it is possible that children with asthma attacks, as well as children with ataques de nervios, share the common feeling of being out of control. Thus, it may be that responding affirmatively to whether the child had an ataque may imply a severe exacerbation of an asthma symptom. Since we do not have a detailed definition of what defines an attack, interpretation of this question is somewhat subjective. Future work should address the differential diagnosis of psychiatric symptoms and respiratory distress in order to ensure that appropriate intervention is used.

Finally, it is possible that the co-occurrence of asthma and internalizing disorders is related to a common third factor that is associated with a higher risk of both asthma and depressive and anxiety disorders. Genetic associations between mental health and atopy (which is linked to asthma) have been found in the literature.26,46 It is also possible that a common environmental stressor, such as low socioeconomic status or early trauma (e.g., childhood abuse), both of which are independently associated with asthma/respiratory disease and internalizing disorders, mediates the relation. It has been suggested that such early adverse experiences may influence the development of immune function, thereby increasing vulnerability to both asthma and depressive disorders, although the precise mechanisms involved in this hypothesized link have yet to be identified. Future studies may be useful in untangling these possible influences on the association between asthma and internalizing disorders.

Limitations
First, while the study made use of a community, population-based sample, it consisted only of children from Puerto Rico. Thus, our findings may not be generalizable to other groups of children on the U.S. mainland. Second, because the original survey did not intend to assess specifically the relationship between asthma and mental health, we were limited to rather simple asthma measures that were based on parental reports and did not include medical chart verification or classification of asthma severity. Third, the reports of asthma were lifetime, whereas the assessments for the psychiatric disorders were for 12 months. This discrepancy in reporting periods could have an impact on findings, particularly given the episodic nature of asthma. As in any observational study, there might be other residual factors (e.g., diagnostic biases) that could account for the observed associations. Future studies should attempt to delineate the multiple factors (e.g., psychosocial, cognitive) that could explain the findings.

Implications
The results of this population-based study of Puerto Rican children showed that having an asthma diagnosis was associated with any depressive disorder and with one specific symptom of separation anxiety. Having had an asthma attack, however, was associated with meeting criteria for any depressive disorder and any anxiety disorder, as well as for the specific diagnostic categories of separation anxiety disorder and major depressive disorder and was associated with some symptoms of depression, separation anxiety, and generalized anxiety. Future studies should consider disentangling diagnostic and reporting issues such as symptom perceptions, patient-provider communication regarding diagnosis, and distinguishing anxiety from asthma symptoms (e.g., dyspnea). Possible misdiagnosis of either asthma or anxiety could be the result of confusion over physiological versus psychiatric symptoms (i.e., symptoms of separation anxiety or panic attack), such as breathlessness. Relying on parental reports in both the clinical and research setting could lead to potential diagnostic biases. Moreover, pediatricians should be mindful of the potential comorbidity of internalizing disorders and asthma in children with severe asthma. Given consistent data suggesting mental health concerns associated with asthma and respiratory disease among adults, including major depression, panic attacks, and a greater prevalence of suicide attempts, consideration of the potential for preventive intervention, both in terms of physical and mental health consequences of childhood-onset asthma later in life should be considered when planning services for youth with asthma.


  ACKNOWLEDGMENTS

 
Supported in part by NIMH grants MH-54827 and MH-59876 (the Latino Research Program Project).

The authors thank Dr. Rafael Ramirez and Mr. Pedro Garcia for help in the analysis of data and Dr. Peter Guarnaccia and Mr. Onell Calderas for comments on an early draft of the article.


  REFERENCES

 
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 INTRODUCTION
 METHOD
 RESULTS
 DISCUSSION
 REFERENCES
 

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