Behavioral Sleep Medicine
ISSN: 1540-2002 (Print) 1540-2010 (Online) Journal homepage: http://www.tandfonline.com/loi/hbsm20
Association Between Childhood Sleep-Disordered Breathing and Disruptive Behavior Disorders in Childhood and Adolescence Evelyn Constantin, Nancy C. P. Low, Erika Dugas, Igor Karp & Jennifer O'Loughlin To cite this article: Evelyn Constantin, Nancy C. P. Low, Erika Dugas, Igor Karp & Jennifer O'Loughlin (2015) Association Between Childhood Sleep-Disordered Breathing and Disruptive Behavior Disorders in Childhood and Adolescence, Behavioral Sleep Medicine, 13:6, 442-454, DOI: 10.1080/15402002.2014.940106 To link to this article: http://dx.doi.org/10.1080/15402002.2014.940106
Published online: 07 Aug 2014.
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Citing articles: 2 View citing articles
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Date: 05 November 2015, At: 13:51
Behavioral Sleep Medicine, 13:442–454, 2015 Copyright © Taylor & Francis Group, LLC ISSN: 1540-2002 print/1540-2010 online DOI: 10.1080/15402002.2014.940106
ARTICLES
Downloaded by [96.54.196.29] at 13:51 05 November 2015
Association Between Childhood Sleep-Disordered Breathing and Disruptive Behavior Disorders in Childhood and Adolescence Evelyn Constantin Department of Pediatrics McGill University
Nancy C. P. Low Department of Psychiatry McGill University
Erika Dugas Centre de Recherche du Centre Hospitalier de l’Université de Montréal
Igor Karp Centre de Recherche du Centre Hospitalier de l’Université de Montréal; Department of Social and Preventive Medicine University of Montréal
Jennifer O’Loughlin Centre de Recherche du Centre Hospitalier de l’Université de Montréal; Department of Social and Preventive Medicine University of Montréal; Institut national de santé publique du Québec
Correspondence should be addressed to Evelyn Constantin, MD, MSc(Epi), Montreal Children’s Hospital, 2300 Tupper Street, Room C-508, Montreal, Quebec, Canada H3H 1P3. E-mail: [email protected]
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We examined the association between sleep-disordered breathing (SDB) and disruptive behavior disorders in 605 children participating in a population-based cohort study. Nineteen percent of children snored (sometimes or often) and 10% had obstructive sleep apnea (OSA) symptoms. Thirteen percent had an ADHD diagnosis or symptoms and 5–9% had behavioral problems or a conduct disorder. Snoring or OSA symptoms were associated with a twofold difference in the odds of ADHD diagnosis or symptoms. OSA symptoms were associated with a threefold to fourfold difference in the odds of behavioral problems or conduct disorder. Clinicians should consider inquiring about SDB in children with disruptive behavior disorders and should also consider disruptive behavior disorders as potential sequelae of SDB.
Sleep-disordered breathing in children is characterized by abnormal patterns of respiration and/or ventilation during sleep (Marcus et al., 1999). The spectrum of sleep-disordered breathing spans primary snoring to the most severe form, obstructive sleep apnea (OSA). OSA is characterized by partial or complete upper airway obstruction, leading to disrupted sleep and abnormal gas exchange (Brouillette, Fernbach, & Hunt, 1982; Guilleminault, Korobkin, & Winkle, 1981; Loughlin et al., 1996). The prevalence of habitual snoring in children is 12–15% (Ali, Pitson, & Stradling, 1993; Castronovo et al., 2003; Zhang, Spickett, Rumchev, Lee, & Stick, 2004). More recently, Lumeng and Chervin (2008) reported that the prevalence of snoring is 7.5%, and the prevalence of OSA is 1–5% (Lumeng & Chervin, 2008; Marcus et al., 2012). OSA in children has been associated with failure to thrive, cardiovascular disorders including pulmonary and systemic hypertension, learning deficits, and behavioral problems including attention deficit hyperactivity disorder (ADHD; Ali, Pitson, & Stradling, 1994; Amin et al., 2002; Amin et al., 2005; Brouillette et al., 1982; Brouilette et al., 1984; Chervin & Archbold, 2001; Gaultier, 1992; Gozal, 1998; Gozal, Serpero, Sans Capdevila, & Kheirandish-Gozal, 2008; Guilleminault et al., 1981; Menashe, Farrehi, & Miller, 1965; Suratt et al., 2007; Verhulst et al., 2007). ADHD is one of the most prevalent psychiatric conditions in children, with 3–12% of school-aged children affected (Faraone, Sergeant, Gillberg, & Biederman, 2003; Mandelbaum, 2006). It is characterized by inattention, hyperactivity, and impulsivity, and its diagnosis is established if any symptoms of inattention, hyperactivity, or impulsivity occur before the age of 7 years and if functioning is impaired in two or more settings (e.g., home, school, daycare, etc.; Diagnostic and Statistical Manual of Mental Disorders [4th ed., text rev.; DSM-IV-TR], APA, 2000). ADHD symptoms may lead to poor social development (i.e., loss of friends or inability to sustain friendships), academic failure, and family conflict (Classi, Milton, Ward, Sarsour, & Johnston, 2012). Symptoms often persist into adulthood, adversely affecting occupational performance (Biederman & Faraone, 2005). The high prevalence and chronicity of ADHD, as well as the comorbidity (e.g., oppositional defiant disorder, depression, generalized anxiety disorder, and substance misuse) associated with ADHD (Elia, Ambrosini, & Berrettini, 2008; van Emmerik-van Oortmerssen et al., 2012) have led the Centers for Disease Control and Prevention to identify ADHD as a public health concern (Doshi et al., 2012). There is a strong link between sleep-disordered breathing in children and ADHD (O’Brien et al., 2003; Silvestri et al., 2009; Weiss & Salpekar, 2010), possibly related to the sleep disruption and fragmentation caused by sleep-disordered breathing (Beebe, 2006). Up to one third of children with frequent loud snoring and/or OSA show symptoms of ADHD (Gruber et al., 2009). Daytime symptoms of OSA can manifest as paradoxical hyperactivity, neurocognitive deficits, and behavioral problems such as aggressivity, impulsivity, and oppositional behavior
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(Blunden, Lushington, Kennedy, Martin, & Dawson, 2000; Owens, 2008). Sleep-disordered breathing has also been associated with compromised academic performance (Gozal & Pope, 2001) and may result in learning difficulties and academic failure in the same way as primary disruptive behavioral disorders (i.e., ADHD, oppositional defiant disorder, conduct disorderthose disorders unrelated to sleep-disordered breathing). Increased arousals/awakenings in children may be a defense for compromised respiratory drive due to sleep-disordered breathing and can result in the cognitively compromised profile seen in ADHD (Miano et al., 2011). There is improvement in ADHD symptoms following adenotonsillectomy, the most common treatment for OSA, indirectly providing evidence of a possible mechanism underpinning the association between OSA and ADHD (i.e., resolution of OSA with adenotonsillectomy leads to improvement of ADHD; Ali, Pitson, & Stradling, 1996; Chervin et al., 2006; Friedman et al., 2003; Goldstein, Post, Rosenfeld, & Campbell, 2000). Moreover, one study reported greater improvement in ADHD symptoms in children with mild OSA who underwent adenotonsillectomy compared with those who continued treatment with methylphenidate, a medication commonly used to treat ADHD (Wei, Mayo, Smith, Reese, & Weatherly, 2007). Treatment of OSA has also been associated with improvement in academic performance (Ali et al., 1996; Gozal, 1998; Stradling, Thomas, Warley, Williams, & Freeland, 1990). Conduct problems (e.g., bullying, starting fights, destruction of property, and deceitfulness) are also frequent in children with sleep-disordered breathing (Arman et al., 2005; Chervin, Dillon, Archbold, & Ruzicka, 2003). Chervin et al. (2003) reported that increasing severity of sleep-disordered breathing was positively associated with level of conduct symptoms as measured by the Conduct Problem Index. There are few population-based studies examining the association between sleep-disordered breathing and disruptive behavior disorders (Arman et al., 2005; Brockmann et al., 2012). Arman et al. (2005) reported that habitual snorers in a population-based sample of children in Istanbul had higher rates of inattention, hyperactivity, conduct symptoms, and oppositional defiant behavior than nonsnorers and non-habitual snorers (Arman et al., 2005). Brockmann and colleagues conducted a cross-sectional study using a community-based sample of children 7–17 years old in Santiago, Chile (Brockmann et al., 2012). They found a high prevalence of snoring and symptoms of sleep-disordered breathing in their sample, as well as an association between the presence of sleep-disordered breathing symptoms and hyperactive behavior and poor academic performance (Brockmann et al., 2012). As mentioned previously, numerous clinic-based studies have examined the association between sleep-disordered breathing and ADHD. Some studies have evaluated other disruptive behavior disorders including oppositional defiant disorder and conduct disorder. However, there are few population-based studies to date. The objective of this study was to examine, in a large population-based sample, the association between symptoms of sleep-disordered breathing during childhood and disruptive behavior disorders in childhood and/or adolescence.
METHODS Data were drawn from the Nicotine Dependence in Teens (NDIT) Study, an ongoing prospective cohort investigation of 1,293 students recruited in 1999–2000 from all grade 7 classes in a convenience sample of 10 secondary schools located in urban, suburban, and rural areas in
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or near Montreal, Canada (O’Loughlin, Karp, Koulis, Paradis, & DiFranza, 2009). Self-report questionnaires were administered at school every 3 months during the 10-month school year from grades 7 to 11, for a total of 20 survey cycles during secondary school. In 2007–2008 (i.e., in survey cycle 21) and in 2012 (i.e., in survey cycle 22), when participants were aged 20 and 24 years on average, respectively, data were collected in mailed self-report questionnaires. In 2009–2010, when participants were aged 22 years on average, self-report questionnaires were mailed to 1,009 parents of participants who continued to participate in the NDIT study (29 participants did not want us to contact their parents; 221 refused to continue participation and 34 were lost to follow-up), representing 78% of the original 1,293 participants. Parental data were collected in three questionnaires: a questionnaire pertaining to the mother completed by the mother .n D 597/, a questionnaire pertaining to the father completed by the father .n D 478/, and a questionnaire completed by either parent that collected data on the NDIT participant (n D 647, 64% of the 1,009 participants). Demographic data (age, sex, birth country, language most often spoken at home) were drawn from the child questionnaire; all other data were drawn from the parent questionnaire. All NDIT participants provided assent and their parents provided informed consent. The study was approved by the Montreal Department of Public Health Ethics Review Committee, the McGill University Institutional Review Board, and the Ethics Research Committee of the Centre de Recherche du Centre Hospitalier de l’Université de Montréal. Study Variables Data on disruptive behavior diagnoses and symptoms were drawn from the parent questionnaire. Diagnosed ADHD (yes, no) was measured by: “Was ‘NDIT participant’ ever diagnosed by a health professional with attention deficit hyperactivity disorder (ADHD)?” If yes, parents reported age at diagnosis and whether medication was prescribed. ADHD symptoms were measured using the attention problems scale of the Child Behavior Checklist (CBCL; Achenbach & Rescorla, 2001): “Do any of the following describe ‘NDIT participant’ either in elementary or high school: (i) frequently interrupted others; (ii) was easily distracted; (iii) often fidgeted or squirmed in seat; (iv) often did not listen when spoken to; (v) frequently avoided homework.” Response choices included “not at all like him/her,” “a bit like him/her,” and “a lot like him/her” and were scored 0, 1, and 2, respectively. Scores for each item were summed (range 0–10; median [IQR] D 1 [3]). If they scored 6, participants were categorized (yes, no) as having ADHD symptoms possibly indicative of a disorder. The attention problems scale of the CBCL has been reported to have excellent convergence with the diagnosis of ADHD based on structured interview (Biederman et al., 1993). Diagnosed behavioral problems (yes, no) were measured by: “Was ‘NDIT participant’ ever diagnosed by a health professional with behavioral problems (oppositional defiant disorder, conduct disorder)?” If yes, parents reported age at diagnosis. Data on conduct disorder symptoms were collected using the delinquent behavior scale of the CBCL: “Do any of the following describe ‘NDIT participant’ either in elementary or high school: (i) ran away from home overnight; (ii) often stole things or shoplifted; (iii) frequently skipped school; (iv) deliberately destroyed others’ property; (v) often started fights with neighbours, schoolmates; (vi) was physically cruel to animals; (vii) broke into a house or car; (viii) often did not want to go to school; (ix) frequently lied; (x) deliberately hurt others physically;
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and (xi) often bullied, threatened, or intimidated others?” Response choices included “not at all like him/her,” “a bit like him/her,” and “a lot like him/her” and scored 0, 1, and 2, respectively. Scores for each item were summed (scores from 0–22; median [IQR] D 0 [1]). If they scored 5 (i.e., child threshold), participants were categorized (yes, no) as having conduct disorder symptoms possibly indicative of a disorder. Since the questions were asked about both elementary and high school, we also categorized participants using the adolescent threshold ( 8). The delinquent behavior scale of the CBCL has been reported to have excellent convergence with the diagnosis of conduct disorder based on structured interview (Edelbrock & Costello, 1988). Parents indicated (yes, no, don’t know) if the NDIT participant had ever received services for learning or behavioral problems and if he or she had ever been held back in school (yes, no, don’t know). Sleep-disordered breathing was measured in the parent questionnaires by: “During childhood, how often (never, rarely, sometimes, often, don’t know) did ‘NDIT participant’ : : : (i) snore; (ii) snore very loudly; (iii) breathe forcefully or noisily while sleeping; (iv) have problems or difficulty breathing while sleeping; (v) stop breathing or wake up gasping for air while sleeping. For analysis, participants were categorized into one of four mutually exclusive categories: (a) no snoring or OSA symptoms; (b) snoring, that is, snores or snores very loudly sometimes or often, and responses to items (iii), (iv) and (v) were never or rarely; (c) possible OSA: participants had snoring and in addition, responded sometimes or often to items (iii), (iv) or (v); (d) this category included all remaining participants (i.e., those whose parents reported that child rarely snored or parents don’t know). Sleep-disordered breathing symptoms as reported on parental questionnaires correspond well with the presence of objectively determined sleep-disordered breathing symptoms, including snoring, supporting the accuracy and usefulness of parental reporting of sleep-disordered breathing symptoms in children (MontgomeryDowns, O’Brien, Holbrook, & Gozal, 2004). All of the sleep-disordered breathing items used in our study were similar to the items described in the Sleep Disordered Breathing Questions section of the validated instrument by Montgomery-Downs and colleagues, specifically (a) presence of snoring, (b) frequency of snoring, (c) loudness of snoring, (d) struggling to breathe while asleep, and (e) stop breathing during sleep (Montgomery-Downs et al., 2004). Data on participants’ age, sex, language spoken most often at home (French, other), and born in Canada (yes, no) were drawn from participants’ baseline questionnaires completed in grade 7. Data on parent’s age and mother’s education (i.e., completed university [yes, no]) were drawn from the parent questionnaire. Data Analysis Forty-two participants (7% of 647) whose parents indicated that they had been born prematurely at < 37 weeks gestation were excluded because of possible OSA comorbidity related to prematurity (Raynes-Greenow et al., 2012). Therefore the analytic sample included 605 participants. Odds ratios (OR) and their 95% confidence intervals (CIs) for the associations between history of sleep-disordered breathing and history of each of the study outcomes (i.e., diagnosed ADHD and/or ADHD symptoms, diagnosed behavioral problems or conduct disorder symptoms, received services for learning or behavioral problems, and ever held back in school) were estimated, one at a time, in univariate and multivariable logistic regression models. In the latter model, sex and mother’s education were included as potential confounders (Barkley, 1990;
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Moffitt & Caspi, 2001; Odgers et al., 2012; Rieppi et al., 2002; Silverthorn, & Frick, 1999; Silverthorn, Frick, & Reynolds, 2001; Tillman, & Granvald, 2014). Analyses were conducted using SPSS software, Version 16.0 (SPSS Inc., Chicago, IL).
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RESULTS Of 1,009 participants whose parents were mailed questionnaires, 647 (64%) returned a completed questionnaire pertaining to the NDIT participant. There were few important differences in baseline characteristics between participants whose parents completed the questionnaire and those whose parents did not (Table 1). Parents who completed the questionnaire pertaining to the NDIT participant (84% were the biologic mother) were aged 51 (SD D 7) years on average. Eighteen percent of boys and 9% of girls .p D 0:002/ had been diagnosed with ADHD by a health care professional and/or had ADHD symptoms (Table 2). The mean age at ADHD diagnosis was 10 .SD D 4/ years in boys, and 10 .SD D 5/ years in girls. The majority (77%) of children diagnosed with ADHD by a health care professional were reportedly diagnosed by age 10. A relatively high proportion of those diagnosed with ADHD (71% of boys and 82% of girls) had been prescribed medication for it. Nine percent (using the child threshold) and 5% (using the adolescent threshold) of participants had been diagnosed with behavioral problems or had conduct disorder symptoms (Table 2). There was no statistically significant difference in the proportion by sex. The mean age at diagnosis of behavioral problems was 11 years .SD D 4/ in boys, and 12 years .SD D 5/ in girls. Almost 60% of children diagnosed with behavioral problems/conduct disorder by a health care professional were reportedly diagnosed during adolescence (at age 13 to 19 years). The most frequently reported symptoms of sleep-disordered breathing were snoring (19%) and breathing forcefully or noisily while sleeping (sometimes or often; 14%). Lower proportions of participants snored very loudly (sometimes or often; 8%), had problems or difficulty breathing while sleeping (sometimes or often; 9%), and stopped breathing or woke up gasping for air while sleeping (sometimes or often; 2%). Ten percent of participants had symptoms
TABLE 1 Comparison of Baseline Characteristics of Participants Whose Parents Did and Did Not Complete the Parent Questionnaire Pertaining to the NDIT Participant (NDIT Study, Montreal, Canada, 1999–2010)
Age, y, mean (SD) Male, % French spoken at home, % Mother university-educated, %* Born in Canada, % Note.
Parent Completed Questionnaire (n D 647)
Parent Did Not Complete Questionnaire (n D 646)
p-value for Difference
12.7 (0.4) 46.7 32.1 45.7 95.8
12.9 (0.6) 49.7 28.0 42.2 88.4
ISSN: 1540-2002 (Print) 1540-2010 (Online) Journal homepage: http://www.tandfonline.com/loi/hbsm20
Association Between Childhood Sleep-Disordered Breathing and Disruptive Behavior Disorders in Childhood and Adolescence Evelyn Constantin, Nancy C. P. Low, Erika Dugas, Igor Karp & Jennifer O'Loughlin To cite this article: Evelyn Constantin, Nancy C. P. Low, Erika Dugas, Igor Karp & Jennifer O'Loughlin (2015) Association Between Childhood Sleep-Disordered Breathing and Disruptive Behavior Disorders in Childhood and Adolescence, Behavioral Sleep Medicine, 13:6, 442-454, DOI: 10.1080/15402002.2014.940106 To link to this article: http://dx.doi.org/10.1080/15402002.2014.940106
Published online: 07 Aug 2014.
Submit your article to this journal
Article views: 177
View related articles
View Crossmark data
Citing articles: 2 View citing articles
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=hbsm20 Download by: [96.54.196.29]
Date: 05 November 2015, At: 13:51
Behavioral Sleep Medicine, 13:442–454, 2015 Copyright © Taylor & Francis Group, LLC ISSN: 1540-2002 print/1540-2010 online DOI: 10.1080/15402002.2014.940106
ARTICLES
Downloaded by [96.54.196.29] at 13:51 05 November 2015
Association Between Childhood Sleep-Disordered Breathing and Disruptive Behavior Disorders in Childhood and Adolescence Evelyn Constantin Department of Pediatrics McGill University
Nancy C. P. Low Department of Psychiatry McGill University
Erika Dugas Centre de Recherche du Centre Hospitalier de l’Université de Montréal
Igor Karp Centre de Recherche du Centre Hospitalier de l’Université de Montréal; Department of Social and Preventive Medicine University of Montréal
Jennifer O’Loughlin Centre de Recherche du Centre Hospitalier de l’Université de Montréal; Department of Social and Preventive Medicine University of Montréal; Institut national de santé publique du Québec
Correspondence should be addressed to Evelyn Constantin, MD, MSc(Epi), Montreal Children’s Hospital, 2300 Tupper Street, Room C-508, Montreal, Quebec, Canada H3H 1P3. E-mail: [email protected]
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We examined the association between sleep-disordered breathing (SDB) and disruptive behavior disorders in 605 children participating in a population-based cohort study. Nineteen percent of children snored (sometimes or often) and 10% had obstructive sleep apnea (OSA) symptoms. Thirteen percent had an ADHD diagnosis or symptoms and 5–9% had behavioral problems or a conduct disorder. Snoring or OSA symptoms were associated with a twofold difference in the odds of ADHD diagnosis or symptoms. OSA symptoms were associated with a threefold to fourfold difference in the odds of behavioral problems or conduct disorder. Clinicians should consider inquiring about SDB in children with disruptive behavior disorders and should also consider disruptive behavior disorders as potential sequelae of SDB.
Sleep-disordered breathing in children is characterized by abnormal patterns of respiration and/or ventilation during sleep (Marcus et al., 1999). The spectrum of sleep-disordered breathing spans primary snoring to the most severe form, obstructive sleep apnea (OSA). OSA is characterized by partial or complete upper airway obstruction, leading to disrupted sleep and abnormal gas exchange (Brouillette, Fernbach, & Hunt, 1982; Guilleminault, Korobkin, & Winkle, 1981; Loughlin et al., 1996). The prevalence of habitual snoring in children is 12–15% (Ali, Pitson, & Stradling, 1993; Castronovo et al., 2003; Zhang, Spickett, Rumchev, Lee, & Stick, 2004). More recently, Lumeng and Chervin (2008) reported that the prevalence of snoring is 7.5%, and the prevalence of OSA is 1–5% (Lumeng & Chervin, 2008; Marcus et al., 2012). OSA in children has been associated with failure to thrive, cardiovascular disorders including pulmonary and systemic hypertension, learning deficits, and behavioral problems including attention deficit hyperactivity disorder (ADHD; Ali, Pitson, & Stradling, 1994; Amin et al., 2002; Amin et al., 2005; Brouillette et al., 1982; Brouilette et al., 1984; Chervin & Archbold, 2001; Gaultier, 1992; Gozal, 1998; Gozal, Serpero, Sans Capdevila, & Kheirandish-Gozal, 2008; Guilleminault et al., 1981; Menashe, Farrehi, & Miller, 1965; Suratt et al., 2007; Verhulst et al., 2007). ADHD is one of the most prevalent psychiatric conditions in children, with 3–12% of school-aged children affected (Faraone, Sergeant, Gillberg, & Biederman, 2003; Mandelbaum, 2006). It is characterized by inattention, hyperactivity, and impulsivity, and its diagnosis is established if any symptoms of inattention, hyperactivity, or impulsivity occur before the age of 7 years and if functioning is impaired in two or more settings (e.g., home, school, daycare, etc.; Diagnostic and Statistical Manual of Mental Disorders [4th ed., text rev.; DSM-IV-TR], APA, 2000). ADHD symptoms may lead to poor social development (i.e., loss of friends or inability to sustain friendships), academic failure, and family conflict (Classi, Milton, Ward, Sarsour, & Johnston, 2012). Symptoms often persist into adulthood, adversely affecting occupational performance (Biederman & Faraone, 2005). The high prevalence and chronicity of ADHD, as well as the comorbidity (e.g., oppositional defiant disorder, depression, generalized anxiety disorder, and substance misuse) associated with ADHD (Elia, Ambrosini, & Berrettini, 2008; van Emmerik-van Oortmerssen et al., 2012) have led the Centers for Disease Control and Prevention to identify ADHD as a public health concern (Doshi et al., 2012). There is a strong link between sleep-disordered breathing in children and ADHD (O’Brien et al., 2003; Silvestri et al., 2009; Weiss & Salpekar, 2010), possibly related to the sleep disruption and fragmentation caused by sleep-disordered breathing (Beebe, 2006). Up to one third of children with frequent loud snoring and/or OSA show symptoms of ADHD (Gruber et al., 2009). Daytime symptoms of OSA can manifest as paradoxical hyperactivity, neurocognitive deficits, and behavioral problems such as aggressivity, impulsivity, and oppositional behavior
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(Blunden, Lushington, Kennedy, Martin, & Dawson, 2000; Owens, 2008). Sleep-disordered breathing has also been associated with compromised academic performance (Gozal & Pope, 2001) and may result in learning difficulties and academic failure in the same way as primary disruptive behavioral disorders (i.e., ADHD, oppositional defiant disorder, conduct disorderthose disorders unrelated to sleep-disordered breathing). Increased arousals/awakenings in children may be a defense for compromised respiratory drive due to sleep-disordered breathing and can result in the cognitively compromised profile seen in ADHD (Miano et al., 2011). There is improvement in ADHD symptoms following adenotonsillectomy, the most common treatment for OSA, indirectly providing evidence of a possible mechanism underpinning the association between OSA and ADHD (i.e., resolution of OSA with adenotonsillectomy leads to improvement of ADHD; Ali, Pitson, & Stradling, 1996; Chervin et al., 2006; Friedman et al., 2003; Goldstein, Post, Rosenfeld, & Campbell, 2000). Moreover, one study reported greater improvement in ADHD symptoms in children with mild OSA who underwent adenotonsillectomy compared with those who continued treatment with methylphenidate, a medication commonly used to treat ADHD (Wei, Mayo, Smith, Reese, & Weatherly, 2007). Treatment of OSA has also been associated with improvement in academic performance (Ali et al., 1996; Gozal, 1998; Stradling, Thomas, Warley, Williams, & Freeland, 1990). Conduct problems (e.g., bullying, starting fights, destruction of property, and deceitfulness) are also frequent in children with sleep-disordered breathing (Arman et al., 2005; Chervin, Dillon, Archbold, & Ruzicka, 2003). Chervin et al. (2003) reported that increasing severity of sleep-disordered breathing was positively associated with level of conduct symptoms as measured by the Conduct Problem Index. There are few population-based studies examining the association between sleep-disordered breathing and disruptive behavior disorders (Arman et al., 2005; Brockmann et al., 2012). Arman et al. (2005) reported that habitual snorers in a population-based sample of children in Istanbul had higher rates of inattention, hyperactivity, conduct symptoms, and oppositional defiant behavior than nonsnorers and non-habitual snorers (Arman et al., 2005). Brockmann and colleagues conducted a cross-sectional study using a community-based sample of children 7–17 years old in Santiago, Chile (Brockmann et al., 2012). They found a high prevalence of snoring and symptoms of sleep-disordered breathing in their sample, as well as an association between the presence of sleep-disordered breathing symptoms and hyperactive behavior and poor academic performance (Brockmann et al., 2012). As mentioned previously, numerous clinic-based studies have examined the association between sleep-disordered breathing and ADHD. Some studies have evaluated other disruptive behavior disorders including oppositional defiant disorder and conduct disorder. However, there are few population-based studies to date. The objective of this study was to examine, in a large population-based sample, the association between symptoms of sleep-disordered breathing during childhood and disruptive behavior disorders in childhood and/or adolescence.
METHODS Data were drawn from the Nicotine Dependence in Teens (NDIT) Study, an ongoing prospective cohort investigation of 1,293 students recruited in 1999–2000 from all grade 7 classes in a convenience sample of 10 secondary schools located in urban, suburban, and rural areas in
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or near Montreal, Canada (O’Loughlin, Karp, Koulis, Paradis, & DiFranza, 2009). Self-report questionnaires were administered at school every 3 months during the 10-month school year from grades 7 to 11, for a total of 20 survey cycles during secondary school. In 2007–2008 (i.e., in survey cycle 21) and in 2012 (i.e., in survey cycle 22), when participants were aged 20 and 24 years on average, respectively, data were collected in mailed self-report questionnaires. In 2009–2010, when participants were aged 22 years on average, self-report questionnaires were mailed to 1,009 parents of participants who continued to participate in the NDIT study (29 participants did not want us to contact their parents; 221 refused to continue participation and 34 were lost to follow-up), representing 78% of the original 1,293 participants. Parental data were collected in three questionnaires: a questionnaire pertaining to the mother completed by the mother .n D 597/, a questionnaire pertaining to the father completed by the father .n D 478/, and a questionnaire completed by either parent that collected data on the NDIT participant (n D 647, 64% of the 1,009 participants). Demographic data (age, sex, birth country, language most often spoken at home) were drawn from the child questionnaire; all other data were drawn from the parent questionnaire. All NDIT participants provided assent and their parents provided informed consent. The study was approved by the Montreal Department of Public Health Ethics Review Committee, the McGill University Institutional Review Board, and the Ethics Research Committee of the Centre de Recherche du Centre Hospitalier de l’Université de Montréal. Study Variables Data on disruptive behavior diagnoses and symptoms were drawn from the parent questionnaire. Diagnosed ADHD (yes, no) was measured by: “Was ‘NDIT participant’ ever diagnosed by a health professional with attention deficit hyperactivity disorder (ADHD)?” If yes, parents reported age at diagnosis and whether medication was prescribed. ADHD symptoms were measured using the attention problems scale of the Child Behavior Checklist (CBCL; Achenbach & Rescorla, 2001): “Do any of the following describe ‘NDIT participant’ either in elementary or high school: (i) frequently interrupted others; (ii) was easily distracted; (iii) often fidgeted or squirmed in seat; (iv) often did not listen when spoken to; (v) frequently avoided homework.” Response choices included “not at all like him/her,” “a bit like him/her,” and “a lot like him/her” and were scored 0, 1, and 2, respectively. Scores for each item were summed (range 0–10; median [IQR] D 1 [3]). If they scored 6, participants were categorized (yes, no) as having ADHD symptoms possibly indicative of a disorder. The attention problems scale of the CBCL has been reported to have excellent convergence with the diagnosis of ADHD based on structured interview (Biederman et al., 1993). Diagnosed behavioral problems (yes, no) were measured by: “Was ‘NDIT participant’ ever diagnosed by a health professional with behavioral problems (oppositional defiant disorder, conduct disorder)?” If yes, parents reported age at diagnosis. Data on conduct disorder symptoms were collected using the delinquent behavior scale of the CBCL: “Do any of the following describe ‘NDIT participant’ either in elementary or high school: (i) ran away from home overnight; (ii) often stole things or shoplifted; (iii) frequently skipped school; (iv) deliberately destroyed others’ property; (v) often started fights with neighbours, schoolmates; (vi) was physically cruel to animals; (vii) broke into a house or car; (viii) often did not want to go to school; (ix) frequently lied; (x) deliberately hurt others physically;
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and (xi) often bullied, threatened, or intimidated others?” Response choices included “not at all like him/her,” “a bit like him/her,” and “a lot like him/her” and scored 0, 1, and 2, respectively. Scores for each item were summed (scores from 0–22; median [IQR] D 0 [1]). If they scored 5 (i.e., child threshold), participants were categorized (yes, no) as having conduct disorder symptoms possibly indicative of a disorder. Since the questions were asked about both elementary and high school, we also categorized participants using the adolescent threshold ( 8). The delinquent behavior scale of the CBCL has been reported to have excellent convergence with the diagnosis of conduct disorder based on structured interview (Edelbrock & Costello, 1988). Parents indicated (yes, no, don’t know) if the NDIT participant had ever received services for learning or behavioral problems and if he or she had ever been held back in school (yes, no, don’t know). Sleep-disordered breathing was measured in the parent questionnaires by: “During childhood, how often (never, rarely, sometimes, often, don’t know) did ‘NDIT participant’ : : : (i) snore; (ii) snore very loudly; (iii) breathe forcefully or noisily while sleeping; (iv) have problems or difficulty breathing while sleeping; (v) stop breathing or wake up gasping for air while sleeping. For analysis, participants were categorized into one of four mutually exclusive categories: (a) no snoring or OSA symptoms; (b) snoring, that is, snores or snores very loudly sometimes or often, and responses to items (iii), (iv) and (v) were never or rarely; (c) possible OSA: participants had snoring and in addition, responded sometimes or often to items (iii), (iv) or (v); (d) this category included all remaining participants (i.e., those whose parents reported that child rarely snored or parents don’t know). Sleep-disordered breathing symptoms as reported on parental questionnaires correspond well with the presence of objectively determined sleep-disordered breathing symptoms, including snoring, supporting the accuracy and usefulness of parental reporting of sleep-disordered breathing symptoms in children (MontgomeryDowns, O’Brien, Holbrook, & Gozal, 2004). All of the sleep-disordered breathing items used in our study were similar to the items described in the Sleep Disordered Breathing Questions section of the validated instrument by Montgomery-Downs and colleagues, specifically (a) presence of snoring, (b) frequency of snoring, (c) loudness of snoring, (d) struggling to breathe while asleep, and (e) stop breathing during sleep (Montgomery-Downs et al., 2004). Data on participants’ age, sex, language spoken most often at home (French, other), and born in Canada (yes, no) were drawn from participants’ baseline questionnaires completed in grade 7. Data on parent’s age and mother’s education (i.e., completed university [yes, no]) were drawn from the parent questionnaire. Data Analysis Forty-two participants (7% of 647) whose parents indicated that they had been born prematurely at < 37 weeks gestation were excluded because of possible OSA comorbidity related to prematurity (Raynes-Greenow et al., 2012). Therefore the analytic sample included 605 participants. Odds ratios (OR) and their 95% confidence intervals (CIs) for the associations between history of sleep-disordered breathing and history of each of the study outcomes (i.e., diagnosed ADHD and/or ADHD symptoms, diagnosed behavioral problems or conduct disorder symptoms, received services for learning or behavioral problems, and ever held back in school) were estimated, one at a time, in univariate and multivariable logistic regression models. In the latter model, sex and mother’s education were included as potential confounders (Barkley, 1990;
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Moffitt & Caspi, 2001; Odgers et al., 2012; Rieppi et al., 2002; Silverthorn, & Frick, 1999; Silverthorn, Frick, & Reynolds, 2001; Tillman, & Granvald, 2014). Analyses were conducted using SPSS software, Version 16.0 (SPSS Inc., Chicago, IL).
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RESULTS Of 1,009 participants whose parents were mailed questionnaires, 647 (64%) returned a completed questionnaire pertaining to the NDIT participant. There were few important differences in baseline characteristics between participants whose parents completed the questionnaire and those whose parents did not (Table 1). Parents who completed the questionnaire pertaining to the NDIT participant (84% were the biologic mother) were aged 51 (SD D 7) years on average. Eighteen percent of boys and 9% of girls .p D 0:002/ had been diagnosed with ADHD by a health care professional and/or had ADHD symptoms (Table 2). The mean age at ADHD diagnosis was 10 .SD D 4/ years in boys, and 10 .SD D 5/ years in girls. The majority (77%) of children diagnosed with ADHD by a health care professional were reportedly diagnosed by age 10. A relatively high proportion of those diagnosed with ADHD (71% of boys and 82% of girls) had been prescribed medication for it. Nine percent (using the child threshold) and 5% (using the adolescent threshold) of participants had been diagnosed with behavioral problems or had conduct disorder symptoms (Table 2). There was no statistically significant difference in the proportion by sex. The mean age at diagnosis of behavioral problems was 11 years .SD D 4/ in boys, and 12 years .SD D 5/ in girls. Almost 60% of children diagnosed with behavioral problems/conduct disorder by a health care professional were reportedly diagnosed during adolescence (at age 13 to 19 years). The most frequently reported symptoms of sleep-disordered breathing were snoring (19%) and breathing forcefully or noisily while sleeping (sometimes or often; 14%). Lower proportions of participants snored very loudly (sometimes or often; 8%), had problems or difficulty breathing while sleeping (sometimes or often; 9%), and stopped breathing or woke up gasping for air while sleeping (sometimes or often; 2%). Ten percent of participants had symptoms
TABLE 1 Comparison of Baseline Characteristics of Participants Whose Parents Did and Did Not Complete the Parent Questionnaire Pertaining to the NDIT Participant (NDIT Study, Montreal, Canada, 1999–2010)
Age, y, mean (SD) Male, % French spoken at home, % Mother university-educated, %* Born in Canada, % Note.
Parent Completed Questionnaire (n D 647)
Parent Did Not Complete Questionnaire (n D 646)
p-value for Difference
12.7 (0.4) 46.7 32.1 45.7 95.8
12.9 (0.6) 49.7 28.0 42.2 88.4
