Arch Environ Contam Toxicol (2015) 68:442–450 DOI 10.1007/s00244-014-0108-5
Screening for Childhood Lead Poisoning in the Industrial Region of Fez, Morocco S. Bouftini • J. Bahhou • B. Lelievre • J. M. Chao de la Barca • A. Turcant B. Diquet • S. Abourazzak • S. Chaouki • M. Hida • A. Khattabi • C. Nejjari • A. Amarti • S. Achour
•
Received: 12 May 2014 / Accepted: 20 November 2014 / Published online: 16 December 2014 Ó Springer Science+Business Media New York 2014
Abstract The study objectives were to estimate lead poisoning prevalence among children living next to an industrial area, to compare it to that in a control population, and to establish clinical and biological follow-up of the poisoned children. This is a descriptive cross-sectional study including 150 children (exposed and unexposed) performed between January 2012 and April 2013. It was meant to determine blood lead levels (BLLs) in children considered to be an exposed population (EP N 90), living in the industrial area Ain Nokb Fez compared with BLLs of children of other areas belonging to the same city supposed to be unexposed [UP (N = 60)]. A sociodemographic questionnaire was obtained, and a blood lead analysis was performed. Clinical and biological follow-up has been performed of poisoned children. The sample consisted of 90 EP children with an average age of 6.82 ± 3.32 years and male-to-female sex ratio (SR) of 1.5 and 60 UP children with an average age of 6.45 ± 3.29 years and an SR
of 1.2. Among the 150 children recruited, the average of BLLs was 58.21 ± 36 lg/L (18–202.3 lg/L). The average of BLLs in EP children (71 ± 40 lg/L) was statistically greater (p \ 0.0001) than that registered in UP children (38 ± 13 lg/L). All poisoned children belonged to the EP group at a prevalence of 21.1 %. The clinical and biological examinations of poisoned children showed a few perturbations such as anemia, hypocalcaemia, and deficiencies in magnesium and iron. No renal disease or objective neurological disorders were observed. In the follow-up of the children with BLL C100 lg/L (19 cases). BLL monitoring showed a significant decrease in average of blood concentration ranging from 136.75 ± 32.59 to 104.58 ± 32.73 lg/L (p \ 0.0001) and in lead poisoning prevalence (p \ 0.001), which decreased to 7.8 % from 21.1. Our study showed a high prevalence of lead poisoning (21.1 %) in EP children. The relocation of the industrial site associated with corrective and preventive measures has contributed to a decrease of
S. Bouftini (&) J. Bahhou Laboratory of Analysis and Modeling of Continental Ecosystems, Faculty of Science Dhar El Mehraz (FSDM), Universite´ Sidi Mohamed Ben Abdellah (USMBA), Fez, Morocco e-mail: [email protected]
A. Amarti Laboratory of Medical Analysis, Faculty of Medicine, University Hospital and Medical Centre of Biomedical and Translational Research, Universite´ Sidi Mohamed Ben Abdellah (USMBA), Fez, Morocco
B. Lelievre J. M. C. de la Barca A. Turcant B. Diquet Pharmacology-Toxicology Laboratory, University Hospital of Angers, Angers, France S. Abourazzak S. Chaouki M. Hida Pediatric Department, Hassan II University Hospital of Fez, Fez, Morocco A. Khattabi C. Nejjari Laboratory of Epidemiology, Clinical Research and Community Health, Faculty of Medicine and Pharmacy, Universite´ Sidi Mohamed Ben Abdellah (USMBA), Fez, Morocco
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S. Achour Laboratory of Medical Analysis, Toxicology Unit, Faculty of Medicine, University Hospital of Fez and Medical Centre of Biomedical and Translational Research, Universite´ Sidi Mohamed Ben Abdellah (USMBA), Fez, Morocco
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exposure and lead poisoning prevalence in the aforementioned population.
Childhood lead poisoning is a global public health problem that has been highlighted in developed countries since the 1980s, but it is underestimated in developing countries (Falk 2003; UNICEF-PNUE 1997). Lead is of growing concern because of its known toxicity even at low levels (Bellinger 2008). The World Health Organization (WHO) estimates that lead poisoning causes 0.6 % of the global burden of disease and contributes to approximately 600,000 cases of intellectual disability in children annually (WHO 2010b). In Morocco, in addition to known sources of lead exposure, there are other specific causes such as the use of glazed utensils, products of traditional medicine such as kohl, and the presence of industrial and handicraft agglomerates exposing citizens to the risk of lead exposure and poisoning. This country is at high risk with regard to its important artisanal and traditional activities based primarily on metallurgy, pottery in poor working conditions, and a lack of respect for the regulations concerning specific measures prevention and health rules applicable to the institutions. However, few studies of lead human exposure in an industrial environment have been published (Laraqui et al. 2000). Young children are particularly exposed to lead because of behavioral factors such as frequent hand-to-mouth activities, biological factors including greater gastrointestinal absorption, and the development of their nervous system (Bellinger 2004; Oulhote et al. 2011; Lidsky and Schneider 2003). Emerging evidence has also suggested that even children with blood lead concentrations \100 lg/L are at significant risk to decreased cognitive development and functioning including intelligence quotient deficits (Canfield et al. 2003; Surkan et al. 2007; Liu et al. 2013) and poor academic performance (Chandramouli et al. 2009; Wang et al. 2002). Other studies have shown that environmental and occupational lead exposures increase cancer risk, particularly lung and stomach cancers (Fu and Boffetta 1995; World Health Organization International Agency for Research on Cancer 2006). Lead pollution is a threat to health, especially for children who live in the surrounding communities of artisanal and industrial sites, such as mineral smelters and refineries, where exposure to heavy metals through inhalation and ingestion of contaminated soil and dust is possible (UNICEF-PNUE 1997; WHO 2010b). In 2010, a Nigerian study of children living in villages where artisanal gold mining was practiced found that 97 % had BLLs [450 lg/L (Dooyema et al. 2012). To our knowledge, no study concerning childhood lead poisoning in an industrial environment in Morocco has been
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performed so far. In this context, we chose for our study the industrial site of Ain Nokbi, which is located in an urban agglomeration in the city of Fez. It is known for its activities based essentially on pottery, tanning, brassware, ceramics, and mosaic. It contains foundries for the manufacture of raw materials (enamel) based on a mixture containing [74 % of lead, which is extracted from old pipes brought to a temperature of 1,200 °C. This site also contains traditional ovens (168 traditional ones) reserved for baking pottery that emit emanations whose lead content is approximately 212.87 lg/m3 (Laraqui et al. 2000) (Fig. 1). This value exceeds the maximum concentration allowed in the workplace, which is 150 lg/m3 (Institute for Public Health Surveillance 1999); this can be explained by the escape of lead salts contained in galena when backing pottery. The objectives of the study were to evaluate lead exposure and estimate lead poisoning prevalence among children living near the study area to compare them with those of a control population of children who do not live in the abovementioned region and, finally, to establish clinical and biological follow-up for the children having BLLs C100 lg/L.
Materials and Methods Ethics Statement This study was approved by the Ethical Committee of the University Hospital Hassan II (Morocco). Written informed consent was obtained from all of the participants’ parents or guardians after they had been fully informed about the study details. A questionnaire was devised for the children. The Study Site Fez is located in the region of Fez-Boulemane in central northern Morocco with a population of 1,050,000 inhabitants. It is the capital of artisanal and industrial activities. Since the 1970s, the artisanal place, Ain Nokbi, was implanted in the Fez old medina; it employs approximately 250 craftsmen (potters and tanners), and it is an essential catalyst for social and economic development of the region. Agglomerations of new habitats (built after 1985) are located around the industrial site. The latter generates environmental pollution resulting from industrial discharges and craft. A few months before the beginning of our study, this site was moved to a nearby place (Fig. 2). Study Population This is a descriptive cross-sectional study performed between January 2012 and April 2013 on 150 children
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Fig. 1 Polluting fumes and toxic emissions from the traditional ovens in the industrial area Ain Nokbi (EP)
(exposed and unexposed) whose ages ranged from 6 months to 12 years. It was meant to determine BLLs in children considered to be an exposed population [EP (N = 90)] who live in the industrial area Ain Nokbi Fez compared with BLLs of children of other areas of the same city considered to be unexposed [UP (N = 60)]. The EP children were recruited at the health center located in the area at risk and UP children at the Fez University Hospital. They were selected in a random manner during pediatric consultation and based on the address of their habitat. Exclusion criteria included severe diseases that involve vital prognosis or antecedent of recent blood transfusion. Parents or guardians of each participating child were asked to complete a sociodemographic questionnaire including queries on age, parental occupation, smoking, type of housing, type of water consumption, use of kohl, and use of lead-based utensils. Dosage and Interpretation of Blood Lead Levels Five milligrams of venous blood sample was collected from each child in trace-metal free ethylene diamine tetraacetic acid-vacutainer tubes at the time of recruitment in the health centre and in the hospital university. When collecting the samples, precautionary measures were taken to exclude the possibility of sample contamination from lead on the skin. The lead analyses were performed in the Toxicology and Pharmacology Laboratory at the University Hospital of Angers, France, using inductively coupled plasma-mass spectrometry (ICP–MS) with the quantization ion [Pb (m/
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z = 208)] using rhenium as an internal standard [Re (m/ z = 185)]. The blood is initially diluted 1/2 in a solution of 0.2 % Triton in suprapur HNO3 0.5 % before final dilution (1/ 20) as calibrants. This technique is considered to be sensitive and reliable for the determination of such metals (White 1999; Zhang et al. 2010). The limit of quantification is 12.5 lg/L, and the limit of detection is approximately 4 lg/L. According to the classification given by the Centers of Disease Control and Prevention (CDC 2005), children of our study were classified in accordance with their BLLs as follows: class I = BLL \100 lg/L; class IIa = BLL 100 to B149 lg/L; and class IIb = BLL 150 to B249 lg/L). Only children with BLL C100 lg/L will benefit from a clinical examinations which will be performed by a group of medical specialists (neurologists, pediatricians, pediatric endocrinologists, and toxicologists), biological tests (complete blood count, renal and hepatic function, and determination of iron, calcium, and magnesium), and medical follow-up. Parents of participants will also be invited to attend awareness sessions concerning the hygiene advice to follow to decrease lead exposure. BLL control as well as clinical and biological examinations will be performed 9 months after the first screening to check the evolution of exposure in children who had BLLs C100 lg/L. Determination of Lead Content in Water As a complement to the study, water samples were taken after one-night stagnation from the households of the children with BLLs C100 lg/L. This allowed evaluation of the
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Fig. 2 Location of Ain Nokbi industrial sites in the city of Fez, Morocco
maximum exposure to lead from drinking water. The water samples were collected in precleaned polyethylene bottles; the samples were stabilized with 1 mL of nitric acid; and blanks were taken. The analytical technology used was inductively coupled plasma-atomic emission spectrometry (ICP–AES). The determination of lead in the air was not performed due to the lack of technical means to do so. Statistic Analysis Statistical analysis was performed with SPSS software (Statistical Product and Services Solutions, version 17, SPSS Inc, Chicago, IL). Comparison of averages was performed by way of classical parametric testing depending on the nature of the variables to be compared as well as nonparametric tests in case of some weaknesses or strengths. To test significance evolution of BLL in terms of prevalence and concentration means, statistical tests for matched series were used. A p value \0.05 was considered significant.
Results Sample Characteristics The sample consisted of 90 EP children with an average age of 6.82 ± 3.32 years and male-to-female (M/F) SR of 1.5 and 60 UP children with an average age of 6.45 ± 3.29 years an M/F SR of 1.2. As listed in Table 1, the two populations were comparable regarding various sociodemographic parameters including exposure to passive smoke inhalation. According to the questionnaire, pica behavior was noted in 50 % of both EP and UE children. The average age of living habitats was 28.44 ± 6.98 years for EP children and 24.4 ± 9.93 years for UP children. The existence of lead pipes was reported at 2 % for EP and at 2 % for UP children. Lead Exposure Among the 150 children recruited in the survey, the average of BLLs was 58.21 ± 36 lg/L in the population with
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Table 1 General characteristics of EP and UP study participants (N = 150) Characteristics
EP
UP
p
N = 90
%
N = 60
%
0–6
35
38.9
25
41.6
6–12 Sex
55
61.1
35
58.3
Male
54
60
33
55
Female
36
40
27
45
Classes by age (year) 0.05
0.06
Pica Yes
49
54.4
28
46.6
No
41
45.5
32
53.3
Yes
42
46.6
35
58.3
No
47
52.2
25
41.6
0.22
Use of glazed utensils 0.31
Parents’ function at risk Yes
33
36.6
16
26.6
No
57
63.3
44
73.3
0.14
Passive smoke inhalation Yes
54
60
33
55
0.33
No Use of kohl (mothers and/or children)
36 90
40 100
27 60
45 100
-
Consumption of tap water
90
100
60
100
-
For use of glazed ustensils N(UP): 89
extremes ranging from 18 to 202.3 lg/L, and the median value of BLLs was 48 lg/L. In both populations, BLLs were greater in male than in female children (p \ 0.001).
Fig. 3 Distribution of BLLs of the two study populations (EP and UP) in terms of the exposure. Study exposed, unexposed (N = 150)
Blood lead concentration was not statistically significant with respect to age. The average of BLLs of EP (71.43 ± 40 lg/L) children was statistically greater (p \ 0.0001) than that of UP (38.38 ± 13 lg/L) children. The distribution of blood lead according to exposure is illustrated in Fig. 3. Among 90 EP children, 71 (78.88 %) had BLLs \100 lg/L (class I) with an average of 53.96 ± 17.35 lg/ L, a minimum of 18.77 lg/L, and a maximum of 99.27 lg/ L. The 19 (21.11 %) children that remained had BLLs C100 lg/L with an average of 136.75 ± 32.59 lg/L, a minimum of 103.2 lg/L, and a maximum of 202.3 lg/L. Of those 19 children, 6 had BLLs between 100 and 149 lg/ L (class IIa), and 13 had BLLs between 150 and 249 lg/L (class IIb). No patient had BLL [ 250 lg/L (class III). The prevalence of lead poisoning in this EP is 21.1 % (95 % CI 20.21–21.99 %). For all 60 UP children, BLLs did not reach 100 lg/L, and thus they all belonged to class I (B100 lg/L) with an average of 38.38 ± 13 lg/L, a minimum of 18.22 lg/L, and a maximum of 90.05 lg/L. The average BLL of E children was relatively greater than that of UP children regardless of the age of habitats, the parents’ jobs at risk, the nature of water consumption, the use of traditional utensils or kohl, and the presence of pica behavior or passive smoke inhalation (Table 2). Consumption of tap water was found among 100 % of the study population. In addition, water samples analyzed from children with BLLs C 100 lg/L did not show lead levels [10 lg/L, thus meeting drinking water standards set by WHO (2008).
40
Unexposed Population
Exposed Population
35 30
Effective
25 20 15 10
[180 - 200
[200 - 220
[120 - 140
[160 - 180
[100 - 120
[140 - 160
[80 - 100
[60 - 80
[40 - 60
[
[0 - 19
[
[
123
[
[
Classes of BLLs
[
[
[
[
[
[
0
[20 - 40
5
Arch Environ Contam Toxicol (2015) 68:442–450
447
Table 2 Distributions of average BLLs according to exposure factors in EP and UP children (N = 150)
Table 3 Monitoring clinical, biological, and toxicological problems presented by children with BLLs 100 lg/L (N = 19)
Exosure factors
BLL groups and problems
EP No.
UP Mean of BLLs (±SD)
No.
p
After 9 months
No.
%
No.
%
Class I (BLL B100 lg/L)
0
0
12
63.2
Class II a (100B BLL B149 lg/L)
6
31.5
7
36.8
Class II b (BLL 150 to B249 lg/L)
13
68.5
0
0
Mean of BLLs (±SD)
90
71 ± 40
60
38 ± 13
\0.0001
\6
35
71 – 43.8
26
42.8 – 14.3
\0.001
[6
55
71.4 – 37.4
34
35 – 11.3
Total
At the time of screening
Age (year) \0.0001
Sex
BLL group
Clinical and biological perturbations
Male
57
77.3 ± 43.7
27
43.3 ± 14.9
\0.001
Female
33
61.2 ± 30.9
33
32.3 ± 10.8
\0.001
Pica
Clinical signs Neurological disorders
25
54.34
21
45.65
Gastrointestinal disorders
9
90
1
10
Yes
49
72.9 – 38.5
28
38.2 – 11
0.0001
Locomotor disorders
6
54.54
5
45.45
No
41
69.6 – 42.2
32
38.5 – 14.9
0.001
Other signs
16
53.33
14
46.66
Anemia
7
77.77
2
22.22
Hypocalcemia
8
72.72
3
27.27
Iron deficiency Magnesium deficiency
4 18
66.66 51.42
2 17
33.33 48.57
Parents’ function at risk
Biological signs
Yes
33
71 – 36.5
16
38.8 – 11.3
0.0001
No
57
72.8 – 46.3
44
38.2 – 13.9
\0.0002
Use of glazed utensils Yes 42 72.9 – 40.9
35
39 – 15.3
70.5 – 39.6
25
37.8 – 11.5
No
47
0.002 0.0001
BLLs blood lead levels
BLLs blood lead levels
Clinical and Biological Aspects The results of clinical and biological tests are listed in Table 3. Clinical examinations highlighted essentially neurological disorders in 25 cases including microcephaly (3 cases), epilepsy (1 case), headache (5 cases), restlessness (6 cases), language and walking delays (3 cases), and lack of concentration (7 cases). Digestive disorders were present in 9 children as oral and dental disorders, e.g., Burton’s lines (3 cases), abdominal pain (3 cases), nausea (2 cases), constipation (1 case), locomotor disorders represented by growth retardation (4 cases), and muscle and joint pain (2 cases). The results of the biological examinations showed the existence of hypochromic microcytic anemia (7 cases) and hypocalcaemia (8 cases). The decrease in serum ferritin values was found in four children, and no renal or liver failures were detected. However, 95 % of poisoned children had magnesium deficiency. Follow-Up of Children with BLLs C100 lg/L In the follow-up of these children (19 cases), BLL monitoring and biological and clinical examinations were performed 9 months after the first screening and showed a significant decrease in the average of blood lead concentration from 136.75 ± 32.59 to 104.58 ± 32.73 lg/L (p \ 0.0001) and in the prevalence (p \ 0.001) of lead poisoning from 21.1 % (95 % CI 20.21–21.99 %) to 7.8 %
(95 % CI 7.22–8.38 %). Among the 19 children, 12 belonging to class II became class I. Seven of them belonging to class IIb became class IIa (Table 3). In addition, clinicobiological monitoring showed a decrease in the number of clinical disorders (abdominal pain, constipation, and pallor) and biological disturbances (anemia and hypocalcaemia) (Table 3).
Discussion In this study, average BLLs in EP (71.43 ± 40 lg/L) children was significantly greater compared with that recorded in UP (38.38 ± 13 lg/L) children. The same result was observed in a study performed among children living in the immediate vicinity of battery shops where EP children had average BLLs that were significantly greater (498.8 ± 14.95 lg/L) compared with that of EP children (99.2 ± 1.90 lg/L) (Suplido and Ong 2000). Compared with international data, the average BLL of EP children (71.43 ± 40 lg/L) was greater than that recorded in children living near an industrial site in the same region of study (48.23 lg/L) (Laamech et al. 2014), but it was less important than that recorded in exposed children living in the immediate vicinity of battery shop who had significantly higher mean BLLs (498.8 lg/L) (Suplido and Ong 2000). The maximum BLL recorded in this population was 202.3 lg/L, which is significantly lower than that recorded in children living near the gold-mining
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area in the northwest of Nigeria, where it exceeds 450 lg/L (Dooyema et al. 2012). The average BLL of UP children was 38.38 ± 13 lg/L, which is greater than the average value recorded in Swedish children (14 lg/L) and children in Ecuador (31.7 lg/L) (Hruba et al. 2012) suggesting that exposures are still occurring. Sources are not apparently linked to pica, the use of glazed pottery, or the use of cosmetics products, but they still must be identified. In our survey, the BLL average found in males was significantly greater than that in females. Similar findings have been reported by other investigators (Becker et al. 2002; Needham et al. 2005; Alimonti et al. 2005 and Wilhelm et al. 2004). This can be explained by the turbulent and restless behavior of boys, who frequent a more external environment. In accordance with the Vietnam Study (Sanders et al. 2014), the effect of age was not observed between our two age groups. The prevalence of abnormal BLLs (C100 lg/L) was significantly greater (p \ 0.0001) in EP children (21.11 %). This value is greater compared with that of registered among children in Settat city (14.3 %) (El Kettani et al. 2010). A similar study concerning the exposure of children residing in a smelting craft village in Vietnam recorded prevalence rates of 80 %, which is largely exceeds that recorded by our study (Sanders et al. 2014). In our study, the exposure factors studied (age of habitats, parents’ jobs at risk, water consumption, use of traditional utensils or kohl, and presence of pica behavior or passive smoke inhalation) did not influence lead exposure in EP children. Atmospheric pollution remains a major factor that seems to be responsible for the exposure to lead in children in this area who can usually absorb several tens of milligrams of dust per day (INSERM 1999; Lanphear et al. (1998). Many studies in this direction have shown that the illegal use of lead has impacts on the environment and on the health of children in several countries (Dooyema et al. 2012; Kuijp et al. 2013; Suplido and Ong 2000; Garcia Vargas et al. 2001). In the same direction, a Senegalese study, performed after the death of 18 children living on the outskirts of the city of Dakar, recorded severe lead poisoning from recycling of lead batteries (Haefliger et al. 2009). Moreover, the use of kohl, which is a cosmetic product for the eyes, is widely disseminated in the Maghreb countries and remains an ancestral and cultural practice among women and children. It is known for its medicinal, pharmacological, and prophylactic properties. Even if kohl contains lead and is used by 100 % of the study population, we cannot conclude its contribution to lead exposure on the basis of this study, although many studies have established a correlation between the use of kohl and abnormally high BLLs (Sainte et al. 2010; Al-Ashban et al. 2004; De Caluwe 2009).
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In addition to kohl, the use of glazed utensils, in particular the Moroccan tagine, can be also a factor influencing BLLs positively. In fact, several cases of lead poisoning have been identified as a result of the use of artisanal ceramics (Hellstrom-Lindberg et al. 2006; Bossi et al. 1991) and artisanal glazed potteries, especially tagine (Hellstrom-Lindberg et al. 2006; Sabouraud et al. 2009; Yazbeck et al. 2007). In France and the United States in nonindustrial environments, lead-based paint is considered to be the primary source of lead in children with BLLs C100 lg/L, especially for children who live in older homes (Jacobs et al. 2002). This factor has not been found in this study because for the UP children, their habitations were new, so they do not have lead-based paint; for the EP children, the walls of their habitations were uniquely covered with lime. The lead level in drinking water is also an aggravating BLLs factor, in our study, analysis of water consumption from households of children with BLL C100 lg/L, has shown normal rates, thus eliminating water origin in exposure. The clinical and biological examinations showed a few perturbations such as anemia, hypocalcaemia, and magnesium and iron deficiencies. These perturbations may be related to lead exposure because they may result from hygienic and dietary habits because the socioeconomic and cultural level of the population is low. The cases of microcephaly, epilepsy, or the appearance of Burton’s lines cannot be related to the BLLs measured in this study because BLLs are not at all representative of past exposures; however, but they can be linked to much greater past exposures. In our study, no renal disease or objective neurological disorders such as encephalopathy and neuropathy were observed in children having BLLs C100 lg/L. Indeed, renal disease was not observed in exposed workers who have BLLs \400 lg/L, and for objective neurological disorders, BLLs must be [500 lg/L in children (Garnier 2005; Roels 2002; WHO 2010a). No chelation therapy was prescribed for our patients because BLLs records did not exceed 450 lg/L (CDC 2002; Garnier 2005). However, children with BLLs C100 lg/L received prescription medication including vitamins, iron, calcium, and magnesium. Parents have benefited from an education and awareness program organized by medical doctors of Fez University Hospital to highlight the risks associated with lead exposure and explain hygienic and dietetic measures to decrease exposure. Nine months later, we noted a significant decrease in BLLs (from 136.75 ± 32.59 lg/L) to (104.58 ± 32.73 lg/ L) and in lead poisoning prevalence (21.1–7.8 %). Our data are in agreement with those found in the follow-up study on lead exposure in children living in a smelter community in northern Mexico, which noted a decrease in BLLs of
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17 % after 1 year (from 101.2 to 84 lg/L) (Rubio-Andrade et al. 2011). This could be explained by the timeline of relocation of the industrial site, a positive impact of sensitizing (communication, information, education) with normal changes in hygienic habits, and lead distribution from blood to hard tissues.
Conclusion Our study showed a high prevalence of BLLs C100 lg/L (21.1 %) in the exposed population. The relocation of the industrial site associated with corrective and preventive measures has helped to decrease exposure as well as decrease the prevalence of BLLs C100 lg/L to 7.8 %. These results justify prolonging this study by a mass screening program in this region and around lead industrial sources so as to set up corrective and preventive measures. This region needs more studies to address rational mitigation and remediation measures to decrease exposure to safe levels. Finally, follow-up studies should be encouraged to gain better scientific knowledge of metal exposure and the effect of mitigation and remediation measures in contaminated sites. Acknowledgments We thank Amraoui Allal (Director of Health of the Fez-Boulemane region), Asbai Abdellah (delegate of the Ministry of Health of Fez [for the facilities given to perform the study]), and Mr. Sbai (chief doctor of the Health Center of Ain Nokbi Fez) for their generous assistance. We are extremely grateful to all of the families who have participated in the stud and, to laboratory technicians, doctors, and nurses. Finally, we thank all those who participated directly or indirectly in this research study.
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449 Centers for Disease Control and Prevention (2002) Managing elevated blood lead levels among young children: Recommendations from the Advisory Committee on Childhood Lead Poisoning Prevention. CDC, Atlanta Chandramouli K, Steer CD, Ellis M, Emond AM (2009) Effects of early childhood lead exposure on academic performance and behaviour of school age children. Arch Dis Child 94(11): 844–848 De Caluwe JP (2009) Lead poisoning caused by prolonged use of kohl, an underestimated cause in French-speaking countries. J Fr Ophthalmol 32(7):459–463 Dooyema CA, Neri A, Lo YC, Durant J, Dargan PI, Swarthout T et al (2012) Outbreak of fatal childhood lead poisoning related to artisanal gold mining in northwestern Nigeria, 2010. Environ Health Perspect 120(4):601–607 El Kettani S, Khassouani CE, Fennich W, Azzouzi E, Bouchaib A, Mauras Y (2010) Evaluation de l’impre´gnation au plomb d’une population rurale utilisant les eaux use´es a` des fins agricoles dans la re´gion de Settat au Maroc. Environ Risques Sante´ 9(5): 419–427 Falk H (2003) International environmental health for the pediatrician: case study of lead poisoning. Pediatrics 112(1 Pt 2):259–264 Fonds des Nations Unies Pour l’Enfance-Programme des Nations Unies Pour l’Environnement (1997) L’intoxication des enfants par le plomb: information visant a susciter le plaidoyer et l’action. UNICEF, New York, NY. http://www.chem.unep.ch/irptc/Pub lications/leadpoison/lead_fre.pdf. Accessed 11 Sept 2012 Fu H, Boffetta P (1995) Cancer and occupational exposure to inorganic lead compounds: a meta-analysis of published data. Occup Environ Med 52(2):73–81 Garcia Vargas GG, Rubio Andrade M, Del Razo LM, Borja Aburto V, Vera Aguilar E et al (2001) Lead exposure in children living in a smelter community in region Lagunera, Mexico. J Toxicol Environ Health A 62(6):417–429 Garnier R (2005) Toxicity of lead and lead compounds. EMC Toxicol Pathol 2(2):67–88 Haefliger P, Mathieu-Nolf M, Lociciro S, Ndiaye C, Coly M, Diouf A et al (2009) Mass lead intoxication from informal used lead-acid battery recycling in Dakar, Senegal. Environ Health Perspect 117(10):1535–1540 Hellstrom-Lindberg E, Bjorklund A, Karlson-Stiber C, Harper P, Selden AI (2006) Lead poisoning from souvenir earthenware. Int Arch Occup Environ Health 79(2):165–168 Hruba F, Stromberg U, Cerna M, Chen C, Harari F, Harari R et al (2012) Blood cadmium, mercury, and lead in children: an international comparison of cities in six European countries, and China, Ecuador, and Morocco. Environ Int 41:29–34 Institut National de la Sante´ et de la Recherche Me´dicale (1999) Plomb dans l’environnement: Quels risques pour la sante´? INSERM, Paris, p 462 Institute for Public Health Surveillance (1999) Intoxication par le plomb chez l’enfant: Place de la surveillance et implications de l’IVS. INVS, France. http://opac.invs.sante.fr/doc_num.php?explnum_ id=4920 Jacobs DE, Clickner RP, Zhou JY, Viet SM, Marker DA, Rogers JW et al (2002) The prevalence of lead-based paint hazards in U.S. housing. Environ Health Perspect 110(10):A599–A606 Laamech J, Bernard A, Dumont X, Benazzouz B, Lyoussi B (2014) Blood lead, cadmium and mercury among children from urban, industrial and rural areas of Fez Boulemane region (Morocco): relevant factors and early renal effects. Int J Occup Med Environ Health 27(4):641–659 Lanphear BP, Matte TD, Rogers J, Clickner RP, Dietz B, Bornschein RL et al (1998) The contribution of lead-contaminated house dust and residential soil to children’s blood lead levels. A pooled analysis of 12 epidemiologic studies. Environ Res 79(1):51–68
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450 Laraqui CH, Caubet A, Laraqui O, Rahhali AE, Curtes JP, Verger C (2000) Health risks study in a pottery environment in Morocco. Sante´ 10(4):249–254 Lidsky TI, Schneider JS (2003) Lead neurotoxicity in children: basic mechanisms and clinical correlates. Brain 126(Pt 1):5–19 Liu J, Li L, Wang Y, Yan C, Liu X (2013) Impact of low blood lead concentrations on IQ and school performance in Chinese children. PLoS One 8(5):e65230 Needham LL, Barr DB, Caudill SP, Pirkle JL, Turner WE, Osterloh J et al (2005) Concentrations of environmental chemicals associated with neurodevelopmental effects in U.S. population. Neurotoxicology 26(4):531–545 Oulhote Y, Le Bot B, Poupon J, Lucas JP, Mandin C, Etchevers A et al (2011) Identification of sources of lead exposure in French children by lead isotope analysis: a cross-sectional study. Environ Health 10:75 Roels HA (2002) Controlling the risk of nephrotoxicity in men occupationally exposed to inorganic mercury, lead, or cadmium through monitoring biomarkers of exposure. Arch Public Health 60(3):203–215 Rubio-Andrade M, Valdes-Perezgasga F, Alonso J, Rosado JL, Cebrian ME, Garcia-Vargas GG (2011) Follow-up study on lead exposure in children living in a smelter community in northern Mexico. Environ Health 10:66 Sabouraud S, Coppe´re´ B, Rousseau C, Testud F, Pulce C, Tholly F et al (2009) Environmental lead poisoning from lead-glazed earthenware used for storing drinks. Rev Me´d Intern 30(12): 1038–1043 Sainte C, Gille S, Montout P, Droguet C, Coursimault A, Fargette B (2010) Use of kohl, an underestimated cause of childhood lead poisoning—measurements of content with wavelength dispersive X-ray spectrometry analysis and an ICP-OES spectrometer. Ann Toxicol Anal 22(4):181–185 Sanders AP, Miller SK, Nguyen V, Kotch JB, Fry RC (2014) Toxic metal levels in children residing in a smelting craft village in Vietnam: a pilot biomonitoring study. BMC Public Health 14:114 Suplido ML, Ong CN (2000) Lead exposure among small-scale battery recyclers, automobile radiator mechanics, and their children in Manila, the Philippines. Environ Res 82(3):231–238 Surkan PJ, Zhang A, Trachtenberg F, Daniel DB, McKinlay S, Bellinger DC (2007) Neuropsychological function in children
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Arch Environ Contam Toxicol (2015) 68:442–450 with blood lead levels \10 microg/dL. Neurotoxicology 28(6): 1170–1177 van der Kuijp TJ, Huang L, Cherry CR (2013) Health hazards of China’s lead-acid battery industry: a review of its market drivers, production processes, and health impacts. Environ Health 12:61 Wang CL, Chuang HY, Ho CK, Yang CY, Tsai JL, Wu TS et al (2002) Relationship between blood lead concentrations and learning achievement among primary school children in Taiwan. Environ Res 89(1):12–18 White MA (1999) A comparison of inductively coupled plasma mass spectrometry with electrothermal atomic absorption spectrophotometry for the determination of trace elements in blood and urine from non occupationally exposed populations. J Trace Elem Med Biol 13(1–2):93–101 Wilhelm M, Ewers U, Schulz C (2004) Revised and new reference values for some trace elements in blood and urine for human biomonitoring in environmental medicine. Int J Hyg Environ Health 207(1):69–73 World Health Organization (2008) Guidelines for drinking-water quality: Incorporating first addendum, 3rd edn. WHO, Geneva,p 688 World Health Organization (2010a) Childhood lead poisoning. WHO, Geneva, Switzerland. http://www.who.int/ceh/publications/lead guidance.pdf World Health Organization (2010b) Exposure to lead: a major public health concern. WHO, Geneva, Switzerland. http://www.who. int/ipcs/features/lead.pdf. Accessed 4 May 2014 World Health Organization International Agency for Research on Cancer (2006) Inorganic and organic lead compounds. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Vol 87. http://www.inchem.org/documents/iarc/vol87/ volume87.pdf Yazbeck C, Cheymol J, Dandres AM, Barbery-Courcoux AL (2007) Lead exposure in pregnant women and newborns: a screening update. Arch Pediatr 14(1):15–19 Zhang XW, Li YH, Yang LS, Li HR, Wang WY (2010) Determination of five trace elements (Pb, Cd, Se, As and Hg) in human whole blood by temperature-controllable wet digestion and ICPMS technique. Guang Pu Xue Yu Guang Pu Fen Xi 30(7): 1972–1974
Screening for Childhood Lead Poisoning in the Industrial Region of Fez, Morocco S. Bouftini • J. Bahhou • B. Lelievre • J. M. Chao de la Barca • A. Turcant B. Diquet • S. Abourazzak • S. Chaouki • M. Hida • A. Khattabi • C. Nejjari • A. Amarti • S. Achour
•
Received: 12 May 2014 / Accepted: 20 November 2014 / Published online: 16 December 2014 Ó Springer Science+Business Media New York 2014
Abstract The study objectives were to estimate lead poisoning prevalence among children living next to an industrial area, to compare it to that in a control population, and to establish clinical and biological follow-up of the poisoned children. This is a descriptive cross-sectional study including 150 children (exposed and unexposed) performed between January 2012 and April 2013. It was meant to determine blood lead levels (BLLs) in children considered to be an exposed population (EP N 90), living in the industrial area Ain Nokb Fez compared with BLLs of children of other areas belonging to the same city supposed to be unexposed [UP (N = 60)]. A sociodemographic questionnaire was obtained, and a blood lead analysis was performed. Clinical and biological follow-up has been performed of poisoned children. The sample consisted of 90 EP children with an average age of 6.82 ± 3.32 years and male-to-female sex ratio (SR) of 1.5 and 60 UP children with an average age of 6.45 ± 3.29 years and an SR
of 1.2. Among the 150 children recruited, the average of BLLs was 58.21 ± 36 lg/L (18–202.3 lg/L). The average of BLLs in EP children (71 ± 40 lg/L) was statistically greater (p \ 0.0001) than that registered in UP children (38 ± 13 lg/L). All poisoned children belonged to the EP group at a prevalence of 21.1 %. The clinical and biological examinations of poisoned children showed a few perturbations such as anemia, hypocalcaemia, and deficiencies in magnesium and iron. No renal disease or objective neurological disorders were observed. In the follow-up of the children with BLL C100 lg/L (19 cases). BLL monitoring showed a significant decrease in average of blood concentration ranging from 136.75 ± 32.59 to 104.58 ± 32.73 lg/L (p \ 0.0001) and in lead poisoning prevalence (p \ 0.001), which decreased to 7.8 % from 21.1. Our study showed a high prevalence of lead poisoning (21.1 %) in EP children. The relocation of the industrial site associated with corrective and preventive measures has contributed to a decrease of
S. Bouftini (&) J. Bahhou Laboratory of Analysis and Modeling of Continental Ecosystems, Faculty of Science Dhar El Mehraz (FSDM), Universite´ Sidi Mohamed Ben Abdellah (USMBA), Fez, Morocco e-mail: [email protected]
A. Amarti Laboratory of Medical Analysis, Faculty of Medicine, University Hospital and Medical Centre of Biomedical and Translational Research, Universite´ Sidi Mohamed Ben Abdellah (USMBA), Fez, Morocco
B. Lelievre J. M. C. de la Barca A. Turcant B. Diquet Pharmacology-Toxicology Laboratory, University Hospital of Angers, Angers, France S. Abourazzak S. Chaouki M. Hida Pediatric Department, Hassan II University Hospital of Fez, Fez, Morocco A. Khattabi C. Nejjari Laboratory of Epidemiology, Clinical Research and Community Health, Faculty of Medicine and Pharmacy, Universite´ Sidi Mohamed Ben Abdellah (USMBA), Fez, Morocco
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S. Achour Laboratory of Medical Analysis, Toxicology Unit, Faculty of Medicine, University Hospital of Fez and Medical Centre of Biomedical and Translational Research, Universite´ Sidi Mohamed Ben Abdellah (USMBA), Fez, Morocco
Arch Environ Contam Toxicol (2015) 68:442–450
exposure and lead poisoning prevalence in the aforementioned population.
Childhood lead poisoning is a global public health problem that has been highlighted in developed countries since the 1980s, but it is underestimated in developing countries (Falk 2003; UNICEF-PNUE 1997). Lead is of growing concern because of its known toxicity even at low levels (Bellinger 2008). The World Health Organization (WHO) estimates that lead poisoning causes 0.6 % of the global burden of disease and contributes to approximately 600,000 cases of intellectual disability in children annually (WHO 2010b). In Morocco, in addition to known sources of lead exposure, there are other specific causes such as the use of glazed utensils, products of traditional medicine such as kohl, and the presence of industrial and handicraft agglomerates exposing citizens to the risk of lead exposure and poisoning. This country is at high risk with regard to its important artisanal and traditional activities based primarily on metallurgy, pottery in poor working conditions, and a lack of respect for the regulations concerning specific measures prevention and health rules applicable to the institutions. However, few studies of lead human exposure in an industrial environment have been published (Laraqui et al. 2000). Young children are particularly exposed to lead because of behavioral factors such as frequent hand-to-mouth activities, biological factors including greater gastrointestinal absorption, and the development of their nervous system (Bellinger 2004; Oulhote et al. 2011; Lidsky and Schneider 2003). Emerging evidence has also suggested that even children with blood lead concentrations \100 lg/L are at significant risk to decreased cognitive development and functioning including intelligence quotient deficits (Canfield et al. 2003; Surkan et al. 2007; Liu et al. 2013) and poor academic performance (Chandramouli et al. 2009; Wang et al. 2002). Other studies have shown that environmental and occupational lead exposures increase cancer risk, particularly lung and stomach cancers (Fu and Boffetta 1995; World Health Organization International Agency for Research on Cancer 2006). Lead pollution is a threat to health, especially for children who live in the surrounding communities of artisanal and industrial sites, such as mineral smelters and refineries, where exposure to heavy metals through inhalation and ingestion of contaminated soil and dust is possible (UNICEF-PNUE 1997; WHO 2010b). In 2010, a Nigerian study of children living in villages where artisanal gold mining was practiced found that 97 % had BLLs [450 lg/L (Dooyema et al. 2012). To our knowledge, no study concerning childhood lead poisoning in an industrial environment in Morocco has been
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performed so far. In this context, we chose for our study the industrial site of Ain Nokbi, which is located in an urban agglomeration in the city of Fez. It is known for its activities based essentially on pottery, tanning, brassware, ceramics, and mosaic. It contains foundries for the manufacture of raw materials (enamel) based on a mixture containing [74 % of lead, which is extracted from old pipes brought to a temperature of 1,200 °C. This site also contains traditional ovens (168 traditional ones) reserved for baking pottery that emit emanations whose lead content is approximately 212.87 lg/m3 (Laraqui et al. 2000) (Fig. 1). This value exceeds the maximum concentration allowed in the workplace, which is 150 lg/m3 (Institute for Public Health Surveillance 1999); this can be explained by the escape of lead salts contained in galena when backing pottery. The objectives of the study were to evaluate lead exposure and estimate lead poisoning prevalence among children living near the study area to compare them with those of a control population of children who do not live in the abovementioned region and, finally, to establish clinical and biological follow-up for the children having BLLs C100 lg/L.
Materials and Methods Ethics Statement This study was approved by the Ethical Committee of the University Hospital Hassan II (Morocco). Written informed consent was obtained from all of the participants’ parents or guardians after they had been fully informed about the study details. A questionnaire was devised for the children. The Study Site Fez is located in the region of Fez-Boulemane in central northern Morocco with a population of 1,050,000 inhabitants. It is the capital of artisanal and industrial activities. Since the 1970s, the artisanal place, Ain Nokbi, was implanted in the Fez old medina; it employs approximately 250 craftsmen (potters and tanners), and it is an essential catalyst for social and economic development of the region. Agglomerations of new habitats (built after 1985) are located around the industrial site. The latter generates environmental pollution resulting from industrial discharges and craft. A few months before the beginning of our study, this site was moved to a nearby place (Fig. 2). Study Population This is a descriptive cross-sectional study performed between January 2012 and April 2013 on 150 children
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Fig. 1 Polluting fumes and toxic emissions from the traditional ovens in the industrial area Ain Nokbi (EP)
(exposed and unexposed) whose ages ranged from 6 months to 12 years. It was meant to determine BLLs in children considered to be an exposed population [EP (N = 90)] who live in the industrial area Ain Nokbi Fez compared with BLLs of children of other areas of the same city considered to be unexposed [UP (N = 60)]. The EP children were recruited at the health center located in the area at risk and UP children at the Fez University Hospital. They were selected in a random manner during pediatric consultation and based on the address of their habitat. Exclusion criteria included severe diseases that involve vital prognosis or antecedent of recent blood transfusion. Parents or guardians of each participating child were asked to complete a sociodemographic questionnaire including queries on age, parental occupation, smoking, type of housing, type of water consumption, use of kohl, and use of lead-based utensils. Dosage and Interpretation of Blood Lead Levels Five milligrams of venous blood sample was collected from each child in trace-metal free ethylene diamine tetraacetic acid-vacutainer tubes at the time of recruitment in the health centre and in the hospital university. When collecting the samples, precautionary measures were taken to exclude the possibility of sample contamination from lead on the skin. The lead analyses were performed in the Toxicology and Pharmacology Laboratory at the University Hospital of Angers, France, using inductively coupled plasma-mass spectrometry (ICP–MS) with the quantization ion [Pb (m/
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z = 208)] using rhenium as an internal standard [Re (m/ z = 185)]. The blood is initially diluted 1/2 in a solution of 0.2 % Triton in suprapur HNO3 0.5 % before final dilution (1/ 20) as calibrants. This technique is considered to be sensitive and reliable for the determination of such metals (White 1999; Zhang et al. 2010). The limit of quantification is 12.5 lg/L, and the limit of detection is approximately 4 lg/L. According to the classification given by the Centers of Disease Control and Prevention (CDC 2005), children of our study were classified in accordance with their BLLs as follows: class I = BLL \100 lg/L; class IIa = BLL 100 to B149 lg/L; and class IIb = BLL 150 to B249 lg/L). Only children with BLL C100 lg/L will benefit from a clinical examinations which will be performed by a group of medical specialists (neurologists, pediatricians, pediatric endocrinologists, and toxicologists), biological tests (complete blood count, renal and hepatic function, and determination of iron, calcium, and magnesium), and medical follow-up. Parents of participants will also be invited to attend awareness sessions concerning the hygiene advice to follow to decrease lead exposure. BLL control as well as clinical and biological examinations will be performed 9 months after the first screening to check the evolution of exposure in children who had BLLs C100 lg/L. Determination of Lead Content in Water As a complement to the study, water samples were taken after one-night stagnation from the households of the children with BLLs C100 lg/L. This allowed evaluation of the
Arch Environ Contam Toxicol (2015) 68:442–450
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Fig. 2 Location of Ain Nokbi industrial sites in the city of Fez, Morocco
maximum exposure to lead from drinking water. The water samples were collected in precleaned polyethylene bottles; the samples were stabilized with 1 mL of nitric acid; and blanks were taken. The analytical technology used was inductively coupled plasma-atomic emission spectrometry (ICP–AES). The determination of lead in the air was not performed due to the lack of technical means to do so. Statistic Analysis Statistical analysis was performed with SPSS software (Statistical Product and Services Solutions, version 17, SPSS Inc, Chicago, IL). Comparison of averages was performed by way of classical parametric testing depending on the nature of the variables to be compared as well as nonparametric tests in case of some weaknesses or strengths. To test significance evolution of BLL in terms of prevalence and concentration means, statistical tests for matched series were used. A p value \0.05 was considered significant.
Results Sample Characteristics The sample consisted of 90 EP children with an average age of 6.82 ± 3.32 years and male-to-female (M/F) SR of 1.5 and 60 UP children with an average age of 6.45 ± 3.29 years an M/F SR of 1.2. As listed in Table 1, the two populations were comparable regarding various sociodemographic parameters including exposure to passive smoke inhalation. According to the questionnaire, pica behavior was noted in 50 % of both EP and UE children. The average age of living habitats was 28.44 ± 6.98 years for EP children and 24.4 ± 9.93 years for UP children. The existence of lead pipes was reported at 2 % for EP and at 2 % for UP children. Lead Exposure Among the 150 children recruited in the survey, the average of BLLs was 58.21 ± 36 lg/L in the population with
123
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Table 1 General characteristics of EP and UP study participants (N = 150) Characteristics
EP
UP
p
N = 90
%
N = 60
%
0–6
35
38.9
25
41.6
6–12 Sex
55
61.1
35
58.3
Male
54
60
33
55
Female
36
40
27
45
Classes by age (year) 0.05
0.06
Pica Yes
49
54.4
28
46.6
No
41
45.5
32
53.3
Yes
42
46.6
35
58.3
No
47
52.2
25
41.6
0.22
Use of glazed utensils 0.31
Parents’ function at risk Yes
33
36.6
16
26.6
No
57
63.3
44
73.3
0.14
Passive smoke inhalation Yes
54
60
33
55
0.33
No Use of kohl (mothers and/or children)
36 90
40 100
27 60
45 100
-
Consumption of tap water
90
100
60
100
-
For use of glazed ustensils N(UP): 89
extremes ranging from 18 to 202.3 lg/L, and the median value of BLLs was 48 lg/L. In both populations, BLLs were greater in male than in female children (p \ 0.001).
Fig. 3 Distribution of BLLs of the two study populations (EP and UP) in terms of the exposure. Study exposed, unexposed (N = 150)
Blood lead concentration was not statistically significant with respect to age. The average of BLLs of EP (71.43 ± 40 lg/L) children was statistically greater (p \ 0.0001) than that of UP (38.38 ± 13 lg/L) children. The distribution of blood lead according to exposure is illustrated in Fig. 3. Among 90 EP children, 71 (78.88 %) had BLLs \100 lg/L (class I) with an average of 53.96 ± 17.35 lg/ L, a minimum of 18.77 lg/L, and a maximum of 99.27 lg/ L. The 19 (21.11 %) children that remained had BLLs C100 lg/L with an average of 136.75 ± 32.59 lg/L, a minimum of 103.2 lg/L, and a maximum of 202.3 lg/L. Of those 19 children, 6 had BLLs between 100 and 149 lg/ L (class IIa), and 13 had BLLs between 150 and 249 lg/L (class IIb). No patient had BLL [ 250 lg/L (class III). The prevalence of lead poisoning in this EP is 21.1 % (95 % CI 20.21–21.99 %). For all 60 UP children, BLLs did not reach 100 lg/L, and thus they all belonged to class I (B100 lg/L) with an average of 38.38 ± 13 lg/L, a minimum of 18.22 lg/L, and a maximum of 90.05 lg/L. The average BLL of E children was relatively greater than that of UP children regardless of the age of habitats, the parents’ jobs at risk, the nature of water consumption, the use of traditional utensils or kohl, and the presence of pica behavior or passive smoke inhalation (Table 2). Consumption of tap water was found among 100 % of the study population. In addition, water samples analyzed from children with BLLs C 100 lg/L did not show lead levels [10 lg/L, thus meeting drinking water standards set by WHO (2008).
40
Unexposed Population
Exposed Population
35 30
Effective
25 20 15 10
[180 - 200
[200 - 220
[120 - 140
[160 - 180
[100 - 120
[140 - 160
[80 - 100
[60 - 80
[40 - 60
[
[0 - 19
[
[
123
[
[
Classes of BLLs
[
[
[
[
[
[
0
[20 - 40
5
Arch Environ Contam Toxicol (2015) 68:442–450
447
Table 2 Distributions of average BLLs according to exposure factors in EP and UP children (N = 150)
Table 3 Monitoring clinical, biological, and toxicological problems presented by children with BLLs 100 lg/L (N = 19)
Exosure factors
BLL groups and problems
EP No.
UP Mean of BLLs (±SD)
No.
p
After 9 months
No.
%
No.
%
Class I (BLL B100 lg/L)
0
0
12
63.2
Class II a (100B BLL B149 lg/L)
6
31.5
7
36.8
Class II b (BLL 150 to B249 lg/L)
13
68.5
0
0
Mean of BLLs (±SD)
90
71 ± 40
60
38 ± 13
\0.0001
\6
35
71 – 43.8
26
42.8 – 14.3
\0.001
[6
55
71.4 – 37.4
34
35 – 11.3
Total
At the time of screening
Age (year) \0.0001
Sex
BLL group
Clinical and biological perturbations
Male
57
77.3 ± 43.7
27
43.3 ± 14.9
\0.001
Female
33
61.2 ± 30.9
33
32.3 ± 10.8
\0.001
Pica
Clinical signs Neurological disorders
25
54.34
21
45.65
Gastrointestinal disorders
9
90
1
10
Yes
49
72.9 – 38.5
28
38.2 – 11
0.0001
Locomotor disorders
6
54.54
5
45.45
No
41
69.6 – 42.2
32
38.5 – 14.9
0.001
Other signs
16
53.33
14
46.66
Anemia
7
77.77
2
22.22
Hypocalcemia
8
72.72
3
27.27
Iron deficiency Magnesium deficiency
4 18
66.66 51.42
2 17
33.33 48.57
Parents’ function at risk
Biological signs
Yes
33
71 – 36.5
16
38.8 – 11.3
0.0001
No
57
72.8 – 46.3
44
38.2 – 13.9
\0.0002
Use of glazed utensils Yes 42 72.9 – 40.9
35
39 – 15.3
70.5 – 39.6
25
37.8 – 11.5
No
47
0.002 0.0001
BLLs blood lead levels
BLLs blood lead levels
Clinical and Biological Aspects The results of clinical and biological tests are listed in Table 3. Clinical examinations highlighted essentially neurological disorders in 25 cases including microcephaly (3 cases), epilepsy (1 case), headache (5 cases), restlessness (6 cases), language and walking delays (3 cases), and lack of concentration (7 cases). Digestive disorders were present in 9 children as oral and dental disorders, e.g., Burton’s lines (3 cases), abdominal pain (3 cases), nausea (2 cases), constipation (1 case), locomotor disorders represented by growth retardation (4 cases), and muscle and joint pain (2 cases). The results of the biological examinations showed the existence of hypochromic microcytic anemia (7 cases) and hypocalcaemia (8 cases). The decrease in serum ferritin values was found in four children, and no renal or liver failures were detected. However, 95 % of poisoned children had magnesium deficiency. Follow-Up of Children with BLLs C100 lg/L In the follow-up of these children (19 cases), BLL monitoring and biological and clinical examinations were performed 9 months after the first screening and showed a significant decrease in the average of blood lead concentration from 136.75 ± 32.59 to 104.58 ± 32.73 lg/L (p \ 0.0001) and in the prevalence (p \ 0.001) of lead poisoning from 21.1 % (95 % CI 20.21–21.99 %) to 7.8 %
(95 % CI 7.22–8.38 %). Among the 19 children, 12 belonging to class II became class I. Seven of them belonging to class IIb became class IIa (Table 3). In addition, clinicobiological monitoring showed a decrease in the number of clinical disorders (abdominal pain, constipation, and pallor) and biological disturbances (anemia and hypocalcaemia) (Table 3).
Discussion In this study, average BLLs in EP (71.43 ± 40 lg/L) children was significantly greater compared with that recorded in UP (38.38 ± 13 lg/L) children. The same result was observed in a study performed among children living in the immediate vicinity of battery shops where EP children had average BLLs that were significantly greater (498.8 ± 14.95 lg/L) compared with that of EP children (99.2 ± 1.90 lg/L) (Suplido and Ong 2000). Compared with international data, the average BLL of EP children (71.43 ± 40 lg/L) was greater than that recorded in children living near an industrial site in the same region of study (48.23 lg/L) (Laamech et al. 2014), but it was less important than that recorded in exposed children living in the immediate vicinity of battery shop who had significantly higher mean BLLs (498.8 lg/L) (Suplido and Ong 2000). The maximum BLL recorded in this population was 202.3 lg/L, which is significantly lower than that recorded in children living near the gold-mining
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area in the northwest of Nigeria, where it exceeds 450 lg/L (Dooyema et al. 2012). The average BLL of UP children was 38.38 ± 13 lg/L, which is greater than the average value recorded in Swedish children (14 lg/L) and children in Ecuador (31.7 lg/L) (Hruba et al. 2012) suggesting that exposures are still occurring. Sources are not apparently linked to pica, the use of glazed pottery, or the use of cosmetics products, but they still must be identified. In our survey, the BLL average found in males was significantly greater than that in females. Similar findings have been reported by other investigators (Becker et al. 2002; Needham et al. 2005; Alimonti et al. 2005 and Wilhelm et al. 2004). This can be explained by the turbulent and restless behavior of boys, who frequent a more external environment. In accordance with the Vietnam Study (Sanders et al. 2014), the effect of age was not observed between our two age groups. The prevalence of abnormal BLLs (C100 lg/L) was significantly greater (p \ 0.0001) in EP children (21.11 %). This value is greater compared with that of registered among children in Settat city (14.3 %) (El Kettani et al. 2010). A similar study concerning the exposure of children residing in a smelting craft village in Vietnam recorded prevalence rates of 80 %, which is largely exceeds that recorded by our study (Sanders et al. 2014). In our study, the exposure factors studied (age of habitats, parents’ jobs at risk, water consumption, use of traditional utensils or kohl, and presence of pica behavior or passive smoke inhalation) did not influence lead exposure in EP children. Atmospheric pollution remains a major factor that seems to be responsible for the exposure to lead in children in this area who can usually absorb several tens of milligrams of dust per day (INSERM 1999; Lanphear et al. (1998). Many studies in this direction have shown that the illegal use of lead has impacts on the environment and on the health of children in several countries (Dooyema et al. 2012; Kuijp et al. 2013; Suplido and Ong 2000; Garcia Vargas et al. 2001). In the same direction, a Senegalese study, performed after the death of 18 children living on the outskirts of the city of Dakar, recorded severe lead poisoning from recycling of lead batteries (Haefliger et al. 2009). Moreover, the use of kohl, which is a cosmetic product for the eyes, is widely disseminated in the Maghreb countries and remains an ancestral and cultural practice among women and children. It is known for its medicinal, pharmacological, and prophylactic properties. Even if kohl contains lead and is used by 100 % of the study population, we cannot conclude its contribution to lead exposure on the basis of this study, although many studies have established a correlation between the use of kohl and abnormally high BLLs (Sainte et al. 2010; Al-Ashban et al. 2004; De Caluwe 2009).
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In addition to kohl, the use of glazed utensils, in particular the Moroccan tagine, can be also a factor influencing BLLs positively. In fact, several cases of lead poisoning have been identified as a result of the use of artisanal ceramics (Hellstrom-Lindberg et al. 2006; Bossi et al. 1991) and artisanal glazed potteries, especially tagine (Hellstrom-Lindberg et al. 2006; Sabouraud et al. 2009; Yazbeck et al. 2007). In France and the United States in nonindustrial environments, lead-based paint is considered to be the primary source of lead in children with BLLs C100 lg/L, especially for children who live in older homes (Jacobs et al. 2002). This factor has not been found in this study because for the UP children, their habitations were new, so they do not have lead-based paint; for the EP children, the walls of their habitations were uniquely covered with lime. The lead level in drinking water is also an aggravating BLLs factor, in our study, analysis of water consumption from households of children with BLL C100 lg/L, has shown normal rates, thus eliminating water origin in exposure. The clinical and biological examinations showed a few perturbations such as anemia, hypocalcaemia, and magnesium and iron deficiencies. These perturbations may be related to lead exposure because they may result from hygienic and dietary habits because the socioeconomic and cultural level of the population is low. The cases of microcephaly, epilepsy, or the appearance of Burton’s lines cannot be related to the BLLs measured in this study because BLLs are not at all representative of past exposures; however, but they can be linked to much greater past exposures. In our study, no renal disease or objective neurological disorders such as encephalopathy and neuropathy were observed in children having BLLs C100 lg/L. Indeed, renal disease was not observed in exposed workers who have BLLs \400 lg/L, and for objective neurological disorders, BLLs must be [500 lg/L in children (Garnier 2005; Roels 2002; WHO 2010a). No chelation therapy was prescribed for our patients because BLLs records did not exceed 450 lg/L (CDC 2002; Garnier 2005). However, children with BLLs C100 lg/L received prescription medication including vitamins, iron, calcium, and magnesium. Parents have benefited from an education and awareness program organized by medical doctors of Fez University Hospital to highlight the risks associated with lead exposure and explain hygienic and dietetic measures to decrease exposure. Nine months later, we noted a significant decrease in BLLs (from 136.75 ± 32.59 lg/L) to (104.58 ± 32.73 lg/ L) and in lead poisoning prevalence (21.1–7.8 %). Our data are in agreement with those found in the follow-up study on lead exposure in children living in a smelter community in northern Mexico, which noted a decrease in BLLs of
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17 % after 1 year (from 101.2 to 84 lg/L) (Rubio-Andrade et al. 2011). This could be explained by the timeline of relocation of the industrial site, a positive impact of sensitizing (communication, information, education) with normal changes in hygienic habits, and lead distribution from blood to hard tissues.
Conclusion Our study showed a high prevalence of BLLs C100 lg/L (21.1 %) in the exposed population. The relocation of the industrial site associated with corrective and preventive measures has helped to decrease exposure as well as decrease the prevalence of BLLs C100 lg/L to 7.8 %. These results justify prolonging this study by a mass screening program in this region and around lead industrial sources so as to set up corrective and preventive measures. This region needs more studies to address rational mitigation and remediation measures to decrease exposure to safe levels. Finally, follow-up studies should be encouraged to gain better scientific knowledge of metal exposure and the effect of mitigation and remediation measures in contaminated sites. Acknowledgments We thank Amraoui Allal (Director of Health of the Fez-Boulemane region), Asbai Abdellah (delegate of the Ministry of Health of Fez [for the facilities given to perform the study]), and Mr. Sbai (chief doctor of the Health Center of Ain Nokbi Fez) for their generous assistance. We are extremely grateful to all of the families who have participated in the stud and, to laboratory technicians, doctors, and nurses. Finally, we thank all those who participated directly or indirectly in this research study.
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