A systematic review of challenging behaviors in children exposed prenatally to substances of abuse

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Research in Developmental Disabilities 29 (2008) 483–502

Review

A systematic review of challenging behaviors in children exposed prenatally to substances of abuse Dennis R. Dixon, Patricia F. Kurtz *, Michelle D. Chin Kennedy Krieger Institute, The Johns Hopkins University School of Medicine, United States Received 1 May 2007; received in revised form 25 May 2007; accepted 30 May 2007

Abstract A review of the existing literature on the occurrence of challenging behavior among children with prenatal drug exposure was conducted. While a large number of studies were identified that evaluated various outcomes of prenatal drug exposure, only 37 were found that directly evaluated challenging behaviors. Of the 37 studies, 23 focused on prenatal cocaine exposure, and 14 focused on prenatal alcohol exposure; most studies relied on broadband measures such as the CBCL for the assessment of challenging behavior. Among the 37 studies, a clear role for the postnatal environment on developing challenging behaviors was evident; however, prenatal alcohol exposure showed a much clearer independent effect upon challenging behaviors than was noted in the prenatal cocaine studies. Additionally, only 3 of the 37 studies addressed interventions for challenging behaviors, each of which showed an improvement in child behavior or parent–child interactions. As researchers have continued to show the importance of the postnatal environment, it is likely that interventions addressing specific environmental risk factors will be helpful to reduce or prevent challenging behaviors among this population. # 2007 Published by Elsevier Ltd. Keywords: Challenging behavior; Prenatal exposure; Review; Treatment

Contents 1.

Method. . . . . . . . . . . . 1.1. Literature search. 1.2. Parameters. . . . . 1.3. Reliability . . . . .

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* Corresponding author at: Kennedy Krieger Institute, Neurobehavioral Unit Outpatient Clinic, 707 N. Broadway, Baltimore, MD 21205, United States. Tel.: +1 443 923 2894. E-mail addresses: [email protected], [email protected] (P.F. Kurtz). 0891-4222/$ – see front matter # 2007 Published by Elsevier Ltd. doi:10.1016/j.ridd.2007.05.006

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Results . . . . . . . . . . . . . . . . . . 2.1. Prenatal cocaine exposure 2.2. Prenatal alcohol exposure 2.3. Treatment studies . . . . . . Discussion . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . References . . . . . . . . . . . . . . .

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The effects of prenatal drug exposure on infant development have received much attention over the past 30 years. Because of the importance and emotional saliency of the topic there have been a number of studies and reviews on the impact of exposure to particular substances (e.g., Frank, Augustyn, Grant Knight, Pell, & Zuckerman, 2001; Jacobson & Jacobson, 2002) or general exposure (Hans, 2002). Prenatal exposure to alcohol has been the most extensively studied. As such, exposure is now known to produce fetal alcohol syndrome, a specific pattern of malformations characterized by distinctive facial features, growth deficiencies, and organ malformation (Ornoy, 2002). Additionally, a range of specific deficits have been noted. Neurobehavioral deficits associated with prenatal alcohol exposure include inattention and impulsivity (Streissguth, Barr, & Martin, 1984), slower processing speed (Jacobson, Jacobson, Sokol, Martier, & Ager, 1993), memory deficits (Mattson, Riley, Gramling, Delis, & Jones, 1998), lower IQ scores (Mattson, Riley, Gramling, Delis, & Jones, 1997), and childhood-onset depression (O’Connor & Paley, 2006). Heroin exposure to the developing fetus produces similar effects, including decreased growth and head size. Postnatal effects of heroin exposure include withdrawal symptoms, developmental delay, and hyperactivity (Barr & Jones, 1994; Moe, 2002). Recent studies on prenatal exposure to cocaine also show a number of deficits. As with prenatal alcohol exposure, birth defects are common among infants prenatally exposed to cocaine, showing reduced birth weight, head circumference, and length (Chasnoff, Griffith, MacGregor, Dirkes, & Burns, 1989; Datta-Bhutada, Johnson, & Rosen, 1998). Neurobehavioral studies have found particular problems with arousal and regulation (Bard, Coles, Platzman, & Lynch, 2000), motor and state regulation (Delaney-Black et al., 1996), attention (Gaultney, Gingras, Martin, & DeBrule, 2005; Heffelfinger, Craft, White, & Shyken, 2002), and language development (Beeghly et al., 2006). Early studies on prenatal exposure presented a rather bleak view for the future of exposed children, with predictions of behavioral epidemics among school-aged children. However, more recent studies indicate that, depending upon the substance, prenatal exposure alone is not sufficient to account for the poor outcomes of exposed children. Rather, negative child outcomes are best predicted by a model consisting of the interactions between biological effects from the exposure with aspects of the postnatal environment, such as socioeconomic status, caregiver mental health, and caregiver drug use (Brown, Bakeman, Coles, Platzman, & Lynch, 2004; Frank et al., 2001). Studies evaluating the role of the postnatal environment on developmental outcomes find a much smaller independent effect from prenatal cocaine exposure on child development (Frank et al., 2002; Hurt, Malmud, Betancourt, Brodsky, & Giannetta, 2001) or IQ scores (Frank et al., 2005). Predicting the outcome of prenatal exposure is a complicated process, requiring an understanding of a number of patient-specific variables. This is particularly the case regarding the development of challenging behaviors among children with prenatal exposure.

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While biological sequelae have received much attention, studies on the impact of prenatal exposure upon a child’s behavior have not been as prevalent. Children with prenatal exposure to alcohol, cocaine or heroin are at risk for neurobehavioral problems such as impulsivity, poor sustained attention, and poor memory. Children with prenatal exposure may also be at risk for developing challenging behaviors. Challenging behaviors typically include aggression, violent or destructive outbursts, stereotypy, and self-injury (Matson & Nebel-Schwalm, 2007). These behaviors impair child development by resulting in social isolation, loss of education opportunities, and impeded education integration. Challenging behaviors are a significant concern for persons with developmental disabilities and occur in a large percent of the population (Holden & Gitlesen, 2006). Among persons with developmental disabilities, aggression has been reported as the most frequently occurring behavior (Holden & Gitlesen, 2006; Noone, Jones, & Hastings, 2006). Further, challenging behaviors are among the primary reasons for residential placement (Robertson et al., 2004). It is likely that clinicians, care providers, or educators of children with prenatal drug exposure may need to address challenging behavior. However, few studies have focused on challenging behavior in this population. Many questions regarding the nature of the challenging behaviors and their responsiveness to treatment remain. The purpose of this paper was to provide a datadriven review of the existing literature on challenging behavior as exhibited by children who were prenatally exposed to illicit substances. 1. Method 1.1. Literature search Searches for all studies referenced in the PubMed and PsycINFO databases were conducted on children prenatally exposed to substances of abuse. The search parameters included: cocaine, alcohol, heroin, prenatal exposure, fetal exposure, and intrauterine exposure. This initial search produced a list of 783 articles. While no particular time range was specified, the output produced articles from 1969-mid December 2006. This list was further reduced to exclude the following: articles with nicotine, amphetamine, methadone, marijuana, barbituates, and any other substances other than alcohol, cocaine, or heroin as the major drug of exposure; articles other than peer-reviewed research articles (e.g., letters to the editor, magazine articles, book chapters); and articles using animals as subjects. Indeed, the only limit indicated for this search was ‘‘human,’’ to exclude all animal studies. Thus, 398 articles were reviewed using a standardized coding sheet created for this review. This resulted in data being collected on a total of 337 studies. These search procedures may not have resulted in an exhaustive review. However, the results should be representative of current trends and practices regarding challenging behaviors in this population. 1.2. Parameters A standardized coding sheet was used for each of the 337 identified articles. To ascertain the focus of studies on prenatal exposure to substances of abuse, five broad categories were used to identify the topic areas reported in each study: psychosocial adjustment, cognitive, neurobehavioral, psychometric, and review. The psychosocial adjustment category included areas such as problem behavior of adults who had prenatal exposure, attachment problems,

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interaction problems, wakefulness and infant sleep patterns, infant feeding and sucking, caregiving environment, and challenging behaviors, which is the focus of this review. The cognitive category included the subcategories of language, IQ/adaptive, and attention (e.g., vigilance, impulsivity, distractibility). The neurobehavioral category was the most inclusive, with the subcategories of psychomotor (e.g., reaction time), motor (e.g., balance, reflex, reaching)/physical (e.g., birthweight, head circumference, physical deformities/malformations, links to medical conditions), neurological (e.g., brain damage, scans, EEG), and sensory (e.g., hearing, vision). The psychometric category included studies wherein the primary purpose was to evaluate the psychometric properties of a particular measure or assessment scale. The final category of review included articles that did not present original data but reviewed previous studies. Reviews comprised 30.5% of the final 337 articles. After removing these reviews from further analysis, an original data category was created, with a total of 241 articles. Regarding the breakdown of primary exposures, 56.8% of articles targeted alcohol, 47.7% targeted cocaine, 16.3% targeted nicotine and 6.6% targeted opiates. In regards to the type of exposure reported within the original data articles, 22.4% discussed more than one primary drug of exposure, while nearly 50% of all the articles enquired about maternal use of various drugs as secondary exposures. Given that secondary exposures were not the focus of this review, these data are not reported. Of the 241 articles, topics were as follows: 24.5% reported on some form of psychosocial adjustment; 16.2% reported on language; 30.3% reported some measure of IQ/adaptive skills; 20.3% reported on some aspect of attention; 23.7% reported psychomotor effects; 56% reported motor effects; 12.4% reported neurological effects; 7.5% reported sensory effects; and 1.2% evaluated the psychometric properties of assessment scales. Of the studies reporting on psychosocial adjustment among children with prenatal drug exposure, 37 were identified that focused on challenging behaviors. Challenging behavior for these studies included any study reporting some measure of externalizing behaviors, whether through indirect (e.g., CBCL) or direct assessment (observation). None of the 37 studies on challenging behaviors focused on nicotine or opiates as the primary exposure. These 37 studies were reviewed in depth in regards to their participants, the methods of assessing challenging behaviors, their conclusions, and if the postnatal environment was controlled for or examined. 1.3. Reliability Independent reviewers collected reliability data for 25% of the final sample of 241 articles. Inter-rater agreement was calculated for each of the following categories, and averaged 89.5%: exposure types, including alcohol, opiate, cocaine, and nicotine; and topics of psychosocial adjustment, language, IQ/adaptive, attention, psychomotor, motor, neurological, and sensory topics. 2. Results Thirty-seven studies were identified that examined challenging behaviors in children with prenatal exposure and met criteria for an in-depth review. Table 1 displays a breakdown of the identified studies in relation to sample characteristics, study description and study findings. Table 1 also lists the methods used to measure or define challenging behavior. Only measures used to assess for challenging behavior are reported.

Table 1 A breakdown of studies on challenging behaviors in children with prenatal drug exposure Authors

Assessment

Description

Results

407 mothers and children. 210 with prenatal cocaine exposure. 197 unexposed controls 476 mothers and children. 253 with prenatal cocaine exposure. 223 unexposed controls

Evaluation of challenging behaviors among 7 year-old children with and without prenatal cocaine exposure Evaluation of the role of prenatal cocaine exposure and postnatal maternal drug use on challenging behaviors among 5 year-old children Evaluated the effects of both amount of prenatal alcohol exposure and pattern of alcohol exposure (binge drinking) Hypothesized that the risk factors of prenatal cocaine exposure, gender, and a high-risk environment would contribute to challenging behaviors Evaluation of impulse control among 2 year-old children with and without prenatal cocaine exposure

Caregiver rated challenging behaviors were not related to level of prenatal cocaine exposure Cocaine exposure was not related to CBCL scores. However, postnatal maternal drug use was related to CBCL scores The amount of alcohol exposure did not predict behavioral outcomes. However, binge drinking was related to challenging behaviors All factors were associated with aggression

Direct

CBCL

NA

CBCL

NA

Bailey et al. (2004)

TRF

NA

499 children with prenatal alcohol exposure

Bendersky et al. (2006)

LRRH; CBCL

Hitting or kicking a punching doll

206 children. 83 with prenatal cocaine exposure

Bendersky and Lewis (1998)

NA

77 children. 51 with prenatal cocaine exposure. 26 unexposed controls

Bennett et al. (2002)

CBCL

Taking a cookie when told not to. Scored on Latency to reach, take, and eat the cookie NA

Brown et al. (2004)

CBCL

NA

Accornero, Anthony, Morrow, Xue, and Bandstra (2006) Accornero et al. (2002)

223 children. 85 with prenatal cocaine exposure, 61 of which also had alcohol exposure. 138 without prenatal cocaine exposure, 21 of which had prenatal alcohol exposure 146 children. 83 with prenatal cocaine exposure, 49 of which lived with parent. 63 unexposed

Evaluated the effects of both prenatal cocaine exposure and postnatal environment on challenging behaviors

Evaluated the effects of both prenatal cocaine exposure and postnatal caregiver environment at 2 years of age

Cocaine exposure resulted in lower latencies to reach, take, and eat the cookie. The amount of time the parent interacted with the child significantly impacted child behavior

Cocaine specific effects were low to nonexistent. Mother depression and harsh discipline were the highest predictors of challenging behaviors CBCL scores were lower for exposed children who were living with nonparents than those who were. Any differences found in CBCL scores were related to postnatal care

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Participants

Indirect

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488

Table 1 (Continued ) Authors

Assessment

Description

Results

68 mother-child dyads. 25 with alcohol exposure throughout pregnancy, 21 with no exposure, and 22 with early exposure who stopped drinking after educational interventions 100 children with prenatal cocaine/opiate exposure. 49 received intervention, 51 standard care

Evaluated the role that amount of alcohol had on challenging behavior

Significant differences were found among groups for challenging behaviors. However, these differences were no longer significant after controlling for current maternal alcohol use The intervention group showed lower CBCL scores for externalizing, internalizing, depression, and total score

Indirect

Direct

Brown et al. (1991)

CBCL

Impulsivity, activity level, aggression, compliance

Butz et al. (2001)

CBCL

NA

Chasnoff et al. (1998)

CBCL

NA

170 children. 95 with prenatal cocaine/ polydrug exposure, 75 unexposed

Delaney-Black et al. (2004)

PROBS-14

NA

473 children. 204 with prenatal cocaine exposure

Delaney-Black et al. (1998)

CTRS; PROBS-14

NA

102 children. 27 with prenatal cocaine exposure

Delaney-Black et al. (2000)

TRF

NA

471 children (parent–child dyads). 201 with prenatal cocaine exposure

Dennis et al. (2006)

NSSQ, SEI

174 mother-child dyads. 65 with Compliance; making demands; prenatal cocaine exposure, 109 unexposed complaining; disruptions; aggression (hitting or kicking)

Evaluated the effects of parent support and education upon the emotional-behavioral outcomes of prenatally exposed children at 36 months Evaluated the potency and direction of biological and environmental factors on cognitive and behavioral development in children at 4, 5, and 6 years old Evaluated the degree to which quantity of exposure and gender moderated behavioral outcomes Evaluated the effect of prenatal cocaine exposure on measures of problem behaviors Evaluated the relationship between behavior problems and prenatal cocaine exposure

Evaluated frustration reactivity and regulation among children with prenatal cocaine exposure

Children with prenatal exposure had much higher ratings of challenging behaviors. A path analysis indicated that the home environment did not effect CBCL scores Persistent exposure showed the most marked differences in challenging behaviors. Cocaine exposure was related to challenging behaviors only in boys The cocaine exposure group showed higher scores on both the CTRS and PROBS Cocaine exposure alone did not show significant differences in TRF scores. However, gender did show a significant difference. When gender differences were evaluated relative to cocaine exposure, exposed males were twice as likely as controls to show behavior problems Children with prenatal cocaine exposure were quicker to engage in challenging behaviors

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Participants

Study questionnaire

NA

Gentry et al. (1998)

CBCL

NA

Griffith et al. (1994)

CBCL

NA

Hawley et al. (1995)

CBCL

NA

Heller et al. (1996)

NA

Kilbride et al. (2006)

CBCL; PCERA

Demand, request, question, positive feedback, agreement, disagreement, providing information, and other NA

Lynch et al. (2003)

SSRI; CBCL

Mattson and Riley (2000) Messinger et al. (2004)

8285 mothers of children with or without prenatal alcohol, marijuana, or nicotine exposure 3 children diagnosed with FAS and ADHD

Five mother–child dyads. All children were exposed prenatally to cocaine and other substances

Evaluated outcomes from prenatal exposure to alcohol, marijuana, or nicotine at 3 years old Evaluated challenging behaviors among school-age children with prenatal alcohol exposure Evaluated the developmental and behavioral outcome of prenatal substance exposure at 3-years Evaluated challenging behaviors among preschool children with and without prenatal cocaine exposure Evaluated mother–child dyads to identify behavior patterns and antecedent adult behaviors

51 parent–child dyads. 39 with prenatal cocaine exposure. 12 unexposed

Evaluated the effects of case management on the development of challenging behaviors

NA

250 adolescent-mother dyad with differential prenatal alcohol exposure

CBCL

NA

BRS

NA

88 children between ages 4-16 years: 55 prenatally exposed to alcohol, 33 controls 1227 infants, 522 with prenatal cocaine exposure, 98 with prenatal opiate exposure

Examined the incidence of delinquent behavior among adolescents prenatally exposed to alcohol relative to postnatal environmental factors Evaluated challenging behaviors among children with prenatal alcohol exposure Evaluated the effects of prenatal cocaine and opiate exposure on mental, motor, and behavioral outcomes longitudinally between 1 and 3 years old

99 children with prenatal cocaine exposure, 24 with polydrug exposure, 25 unexposed children 44 preschool children. 20 with prenatal cocaine exposure, 24 unexposed

Prenatal alcohol exposure was related to difficulty of child management and number of tantrums All three children exhibited behavior dysfunction in four or more categories of challenging behavior The drug exposure groups showed greater aggressive, destructive, and externalizing behaviors Found significant differences in emotional and behavioral status

Not all dyads displayed negative interactions. Two of the five showed significant negative interactions, of which both showed clear parental antecedents

Pre and post ratings of challenging behaviors did not differ among children with and without prenatal cocaine exposure. Differences were observed in parent–child interactions Did not find a relationship to prenatal alcohol exposure and delinquent behavior. Postnatal Environmental factors were significant Found significant differences among groups on measure of challenging behavior After controlling for birth weight and environmental risks, prenatal exposure was not related to mental, motor, or behavioral deficits

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Faden and Graubard (2000)

489

490

Table 1 (Continued ) Authors

Assessment

Description

Results

Evaluated the degree to which gender and alcohol exposure would moderate teacher-reported behavior Evaluated the impact of a child friendship training program vs. a delayed treatment control for children with FASD Evaluated the occurrence of challenging behaviors among adolescents with differential levels of prenatal alcohol exposure Evaluated the effects of prenatal cocaine exposure on challenging behaviors at 1 and 3 years

Cocaine plus alcohol exposure resulted in higher challenging behaviors, but not for cocaine alone. Gender also altered the topography of challenging behaviors Children with FASD showed a clear improvement in social skills and significant reduction in challenging behaviors Adolescents with greater prenatal alcohol exposure and exposure to binge drinking showed greater challenging behaviors

Indirect

Direct

Nordstrom Bailey et al. (2005)

TRF

NA

499 infants, 214 with prenatal cocaine and alcohol exposure

O’Connor et al. (2006)

SSRS

NA

100 children with fetal alcohol spectrum disorders

Olson et al. (1997)

LCS; CBCL

NA

464 children with differential prenatal alcohol exposure

Richardson (1998)

CBCL

NA

Richardson, Conroy, and Day (1996)

CBCL

NA

325 mother-child dyads. Cocaine use during pregnancy varied by trimester and frequency of use 551 mother-child dyads, 28 with prenatal cocaine exposure

Roebuck, Mattson, and Riley (1999)

PIC

NA

64 children, 32 with prenatal alcohol exposure, 32 unexposed controls

Savage et al. (2005)

TRF

NA

67 children, 31 with prenatal cocaine exposure, 36 unexposed controls

Schonfeld, Mattson, and Riley (2005)

SMM; CDQ

NA

56 children, between ages 10–18: 27 alcohol-exposed, 29 controls

Sood et al. (2001)

CBCL

NA

506 parent–child dyads. 66 with moderate to heavy prenatal alcohol exposure, 323 mild exposure, 117 unexposed

Examined challenging behaviors among children with and without prenatal cocaine exposure at age 6 Examined behavioral and psychosocial profiles of children with prenatal alcohol exposure Examined attention, impulse control, and challenging behaviors among children with prenatal cocaine exposure Examined challenging behavior among children with and without FASC Evaluated the effects of low to high levels of prenatal alcohol exposure of challenging behaviors

First trimester cocaine use was related increased challenging behaviors

Once environmental factors were controlled, challenging behaviors did not differ among groups Differences between groups were significant on all PIC subscales, except hyperactivity Significant differences were found for internalizing behaviors only Delinquency was higher in the alcohol-exposed group, and specific sociomoral values were predictive of delinquent behavior Exposure groups differed significantly on externalizing, internalizing, and total challenging behaviors

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Participants

CBCL

NA

Steinhausen and Spohr (1998)

TRF & CBCL

NA

506 parent–child dyads. 117 without prenatal alcohol exposure, 95 of which had prenatal cocaine exposure. 389 with prenatal alcohol exposure, 197 of which also had prenatal cocaine exposure 27 (CBCL) & 16 (TRF) children with prenatal alcohol exposure

Steinhausen, Williams, DBC Metzke, and Spohr (2003)

NA

12 children with moderate FAS, 26 with mild FAS, and 15 matched controls

Streissguth, Barr, and Sampson (1990)

CPRS; MPRS

NA

482 children, 154 with prenatal alcohol exposure, 328 unexposed

Warner et al. (2006)

CPRS; ECBIIS NA

256 children, 123 with prenatal cocaine exposure, 133 unexposed

Examined the interaction of prenatal alcohol exposure and gender on childhood challenging behaviors after prenatal cocaine exposure

Prenatal cocaine exposure was associated with adverse effects on exposed child behavior, which was moderated by gender as well as prenatal alcohol exposure

Examined the long-term outcome of prenatal alcohol exposure

High t-scores were found for most indices of the CBCL and TRF. The most prominent elevations were for social and attention problems Examined differences among the three Significant differences were found between groups on the subscales of the DBC the control and FAS groups on all subscales of the DBC. These differences were most noted for the disruptive and antisocial scales Examined challenging behavior among Parents and teachers rated challenging 7-year old children with prenatal behavior higher for a greater percentage of alcohol exposure exposed children relative to controls Examined challenging behaviors among Caregiver depression was the only significant 3-year old children with prenatal cocaine predictor of challenging behaviors exposure

BRS: Behavior Rating Scale; CBCL: Child Behavior Checklist; CDQ: Conduct Disorder Questionnaire; CPRS: Conners’ Parent Rating Scale; CTRS: Conners’ Teacher Rating Scale; DBC: Developmental Behavior Checklist; ECBIIS: Eyberg Child Behavior Inventory Intensity Scale; LCS: Lifestyles Choices Survey; LRRH: Leifer-Roberts Response Hierarchy; MPRS: Myklebust Pupil Rating Scale; NSSQ: Norbeck Social Support Questionnaire; PCERA: Parent–Child Early Relational Assessment; PIC: Personality Inventory for Children; PROB-14: Problem Behavior Scale 14; SEI: Social Environment Inventory; SMM: Socio-Moral reflection Measure; SSRI: Seattle Self-Report Instrument; SSRS: Social Skills Rating System; TRF: Teacher Report Form.

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Sood et al. (2005)

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A review of the studies presented in Table 1 shows that while a number of assessment scales have been used, the Child Behavior Checklist (CBCL; Achenbach, 1991a) is the most prominent, followed by the Teacher Report Form (TRF; Achenbach, 1991b) of the same battery. Few studies employed measures that were focused on challenging behavior such as the PROB14 (Delaney-Black et al., 2004). Direct observations were used infrequently. We found five studies that used direct observations of challenging behavior, with all using specific target behavior definitions. The findings of studies examining the behavioral outcomes of prenatal exposure to cocaine or alcohol are summarized in Tables 2 and 3, respectively. No studies were found that addressed challenging behaviors among children with a focus on prenatal heroin exposure. A number of studies included children who were exposed to more than one substance. In such cases, if the study topic focused on prenatal exposure of a particular substance the study was reported on that respective table. For example, Sood et al. (2005) reported on the moderating effects of gender and prenatal alcohol exposure on the behavioral outcomes of children exposed prenatally to cocaine, therefore, this study is reported in Table 2. Information regarding the substance of exposure for each study is available in Table 1. 2.1. Prenatal cocaine exposure Twenty-one of the 37 articles on challenging behavior focused on prenatal cocaine exposure. Thirteen studies reported a significant effect on challenging behavior from prenatal cocaine exposure. Nine studies did not find an independent effect on problem behavior from prenatal cocaine exposure once confounding variables such as the postnatal environment were controlled Table 2 Breakdown of cocaine impact, environmental impact, and if environment was studied Study

Cocaine impact

Environment impact

Environment controlled/examined

Accornero et al. (2006) Accornero et al. (2002) Bendersky et al. (2006) Bendersky and Lewis (1998) Bennett et al. (2002) Brown et al. (2004) Chasnoff et al. (1998) Delaney-Black et al. (2004) Delaney-Black et al. (1998) Delaney-Black et al. (2000) Dennis et al. (2006) Griffith et al. (1994) Hawley et al. (1995) Heller et al. (1996) Kilbride et al. (2006) Messinger et al. (2004) Nordstrom Bailey et al. (2005) Richardson (1998) Richardson et al. (1996) Savage et al. (2005) Sood et al. (2005) Warner et al. (2006)

No No Yes Yes No No Yes Yes Yes Yes Yes Yes Yes No No No Yes Yes No Yes Yes No

Controlled but Yes Yes Yes Yes Yes No Controlled but Not Examined Yes Controlled but Not Examined Not Examined Yes Yes Controlled but Controlled but Controlled but Controlled but Not Examined Controlled but Yes

Controlled Examined Examined Examined Examined Examined Examined Controlled No Examined Controlled No No Examined Examined Controlled Controlled Controlled Controlled No Controlled Examined

not examined

not examined

not examined

not not not not

examined examined examined examined

not examined

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Table 3 Breakdown of alcohol impact, environmental impact, and if environment was studied Study

Alcohol impact

Environment impact

Environment controlled/examined

Nordstrom Bailey et al. (2005) Brown et al. (1991) Faden and Graubard (2000) Gentry et al. (1998) Lynch et al. (2003) Mattson and Riley (2000) Olson et al. (1997) Roebuck et al. (1999) Schonfeld et al. (2005) Sood et al. (2001) Steinhausen and Spohr (1998) Steinhausen et al. (2003) Streissguth et al. (1990)

Yes Yes Yes Yes No Yes Yes Yes Yes Yes Yes Yes Yes

Controlled but Yes Not examined Not examined Yes Controlled but Controlled but Not examined Not examined Yes Not examined Not examined Controlled but

Controlled Examined No No Examined Controlled Controlled No No Examined No No Controlled

not examined

not examined not examined

not examined

for. Of the 10 studies that examined the effect of the postnatal environment on problem behaviors, nine found a significant impact (Table 2). Four studies were identified that reported on problem behaviors but did not control for or examine the impact of the postnatal environment (Delaney-Black et al., 1998; Griffith, Azuma, & Chasnoff, 1994; Hawley, Halle, Drasin, & Thomas, 1995; Savage, Brodsky, Malmud, Giannetta, & Hurt, 2005). An evaluation of prenatal polydrug exposure and outcome at 3-years of age was conducted by Griffith et al. (1994). Regarding challenging behaviors, the authors found that exposed children were rated higher on a measure of aggressive, destructive, and other externalizing behaviors than nonexposed children. However, as this was an early study evaluating behavioral outcomes, the authors did not evaluate the role of the home environment of continued parental drug use as later studies have. Likewise, Hawley et al. (1995) found significant differences among children with and without prenatal cocaine exposure. While they were one of the first to discuss the possible impact of the postnatal environment such as maternal characteristics, their study evaluating exposed children did not control for the effect of the postnatal environment. More recently, researchers have included the postnatal environment among the confounding factors that need to be controlled. Further, an emphasis has been made on factors that may moderate the effect of prenatal cocaine exposure. Among these studies, a number of researchers have reported on the independent effect of prenatal cocaine exposure on childhood challenging behaviors. However, of the 18 studies that examined or controlled for the effects of the postnatal environment, 9 found prenatal cocaine exposure to have an independent effect, whereas 9 did not (Table 2). Among the studies that found prenatal cocaine exposure to have an independent effect, 5 also reported on the moderating effects of other factors such as prenatal alcohol exposure or gender (Dennis, Bendersky, Ramsay, & Lewis, 2006; Nordstrom Bailey et al., 2005; Sood et al., 2005). For example, Dennis et al. (2006) used direct observation coupled with indirect assessments of the home environment to evaluate the degree to which prenatal cocaine exposure would be associated with greater frustration reactivity and greater difficulty regulating behavior. After controlling for environmental effects, the authors found that prenatally exposed children were quicker to express frustration and were more disruptive. Their effects were strongest among prenatally exposed boys relative to prenatally exposed girls.

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Similarly, Delaney-Black et al. (2000) evaluated teacher ratings of the behavior of children with and without prenatal cocaine exposure. After controlling for gender, prenatal exposure to other substances, and significant postnatal environment factors, they found that boys with prenatal cocaine exposure showed much higher scores on externalizing and delinquent behavior. Delaney-Black et al. (2004) further evaluated the degree to which the quantity of exposure and gender would moderate the impact of prenatal cocaine exposure on developing behavior problems. They found that persistent exposure showed the greatest differences in PROB-14 scores. Additionally, cocaine exposure was related to behavior problems in the male participants, suggesting that female gender may serve a protective role. Further evidence supporting a moderating effect of gender and prenatal alcohol exposure upon the effects of prenatal cocaine exposure was presented by Nordstrom Bailey et al. (2005). They found that among children with varying degrees of alcohol and cocaine exposure, boys with both prenatal alcohol and cocaine exposure had significantly higher delinquent behavior scores as rated by teachers than boys without prenatal cocaine exposure. Additionally, prenatal cocaine exposure resulted in significant externalizing behavior scores among boys who also had prenatal alcohol exposure but not among boys with cocaine exposure alone. This study highlights the importance of considering the combined effect of prenatal alcohol and cocaine exposure. Data on caregiver report of challenging behaviors also supports a moderating role of gender and prenatal alcohol exposure on the behavioral effects of prenatal cocaine exposure. Sood et al. (2005) presented data on children who varied in the presence or absence of both prenatal cocaine exposure or prenatal alcohol exposure. By stratifying their results based upon alcohol and cocaine exposure, the authors found that girls with prenatal cocaine exposure but not prenatal alcohol exposure, showed significantly elevated scores on parent report of challenging behaviors. This study is also of particular note for finding an independent effect of prenatal cocaine exposure, after controlling for confound environmental and prenatal factors. Among the factors that may moderate the effect of prenatal cocaine exposure has been variables within the postnatal environment. While studies have shown an independent effect of prenatal cocaine exposure on childhood challenging behaviors, the importance of the postnatal environment has increasingly been shown to be an important consideration. We found 10 studies that directly examined the role of the postnatal environment upon challenging behaviors in children with prenatal cocaine exposure. Of the 10 studies, 9 found the postnatal environment to have an impact upon challenging behaviors (Accornero, Morrow, Bandstra, Johnson, & Anthony, 2002; Bendersky, Bennett, & Lewis, 2006; Bendersky & Lewis, 1998; Bennett, Bendersky, & Lewis, 2002; Brown et al., 2004; Delaney-Black et al., 2000; Heller, Sobel, & Tanaka-Matsumi, 1996; Kilbride, Castor, & Fuger, 2006; Warner et al., 2006), one did not (Chasnoff et al., 1998). The relationship of prenatal cocaine exposure and impulse control among 2-year old children was evaluated by Bendersky and Lewis (1998). In their study, an examiner gave a toy to the child and placed a cookie on a table then left the child and their mother in the examination room. Latency to reach for, take, and eat the cookie was measured by direct observation as an indication of impulse control. They found that children with prenatal cocaine exposure had a shorter latency to take the cookie than unexposed controls. Of particular note though for the purpose of this review, was that the level of interaction the mother had with the child during the wait period was a significant factor in the latency to take the cookie. In 2002, Bennett and colleagues reported on the outcome of prenatal exposure to cocaine at 4 years of age. Based upon their previous results, they hypothesized that prenatal cocaine exposure would predict child emotional-behavior problems after all other variables had been controlled. Further, they hypothesized that psychosocial variables would predict IQ and emotional-

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behavioral adjustment better than cocaine exposure alone. They found mixed results for the predictive use of cocaine exposure, showing an impact on lower IQ scores and verbal reasoning scores only among males. Regarding environmental factors though, maternal harsh discipline, maternal depressive symptoms, and environmental risk predicted externalizing problems. In a related study, Accornero et al. (2002) examined the behavioral outcome of preschoolers exposed prenatally to cocaine, with special attention to the role of maternal drug use in the postnatal environment. They hypothesized that prenatal cocaine exposure would relate to behavior at 5 years of age. Second, they hypothesized that recent maternal drug use and psychological distress would relate to behavior difficulties as measured by the CBCL. They found that the postnatal environment was the key factor and that cocaine exposure alone was not sufficient to predict behavior problems. Their results indicated that it was the drug use and environment of psychological distress that was the most important factor. Brown et al. (2004) evaluated the effect of prenatal cocaine exposure among 2-year-old children who were living either in parental or non-parental care. They found that the postnatal caregiver was the most important factor in considering behavior problems as measure by the CBCL. In their sample, living with non-parents was a protective factor for not developing challenging behaviors among children with prenatal cocaine exposure. This study highlights the importance of the postnatal caregiver in the development of challenging behaviors. Bendersky et al. (2006) report on the occurrence of aggression among 206 children prenatally exposed to cocaine. They used multiple methods of measuring aggression and hypothesized that a number of risk factors would increase aggression at age 5, including male gender, prenatal cocaine exposure, and a high-risk environment. A multiple regression analysis indicated that cocaine exposure, gender, and environmental risk were all related the aggression score. Heller et al. (1996) reported on one of the few attempts to evaluate problems in parent–child interactions and provide direction for future treatment. By conducting direct behavior observations the authors were able to evaluate parent–child interactions and describe patterns of interactions. They found that two of the five parent–child dyads showed clear patterns of negative parental antecedents to the interaction breakdown. Structural equation modeling is a powerful to tool to evaluate predictors of childhood challenging behaviors. Warner et al. (2006) tested a model to predict challenging behaviors among children with prenatal cocaine exposure that included a number of prenatal and postnatal variables such as child sex, prenatal drug exposure, the quality of the home environment, and caregiver depression. They found that caregiver depression was the only significant predictor of challenging behaviors. The one study that did not find an impact from the postnatal environment upon problem behaviors was conducted by Chasnoff et al. (1998), who reported on the behavioral outcome of prenatal exposure to cocaine and other drugs. They found that cocaine exposure was a significant factor in the development of behavior problems as measured by the CBCL. They report that a path analysis indicated the relative lack of causality that the quality of the home environment had on CBCL scores. 2.2. Prenatal alcohol exposure Thirteen of the 37 articles focused on the effects of prenatal alcohol exposure on challenging behaviors. Twelve of the 13 studies found an independent effect of prenatal exposure on challenging behavior. Of the 13 studies, 3 directly examined the role of the postnatal environment on challenging behaviors, four controlled for but did not examine postnatal factors, and six did

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not control or examine environmental factors. Table 3 displays the findings of these studies relative to the environmental variables controlled for or examined. In a carefully controlled analysis of behavior problems subsequent to prenatal alcohol exposure, Bailey et al. (2004) found that the amount of prenatal alcohol exposure was not related to behavior outcomes. However, significant effects were found for the pattern of alcohol exposure such that binge drinking was a much higher risk factor for behavior problems. These findings highlight the need for a multifaceted approach to studying prenatal exposure; simply looking at the overall amount of alcohol exposure would have obscured their results and suggested a lesser impact than was found. Faden and Graubard (2000) evaluated behavioral and developmental outcomes of prenatal exposure to alcohol, marijuana, or nicotine. Their results indicated that parental report of activity level, greater difficulty of child management, tantrums, and eating problems were related to prenatal exposure. Postnatal environmental factors were not evaluated. Mattson and Riley (2000) evaluated the behavioral effects of prenatal alcohol exposure on the development of challenging behavior with particular effort to control for significant postnatal factors such as intellectual functioning and socioeconomic status. They found that after controlling for confounding variables, prenatal alcohol exposure had an independent effect upon challenging behaviors as reported by caregivers. Steinhausen and Spohr (1998) reported on the long-term outcome of prenatal alcohol exposure. Challenging behaviors were reported by parents and teachers on the CBCL and TRF. Mean t-scores showed elevations on social problems and attention problems on the CBCL and social problems, thought problems, attention problems, and delinquent problems on the TRF. However, these results are limited by lack of a control group for comparison. Steinhausen et al. (2003) examined differences on subscales of the Developmental Behavior Checklist (DBC) among three groups of children, 12 with moderate prenatal alcohol syndrome, 26 with mild FAS, and 15 matched controls. They found significant differences among groups for all subscales of the DBC, with most notable differences on the disruptive and antisocial subscales. Only three studies directly examined the effect of the postnatal environment on problem behaviors among children prenatally exposed to alcohol (Brown et al., 1991; Lynch, Coles, Corley, & Falek, 2003; Sood et al., 2001). Of these studies, all three found the postnatal environment to have a significant impact upon problem behaviors. Lynch et al. (2003) examined delinquency as an outcome of prenatal exposure to alcohol. Their results indicated that prenatal exposure to alcohol did not directly relate to delinquency, but rather that life stress, drug use, and parental supervision were much more significant in predicting delinquency. They highlight the importance of controlling for psychosocial risk factors in the evaluation of behavioral outcomes of prenatal exposure. In another study, the effects of prenatal alcohol exposure on attention and behavior was examined Brown et al. (1991). The authors evaluated the role that amount of alcohol exposure had on behavioral outcomes among school age children. Significant effects were noted for both internalizing and externalizing behaviors. However, when current maternal drinking was controlled, the effects were no longer significant. Finally, Sood et al. (2001) evaluated the dose–response effect of prenatal alcohol exposure for adverse child behavior outcomes at 6 and 7 years of age. They found that children with any level of prenatal alcohol exposure were rated higher on both internalizing and externalizing behavior problems by their caregivers. These differences were even present among children with low levels of prenatal alcohol exposure. While maternal psychopathology and child gender were

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strong predictors of challenging behavior, the authors found that prenatal alcohol exposure also had an independent effect upon behavior. 2.3. Treatment studies Only 3 of the 37 studies on challenging behavior evaluated treatment outcomes (Butz et al., 2001; Kilbride et al., 2006; O’Connor et al., 2006). Of these three studies, all the researchers found that by manipulating the postnatal environment through parent education or child skills training, challenging behaviors were decreased. Butz et al. (2001) report one of the few studies examining treatment of child behavior problems in children with prenatal drug exposure through the means of parent education and follow-up. Their study demonstrates the efficacy of a nurse intervention, consisting of parent support and education to reduce parent ratings of child challenging behavior among children at 36 months of age. Kilbride et al. (2006) evaluated the outcome of early case management on the behavioral outcome of children with prenatal cocaine exposure. While they did not find any differences on parent-reported challenging behaviors relative to prenatal cocaine exposure status, they did find that mother-child dyads in the case management group showed more positive interactions than the dyads receiving routine care. In one of the few treatment studies for challenging behaviors in children with prenatal drug or alcohol exposure, O’Connor et al. (2006) demonstrated the efficacy of Child Friendship Training (CFT) to improve social skills and reduce challenging behavior. In their study, the CFT group showed a significant improvement in challenging behavior in contrast to the Delayed Treatment Control (DTC) group. When CFT was implemented in the DTC group a similar reduction in challenging behavior was found. 3. Discussion The outcome of prenatal exposure to substances of abuse has received significant attention from researchers. However, few studies have examined challenging behaviors as an outcome of prenatal exposure. Further still, is the lack of studies addressing the treatment of challenging behavior among children with prenatal exposure. Of the 241 studies on prenatal exposure that were identified for this review, only three studies were found that evaluated some form of intervention. The way in which challenging behaviors have been measured in studies is also of note. By far, the CBCL has been the most popular method for assessing challenging behaviors among children with prenatal exposure. The CBCL is a measure that gives a broad assessment of child behavior and is typically completed by parents. The CBCL may be categorized as a broad-band measure of child behavior. Broad-band measures have the advantage of assessing a number of domains in a relatively short amount of time. However, a drawback is the lack of detailed information that a more narrow-band measure would provide. Narrow-band measures have the advantage of a restricted scope of behaviors measured but a relatively rich amount of information gathered regarding those behaviors. Measures such as the Behavior Problems Inventory (Rojahn, Matson, Lott, Esbensen, & Smalls, 2001) and the PROB-14 (Delaney-Black et al., 2000) are good examples of such assessment instruments. Likewise, studies that use direct observation of clearly defined behaviors also provide richer information regarding challenging behaviors. Regarding the studies on prenatal cocaine exposure reviewed in the present study, six of the nine studies that

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did not find an independent effect on challenging behaviors measured behavior with the CBCL. Of the studies that found an independent effect from prenatal cocaine exposure, less than half used the CBCL. Among the studies that found a significant impact from prenatal cocaine exposure, the use of narrow-band measures and direct observations were much more prominent. It is likely that the behavioral effects of prenatal cocaine exposure are significant yet subtle and require more sensitive methods of measurement. Another finding of our review is that the role of the postnatal environment in the emergence of challenging behavior has received increasing attention from researchers. With regard to prenatal cocaine exposure, once environmental factors are examined, any independent effect of prenatal cocaine exposure is significantly reduced. Regarding the studies that controlled or examined the role of the postnatal environment in developing challenging behavior among children with prenatal cocaine exposure, only half found an independent effect from cocaine exposure whereas 90% of the studies that the examined postnatal environmental effects found significant and usually more prominent effects on challenging behaviors. Apart from the results of Chasnoff et al. (1998), every researcher that examined the impact of the postnatal environment found significant effects. A slightly different outcome was found for studies on prenatal alcohol exposure. First, fewer studies have been conducted to evaluate challenging behaviors among this group of children. Of these studies, almost all have found prenatal alcohol exposure to have an independent effect on challenging behavior. However, as was found with the cocaine studies, the postnatal environment plays a large role in the development of challenging behaviors. Of the studies that evaluated the role of the postnatal environment, all found a significant impact upon challenging behaviors. A number of studies on challenging behavior specifically excluded persons with low IQ scores from participation in their sample (e.g., Sood et al., 2001). However, the diagnosis of intellectual disability occurs frequently among persons with fetal alcohol syndrome (Burd, CotsonasHassler, Martsolf, & Kerbeshian, 2003; Coles, 2006). This is of particular concern because as intellectual functioning declines reports of challenging behavior increase (Holden & Gitlesen, 2006). It is likely that children with comorbid prenatal exposure and as a diagnosis of intellectual disability would show higher rates of challenging behaviors. While excluding participants with intellectual disabilities may improve experimental control in one domain, it is likely to result in an underestimation of challenging behaviors. It is notable that only three studies were found that addressed interventions for the reduction of challenging behavior; however, all three found positive results. Both Butz et al. (2001) and Kilbride et al. (2006) used interventions that targeted parent variables such as emotional and financial support and parenting education. Both were found to either improve parent–child interactions (Kilbride et al., 2006) or improve challenging behavior (Butz et al., 2001). O’Connor et al. (2006) targeted both parent and child skills and found significant reduction in challenging behavior and improvement in social skills. The studies in this review serve to highlight the importance of the postnatal environment in the development of challenging behaviors. Overall, the studies reviewed found that prenatal exposure, particularly to alcohol, has a significant effect upon challenging behaviors; however, the role of the postnatal environment should not be neglected. Specific environmental risk factors identified include recent maternal drug use (Accornero et al., 2002), high life stress and low parent supervision (Lynch et al., 2003), maternal psychopathology (Sood et al., 2001), custody changes, current drug use in home, and violence exposure (Delaney-Black et al., 2000). While a number of researchers have described models to explain the neurological impact of exposure to predict particular behavioral deficits, the effects of parenting skills, at risk environments, and

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behavioral principles upon the emergence of challenging behaviors should not be overlooked. Similarly, the few treatment studies showed relatively powerful effects (Butz et al., 2001; O’Connor et al., 2006). With more targeted behavioral interventions specific challenging behaviors could be addressed. The treatment of challenging behavior in this population is an area in need of further investigation. Future research would benefit from further evaluation of the interaction between prenatal exposure variables and postnatal environmental variables. The use of narrow-band assessment instruments and direct observation of behavior will improve the detection of subtle yet significant behavioral outcomes from prenatal drug exposure. In light of the significant role that the environment plays in the development of challenging behaviors, it is clear that more treatment studies are needed to address challenging behaviors through a behavioral approach. Direct interventions for both parents and exposed children should do much to decrease or prevent challenging behavior, and ultimately, reducing the impact of prenatal exposure on the lives of exposed children. Acknowledgements The authors would like to thank Joe Wilson, Danielle Gureghian, Kim Kirby and Eileen Klein for their assistance with data collection, and Carol Fendlay for editorial support. References Accornero, V. H., Anthony, J. C., Morrow, C. E., Xue, L., & Bandstra, E. S. (2006). Prenatal cocaine exposure: An examination of childhood externalizing and internalizing behavior problems at age 7 years. Epidemiologia e Psichiatria Social, 15, 20–29. Accornero, V. H., Morrow, C. E., Bandstra, E. S., Johnson, A. L., & Anthony, J. C. (2002). Behavioral outcome of preschoolers exposed prenatally to cocaine: Role of maternal behavioral health. Journal of Pediatric Psychology, 27, 259–269. Achenbach, T. M. (1991a). Manual for the child behavior checklist/4–18 & 1991 profile. Burlington: University of Vermont, Department of Psychiatry. Achenbach, T. M. (1991b). Manual for the teacher’s report form and 1991 profile. Burlington: University of Vermont, Department of Psychiatry. Bailey, B. N., Delaney-Black, V., Covington, C. Y., Ager, J., Janisse, J., Hannigan, J. H., et al. (2004). Prenatal exposure to binge drinking and cognitive and behavioral outcomes at age 7 years. American Journal of Obstetrics and Gynecology, 191, 1037–1043. Bard, K. A., Coles, C. D., Platzman, K. A., & Lynch, M. E. (2000). The effects of prenatal drug exposure, term status, and caregiving on arousal and arousal modulation in 8 week-old infants. Developmental Psychobiology, 36, 194–212. Barr, G. A., & Jones, K. J. (1994). Opiate withdrawal in the infant. Neurotoxicology and Teratology, 16, 219–225. Beeghly, M., Martin, B., Rose-Jacobs, R., Cabral, H., Heerin, T., Augustyn, M., et al. (2006). Prenatal cocaine exposure and children’s language functioning at 6 ant 9.5 years: Moderating effects of child age, birthweight and gender. Journal of Pediatric Psychology, 31, 98–115. Bendersky, M., & Lewis, M. (1998). Prenatal cocaine exposure and impulse control at two years. Annals of the New York Academy of Sciences, 365–367. Bendersky, M., Bennett, D., & Lewis, M. (2006). Aggression at age 5 as a function of prenatal exposure to cocaine, gender, and environmental risk. Journal of Pediatric Psychology, 31, 71–84. Bennett, D. S., Bendersky, M., & Lewis, M. (2002). Children’s intellectual and emotional-behavioral adjustment at 4 years as a function of cocaine exposure, maternal characteristics, and environmental risk. Developmental Psychology, 3, 648–658. Brown, J. V., Bakeman, R., Coles, C. D., Platzman, K. A., & Lynch, M. E. (2004). Prenatal cocaine exposure: A comparison of 2-year-old children in parental and nonparental care. Child Development, 75, 1282–1295.

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