Parent-child interactions in children with asthma and anxiety

Behaviour Research and Therapy 97 (2017) 242e251

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Parent-child interactions in children with asthma and anxiety Gemma Sicouri a, Louise Sharpe a, Jennifer L. Hudson b, Joanne Dudeney a, Adam Jaffe c, d, Hiran Selvadurai e, f, Caroline Hunt a, * a

School of Psychology, The University of Sydney, NSW, Australia Department of Psychology, Macquarie University, NSW, Australia c Discipline of Paediatrics, School of Women's and Children's Health, Medicine, University of New South Wales, NSW, Australia d Department of Paediatric Respiratory Medicine, Sydney Children's Hospital, Randwick, NSW, Australia e The Children's Hospital at Westmead Clinical School, Discipline of Paediatrics and Child Health, Faculty of Medicine, University of Sydney, NSW, Australia f Department of Respiratory Medicine, The Children's Hospital at Westmead, Westmead, NSW, Australia b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 1 March 2017 Received in revised form 18 July 2017 Accepted 21 August 2017

Anxiety disorders are highly prevalent in children with asthma yet very little is known about the parenting factors that may underlie this relationship. The aim of the current study was to examine observed parenting behaviours e involvement and negativity - associated with asthma and anxiety in children using the tangram task and the Five Minute Speech Sample (FMSS). Eighty-nine parent-child dyads were included across four groups of children (8e13 years old): asthma and anxiety, anxiety only, asthma only and healthy controls. Overall, results from both tasks showed that parenting behaviours of children with and without asthma did not differ significantly. Results from a subcomponent of the FMSS indicated that parents of children with asthma were more overprotective, or self-sacrificing, or nonobjective than parents of children without asthma, and this difference was greater in the non-anxious groups. The results suggest that some parenting strategies developed for parents of children with anxiety may be useful for parents of children with asthma and anxiety (e.g. strategies targeting involvement), however, others may not be necessary (e.g. those targeting negativity). © 2017 Elsevier Ltd. All rights reserved.

Keywords: Anxiety disorders Asthma Parenting Children

Asthma is the most common chronic illness of childhood, with a prevalence of 9.5% (Akinbami et al., 2012). It is a serious respiratory disease, characterized by a reversible inflammatory condition of airways, with symptoms including coughing, wheezing and difficulty breathing. Children with asthma have been shown to be at increased risk of internalizing disorders, such as anxiety and depression (Lu et al., 2012; Pinquart & Shen, 2011). A recent metaanalysis found that approximately 1 in 5 children have been found to have an anxiety disorder (Dudeney, Sharpe, Jaffe, Jones, & Hunt, 2017; Katon et al., 2007), which is three times as high as the prevalence of anxiety disorders in healthy children (Lawrence et al., 2015). Compared to children with asthma and no anxiety, children with comorbid asthma and anxiety experience increased asthma symptom burden (Richardson et al., 2006), reduced physical and emotional functioning (McCauley, Katon, Russo, Richardson, & Lozano, 2007), greater use of health services (Fernandes et al.,

* Corresponding author. School of Psychology, M02F Mallet Street Campus, The University of Sydney, NSW 2006, Australia. E-mail address: [email protected] (C. Hunt). http://dx.doi.org/10.1016/j.brat.2017.08.010 0005-7967/© 2017 Elsevier Ltd. All rights reserved.

2010) and have a greater risk of being a smoker as an adolescent (Bush et al., 2007). Yet, despite the evidence of the high comorbidity and serious consequences of childhood asthma and anxiety, very little is known about the parenting factors that might underlie the association. This is particularly relevant for treatment because research shows that children with asthma and anxiety do not respond as well to cognitive behavioural interventions developed for healthy children with anxiety (Papneja & Manassis, 2006), and tend not to include parents in treatment (Marriage & Henderson, 2012). As such, it is crucial that research determines whether parenting behaviours are associated with anxiety disorders in children with asthma, and whether these behaviours are the same or different in healthy children with anxiety. If different, anxiety-focused interventions which include parents may be targeting the wrong parenting processes if delivered to children with asthma. Theories of childhood anxiety posit that parenting characterized by overinvolvement (overprotection/control) and negativity (rejection/criticism) are associated with anxious symptomatology in children (Chorpita & Barlow, 1998; Craske, 1999; Dadds & Roth,

G. Sicouri et al. / Behaviour Research and Therapy 97 (2017) 242e251

2001; Manassis & Bradley, 1994; Rapee, 1997, 2012). An overinvolved parenting style is hypothesized to reinforce the child's vulnerability to anxiety by increasing the child's perception of threat by reducing the child's perceived control over their environment and supporting the child's avoidance of threat. Parental negativity is hypothesized to adversely affect the child's selfesteem and integrity, as well as undermine the child's emotional regulation (Gottman, Katz, & Hooven, 1997), which may put children at increased risk for developing anxiety problems. Empirical research has provided broad support for the association between parental overinvolvement and childhood anxiety disorders, although results have been somewhat less consistent regarding the relationship between parental negativity and childhood anxiety (Bogels & Brechman-Toussaint, 2006; McLeod, Wood, & Weisz, 2007, 2011). It is possible that similar parenting styles are associated with anxiety in children with asthma. Whilst family and parenting factors have been highlighted as important for influencing childhood asthma outcomes (Kaugars, Klinnert, & Bender, 2004; Minuchin et al., 1975; Mrazek, Klinnert, Mrazek, & Macey, 1991, 1996; Wood et al., 2006; 2007), to date there has been limited empirical research investigating specific parenting styles associated with childhood asthma and anxiety. What parenting styles might be expected for parents of children with asthma? Similar to other chronic illnesses, asthma requires intensive medical management, and, as a result, places considerable demands on parents or caregivers involved in caring for their child (Frankel & Wamboldt, 1998; Kaugars et al., 2004; Morawska, Stelzer, & Burgess, 2008). Parents may respond by being protective of their child, in an attempt to maintain the health of their child and regulate their own exposure to stress. Such parental protection or involvement could be seen as an understandable and natural response to managing a child with a chronic illness. However, excessive overprotective parenting may not be helpful, and what begins as well intentioned parental helping may inadvertently be transformed as there is a tension between conflicting responsibilities: the responsibility to ensure the child remains healthy and adheres to medical treatment versus the responsibility to facilitate the child's independence and selfmanagement (Anderson & Coyne, 1991, 1993; Coyne, Wortman, & Lehman, 1988; Holmbeck et al., 2002). Parents of children with asthma may also have to manage a number of potentially difficult interactions with the child several times a day (Calam et al., 2003) primarily around adherence to the child's medication regime, and parents' may develop a more involved or negative/critical parenting style in response to these interactions. In addition, parents (primarily mothers) of children with asthma experience higher levels of anxious symptoms compared to parents of children without asthma (Easter, Sharpe, & Hunt, 2015), which may exacerbate an overinvolved and negative parenting style, as has been proposed in the child anxiety literature (Ginsburg & Schlossberg, 2002; Ginsburg, Grover, Cord, & lalongo, 2006; Hudson & Rapee, 2002; Rapee, 2001; Whaley, Pinto, & Sigman, 1999). Early empirical research supports the notion that parents of children with asthma are more overinvolved and negative compared to parents of children without asthma (Block, Harvey, & Jennings, 1966; Byrne & Murrell, 1977; Hermanns et al., 1989; Schobinger et al., 1992, 1993). However, the majority of this research relied on retrospective or self-report measures of parenting which may be limited by providing information on perceived rather than actual childhood practices. Three studies that used a direct observation measure e the Five Minute Speech Task found that parents of children with asthma (aged 6e13 years old) were more negative and critical compared to mothers of children without asthma (Hermanns et al., 1989; Schobinger et al., 1992, 1993), and that increased frequency of asthma attacks and

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asthma severity were associated with mothers' critical attitudes but not with fathers’ (Hermanns et al., 1989). However, this research did not differentiate between the parenting styles of parents of children with asthma and parents of children with comorbid asthma and anxiety. Therefore, the parenting styles associated with anxiety in children with asthma remains unclear. Psychological disorders, including anxiety, are highly prevalent in children with chronic illnesses other than asthma (for example, diabetes, epilepsy, spina bifida) (Pinquart & Shen, 2011). Relatedly, a handful of studies have sought to demonstrate that parenting is associated with child psychological outcomes in the context of childhood chronic illness, rather than asthma specifically (Anderson & Coyne, 1991, 1993; Holmbeck et al., 2002; Ong, Nolan, Irvine, & Kovacs, 2011). This research is consistent with the argument that parenting styles are a factor associated with anxiety for children with asthma. For example, Holmbeck et al. (2002) tested a meditational model of associations between parental overprotectiveness, behavioural autonomy and psychosocial adjustment in families with 8 and 9-year-old children with spina bifida compared a healthy control group. They found that parents of children with spina bifida were significantly more overprotective than parents of children without spina bifida, and that parental overprotectiveness (measured by a self-report questionnaire) was associated with less behavioural autonomy in children, which in turn was associated with more internalizing problems (depression), in these children. Whether these results generalise to children with asthma, or children with other chronic illnesses, remains to be investigated. The aim of the current study was to investigate the association between parenting styles as they relate to child asthma and anxiety status. This study examined parental overinvolvement and negativity using two direct observation measures, namely the tangram task and a Five Minute Speech Sample (FMSS). Four groups were compared: children with asthma and a comorbid anxiety disorder (“asthma and anxiety”), children with anxiety disorders only (“anxiety only”), children with asthma only (“asthma only”) and healthy control children (i.e. with no asthma or an anxiety disorder). Children between the ages of 8 and 13 years old were included as the parenting behaviours of interest were considered more likely to be present during this developmental period and the direct observation measures were designed and validated for this age group (Hudson & Rapee, 2001; Gar & Hudson, 2008). It was hypothesized that parents of children with asthma would display greater overinvolvement and negativity compared to parents of children without asthma, and this difference would be greater for the non-anxious groups compared to the anxious groups (i.e. there would be an interaction effect). Consistent with previous research, it was also hypothesed was that parents of children with anxiety would display greater levels of parental overinvolvement and negativity compared to children without anxiety, regardless of the child's asthma status. 1. Method 1.1. Participants Participants were children and one their parents (“dyads”). Children were included in the study if they were aged between 8 and 13 years old. Inclusion criteria for children in the asthma groups was a diagnosis of asthma from a respiratory physician, no comorbid respiratory conditions, and the asthma was monitored by optimal and stable respiratory medications. Inclusion criteria for participants in the anxiety groups was a diagnosis of an anxiety disorder. Inclusion criteria for the control group included never being diagnosed with asthma nor any other chronic health

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condition, not meeting criteria for a diagnosis of any anxiety disorder, and falling below a clinical cut-off point on self-/parentreport measures of anxiety. Exclusion criteria for the whole sample included participation in a psychological treatment for anxiety in the past 12 months, hospitalization for asthma in the past month, a lack of English literacy, a condition that would hinder their participation, such as traumatic brain injury. Participants were recruited from the community via advertisements in print and online media and through one independent school in Sydney, Australia. Children with anxiety were offered free CBT treatment at the University of Sydney, Australia. Eighty-five percent of people who contacted us with interest in the project, ultimately took part. Participants with asthma were additionally recruited through the Sydney Children's Hospitals Network. The recruitment rate for participants recruited through the Sydney Children's Hospitals Network was 24%.

2. Measures 2.1. Demographic information Parents completed a demographic questionnaire that included questions about the child's age, gender, chronic illnesses, parental occupation and education level. A SES score was calculated based on parents' occupation and education level as per the method described by Hollingshead (1975) (Hollingshead, 1975). A SES score from 8 to 66 was based on reported parental education level and occupation, with higher scores indicating higher SES.

2.2. Child anxiety diagnosis All children were assessed for an anxiety disorder by registered psychologists using the Anxiety Disorders Interview Schedule-IV Child and Parent Version (ADIS C/P; Silverman & Albano, 1996). The ADIS: C/P is a semi-structured clinical interview and is suitable for young people aged 6 years and above. It has demonstrated good psychometric properties (March & Albano, 1998), with high interrater reliability (Chavira, Stein, Bailey, & Stein, 2004) and testretest reliability (Silverman, Saavedra, & Pina, 2001). Diagnoses and clinical severity ratings (CSRs; on a scale of 0e8 whereby ratings above 4 indicate clinically impairing symptoms) were assigned based on a composite parent and child report. Twenty percent (n ¼ 18) of the ADIS C/P interviews were audiotaped and coded by a different registered psychologist trained in scoring the ADIS. Interrater reliability was excellent (k ¼ 1.0 for the presence of an anxiety diagnosis; ¼ .95 for the primary diagnosis). Disagreements were resolved by consensus. Assessments were conducted under the supervision of a senior clinical psychologist (CH).

2.3. Child anxiety symptoms To support the distinction between the anxious and nonanxious groups, child anxiety symptoms were measured using the Spence Child Anxiety Scale eParent and Child Report (SCAS-P; Nauta et al., 2004; SCAS-C; Spence, 1998). The SCAS-C and SCAS-P contain 38 anxiety items that all load on a single higher order scale (scores range from 0 to 114) measuring anxiety symptoms. The scale has shown to significantly differentiate between clinically anxious and non-anxious children and has demonstrated good internal consistency and test-retest reliability (Nauta et al., 2004; Spence, 1998). The internal consistency for the current sample was a ¼ .88 and a ¼ .90 for the SCAS-C and the SCAS-P respectively.

2.4. Asthma symptom control Asthma symptom control was assessed using the Asthma Therapy Assessment Questionnaire (Skinner et al., 2004), a parentcompleted questionnaire for children and adolescents (5e17 years old). The ATAQ contains questions about asthma symptoms and control over asthma (such as breathing difficulty, wheezing when not exercising, missing school due to asthma) over the past week, with higher scores indicating lower symptom control (range 0e7). The ATAQ has good internal consistency and has been validated against objective measures of asthma and health care utilization (Skinner et al., 2004). The internal consistency for the asthma sample was acceptable (a ¼ .69). 2.5. Asthma quality of life Asthma quality of life was assessed using the Pediatric Asthma Quality of Life Questionnaire (PAQLQ; Juniper et al., 1996). The PAQLQ is an interviewer-administered 23 item scale assessing areas of daily function (physical, emotional, social) that children with asthma report as most troublesome. It is designed for children and adolescents 7e17 and shows good levels of reliability and validity (Juniper et al., 1996). The internal consistency for the total PAQLQ score was a ¼ .96. 2.6. Parent anxiety To measure symptoms of parental anxiety, parents completed the anxiety subscale of the Depression Anxiety Stress Scales e Short Form ((DASS21; Lovibond & Lovibond, 1995). The DASS 21 is a wellestablished 21-item self-report measure and has demonstrated good internal consistency and validity for each of the subscales (Antony, Bieling, Cox, Enns, & Swinson, 1998). The internal consistency for the current sample was a ¼ .85. 2.7. Task 1: tangram task The tangram task consists of a series of puzzles, which involves the child placing geometric pieces together to form larger shapes outlined on a set of templates. The tangram task was designed to be slightly too difficult for the child to complete in a five-minute period. The parent was given the following instructions before the commencement of the task: “This is a test of your child's ability. We want to see how good he/she is at thinking. Mum/Dad, you are going to sit there for support and you will have the answers for interest. Most kids can do it but some find it a bit hard to get going. You can help if you think he/she really needs it.” There were two sets of tangrams, each appropriate for a different age group. A set of three coloured tangrams was given to children between the ages of 8 and 10 years and a set of five black tangrams to children between the ages of 11 and 13 years. The tangram puzzles used in the current study were the same puzzles used in the original study (Hudson & Rapee, 2001). The child's ability to do the tangram task was not important to the study; rather, the parent-child interaction whilst the child was doing the task was of primary interest. The parent was given the answers to the puzzle to ensure that help was not limited by the parent's own skill. Each parent-child interaction was videotaped. Each parent-child interaction was rated on the degree of parental overinvolvement and negativity using the coding manual developed by Hudson and Rapee (2001) (Hudson & Rapee, 2001). The overinvolvement and negativity factors represent two distinct theoretical constructs and empirically tested factors (refer to Hudson & Rapee, 2001). Interactions were coded on nine global scales consisting of an

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eight-point continuum ranging from zero to eight. The involvement factor consisted of the following global scales: (i) the general degree of parental involvement; (ii) the degree of unsolicited help (intrusiveness); (iii) the degree to which the parent physically touched the tangram pieces; (iv) the parent's posture; (v) the parent's focus during the interaction (towards the child or towards the task). To determine the degree of parental involvement, the parent's average score across the five scales was calculated. The involvement factor represents an overall measure of the degree of help the parent gave during the task, with high scores indicating overinvolvement. The negativity factor assessed the degree of parental warmth during the interaction and comprised of the following global scales: i) general mood/atmosphere of the interaction; (ii) parent's degree of positive affect; (iii) parent's tension; (iv) parent's degree of verbal and non-verbal encouragement/criticism. To determine the degree of parental negativity, the parent's average score across the four scales was calculated. High scores on this factor indicated that an interaction was characterized as critical, tense or angry. Coders were clinical psychology trainees who were trained in the coding system until 80% agreement was reached (GS & AK). One coder, blind to the diagnostic status of the child, rated every parentchild interaction (GS). Thirty-two percent (n ¼ 28) of the interactions were chosen at random and scored by a second coder, also blind to the diagnostic status of the child (AK). Inter-rater correlations were calculated using Shrout and Fleiss' (1979) model 2 (Rater's random). Both the Involvement factor and the Warmth factor demonstrated excellent inter-rater reliability, ICC (2,1) ¼ .95, p < .001 and ICC (2,1) ¼ .93, p < .001 respectively. The final scores used were those provided by the coder who scored all of the parent-child interactions.

2.8. Task 2: Five Minute Speech Sample (FMSS) The FMSS is a measure of Expressed Emotion (EE) (Magana et al., 1986). The instructions given to the parent was as follows: “I'd like to hear your thoughts and feelings about (child's name) in your own words and without my interrupting with any questions or comments. When I ask you to begin, I'd like you to speak for 5 min, telling me what kind of person (child's name) is and how the two of you get along together. After you begin to speak, I prefer not to answer any questions until after the five minutes.” The speech samples were audiotaped and transcribed. Two measurements of EE were taken from the FMSS according to the method described by Magana-Amato (1990) (Magana et al., 1986): Emotional Overinvolvement (EOI) and Criticism (CRIT), which were designed to represent parental involvement and negativity. A high EOI score was given based on: (i) the presence of an emotional display (for example, crying); (ii) reports of selfsacrificing, overprotective, or lack of objective statements about the child, or a combination of the two or more of the following: (i) excessive detail about the past; (ii) a statement of love of willingness to do anything for the child; or (iii) exaggerated praise of the child as indicated by five or more positive remarks. Borderline EOI was rated if moderate evidence of the category was found. In acknowledgement of the possible limitations of measuring the overall EOI component in young populations (McCarty & Weisz, 2002), and to be consistent with previous research assessing EOI in young populations (Gar & Hudson, 2008), the approach to scoring EOI was as follows: coders scored the overall EOI component and, although all five subcategories of EOI were coded and analyzed, the two individual scoring criteria (overprotective/selfsacrificing/lack of objectivity and emotional display) found to be

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positively related to maternal reports of child psychopathology (McCarty & Weisz, 2002), were of primary interest in this study. A high CRIT rating was given if any of the following were present: (i) a negative initial statement; (ii) a negative relationship rating; (iii) one or more critical statements; or (iv) the presence of dissatisfaction. Borderline CRIT was rated if moderate evidence of the category was found. Each of the four CRIT criteria has been found to relate positively to maternal reports of child psychopathology (McCarty & Weisz, 2002) overall CRIT component was measured and analyzed. Two coders (GS & AK) were trained by a certified rater (JH) until 90% agreement on the EE subgroups was reached. One coder, who served as the primary coder, scored all of the speech samples, and the second coder coded 26% (n ¼ 23) of the speech samples, which were chosen at random. The coders were unaware of the diagnostic status of the child. In line with the method adopted in previous studies (Hirshfeld, Biederman, Brody, & Faraone, 1997), and suggested by the coding manual when coding for groups that may be reluctant to express strong views about their relatives (e.g. parents of young children), the borderline-CRIT and borderline-EOI cases were included in the high category. Inter-rater agreement rates for the categories were all in the good to excellent range. The kappa values were as follows: CRIT (low versus borderline-high), k ¼ .96; EOI (low-borderline versus high), k ¼ .82; EOI subscales: emotional display, k ¼ 1.0; overprotective/self-sacrificing/lack of objectivity, k ¼ .72. The measures used in the final analyses were those provided by the primary coder.

3. Procedure On the day of the experiment, children and one of their parents completed written consent forms and children under 12 provided assent. Participants undertook the diagnostic interview, which consisted of separate parent and child interviews. Participants were then seated next to each other in a room while the experimenter read aloud the instructions for the tangram task. Following this first task, children left the room and parents completed the FMSS. Following completion of the tasks, families were debriefed about the true nature of the study. The two tasks were given in random order. The procedures in the study formed part of a larger study assessing anxiety in children with asthma and were approved by both the University of Sydney Human Ethics Committee and Sydney Children's Hospitals Network Human Ethics Committee.

4. Statistical analysis All analyses were conducted with SPSS version 22.0. Differences between groups on demographic variables and questionnaire measures were assessed using two-way analysis of variance (ANOVA) with child anxiety status (anxiety present or anxiety absent) and child asthma status (asthma present or asthma absent) as the two independent variables, or chi-squared analysis for categorical variables. For the tangram task, main effects and interaction effects on parental involvement and negativity were investigated using twoway analysis of variance (ANOVA), with child anxiety status (present or anxiety absent) and child asthma status (present or asthma absent) as the independent variables. For the FMSS task, differences between the groups were investigated with chi-square tests as the data was categorical, using a similar approach adopted by Gar and Hudson (2008). The critical alpha was set at p < .01 to avoid inflation of the type 1 error rate.

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5. Results 5.1. Participant characteristics The sample demographic information is shown in Table 1. Participants were 89 children (M ¼ 9.7 years; SD ¼ 1.5) and one of their parents (“dyads”). Children fell in to one of four groups; asthma and anxiety (n ¼ 29), asthma only (n ¼ 15); anxiety only (n ¼ 21); and healthy controls (n ¼ 24). There were no significant differences in child's age, gender, parent's age, ethnicity, family composition and SES between the four groups. The proportion of mothers reported to be the primary caregiver was lower in the healthy control group compared to the other three groups, c2(3, N ¼ 89) ¼ 13.97, p ¼ .003. However, involvement and negativity did not differ between mother and father caregivers, t(87) ¼ 1.69, p ¼ .095 and t(88) ¼ 0.79, p ¼ .434 respectively, and excluding fathers from the main analyses resulted in no differences in the significant results. Thus primary caregiver status was not controlled in the analyses. 5.2. Descriptive measures The primary diagnoses of the children in the anxious groups were: generalised anxiety disorder 46% (n ¼ 23) separation anxiety disorder 22% (n ¼ 11), social phobia 18% (n ¼ 9), and specific phobia 14%, (n ¼ 7). Sixty-four percent (n ¼ 32) of children with anxiety met criteria for at least one additional anxiety disorder and no children met diagnostic criteria for a mood disorder. Sixty-four percent (n ¼ 32) of children with anxiety met criteria for at least one additional anxiety disorder and no children met diagnostic criteria for a mood disorder. The mean scores for the questionnaire measures are shown in Table 2. Differences between the groups on the questionnaire measures were assessed using two-way ANOVA's with child anxiety status (present or absent) and child asthma status (present or absent) as the two independent variables. Child anxiety symptoms

were higher in the anxious groups compared to the non-anxious groups on the SCAS-C, F(1, 85) ¼ 35.95, p < .001, and the SCAS-P, F(1, 85) ¼ 61.81, p < .001, which supported the diagnostic distinction between the groups. There were no significant differences between the asthma groups on asthma symptom control (ATAQ), F(1, 43) ¼ 0.34, p ¼ .854, and asthma quality of life (PAQLQ), F(1, 43) ¼ 1.04, p ¼ .313, respectively and thus the asthma groups were considered similar in terms of disease severity. There were no significant differences between the groups on parent anxiety symptoms (p > .01). 6. Task 1: tangram task 6.1. Preliminary analyses There were no significant relationships between parental overinvolvement and the child's age, (r ¼ .11, n ¼ 89, p ¼ .324), nor between parental negativity and the child's age, (r ¼ .43, n ¼ 89, p ¼ .688). Involvement and negativity did not differ by gender, t(87) ¼ 1.26, p ¼ .210 and t(87) ¼ 1.52, p ¼ .132 respectively. There was a moderate and significant correlation between negativity and involvement (r ¼ .50, p < .001). 6.2. Involvement Table 3 shows the means and standard deviation for involvement across the four groups. There was not a clear significant main effect of asthma status on the level of involvement, F(1, 85) ¼ 3.96, p ¼ .050, h2 ¼ .45, and no significant interaction effect, F(1, 85) ¼ 0.98 p ¼ .325, h2 ¼ .01, which did not support our first hypothesis. A significant main effect was found for child anxiety status, F(1, 85) ¼ 15.41, p < .001, h2 ¼ .15, which supported our second hypothesis. In other words, parents of children with anxiety were more involved than parents of children without anxiety, regardless of the child's asthma status.

Table 1 Demographic Variables Across Groups.

Age in years M (SD) Gender, Male % (n) Ethnicity % (n) Australian/Oceanic Asian European Primary Caregiver % Mothers (n) Age in years, M (SD) Family composition % (n) Married Single/divorced Other Family SES, M (SD) Other physical illnesses % (n) Length of asthma diagnosis in year, M (SD) Frequency of asthma Symptoms % (n) Daily Weekly Every 1e3 months Yearly > Yearly No. of asthma medications Frequency of medication % (n) Every day Intermittent Note. SES ¼ socioeconomic status score.

Asthma & Anxiety (n ¼ 29)

Anxiety Only (n ¼ 21)

Asthma Only (n ¼ 15)

Healthy Control (n ¼ 24)

10.0 (1.5) 59 (17)

9.2 (1.1) 57 (12)

10.1 (1.5) 73 (11)

9.5 (1.5) 58 (14)

76 (22) 7 (2) 4 (1)

86 (18) 10 (2) 5 (1)

80 (12) 7 (1) 0 (0)

92 (22) 4 (1) 0 (0)

93 (27) 43.3 (6.9)

100 (21) 41.9 (4.6)

100 (15) 42.0 (5.5)

71 (17) 44.2 (3.8)

83 (24) 17 (5) 0 (0) 42.9 (16.3) 43 (12) 5.1 (3.7)

76 (16) 14 (3) 10 (2) 53.5 (9.7) 0 (0)

87 (13) 13 (2) 0 (0) 48.0 (11.2) 35 (5) 5.1 (3.7)

88 (21) 8 (2) 4 (1) 54.9 (5.3) 0 (0)

e

e

4 (1) 22 (6) 34 (10) 40 (12) 0 2.7 (1.4)

e e e e e e

0 (0) 16 (2) 42 (6) 17 (3) 25 (4) 2.4 (1.0)

e e e e e

91 (26) 9 (3)

e e

83 (12) 17 (3)

e e

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Table 2 Means and Standard Deviations (in Parentheses) for Questionnaire Measures Across Groups.

SCAS-C* SCAS-P* ATAQ PAQLQ DASS 21 (Anxiety subscale)

Asthma & Anxiety

Anxiety Only

Asthma Only

Healthy Control

35.79 (15.58) 29.48 (11.15) 3.82 (2.44) 4.96 (1.30) 5.40 (7.93)

34.81 (15.08) 25.04 (10.27) e e 2.70 (4.27)

18.07 (8.45) 12.20 (6.99) 3.67 (2.94) 5.39 (1.31) 1.73 (3.40)

18.79 (7.65) 10.71 (6.42) e e 1.30 (3.37)

Note. SCAS-C ¼ Spence Children's Anxiety Scale; SCAS-P ¼ Spence Children's Anxiety Scale e Parent Report; ATAQ ¼ Asthma Therapy Assessment Questionnaire; PAQLQ ¼ Pediatric Asthma Quality of Life Questionnaire. * Significant difference between groups (anxiety versus no anxiety) p < .001.

Table 3 Mean Involvement and Negativity on the Tangram Task. Factor

Involvement* Negativity*

Asthma & Anxiety

Anxiety Only

M

SD

M

SD

M

SD

M

SD

4.90 3.06

1.32 1.07

4.14 2.99

1.21 1.11

3.65 2.47

1.13 1.04

3.40 1.90

0.89 0.62

Asthma Only

Healthy Control

* Significant difference between groups (anxiety versus no anxiety) p < .001.

6.3. Negativity There was no significant effect of asthma status on the level of negativity, F(1, 85) ¼ 2.29 p ¼ .134, h2 ¼ .03, and no interaction effect, F(1, 85) ¼ 1.38, p ¼ .244, h2 ¼ .02 (see Table 3), which was contrary to our predictions. Similar to the results for involvement and consistent with our predictions, there was a significant main effect for child anxiety status for parental negativity, F(1, 85) ¼ 15.76 p < .001, h2 ¼ .16 indicating that parents of children with anxiety displayed greater negativity compared to parents of children without anxiety.

With regard to the subscales of the EOI, parents of children with asthma displayed significantly more overprotective/selfsacrificing/non-objective behaviours than parents of children without asthma, c2(1, N ¼ 89) ¼ 8.82, p ¼ .003, F ¼ .32 regardless of child anxiety status, which is in contrast to the results for the tangram task and overall EOI scale, and supports our predictions. Further, there was a greater prevalence of overprotective/selfsacrificing/lack of objectivity for parents of children with asthma compared to parents of healthy controls, c2(1, N ¼ 44) ¼ 8.05, p ¼ .005, F ¼ .45 but no difference between the anxious groups, c2(1, N ¼ 50) ¼ 1.42, p ¼ .233, F ¼ .17. In support of our predictions, parents of children with anxiety displayed significantly more overprotective/self-sacrificing/ nonobjective behaviours than parents of children without anxiety, c2(1, N ¼ 89) ¼ 8.72, p ¼ .003, F ¼ .31 regardless of child asthma status. Emotional display was only present in three cases, all of which were among parents of children with asthma and anxiety, therefore, rates of emotional display was highest in the asthma and anxiety group compared to the other three groups, c2(3, N ¼ 89) ¼ 8.65, p ¼ .034. 7.3. Criticism (CRIT)

7. Task 2: FMSS 7.1. Preliminary analyses Age and gender were not related to the overall EOI or CRIT scores, nor to either of the EOI subscales, all ps > 0.05. 7.2. Emotional Overinvolvement (EOI) Table 4 shows the frequencies of EOI and EOI subcategories for each group. Similar to the results for the tangram task, and contrary to our predictions, there was no relationship between child asthma status and rates of EOI, c2(1, N ¼ 89) ¼ 1.69, p ¼ .194, F ¼ .14. Further, there was no difference between the two groups in which the child was anxious (asthma and anxiety group and anxiety only group), c2 (1, N ¼ 50) ¼ 0.18, p ¼ .668, F ¼ .06 and no difference between the groups in which the child was not anxious, c2(1, N ¼ 44) ¼ 2.83, p ¼ .092, F ¼ .27. In support of our predictions, results showed that rates of EOI were significantly higher in parents of children with anxiety than parents of children without anxiety, c2(1, N ¼ 89) ¼ 4.74, p ¼ .003, F ¼ .23, regardless of child asthma status.

Table 4 shows the frequencies of CRIT ratings for each group. There was no significant effect of child asthma status on the level of CRIT across the four groups, c2(1, N ¼ 89) ¼ 0.01, p ¼ .909, F ¼ .01 which was inconsistent with our hypotheses. However, levels of CRIT were higher in the anxiety only group compared to anxiety and asthma group, c2(1, N ¼ 50) ¼ 3.95, p ¼ .047, F ¼ .28 which was not predicted. There were no significant differences between the non-anxious groups, c2(1, N ¼ 44) ¼ 1.68, p ¼ .196, F ¼ .21. Results also showed that parents were significantly more critical of children with anxiety compared to children without anxiety, c2(1, N ¼ 89) ¼ 8.92, p ¼ .003, F ¼ .32, thus supporting our predictions. 8. Discussion The current study investigated observed parental involvement and negativity as they relate to child asthma and anxiety status using the tangram task and FMSS. Contrary to our hypotheses, there were no significant differences in parenting styles for parents of children with asthma compared to parents of children without asthma on overall measures of involvement and negativity on both tasks. However, in support of our first hypothesis, results from the

Table 4 Frequencies of EOI, EOI subscales and CRIT from the FMSS.

Borderline-high EOI (%) Emotional display (% present) Overprotection/self-sacrificing/lack of objectivity (% borderline or present) Borderline-high CRIT (%)

Asthma & Anxiety

Anxiety Only

Asthma Only

Healthy Control

75.9 13.8 55.2 48.3

81.0 0.0 38.1 76.2

73.3 0.0 40.0 40.0

45.8 0.0 4.2 20.8

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subscale of the FMSS showed that parents of children with asthma were more overprotective, or selfesacrificing or non-objective, than parents of children without asthma, and this difference was greater in the non-anxious groups (asthma only group versus the healthy control group). Consistent with previous research, and in line with our second hypothesis, results from both tasks demonstrated that parents of children with anxiety were more overinvolved and negative compared to children without anxiety, regardless of the child's asthma status. Contrary to our predictions, parents of children with asthma did not display greater levels of involvement or negativity compared to parents of children without asthma in the tangram task. Given our small sample size for the asthma groups it is possible that a larger sample may have provided enough power to support our finding for parental involvement as there was a trend towards significance (p ¼ 0.05; we required a sample size of 21 in each group to detect a medium to large effect), however further research with a larger sample size is needed to examine this assertion. In regard to parental involvement, this result is inconsistent with research showing that mothers of children with asthma are more overinvolved than mothers of healthy children (Block et al., 1966; Byrne & Murrell, 1977), but is consistent with research in medical settings that has demonstrated no relationship between parental involvement and a child's medical history (Thomasgard & Metz, 1997; Thomasgard, Shonkoff, Metz, & Edelbrock, 1995). In regard to parental negativity, our results are inconsistent with studies showing parents of children with asthma as more negative and critical compared to parents of children without asthma (Hermanns et al., 1989; Schobinger et al., 1992, 1993). However, these studies did not measure or control for child anxiety, and thus the impact of child asthma status may have been overestimated. In other words, higher levels of anxious symtomotology in the asthma group may have elicited more negative and critical parenting behaviours in those studies. Alternatively, our findings may reflect the age of the sample used in the present study. It may be that more negative and critical parenting-child interactions occur when children with asthma are older, as children/adolescents attempt to take more responsibility for the management of their illness and seek greater independence from their parents. However, this explanation does not explain the discrepant result with Hermanns et al. (1989) and Schobinger et al. (1992; 1993) studies as the age range used was similar. Future research could investigate parenting of children across a wider age range to examine whether negativity is more strongly associated with asthma and anxiety in older children compared to younger children. Alternative measures of parental involvement and negativity were obtained from the FMSS. Consistent with the results for the tangram task, there were no associations between overall levels of parental involvement or parental negativity and child asthma status. However, the FMSS subscale measuring overprotective/selfsacrificing/nonobjective behaviours was associated with child asthma status. This result is consistent with our predictions, and, if our findings are correct, suggests that this subscale measure may be particularly important for understanding anxiety in children with asthma. The FMSS subscale appears to most closely resemble a subcomponent of parental involvement known as parental intrusiveness, which has been highlighted as being particularly relevant to child anxiety in healthy children (McLeod et al., 2011). When parents act intrusively they tend to take over tasks that children could do independently (i.e., it is at odds with the child's developmental level), and this may impact on the child's self-efficacy and perceived control (Bandura, 1997; Muris, 2002). While intrusive parenting behaviours might be understandable and somewhat adaptive in the context of managing a child's chronic illness - for

example managing a child's medication - parents may inadvertently be affecting their child's perceived control and efficacy over managing their illness, which may confer partial risk for child anxiety. An additional unexpected finding from the FMSS showed that parental negativity was higher in the anxiety only group compared to the asthma and anxiety group, but that the two non-anxiety groups (asthma only and healthy control) were statistically equivalent. It may be that parents of children with asthma and anxiety are less critical compared to parents of children with anxiety only, because of the child's asthma. In other words, parents are less forthcoming with their criticism and thus “accommodating” their child's anxiety in the context of their child's illness. The lower levels of parental negativity in the asthma and anxiety group compared to the anxiety only group is particularly relevant for treatment. Current cognitive behavioural interventions for children with anxiety which include parents in treatment target both parental overprotection and negativity (Rapee, Schniering, & Hudson, 2009). Thus, it may be that treatments addressing parental negativity may not be of great need, and would be better to focus on areas with greater need, such as parental overinvolvement. Taken together, the results from both tasks suggest that parenting behaviours of parents of children with asthma compared to behaviours or parents of children without asthma do not differ as much as hypothesized. The exceptions to this finding were the higher levels of overprotective/self-sacrificing/nonobjective behaviours on the subcomponent measure of the FMSS for the asthma and anxiety group, and slightly lower levels of negativity for this group compared to the anxiety only group. Finally, results from the current study support and extend previous research showing that parents of children with anxiety are more overinvolved compared to parents of non-anxious children (Bogels & Brechman-Toussaint, 2006; Gar & Hudson, 2008; Hudson & Rapee, 2001; McLeod et al., 2007). Although the research literature is less consistent on the association between parental negativity and child anxiety, we found evidence of an association between child anxiety and parental negativity using both tasks, which is consistent with other studies using direct observation measures (Gar & Hudson, 2008; Hudson & Rapee, 2001). Our findings extend previous research by demonstrating that parental involvement and negativity are associated with anxiety in children with asthma, as well as anxiety in healthy children. The clinical implications of the current findings are twofold. First, our results suggest it may be worthwhile to include parents in treatments designed for children with comorbid asthma and anxiety. To date, the few studies that have investigated the efficacy of CBT for children with asthma and anxiety have not included parents, which may have meant that the treatment was suboptimal (Marriage & Henderson, 2012; Park, Sawyer, & Glaun, 1996). Although evidence for the efficacy of including parents in CBT treatment for healthy children with anxiety is mixed (Manassis et al., 2014), parenting strategies have been successfully incorporated into CBT treatments for other chronic illnesses, such as pain (Palermo, 2012) - which have resulted in efficacious outcomes for reducing children's pain (Palermo, Valrie, & Karlson, 2014). It seems possible that including parenting strategies which focuses on parenting behaviours associated with child anxiety in children with asthma could lead to enhanced physical and mental health outcomes for these children, however further research is needed to assess this. Second, our results may suggest that some of the strategies that have already been developed for working with parents with healthy children with anxiety may be useful for parents of children with asthma and comorbid anxiety (e.g. strategies targeting involvement), however, others may not be necessary (e.g. those targeting negativity). Therefore, targeted parenting

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interventions for parents of children with asthma and anxiety over and above what is already in place for children with anxiety are not needed, except to perhaps focus more on parental involvement than parental negativity. The results of the current study raise the question whether the same parental processes (namely, parental) which moderate anxiety in children with and without asthma also moderate anxiety in children with other chronic illnesses. Indeed, parents of children with other chronic illnesses have been found to be more overprotective or controlling than parents of children without those chronic illnesses (Holmbeck et al., 2002), or equally overprotective of children with different chronic illnesses (cancer, asthma, diabetes and cystic fibrosis; Hullmann et al., 2010). Thus, parenting strategies included in current anxiety treatments for children could potentially be useful for children with anxiety and chronic illnesses in general. Given that there is a lack of evidence-based psychological treatments for these children (Eccleston, Fisher, Law, Bartlett, & Palermo, 2015; Pao & Bosk, 2011), this is potentially useful information for practitioners and researchers developing treatments for children in these populations. Results from the current study should be interpreted in light of its limitations. First, the sample size for the asthma only group was small, which suggests that power may have been an issue for some of the non-significant findings. Despite extensive efforts to recruit children with asthma over a significant time period, in part, the high prevalence of anxiety in children with asthma reflects the high comorbidity between the two disorders. Nevertheless, future studies should include enough participants in each group to ensure sufficient power to compare parental behaviours across asthma groups. Second, the offer of CBT treatment for children with anxiety may have led to stronger effects for child anxiety as parents may have been more willing to express parenting behaviours associated with child anxiety in order to be eligible for treatment. However, parents were offered treatment regardless of their child's anxiety status, thus it is unlikely that differences in parenting reflected differences in incentives for participation. Third, the majority of participants in this study were Caucasian and the parents were highly educated, thus the extent to which the findings generalise to other populations remains unknown. Finally, the current study was cross-sectional and thus cannot determine the direction of effects between parenting behaviours and anxiety in children with asthma. Longitudinal and experimental designs would help to elucidate the multi-faceted reciprocal influences of child anxiety and child asthma on parent-child interactions. In conclusion, the current study replicated well-documented findings that parental involvement and negativity are associated with child anxiety. A particular subcomponent of parental involvement measuring overprotective, self-sacrificing or nonobjective behaviours appears not only to characterise interactions between parents and their children with anxiety, but also those with asthma. While these parenting behaviours are understandable in the context of managing a child with chronic illness, health professionals working with this population could be made aware of parenting behaviours which may be associated with child anxiety and include parents as part of treatment programs designed to manage a child's asthma. Future research is recommended to elucidate the mechanisms and reciprocal influences of parenting on anxiety in children with asthma, and test these theories using measures of subcomponents of parental involvement in longitudinal or experimental designs.

Conflict of interest The authors declare no conflict of interest.

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Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Acknowledgements We would like to thank Sarah Lorimer for her assistance testing participants and Anna Kelly for her assistance in coding the tangram and FMSS tasks. We would also like to thank the staff at the Sydney Children's Hospitals Network for assisting us with recruitment. References Akinbami, L. J., Moorman, J. E., Bailey, C., Zahran, H. S., King, M., Johnson, C. A., et al. (2012). Trends in asthma prevalence, health care use, and mortality in the United States, 2001-2010. NCHS Data Brief, 94, 1e8. Anderson, B. J., & Coyne, J. C. (1991). “Miscarried helping” in the families of children and adolescents with chronic diseases. In Advances in child health psychology (pp. 167e177). Gainesville, FL ; Gainesville, FL: J Hillis Miller Health Science Center; University of Florida Press; US; US. Anderson, B. J., & Coyne, J. C. (1993). Family context and compliance behavior in chronically ill children. In Developmental aspects of health compliance behavior (pp. 77e89). Hillsdale, NJ, England: Lawrence Erlbaum Associates, Inc; England. Antony, M. M., Bieling, P. J., Cox, B. J., Enns, M. W., & Swinson, R. P. (1998). Psychometric properties of the 42-item and 21-item versions of the depression anxiety stress scales in clinical groups and a community sample. [Empirical study]. Psychological Assessment, 10(2), 176e181. http://dx.doi.org/10.1037/ 1040-3590.10.2.176. Bandura, A. (1997). Self-efficacy: The exercise of control. New York, NY: W H Freeman/ Times Books/Henry Holt & Co; US. Block, J., Harvey, E., & Jennings, P. H. (1966). Clinicians' conceptions of the asthmatogenic mother. Archives of General Psychiatry, 15(6), 610e618. http://dx.doi. org/10.1001/archpsyc.1966.01730180050007. Bogels, S. M., & Brechman-Toussaint, M. L. (2006). Family issues in child anxiety: Attachment, family functioning, parental rearing and beliefs. [Literature Review]. Clinical Psychology Review, 26(7), 834e856. http://dx.doi.org/10.1016/j. cpr.2005.08.001. Bush, T., Richardson, L., Katon, W., Russo, J., Lozano, P., McCauley, E., et al. (2007). Anxiety and depressive disorders are associated with smoking in adolescents with asthma. [Research Support, N.I.H., Extramural]. Journal of Adolescent Health, 40(5), 425e432. Byrne, D., & Murrell, T. (1977). Self descriptions of mothers of asthmatic children. Australian and New Zealand Journal of Psychiatry, 11(3), 179e183. http://dx.doi. org/10.3109/00048677709159558. Calam, R., Gregg, L., Simpson, B., Morris, J., Woodcock, A., & Custovic, A. (2003). Childhood asthma, behavior problems, and family functioning. [Research Support, Non-U.S. Gov't]. Journal of Allergy & Clinical Immunology, 112(3), 499e504. Chavira, D. A., Stein, M. B., Bailey, K., & Stein, M. T. (2004). Comorbidity of generalized social anxiety disorder and depression in a pediatric primary care sample. [Empirical Study; Quantitative Study]. Journal of Affective Disorders, 80(2e3), 163e171. http://dx.doi.org/10.1016/S0165-0327%2803%2900103-4. Chorpita, B. F., & Barlow, D. H. (1998). The development of anxiety: The role of control in the early environment. Psychological Bulletin, 124(1), 3e21. http://dx. doi.org/10.1037/0033-2909.124.1.3. Coyne, J. C., Wortman, C. B., & Lehman, D. R. (1988). The other side of support: Emotional overinvolvement and miscarried helping. In Marshaling social support: Formats, processes, and effects (pp. 305e330). Thousand Oaks, CA: Sage Publications, Inc; US. Craske, M. G. (1999). Anxiety disorders: Psychological approaches to theory and treatment. Boulder, CO: Westview Press; US. Dadds, M. R., & Roth, J. H. (2001). Family processes in the development of anxiety problems. In The developmental psychopathology of anxiety (pp. 278e303). New York, NY: Oxford University Press; US. Dudeney, J., Sharpe, L., Jaffe, A., Jones, E. B., & Hunt, C. (2017). Anxiety in youth with asthma: A meta-analysis. Pediatric Pulmonology, 9999, 1e9. https://doi.org/10. 1002/ppul.23689. Easter, G., Sharpe, L., & Hunt, C. J. (2015). Systematic review and meta-analysis of anxious and depressive symptoms in caregivers of children with asthma. [Literature Review; Systematic Review; Meta Analysis]. Journal of Pediatric Psychology, 40(7), 623e632. http://dx.doi.org/10.1093/jpepsy/jsv012. Eccleston, C., Fisher, E., Law, E., Bartlett, J., & Palermo, T. M. (2015). Psychological interventions for parents of children and adolescents with chronic illness. Cochrane Database of Systematic Reviews, (4)http://dx.doi.org/10.1002/ 14651858.CD009660.pub3. Art. No.: CD009660. Fernandes, L., Fonseca, J., Martins, S., Delgado, L., Pereira, A. C., Vaz, M., et al. (2010). Association of anxiety with asthma: Subjective and objective outcome measures. Psychosomatics, 51(1), 39e46. http://dx.doi.org/10.1176/appi.psy.51.1.39. Frankel, K., & Wamboldt, M. Z. (1998). Chronic childhood illness and maternal

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