Psychiatry Research 228 (2015) 797–802
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Insomnia symptoms, behavioral/emotional problems, and suicidality among adolescents of insomniac and non-insomniac parents Xianchen Liu a,b,n, Zhongtang Zhao a, Cunxian Jia a a b
Department of Epidemiology & Health Statistics, Shandong University School of Public Health and Center for Suicide Prevention Research, Jinan, China The University of Tennessee Health Science Center, Memphis, TN 38163, USA
art ic l e i nf o
a b s t r a c t
Article history: Received 5 January 2015 Received in revised form 27 April 2015 Accepted 20 May 2015 Available online 30 May 2015
The aim of this study was to examine insomnia symptoms, behavioral problems, and suicidality among adolescents of insomniac parents (IP) and non-insomniac parents (NIP). A family survey of sleep and health was conducted among 1090 adolescents and their parents in Jinan, China. Adolescents completed a sleep and health questionnaire to report their sleep and mental health problems. Parents reported their insomnia symptoms and history of mental disorders. Insomnia, behavioral problems, and suicidal behavior were compared between IP adolescents and NIP adolescents. IP adolescents were more likely than NIP adolescents to report insomnia symptoms, use of sleep medication, suicidal ideation, suicide plan, and suicide attempt. IP adolescents scored significantly higher than NIP adolescents on withdrawn and externalizing behavioral problems. After adjustment for demographics and behavioral problems, parental insomnia remained to be significantly associated with adolescent suicidal ideation and suicide plan. Our findings support the need for early screening and formal assessment of sleep and mental health in adolescents of insomniac parents. & 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Insomnia Family study Behavioral/emotional problems Suicidality Adolescent
1. Introduction Sleep in adolescents is characterized by insufficient sleep, increased daytime sleepiness, and a tendency to develop irregular sleep patterns and sleep disturbances (Carskadon and Acebo, 2002; Liu et al., 2008; Gradisar et al., 2011). Sleep insufficiency and sleep problems influence child's school performance and mental health (Dahl and Lewin, 2002; Roberts et al., 2002). Sleep changes and sleep disturbances during adolescence are associated with multiple biological, developmental, psychological, socialcultural, familial, and school factors (Carskadon and Acebo, 2002; Dauvilliers et al., 2005; Owens, 2005). Although several studies have examined familial aggregation and genetic transmission of sleep behavior, sleep quality, and some sleep disorders (Partinen et al., 1983; Dauvilliers et al., 2005; Watson et al., 2006; Zhang et al., 2009; Wing et al., 2012), little is known about mental health problems and suicidal behavior among adolescents of parents with insomnia. Several twin studies have generally shown modest levels of genetic determination with heritability estimates in the range of
n Correspondence to: Shandong University Center for Suicide Prevention Research, No. 44, Wenhua Xi Road, Jinan, Shandong, 250012, China. E-mail address: [email protected] (X. Liu).
http://dx.doi.org/10.1016/j.psychres.2015.05.023 0165-1781/& 2015 Elsevier Ireland Ltd. All rights reserved.
20–57% for various aspects of sleep behaviors and symptoms, including sleep timing, morningness–eveningness, overall sleep quality, and polysomnographic (PSG) sleep parameters (Linkowski, 1999; Watson et al., 2006). In a recent family study of insomnia in 5695 school-aged children and 4939 parents, Zhang et al. (2009) reported a robust familial aggregation of insomnia. The authors found that the prevalence of insomnia significantly increased with parental insomnia status, from 3.0% for children of parents without insomnia, to 7.1% for those whose fathers alone had insomnia, 9.5% for those whose mothers alone had insomnia, and 11.9% for those whose parents both had insomnia. However, in this study, insomnia symptoms of children and parents were reported by parents only and that some important confounding factors such as present mental health status in children and parents were not measured. In another study of the similarities between adolescent and parent sleep patterns (n ¼293), sleep in mothers, but not fathers, was significantly correlated with adolescent sleep onset latency (Brand et al., 2009a). However, both parental and adolescent sleep was rated by adolescent children. Reporting of parental sleep may be biased by the adolescents' own mood and information processing. Sleep disorders in parents may not only relate to their offspring's sleep through genetic or non-genetic mechanisms, but may also have direct or indirect effects on child mental health (Bernert et al., 2007; Gregory et al., 2012). For example, parental
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X. Liu et al. / Psychiatry Research 228 (2015) 797–802
insomnia may increase the risk of their offspring's behavioral and emotional problems by genetic transmission of sleep problems as described above. The association between adolescent sleep problems and psychopathology, behavioral problems, and daily functioning in adolescents has been well established (Breslau et al., 1996; Liu and Zhou, 2002; Roberts et al., 2002; Buysse et al., 2008; Blank et al., 2015). Parental insomnia may also increase family stress and influence parenting functioning (Bernert et al., 2007; Gregory et al., 2012), which, in turn, increases risk of offspring's psychopathology. Furthermore, the risk of offspring's psychopathology could be increased due to the interaction of shared genetic and environmental factors associated with parental insomnia (Gehrman et al., 2011). However, little is known about sleep problems and psychopathology in the offspring of parents with insomnia. The current study addressed these aforementioned limitations by asking adolescents and parents to report their own sleep problems separately and examined insomnia symptoms, behavioral/emotional problems, and suicidal behavior among adolescent offspring of insomniac parents (IP) compared with those of non-insomniac parents (NIP).
2. Method 2.1. Participants This report represents part of an epidemiological project on sleep and adolescent health in three public middle school and three public high schools, conducted in March–April of 2005, in Jinan city, China. The sampling and procedure have been described elsewhere (Liu et al., 2008). Briefly, this study was designed to obtain a sample of approximately 1000 participants with about 500 7th graders and 500 10th graders. We restricted our participants to 7th and 10th graders in order to follow them for two years before graduation. After getting permission from the principals of the target schools before implementation of the study, we randomly selected 16 classes of 7th graders and 10 classes of 10th graders on the basis of the class sizes of the six target schools. All of the students in the target classes were recruited as potential participants.
2.2. Procedure Self-administered paper-and-pencil questionnaires were used to collect data on adolescent and parent sleep via the Adolescent Health Questionnaire (AHQ) and Parent and Family Questionnaire (PFQ). Adolescents were asked to complete the AHQ within one and half hours in the classroom setting during school days. Adolescents who returned the AHQ were asked to bring the PFQ to their parents to obtain parental sleep problems. One of the parents was invited to fill out the PFQ, either mother or father, chosen by the family. The PFQ asked about parent's sleep problems and history of mental disorders for both parents and was completed by the parent within 2 weeks. This procedure of data collection was approved by the Research Ethical Committee of Shandong University and target schools. Students and parents were invited to participate in the survey and their participation was voluntary without any penalties for nonparticipation. This is the most commonly used procedure to conduct school-based surveys in China (Liu et al., 2000, 2001).
2.3. Measures of sleep problems and behavioral/emotional problems in adolescents Adolescent sleep problems during the past month were assessed by the AHQ, which includes a set of items designed to elicit information about sleep, demographics, health history, lifestyles, and behavioral and emotional problems (Liu et al., 2008). Three items were used to evaluate insomnia: difficulty initiating sleep (DIS), difficulty maintaining sleep (DMS), and early morning awaking (EMA). Two items addressed use of sleep medication (“How often do you use prescribed/nonprescribed sleep pills?”). All of the problem items were answered with frequency responses of less than once per week, 1–2 times per week, 3–5 times per week, or almost every day. Insomnia symptom was considered clinically significant if the problem occurred at least three times a week. The internal consistency (Chronbach α) was 0.66 for sleep items with the current sample. The Youth Self-Report (YSR) of Child Behavior Checklist was used to measure adolescent behavioral problems (Achenbach, 1991). As a screening instrument, it has been applied widely in clinical assessment and research. It comprises 103 problem items to which the respondent can answer “0” if the problem is not true of him or herself, “1” if the item is somewhat or sometimes true, and “2” if it is very
true or often true. The participant was asked to score each item that describes him or her now or within the past six months. By summing 1 s and 2 s on all problem items, eight syndromes (withdrawn, somatic complaints, anxious/depressed, social problems, thought problems, attention problems, delinquent behavior, and aggressive behavior) and two second-order factors (internalizing and externalizing) can be assessed. The externalizing factor is made up of the aggressive behavior and delinquent behavior; the internalizing factor is made up of the anxious/depressed, withdrawn and somatic complaints. A Chinese version of the YSR was used in this study, which has been reported to have satisfactory reliability and validity (Liu et al., 1987, 2000). The Cronbach α was 0.77 for withdrawn, 0.82 for somatic complaints, 0.88 for anxious/depressed, 0.74 for social problems, 0.76 for thought problems, 0.80 for attention problems, 0.74 for delinquent behavior, and 0.88 aggressive behavior with the current sample. 2.4. Measures of insomnia and history of mental disorders in parents Sleep problems and history of mental disorders among parents were assessed by the PFQ. The parent was asked “Do you often have sleep problems, such as difficulty falling sleep, difficulty maintaining sleep, or early morning awakening?” and “Does your spouse often have sleep problems, such as difficulty falling sleep, difficulty maintaining sleep, or early morning awakening?” If the answer was “yes”, the father or mother was considered to have insomnia symptoms. Insomnia symptoms for fathers and mothers were recorded, separately (Liu et al., 2008). The parent was asked two questions about the history of mental disorders. “Have you/your spouse ever seen a doctor for mental health problems, such as mental disorders, alcohol abuse, or drug dependence?” “Have you/your spouse ever been hospitalized due to mental health problems, such as mental disorders, alcohol abuse, or drug dependence?” If the answer was “yes” for either question, the father or mother was considered to have mental health problems. Similar to insomnia questions, mother's and father's histories were recorded, separately. 2.5. Measure of suicidal and self-injury behavior The AHQ has four questions concerning suicidal and self-injury behavior, which were adapted from our previous survey (Liu et al., 2000; Liu and Tein, 2005) and Teen Health 2000 (Roberts et al., 1998). The first question represents suicidal ideation: “I have thought seriously about killing myself.” The second question indicates suicide plan: “I have had a plan to kill myself.” The third question indicates suicide attempts” “I have tried to kill myself.” The 4th question is to ask about self-injury: “I have deliberately tried to hurt myself.” All of the questions ask about adolescent suicidal behavior over the entire lifetime and have a “yes/no” answer. If a respondent answered “yes” on a question, he or she was considered to have the behavior. The Cronbach α was 0.69 for the suicidal items with the current sample. 2.6. Statistical analysis Chi-square tests or student t tests were performed to examine the differences between IP adolescents and NIP adolescent in terms of age, sex, and residence (rural vs. urban). Rural vs. urban residence was used to indicate social economic status of the adolescent's family as there were huge differences in family income, parental education, and parental occupation between rural and urban residents in China (Xie and Zhou, 2014). General linear models were performed to examine the differences of mean scores on behavioral/emotional problem scales between IP adolescents and NIP adolescents, adjusting for potential confounding effects of age, sex, residence, and insomnia symptoms in the adolescents. Logistic regression analyses were performed to examine the associations of parental insomnia symptoms with use of sleep medication, insomnia symptoms and suicidal behavior in the adolescents. Age, sex, residence, internalizing and externalizing problems in the adolescents were adjusted when examining the association between parental insomnia and adolescent insomnia symptoms and use of sleep medication. Age, sex, residence, insomnia symptoms, and internalizing and externalizing problems in the adolescents were adjusted when examining the association between parental insomnia symptoms and adolescent suicidal behavior. Odds ratios (ORs) and their 95% confidence intervals (CIs) were calculated to quantify these associations. All statistical analyses were performed using IBM SPSS Statistics for Windows, Version 20.0 (Armonk, NY: IBM Corp).
3. Results Of 1090 students who were asked to participate, 1066 (97.8%) returned AHQs and 838 (76.9%) had parent-completed PFQs. A total of 798 adolescents whose parents answered the questions about insomnia were included in this analysis, including 43 adolescents of insomniac parents (16 students of fathers, 24 students of mothers,
X. Liu et al. / Psychiatry Research 228 (2015) 797–802
and three students of both parents) and 755 adolescents of noninsomniac parents. Demographics of adolescents whose parents had or did not have insomnia symptoms are presented in Table 1. There were significant differences in grade (χ2 ¼4.90, po0.05) and residence (χ2 ¼8.29, po0.01). IP adolescents were more likely than NIP adolescents to be 7th graders and to live in urban areas. Only one IP adolescent and two NIP adolescents had a parental history of reported mental disorders.
3.1. Insomnia symptoms and use of sleep medication Table 2 presents prevalence rates of insomnia symptoms and use of sleep medication in adolescents of parents with or without insomnia symptoms. The prevalence rate of any insomnia symptom was significantly higher in IP adolescents than in NIP adolescents (27.8% vs. 14.2%, OR¼ 2.32, 95% CI ¼1.08–4.98), in particular for DIS (20.0% vs. 5.6%, OR ¼4.23, 95% CI ¼1.83–9.77). After adjusting for sex, age, residence, and internalizing and externalizing problems, the ORs had minor changes and remained significant. Use of sleep medication was more prevalent in IP adolescents than in NIP adolescents (7.9% vs. 2.0%, OR¼ 4.21, 95% CI ¼ 1.16– 15.32). After adjustment for sex, age, residence, and internalizing and externalizing problems, IP adolescents were still more likely than NIP adolescents to report use of sleep medication (OR ¼4.65, 95% CI ¼1.14–18.94) (Table 2). Table 1 Demographic characteristics of adolescents of parents who had or did not have insomnia symptoms.
Sex Male, % Female, % Grade 7th, % 10th, % Age, mean (S.D.) Residence Urban, % Rural, % n
Adolescents of insomniac parents (n¼ 43)
Adolescents of noninsomniac parents (n¼ 755)
χ2/ttest
51.2 48.8
56.7 43.3
0.51
69.8 30.2 14.42(1.47)
52.5 47.5 14.88(1.62)
4.90n
62.8 37.2
40.5 59.5
1.79
8.29nn
po 0.05. p o0.01.
nn
799
3.2. Behavioral/emotional problems Table 3 presents mean scores and standard deviations of YSR subscales for adolescents of parents with or without insomnia symptoms. All scale scores except Thought problems were rated higher in IP adolescents than in NIP adolescents. After adjustment for sex, age, residence, and adolescent insomnia symptoms, the mean scores on withdrawn (F(1, 792)¼ 5.77, p o0.05), delinquent behavior (F(1, 792)¼ 4.55, po0.05), aggressive behavior (F(1, 792) ¼ 4.17, p o0.05), and externalizing problems (F(1, 792)¼ 4.85, po 0.05) were significantly higher in IP adolescents than in NIP adolescents. 3.3. Suicidality As shown in Table 4, IP adolescents reported higher prevalence of suicidal behaviors and self-injury than NIP adolescents, including suicidal ideation (16.7% vs. 5.3%, OR ¼3.56, 95% CI ¼ 1.49–8.51), suicide plan (9.5% vs. 1.5%, OR¼ 7.10, 95% CI ¼2.16–23.34), suicide attempt (9.5% vs. 1.7%, OR¼ 1.87–19.25), and deliberate self-injury (16.7% vs. 6.5%,OR ¼2.87, 95 CI% ¼1.21–6.78). After adjustment for Table 3 Mean Youth Self Report scale scores (SD) among adolescents of parents who had or did not have insomnia symptoms.
Withdrawn Somatic complaints Anxious/ depressed Social problems Thought problems Attention problems Delinquent behavior Aggressive behavior Internalizing problems Externalizing problems
Adolescents of insomniac Adolescents of nonparents (n ¼43) insomniac parents (n¼ 755)
Fa
2.45 (2.92) 1.48 (1.92)
1.45 (2.05) 1.11 (2.26)
5.77n 0.10
4.53 (5.16)
2.89 (4.20)
2.59
2.18 (2.59)
1.51 (2.10)
1.31
0.98 (1.80)
1.00 (1.74)
0.03
3.10 (2.86)
2.44 (2.88)
0.92
2.08 (3.03)
1.22 (2.02)
4.55n
5.55 (5.27)
3.65 (4.46)
4.17n
8.13 (8.54)
5.22 (7.27)
2.37
7.63 (7.88)
4.85 (6.09)
4.85n
a General linear model, adjusting for sex, age, residence, and insomnia symptoms in adolescents. n p o 0.05.
Table 2 Insomnia symptoms and use of sleep medication among adolescents of parents who had or did not have insomnia symptoms. % Adolescents of insomniac parents (n ¼43) % Adolescents of non-insomniac parents (n¼ 755) Odd ratio (95% CI) Unadjusted Insomnia symptomsa Difficulty initiating sleep Difficulty maintaining sleep Early morning awaking Any Use of sleep medicationb **
20.0 5.6
5.6 2.1
7.9 27.8 7.9
3.1 14.2 2.0
p o 0.01. a
At least 3 times a week. At least once a week. c Adjusted for sex, age, residence, internalizing problems, and externalizing problems. n po 0.05. nnn p o 0.001. b
Adjustedc
4.23*** (1.83–9.77) 4.34*** (1.77–10.66) 2.81 (0.61–12.93) 3.55 (0.71–17.73) 2.70 (0.77–9.44) 2.32* (1.08–4.98) 4.21* (1.16–15.32)
2.14 (0.56–8.22) 2.56* (1.12–5.88) 4.65* (1.14–18.94)
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Table 4 Suicidal behavior among adolescents of parents who had or did not have insomnia symptoms. % Adolescents of insomniac parents (n¼ 43)
Suicidal ideation Suicide plan Suicide attempt Deliberate self-injury
16.7 9.5 9.5 16.7
% Adolescents of non-insomniac parents (n¼ 755)
5.3 1.5 1.7 6.5
Odd ratio (95% CI) Unadjusted
Adjusteda
3.56** 7.10*** 5.99*** 2.87*
3.23* 6.96* 3.91 1.58
(1.49–8.51) (2.16–23.34) (1.87–19.25) (1.21–6.78)
(1.16–9.02) (1.36–35.76) (0.91–16.78) (0.55–4.51)
a
Adjusted for sex, grade, residence, insomnia, and internalizing and externalizing problems. po 0.05. nn p o0.01. nnn p o0.001. n
sex, age, residence, insomnia symptoms, and internalizing and externalizing problems in the adolescents, parental insomnia was still significantly associated with increased risk for suicidal ideation (OR ¼3.23, 95% CI ¼1.16–9.02) and suicide plan (OR ¼6.96, 95% CI ¼1.36–35.76) (Table 4).
4. Discussion Insomnia is a known risk factor for mental disorders, but whether this risk extends to the mental health of offspring of parents with insomnia is unknown. To our knowledge, this is the first study to comprehensively examine insomnia symptoms, behavioral/emotional problems, and suicidal behavior among adolescent offspring of insomniac parents compared with those of non-insomniac parents. Our major findings are summarized below. First, compared with NIP adolescents, IP adolescents were more likely to report insomnia symptoms (OR ¼2.6) and use of sleep medication (OR¼ 4.7). IP adolescents had more internalizing and externalizing behavioral problems than NIP adolescents. Furthermore, parental insomnia symptoms were associated with increased risk for adolescent suicidal ideation (OR ¼3.2) and suicide plan (OR ¼7.0) after adjustment for age, sex, residence, insomnia symptoms, and internalizing and externalizing problems in the adolescents. The prevalence of insomnia symptoms among adolescent offspring of insomniac parents was significantly increased. After controlling for the potential confounding effects of demographics and internalizing and externalizing behavioral problems, PI adolescents were 2.6-fold more likely than NIP adolescents to report any insomnia symptoms, suggesting that it was unlikely that parent-offspring associations could be explained by demographic factors and present mental health status. These findings support recent genetic epidemiological studies that have demonstrated a modest familial aggregation and genetic transmission of sleep behavior (Partinen et al., 1983; Dauvilliers et al., 2005) and significant genetic effects on insomnia (Bastien and Morin, 2000; Zhang et al., 2009; Gehrman et al., 2011; Wing et al., 2012). Parental sleep problems may also exert negative impact on child's sleep indirectly via poor family environment and poor family functioning and parental style as a result of parental insomnia (Bernert et al., 2007; Brand et al., 2009a, 2009b; Gregory et al., 2012). Further familial/genetic studies are needed to examine whether and the extent to which the parent-adolescent association of insomnia is determined by family environment, genetic effect, or the interaction of both. Sleep disorders in parents may not only have a negative impact on their offspring's sleep, but also exert negative impacts on mental health directly and/or indirectly (Bernert et al., 2007; Gregory et al., 2012). In the current study, we found that all behavioral/emotional problem scale scores except Thought problems
were rated higher in IP adolescents than in NIP adolescents. After adjustment for sex, age, residence, insomnia symptoms in the adolescents, the mean scores on withdrawn, delinquent behavior, aggressive behavior, and externalizing problems were still significantly higher in IP adolescents than in NIP adolescents. These findings suggest that parental insomnia symptoms may exert negative impact on a range of internalizing and externalizing behavior problems among adolescent offspring, independent of genetic transmission of insomnia. Although further studies are warranted, the association of parental insomnia with both internalizing (withdrawn) and externalizing problems may have two explanations. First, internalizing and externalizing problems are highly correlated in childhood and adolescents (Achenbach, 1991; Liu et al., 2001). Second, the impact of parental insomnia on internalizing and externalizing problems may share similar mechanisms as described below. The impact of parental insomnia on adolescent psychopathology may be due to genetic and environmental effects or the interaction of both. First, parental insomnia is associated with increased risk for offspring sleep problems genetically (Partinen et al., 1983; Zhang et al., 2009; Dauvilliers et al., 2005; Wing et al., 2012), which in turn increase risk for psychopathology, such as depression and aggressive problems in children and adolescents. Children with sleep disorders such as insomnia have been observed to be at increased risk for neurobehavioral problems such as impairments in cognition, mood, attention, and behavior (Dahl and Lewin, 2002; Roberts et al., 2002) and internalizing and externalizing behavioral problems (Liu and Zhou, 2002). Second, parental insomnia may cause family stress and negatively influence parenting functioning and family interactions, all of which are in turn associated with increased risk for g poor sleep and psychopathology in adolescent offspring (Bernert et al., 2007; Brand et al., 2009a, 2009b; Gregory et al., 2012). Several studies have shown that family life stress or negative family life events were significantly associated with increased risk of insomnia symptoms, even after controlling for depression (Liu and Tein, 2005; Bernert et al., 2007). A number of studies have documented the association between parent functioning and a range of childhood problems, including internalizing and externalizing behavior problems and sleep disturbances (Obradović and Hipwell, 2010; Rhoades et al., 2012; Schoenfelder et al., 2015). In a recent study of similarities in sleep patterns between adolescents and parents, Brand et al. (2009b) concluded that mother's poor sleep has a direct impact on parenting style, which in turn affects adolescents' psychological functioning and sleep. Finally, insomnia in the parents may be accompanied by psychopathology in the parents (Liu et al., 2007; Buysse, 2013). Thus, the elevated psychopathology in adolescents may be a genetic/ environmental result of parental psychopathology, and insomnia is simply the symptom of the parental pathology that we measured. In the current study, we found that IP adolescents reported much higher prevalence of suicidal behaviors and self-injury than NIP adolescents. The increased suicidal risk may be due to increased
X. Liu et al. / Psychiatry Research 228 (2015) 797–802
sleep problems and behavioral/emotional problems in adolescent offspring of parents with insomnia. It is well known that internalizing and externalizing problems are associated with increased risk for suicidality in adolescents (Liu et al., 2005; Kelleher et al., 2012). Recent studies have demonstrated that short sleep duration and sleep problems including insomnia are associated with suicidal behavior (Liu and Buysse, 2006; Pigeon et al., 2012; Bernert et al., 2014). After adjustment for sex, age, residence, insomnia symptoms, and internalizing and externalizing problems in the adolescents, parental insomnia was still significantly associated with 3-fold increased risk for suicidal ideation and 7-fold increased risk for suicide plan. This finding suggests that suicidal behavior in adolescents of insomniac parents could not be entirely attributed to adolescent mental health status and insomnia due to genetic transmission. It would be important to further examine the biological mechanisms and potential psychological pathways between parental insomnia and adolescent suicidal risk. Several limitations should be considered in the interpretation of our results. First, the present study was limited by our reliance on self-report questionnaires, particularly in the measurement of insomnia symptoms. For example, parental insomnia was simply asked using one single question (i.e., “Do you often have…? and “Does your spouse often have…?”) and only one parent was asked to answer the question for both parents. This may be why the prevalence rate of insomnia was markedly lower in this sample of parents than those in most previous adult studies using several questions to ask insomnia symptoms like DIS, DMS, and EMA separately or studies using clinical interviews (Ohayon and Smirne, 2002; Buysse, 2013). Parents who reported a history of insomnia may represent a group of individuals with severe and chronic insomnia. The association of insomnia between parents and adolescent offspring or the familial aggregation of insomnia may be underestimated (Wing et al., 2012). Second, because the small number of parents with insomnia, we did not have enough statistical power to distinguish the paternal and maternal effects although the impact of paternal and maternal sleep on adolescent sleep and psychopathology may differ (Brand et al., 2009a; Zhang et al., 2009; Wing et al., 2012). Third, we did not include psychiatric history of parents in the statistical analysis due to the fact that only one IP adolescent and two NIP adolescents had a parental history of reported mental disorders. However, the association between parental insomnia and adolescent suicidal behavior is less likely to be explained by genetic transmission of parental psychiatric disorders as the association remained significant after adjustment for adolescent internalizing and externalizing behavior problems and insomnia in the adolescents. Furthermore, no causality of parental insomnia and adolescent offspring's psychopathology and suicidality can be made from the cross-sectional study. In conclusion, this is the first study to examine the impact of parental insomnia on adolescent insomnia symptoms, behavioral/ emotional problems, and suicidal behavior. Parental insomnia symptoms are not only associated with elevated risk for insomnia but also with elevated risks for use of sleep medication, a range of internalizing and externalizing behavior problems and suicidal behavior in adolescent offspring. Our findings support the need for early screening and formal assessment of sleep and mental health in adolescents of parents with insomnia. It is possible, although unproven at this time, that family interventions to enhance sleep quality could attenuate risk for the development of sleep disturbances, psychopathology, and suicidal behavior in adolescent offspring of parents with insomnia.
Acknowledgments This study was supported in part by the Multi-Investigator Proposal Development Grant Program, Arizona State University.
801
The authors thank all participating teachers, parents and students, and Dr. Daniel Buysse, Professor of Psychiatry, University of Pittsburgh School of Medicine, for his insightful comments on an early draft of the manuscript. All authors reported no financial interests or potential conflicts of interest related to the study.
References Achenbach, T.M., 1991. Manual for the Youth Self-Report and 1991 Profile. Department of Psychiatry, University of Vermont, Burlington, VT. Bastien, C.H., Morin, C.M., 2000. Familial incidence of insomnia. Journal of Sleep Research 9, 49–54. Bernert, R.A., Merrill, K.A., Braithwaite, S.R., Van Orden, K.A., Joiner, T.E., 2007. Family life stress and insomnia symptoms in a prospective evaluation of young adults. Journal of Family Psychology 21, 58–66. Bernert, R.A., Turvey, C.L., Conwell, Y., Joiner, T.E., 2014. Association of poor subjective sleep quality with risk for death by suicide during a 10-year period: a longitudinal, population-based study of late life. JAMA Psychiatry 71, 1129–1137. Blank, M., Zhang, J., Lamers, F., Taylor, A.D., Hickie, I.B., Merikangas, K.R., 2015. Health correlates of insomnia symptoms and comorbid mental disorders in a nationally representative sample of US adolescents. Sleep 38, 197–204. Brand, S., Gerber, M., Hatzinger, M., Beck, J., Holsboer-Trachsler, E., 2009a. Evidence for similarities between adolescents and parents in sleep patterns. Sleep Medicine 10, 1124–1131. Brand, S., Hatzinger, M., Beck, J., Holsboer-Trachsler, E., 2009b. Perceived parenting styles, personality traits and sleep patterns in adolescents. Journal of Adolescence 32, 1189–1207. Breslau, N., Roth, T., Rosenthal, L., Andreski, P., 1996. Sleep disturbance and psychiatric disorders: a longitudinal epidemiological study of young adults. Biological Psychiatry 39, 411–418. Buysse, D.J., 2013. Insomnia. The Journal of the American Medical Association 309, 706–716. Buysse, D.J., Angst, J., Gamma, A., Ajdacic, V., Eich, D., Rössler, W., 2008. Prevalence, course, and comorbidity of insomnia and depression in young adults. Sleep 31, 473–480. Carskadon, M.A., Acebo, C., 2002. Regulation of sleepiness in adolescents: update, insights, and speculation. Sleep 15, 606–614. Dahl, R.E., Lewin, D.S., 2002. Pathways to adolescent health: sleep regulation and behavior. Journal of Adolescence Health 31, 175–184. Dauvilliers, Y., Maret, S., Tafti, M., 2005. Genetics of normal and pathological sleep in humans. Sleep Medicine Review 9, 91–100. Gehrman, P.R., Meltzer, L.J., Moore, M., Pack, A.I., Perlis, M.L., Eaves, L.J., Silberg, J.L., 2011. Heritability of insomnia symptoms in youth and their relationship to depression and anxiety. Sleep 34, 1641–1646. Gregory, A.M., Moffitt, T.E., Ambler, A., Arseneault, L., Houts, R.M., Caspi, A., 2012. Maternal insomnia and children's family socialization environments. Sleep 35, 579–582. Gradisar, M., Gardner, G., Dohnt, H., 2011. Recent worldwide sleep patterns and problems during adolescence: a review and meta-analysis of age, region, and sleep. Sleep Medicine 12, 110–118. Kelleher, I., Lynch, F., Harley, M., Molloy, C., Roddy, S., Fitzpatrick, C., Cannon, M., 2012. Psychotic symptoms in adolescence index risk for suicidal behavior: findings from 2 population-based case-control clinical interview studies. Achieves of General Psychiatry 29, 1–7. Linkowski, P., 1999. EEG sleep patterns in twins. Journal of Sleep Research 8 (Suppl 1), S 11–S 13. Liu, X.C., Buysse, D.J., 2006. Sleep and youth suicidal behavior: a neglected field. Current Opinion in Psychiatry 19, 288–293. Liu, X.C., Buysse, D.J., Gentzler, A.L., Kiss, E., Mayer, L., Kapornai, K., Vetró, A., Kovacs, M., 2007. Insomnia and hypersomnia associated with depressive phenomenology and comorbidity in childhood depression. Sleep 30, 83–90. Liu, X.C., Guo, C.Q., Liu, L.Q., Sun, L.M., 1987. Reliability and validity of the youth self report in Chinese adolescents. Chinese Journal of Mental Health 11, 200–203. Liu, X.C., Kurita, H., Uchiyama, M., Okawa, M., Liu, L.Q., Ma, D.D., 2000. Life events, locus of control and behavioral problems among Chinese adolescents. Journal of Clinical Psychology 56, 1565–1577. Liu, X.C., Sun, Z., Neiderhiser, J.M., Uchiyama, M., Okawa, M., Rogan, W., 2001. Behavioral and emotional problems in Chinese adolescents: parent and teacher reports. Journal of the American Academy of Child & Adolescent Psychiatry 40, 828–836. Liu, X.C., Tein, J.Y., Sandler, I., Zhao, Z.T., 2005. Psychopathology associated with suicide attempts among rural adolescents of China. Suicide and LifeThreatening Behavior 35, 265–276. Liu, X.C., Tein, J.Y., 2005. Life events, psychopathology, and suicidal behavior in Chinese adolescents. Journal of Affective Disorders 86, 195–203. Liu, X.C., Zhao, Z.T., Jia, C.X., Buysse, D.J., 2008. Sleep patterns and disturbances among Chinese adolescents: associations with parental sleep. Pediatrics 121, 1165–1173. Liu, X.C., Zhou, H.B., 2002. Sleep duration, insomnia and behavioral problems among Chinese adolescents. Psychiatry Research 111, 75–85.
802
X. Liu et al. / Psychiatry Research 228 (2015) 797–802
Obradović, J., Hipwell, A., 2010. Psychopathology and social competence during the transition to adolescence: the role of family adversity and pubertal development. Developmental Psychopathology 22, 621–634. Ohayon, M.M., Smirne, S., 2002. Prevalence and consequences of insomnia disorders in the general population of Italy. Sleep Medicine 3, 115–120. Owens, J.A., 2005. Introduction: culture and sleep in children. Pediatrics 115 (1 Suppl), S 201–S 203. Partinen, M., Kaprio, J., Koskenvuo, M., Putkonen, P., Langinvainio, H., 1983. Genetic and environmental determination of human sleep. Sleep 6, 179–185. Pigeon, W.R., Pinquart, M., Conner, K., 2012. Meta-analysis of sleep disturbance and suicidal thoughts and behaviors. Journal of Clinical Psychiatry 73, e1160–1167. Rhoades, K.A., Leve, L.D., Harold, G.T., Mannering, A.M., Neiderhiser, J.M., Shaw, D.S., Natsuaki, M.N., Reiss, D., 2012. Marital hostility and child sleep problems: direct and indirect associations via hostile parenting. Journal of Family Psychology 26, 488–498. Roberts, R.E., Roberts, C.R., Chen, I.G., 2002. Impact of insomnia on future functioning of adolescents. Journal of Psychosomatic Research 53, 561–569.
Roberts, R.E., Roberts, C.R., Chen, Y.R., 1998. Suicidal thinking among adolescents with a history of attempted suicide. Journal of the American Academy of Child & Adolescent Psychiatry 37, 1294–1300. Schoenfelder, E.N., Tein, J.Y., Wolchik, S., Sandler, I.N., 2015. Effects of the family bereavement program on academic outcomes, educational expectations and job aspirations 6 years later: the mediating role of parenting and youth mental health problems. Journal of Abnormal Child Psychology 43, 229–241. Watson, N.F., Goldberg, J., Arguelles, L., Buchwald, D., 2006. Genetic and environmental influences on insomnia, daytime sleepiness, and obesity in twins. Sleep 29, 645–649. Wing, Y.K., Zhang, J., Lam, S.P., Li, S.X., Tang, N.L., Lai, K.Y., Li, A.M., 2012. Familial aggregation and heritability of insomnia in a community-based study. Sleep Medicine 13, 985–990. Xie, Y., Zhou, X., 2014. Income inequality in today's China. Proceedings of the National Academy of Sciences of the United States of America 111, 6928–6933. Zhang, J., Li, A.M., Kong, A.P., Lai, K.Y., Tang, N.L., Wing, Y.K., 2009. A communitybased study of insomnia in Hong Kong Chinese children: prevalence, risk factors and familial aggregation. Sleep Medicine 10, 1040–1046.
Contents lists available at ScienceDirect
Psychiatry Research journal homepage: www.elsevier.com/locate/psychres
Insomnia symptoms, behavioral/emotional problems, and suicidality among adolescents of insomniac and non-insomniac parents Xianchen Liu a,b,n, Zhongtang Zhao a, Cunxian Jia a a b
Department of Epidemiology & Health Statistics, Shandong University School of Public Health and Center for Suicide Prevention Research, Jinan, China The University of Tennessee Health Science Center, Memphis, TN 38163, USA
art ic l e i nf o
a b s t r a c t
Article history: Received 5 January 2015 Received in revised form 27 April 2015 Accepted 20 May 2015 Available online 30 May 2015
The aim of this study was to examine insomnia symptoms, behavioral problems, and suicidality among adolescents of insomniac parents (IP) and non-insomniac parents (NIP). A family survey of sleep and health was conducted among 1090 adolescents and their parents in Jinan, China. Adolescents completed a sleep and health questionnaire to report their sleep and mental health problems. Parents reported their insomnia symptoms and history of mental disorders. Insomnia, behavioral problems, and suicidal behavior were compared between IP adolescents and NIP adolescents. IP adolescents were more likely than NIP adolescents to report insomnia symptoms, use of sleep medication, suicidal ideation, suicide plan, and suicide attempt. IP adolescents scored significantly higher than NIP adolescents on withdrawn and externalizing behavioral problems. After adjustment for demographics and behavioral problems, parental insomnia remained to be significantly associated with adolescent suicidal ideation and suicide plan. Our findings support the need for early screening and formal assessment of sleep and mental health in adolescents of insomniac parents. & 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Insomnia Family study Behavioral/emotional problems Suicidality Adolescent
1. Introduction Sleep in adolescents is characterized by insufficient sleep, increased daytime sleepiness, and a tendency to develop irregular sleep patterns and sleep disturbances (Carskadon and Acebo, 2002; Liu et al., 2008; Gradisar et al., 2011). Sleep insufficiency and sleep problems influence child's school performance and mental health (Dahl and Lewin, 2002; Roberts et al., 2002). Sleep changes and sleep disturbances during adolescence are associated with multiple biological, developmental, psychological, socialcultural, familial, and school factors (Carskadon and Acebo, 2002; Dauvilliers et al., 2005; Owens, 2005). Although several studies have examined familial aggregation and genetic transmission of sleep behavior, sleep quality, and some sleep disorders (Partinen et al., 1983; Dauvilliers et al., 2005; Watson et al., 2006; Zhang et al., 2009; Wing et al., 2012), little is known about mental health problems and suicidal behavior among adolescents of parents with insomnia. Several twin studies have generally shown modest levels of genetic determination with heritability estimates in the range of
n Correspondence to: Shandong University Center for Suicide Prevention Research, No. 44, Wenhua Xi Road, Jinan, Shandong, 250012, China. E-mail address: [email protected] (X. Liu).
http://dx.doi.org/10.1016/j.psychres.2015.05.023 0165-1781/& 2015 Elsevier Ireland Ltd. All rights reserved.
20–57% for various aspects of sleep behaviors and symptoms, including sleep timing, morningness–eveningness, overall sleep quality, and polysomnographic (PSG) sleep parameters (Linkowski, 1999; Watson et al., 2006). In a recent family study of insomnia in 5695 school-aged children and 4939 parents, Zhang et al. (2009) reported a robust familial aggregation of insomnia. The authors found that the prevalence of insomnia significantly increased with parental insomnia status, from 3.0% for children of parents without insomnia, to 7.1% for those whose fathers alone had insomnia, 9.5% for those whose mothers alone had insomnia, and 11.9% for those whose parents both had insomnia. However, in this study, insomnia symptoms of children and parents were reported by parents only and that some important confounding factors such as present mental health status in children and parents were not measured. In another study of the similarities between adolescent and parent sleep patterns (n ¼293), sleep in mothers, but not fathers, was significantly correlated with adolescent sleep onset latency (Brand et al., 2009a). However, both parental and adolescent sleep was rated by adolescent children. Reporting of parental sleep may be biased by the adolescents' own mood and information processing. Sleep disorders in parents may not only relate to their offspring's sleep through genetic or non-genetic mechanisms, but may also have direct or indirect effects on child mental health (Bernert et al., 2007; Gregory et al., 2012). For example, parental
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insomnia may increase the risk of their offspring's behavioral and emotional problems by genetic transmission of sleep problems as described above. The association between adolescent sleep problems and psychopathology, behavioral problems, and daily functioning in adolescents has been well established (Breslau et al., 1996; Liu and Zhou, 2002; Roberts et al., 2002; Buysse et al., 2008; Blank et al., 2015). Parental insomnia may also increase family stress and influence parenting functioning (Bernert et al., 2007; Gregory et al., 2012), which, in turn, increases risk of offspring's psychopathology. Furthermore, the risk of offspring's psychopathology could be increased due to the interaction of shared genetic and environmental factors associated with parental insomnia (Gehrman et al., 2011). However, little is known about sleep problems and psychopathology in the offspring of parents with insomnia. The current study addressed these aforementioned limitations by asking adolescents and parents to report their own sleep problems separately and examined insomnia symptoms, behavioral/emotional problems, and suicidal behavior among adolescent offspring of insomniac parents (IP) compared with those of non-insomniac parents (NIP).
2. Method 2.1. Participants This report represents part of an epidemiological project on sleep and adolescent health in three public middle school and three public high schools, conducted in March–April of 2005, in Jinan city, China. The sampling and procedure have been described elsewhere (Liu et al., 2008). Briefly, this study was designed to obtain a sample of approximately 1000 participants with about 500 7th graders and 500 10th graders. We restricted our participants to 7th and 10th graders in order to follow them for two years before graduation. After getting permission from the principals of the target schools before implementation of the study, we randomly selected 16 classes of 7th graders and 10 classes of 10th graders on the basis of the class sizes of the six target schools. All of the students in the target classes were recruited as potential participants.
2.2. Procedure Self-administered paper-and-pencil questionnaires were used to collect data on adolescent and parent sleep via the Adolescent Health Questionnaire (AHQ) and Parent and Family Questionnaire (PFQ). Adolescents were asked to complete the AHQ within one and half hours in the classroom setting during school days. Adolescents who returned the AHQ were asked to bring the PFQ to their parents to obtain parental sleep problems. One of the parents was invited to fill out the PFQ, either mother or father, chosen by the family. The PFQ asked about parent's sleep problems and history of mental disorders for both parents and was completed by the parent within 2 weeks. This procedure of data collection was approved by the Research Ethical Committee of Shandong University and target schools. Students and parents were invited to participate in the survey and their participation was voluntary without any penalties for nonparticipation. This is the most commonly used procedure to conduct school-based surveys in China (Liu et al., 2000, 2001).
2.3. Measures of sleep problems and behavioral/emotional problems in adolescents Adolescent sleep problems during the past month were assessed by the AHQ, which includes a set of items designed to elicit information about sleep, demographics, health history, lifestyles, and behavioral and emotional problems (Liu et al., 2008). Three items were used to evaluate insomnia: difficulty initiating sleep (DIS), difficulty maintaining sleep (DMS), and early morning awaking (EMA). Two items addressed use of sleep medication (“How often do you use prescribed/nonprescribed sleep pills?”). All of the problem items were answered with frequency responses of less than once per week, 1–2 times per week, 3–5 times per week, or almost every day. Insomnia symptom was considered clinically significant if the problem occurred at least three times a week. The internal consistency (Chronbach α) was 0.66 for sleep items with the current sample. The Youth Self-Report (YSR) of Child Behavior Checklist was used to measure adolescent behavioral problems (Achenbach, 1991). As a screening instrument, it has been applied widely in clinical assessment and research. It comprises 103 problem items to which the respondent can answer “0” if the problem is not true of him or herself, “1” if the item is somewhat or sometimes true, and “2” if it is very
true or often true. The participant was asked to score each item that describes him or her now or within the past six months. By summing 1 s and 2 s on all problem items, eight syndromes (withdrawn, somatic complaints, anxious/depressed, social problems, thought problems, attention problems, delinquent behavior, and aggressive behavior) and two second-order factors (internalizing and externalizing) can be assessed. The externalizing factor is made up of the aggressive behavior and delinquent behavior; the internalizing factor is made up of the anxious/depressed, withdrawn and somatic complaints. A Chinese version of the YSR was used in this study, which has been reported to have satisfactory reliability and validity (Liu et al., 1987, 2000). The Cronbach α was 0.77 for withdrawn, 0.82 for somatic complaints, 0.88 for anxious/depressed, 0.74 for social problems, 0.76 for thought problems, 0.80 for attention problems, 0.74 for delinquent behavior, and 0.88 aggressive behavior with the current sample. 2.4. Measures of insomnia and history of mental disorders in parents Sleep problems and history of mental disorders among parents were assessed by the PFQ. The parent was asked “Do you often have sleep problems, such as difficulty falling sleep, difficulty maintaining sleep, or early morning awakening?” and “Does your spouse often have sleep problems, such as difficulty falling sleep, difficulty maintaining sleep, or early morning awakening?” If the answer was “yes”, the father or mother was considered to have insomnia symptoms. Insomnia symptoms for fathers and mothers were recorded, separately (Liu et al., 2008). The parent was asked two questions about the history of mental disorders. “Have you/your spouse ever seen a doctor for mental health problems, such as mental disorders, alcohol abuse, or drug dependence?” “Have you/your spouse ever been hospitalized due to mental health problems, such as mental disorders, alcohol abuse, or drug dependence?” If the answer was “yes” for either question, the father or mother was considered to have mental health problems. Similar to insomnia questions, mother's and father's histories were recorded, separately. 2.5. Measure of suicidal and self-injury behavior The AHQ has four questions concerning suicidal and self-injury behavior, which were adapted from our previous survey (Liu et al., 2000; Liu and Tein, 2005) and Teen Health 2000 (Roberts et al., 1998). The first question represents suicidal ideation: “I have thought seriously about killing myself.” The second question indicates suicide plan: “I have had a plan to kill myself.” The third question indicates suicide attempts” “I have tried to kill myself.” The 4th question is to ask about self-injury: “I have deliberately tried to hurt myself.” All of the questions ask about adolescent suicidal behavior over the entire lifetime and have a “yes/no” answer. If a respondent answered “yes” on a question, he or she was considered to have the behavior. The Cronbach α was 0.69 for the suicidal items with the current sample. 2.6. Statistical analysis Chi-square tests or student t tests were performed to examine the differences between IP adolescents and NIP adolescent in terms of age, sex, and residence (rural vs. urban). Rural vs. urban residence was used to indicate social economic status of the adolescent's family as there were huge differences in family income, parental education, and parental occupation between rural and urban residents in China (Xie and Zhou, 2014). General linear models were performed to examine the differences of mean scores on behavioral/emotional problem scales between IP adolescents and NIP adolescents, adjusting for potential confounding effects of age, sex, residence, and insomnia symptoms in the adolescents. Logistic regression analyses were performed to examine the associations of parental insomnia symptoms with use of sleep medication, insomnia symptoms and suicidal behavior in the adolescents. Age, sex, residence, internalizing and externalizing problems in the adolescents were adjusted when examining the association between parental insomnia and adolescent insomnia symptoms and use of sleep medication. Age, sex, residence, insomnia symptoms, and internalizing and externalizing problems in the adolescents were adjusted when examining the association between parental insomnia symptoms and adolescent suicidal behavior. Odds ratios (ORs) and their 95% confidence intervals (CIs) were calculated to quantify these associations. All statistical analyses were performed using IBM SPSS Statistics for Windows, Version 20.0 (Armonk, NY: IBM Corp).
3. Results Of 1090 students who were asked to participate, 1066 (97.8%) returned AHQs and 838 (76.9%) had parent-completed PFQs. A total of 798 adolescents whose parents answered the questions about insomnia were included in this analysis, including 43 adolescents of insomniac parents (16 students of fathers, 24 students of mothers,
X. Liu et al. / Psychiatry Research 228 (2015) 797–802
and three students of both parents) and 755 adolescents of noninsomniac parents. Demographics of adolescents whose parents had or did not have insomnia symptoms are presented in Table 1. There were significant differences in grade (χ2 ¼4.90, po0.05) and residence (χ2 ¼8.29, po0.01). IP adolescents were more likely than NIP adolescents to be 7th graders and to live in urban areas. Only one IP adolescent and two NIP adolescents had a parental history of reported mental disorders.
3.1. Insomnia symptoms and use of sleep medication Table 2 presents prevalence rates of insomnia symptoms and use of sleep medication in adolescents of parents with or without insomnia symptoms. The prevalence rate of any insomnia symptom was significantly higher in IP adolescents than in NIP adolescents (27.8% vs. 14.2%, OR¼ 2.32, 95% CI ¼1.08–4.98), in particular for DIS (20.0% vs. 5.6%, OR ¼4.23, 95% CI ¼1.83–9.77). After adjusting for sex, age, residence, and internalizing and externalizing problems, the ORs had minor changes and remained significant. Use of sleep medication was more prevalent in IP adolescents than in NIP adolescents (7.9% vs. 2.0%, OR¼ 4.21, 95% CI ¼ 1.16– 15.32). After adjustment for sex, age, residence, and internalizing and externalizing problems, IP adolescents were still more likely than NIP adolescents to report use of sleep medication (OR ¼4.65, 95% CI ¼1.14–18.94) (Table 2). Table 1 Demographic characteristics of adolescents of parents who had or did not have insomnia symptoms.
Sex Male, % Female, % Grade 7th, % 10th, % Age, mean (S.D.) Residence Urban, % Rural, % n
Adolescents of insomniac parents (n¼ 43)
Adolescents of noninsomniac parents (n¼ 755)
χ2/ttest
51.2 48.8
56.7 43.3
0.51
69.8 30.2 14.42(1.47)
52.5 47.5 14.88(1.62)
4.90n
62.8 37.2
40.5 59.5
1.79
8.29nn
po 0.05. p o0.01.
nn
799
3.2. Behavioral/emotional problems Table 3 presents mean scores and standard deviations of YSR subscales for adolescents of parents with or without insomnia symptoms. All scale scores except Thought problems were rated higher in IP adolescents than in NIP adolescents. After adjustment for sex, age, residence, and adolescent insomnia symptoms, the mean scores on withdrawn (F(1, 792)¼ 5.77, p o0.05), delinquent behavior (F(1, 792)¼ 4.55, po0.05), aggressive behavior (F(1, 792) ¼ 4.17, p o0.05), and externalizing problems (F(1, 792)¼ 4.85, po 0.05) were significantly higher in IP adolescents than in NIP adolescents. 3.3. Suicidality As shown in Table 4, IP adolescents reported higher prevalence of suicidal behaviors and self-injury than NIP adolescents, including suicidal ideation (16.7% vs. 5.3%, OR ¼3.56, 95% CI ¼ 1.49–8.51), suicide plan (9.5% vs. 1.5%, OR¼ 7.10, 95% CI ¼2.16–23.34), suicide attempt (9.5% vs. 1.7%, OR¼ 1.87–19.25), and deliberate self-injury (16.7% vs. 6.5%,OR ¼2.87, 95 CI% ¼1.21–6.78). After adjustment for Table 3 Mean Youth Self Report scale scores (SD) among adolescents of parents who had or did not have insomnia symptoms.
Withdrawn Somatic complaints Anxious/ depressed Social problems Thought problems Attention problems Delinquent behavior Aggressive behavior Internalizing problems Externalizing problems
Adolescents of insomniac Adolescents of nonparents (n ¼43) insomniac parents (n¼ 755)
Fa
2.45 (2.92) 1.48 (1.92)
1.45 (2.05) 1.11 (2.26)
5.77n 0.10
4.53 (5.16)
2.89 (4.20)
2.59
2.18 (2.59)
1.51 (2.10)
1.31
0.98 (1.80)
1.00 (1.74)
0.03
3.10 (2.86)
2.44 (2.88)
0.92
2.08 (3.03)
1.22 (2.02)
4.55n
5.55 (5.27)
3.65 (4.46)
4.17n
8.13 (8.54)
5.22 (7.27)
2.37
7.63 (7.88)
4.85 (6.09)
4.85n
a General linear model, adjusting for sex, age, residence, and insomnia symptoms in adolescents. n p o 0.05.
Table 2 Insomnia symptoms and use of sleep medication among adolescents of parents who had or did not have insomnia symptoms. % Adolescents of insomniac parents (n ¼43) % Adolescents of non-insomniac parents (n¼ 755) Odd ratio (95% CI) Unadjusted Insomnia symptomsa Difficulty initiating sleep Difficulty maintaining sleep Early morning awaking Any Use of sleep medicationb **
20.0 5.6
5.6 2.1
7.9 27.8 7.9
3.1 14.2 2.0
p o 0.01. a
At least 3 times a week. At least once a week. c Adjusted for sex, age, residence, internalizing problems, and externalizing problems. n po 0.05. nnn p o 0.001. b
Adjustedc
4.23*** (1.83–9.77) 4.34*** (1.77–10.66) 2.81 (0.61–12.93) 3.55 (0.71–17.73) 2.70 (0.77–9.44) 2.32* (1.08–4.98) 4.21* (1.16–15.32)
2.14 (0.56–8.22) 2.56* (1.12–5.88) 4.65* (1.14–18.94)
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Table 4 Suicidal behavior among adolescents of parents who had or did not have insomnia symptoms. % Adolescents of insomniac parents (n¼ 43)
Suicidal ideation Suicide plan Suicide attempt Deliberate self-injury
16.7 9.5 9.5 16.7
% Adolescents of non-insomniac parents (n¼ 755)
5.3 1.5 1.7 6.5
Odd ratio (95% CI) Unadjusted
Adjusteda
3.56** 7.10*** 5.99*** 2.87*
3.23* 6.96* 3.91 1.58
(1.49–8.51) (2.16–23.34) (1.87–19.25) (1.21–6.78)
(1.16–9.02) (1.36–35.76) (0.91–16.78) (0.55–4.51)
a
Adjusted for sex, grade, residence, insomnia, and internalizing and externalizing problems. po 0.05. nn p o0.01. nnn p o0.001. n
sex, age, residence, insomnia symptoms, and internalizing and externalizing problems in the adolescents, parental insomnia was still significantly associated with increased risk for suicidal ideation (OR ¼3.23, 95% CI ¼1.16–9.02) and suicide plan (OR ¼6.96, 95% CI ¼1.36–35.76) (Table 4).
4. Discussion Insomnia is a known risk factor for mental disorders, but whether this risk extends to the mental health of offspring of parents with insomnia is unknown. To our knowledge, this is the first study to comprehensively examine insomnia symptoms, behavioral/emotional problems, and suicidal behavior among adolescent offspring of insomniac parents compared with those of non-insomniac parents. Our major findings are summarized below. First, compared with NIP adolescents, IP adolescents were more likely to report insomnia symptoms (OR ¼2.6) and use of sleep medication (OR¼ 4.7). IP adolescents had more internalizing and externalizing behavioral problems than NIP adolescents. Furthermore, parental insomnia symptoms were associated with increased risk for adolescent suicidal ideation (OR ¼3.2) and suicide plan (OR ¼7.0) after adjustment for age, sex, residence, insomnia symptoms, and internalizing and externalizing problems in the adolescents. The prevalence of insomnia symptoms among adolescent offspring of insomniac parents was significantly increased. After controlling for the potential confounding effects of demographics and internalizing and externalizing behavioral problems, PI adolescents were 2.6-fold more likely than NIP adolescents to report any insomnia symptoms, suggesting that it was unlikely that parent-offspring associations could be explained by demographic factors and present mental health status. These findings support recent genetic epidemiological studies that have demonstrated a modest familial aggregation and genetic transmission of sleep behavior (Partinen et al., 1983; Dauvilliers et al., 2005) and significant genetic effects on insomnia (Bastien and Morin, 2000; Zhang et al., 2009; Gehrman et al., 2011; Wing et al., 2012). Parental sleep problems may also exert negative impact on child's sleep indirectly via poor family environment and poor family functioning and parental style as a result of parental insomnia (Bernert et al., 2007; Brand et al., 2009a, 2009b; Gregory et al., 2012). Further familial/genetic studies are needed to examine whether and the extent to which the parent-adolescent association of insomnia is determined by family environment, genetic effect, or the interaction of both. Sleep disorders in parents may not only have a negative impact on their offspring's sleep, but also exert negative impacts on mental health directly and/or indirectly (Bernert et al., 2007; Gregory et al., 2012). In the current study, we found that all behavioral/emotional problem scale scores except Thought problems
were rated higher in IP adolescents than in NIP adolescents. After adjustment for sex, age, residence, insomnia symptoms in the adolescents, the mean scores on withdrawn, delinquent behavior, aggressive behavior, and externalizing problems were still significantly higher in IP adolescents than in NIP adolescents. These findings suggest that parental insomnia symptoms may exert negative impact on a range of internalizing and externalizing behavior problems among adolescent offspring, independent of genetic transmission of insomnia. Although further studies are warranted, the association of parental insomnia with both internalizing (withdrawn) and externalizing problems may have two explanations. First, internalizing and externalizing problems are highly correlated in childhood and adolescents (Achenbach, 1991; Liu et al., 2001). Second, the impact of parental insomnia on internalizing and externalizing problems may share similar mechanisms as described below. The impact of parental insomnia on adolescent psychopathology may be due to genetic and environmental effects or the interaction of both. First, parental insomnia is associated with increased risk for offspring sleep problems genetically (Partinen et al., 1983; Zhang et al., 2009; Dauvilliers et al., 2005; Wing et al., 2012), which in turn increase risk for psychopathology, such as depression and aggressive problems in children and adolescents. Children with sleep disorders such as insomnia have been observed to be at increased risk for neurobehavioral problems such as impairments in cognition, mood, attention, and behavior (Dahl and Lewin, 2002; Roberts et al., 2002) and internalizing and externalizing behavioral problems (Liu and Zhou, 2002). Second, parental insomnia may cause family stress and negatively influence parenting functioning and family interactions, all of which are in turn associated with increased risk for g poor sleep and psychopathology in adolescent offspring (Bernert et al., 2007; Brand et al., 2009a, 2009b; Gregory et al., 2012). Several studies have shown that family life stress or negative family life events were significantly associated with increased risk of insomnia symptoms, even after controlling for depression (Liu and Tein, 2005; Bernert et al., 2007). A number of studies have documented the association between parent functioning and a range of childhood problems, including internalizing and externalizing behavior problems and sleep disturbances (Obradović and Hipwell, 2010; Rhoades et al., 2012; Schoenfelder et al., 2015). In a recent study of similarities in sleep patterns between adolescents and parents, Brand et al. (2009b) concluded that mother's poor sleep has a direct impact on parenting style, which in turn affects adolescents' psychological functioning and sleep. Finally, insomnia in the parents may be accompanied by psychopathology in the parents (Liu et al., 2007; Buysse, 2013). Thus, the elevated psychopathology in adolescents may be a genetic/ environmental result of parental psychopathology, and insomnia is simply the symptom of the parental pathology that we measured. In the current study, we found that IP adolescents reported much higher prevalence of suicidal behaviors and self-injury than NIP adolescents. The increased suicidal risk may be due to increased
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sleep problems and behavioral/emotional problems in adolescent offspring of parents with insomnia. It is well known that internalizing and externalizing problems are associated with increased risk for suicidality in adolescents (Liu et al., 2005; Kelleher et al., 2012). Recent studies have demonstrated that short sleep duration and sleep problems including insomnia are associated with suicidal behavior (Liu and Buysse, 2006; Pigeon et al., 2012; Bernert et al., 2014). After adjustment for sex, age, residence, insomnia symptoms, and internalizing and externalizing problems in the adolescents, parental insomnia was still significantly associated with 3-fold increased risk for suicidal ideation and 7-fold increased risk for suicide plan. This finding suggests that suicidal behavior in adolescents of insomniac parents could not be entirely attributed to adolescent mental health status and insomnia due to genetic transmission. It would be important to further examine the biological mechanisms and potential psychological pathways between parental insomnia and adolescent suicidal risk. Several limitations should be considered in the interpretation of our results. First, the present study was limited by our reliance on self-report questionnaires, particularly in the measurement of insomnia symptoms. For example, parental insomnia was simply asked using one single question (i.e., “Do you often have…? and “Does your spouse often have…?”) and only one parent was asked to answer the question for both parents. This may be why the prevalence rate of insomnia was markedly lower in this sample of parents than those in most previous adult studies using several questions to ask insomnia symptoms like DIS, DMS, and EMA separately or studies using clinical interviews (Ohayon and Smirne, 2002; Buysse, 2013). Parents who reported a history of insomnia may represent a group of individuals with severe and chronic insomnia. The association of insomnia between parents and adolescent offspring or the familial aggregation of insomnia may be underestimated (Wing et al., 2012). Second, because the small number of parents with insomnia, we did not have enough statistical power to distinguish the paternal and maternal effects although the impact of paternal and maternal sleep on adolescent sleep and psychopathology may differ (Brand et al., 2009a; Zhang et al., 2009; Wing et al., 2012). Third, we did not include psychiatric history of parents in the statistical analysis due to the fact that only one IP adolescent and two NIP adolescents had a parental history of reported mental disorders. However, the association between parental insomnia and adolescent suicidal behavior is less likely to be explained by genetic transmission of parental psychiatric disorders as the association remained significant after adjustment for adolescent internalizing and externalizing behavior problems and insomnia in the adolescents. Furthermore, no causality of parental insomnia and adolescent offspring's psychopathology and suicidality can be made from the cross-sectional study. In conclusion, this is the first study to examine the impact of parental insomnia on adolescent insomnia symptoms, behavioral/ emotional problems, and suicidal behavior. Parental insomnia symptoms are not only associated with elevated risk for insomnia but also with elevated risks for use of sleep medication, a range of internalizing and externalizing behavior problems and suicidal behavior in adolescent offspring. Our findings support the need for early screening and formal assessment of sleep and mental health in adolescents of parents with insomnia. It is possible, although unproven at this time, that family interventions to enhance sleep quality could attenuate risk for the development of sleep disturbances, psychopathology, and suicidal behavior in adolescent offspring of parents with insomnia.
Acknowledgments This study was supported in part by the Multi-Investigator Proposal Development Grant Program, Arizona State University.
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The authors thank all participating teachers, parents and students, and Dr. Daniel Buysse, Professor of Psychiatry, University of Pittsburgh School of Medicine, for his insightful comments on an early draft of the manuscript. All authors reported no financial interests or potential conflicts of interest related to the study.
References Achenbach, T.M., 1991. Manual for the Youth Self-Report and 1991 Profile. Department of Psychiatry, University of Vermont, Burlington, VT. Bastien, C.H., Morin, C.M., 2000. Familial incidence of insomnia. Journal of Sleep Research 9, 49–54. Bernert, R.A., Merrill, K.A., Braithwaite, S.R., Van Orden, K.A., Joiner, T.E., 2007. Family life stress and insomnia symptoms in a prospective evaluation of young adults. Journal of Family Psychology 21, 58–66. Bernert, R.A., Turvey, C.L., Conwell, Y., Joiner, T.E., 2014. Association of poor subjective sleep quality with risk for death by suicide during a 10-year period: a longitudinal, population-based study of late life. JAMA Psychiatry 71, 1129–1137. Blank, M., Zhang, J., Lamers, F., Taylor, A.D., Hickie, I.B., Merikangas, K.R., 2015. Health correlates of insomnia symptoms and comorbid mental disorders in a nationally representative sample of US adolescents. Sleep 38, 197–204. Brand, S., Gerber, M., Hatzinger, M., Beck, J., Holsboer-Trachsler, E., 2009a. Evidence for similarities between adolescents and parents in sleep patterns. Sleep Medicine 10, 1124–1131. Brand, S., Hatzinger, M., Beck, J., Holsboer-Trachsler, E., 2009b. Perceived parenting styles, personality traits and sleep patterns in adolescents. Journal of Adolescence 32, 1189–1207. Breslau, N., Roth, T., Rosenthal, L., Andreski, P., 1996. Sleep disturbance and psychiatric disorders: a longitudinal epidemiological study of young adults. Biological Psychiatry 39, 411–418. Buysse, D.J., 2013. Insomnia. The Journal of the American Medical Association 309, 706–716. Buysse, D.J., Angst, J., Gamma, A., Ajdacic, V., Eich, D., Rössler, W., 2008. Prevalence, course, and comorbidity of insomnia and depression in young adults. Sleep 31, 473–480. Carskadon, M.A., Acebo, C., 2002. Regulation of sleepiness in adolescents: update, insights, and speculation. Sleep 15, 606–614. Dahl, R.E., Lewin, D.S., 2002. Pathways to adolescent health: sleep regulation and behavior. Journal of Adolescence Health 31, 175–184. Dauvilliers, Y., Maret, S., Tafti, M., 2005. Genetics of normal and pathological sleep in humans. Sleep Medicine Review 9, 91–100. Gehrman, P.R., Meltzer, L.J., Moore, M., Pack, A.I., Perlis, M.L., Eaves, L.J., Silberg, J.L., 2011. Heritability of insomnia symptoms in youth and their relationship to depression and anxiety. Sleep 34, 1641–1646. Gregory, A.M., Moffitt, T.E., Ambler, A., Arseneault, L., Houts, R.M., Caspi, A., 2012. Maternal insomnia and children's family socialization environments. Sleep 35, 579–582. Gradisar, M., Gardner, G., Dohnt, H., 2011. Recent worldwide sleep patterns and problems during adolescence: a review and meta-analysis of age, region, and sleep. Sleep Medicine 12, 110–118. Kelleher, I., Lynch, F., Harley, M., Molloy, C., Roddy, S., Fitzpatrick, C., Cannon, M., 2012. Psychotic symptoms in adolescence index risk for suicidal behavior: findings from 2 population-based case-control clinical interview studies. Achieves of General Psychiatry 29, 1–7. Linkowski, P., 1999. EEG sleep patterns in twins. Journal of Sleep Research 8 (Suppl 1), S 11–S 13. Liu, X.C., Buysse, D.J., 2006. Sleep and youth suicidal behavior: a neglected field. Current Opinion in Psychiatry 19, 288–293. Liu, X.C., Buysse, D.J., Gentzler, A.L., Kiss, E., Mayer, L., Kapornai, K., Vetró, A., Kovacs, M., 2007. Insomnia and hypersomnia associated with depressive phenomenology and comorbidity in childhood depression. Sleep 30, 83–90. Liu, X.C., Guo, C.Q., Liu, L.Q., Sun, L.M., 1987. Reliability and validity of the youth self report in Chinese adolescents. Chinese Journal of Mental Health 11, 200–203. Liu, X.C., Kurita, H., Uchiyama, M., Okawa, M., Liu, L.Q., Ma, D.D., 2000. Life events, locus of control and behavioral problems among Chinese adolescents. Journal of Clinical Psychology 56, 1565–1577. Liu, X.C., Sun, Z., Neiderhiser, J.M., Uchiyama, M., Okawa, M., Rogan, W., 2001. Behavioral and emotional problems in Chinese adolescents: parent and teacher reports. Journal of the American Academy of Child & Adolescent Psychiatry 40, 828–836. Liu, X.C., Tein, J.Y., Sandler, I., Zhao, Z.T., 2005. Psychopathology associated with suicide attempts among rural adolescents of China. Suicide and LifeThreatening Behavior 35, 265–276. Liu, X.C., Tein, J.Y., 2005. Life events, psychopathology, and suicidal behavior in Chinese adolescents. Journal of Affective Disorders 86, 195–203. Liu, X.C., Zhao, Z.T., Jia, C.X., Buysse, D.J., 2008. Sleep patterns and disturbances among Chinese adolescents: associations with parental sleep. Pediatrics 121, 1165–1173. Liu, X.C., Zhou, H.B., 2002. Sleep duration, insomnia and behavioral problems among Chinese adolescents. Psychiatry Research 111, 75–85.
802
X. Liu et al. / Psychiatry Research 228 (2015) 797–802
Obradović, J., Hipwell, A., 2010. Psychopathology and social competence during the transition to adolescence: the role of family adversity and pubertal development. Developmental Psychopathology 22, 621–634. Ohayon, M.M., Smirne, S., 2002. Prevalence and consequences of insomnia disorders in the general population of Italy. Sleep Medicine 3, 115–120. Owens, J.A., 2005. Introduction: culture and sleep in children. Pediatrics 115 (1 Suppl), S 201–S 203. Partinen, M., Kaprio, J., Koskenvuo, M., Putkonen, P., Langinvainio, H., 1983. Genetic and environmental determination of human sleep. Sleep 6, 179–185. Pigeon, W.R., Pinquart, M., Conner, K., 2012. Meta-analysis of sleep disturbance and suicidal thoughts and behaviors. Journal of Clinical Psychiatry 73, e1160–1167. Rhoades, K.A., Leve, L.D., Harold, G.T., Mannering, A.M., Neiderhiser, J.M., Shaw, D.S., Natsuaki, M.N., Reiss, D., 2012. Marital hostility and child sleep problems: direct and indirect associations via hostile parenting. Journal of Family Psychology 26, 488–498. Roberts, R.E., Roberts, C.R., Chen, I.G., 2002. Impact of insomnia on future functioning of adolescents. Journal of Psychosomatic Research 53, 561–569.
Roberts, R.E., Roberts, C.R., Chen, Y.R., 1998. Suicidal thinking among adolescents with a history of attempted suicide. Journal of the American Academy of Child & Adolescent Psychiatry 37, 1294–1300. Schoenfelder, E.N., Tein, J.Y., Wolchik, S., Sandler, I.N., 2015. Effects of the family bereavement program on academic outcomes, educational expectations and job aspirations 6 years later: the mediating role of parenting and youth mental health problems. Journal of Abnormal Child Psychology 43, 229–241. Watson, N.F., Goldberg, J., Arguelles, L., Buchwald, D., 2006. Genetic and environmental influences on insomnia, daytime sleepiness, and obesity in twins. Sleep 29, 645–649. Wing, Y.K., Zhang, J., Lam, S.P., Li, S.X., Tang, N.L., Lai, K.Y., Li, A.M., 2012. Familial aggregation and heritability of insomnia in a community-based study. Sleep Medicine 13, 985–990. Xie, Y., Zhou, X., 2014. Income inequality in today's China. Proceedings of the National Academy of Sciences of the United States of America 111, 6928–6933. Zhang, J., Li, A.M., Kong, A.P., Lai, K.Y., Tang, N.L., Wing, Y.K., 2009. A communitybased study of insomnia in Hong Kong Chinese children: prevalence, risk factors and familial aggregation. Sleep Medicine 10, 1040–1046.
