JOURNAL OF APPLIED TOXICOLOGYJ. Appl. Toxicol. 21, 349–352 (2001)DOI:10.1002/jat.771

Teeth and Blood Lead Levels in EgyptianSchoolchildren: Relationship to Health Effects

Magdy Omar,1 Mohamed Ibrahim,2 Hala Assem,1∗ Yehia Moustafa2 and Fathi Battah1

1 Department of Pediatrics, Faculty of Medicine, University of Alexandria, Egypt2 Public Health, Faculty of Medicine, University of Alexandria, Egypt

Key words: lead; teeth lead; blood lead; paediatric lead exposure; rural; urban; neurological symptoms.

The objective of this work was to study teeth and blood lead levels in Egyptian schoolchildren and torelate lead levels to sociodemographic and environmental factors, the degree of urbanization and suspectedmanifestations of possible lead exposure.

The study was conducted on 60 children aged 6–12 years: 30 children living in an urban area at AlexandriaCity and 30 children living in a rural area at Kafr El-Sheikh Province. Both groups are matched for age andgender. Every child was subjected to history taking, clinical examination and IQ measurements. Laboratoryinvestigations included measuring teeth and blood lead levels, haemoglobin, serum iron and total iron bindingcapacity. The results showed that the mean blood lead level of children in Alexandria was significantly higherthan that of the children in Kafr El-Sheikh; also 56.7% and 6.7% of children from Alexandria and Kafr El-Sheikh had a blood lead level of >20 µg dl−1, with the most frequent symptoms of headache, arthralgia andlack of school interest. The children in Alexandria had significantly lower mean teeth lead and haemoglobinlevels than those of the Kafr El-Sheikh group. A history of wrapping sandwiches in newspapers, age anddistance between the home and school were significant predictors of lead exposure.

These findings support the concept that teeth lead concentration may be a valid addition to the indicatorsused for assessment of the body burden of environmental lead. In addition, children living in urban areassuch as Alexandria need special consideration regarding protection from lead exposure, as well as teeth andblood lead evaluation. Copyright 2001 John Wiley & Sons, Ltd.

INTRODUCTION

Lead is an extremely toxic metal: even a single atom oflead, once in the human body, binds to a protein andinduces some damage; the greater the exposure, the moreserious the effects.1 The rapid urbanization of many partsin Egypt has increased the risk of environmental pollutionand exposure to many hazardous products such as lead.2

Health-concerned personnel are confronted now withdata demonstrating that 3–4 million children are exposedto lead globally, most of whom may have no symptoms,therefore sensitive measures are required to detect leadexposure in children. The more serious effects of leadexposure are due to low-level exposure for long periods,especially on developing brain, therefore knowledge ofthe skeletal burden of lead is of critical importance.1,3

The potential for using lead in whole deciduous teeth,enamel or dentine as an indicator of past exposure ofchildren to lead and as a proxy for skeletal lead has beenwell documented in many studies.3 – 5

The advantage of deciduous teeth lead over bloodlead analysis lies in the incorporation of lead into thetooth during several years from in utero to exfoliation,compared with blood that has an approximate 30-daymean life.3

* Correspondence to: H. Assem, 11 Hani Ali Kamel Street, Sidi Gaber,Alexandria 21311, Egypt. E-mail: halaassem@yahoo.com

AIM

The present work was carried out to study teeth and bloodlead levels in Egyptian schoolchildren and to relate themto demographic and environmental factors, the degree ofurbanization and suspected manifestations of possible leadexposure.

SUBJECTS AND METHODS

The present study was conducted on 30 children(15 males, 15 females) randomly selected from an urbanarea (Alexandria City) and 30 children (14 males, 16females) randomly selected from a rural area (villagesin Kafr El-Sheikh Province). The children were aged6–12 years with mean age ±SD = 9.55 ± 1.82 and8.50 ± 2.51 years, respectively. Both groups were mat-ched for age and gender. The unit of observation wasschoolchildren presenting at dental clinics for tooth extrac-tion or children shedding their teeth. A pilot study wasundertaken before this work to indicate any difficultiesthat may arise.

An interview was conducted for every chosen childand his/her parents for detailed history taking, with spe-cial consideration of residence, environmental exposureto lead, school performance and any symptoms indicating

Copyright 2001 John Wiley & Sons, Ltd.

Received 5 January 2001Revised 21 March 2001

Accepted 21 March 2001

350 M. OMAR ET AL.

lead exposure or toxicity. A written consent for approvalto participate in the study was taken from the parents ofthe children.

Clinical assessment and IQ testing using the WechslerIntelligence Scale6 in addition to anthropometric measure-ments were carried out. Laboratory investigations includedthe determination of blood lead level versus an appropriatestandard using an atomic absorption spectrophotometer,7

in addition to the determination of haemoglobin, serumiron,8 total iron binding capacity9 and the examination ofred blood cell morphology for stippling.

Lead level in deciduous teeth

Deciduous teeth were collected after spontaneous shed-ding or extraction. Teeth that were carious or con-tained dental fillings were excluded. The whole tooth wascleaned with soap and water and then with 6% hydro-gen peroxide for 1 h to remove dirt and blood debris.After that, the tooth was dried, its weight was measuredand it was completely wet digested in 16 M nitric acidand 3.4 M perchloric acid.10,11 The teeth lead level wasdetermined versus an appropriate standard using atomicabsorption spectrophotometry and results were expressedas µg g−1 dry weight of whole tooth.11

Statistical design

The SPSS-PC V 6.0 F/W software package program wasused for statistical analysis of data. Data are presentedas means ± SD. Methods of analysis were applied asappropriate for comparative statistics.

RESULTS AND DISCUSSION

The present study showed that the mean blood leadlevel was significantly higher in urban children living inAlexandria than in rural children from Kafr El-Sheikh,with mean levels of 22.13 and 14.20 µg dl−1, respec-tively, with a significantly higher proportion of children inAlexandria having blood lead levels >20 µg dl−1 (56.7%vs. 6.7%). (Table 1) This may be attributed to the greaterindustrialization of this urban area: more exhaust fumesfrom cars, industrial emissions and use of canned foodand possible water contamination.5

The blood lead levels found in urban children fromAlexandria City are considered very high when compared

Table 1—Ascending cumulative frequency of blood lead levels(µg dl−1) of children in an urban area (Alexandria) and a ruralarea (Kafr El-Sheikh)

Urban (n = 30) Rural (n = 30)Blood lead Student’s(µg dl−1) No. % No. % t-test

�30 3 10 0 0

�25 9 30 0 0

�20 17 56.7 2 6.7

�15 26 86.7 15 50

�10 29 96.7 26 86.7

>9 30 100 30 100

Range 9–35 9–22 t = 4.66

Mean ± SD 22.13 ± 8.56 14.20 ± 3.65 p < 0.001∗

with other results in the literature. Twenty-nine children inAlexandria (96.7%) had blood lead levels of >10 µg dl−1

and thus were considered lead poisoned.1 Seventeen chil-dren in the same group (56.7%) had levels of >20 µg dl−1,which indicates significant hazard compared with only6.7% of rural children from Kafr El-Sheikh, with a sig-nificant difference between both groups (χ 2 = 17.33). ElAraby et al.12 reported that the lower mean blood leadlevel of 15.64 ± 6.58 µg dl−1 in a group of infants andchildren from Alexandria aged 9 days to 12 years may bedue to the inclusion of very young age.

Binns et al.13 studied blood lead levels in 767 childrenin Illinois and reported blood lead levels of >10 µg dl−1

in only 52 and >20 µg dl−1 in 9 children. Al-Saleh et al.14

found that 20% of the studied children from Saudi Arabiahad blood lead levels of >12.59 µg dl−1.

As regards teeth lead levels, the results of the presentstudy showed that they were significantly higher in urbanchildren from Alexandria than in rural children from KafrEl-Sheikh, with mean levels of 7.96 ± 5.20 and 4.97 ±3.77 µg g−1 respectively (Table 2). The detected teeth leadlevels are comparable with other reports from differ-ent areas of the world (8.6 µg g−1 in South Australia,10

3.3 µg g−1 in Boston, USA15 and 4.6 µg g−1 in Taiwan5).In harmony with the present findings, Rabinowitz et al.5

reported a significantly higher dentine lead level in urbanchildren than rural counterparts in Taiwan. They attributedtheir results to more exposure to automobile traffic amongurban school-age children and they also reported higherlead levels in those children of schools near lead smelters.

A trend of positive correlation was found between teethand blood lead levels but this did not reach statisticalsignificance (r = 0.21, P = 0.09). On the other hand, theresults of studies done in Belgium by Cleymaet et al.3

and by Habercam et al.16 in Charleston, South Carolina,USA, showed a significantly positive correlation betweenenamel lead and blood lead.

Teeth lead levels did not differ much according to site,side or the type of teeth studied. Many investigators inother countries have reported different patterns of leadconcentrations among molars, canines and incisors. Somereported that incisors have higher levels,11,17,18 whereasothers reported higher lead levels in molars.16

The results of the present study showed a statisticallynon-significant difference regarding blood and teeth leadlevels between boys and girls. Males showed relativelyhigher blood lead levels than females (mean ± SD =18.40 ± 6.60 and 16.80 ± 6.19 µg dl−1, respectively) andhigher teeth lead than females (7.06 ± 5.05 and 5.90 ±4.40 µg/g−1, respectively). Similar conclusions werereached by studies in Taiwan, USA, Finland and

Table 2—Ascending cumulative frequency of teeth lead levels(µg g−1) of children in an urban area (Alexandria) and a ruralarea (Kafr El-Sheikh)

Urban (n = 30) Rural (n = 30)Teeth lead Student’s

(µg g−1) No. % No. % t-test

�15 5 16.7 1 3.3

�10 7 23.3 4 13.3

�5 19 63.3 11 36.7

>0.5 30 100 30 100

Range 0.89–18.62 1.06–17.39 t = 2.55

Mean ± SD 7.96 ± 5.20 4.97 ± 3.77 p = 0.01∗

Copyright 2001 John Wiley & Sons, Ltd. J. Appl. Toxicol. 21, 349–352 (2001)

TOOTH LEAD IN SCHOOLCHILDREN 351

Australia.4,5,19,20 In contrast, El-Araby et al.12 found thatexposed females had higher levels of blood lead thanexposed males.

Children from rural Kafr El-Sheikh showed asignificantly higher haemoglobin percentage than childrenfrom Alexandria City (79.60 ± 15.09 and 86.66 ± 11.30,respectively). In addition, rural children showed higherlevels of serum iron (50.23 ± 20.30 and 54.13 ±34.56 µg dl−1, respectively) and lower total iron bindingcapacity than the urban children, but the difference wasnot statistically significant (365.27 ± 95.41 and 322.43 ±87.23 µg dl−1, respectively) (Table 3). Moreover, asignificant negative correlation was detected between bothblood and teeth lead levels with haemoglobin levels(r = −0.276 and −0.339, respectively). The haemoglobinpercentage was significantly lower in children with ablood lead level of >20 µg dl−1 (mean ± SD = 76.50 ±13.60 and 85.98 ± 12.87%, respectively).

A negative correlation was observed also betweenserum iron and both blood and teeth lead levels but thisdid not reach statistical significance. (r = −0.101 and−0.224, respectively) A similar but positive trend wasobserved with the total iron binding capacity, which wasonly significant with the teeth lead level (r = 0.533, P <0.05) The association between lead exposure and anaemiais well known. Anaemia is the most common haemato-logical manifestation of lead poisoning and increases infrequency and severity with increasing blood lead level. Alead level of >5 µg dl−1 inhibits haeme biosynthesis dueto blocking of the conversion of 6-aminolevulinic acid toporphobilinogen.21 However, none of our cases had evi-dence of basophilic stippling, therefore it was neither aspecific nor a constant finding in lead poisoning.

One of the main concerns with regard to lead exposurein children has been the effect on the neuropsychologi-cal and cognitive performance of exposed children. Sev-eral studies have looked for the effects of lead exposureon children’s intelligence and cognitive function. Epi-demiological studies indicate a moderate inverse relationbetween the body burden of lead (measured as blood orteeth lead concentrations) and the neuropsychological orcognitive performance of children.22,23

McMichael et al.10 reported that for an increase in bloodlead concentration from 10 to 30 µg dl−1 the estimatedreduction of IQ was 4.4–5.3 points. Needleman et al.15

found that behavioural function was inversely related todentine lead levels, whereas Pocock et al.24 found that the

Table 3—Comparison between haemoglobin (Hb%), serum ironand total iron binding capacity of children in an urban area(Alexandria) and a rural area (Kafr El-Sheikh)

Urban Rural Student’s

Variable (n = 30) (n = 30) t-test

Hb%

Range 61–110 66–110 t = 2.05

Mean ± SD 79.60 ± 15.09 86.66 ± 11.30 P = 0.04∗

Serum iron (µg g−1)

Range 18–118 18–152 t = 0.53

Mean ± SD 50.23 ± 20.39 54.13 ± 34.56 P = 0.59

Total iron binding

capacity (µg g−1)

Range 169–568 164–510 t = 1.81

Mean ± SD 365.27 ± 95.41 322.27 ± 87.23 P = 0.07

blood lead level measured at ∼2 years was significantlyinversely related to IQ.

A negative correlation was found between IQ and bothblood and teeth lead levels in the studied children, butit did not reach statistical significance (r = −0.08 and−0.05, respectively; P > 0.05). Failure to reach statisticalsignificance in our study can be due to several factorssuch as socioeconomic status, genetic factors, parentaleducation and intelligence, which are likely to confoundthe relation between lead exposure and IQ. Furthermore,the relatively small number of children studied may playa role. It is worth mentioning, however, that some of ourchildren with low IQ had relatively high teeth and/or bloodlead levels.

With regard to symptoms that can be attributed to leadexposure, the most frequent symptoms in children wereheadache and arthralgia, followed by lack of school inter-est, then anorexia and, less frequently, neurological dis-turbances, vomiting and bloody diarrhoea. No significantrelation to lead levels being more or less than 20 µg dl−1

could be detected. Similar findings were reported by El-Araby et al.12

On studying the different variables that may affect leadlevel in the teeth or blood, we studied the effects ofage, gender, location of the home (either main street orside street), distance between home and school, presenceof factories or workshops, transportation and method ofwrapping the sandwiches. Multiple logistic regressionanalysis of these variables identified that a history ofwrapping sandwiches with newspapers and the age of thechild were significant predictors of lead exposure in theAlexandria group, whereas the distance between homeand school was significant among children in the KafrEl-Sheikh group (t = 2.49, 2.41, 2.20, respectively).

Studying the sociodemographic factors that may affectthe lead level in children, a significant difference wasnot found regarding blood and teeth lead level amongchildren of educated and non-educated parents. Similarfindings were found by El-Araby et al.,12 but in a studyby McMichael et al.10 less parental education was asso-ciated with a high lead level. With regard to the father’soccupation, we found that children of street sellers hadthe highest mean blood lead levels, followed by clerksand industrial workers, whereas children of farmers hadthe lowest levels; the differences were statistically sig-nificant. This could be explained by the following: streetsellers are exposed to more vehicle emissions and clerksmay deal more with printed materials with lead content.Furthermore, the possibility of lead exposure is more inindustrial workers than others. Among these occupationalgroups, contaminated workers’ hands and/or clothes couldbe the lead source to the household. These results indicatethat the father’s occupation might be a source of pollutionfor indoor family members, including children.

Other studied factors, such as family income per capitaper month, number of siblings and the mother’s education,were not significantly associated with higher blood leadlevels.

It can be concluded from the present study that leadexposure is more in urban areas such as Alexandria Citythan in rural areas such as the villages of Kafr El-SheikhProvince, as indicated by the higher blood and teeth leadlevels in children living in Alexandria. These higher levelswere associated with a degree of anaemia and lack ofschool interest. In addition, examination of deciduous

Copyright 2001 John Wiley & Sons, Ltd. J. Appl. Toxicol. 21, 349–352 (2001)

352 M. OMAR ET AL.

teeth lead may provide a useful index to exposure inprevious years and may indicate cumulative exposure tolead. This might be particularly useful in children withunexplained symptoms such as headache, arthralgia orlack of school interest.

Recommendations

(i) Prevention of lead exposure should be directedat the higher risk groups such as those in citieslike Alexandria by expansion of usage of unleaded

gasoline for all vehicles. Factories and workshopsshould be built away from residential areas. Also,the use of lead in industry should be restricted.

(ii) Mothers should be advised not to use newspapers forwrapping sandwiches.

(iii) Deciduous teeth could be examined in childrenwith unexplained mental retardation or poor schoolperformance when blood lead levels are not toohigh.

(iv) More studies on wider sectors are needed to studyteeth lead levels in relation to lead exposure.

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Copyright 2001 John Wiley & Sons, Ltd. J. Appl. Toxicol. 21, 349–352 (2001)