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Association of Prenatal and Childhood Blood Lead Concentrations with Criminal Arrests in Early Adulthood John Paul Wright1, Kim N. Dietrich2*, M. Douglas Ris3, Richard W. Hornung3, Stephanie D. Wessel2, Bruce P. Lanphear3, Mona Ho3, Mary N. Rae2 1 Cincinnati Children’s Environmental Health Center, Division of Criminal Justice, University of Cincinnati, Cincinnati, Ohio, United States of America, 2 Cincinnati Children’s Environmental Health Center, Division of Epidemiology and Biostatistics, Department of Environmental Health, University of Cincinnati College of Medicine, Cincinnati, Ohio, United States of America, 3 Cincinnati Children’s Environmental Health Center, Cincinnati Children’s Hospital Medical Center, Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, United States of America Funding: This work was supported by grants from the National Institute of Environmental Health Sciences (PO1-ES011261 and RO1-ES015559– 01) and the United States Environmental Protection Agency (R82938901). The funding agencies played no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: Two of the study’s authors, BPL and RH, are on the editorial board of PLoS Medicine. BPL and KND sporadically serve as expert witnesses without personal financial gain. Academic Editor: John Balmes, University of California San Francisco, United States of America Citation: Wright JP, Dietrich KN, Ris MD, Hornung RW, Wessel SD, et al. (2008) Association of prenatal and childhood blood lead concentrations with criminal arrests in early adulthood. PLoS Med 5(5): e101. doi:10.1371/journal.pmed.0050101 Received: August 14, 2007 Accepted: March 18, 2008 Published: May 27, 2008 Copyright: 2008 Wright et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Abbreviations: ADHD, attention deficit hyperactivity disorder; CI, confidence interval; RR, rate ratio; SES, socioeconomic status * To whom correspondence should be addressed. E-mail: kim.dietrich@ uc.edu ABSTRACT Background Childhood lead exposure is a purported risk factor for antisocial behavior, but prior studies either relied on indirect measures of exposure or did not follow participants into adulthood to examine the relationship between lead exposure and criminal activity in young adults. The objective of this study was to determine if prenatal and childhood blood lead concentrations are associated with arrests for criminal offenses. Methods and Findings Pregnant women were recruited from four prenatal clinics in Cincinnati, Ohio if they resided in areas of the city with a high concentration of older, lead-contaminated housing. We studied 250 individuals, 19 to 24 y of age, out of 376 children who were recruited at birth between 1979 and 1984. Prenatal maternal blood lead concentrations were measured during the first or early second trimester of pregnancy. Childhood blood lead concentrations were measured on a quarterly and biannual basis through 6.5 y. Study participants were examined at an inner-city pediatric clinic and the Cincinnati Children’s Hospital Medical Center in Cincinnati, Ohio. Total arrests and arrests for offenses involving violence were collected from official Hamilton County, Ohio criminal justice records. Main outcomes were the covariate-adjusted rate ratios (RR) for total arrests and arrests for violent crimes associated with each 5 lg/dl (0.24 lmol/l) increase in blood lead concentration. Adjusted total arrest rates were greater for each 5 lg/dl (0.24 lmol/l) increase in blood lead concentration: RR ¼ 1.40 (95% confidence interval [CI] 1.07–1.85) for prenatal blood lead, 1.07 (95% CI 0.88–1.29) for average childhood blood lead, and 1.27 (95% CI 1.03–1.57) for 6-year blood lead. Adjusted arrest rates for violent crimes were also greater for each 5 lg/dl increase in blood lead: RR ¼ 1.34 (95% CI 0.88–2.03) for prenatal blood lead, 1.30 (95% CI 1.03–1.64) for average childhood blood lead, and 1.48 (95% CI 1.15–1.89) for 6-year blood lead. Conclusions Prenatal and postnatal blood lead concentrations are associated with higher rates of total arrests and/or arrests for offenses involving violence. This is the first prospective study to demonstrate an association between developmental exposure to lead and adult criminal behavior. The Editors’ Summary of this article follows the references. PLoS Medicine | www.plosmedicine.org May 2008 | Volume 5 | Issue 5 | e101 0732 PLoSMEDICINE Introduction Early onset of aggressive or violent behavior is a precursor to a life course marred by limited social and educational achievement, incarceration, underemployment, and prema- ture mortality [1,2]. These maladaptive behavioral patterns, which often emerge early in life, remain highly stable . These facts highlight the importance of identifying risk factors that may place youth on an early developmental trajectory toward a career of crime and violence. A meta-analysis of 34 independent studies identiﬁed and prioritized risk factors for serious, violent criminal behavior . The most consistent risk factors were male gender, prenatal exposure to tobacco smoke, having antisocial parents, and low family socioeconomic status. In contrast, few studies have evaluated the consequences of childhood lead exposure as a risk factor for criminal behavior. Some epidemiological studies have found a relationship between childhood lead exposure and antisocial behavior. In a study of Philadelphia youth, a history of lead poisoning was among the most signiﬁcant predictors of adolescent delin- quency and adult criminality in males . Bone lead levels were associated with delinquent behavior in a retrospective cohort study of 11-year-old Pittsburgh children . In Cincinnati, prenatal and childhood blood lead concentra- tions were associated with an increased risk for antisocial behavior and delinquency in adolescence . Finally, elevated bone lead levels were observed in juvenile court–adjudicated delinquents residing in Allegheny County, Pennsylvania compared to matched controls . These studies suggest that exposure to environmental lead during childhood is associ- ated with the development of conduct problems and delinquent behavior. In consideration of these ﬁndings, it is noteworthy that a number of recent ecological investigations correlating leaded gasoline sales or atmospheric lead levels with crime rates also support an association between lead exposure and criminal behavior [9–12]. Questions remain, however, because these studies were cross-sectional (hence causality cannot be ﬁrmly established), relied on indirect measures of lead exposure, or did not follow participants into adulthood. Here, we report the results of a long-term prospective study on the effects of one potential childhood risk factor of adult arrests, elevated prenatal and childhood blood lead concentrations. Methods Participants The Cincinnati Lead Study (CLS) is a birth cohort recruited from late 1979 to early 1984. The CLS enrolled women in their ﬁrst or early second trimester of pregnancy who attended four prenatal clinics within impoverished Cincin- nati neighborhoods with a high concentration of older, lead- contaminated housing . Women were excluded or ineligible if they were known to be addicted to drugs, were known to have diabetes or a neurological or psychiatric condition, or refused prenatal participation. Newborns were excluded if their gestational age was less than 35 wk, birth weight less than 1,500 g, Apgar score at 5 min less than 6, or if genetic or other serious medical issues were present at birth. This process netted 376 newborns who were recruited at birth (i.e., informed oral and written consent was obtained from the mother in the hospital and a blood lead sample was obtained from the newborn). Of these newborns 305 were developmentally examined at the CLS follow-up clinic when they were 3 and 6 mo of age . They were followed up quarterly through age 5 y and semiannually from age 5 to 6.5 y . A total of 250 CLS participants who were between 19 and 24 y of age and had been followed at least through the ﬁrst 6 y of life participated in the current study. Thus, individuals in the current analysis had serial blood lead concentrations spanning the entire preschool and early school-age period of development. Written informed consent was obtained by the investigator or a senior member of the research staff at each stage of this longitudinal study after it was determined that the participant or the participant’s legal guardian understood the nature of the research. This protocol has been reviewed and approved by the institutional review boards of the University of Cincinnati College of Medicine and the Cincinnati Children’s Hospital Medical Center. The 250 participants in this analysis were not substantially different from those with missing data with regard to baseline perinatal characteristics such as birth weight (3,134 versus 3,138 g), sex (50% versus 54% male), 6-y average Hollingshead  socioeconomic status (SES) total score (18.0 versus 18.3), years of maternal education (11.2 versus 11.1 y), scores on the Home Observation for Measurement of the Environment (the preschool version of a quantitative observational measure of early nurturing and environmental stimulation ) (32.3 versus 33.4), and average childhood blood lead (13.4 versus 14.2 lg/dl). Exposure and Outcome Assessments We examined three measures of blood lead. Prenatal maternal blood lead concentration [lg/dl]) was measured during the ﬁrst or early second trimester of pregnancy. Approximately 50% of the prenatal samples were obtained during the ﬁrst trimester of pregnancy. The difference between maternal blood lead concentration assessed in the ﬁrst and second trimesters was not statistically signiﬁcant (p¼ 0.76) . Postnatal blood lead indices included average childhood blood lead (average of 23 blood lead concen- trations obtained quarterly from age 3 to 60 mo and semiannually from 66 to 78 mo), and 6.5-y blood lead. If a 6.5-y blood lead value was not available for a child, we used the blood lead test from 6 y. We selected 6.5 y blood lead over other serial blood lead measures because preliminary analyses indicated that blood lead measured at 6 y was more highly associated with the number of arrests than blood lead measured at other ages. Complete blood lead data were available for 89%–92% of the cohort at any particular quarterly assessment from 3 mo to 5 y of age. Missing postnatal blood lead concentrations were imputed from a weighted average of a within-participant regression of blood lead on age. This imputation was done to avoid excluding those participants who may have one or only a few missing blood lead tests. Prenatal blood lead concentrations were available for 87% (217/250) of the participants. The primary outcome variable in this study was the individual’s number of criminal arrests since turning 18 y of age. We did not collect data on convictions. Arrest is a more proximate measure of criminal behavior than are PLoS Medicine | www.plosmedicine.org May 2008 | Volume 5 | Issue 5 | e101 0733 Blood Lead and Criminal Arrests conviction data. Arrest typically occurs at the scene of the criminal event or immediately thereafter. Arrest decisions, moreover, usually reﬂect the seriousness of the offense, the offender’s prior record, and the desire of the victim to have the individual arrested. Conversely, conviction data are distal indicators of criminal behavior. Actual criminal convictions derived from a trial represent less than 10% of all criminal arrests. Over 90% of all criminal cases are subject to plea bargaining, in which a plea of ‘‘guilty’’ is usually rewarded with a reduced charge and/or sentence. From the time of arrest it can take upward of 2 y or more before a defendant is tried in a court, or it can take over 1 y from the time of arrest to the time at which a plea deal is accepted by the court. Furthermore, a range of extra-legal variables can enter into the plea and trial process, including the defendant’s economic status, support system, and access to quality defense counsel. We should also add that Hamilton County, Ohio (the study’s catchment area) makes extensive use of ‘‘diversion’’ programs. These programs select individuals with speciﬁed problems or offenses, such as drunken driving or drug abuse and ‘‘divert’’ them from jail or prison into community-based rehabilitation programs. Upon successful completion of the program and a probationary term, many of these programs ‘‘erase’’ the individual’s legal conviction, but not the arrest. Finally, at least for this study, arrest data are substantially more complete than are conviction data. Arrest data in Hamilton County, Ohio are compiled into a single county-wide database and are updated at regular intervals. Court data, however, are not updated regularly. This problem is endemic to court systems nationwide, because courts operate at different levels (city, county, state, Federal) and are under the guidance of individual judges. Data on Criminal Arrests Data on criminal arrests for participants and their mothers were obtained from a computer search of Hamilton County, Ohio criminal justice records. These records provided information on the nature, number, and disposition of arrests. Two reviewers who were blind to participants’ blood lead concentrations independently coded each arrest into one of the following categories: violent offenses (e.g., murder, rape, domestic violence, assault, robbery, or possession of a weapon); offenses against property (e.g., burglary or arson); drug offenses (e.g., trafﬁcking, abuse, or possession); fraud; obstruction of justice; serious motor vehicle offenses (e.g., driving without a license, driving under the inﬂuence of alcohol, or driving under suspension); disorderly conduct; and other offenses, which included offenses that did not ﬁt in any previously mentioned category. Minor motor vehicle offenses, such as speeding, safety restraint violations, lights burned out, failing to stop, and pedestrian offenses were excluded from the analyses. We counted the number of arrests and coded the nature of the offense that led to each arrest. If an individual was charged with more than one offense during a single arrest, then the most serious offense was used for classiﬁcation. Thus, arrest counts were lower than the total number of offenses. Legally determined guilt was not a factor in our coding. Only those offenses that were ﬁled before 31 October 2005 were included in the analyses. Inter-reviewer differences with respect to arrest and category of offense were resolved by a third reviewer who conducted the initial training for criminal record coding. Interobserver agreement as assessed by Cohen’s kappa was 0.93 for maternal offenses and 0.97 for participant offenses. Statistical Analyses We used negative binomial regression models to analyze these data because the counts of arrests were overdispersed when originally examined using Poisson regression models . This model provided a very good ﬁt to these data in terms of the estimated scale parameter. These models were used to estimate the association between blood lead concen- trations and arrest rates adjusted for other important risk factors. We calculated separate models for each blood lead measure. Our dependent variable was the number of criminal arrests for each participant measured as discrete counts, which were positively skewed. To account for the number of years at risk of arrest, we used the log of current age as an offset in all models. To control for potential confounding, we examined variables reﬂecting the effects of other neuro- toxicants such as maternal cigarette and marijuana smoking and consumption of narcotics during pregnancy, as well as variables related to adult criminal involvement in prior studies. Our list of candidate covariates included: sex; a validated measure of the quality of early care-giving and environmental stimulation called the Home Observation for Measurement of the Environment (HOME) inventory score ; birth weight (g); maternal smoking during pregnancy (half-packs consumed per day); maternal alcohol, marijuana, or narcotic use (Y/N); maternal education level (highest grade); maternal IQ ; total prior maternal arrests; SES (average Hollingshead  score); number of children in the home; and whether the mother was on public assistance during the participant’s childhood (Y/N). Data on fathers or male caregivers in the home were not available, since 84% of the households were headed by the mother or a male caregiver was not consistently present. Continuous covariates were examined using linear, polynomial, and log-transformed functions to assess whether simple linear terms were adequate for adjustment of covariate or confounder inﬂuen- ces. Candidate covariates or confounders remained in the ﬁnal multivariable models if they were either statistically signiﬁ- cant (p 0.05) or if their inclusion in the model caused a change of 10% in the rate ratio estimates for lead, regardless of their level of statistical signiﬁcance. We tested the interaction of lead by sex, since some studies have indicated that developing male central nervous systems may be more vulnerable than females’ to environmental insults leading to later behavioral problems . Before deciding upon a ﬁnal multivariable model, regression diagnostics for collinearity and inﬂuence using the methods described in Belsley, et al. were employed . As a measure of the absolute change in arrest rates between participants with higher levels of blood lead compared to those with lower blood lead levels, we deﬁned attributable risk as the average difference in annual arrest rates between participants at the 95th percentile of blood lead and those at the 5th percentile. All signiﬁcance tests were two-tailed. Results for blood lead variables are presented as adjusted rate ratios (RR) for total arrests and arrests for violent crimes. All statistical analyses were conducted with SAS (Statistical Analysis System), version 9.1 . PLoS Medicine | www.plosmedicine.org May 2008 | Volume 5 | Issue 5 | e101 0734 Blood Lead and Criminal Arrests Results The sample was largely African-American (90%), 50% of the participants were male, and 73% of families scored in the lowest two levels of the Hollingshead Four-Factor Index of Social Position . A single female caregiver headed 84% of households. Mean blood lead concentrations (lg/dl) were 8.3 (0.40 lmol/ l) (range 1–26) for maternal prenatal, 13.4 (0.65 lmol/l) (range 4–37) for average childhood, and 8.3 (0.40 lmol/l) (range 2– 33) for 6-y. The mean postnatal blood lead concentration of CLS participants increased to a peak of 17.7 (standard deviation [SD] 9.7) lg/dl (0.85 lmol/l) at 21 mo. After age 21 mo, average blood lead concentrations declined to a mean of 8.4 (SD 4.9) lg/dl (0.40 lmol/l) at 6.5 y. At 6.5 y of age, 67 children (26.9%) had a blood lead concentration above 10 lg/ dl (0.48 lmol/l) (Table 1). Pearson correlations between blood lead indices examined in this study were 0.32 and 0.28 between prenatal and average childhood and 6-y respectively, and 0.80 between average childhood and 6 y. We identiﬁed a total of 800 arrests within the sample. Of these arrests, 108 (14%) were for violent offenses, 90 (11%) involved theft or fraud, 216 (28%) involved drugs, 35 (5%) were for obstruction of justice, 211 (27%) were related to serious motor vehicle offenses, 35 (5%) were for disorderly conduct, and 82 (11%) other. Approximately 55% of participants (62.8% of males, 36.3% of females) had at least one arrest. The mean number of arrests among males was 5.2, which was signiﬁcantly higher than the mean number of 1.1 for females (p , 0.001). The overall mean arrest rate was 0.68 per year after age 18, but the mean arrest rate for males was 4.5 times higher than the female arrest rate (1.1 versus 0.25 per year). Preliminary analysis of the association between blood lead measures and covariates revealed generally weak correlation coefﬁcients ranging from 0.24 to 0.35, indicating a relatively Table 1. Characteristics of the Participants and of their Mothers in the Cincinnati Lead Study (n ¼250) Category Characteristic Total (n ¼250) No. (%) or Mean (SD) Participant Never Arrested (n ¼114) No. (%) or Mean (SD) Participant Ever Arrested (n ¼136) No. (%) or Mean (SD) Participant characteristics Male 125 (50.0%) 34 (29.8%) 91 (66.9%) African-American 225 (90.0%) 99 (86.8%) 126 (92.7%) Age at study date, y 22.5 (1.5) 21.9 (4.8) 22.5 (4.5) Marijuana use 29 (11.6%) 13 (11.4%) 16 (11.8%) Blood lead, lg/dla Prenatal blood leadb 8.3 (3.8) 7.9 (3.2) 8.7 (4.1) Average childhood blood lead 13.4 (6.1) 13.3 (6.7) 13.5 (5.5) 6-year blood lead 8.3 (4.8) 7.6 (4.3) 8.8 (5.0) Maternal characteristics Age at delivery, y 22.5 (4.2) 22.0 (4.0) 22.9 (4.4) Maternal IQ (points) 75.3 (9.3) 76.9 (10.4) 73.9 (8.1) High school graduate 132 (52.8%) 68 (59.6%) 64 (47.1%) HOME inventory at age 3 y (points) 32.3 (6.6) 33.6 (6.3) 31.6 (6.7) Socioeconomic status (Hollingshead score) 18.0 (4.8) 18.5 (5.1) 17.8 (4.5) Marital status Married 39 (15.6%) 21 (18.4%) 18 (13.2%) Single 155 (62.0%) 70 (61.4%) 85 (62.5%) Other 56 (22.4%) 23 (20.2%) 33 (24.3%) Smoked during pregnancy 129 (51.6%) 62 (54.4%) 67 (49.3%) Number of children in home 3.0 (1.4) 2.9 (1.4) 3.1 (1.3) Public assistance 190 (76%) 82 (71.9%) 108 (79.4%) Data presented as n (%) or mean (SD). Average childhood blood lead concentration was defined as the mean of blood lead tests taken from 3 months through the 6-year blood lead test. aTo convert blood lead to lmol/l multiply by 0.04826. bn ¼ 217 for prenatal blood lead. doi:10.1371/journal.pmed.0050101.t001 Table 2. Relationship of Prenatal, Early Childhood Average, and Six-Year Blood Lead Concentrations with Total Arrest Rates in Young Adults Blood Lead Variable Median (5th–95th Percentile), lg/dl a Attributable Risk (95% CI), per Year Rate Ratio for 5 lg/dl Increase in Blood Lead (95% CI) Prenatal 7.8 (2.9–16.0) 0.48 (0.29–0.79) 1.40 (1.07–1.85) Early Childhood Average 12.3 (6.0–26.3) 0.13 (0.03–0.33) 1.07 (0.88–1.29) Six-Year 6.8 (3.4–18.3) 0.39 (0.21–0.68) 1.27 (1.03–1.57) Estimates adjusted for maternal IQ, sex, SES using the Hollingshead Score, and maternal education level. aTo convert blood lead to lmol/l multiply by 0.04826. doi:10.1371/journal.pmed.0050101.t002 PLoS Medicine | www.plosmedicine.org May 2008 | Volume 5 | Issue 5 | e101 0735 Blood Lead and Criminal Arrests small potential for confounding. In multivariable regression analyses of the total number of arrests, we found that the associations between prenatal and 6-y blood lead concen- trations were statistically signiﬁcant. In each model, the blood lead association was adjusted for the cofactors of maternal IQ, sex, SES score, and maternal education. The RRs for total arrests increased for each 5 lg/dl (0.24 lmol/l) increment in blood lead concentration; the RRs were 1.40 (95% conﬁdence interval [CI] 1.07–1.85) for prenatal blood lead, 1.07 (95% CI 0.88–1.29) for average childhood blood lead, and 1.27 (95% CI 1.03–1.57) for 6-y blood lead. The attributable risk was 0.48 arrests/year (95% CI 0.29–0.79) for prenatal blood lead, 0.13 (95% CI 0.03–0.33) for average childhood blood lead, and 0.39 (95% CI 0.21–0.68) for 6-y blood lead (Table 2). The rate of total arrests was modeled as a log-linear function of increasing blood lead concentrations for each of the three blood lead assessments: maternal prenatal (Figure 1A), early childhood (Figure 1B), and 6 y (Figure 1C). In multivariable analyses of violent criminal arrests, we found statistically signiﬁcant associations with both average childhood and 6-y blood lead variables. The RRs for arrests involving violent crimes increased for each 5 lg/dl (0.24 lmol/ l) increment in blood lead; the RRs were1.34 (95% CI 0.88– 2.03) for prenatal blood lead, 1.30 (95% CI 1.03–1.64) for average childhood blood lead, and 1.48 (95% CI 1.15–1.89) for 6-y blood lead. The attributable risk was 0.055 arrests/year (95% CI 0.026–0.118) for prenatal blood lead, 0.077 (95% CI 0.039–0.156) for average childhood blood lead, and 0.087 (95% CI 0.049–0.152) for 6-y blood lead (Table 3). As with the analyses for total arrests, the rate of arrests for violent offenses was modeled as a log-linear function of each of the blood lead indices: maternal prenatal (Figure 2A), early childhood (Figure 2B), and 6 y (Figure 2C). The results for analyses restricted to arrests for nonviolent crimes were similar to those found for all arrests. Speciﬁcally, the RRs for nonviolent arrests for each 5 lg/dl (0.24 lmol/l) in blood lead were 1.40 (95% CI 1.06–1.84) for prenatal blood lead, 1.05 (95% CI 0.86–1.28) for average childhood blood lead, and 1.22 (95% CI 0.97–1.53) for 6-y blood lead. There was no statistical evidence that the shape of the exposure-response relationship differed by sex with any of the blood lead indices for total arrests or arrests for violent offenses. The interaction term for sex was statistically nonsigniﬁcant (p-values for interaction term ranged from 0.42 to 0.79). However, the attributable risk for males was considerably higher than for females. For example, the attributable risk for 6-y blood lead rate was 0.85 arrests/year (95% CI 0.48–1.47) for males and 0.18 (95% CI 0.09–0.33) for females. Discussion In a prospective birth cohort, we found that prenatal and childhood blood lead concentrations were predictors of adult arrests. Prenatal and 6-y blood lead concentrations were signiﬁcantly associated with higher RRs for total arrests. Figure 1. Adjusted Relationship between Blood Lead Concentration and Arrest Rate Ratio For Total Arrests Shown are data for maternal prenatal blood lead concentration (A), early childhood average blood lead concentration (B), and 6-year blood lead concentration (C). Rate ratios are plotted as a function of increasing blood lead from the 5th to the 95th percentiles of blood lead relative to participants at the 5th percentile. Dashed lines are 95% confidence intervals. To convert to lmol/l: (lg/dl) 3 0.04826. doi:10.1371/journal.pmed.0050101.g001 PLoS Medicine | www.plosmedicine.org May 2008 | Volume 5 | Issue 5 | e101 0736 Blood Lead and Criminal Arrests Average childhood as well as later (6-y) blood lead concen- trations were signiﬁcantly associated with higher RRs for arrests involving a violent offense. Data from several recent prospective studies suggest that blood lead concentrations in the later preschool years may be more predictive of cognitive and behavioral problems . However, the potential importance of prenatal blood lead concentrations should not be underestimated, as they were predictive of total arrests in our data. The number of arrests in the CLS cohort was signiﬁcantly higher in males. However, no signiﬁcant inter- actions between sex and blood lead with arrest rates were found. Environmental lead levels as well as crime have dropped over the last 30 y in the US . However, the overall reduction was not uniform; inner-city children, who are predominately African-American, remain particularly vulnerable . Crime and violent crime are concentrated in urban centers in the US where many poor African-Americans reside. One factor in the disproportional representation of African-Americans in crime statistics could well be the historically higher exposures to lead in these communities. Furthermore, recent data from epidemiological studies implicate blood lead concentrations well below the current level of concern adopted by the United States Centers for Disease Control in the development of neurobehavioral deﬁcits . We were unable to explore racial differences in our data since almost all participants were African-American. However, Needleman found that the lead-associated risk for juvenile court-adjudicated delin- quency was present in both African-American and white youth, indicating that these ﬁndings are not restricted to any one racial or ethnic group . The neurodevelopmental consequences associated with lead exposure in previous studies, such as lower IQ, less tolerance for frustration, deﬁcits in attention, hyperactivity, and weak executive control functions, are potent predictors of delinquent and criminal behaviors [26–29]. Attention deﬁcit hyperactivity disorder (ADHD) is a common ﬁnding among juvenile delinquents, and those with ADHD are more likely to have severe cognitive impairments . ADHD is also a known risk factor for criminal behavior in adulthood . A recent analysis of data from the third National Health and Nutrition Examination Survey (NHANES-III) found that higher blood lead concentrations were signiﬁcantly associ- ated with ADHD. Children with blood lead concentrations greater than 2 lg/dl were at a 4.1-fold increased risk of ADHD . Similarly, in experiments with rodents, felines, and nonhuman primates, early lead exposure was associated with increased impulsivity, aggression, antagonistic interactions, reduced social play and abnormal mother–infant interaction [33–36]. Childhood lead exposure therefore seems to place individuals at risk for multiple underlying neurobehavioral deﬁcits associated with a higher probability of later criminal behavior. A number of mechanisms may be at work. Lead interferes with synapse formation, disrupts dopamine systems, and lowers serotonin levels. Lead exposure has been shown to reduce MAO A (monoamine oxidase A) activity, and low MAO A activity has been associated with violent and criminal behaviors . One consequence of these alterations could be neural dysfunction in areas of the brain involved in arousal, emotion, judgment, and behavioral inhibition such as the prefrontal cortex . This study has several limitations. First, most criminal behavior never comes to the attention of authorities; thus, our measure of arrest underestimates actual criminal activity. Had we been able to account for all criminal acts, it is possible that the results of our study may have been different. For example, it could be argued that lead-associated lower intelligence makes it more likely that an offender will be caught (i.e., arrested). However, a recent large-scale prospec- tive study of school-aged children with early blood lead levels similar to those in the CLS suggests that lead impacts social behaviors somewhat independently of IQ . Furthermore, we did not adjust arrest rates for child IQ in our analyses because controlling for a variable that might potentially be on the causal pathway is clearly inappropriate in studies of this kind. Variables along the causal pathway between exposure and outcome cannot be bona ﬁde confounders . Second, we examined only Hamilton County, Ohio records. Although most participants in our cohort continued to reside in Hamilton County, we may have missed some arrests that occurred in other counties. Third, ofﬁcial records of arrest were available only when the participants reached 18 y of age. Thus, the average follow-up was under 5 y. The possibility of bias introduced by nonrandom attrition in the CLS cohort cannot be ruled out, although we found no important differences on key exposure and demographic variables. Fourth, it is always possible in observational studies to have uncontrolled confounding. This can be problematic when it comes to measuring SES, since global assessments of social standing such as the one used in this  and many other studies fail to capture all potentially relevant factors . As pointed out by Weiss and Bellinger  in their discussion of the social ecology of exposure to environmental Table 3. Relationship of Prenatal, Early Childhood Average, and Six-Year Blood Lead Concentrations with Violent Crime Arrest Rates in Young Adults Blood Lead Variable Median (5th–95th Percentile), lg/dla Attributable Risk (95% CI), per Year Rate Ratio for 5 lg/dl Increase in Blood Lead (95% CI) Prenatal 7.8 (2.9–16.0) 0.055 (0.026–0.118) 1.34 (0.88–2.03) Early Childhood Average 12.3 (6.0–26.3) 0.077 (0.039–0.156) 1.30 (1.03–1.64) Six-Year 6.8 (3.4–18.3) 0.087 (0.049–0.152) 1.48 (1.15–1.89) Estimates adjusted for maternal IQ, sex, SES using the Hollingshead Score, and maternal education level. aTo convert blood lead to lmol/l multiply by 0.04826. doi:10.1371/journal.pmed.0050101.t003 PLoS Medicine | www.plosmedicine.org May 2008 | Volume 5 | Issue 5 | e101 0737 Blood Lead and Criminal Arrests pollutants, neurotoxicant exposures are not randomly dis- tributed, but are ‘‘chained’’ to many other risks to normal development that are sometimes quite difﬁcult to partition. Finally, as with all studies of this kind, our measure of dose to the critical organ (brain) was indirect. Blood, as well as other tissues in which lead is often measured such as teeth or bone, are surrogates for dose to the central nervous system. On the other hand, this study has a number of qualities that contribute to the validity of our ﬁndings. To our knowledge this is the ﬁrst prospective study to directly examine the relationship between early exposure to lead and ofﬁcial documentation of arrests in adulthood. Lead dose as assessed by frequent serial blood lead determinations, assessment of a large number of potentially important covariate factors, and careful documentation of criminal arrests were unique aspects of this investigation. Furthermore, the sample was relatively homogenous with respect to sociodemographic variables such as SES and ethnicity; thus decreasing the extent to which strong confounding factors might generate spurious associations. Therefore, we conclude that these data implicate early exposure to lead as a risk factor for behaviors leading to criminal arrest. Acknowledgments We are grateful to members of the Cincinnati Lead Study cohort and their families for their participation. Author contributions. JPW, KND, MDR, and BPL designed the experiments/the study. SDW and KND collected data or did experi- ments for the study. RWH, MH and JPW analyzed the data. KND and SDW enrolled patients. JPW and KND wrote the first draft of the paper. JPW, KND, MDR, RWH, SDW, BPL, and MNR contributed to writing the paper. References 1. Farrington DP (1986) Stepping stones to adult criminal careers. In: Olweus D, Block J, Radke-Yarrow M, editors. Development of Antisocial and Prosocial Behavior. New York: Academic Press. pp. 359–384. 2. Farrington DP (1991) Childhood aggression and adult violence: Early precursors and later-life outcomes.Pepler DJ, Rubin KH, editors. The Development and Treatment of Childhood Aggression. 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Weiss B, Bellinger DC (2006) Social ecology of children’s vulnerability to environmental pollutants. Environ Health Perspect 114: 1479–1485. PLoS Medicine | www.plosmedicine.org May 2008 | Volume 5 | Issue 5 | e101 0739 Blood Lead and Criminal Arrests Editors’ Summary Background. Violent crime is an increasing problem in many countries, but why are some people more aggressive than others? Being male has been identified as a risk factor for violent criminal behavior in several studies, as have exposure to tobacco smoke before birth, having antisocial parents, and belonging to a poor family. Another potential risk factor for antisocial behavior as an adult is exposure to lead during childhood, although few studies have looked directly at whether childhood lead exposure is linked with criminal behavior in adulthood. Lead is a toxic metal that damages the nervous system when ingested or inhaled. It is present throughout the environment because of its widespread use in the past in paint, solder for water pipes, and gasoline. In 1978, 13.5 million US children had a blood lead level above 10 lg/dl, the current US Centers for Disease Control and Prevention blood lead level of concern (the average US blood lead level is 2 lg/dl). Lead paint and solder were banned in 1978 and 1986, respectively, by the US federal government; leaded gasoline was finally phased out in 1996. By 2002, only 310,000 US children had a blood lead level above 10 lg/dl. However, children exposed to lower levels of lead than this—through ingesting flakes or dust residues of old lead paint, for example—can have poor intellectual development and behavioral problems including aggression. Why Was This Study Done? Although some studies have suggested that childhood lead exposure is associated with later criminal behavior, these studies have often relied on indirect measurements of childhood lead exposure such as bone lead levels in young adults or a history of lead poisoning. Other studies that have measured childhood lead exposure directly have not followed their participants into adulthood. In this new study, the researchers investigate the association between actual measurements of prenatal and childhood blood lead concen- trations and criminal arrests in early adulthood to get a clearer idea about whether early lead exposure is associated with subsequent violent behavior. What Did the Researchers Do and Find? Between 1979 and 1984, the researchers recruited pregnant women living in poor areas of Cincinnati, which had a high concentration of older, lead-contaminated housing, into the Cincinnati Lead Study. They measured the women’s blood lead concentrations during pregnancy as an indication of their offspring’s prenatal lead exposure and the children’s blood lead levels regularly until they were six and half years old. They then obtained information from the local criminal justice records on how many times each of the 250 offspring had been arrested between becoming 18 years old and the end of October 2005. The researchers found that increased blood lead levels before birth and during early childhood were associated with higher rates of arrest for any reason and for violent crimes. For example, for every 5 lg/dl increase in blood lead levels at six years of age, the risk of being arrested for a violent crime as a young adult increased by almost 50% (the ‘‘relative risk’’ was 1.48). What Do These Findings Mean? These findings provide strong evidence that early lead exposure is a risk factor for criminal behavior, including violent crime, in adulthood. One possibility, which the authors were unable to assess in this study, is that lead exposure impairs intelligence, which in turn makes it more likely that a criminal offender will be caught (i.e., arrested). The authors discuss a number of limitations in their study—for example, they probably did not capture all criminal behavior (since most criminal behavior does not lead to arrest). Although both environmental lead levels and crime rates have dropped over the last 30 years in the US, the overall reduction was not uniform—inner-city children remain particularly vulnerable to lead exposure. The findings therefore suggest that a further reduction in childhood lead exposure might be an important and achievable way to reduce violent crime. Additional Information. Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed. 0050101. A PLoSMedicine Perspective article by David Bellinger further discusses this study and a related paper on childhood lead exposure and brain volume reduction in adulthood Study researcher Kim Dietrich can be heard talking about ‘‘The Lethal Legacy of Lead’’, a brief MP3 about lead exposure and violent crime Toxtown, an interactive site from the US National Library of Medicine, provides information on environmental health concerns including exposure to lead (in English and Spanish) The US Environmental Protection Agency provides information on lead in paint, dust, and soil and on protecting children from lead poisoning (in English and Spanish) MedlinePlus provides a list of links to information on lead poisoning (in English and Spanish) The US Centers for Disease Control and Prevention provides information about its Childhood Lead Poisoning Prevention Program The UK Health Protection Agency also provides information about lead and its health hazards PLoS Medicine | www.plosmedicine.org May 2008 | Volume 5 | Issue 5 | e101 0740 Blood Lead and Criminal Arrests ever, children exposed to lower levels of lead than this—through ingesting flakes or dust residues of old lead paint, for example—can have poor intellectual development and behavioral problems including aggression. Why Was This Study Done? Although some studies have suggested that childhood lead exposure is associated with later criminal behavior, these studies have often relied on indirect measurements of childhood lead exposure such as bone lead levels in young adults or a history of lead poisoning. Other studies that have measured childhood lead exposure directly have not followed their participants into adulthood. In this new study, the researchers investigate the association between actual measurements of prenatal and childhood blood lead concen- trations and criminal arrests in early adulthood to get a clearer idea about whether early lead exposure is associated with subsequent violent behavior. What Did the Researchers Do and Find? Between 1979 and 1984, the researchers recruited pregnant women living in poor areas of Cincinnati, which had a high concentration of older, lead-contaminated housing, into the Cincinnati Lead Study. They measured the