�9 1986 by The I lumana Press Inc. All rights of anv nature whatsoever reserved. 0163-4984186/I l(X~4X)05502.00

Hair-Aluminum Concentrations and Children's Classroom Behavior

CHARLES M O O N 1 AND MIKE MARLOWE z*

'Department of Educational Foundations, and Instructional Technology, University of Wyoming, Laramie, WY 82071; and

2Department of Language, Reading, and Exceptionalities, Appalachian State University, Boone, NC 28608

Received June 9, 1986; Accepted June 11, 1986

ABSTRACT

The study investigated the relationship between children's hair- A1 concentrations and children's behavioral performance in school. Hair-A1 levels of 102 children drawn from a general school population were correlated with teachers' ratings of the children on the Walker Problem Behavior Identification Checklist (WPBIC). Increasing hair-Al values correlated significantly with increased scores on the WPBIC total scale score. A continuing reexamination of A1 exposure in the young is needed in order to determine the margin of safety re- garding potentially toxic levels of A1.

Index Entries: Low-level aluminum; aluminum toxicity, in chil- dren; hair aluminum concentrations; teachers' behavior rating scale; nonadaptive classroom behavior; Walker Problem Behavior Identifi- cation Checklist.

INTRODUCTION

The behavioral effects of a luminum (AI) have not been extensively studied. Although subtle behavioral changes are noted in certain species soon after A1 infusion, with increasing time, the behavioral changes be- come more severe as overt neuropathological signs appear. Most authors describe a progression of symptoms: The first to appear is reduced motor

*Author to whom all correspondence and reprint requests should be addressed.

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6 34oon and Marlowe

activity and an increased irritability to external stimuli. Progressive weak- ness and incoordination ensue, and this is followed in the terminal stages by seizures and convulsions (1-4).

In humans there appears to be considerable evidence to suggest that elevated AI may be the precipitating neuropathological event in dialysis dementia (5,6), whereas A1 may be a secondary event in Alzheimer 's dis- ease (7). Dialysis dementia, a neurological syndrome observed in some patients undergoing renal dialysis, is characterized by paranoia, person- ality changes, sometimes severe psychoses, confusion, impaired mathe- matical abilities, and delirium. With progression of the disease, a loss of muscle coordination, marked motor abnormalities, and the onset of sei- zures occur, the clinical course terminating in convulsions and death.

Al though A1 is not generally considered to represent an environ- mental hazard, levels of AI routinely encountered in the envi ronment have recently been associated with fine motor deficits (8,9), learning disabilities, (10,11), and behavioral disorders in children (12-17). The purpose of this s tudy was to examine children's classroom behavior in relation to AI values. It was hypothesized that as children's AI concentra- tions increased, their ratings on nonadaptive classroom behaviors would increase.

In this study, AI concentrations were determined via hair samples and atomic absorption spectroscopy. Although blood values are the most widely used indicator of A1 status, blood AI levels, similar to blood levels of other metals, can only serve as an indicator of circulating A1 levels and not total body store (18,19). As a result, there is increased interest in the use of hair as a diagnostic tool for the assessment of trace-metal status. Trace elements are accumulated in hair at concentrations that are gener- ally at least 10 • higher than those present in blood, and hair samples provide a continuous record of exposure to metal pollutants (20-22). Yokel (23) has found that hair AI is a reasonable biopsy technique for es- tablishing excessive systemic A1 exposure. Bryukhanov (24) reported that the content of AI in the hair varied with the intensity of occupational con- tact with AI, and Parkhurt and Pate (25) noted elevated hair-A1 concen- trations in patients on dialysis with encephalopathy syndrome.

METHOD

Subjects The 102 subjects in this study were randomly drawn from two ele-

mentary schools in southeastern Wyoming. Fifty-one were Native Amer- ican Indians and 51 were Caucasian, their mean age was 8.69, with a s tandard deviation (SD) of 1.97. Fifty were male, and the mean social class was 3.22, with an SD of 1.56, as defined by the Hollingshead two- factor index.

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Aluminum and Behavior 7

Classification oral Levels

After obtaining parental permission, children were asked to submit a small sample of hair (about 400 mg) for trace-mineral analysis. Hair samples were collected from the nape of the child's neck, as close to the scalp as possible, by the senior researcher, using stainless-steel scissors. The hair samples were then submitted to Doctor's Data, Inc., a state and Center for Disease Control licensed laboratory in West Chicago, where they were analyzed with the atomic absorption spectroprotometer, the graphite furnace, and the inductively coupled argon plasma quantome- ter (1CP) to determine the children's A1 levels.

Precise quantometer standards are used by Doctor's Data, Inc. to as- sure reliability of results and to meet reproducibility requirements. These include:

(1) Upon receipt, the hair sample is washed thoroughly with deionized water, a nonionic detergent, and an organic sol- vent to remove topical contaminants.

(2) A control sample is run from the initial steps through the entire procedure to assure reproducibility of methods.

(3) At least one of every ten tests is a standard. Working standards are made to assure proper values.

(4) The in-house spiked pool is completely remade and ana- lyzed daily as every 50th specimen as part of the quality con- trol procedure.

(5) Temperature and humidity are controlled to assure reliabil- ity and consistency of the testing instrument.

Walker Problem Behavior Identification Checklist

The Walker Problem Behavior Identification Checklist (WPB1C) (26) is a screening device designed for elementary teachers in selecting chil- dren with behavior problems who may need referral for further psycho- logical evaluatkm and treatment. The WPBIC consists of 50 observable operational statements of classroom behavior that might limit a child's adjustment in school. Differential score weights are assigned to each statement based on their influence in handicapping a child's adjustment. Factor analyzing the 50 items, there are 14 items relating to acting-out (aggressive and disruptive behaviors), 5 items relating to withdrawal (so- cially avoidant and passive behaviors), 11 items relating to distractibililty (poor attentiveness and restlessness, 10 items relating to disturbed peer relations, and 10 items relating to immaturity.

Standardized on 534 elementary-aged children, the mean raw total score was 7.76, with an SD of 10.53. A total scale score of 21 or greater separates disturbed from nondisturbed behavior, and Walker (26) re- ported the split half reliability of the scale of 0.98 and the difference be-

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8 Noon and Marlowe

tween the means of disturbed and nondisturbed children on the scale significant beyond the 0.001 level.

In the present study, classroom teachers were instructed on how to fill out the scale by the senior researcher. All teacher ratings were based on observations of the child's classroom behavior for the past 2 mo prior to hair collection.

RESULTS

The subjects' mean hair-Al value was 8.56 parts per million (ppm) with an SD of 4.25 ppm. According to Doctor's Data, Inc. (27), the ac- cepted upper limit for hair-Al is 30 ppm. Thus, the subjects" hair-A1 values were well within the range of accepted laboratory norms.

The means of SD for the subjects' scores on the WPBIC total scale score were 12.29 and 14.50, respectively. The groups' WPBIC total scale score of 12.29 was within the range of normal behavior (<21), but above the mean raw total score obtained on the non-Indian standardized popu- lation.

Table 1 summarizes the descriptive statistics for the WPBIC total scale, A1, and the significant confounding variables, sex and race. Race was coded "0" for Indians and " l " for Caucasions. Sex was coded "0" for males and "1" for females. The correlation of -0 .36 between total scale and race indicates that there was a tendency for high scores on total scale to be associated with the Indian children and low scores to be associated with the Caucasion children (t = -3.73, p < 0.001). The correlation of - 0.25 between total scale and sex indicates that there was a tendency for high scores on total scale to be associated with males and low scores to be associated with females (t = 2.39, p < 0.05).

Age did not correlate significantly with the WPBIC total scale (0.11, p > 0.10) nor with hair-A1 concentrations (0.15, p > 0.10). The correlation between race and social class was -0.92. There was a strong tendency for Indians to be rated low on the social economic status scale and

TABLE 1 Summary Statistics for All Variables"

Zero-order correlations m

1 2 3 4 X s

(1) WPBICTS I' 1.00 -0.36 -0.25 0.17 12.29 14.50 (2) Race' 1.00 0.08 0.11 0.50 0.50 (3) Sex'; 1.00 0.11 0.49 0.50 (4) Aluminum 1.00 8.56 4.25

"n = J02. "Walker Problem Behavior Identification Checklist Total Scale. 'Coded " '0" for Indians, " 1 " for Caucasians. "Coded " 0 " for males, " 1 " for females.

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Aluminum and Behavior 9

Caucasions to be rated high. Therefore, only race was used as a control variable, since information on social class would be redundant.

Aluminum accounted for about 5% of the variance in the total scale of the WPBIC, F (1.98) = 7.12 and p < 0.01, over and above the approxi- mately 17% accounted for by race and sex. The standardized partial re- gression coefficient for AI was 0.24, with a standard error of 0.09. In other words, total scale increased 0.24 SD/U increase in A1, with race and sex held constant. The 95% confidence interval of the partial raw-score re- gression coefficient for A1 was 0.21-1.42. As the amount of A1 increased, the degree of problem behavior increased, controlling for race and sex.

DISCUSSION

This study's findings support previous studies of correlates between hair-A1 concentrations and children's behavioral performance. Marlowe and Errera (12) in a study of 22 emotionally disturbed and 25 non- disturbed children, reported significant correlates between hair-A1 con- centrations and WPBIC total scale score (0.35, p < 0.05). In addition, the emotionally disturbed subjects were significantly higher in AI, and one disturbed subject, excluded from the study because of suspected AI poisoning, had a hair-A1 level of 440 ppm, which is 14x the accepted upper limit of 30 ppm for hair-Al established by Doctor's Data, Inc. This child had a history of pica, including chewing on AI cans. Marlowe and others (13) reported a significant association between the 16 WPBIC items measuring distractibility and hair-A1 concentrations in 80 rural ele- mentary-aged subjects (0.34, p < 0.05); the WPBIC total score did not cor- relate significantly with hair-AI values, however. Similarly, Marlowe et al. (14) examined hair-Al concentrations to emotionally disturbed chil- dren (n = 37) and controls (1l -- 107). Although there were no differences in A1 levels in the two groups, a significant dose-response relationship between the WPBIC distractibility items and hair-A1 concentrations was noted for all 144 subjects (0.31, p < 0.05); again, the WPBIC total score did not achieve significance with hair-A1 concentrations.

Rees (15) reported treating a hyperactive boy- -who lived near an AI- processing plant--with an elevated hair A1 of 42 ppm. In a subsequent study, Rees (15) examined hair-Al concentrations of 10 severely delin- quent and psychotic adolescent boys. The hair of 9 of 10 boys had eleva- ted hair-AI levels with 6 of the 10 above 52 ppm. In contrast, Rees (15) noted that only 12.4% of 595 patients had elevated levels. Upledger (16) reported that 70% of a sample of 41 disturbed children were elevated in hair AI, and Schmidt et al. (17) reported higher concentrations of hair-A1 in del inquent boys (n = 22) when compared to laboratory norms. Given the above studies, there appears to be an emerging relationship between increasing AI concentrations and decrements in children's behavioral performance. These data suggest that A1 toxicity may not be a threshold

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10 Moon and Marlowe

or "all or none" phenomenon , but, rather, reflects a cont inuum of delete- rious effects.

The values for human hair A1 in the present study are in general agreement with those found in previous studies of children in general populations or normal control groups, e.g., 9.53 (8), 9.33 (9), 9.41 (13), 9.83 (28), and 10.13 ppm (14), and lower than those reported in children with learning and/or behavior disorders, e.g., 23 (10), 13.84 (11), 20.54 (12), and 12.62 ppm (14).

The moderately high mean WPBIC total scale score of the sample may be attributed in part to the employment of a behavioral measure standardizing on a non-Indian, Caucasian population. Moreover, the teachers rating the Indian and Caucasian children were all Caucasians, suggesting a possible rater cultural bias.

CONCLUSION

We now have a fairlv clear picture of the sequence of events in- volved in A1 encephalopathy in the experimental animal. Aluminum ap- pears to enter the brain and bind to chromatin and possibly other cellular structures (29). It causes an increase in the production of protein, and neurofibrillary tangles subsequently appear in the cytoplasm. Shortly after the appearance of tangles, subtle behavioral changes are noted (30). These are followed by electrophysiological (31), neurochemical (32,33), and anatomical changes (34) that become progressively worse.

Unfortunatey, we have a greater understanding of the effect of AI in nonhuman animals than we do in humans. The metal has dramatic ef- fects in certain species, with little or no effect on others. What we do not know is the effect it has on the human species, e.g., there is uncertainty as to whether it induces neurofibrillary tangles in human neurons. Ani- mal research to date suggests that an encephalopathy is seen only in those species that develop tangles, such that if humans do undergo an AI encephalopathy, but do not develop tangles as suggested, this will be the first species reported to do so.

The biological significance of these findings is not clear, especially given the moderately low levels of hair AI reported here. The significance is compromised by the lack of basic information on the variability of AI levels in the hair and its correspondence with variability in the rest of the body's organs and tissues and information on how major background variables, such as sex, race, and age, influence the concentrations. This is an area in which basic research needs to be done before precise meaning- ful applications on an individualized basis will be possible. Aluminum is ubiquitous in our environment, the field of behavioral toxicology is in its infancy, and future studies are needed examining other biopsy materials

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Aluminum and Behavior 11

to be t te r u n d e r s t a n d a l u m i n u m ' s po ten t ia l role in ch i ld ren ' s behaviora l d i sorders .

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