Objective. To investigate whether persistent infant crying is associated with an increased risk for externalizing behavior problems in childhood.
Methods. Sixty-four infants who were referred for persistent crying in infancy (PC; mean age: 3.8 ± 1.3 months) were reassessed at 8 to 10 years of age and compared with 64 classroom controls (CC). The major outcome measure was pervasive hyperactivity or conduct problems defined as parent, child, and teacher ratings that across informants were within the borderline/clinical range according to the Strengths and Difficulties Questionnaire (SDQ). Ratings of other behavior problems, parent ratings of temperament, and teacher assessment of academic achievement were also obtained.
Results. Ten (18.9%) of 53 PC had pervasive hyperactivity problems (child, parent, and teacher reported) compared with 1 (18.9%) of 62 CC (odds ratio: 14.19 [1.75–114.96]). Parents (29 [45.3%] of 64 vs 11 [17.2%] of 64; 4.00 [1.77–9.01]) and children (30 [46.9%] of 64 vs 17 [26.6%] of 64; 2.44 [1.16–5.12]) but not the teachers reported more conduct problems. Parents of PC rated the temperament of their children to be more negative in emotionality (PC mean: 3.0 ± 1.0; CC: 2.4 ± 1.0; effect size: 0.6) and difficult-demanding (PC mean: 5.2 ± 1.3; CC: 6.3 ± 0.9; effect size: 1.0). Academic achievement was reported by teachers to be significantly lower for PC than CC, in particular for those children with pervasive hyperactivity problems.
Conclusions. Infants who are referred for PC problems and associated sleeping or feeding problems are at increased risk for hyperactivity problems and academic difficulties in childhood.
Persistent crying (PC), sometimes called colic and defined as fussing or crying for >3 hours per day on 3 days per week in the past 3 weeks,1,2 is found in approximately 10% to 15% of infants in the first 3 months of life.3,4 Unexplained infant crying is among the most common complaints for which parents seek professional advice in the first year of life.3,5 There is some evidence that parental perceptions of negative infant behavior persist beyond the colic period.5–7 However, negative consequences of colic on observed infant behavior or cognitive development, mother-infant interaction, or maternal coping with the child have been suggested, but few have been found.5,6 Colic in the first 3 months of life seems to be a transitory condition that is associated with temporary delays in certain developmental tasks but no apparent long-term consequences.6,8–12 Possible reasons are that previous study samples were too small to detect such effects,8–11,13,14 the follow-up period extended to only the first months or year of life,15,16 or relied on maternal perceptions of infant mood or temperament in infancy5,7,12,17,18 rather than on reliable diary reports of PC spanning several days.19,20
Others have speculated that not unexplained crying per se but persistent problems with behavioral control, such as the inability to stop crying and to regulate sleeping or feeding behavior in infancy, are precursors of behavior control difficulties such as hyperactivity or conduct problems in childhood.18,21–23 This study prospectively investigated a group of infants who persistently cried in the first 6 months of life and compared them for pervasive hyperactivity and conduct problems and other behavioral and academic difficulties with classrooms control subjects (CC) at the age of 8 to 10 years.
A total of 108 mothers of 2- to 6-month-old infants (mean age: 3.8 ± 1.3 [standard deviation]) who either contacted the self-help group CRY-SIS (n = 53) or came forward to a call in the national press (n = 55) participated in a treatment trial of PC in infancy.24 More than 80% of the mothers had been in contact, often several times, with their primary health care providers regarding prolonged crying before contacting CRY-SIS or the research team directly.24 No organic problems on routine physical examination were found to explain PC at baseline. The 108 mothers completed a standard and previously proven reliable 7-day 24-hour diary19,20,25 that required continuous and mutually exclusive recordings of 5 infant behaviors (sleeping, feeding, fussing, crying, and awake). A total of 101 of 108 infants fussed or cried >3 hours on 3 days in the week (modified Wessel criteria2) and 64 (63%) were successfully traced and agreed to participate at 8 to 10 years of age (33 who had contacted CRY-SIS, 31 who had responded to the call in the national press). The 37 dropouts (D) were compared with the 64 participants (PC) according to mean fuss/cry duration in infancy (t test for independent samples; baseline [mean ± standard deviation] D: 381 ± 177 minutes; PC: 391 ± 170 minutes; t (99) = −0.26; P = .798, not significant [NS]), cry bouts in 24 hours (D: 9.9 ± 4.8; PC: 9.9 ± 4.6; t (99) = −0.08; P = .940, NS) and whether they had contacted a doctor/health visitor for PC problems (D: 81%; PC: 82.8%; χ2 (degrees of freedom [df]: 1) = 0.83; P = .514, NS). Furthermore, D and PC were compared on 18 sociodemographic factors (birth weight, marital status, family income, housing, employment, etc), 12 feeding variables, 3 sleeping variables, 12 health problem items, total health problems, and infant weight at baseline.25 No differences were found for all but the following variables: dropouts had mothers who were in paid employment more often (9 [24.3%] of 37 vs 2 [3.1%] of 64; χ2 (df: 1) = 10.86; P < .001), and the infants were more often in regular day care (6 [16.2%] of 37 vs 3 [4.7%] of 64; χ2 (df: 1) = 3.84; P < .05) at baseline.
Of the 64 infants who were referred for PC, 5 (7.8%) of 64 had only a PC problem; 10 (15.7%) of 64 also had sleeping problems; 20 (31.2%) of 64 had additional feeding problems; and 29 (45.3%) of 64 had crying, sleeping, and feeding problems.
Twenty-four of the participating children (24 [37.5%] of 64) were referred before 12 weeks of age; 8 of 24 did not qualify anymore as persistent criers according to modified Wessel criteria at the follow-up 3 months later (baseline age: 73 ± 10 days; baseline fuss/cry: 4 hours 41 minutes ± 1 hour 7 minutes; follow-up: 2 hours 9 minutes ± 1 hour 14 minutes), whereas 16 of 24 remained persistent criers 3 months later (baseline age: 66 ± 13 days; baseline: 6 hours 21 minutes ± 1 hour 37 minutes; follow-up: 4 hours 33 minutes ± 1 hour 18 minutes). Forty (62.5%) of 64 were referrals after the age of 12 weeks (baseline age: 136 ± 27 days; baseline: 5 hours 26 minutes ± 1 hour 26 minutes; follow-up: 3 hours 13 minutes ± 1 hour 48 minutes). Of the 40 infants who were referred after 12 weeks, 19 were still persistent criers in the follow-up 3 months later (ie, >6 months of age). Thus, all but 8 infants were persistent criers after the age of 3 months.
Of the 64 PC, 31 had been assigned to a no-treatment control condition (received normal primary care) in infancy and 33 had received telephone contact with a parent volunteer from the self-help group CRY-SIS who herself had previously had an infant who persistently cried.24 Fifteen of 33 shared their feelings and coping strategies with the mother (empathy condition), and 18 of 33 were provided with behavioral management advice. The follow-up findings of the original trial indicated that infants reduced crying significantly more in the behavioral management than in the empathy or control condition.24 However, fuss/cry amounts at 3 months’ follow-up were still substantially higher than expected in infants at this age in all 3 subgroups.24
The parents who had consented to participation in the follow-up study were asked to consent for the investigators to approach their children’s teacher when the children were 8 to 10 years of age (9.7 ± 0.6 years). The teachers were asked to select 2 children of the same gender in the class closest in age to the target child. Inclusion criteria for CC were same gender and that they had, according to retrospective parental reports, not cried >3 hours per day on 3 days per week during any week in the first 6 months of life. Four CC were excluded because of PC in infancy. When both control parents agreed to participation and were suitable, 1 was randomly selected to obtain a same size control sample (n = 64). Parents and children were sent a set of standard questionnaires for completion (the child questionnaire was in a separate envelope). When applicable, the reliability coefficients for scales (Cronbach’s α [CA]26) as determined for the total sample (N = 128) and the 64 PC and 64 CC separately are shown in brackets. The parent questionnaire included detailed questions about sociodemographic characteristics and current health,25 including 6 items on eating behavior (eg, eating too little, too much) and 7 items on current sleeping difficulties (eg, problems with falling asleep). Two questionnaires of child temperament, the Emotionality, Activity, Sociability Temperament Survey27 with the subscales shyness (total sample CA: 0.73; PC: 0.73; CC: 0.65), emotionality (0.87; 0.87; 0.84), activity (0.78; 0.80; 0.76), and sociability (0.58; 0.60; 0.57) and the Childhood Temperament Impression Scale (adapted from Wolke et al24) were also included. Principal components analysis with varimax rotation28 of the 13 Childhood Temperament Impression Scale items rated on 9-cm visual analog scales (eg, mood: very bad tempered/irritable to very happy/cheerful) yielded 2 factors: Difficult-Demanding (items: mood, demanding, difficult, unhappy about child’s temperament, stressful; total sample CA: 0.92; PC: 0.92; CC: 0.89) and Adaptability (wariness, adaptability 0.64; 0.62; 0.69). The parents were also asked to complete the Strengths and Difficulties Questionnaire (SDQ29), which consists of 5 subscales: Hyperactivity (CA: 0.79; PC: 0.81; CC: 0.69), Conduct problems (0.67; 0.53; 0.71), Emotional problems (0.81; 0.83; 0.81), Peer problems (0.73; 0.74; 071), and Prosocial behavior (0.76; 0.72; 0.78). A total score based on the first 4 subscales and scale scores for each subscale separately were computed. The SDQ has been shown to be a reliable and valid screening for identifying children who meet Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition criteria and require psychiatric treatment.30,31 A child32 and teacher29 version of the SDQ was also completed by the child and teacher, respectively. The internal consistency coefficients were comparable to those reported for the parents. Furthermore, the total score and each subscale score were dichotomized into normal versus borderline/clinical (score >80th percentile according to Goodman29,33 [replicated by Wolke et al33 for <11-year-olds]). Teachers were also asked to rate the scholastic performance of the child compared with expected standards in the 11 national curriculum subjects English, math, science, technology, geography, history, information technology, art, music, physical education, and religion on 5-point rating scales (1, very below average; 3, average; 5, very above average). Principal components analysis with varimax rotation indicated that the first 7 subjects (English, math, science, technology, geography, history, and information technology) loaded on 1 factor and were combined to give a Total Academic Achievement Score (TAAS; CA: 0.92; PC: 0.91; CC: 0.92). Furthermore, mothers completed the Edinburgh Postnatal Depression Scale34 when their children were 8 to 10 years of age.
Fully completed child and parent questionnaires were available for all PC and CC (N = 128); however, teacher reports for 11 PC and 2 CC were not obtained as parents did not provide consent for completion of teacher ratings. Ethical permission for the study was provided by the University of Hertfordshire Ethical Committee in accordance with the guidelines of the Helsinki Declaration, revised 1983.
Comparisons between PC and CC were conducted using independent sample t test for interval-scaled dependent variables. Effect size (ES) for mean comparisons was computed as Cohen’s d35 (ie, expressed as standard deviation unit differences using g-power software).36 Comparisons on categorical dependent variables were cross-tabulated, and crude odds ratio with 95% confidence interval were determined by logistic regression within SPSS version 10. T tests, odds ratios, and 95% confidence intervals with χ2 statistics are presented with corresponding 2-sided P values (P < .05, < .01, or < .001). Post hoc analyses of mean differences in hyperactivity and conduct scale scores between treatment groups (behavior management, empathy, no-treatment control subjects) were conducted using 1 factorial analysis of variance.
PC and CC were comparable on a wide range of sociodemographic indices (nonsignificant differences, Table 1). Furthermore, mothers did not differ in regard to depression scores (Edinburgh Postnatal Depression Scale mean 8.0 ± 4.6 vs 7.4 ± 5.3; t (df: 126) = 0.65; P = .52, NS). Twelve of 64 (18.8%) PC and 11 of 64 (17.2%) CC mothers scored within the clinical range (score >12)34 (odds ratio: 1.11 [0.45–2.74]; χ2 (df: 1) = 0.05; P = .50, NS).
The primary outcome measures were hyperactivity and conduct problems assessed with the SDQ. The Hyperactivity and Conduct problem scales were moderately correlated for each of the informants: parents (r = 0.50), children (r = 0.47), and teachers (r = 0.44; all P < .01). Parents, children, and teachers consistently rated PC to have higher Hyperactivity scores and to have higher Total Deviance scores than CC in the SDQ (Table 2). Parents and children reported higher Total and Conduct problems for PC than for CC, and parents also reported more Emotional and Peer Problems (Table 2). The Hyperactivity scale was most highly correlated across the 3 informants (all subjects: Pearson’s r child-parent: r = 0.78, P < .001; child-teacher: r = 0.45, P < .001; parent-teacher: r = 0.54, P < .001). PC significantly more often had Hyperactivity scores in the borderline/clinical range than CC as reported by the children (26 [40.6%] of 64 vs 10 [15.6%] of 64; 3.69 [1.60–8.55]; χ2 (df: 1) = 9.89; P < .01), the parents (25 [39.1%] of 64 vs 8 [12.5%] of 64; 4.49 [1.83–10.98]; χ2 (df: 1) = 11.80; P < .001), and the teachers (13 [24.5%] of 53 vs 5 [8.1%] of 62; 3.71 [1.22–11.22]; χ2 (df: 1) = 5.87; P < .05; Fig 1). Ten of 53 PC (18.9%) had pervasive hyperactivity problems in the borderline/clinical range (child, parent, and teacher reported) compared with 1 of 62 of the CC (1.6%; odds ratio: 14.19 [1.75–114.96]; χ2 (df: 1) = 9.84; P < .01). When the stricter criterion of pervasive hyperactivity scores >90th percentile was applied, it just failed to be significantly different between groups (5 [9.4%] of 53 vs 1 [1.6%] of 62; 7.8 [0.90–66.9]; χ2 (df: 1) = 3.54; P < .07). Parents (29 [45.3%] of 64 vs 11 [17.2%] of 64; 4.00 [1.77–9.01]; χ2 (df: 1) = 11.78; P < .001) and children (21 [32.8%] of 64 vs 5 [7.8%] of 64; 2.44 [1.16–5.12]; χ2 (df: 1) = 12.36; P < .001) also reported more conduct problems in the borderline/clinical range (Fig 2).
Pearson’s correlations were computed between the minutes of fuss/cry at baseline (severity of fuss/cry problem) and hyperactivity and conduct scores in the SDQ within the PC group. None of the correlations was statistically significant (Hyperactivity: child SDQ r = 0.23, parent SDQ r = 0.24, teacher SDQ r = 0.11; Conduct: child SDQ r = 0.06, parent SDQ r = 0.09, teacher SDQ r = −0.10).
No differences in Hyperactivity or Conduct scores were found according to treatment in infancy (Hyperactivity: Behavioral management [M = 4.7 ± 3.2], Empathy [M = 4.7 ± 3.8], no-treatment control subjects [M = 4.7 ± 2.7], F2,61 = 0.10; P = .91, NS; Conduct problems: Behavioral management [M = 2.2 ± 1.7], Empathy [M = 2.5 ± 2.5], no-treatment controls [M = 2.4 ± 1.7], F2,61 = 0.11; P = .89, NS).
In the secondary outcome measure TAAS (N = 112), 2 CC had a geography rating missing (CC n = 60) and 1 PC had a technology rating missing (PC n = 52); the PC scored lower, on average, than CC (PC grand mean: 3.1 ± .8; CC grand mean: 3.4 ±.6; t (110) = −2.41; P < .05; ES: 0.4). Comparisons on the individual items of the TAAS showed that persistent criers in infancy scored lower in science (PC mean: 3.2 ± 0.9; CC mean: 3.6 ± 0.7; t (113) = −2.63; P < .01; ES: 0.5), English (PC mean: 3.1 ± 1.1; CC mean: 3.5 ± .8; t (113) = −2.08; P < .05; ES: 0.4), geography (PC mean: 3.1 ± .8; CC mean: 3.4 ± 0.7; t (111) = − 2.27; P < .05; ES: 0.4), and history (PC mean: 3.1 ± 0.8; CC mean: 3.4 ± 0.6; t (113) = −2.04; P < .05; ES: 0.4).
Higher SDQ Hyperactivity and Total Deviance scores of child, parent, and teacher ratings were consistently correlated with lower TAAS scores (Table 3). Furthermore, child and parent ratings of emotional problems, child ratings of peer problems, and teacher ratings of conduct problems were significantly correlated with lower academic achievement (Table 3). The PC with pervasive hyperactivity (10 of 52; 1 TAAS score missing) had much lower academic achievement scores (TAAS means: 2.5 ± 0.8) than the CC (n = 60; 3.4 ± 0.6; t (68) = 4.58; P < .001: ES: 1.1) or PC without pervasive hyperactivity (n = 42; 3.3 ± 0.7; t (50) = 3.16; P < .01; ES: 1.1).
Significant differences were found in parent ratings of child temperament with case children rated as more negative in emotionality (Emotionality, Activity, Sociability Temperament Survey, PC mean: 3.0 ± 1.0; CC mean: 2.4 ± 1.0; t (126) = 3.61; P < .001; ES: 0.6), more difficult-demanding (Temperament Impression Scale, PC mean: 5.2 ± 1.3; CC mean: 6.3 ± 1.0; t (126) = −5.49; P < .001; ES: 1.0), and less adaptable (Temperament Impression Scale: PC mean: 6.1 ± 2.0, CC mean: 6.8 ± 1.7; t (126) = −2.01; P < .05; ES: 0.4). PC had more unregulated eating indicated by eating either too much or too little (PC: 15 [23.4%] of 64; CC: 5 [7.8%] of 64; 3.61 [1.23–10.64]; χ2 (df: 1) = 5.93; P < .05) or eating wrong foods more frequently (PC: 15 [23.4%] of 64; CC: 6 [9.4%] of 64; 3.0 [1.07–8.20]; χ2 (df: 1) = 4.61; P < .05).
This study followed up infants who were identified as being persistent criers in the first 6 months of life until school age. Persistent criers in infancy had more externalizing problems in childhood indicated by higher hyperactivity and conduct problems, negative emotionality, being more difficult and demanding, and being less adaptable than CC. Most notable is that children with previous PC in infancy substantially more often had Hyperactivity scores in the borderline/clinical range than their peers as consistently reported by teachers, parents, and children themselves. Behavioral difficulties, in particular pervasive hyperactivity problems, were related to lower academic achievement. The differences between PC and CC in middle childhood are unlikely to be explained by differences in PC versus CC mothers or systematic bias in ratings. Dropouts did not differ from participants in any baseline measures apart from that mothers who returned to work earlier were less likely to participate when children were 8 to 10 years of age. The PC families at follow-up did not differ on a wide range of sociodemographic indices from CC and the mothers were not more often depressed, and multiple informants were required to define pervasive hyperactivity with a valid screening instrument.29–31 CC were selected on age and gender only, and those with prolonged crying in infancy (6.5% of CC) on parent retrospective report were excluded. We found that for the prospectively studied PC, the baseline reports on fussing/crying correlated r = 0.39 with the retrospective report 9 years later. The fuss/crying amounts were slightly overestimated retrospectively. Thus, most prolonged infancy criers in the control group should have been excluded, if not, the reported findings are conservative estimates of differences in hyperactivity.
Significant associations of difficult temperament in the second or third year of life with externalizing and hyperactivity problems have been reported previously.23,37,38 These findings suggest that pervasive problems of behavior regulation (hyperactivity) and poorer academic achievement are related to problems of controlling behavioral states (eg, crying) detectable already in the first 6 months of life. This is in contrast to previous reports that found only small effects of prolonged crying in early infancy on behavior in the toddler and preschool years.5,8,10,18,39 The differences in findings may be accounted for by differences in the populations studied. First, the infants with prolonged unexplained crying in previous studies were identified when they were well below 3 months of age at a time when cry amounts generally show an increase and mostly reduce spontaneously by 3 months (ie, colic crying40). In this study, all but 8 of the children were still fussing and crying >3 hours a day after 3 months of age when the expected average fuss/cry amount is <1 hour 15 minutes a day in UK infants of comparable age.3 A comparison of the 8 infants who ceased PC after 3 months to the rest with infants in the PC group was not meaningful because of a lack of statistical power. Second, none of the previous longitudinal studies reported on co-associations of PC with sleeping or feeding problems. This self-referred sample showed a high co-association with sleeping and feeding problems that has also been reported for other self-referred samples.41,42 Only 5 infants had just a PC problem, and statistical comparison of these 5 with the 59 infants with multiple behavior problems lacked power. The prevalence of infants with multiple behavior difficulties in infancy is unknown. According to a community study of 5-month-olds, it may be approximately 2% in the infant population.18 Third, although behavioral management did lead to more reduction in fussing/crying in infancy compared with no or empathy intervention, all infants in this study still cried more than normative infants of 4 to 7 months of age.24 There were no differences on behavioral outcome in childhood according to treatment in infancy. The sample thus consisted of infants with highly persistent crying and mostly multiple behavior problems in infancy. The reduced variation in extreme groups may explain that the amount of fussing/crying at baseline did not correlate significantly with Hyperactivity or Conduct scores at 10 years.
The pattern of previous findings and results here leads us to speculate that although colic that resolves by 3 months (ie, is transient) has no or few long-term adverse effects,6,8–11,13,14 those infants with PC and multiple behavior difficulties are at increased risk for externalizing and hyperactivity problems. This is consistent with findings from another recent study of infants who were referred in the first 6 months and had a history of several months of unexplained crying.42 According to parent reports at 30 months, behavior problems were much more frequent in these infants than expected according to the scales norms. However, in the previous study, maternal bias in reporting on behavior could not be excluded. In contrast, our follow-up extends into middle childhood and used several informants, including teachers. Unfortunately, subgroup analysis in our study to test whether single versus multiple infant problems or the persistence of crying problems beyond 3 months of age are more strongly associated with hyperactivity was not possible because of sample size restrictions. Furthermore, although this study used multiple informants to define pervasive hyperactivity problems with a valid screening instrument,29–31 more detailed clinical and neurobehavioral assessment would have been desirable for a firm diagnosis of attention-deficit/hyperactivity disorder according to the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition or hyperkinetic syndrome according to the International Classification of Diseases, 10th Revision.
Alternative pathways may explain the association between infant difficulties in behavior regulation and childhood hyperactivity and warrant future exploration. The heritability of hyperactivity is moderate to high43,44 and has recently been linked to specific genes.45 We may speculate that the individual characteristics of state regulation are stable over time as a result of genetic liability44 or, alternatively, because of underlying neurodevelopmental problems that were not detected in routine examination.46,47 For example, a higher rate of PC as well as more hyperactivity-attention problems have been reported in neurologic at-risk groups such as very low birth weight children.48,49 The neurobiological underpinnings for poorer state regulation may be sought in the biological targets of stimulants, the dopaminergic and noradrenergic system. Alternatively, the early problems with PC and state regulation are challenging to parents. They form negative views5,6,16 that maintain parenting difficulties and the problems that these infants have in state and behavior regulation.50 Thus, the behavior outcome may be a result of a self-fulfilling prophecy related to the earlier labeling.
Whatever the reasons, health professionals should be aware that those with PC problems that last more than several months in infancy and often associated feeding or sleeping difficulties seem to be at increased risk for hyperactivity problems in childhood. Identification of infants and families that are slow to recover from colic and the development of appropriate interventions for these families remain important clinical challenges.22,41,51
We give special thanks to Cerian Hughes, who contributed to the data collection, and to all of the children, parents, and teachers for participation.
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