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Revised February, 1984. 

EPAAJBDOCKgL 

TITLB: Teachers' ratings of children's behaviour inflatio n to 

blood lead levels. 

RUNNING HEAD: Children's behaviour and blood lead levels. 

AUTHORS: William Yule*, Ph.D., Marie^Anne Urbanowicz*, M.Sc., 

Richard Lansdown* Ph.D., and Ian B. Millar^, M.D. 

* Department of Psychology, University of London, Institute of 

Psychiatry. 

+

 Department of Psychological Medicine, The Hospital for Sick 

Children, Great Ormond Street, and, 

/ Greenwich Health District 

2 L J_ 2&/- l£fk>L- *- t>M**; /W. 

Requests for reprints to Dr. W. Yule, Institute of Psychiatry, 

De Crespigny Park,' London, SE^ 8AP, U.K. 

•Ml 

i 

N 
P.3 

ABSTRACT 

Teachers rated the behaviour of 166 childre n whose blood lead 

levels had previousl y been determined. Ratings were made on th e 

Conners Scale , the Rutter Scal e B(2), and Needleman's Scale . ; 

The results broadly replicated the findings of Needleman: (1979) ;: 

in so far as they indicate a relationship between difficulties 

in attention and increased blood lead levels over the normal 

range of blood lead values. "Hyperactivity" on the Rutter and' l4 

Conners scales were found to be significantly related to/children's 

blood lead levels, independent of chronological age. Social • ' 

factors remain uncontrolled in this pilot study. 

2. 
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3. 

INTRODUCTION 

In recent years, there has been a growing concern that levels of lead 

absorption much lower than those leading to lead intoxication may be 

associated with an increase in learning difficulties and behaviour 

problems, (DHSS, 1980). Some authors have claimed particularly that 

increased blood lead concentrations are associated with "hyperactivity" 

(Baloh et al, 1975; David et al, 1972, 1976, 1977, 1979) although this 

has not always been found (Ernhart, Landa and Schell, 1981; Milar et 

al, 1981). Others have reported associations between increased body 

lead burden and impairment in attention (De la Burde and Choate, 1975; 

Needleman et al, 1979). 

Given that lead is a known neurotoxin and that it is well established 

that high doses cause serious brain damage, then it is plausible to 

hypothesize that lower levels of lead exposure may cause lesser degrees 

of damage, with milder or more subtle effects on neuropsychological 

functioning. This plausible hypothesis has proven difficult to investigate. 

Several recent reviews have drawn attention to a number of methodological 

problems which have arisen in studies in this area (Rutter, 1980; DHSS, 1980; 

Needleman and Landrigan, 1981; Yule and Rutter, 1984). 

Firstly, there was the problem of selection bias in sampling either, from 

using clinic based samples or because of high attrition rates. Secondly, 

there are associated problems with the body burden of lead. Blood lead levels 

reflect only recent ingestion of lead and fail to indicate past exposure 

or the duration of exposure. Thus, they cannot differentiate between 

short-term and long-term lead intoxication. In developmental terms, the 

timing of exposure to toxins may be as important as the level of the 

exposure. The quality of blood measurement can be problematical (Vahter, 

1982) and repeated testing is highly desirable. Estimates of the level 

of lead in teeth are considered better indicators -of long-term exposure 

but, of course, teeth can only be analysed when they fall out naturally 

at around 6 to 7 years, an unfortunately early time for the measurement 

of intelligence, attainment and neuropsychological attributes. There is 

some evidence that children who donate teeth are not a random sample of 

the total population (Smith et al, 1983). 
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4. 

Thirdly, the measures of psychological impairment in many studies are 

weak, often involving inadequately validated tests. Too often, large 

batteries of tests have been used with insufficient care taken in 

interpreting a few 'significant' differences which could well be 

attributed to chance. Far too few attempts have been made to replicate 

published studies. Fourthly, and most importantly, few of the early 

studies undertook adequate statistical analyses to control for the 

effects of possible confounding variables. Lead is not distributed 

randomly in the population. Rather, there is a substantial overlap 

between social disadvantage and high level lead exposure. Independently, 

social disadvantage has an adverse influence on children's psychological 

development (Rutter, 1983). Thus, if the effects of lead are to be 

assessed, it is essential to take account of the non-lead effects of 

the social disadvantage with which lead tends to be associated. 

Fifthly, because the effects of lead are likely to be small and because 

of the need to control for confounding variables, it is evident that 

quite large samples are essential if statistically significant differences 

are to be identified. Sixthly, if the main interest is in the effects 

of lead exposure in the general population, it is vital to focus on the 

consequences of blood lead levels below 35 ug/lOOml, as very few 

children in the UK nowadays have levels above 35 in the absence of 

exposure to special hazards, most usually lead in old paint. 

Most of the studies of lead and children's development have been crosssectioned in design, and suffer from the problem of inferring causation 

from correlation. Place of living, income, race, maternal IQ and the 

quality of the care-giving environment have all been found to relate 

to blood lead levels - but they also relate to children's intelligence 

and attainment. Multivariate analyses are required to examine whether 

some or all of the correlation between lead and IQ is due to the fact 

that both lead and IQ themselves are associated with other variables. 

The conceptual and statistical problems involved in disentangling this 

problem are discussed more fully elsewhere (Yule and Rutter, 1984). 

For the present purposes, it is sufficient to note that because the 
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5. 

confounding variables are themselves interrelated , the use pf a single 

co-variate may substantially under-correct for confounding effects; 

whereas the use of many covariates run the risk of over-correction 

(Reichardt, 1979). Different statistica l techniques make different 

assumptions about the psychometric nature of the variables being 

investigated, and assumptions about the nature of shared variance 

(Yule et al , 1981) will determine the order of entry into step-wise 

regression analysis. There is no 'right ' answer as to which technique 

is best in any particula r circumstance, but each investigator needs 

to be aware of the consequences that follow from the choice of statistica l 

procedure. 

Of all -t h e reported studies, tha t by Needleman et al (1979) is the most 

impressive. 2,146 first and second grade children were divided into 

s i x groups according to the estimated level of lead in one discarded 

tooth . Teachers, blind to the tooth lead levels, rated the children's 

behaviour on eleven forced—choices scales. Although no data are given 

on the psychometric propertie s of the scale , teachers' ratings, were 

i 

found to relat e closely to tooth lead levels. Near linea r relation s 

between increasing lead and increasing proportion of teachers' negative 

rating s were reported on eight out of the eleven items. Social factors 

were not controlled in the main analyses. 

These were surprising and challenging findings. The dat a indicated a 

dose—response relationshi p between tooth lead levels and behaviour at 

very low levels of tooth lead. Such findings, if replicated , have 

enormous implications for our understanding of the effects of low leve l 

lead exposure on children's development. 
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Since its publication, Needleman et al's (1979) study has been the subject 

of considerable interest and controversy. Initially, concern centred 

around the selection of the 'high' and 'low' tooth lead groups, the 

nature of the psychological measures, and the handling of confounding 

variables (Rutter, 1980; DHSS, 1980; Yule and Rutter, 1984). More 

recently, the American Environmental Protection Agency examined the study 

with great care and concluded that certain previously unrecognised 

methodological errors were evident, Marchall (1983). A re-analysis 

of Needleman's data will be of great interest. Meanwhile, there 

have been three other general population studies of dental lead 

published. The first two were undertaken by Winneke and his colleagues 

in Duisberg (Winneke, Hrdina and Broekhaus, 1982) and in Stollberg 

(Winneke et al, 1983). In the earlier pilot study, 26 children with 

tooth lead concentration below 3 parts per million (ppm) were compared 

with 26 with levels above 7 ppm. They were assessed on a battery of 

neuropsychological tests, and teachers rated their behaviour. Children 

with the higher tooth lead levels tended to perform less well on the 

tests, but no differences were found on behaviour ratings. The study 

had small numbers and weak control of potentially confounding social 

variables. In the second, major study, carefully selected groups of 

low (below 4.2 ppm), middle (5.8 - 7.2 ppm) and high (above 9.8 ppm) 

tooth leads, amounting to 115 children in all, were tested. This time, 

tests of reaction time were added to the battery and parents provided 

data on 50 possible confounding variables. Again, the highest lead 

group had lowest IQ, but the effect was reduced to non-significant 

levels when confounding variables were controlled. The findings have 

to be treated with caution because of the small sample size, the low 

proportion of children recruited into the study, and the use of 

neuropsychological tests in translation. 
P.8 

7. 

Most recently, Smith et al (1983) have reported on a large scale study 

of 6 to 7 year olds living in London. Screening data were gathered on a 

total population of 6875 children, 60 per cent of whom donated at least 

one tooth. The low lead group (N ° 145) comprised those with a tooth 

lead level of 2.5 ppm or less,the medium lead group (N • 103) had levels 

in the range 5 to 5.5 ppm, and the high lead group (N - 155) were those 

above 8 ppm. Children were given WISC-R, tests of attainment and 

reaction time; teachers completed behaviour rating scales; mothers 

were tested on two subtests of WAIS, and gave detailed information on 

the child's development as well as current social conditions in the 

•home. The three lead groups differed significantly in Full Scale IQ 

(High - 103.7; Medium - 104.9; and Low - 108.7) and in reading. The 

high lead group showed more hyperactivity on the Conners-' scale than 

the others. The IQ differences remained, but were no longer statistically 

significant, following correction for confounding variables. In general, this 

was a very well conducted study which has added considerably to our 

understanding of tooth lead measures and their relationship to children's 

development. However, the children were rather young and overall were 

relatively socially advantaged. More importantly, there are two major 

concerns over their multivariate analyses (Yule and Rutter, 1984). 

Firstly, covariates were selected if they correlated with the dependent 

variable, irrespective of whether they correlated with lead (and many 

did not), when normally covariates are selected if they have significant 

correlations with both the independent and dependent measures. Secondly, 

with 5 to 7 covariates, there is a danger of over-correcting and therefore 

overlooking an effect of lead. 
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8. 

Overall, all four tooth lead studies show a remarkable consistency in 

finding a small difference in IQ between high and low lead groups, even 

after controlling for social factors. There is greater doubt regarding 

the behavioural effects in that the associations with lead levels were 

weak and inconsistent in both the German and the English studies. 

The reasons for the discrepancy with the American study are unclear. 

It was not just a function of controlling for social variables, in that 

the associations were weak even before correction. It could be a matter 

of different measures (all four studies used different scales,), it 

could reflect variations in lead levels (which were substantially higher 

in the Needleman study), or it could be a consequence of population 

differences. 

It is therefore still pertinent to examine the relationship between 

blood lead levels and the ratings of children's behaviour. The present 

study arose from two of the authors' (R. Lansdown and W. Yule) membership 

of the British Department of Health's Working Party on the effects of 

lead on children's health (DHSS, 1980). It began as an attempt to 

examine the use of Needleman's teachers' rating scale in a small sample 

of 166 children for whom estimates of blood lead levels were available. 

The study was intended as a pilot study for more intensive investigations, 

It was mounted quickly in response both to perceived need and to an 

opportunity , and there was not time to gather data on social factors 

other than father's occupation. However, individual measures of 

intelligence and educational attainment were obtained and the results 

on these are reported separately (Yule et al, 1981). In addition, 

teachers completed other standard ratings of children's behaviour. 
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METHOD 9 . 

A 

Sample 

In one of the autonomous screenings of blood lead levels in children 

undertaken by local medical and environmental health authorities in 

response to the ESC directive, in an area subject to an earlier somewhat 

similar survey, (Millar, 1978) 400 children living near a leadworks in 

outer London were studied. Blood samples were taken by venepuncture and 

analysed in the Department of Chemical Pathology and Human Metabolism, 

University of Southampton, under the direction of Professor Barbara Clayton 

and Dr. Trevor Delves. Por the purpose of the present pilot study, it was 

decided to test all primary-school age children in this group whose 

parents and schools consented. 

This paper reports on the results of the teacher ratings of behaviour 

for children aged 6-12 years. The response rate was 3% a__d the sample 

was composed predominantly of children of skilled manual workers. One 

child was found to have a blood lead level of 60jag/100 ml., related 

to the ingestion of paint. She had been chelated before testing began 

and her results have been omitted from the study. Otherwise, blood 

leads ranged from 7 to 32^ig/lOO ml. with a mean of 13.52/ig/100 ml. 

(SD - 4.13). (Pull details of the sample are given in.Yule et al. 1931.) 

On average, the children were 8 years 6 months old (SD • 22 months). 

Their reading ages on the Neale test were, on average, within one month 

of their chronological age. Their spelling and mathematics standard 

scores were, respectively, 94 (SD - 14.8) and 94 (SD - 13.3), again within 

the normal range. Their average WISC-R IQs were: Verbal - 96.8 (SD - 14.2); 

Performance - 100.3 (SD - 13.4); and Pull Scale IQ - 98.2 (SD - 13.4). Thus, 

this sample is well within the normal range of educational attainment 

and intelligence. 
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Teachers' Ratings 

i o 

These were completed in the Summer term 1930, appnftimately one year 

after the blood samples were obtained. In addition to completing the 11 

item Needleman questionnaire, teachers were asked to rate all children 

oh the 26-item Teacher Rating Scale B(2) (Rutter and Yule, 1963) and the 

40-item Conners (Conners, 1969) scale. The B-2 was included as it is 

widely used in Britain as a screening scale for general behavioural or 

emotional difficulties, about which a great deal is known (Rutter, 1967; 

Rutter, Tizard S. Whitmore, 1970; Rutter, Craham, ChadwicK 4 Yule, 1976; 

Rutter, Cox, Tupling, Berger k Yule, 1975). The Conners Scale was' " 

included as it has been widely used in the study of hyperactivity, 

particularly in relation to treatment by drugs (Conners, 1969; Sandberg, 

Rutter and Taylor, 1978). 

Psychological Testing 

This was undertaken by trained psychologists. Children were individually 

assessed on the Wechsler Intelligence Scale for Children-Revised 

(Wechsler, 1974) and the Neale Analysis of Reading Ability, Form A (Neale, 

1958). They were tested in small groups on the Vernon Graded Word Spelling 

Test (Vernon, 1977) and the Vernon Graded Arithmetic-Mathematics Test 

(Vernon and Miller, 1976). 

RESULTS 

a) : The Needleman Questionnaire 

i 

Thel sample was split into quartiles according to blood lead level in order 

to perform statistical analyses analogous to those performed by Needleman 

et al (1979). 
P.12 

11. 

_ 

Table 1 shows the percentage of children in each blood lead quartile 

who received negative ratings from their teachers on each item on the 

Needleman scale. On 2 items there were discernable trends for children 

with higher blood lead levels to receive more negative ratings. The 

overall association, assessed by chi-square, was significant in 5 of the 

11 items. In four others - distractible, not persistent, dependent, 

and disorganised - it seems that children with blood lead levels of 

12^ig/l00 ml. and below receive fewer negative ratings -than those above 

this level. As in the Needleman sample, hyperactivity was noted in very 

few children and was not associated with blood lead level. The results 

are shown graphically in Pigure 1. 

(Figure 1 near here) 

The total scores on the Neeldeman questionnaires differ across the 

four blood lead groupings at a level which is not statistically 

significant (P • 2.15, P • 0.096). There is, however, a trend for 

the total scores to increase with increasing blood i«ad levels with, 

again, the greatest difference occurring at the 12 ng/100 ml. cut off 

point• 

b) The Rutter B(2) Questionnaire 

Table 2 shows the percentage of children above and below the medianlead level being rated as "deviant" - i.e . scoring 1 (Applies somewhat) 

or 2 (Definitely applies) - on the B(2) scale by their class teacher. 

It can be seen that in 20 out of 26 items, children in the upper 50$ 

of lead levels were rated more deviant than those in the lower 5C$. 

The differences were statistically significant (p^0.05) in two items 

- "Squirmy" and "Fights" - and marginally significant (0.05>P>.10) in 
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A further five - "Sucks Thumb", "Bites Nails", "Inert", "Disobedient", 

"Truants". In the ease of "Truants", this was commoner in children 

with lower blood lead levels! The increase in thumb sucking and biting 

nails in the higher lead group is obviously of interest in so far as it 

indicates one behavioural mechanism whereby increased lead can get into 

the body. Overall, however, the associations with individual items are 

small. This probably indicates that only a small proportion of the 

Variance of behavioural deviance and blood lead levels is shared and that 

larger numbers will be needed to understand the nature of the association. 

Recently, a factor analysis of the B(2) scale (Schachar, Rutter and Sfaiith, 

1981) found a separate "overactivity" factor, defined by adding the scores 

on the following items:- RESTLESS + SQUIRM! + CAN'T SETTLE. Children are 

classified as "overactive" if their score is 3 or more on.these items. 

As can be seen in Table 3r significantly more of the children in the 

higher lead groups are classified as "overactive". Indeed, 4.9$ of those 

below the median lead level compared with 19.0$ above are classified as 

"overactive". 

c) The Conners Questionnaire 

As on the B(2) scale, there were few individual items on the Conners 

scale vhich related significantly to blood lead levels. However, the 

scale has been shown by factor-analysis to yield a number of sub-scales 

vhich have been replicated in a variety of studies (Conners, 1969). Table 4 

sunnnarises the results of five one-way analyses of variance in which 

the children have been divided at the median score into low and high 

blood lead groups. As can be seen, on every sub-scale, the children 

vith higher blood lead values are rated as more deviant, and this 

reaches statistical significance in relation to Conduct Probleas, 

Inattentive-Passive and Hyperactivity. 
P.J 4 

13. 

Iew0^<3_?p tho Ceases5 °o seslop -saei. _2©r© tfeaa th® ether two scales^ is 

heavily develepseatally loaded. Younger ehild_?ea therefor© are giv©a 

higher seo?©s!o Yeuage? ehildrea alse hav© higher blood lead levels. 

average @g© ef eu? high©? lead ^oup was 8 years? whilst that of 

eMld_?©a i a th© lew©? 50$ ef th© Meed X©ad distributie a wsy§ 9 yea_?s. 

Thos'Qfo?©,, i t was a©e©0ss_?y t e perfers aa saalysis ef eo^asdsae© es th© 

Ge_aer°_i score to coatrol for th© effects ef ag«o As seea i a fable 4^ 

th© differences regain eves after age is eestrolledo 

^ ) Similarities across the scales 

Fiadiaga. oa iadividua! itea s should b© treat s with eaatioa for two 

yeaaoas. firstly,; the shorter the ®ea_-@s the less reliabl e i t is. 

_k___3ated scores or factor scores §__© always ©ere reliabl e thaa individual 

items. Secondly,, with se aaay individual itea s beiag ©sasiaed,, some 

differences are bcuad t e arise by e__aace0 Over al l three teacher rating 

sc&le&y 77 iadividual itea s wer© rated, l y ehaae© ales© 4 eas be 

expected t e be "significant53 at the % level, l a fact 9 oaly 7 itess 

wer© found to be related t e lead level a. P o 0.05. This ©i^at be 

regarded as iadicstiag oaly chaac© levels but fe? two faet©?ss~ firstly,, 

4 ef the 7 itea s wero ea the _meh shorter Beedlesma Scalej gieeoadly,, 

th© r©@alts ea the ^©©Ideaaa Seal® as a©t©d ©asflier,-, by sad large 

?©plieat© hi® ©arlieg? gstedy0 

HsQt__.©r©9 (Laasdowa ©t al c 1983 )j w© hav© shewa that seer©® ea th© 

-jQS&lesaa Scales are highly related t e scores oa th© Butter Scale. 

KorQover,; iadividual Ueedle@aa Seal© itess shew ae age leadings,, oaly 

eag sex differeace aad oaly two ©igaifieaat relationships with social 
P.15 

class. However, 9 of the 11 items showed significant relationships 

vith WISC-R Pull Scale IQ. It vould seem that the Needleman Scale is 

tapping broadly similar areas to the Rutter and the Conners scales. 

However, it appeara to be more sensitive to body lead levels and this 

may be because it taps behaviour related to focussing attention rather 

thaa wider categories. 

DISCUSSION 

These results broadly replicate the findings of Needleman et al (1979) ia 

respect of teachers' ratings of behaviour. On the same items, there are 

indications of a dose—response relationship betveen increasing lead 

levels and an increased likelihood that teachers record deviant behaviour. 

A number of differences betveen Needleman's study and the present one 

must be noted. Firstly, his scale vas used vith American.'teachers and 

it has not previously been used in Britain. Hovever, it does appear 

that it is being used in a similar way. Secondly the present study has 

smaller numbers and a wider age range of children. Thirdly, the 

estimate of body lead burden came from a single determination of blood 

lead level taken some nine months prior to the teachers' ratings of 

behaviour. With these differences in mind, the similarity to Needleman's 

findings is all the more impressive. 

The results on the factor scores derived from both the Rutter B(2) 

scale and the Conner's Scale provide harder evidence for an association 

betveen increasing blood lead levels and increasing ratings of hyperactivity 

by teachers. It must be remembered that this is an association vithin 

an essentially normal sample of children. They are not seen by their 

teachers as being in aay vay unduly deviant in their behaviour. These 

results can be viewed as the first real confirmation of the existence 

of this relationship. 
P.16 

15. 

However, the results of the present pilot study cannot investigate fully 

the nature of the demonstrated associations. Because father's occupation 

is the sole datum available on social factors, we have not attempted in 

this study to partial out the contribution of social factors to the present 

findings. Many aspects of family life or child rearing practices could 

be related to children's behaviour, intelligence and exposure to lead in 

the environment. Good measures of relevant social and family factors 

are required with larger numbers of children before the nature of the 

relationship between body lead burden and adjustment can be better 

understood. A second such study is now in progress and we await the 

results of that study before exploring the nature of the relationship 

further. 

As noted in the introduction, it is unfortunate that the English (Smith 

et al, 1983) and German (Winneke et al, 1982; 1983) studies did not include 

identical measures as those used by Needleman et al (1979). It remains 

unclear as to the reasons for the largely negative findings with respect 

to behaviour ratings. In part, in view of the present findings, some of 

the difference must have to do with the properties of the scales used; 

in part, different characteristics of the samples may lie behind 

different findings. Smith et al (1983) looked at the youngest group. 

Even younger children were observed during testing in the recent Birmingham 

study (Harvey et al, 1983), where direct observation was not related to 

the blood lead levels. Thus, age of sample may be an important factor. 

Similarly, Smith et al (1983) had a more socially advantaged group than 

either our London sample or the German sample. In both the German 

studies and our own, IQ effects were found to be stronger in the socially 

disadvantaged subgroups. Clearly, this has to be investigated more fully 

in respect of behavioural ratings. 
P.17 

16. 

Despite the similarity between the present findings and those of Needleman 

et al (1979), the findings from other investigations are contradictory. 

It is premature to rule out the possibility of an effect, but, equally, 

there are no strong grounds at present for inferring one. The fact that 

the strong effects on behaviour stem from studies that were unable to 

control for confounding variables must raise real doubts about the 

reality of the effect. On the other hand, the behavioural measures 

have been less adequate than the cognitive assessments and it may be 

that the inconclusive findings simply reflect the weaknesses of the tools 

used to evaluate behaviour (Yule and Rutter, 1984). David et al's 

(1983) finding regarding the apparent behavioural benefits of chelation 

means that the possibility of lead effects on behaviour cannot be 

dismissed. What are needed are well planned longitudinal studies 

which take repeated measures of neuropsychological functioning, academic 

attainment and behaviour. Together with more refined measures of social 

factors, such a longitudinal study would go a long way towards unravelling 

causal relationships, whose nature can only be imperfectly inferred from 

samll cross-sectional studies. 

ACKNOWLEDGEMENTS 

This study was supported by a grant from the Medical Research Council 

(SPG/979/1160). We are grateful to officers of the Inner London and 

Bexley Education Authorities and to the headteachers and teachers for 

their co-operation. We wish to acknowledge the generosity of Drs. 

Taylor and Sandberg in making their unpublished data available to us. 

Miss J. Hunter assisted in the data analysis. 
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P.20 

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. 
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