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Externalizing Problem Behaviors and Headache: A Follow-up Study of Adolescent Finnish Twins

Ruut Virtanen, MD^*, Minna Aromaa, MD, PhD^*, Markku Koskenvuo, MD, PhD^*, Matti Sillanpää, MD, PhD^*,, Lea Pulkkinen, PhD, Liisa Metsähonkala, MD, PhD, Sakari Suominen, MD, PhD^*, Richard J. Rose, PhD^||, Hans Helenius, MSc^¶ and Jaakko Kaprio, MD, PhD^#

^* Department of Public Health, University of Turku, Turku, Finland
Department of Paediatric Neurology, University of Turku, Turku, Finland
Department of Psychology, University of Jyväskylä, Jyväskylä, Finland
^|| Department of Psychology, Indiana University, Bloomington, Indiana
^¶ Department of Biostatistics, University of Turku, Turku, Finland
^# Department of Public Health, University of Helsinki and National Public Health Institute, Helsinki, Finland

	ABSTRACT

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Objective.To examine the association of teacher- and parent-rated behavior with headache in a prospective follow-up study of adolescent Finnish twins.

Methods.Questionnaire data were collected during 1995–2001 from a nationwide sample of Finnish families of 11-year-old twins who were born 1983–1987 (n = 5393) and again at age of 14. Psychological factors were measured by using parents’ and teachers’ ratings of a 37-item multidimensional rating instrument at the ages of 11 and 14.

Results.At age 11, headache frequency (5 categories) was associated with total scales of externalizing and internalizing problem behaviors and adaptive behaviors, assessed by parents, but only with externalizing problem behaviors assessed by teachers. Results were similar at age 14. The incidence of at least monthly headache between the ages of 11 and 14 years was predicted by externalizing problem behaviors and 2 subscales of adaptive behaviors: constructiveness and poor compliance. In twin pairs discordant for headache, externalizing and internalizing problem behaviors were more common among headache sufferers than among headache-nonsufferers. Headache-discordant monozygotic co-twins confirmed the association of externalizing problem behaviors with headache.

Conclusions.The frequency of adolescents’ headache is predicted by psychological factors, especially by externalizing problem behaviors. This seems to be independent of genetic or familial influences on behavior and headache. Behavioral problems may be a sign of worsening of headache or vice versa.

Key Words: child • headache • behavior

Abbreviations: MPNI, Multidimensional Peer Nomination Inventory • MZ, monozygotic • DZ, dizygotic • Tr-MPNI, Teacher Rating Form • Pr-MPNI, Parent Rating Form • OR, odds ratios • CI, confidence interval • CBCL, Child Behavior Checklist

Headache is the most common somatic complaint in children.¹ Its prevalence increases throughout childhood, and at school age up to 75% of children experience occasional headache and 10% experience headache frequently.^2–4

Headache has an impact on child and family life and even on society.⁵ Bell-Hoekstra et al⁶ found that children with the most severe headache reported the lowest quality of life, problems within physical functioning and other physical symptoms, impairment of daily and leisure activities, and social functioning at home. Conversely, migraine in childhood was not related to family and housing conditions, school situation, or peer relations, whereas tension-type headache was associated with a higher rate of divorced parents and fewer peer relations.⁷

Epidemiologic studies have observed a relationship between migraine and psychological factors, especially depression and anxiety.^8,9 Andrasik et al⁸ hypothesized that the higher scores of adolescent migraineurs on measuring depression, anxiety, and somatic complaints are a consequence of migraineurs’ having to live with chronic pain. According to Langeveld et al,¹⁰ lowered psychological functioning and internalizing behavior are not typical for patients who experience migraine or other types of headache, suggesting that internalizing behavior might be related to the experience of chronic pain in general and not specifically related to migraine. Stress has been found to have a clear association with headache, as well. Young adults with a history of childhood headache are significantly more likely to report stress in adolescence than their headache-free control subjects.¹¹ Also, Fearon and Hotopf¹² showed that children with headache are at an increased risk for different psychiatric symptoms in adulthood.

Adolescents who experience chronic headaches have been found to have an association between the experience of recent loss and depression and the onset of headache.⁹ Stressors within the family are commonly associated with increased occurrence of headache.^13–15 Aromaa et al¹⁶ found that concentration difficulties, behavioral problems, and depressive symptoms at preschool age were associated with headache occurrence at school entry. The prospective epidemiologic study of Pine et al¹⁷ studied the association between major depression and headache from late childhood into early adulthood. Major depression was found to predict prospectively the new onset of headaches in young adulthood. Depression and low self-esteem were found to precede headache among girls (aged 11–21 years) but not in boys.¹⁸

In their prospective cohort study of young adults, Merikangas et al¹⁹ showed the combination of anxiety disorder and major depression to be strongly associated with migraine. The migraineurs reported a significantly earlier onset of anxiety symptoms than nonmigraineurs, whereas the onset of depression tended to occur after the onset of migraine. Guidetti et al²⁰ had similar results among adolescents. These results suggest that migraine with anxiety and depression may constitute a distinct syndrome that comprises anxiety, often manifested in early childhood, followed by migraine and then by discrete episodes of depressive disorder in adulthood.

Migraine tends to run in certain families, and many studies have addressed the inheritance of migraine. Still, there is no consensus on the mode of inheritance of different migraine types.²¹ Several twin studies have suggested a strong genetic component for migraine. Genetic factors and the individual-specific environmental factors have been found to play an equally important role in the cause of migraine,^22,23 especially migraine without aura, not only in adults²⁴ but also in children.²⁵ Recently, Wessman et al²⁶ in their family study found significant evidence of linkage between migraine with aura and chromosome 4q24. Genes also play a role in psychological traits.²⁷ Nearly all behaviors that have been studied show moderate to high heritability,²⁸ so both genes and environment play a role in personality and depressive disorders.²⁷

Emotion regulation is found to play a role in the occurrence of chronic pain.²⁹ Pulkkinen³⁰ developed a theoretical model of emotional and behavioral regulation in which emotion regulation helps to maintain internal arousal within a manageable, optimal performance range, whereas behavior regulation helps to adjust reactions to external circumstances. The 2-dimensional model includes inhibitory and enhancing processes. According to Pulkkinen’s³⁰ model, externalizing and internalizing problem behaviors share low emotion regulation in common, but they differ in that Externalizing Problem Behaviors (eg, aggression, impulsivity, inattention) involve activation of behavior, whereas internalizing problem behaviors (eg, anxiety, depression) involve suppression of behavior. On the contrary, adaptive behaviors (eg, constructiveness, compliance, social activity) are characterized by high emotion regulation, which may be expressed by more or less activated or suppressed ways. The model has been used to explain recurrent pain symptoms in children.³¹

To enhance our understanding of the relationship between psychological factors and headache, we studied, in a Finnish twin-family cohort, relationships between emotional and behavioral problems and headache frequency in 11- to 14-year-old schoolchildren. We hypothesized that internalizing problem behaviors and externalizing problem behaviors are related to adolescents’ frequent headache. Our main questions were as follows 1) Do adolescents with frequent headache have more emotional and behavioral problems than other adolescents? 2) Do internalizing and externalizing problem behaviors predict incidence of frequent headache during adolescence? 3) Do emotional and behavioral problems differ in co-twins who are discordant for headache?

	METHODS

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The research is part of a longitudinal study of behavioral development and health habits in 5 consecutive birth cohorts of Finnish twin children, called FinnTwin12.³² The study was launched in September 1994, when all twins who were born in 1983–1987 were identified from the Central Population Registry of Finland as part of the Finnish Twin Cohort studies. Family questionnaires first were mailed in the autumn of the year before the twins reached the age of 12. Excluded were families in which 1 or both co-twins were living outside Finland, co-twins were living apart from both biological parents, the Central Population Registry contained no residential address for a twin, and either twin had died. Five separate questionnaires were mailed at baseline to each twin family: a family questionnaire on the birth, early childhood, and development of the twins, which was followed by a postal mailing of separate questionnaires to both parents and both twins in the late autumn. Eighty-seven percent (n = 2724) of the twin families gave their informed consent to participate in the study. Permission to contact the school was obtained from 93% of these families. In the following spring, the year in which the twin children turned age 12, several months after the baseline questionnaires had been returned, the ratings from parents and classroom teachers of all twins was sought, using a Multidimensional Peer Nomination Inventory (MPNI), developed for this research by co-investigator, Pulkkinen.^30,32,33 Ratings on twins were completed by 93% of teachers and 92% of parents of the entire twin sample.

At the follow-up, questionnaires were mailed in the month of the twins’ 14th birthday. At that age, most questions asked at age 11 were repeated and ratings from teachers of all twins using MPNI were requested. The age 14 follow-up of all twins by postal questionnaire for all 5 birth cohorts had a participation rate of 88%.

At baseline headache, questions were directed only to 4 birth cohorts (born 1984–1987) at the mean age of children of 11.4 years (range: 10.8–12.3). Of the 3966 participants, 51.7% (2051 of 3966) were girls and 48.3% (1915 of 3966) were boys. At follow-up, all 5 cohorts (n = 4710) were asked about headache at the age of 14 (mean: 14.1; range: 13.9–14.9). The gender distribution was 49% (2336 of 4710) for girls and 51% (2374 of 4710) for boys. The zygosity of 3731 twin individuals at age 11 and 4396 at age 14 was determined from a validated questionnaire method.³² The data consisted of 1251 monozygotic (MZ) and 2480 dizygotic (DZ) twins at age 11 and of 1438 MZ and 2958 DZ twins at age 14.

Assessment of Headache
Headache was assessed with a question of headache frequency. At age 11, the twins themselves were asked, "If you think of the period from today to last summer, how often have you had headache after the last summer?": 1) every day or almost every day, 2) more often than once a week but not almost every day, 3) approximately once a week, 4) once a month, 5) less than once a month. Headache frequency was again assessed at age 14 with the question, "How often have you had headache during last few months?" The response scale was the same as at baseline.

Psychological Variables
A multidimensional inventory of children’s social behavior was developed for peer nomination (MPNI),^33,34 and the 37-item Teacher Rating Form (Tr-MPNI) and Parent Rating Form (Pr-MPNI) used in the present study were developed from it.³³ In both the Tr-MPNI and the Pr-MPNI, items were presented in the form of statements (eg, "cannot concentrate in anything"). The teachers and the parents were asked to rate each twin on every item on a 4-point scale as follows: 0 = does not apply, 1 = applies sometimes but not consistently, 2 = certainly applies but not in a pronounced way, 3 = applies in a pronounced way. The ratings yield scores on 3 major psychological factors called: externalizing problem behaviors, consisting of subscales of aggression, impulsivity, and inattention; adaptive behaviors, consisting of subscales of constructiveness, compliance, and social activity; and internalizing problem behaviors, consisting of subscales of depression and anxiety as in the previous analysis by Pulkkinen et al.³³

Statistical Methods
Associations among individuals, between variables and frequency of headache (every day or almost every day, more often than once a week, approximately once a week, once a month, less than once a month) were analyzed using cumulative logistic regression models.³⁵ Because frequency of headache was associated with gender and because the means of psychological variables showed differences between boys and girls,³⁶ analyses of associations between headache and psychological factors were made using gender adjustment. The strength of associations between headache frequency and psychological variables between genders were analyzed by testing interactions of gender and psychological factors in the logistic models. Because the data consisted of observations from twins, observations on twin individuals in a pair may be correlated. The correlations were taken into account by using the Generalized Estimation Equations method in the estimation of standard errors of the parameters. Cumulative odds ratios (ORs) and 95% confidence intervals (CIs) were calculated from the logistic regression models corresponding to the standard deviations.

The associations between psychosocial variables and headache were analyzed within twin pairs, as well. This analysis was of discordant twin pairs, for whom the definition of discordance was made when 1 twin had headache at least monthly but the co-twin less often or not at all. Statistical analysis was then conducted using conditional logistic regression analysis. A separate analysis was performed for MZ and DZ twins. Among DZ twins, the confounding effect of gender was taken into account by limiting the analysis to same-sex pairs. The differences of MZ and DZ twins in the strength of the associations of headache frequency and psychological factors were analyzed by testing interaction terms of twin type with psychological factors in the conditional logistic models. ORs and 95% CIs were calculated from the conditional logistic regression models corresponding to the standard deviation. P < .05 was used as a cutoff point of the significance. Statistical computing was performed with the SAS System for Windows, release 8.2/2001 and SUDAAN program.³⁷

	RESULTS

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Cross-Sectional Analysis at the Ages of 11 and 14
A total of 3513 children answered questionnaires with headache items at both baseline and follow-up. Sixty percent (2096 of 3513) of 11-year-old and 65% (2298 of 3513) of 14-year-old children reported monthly headache, ie, they experienced headache at least once a month. At age 11, 2% had experienced daily headache, 6% reported headache more often than once a week, 14% once a week, and 38% once a month. Among 14-year-old children, the percentages were 2%, 7%, 21%, and 35%, respectively.

In the parents’ ratings of MPNI at the children’s age of 11, all 3 psychological main scales—externalizing and internalizing problem behaviors; adaptive behaviors; and the subscales of inattention, constructiveness, social activity, and depression—were significantly associated with the child’s headache frequency. In the teachers’ ratings of MPNI, externalizing problem behaviors, especially inattention, were found to be associated with headache frequency (Table 1). At age 14, only the teachers’ ratings of MPNI were obtained. The results were similar as 3 years earlier with a statistically significant association between child’s headache frequency and externalizing problem behaviors and inattention.

Psychological Factors That Predict the Incidence of Frequent Headache Between the Ages of 11 and 14
At age 11, a total of 1417 children had no or infrequent headache (less than once a month). In total, 646 of them reported at least monthly headache at follow-up, ie, represent incident cases. In the parental ratings, the following factors assessed at age 11 predicted the incidence of monthly headache at age 14: externalizing problem behaviors, constructiveness, and poor compliance. In teacher’s ratings at age 11, the only statistically significant predictor for headache was externalizing problem behaviors (Table 2).

Analysis of Headache-Discordant Twin Pairs
Twin pairs discordant for headache (pairs being either MZ or same-sex DZ) were identified as pairs in which 1 twin experienced headache at least once a month and the co-twin experienced headache less often or not at all (668 pairs [34% of total sample at age 11] and 778 pairs [33% of total sample at age of 14]). In parental ratings, externalizing and internalizing problem behaviors, adaptive behaviors, inattention, constructiveness, and social activity at the age of 11 were associated with monthly headache at age 14 within these headache-discordant pairs. No statistically significant associations at either age group were found in teacher ratings (Table 3).

The differences of MZ and DZ twins in the strength of the associations of headache frequency and psychological factors were analyzed by testing interaction terms of twin type with psychological factors into the conditional logistic models. With aggression, the interaction was statistically significant at age 14 (P = .02). Significant interactions were found also in the associations of teacher-rated depression and social anxiety at age 11 and monthly headache at age 14 (P = .039 and P = .019). When MZ and DZ twin pairs were analyzed separately, none of the associations of these variables was statistically significant.

	DISCUSSION

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The study demonstrates that headache frequency among 11- and 14-year-old twins is associated with externalizing and internalizing problem behaviors and adaptive behaviors in parents’ reports but only with externalizing problem behaviors in teachers’ reports. The incidence of monthly headache at age 14 was predicted by externalizing problem behaviors and adaptive behaviors. The third major finding was that among headache-discordant pairs, the association of externalizing problem behaviors with monthly headache was also observed.

Our study is based on a large and representative sample of Finnish twins assessed at ages 11 and 14 years. Are twins representative of the population of singletons? Data from other studies^38,39 show that level and variability of psychiatric symptoms reported by twins are similar to those found among nontwin populations. When comparing behavioral problems among twins (n = 1832) and children from the general population (n = 723) in Norway, the levels of attention problems and externalizing behavior were similar, whereas an increased variance was found for externalizing behavior for twins.⁴⁰ In our own Finnish data, the twins have been shown not to differ in means or variances from their 25 000 classmates in the behavioral scales of the MPNI.³⁶ Because of the correlations in observations on twins (for genetic or familial reasons), the Generalized Estimation Equations method was used. This technique provides correct standard errors and P values for the individual-based epidemiologic analyses. Even if there were minor differences between singletons and twins in behavior or headache frequency, the crucial issue is whether the associations that are observed are dependent on twin status. Within this data set, the observed relationships were independent of the zygosity of the twins and whether they came from like-sex or opposite-sex twin pairs.

Previous studies examining the associations between headache and psychopathology have used different assessment measures. Achenbach’s Child Behavior Checklist (CBCL)⁴¹ is a widely used instrument, and there are some studies on CBCL and headache.^8,42 The MPNI compared with the CBCL has some strengths. MPNI covers not only the behavioral and emotional problems included in the CBCL but also both active and passive adjusted behavior. Pulkkinen et al³³ showed the reliability and both concurrent and discriminative validity of the multidimensional inventory developed for peer nomination and teacher and parental assessments. When studying the correlations between these different ratings, results showed that the reliability of parental assessment was lower than peer and teacher assessments, whereas peer nominations and teacher assessments correlated highly with each other. It is possible that teachers’ reports on children’s emotional problems are insensitive, but no self-reports were collected at these ages. In peer nomination, boys were rated behaviorally more uncontrolled than girls, and gender differences in internalizing problem behaviors existed only in social anxiety, with girls scoring higher than boys.³³ It is well known, as well, that prevalence of headache is gender dependent among schoolchildren.^43,44 In the present study, for both the rated psychological factors and headache frequency, the score levels differentiated linearly between boys and girls, and, for that reason, the analysis was conducted after adjustment for gender and, when appropriate, separately by gender.

In the study of Egger et al,⁴⁵ girls with depression and anxiety disorders had significantly greater prevalence of headaches than girls without an internalizing disorder. This association was not found for boys. In the present study, internalizing symptoms seem to be slightly more often associated with headache among girls than boys, and especially adaptive behaviors were significantly associated with onset of headache at age of 14 among girls but not among boys. The analysis of interaction at age 14 revealed that only significant interactions were found with aggression and depression, whereas in the analysis separated by gender, the associations were mild, nonsignificant, and in the opposite direction.

Only a few studies have shown associations between childhood headache and externalizing problem behaviors. Sillanpää et al⁴⁶ found that behavioral problems were significantly more common in 5-year-old children with headache than in others. Also, concentration difficulties have been shown to be associated with the headache occurrence at preschool age.⁴⁷ In a Norwegian follow-up study, a significant association was found among children with behavioral problems at the age of 4 and complaints of headache and abdominal pain at the age of 10.⁴⁸ Crawford et al⁴⁹ found that symptoms of attention-deficit/hyperactivity disorder were associated with migraine headache. These results from studies of younger children are analogous with our results. Externalizing problem behaviors not only are associated with frequent headache among adolescents but also seem to have a significant role in the incidence of frequent headache among adolescents. The association between the frequent headache and the sum score of externalizing problem behaviors was statistically significant as a result of the cumulating effect of the subscales (aggression, impulsivity, and inattention). To our knowledge, this is the first follow-up study of externalizing problem behaviors and headache in adolescents.

Somatic complaints, such as frequent headache, may be used by children as a way to express negative emotions when depression or another emotional disorder occurs.⁵⁰ In the study of Smith et al,⁵¹ 13-year-old adolescents with frequent headache were compared with children with infrequent or no headaches; children in the headache group reported significantly more anxiety than the headache-free group. Converse results also exist.⁵² Our results show that internalizing problem behaviors, especially depression, are associated with frequent headache.

Children with both headache and adjustment problems seem to have problems with their social behavior; they may have concentration difficulties and problems in social relationships and are afflicted by stress in everyday life.^53,54 Metsähonkala et al⁵⁵ found that children with migraine and children with nonmigrainous headache both reported more often problems in getting along with other children than children without headache. Our results suggest that social activity, constructiveness, and lack of compliance were associated with frequent headache among adolescents.

Perquin et al¹ and Egger et al⁵⁶ emphasized that pain comorbidity is a strong factor explaining a sizable proportion of the relationships between frequent headaches and psychological problems. The prevalence of widespread pain was studied previously in the same sample of 11-year-old Finnish twins, and the prevalence of widespread pain was found to be 10% in both genders.⁵⁷ Furthermore, among these same children, it was observed that depression, aggression, and impulsivity as measured by the MPNI have the strongest relationship with recurrent overall pain.³¹

In the present study, teachers’ ratings of behavioral problems differentiate children who experience frequent headache. Conversely, teachers see only a part of children’s lives and may not recognize covert symptoms such as anxiety and depression, or these may not be expressed to the same extent in the class setting as at home. When examining teachers’ reports of the problem behavior of children, Molins and Clopton⁵⁸ found that teachers identified significantly more children with externalizing problems than internalizing problems and significantly more boys than girls as having problems that concerned them. However, when teachers identified children as having internalizing problems, they were just as likely to judge them as needing referral as children with externalizing problems.

To our knowledge, twin studies addressing the nature of the intermediating effects of frequent headache and psychological factors have not been previously conducted. Because both headache and personality characteristics have a substantial genetic component and individual genes associated with both phenotypes have been identified, common genes could underlie both conditions. Nonetheless, we found that externalizing problem behaviors were associated with headache even within headache-discordant MZ co-twins, with a weaker but nonsignificant association within discordant DZ pairs. The weaker associations in DZ twins discordant for headache may be related to statistical power issues when subgroups are concerned or to more complex genetic and environmental information. Thus, our results of relationships between headache frequency and behavioral problems indicate that this relationship is not fully explained by underlying common genes.

Limitations of the Study
The present study dealt only with the prevalence of overall headache and omitted different types of headache. Different causative factors may underlie different headache types and explain the weaker associations in DZ twins.

Clinical Implications
In clinical practice, physicians who treat children with headache should be aware of the possible behavioral problems of the child. Externalizing problem behaviors in a child with frequent headache may be a sign of worsening of headache or vice versa; behavioral problems can cause headache via the implication of outside stressors.

	ACKNOWLEDGMENTS

 
Data collection and analyses were supported by the National Institute on Alcohol Abuse and Alcoholism (grants AA12502 and AA09203 to R.J.R.) and by grants from the Academy of Finland (#100499), the Yrjö Jahnsson Foundation, and the European Union Fifth Framework Program (grant QLG2-CT-2002-01254).

Appreciation is expressed to Inger Vaihinen for secretarial assistance.

	FOOTNOTES

 
Accepted Apr 1, 2004.

Reprint requests to (R.V.) Department of Public Health, University of Turku, Lemminkäisenkatu 1, 20014, Turku, Finland. ruut.virtanen{at}utu.fi

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