http://informahealthcare.com/jmf ISSN: 1476-7058 (print), 1476-4954 (electronic) J Matern Fetal Neonatal Med, Early Online: 1–8 ! 2015 Informa UK Ltd. DOI: 10.3109/14767058.2015.1026255

ORIGINAL ARTICLE

Maternal risk factors associated with lead, mercury and cadmium levels in umbilical cord blood, breast milk and newborn hair

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Arzu Dursun1, Kadriye Yurdakok2, Songul S. Yalcin2, Gulsevin Tekinalp3, Osman Aykut4, Gunnur Orhan4, and Goksel Koc Morgil4 1

Unit of Neonatology, Department of Pediatrics, Dr. Sami Ulus Maternity and Children’s Health and Diseases Training and Research Hospital, Ankara, Turkey, 2Unit of Social Pediatrics, 3Unit of Neonatology, Department of Pediatrics, Hacettepe University Faculty of Medicine, Ankara, Turkey, and 4Analytic Toxicology Laboratory, Refik Saydam National Public Health Agency, Ankara, Turkey Abstract

Keywords

Objective: Lead (Pb), mercury (Hg) and cadmium (Cd) are environmental pollutants that are wide spread throughout the world. The present study aimed to investigate the level of exposure to Pb, Hg and Cd during the prenatal period, and the possible routes of maternal exposure to these toxic heavy metals. Participants: The study included 123 mothers and their newborns. Umbilical cord blood samples were collected immediately after delivery, and breast milk and newborn hair samples were collected between postpartum d 3 and 10. Results: Among the 121 cord blood samples that were analyzed, Pb was present in 120 (99.2%) and the mean level was 1.66 ± 1.60 mg dL1 (range:5detection limit–12.50 mg dL1), whereas Hg was noted in only 2 (1.7%) (15.74 and 33.20 mgL1) and Cd was detected in 24 (19.8%) (range: 5detection limit–6.71 mgL1). The level of Pb in cord blood was 2 mg dL1 in 29% of the samples. Pb, Hg and Cd were detectable in all the newborn hair samples. Discussion: Among the 107 breast milk samples analyzed, 89 (83.2%) had a detectable level of Pb and the mean level was 14.56 ± 12.13 mgL1. Detection rate of Cd in breast milk was higher in women who resided near to city waste disposal site. Detection rate of Cd in cord blood was significantly higher in the women who consumed 2 servings of fish weekly. Maternal exposure to environmental tobacco smoke (ETS) resulted in elevated levels of Pb and Cd in newborn hair samples. Conclusion: Most of the study samples had detectable levels of Pb, Hg and Cd, indicating that there was long-term maternal exposure prior to and during pregnancy, and a considerable number of the cord and breast milk samples had levels that exceeded the present accepted safety level.

Breast milk, cadmium, cord blood, hair, lead, mercury, newborn

Introduction Almost all children are exposed to environmental pollutants beginning with the intrauterine period. Early exposure to chemicals occurs either prior to conception via parental exposure, during pregnancy via the placental barrier or after birth via breast milk or directly from the environment [1,2]. Toxic heavy metals are fat soluble, non-ionizing low molecular weight (51000 Da) chemicals that can quickly cross the placental barrier, depending on blood flow, metabolism, thickness, surface area, lipid and protein content of the membranes and the carrier systems of the placenta, which are variable during pregnancy [3]. Human fetuses and infants are susceptible to heavy metal toxicity due to the rapid growth Address for correspondence: Arzu Dursun, Unit of Neonatology, Department of Pediatrics, Dr. Sami Ulus Maternity and Children’s Health and Diseases Training and Research Hospital, Ankara, Turkey. Fax: +90 312 3170353. E-mail: [email protected]

History Received 19 January 2015 Revised 22 February 2015 Accepted 3 March 2015 Published online 2 April 2015

and development of organs and tissues, especially the central nervous system [4]. Lead (Pb), mercury (Hg) and cadmium (Cd) are wellknown toxic heavy metals that can negatively affect neurodevelopmental and the endocrine system’s role in fetal development. Intrauterine Pb, Hg, Cd exposure is associated with abortion, intrauterine death, cerebral palsy, low birth weight, cognitive dysfunction, low IQ, learning disabilities and hearing and visual dysfunction, and may have some teratogenic effects, especially at high levels of exposure [5,6]; however, these metals are potentially hematotoxic, neurotoxic and nephrotoxic—even at very low levels of exposure [4]. Biological samples are used for biomonitoring of intrauterine exposure to these toxic chemicals; the most widely used are umbilical cord blood and breast milk, and less commonly infant hair. Cord blood has been used in many studies as an index of prenatal toxic chemical exposure. The presence of toxic chemicals in cord blood is indicative of fetal

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exposure, which in turn is associated with a variety of diseases and disorders later in life [4,6]. The level of toxic metals in infant hair may be indicative of long-term intrauterine exposure, whereas the level in breast milk is indicative of maternal body burden and the potential for infant lactational exposure [5]. Heavy metal levels in umbilical cord blood, breast milk and infant hair should be monitored at certain intervals and the possible routes of exposure should be evaluated. By this way, preventive measures could be planned. As such, the present study aimed to measure the level of maternal and fetal exposure to three heavy metals, based on three biological samples (cord blood, breast milk and newborn hair), and to determine the possible routes of exposure.

Materials and methods This cross-sectional study was performed between December _ 2006 and November 2007 at Hacettepe University, Ihsan Dog˘ramacı Children’s Hospital, Ankara, Turkey. The study protocol was approved by the Hacettepe University, School of Medicine Institutional Review Board (LUT 0657, 2006). Mothers were fully informed about the study and those who participated provided written informed consent prior to giving birth. Exclusion criteria were maternal age 518 years, pregnancy due to in vitro fertilization or intracytoplasmic sperm injection, gestational age534 weeks and441 weeks and fetal death. Umbilical cord blood, newborn hair and breast milk samples were obtained from 123 healthy mothers with a negative history of occupational exposure to Pb, Hg and Cd who had been living in Ankara for 5 years before becoming pregnant, and their newborns. Participants and samplings This study included only healthy pregnant women. Exclusion criteria were as women with any chronic disease like hypertension, diabetes mellitus, heart disease, rheumatic diseases or pregnant women with any pregnancy complication like preeclampsia, eclampsia, pregnancy-induced diabetes mellitus. In total, 174 eligible healthy pregnant women agreed to participate in the study, of which 51 and their newborns were excluded due to incomplete study questionnaire, improper collection of biological samples or dropping out. In all, 123 of the 174 healthy mother–newborn pairs (83.7%) were included in the study. Pb, Hg and Cd levels were measured in 121 cord blood samples, 107 breast milk samples and 112 newborn hair samples, as some of the collected samples were insufficient for analysis. One hundred and seven participants had all three samples (cord blood, breast milk and newborn hair). Questionnaire The mothers were interviewed by a medical doctor (A.D.) in the antenatal unit and a 61-item questionnaire was used to assess personal, environmental and nutritional toxic heavy metal exposure risk factors. The questionnaire was used to collect data on demographic, socioeconomic and general health status (such as anemia during pregnancy, chronic diseases, drug use during pregnancy) variables, as well as on routes of toxic heavy metal exposure during the period

J Matern Fetal Neonatal Med, Early Online: 1–8

preceding pregnancy and during pregnancy (such as the use of lead-glazed tableware and ceramics, lead pipes for plumbing in the home, type of home heating system, fish consumption, dental amalgam fillings, battery exposure, environmental tobacco smoke [ETS], residing near to a city waste disposal site). Measurement of Pb, Hg and Cd The level of Pb, Hg and Cd in cord blood, breast milk and newborn hair was measured at Refik Saydam National Public Health Agency, Ankara, Turkey. Samples were analyzed via inductively coupled plasma mass spectrometry (ICP-MS) using an Agilent 7500a instrument (Agilent, Santa Clara, CA). The lowest limit of quantitation (LLOQ) in cord blood and breast milk was 0.03 mg L1 for Pb and 0.02 mg L1 for Hg and Cd. The LLOQ in newborn hair was 0.00003 mgg1 for Pb and 0.00002 mgg1 for both Hg and Cd. Umbilical cord blood samples were obtained at the time of delivery. Cord blood samples (5–10 mL) collected in tubes containing EDTA were frozen immediately after collection and kept frozen (20  C) until analyzed. Breast milk samples were collected into clean polyethylene tubes via manual pumping 2–10 d after delivery. All the breast milk samples were frozen immediately after collection and kept frozen (20  C) until analyzed. Newborn hair samples were obtained within 48 h of delivery. About 3 g of hair was cut from the nape of the neck close to the scalp, as 1.5–2-cm long strands. To avoid contamination clean stainless steel scissors and disposable vinyl examination gloves were used to cut the hair samples. Hair samples were placed into polyethylene bags provided by the laboratory performing the analysis. In order to minimize the polyatomic interference, 65% nitric acid (concentrated grade [Merck 452]), reagent water equivalent to ASTM type 1 (ASTM D 1193; N18 m cm resistivity), 0.5% (v/v) nitric acid, a tuning solution (for sensitivity tuning: 10 mg L1 for each of the metals Li, Y and Tl in 1% HNO3) and a single-element standard stock solution for Pb and Cd (1000 ppm) were used. Next, 1 g cord blood samples, 1 g breast milk samples and 0.2 g newborn hair samples were accurately weighed, placed in a dry XP1500 vessel and then 5 mL of HNO3 and 5 mL of distilled water were added. This mixture was placed in a microwave oven for digestion. Following digestion, the samples were diluted with 25 mL of distilled water. The standard working solutions and the biological samples in the polyethylene tubes were placed in an ICP-MS automatic sequencer to measure the concentration of Pb, Hg and Cd (Yokogawa Analytical Systems, Inc., Hachioji-Shi, Tokyo, Japan) [7]. The level of Pb in cord blood indicating toxicity was accepted as 2 mg dL1, according to Gilbert and Wiess [8], and the level of Hg in cord blood indicative of toxicity was accepted as 5.8 mg L1[9]. There is no consensus on the toxic level of Pb, Hg and Cd in breast milk and newborn hair, or for Cd in cord blood. Statistical analysis Data were analyzed using SPSS v.13.0 for Windows (SPSS Inc, Chicago, IL). The normality of data distribution was determined using the Kolmogorov–Smirnov test.

Maternal risk factors associated with Pb, Hg, and Cd levels in newborn

DOI: 10.3109/14767058.2015.1026255

The independent sample t-test was used for continuous variables with normal distribution. For variables with skewed distribution the Mann–Whitney U-test was used for comparison. To compare proportions the 2 or Fisher’s exact test was used, when applicable. The correlations between the level of same heavy metal in umbilical cord blood, breast milk and newborn hair, and the correlations between the levels of heavy metals in the same biologic material were examined. The level of statistical significance was set at p  0.05.

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Results Characteristics of the mothers and newborns are shown in Table 1. Mean age of the mothers was 30.6 ± 4.9 years, and 40% were multiparous (Table 1). Mean gestational age was 38.6 ± 1.2 weeks. The prematurity rate was 6.5%, and mean birth weight and length were 3310 ± 422 g and 48.6 ± 4.4 cm, respectively. Physical examination of all the newborns was normal. The mean Pb level in umbilical cord blood, breast milk and newborn hair samples was 1.66 ± 1.60 mg dL1, 14.56 ± 12.13 mgL1 and 2.72 ± 1.44 mgg1, respectively (Table 2). The median Hg level in breast milk was 1.36 mgL1 (range: 5Detection limit [Dl]–11.52 mgL1; 25th–75th percentiles: 5Dl–7.28 mgL1) and the mean Hg level in newborn hair was 0.23 ± 0.23 mgg1. Hg was detected in only two cord blood samples (33.20 and 15.74 mgL1). The mean Cd level in newborn hair was 0.07 ± 0.04 mgg1 (range: 0.01–0.22 mgg1). Cd was detected in 24 (19.8%) of the 121 cord blood samples and 10 (9.3%) of the 107 breast milk samples. The Pb level in umbilical cord blood was higher than the safe level in 29% (n ¼ 35) of the cases, versus 1.7% (n ¼ 2) for Hg. There was only one case (0.8%) with an umbilical cord Pb level 410 mg dL1 (12.50 mg dL1). The relationship between demographic characteristics, routes of exposure and level of Pb, Hg and Cd are given in Table 1. Demographic findings of the newborns and the mothers. Mother

Mean ± SD

Range

Age (year) Gravidity Parity Interval between two pregnancies (month) Maternal education Primary school High school University Business Employed Unemployed Newborns Weight (g) Length (cm) Head circumference (cm) Gestation (wk)

30.5 ± 4.9 2.2 ± 1.4 1.7 ± 0.8 54.4 ± 38.9

21–46 1–10 1–5 11–199

Premature birth Mode of delivery Spontaneous vaginal delivery Cesarean Section Gender Female Male Total

n (%) 24 (19.5) 33 (26.8) 66 (53.7) 65 (53) 58 (47) Mean ± SD 3310 ± 422 49.8 ± 1.3 34.8 ± 1.2 38.6 ± 1.2 n (%) 8 (6.5) 31 (25) 92 (75) 59 (48) 64 (52) 123 (100)

Range 2400–4350 47–53 32–38 345/7–41

3

Table 3. Maternal anthropometry, level of education, interval between two pregnancies and parity, gestational age, neonatal anthropometry, gender and mode of delivery were not affected by Pb or Hg levels in the biological samples. The mean Pb level in cord blood was higher in the mothers aged 435 years than in those aged 535 years (2.20 ± 2.34 mg dL1 versus 1.52 ± 1.31 mg dL1, p50.05). The level of Pb and Hg in the newborn hair of infants born to mothers that were unemployed was higher than in the newborn hair of infants born to mothers that were employed (Pb: 3.15 ± 1.62 versus 2.35 ± 1.18 mgg1, p ¼ 0.003; Hg: 0.29 ± 0.27 versus 0.19 ± 0.20 mgg1, p50.05). Infants of mothers with a history of exposure to ETS during childhood had a higher level of Pb in newborn hair (2.97 ± 1.69 versus 2.32 ± 0.91 mgg1, p50.05). The mean Cd level in newborn hair was significantly higher in those whose mothers were exposed to ETS during pregnancy (Table 3). Mothers who were exposed to insecticide during pregnancy had a higher level of Pb in breast milk than those not exposed to insecticide (17.03 ± 11.8 versus 12.31 ± 12.05 mgL1, p50.05). The level of Pb in the biological samples did not differ according to maternal battery exposure, maternal use of lead-glazed ceramics, lead in home plumbing and type of home heating system. Similarly, the Hg level in breast milk and newborn hair did not differ according to maternal amalgam tooth fillings or maternal fish consumption. Only two umbilical cord blood samples were positive for Hg, both of which had a level 45.8 mgL1. One of these mothers was aged 30 years and was exposed to ETS both before and during pregnancy. Prior to becoming pregnant she had seven amalgam tooth fillings and received two more during her pregnancy. During her pregnancy she had consumed one serving of fish each week. Her cord blood and newborn hair Hg levels were 33.20 mgL1 and 0.06 mgg1, respectively. The level of Hg in her breast milk was below the detectable limit. The other mother was aged 24 years and regularly smoked before pregnancy, but was not exposed to ETS during pregnancy. She ate three servings of fish each week during pregnancy. Her cord blood, breast milk and newborn hair Hg levels were 15.74 mgL1, 8.69 mgL1 and 0.25 mgg1, respectively. In all, six of the mothers in the study were residing near to city waste disposal site, but breast milk samples were analyzed for toxic heavy metals in only five. Cd was detected in the breast milk of three of these five mothers (60%) versus eight (8.4%) of the other 102 mothers. Eleven mothers were living in houses that used stove heating and Cd was detected in the breast milk of three (27.3%) of the 11 mothers who heated their homes with a stove, versus seven (7.3%) of the 96 mothers who had a radiator system in their home; however, among the 77 mothers whose childhood home was heated by stove three (3.9%) had Cd detected in their breast milk, versus seven (23.3%) of the 30 whose childhood home was heated by radiator. Among the mothers with a history of ETS exposure during pregnancy, the level of Cd in newborn hair was significantly higher, as compared to the mothers without such a history (0.08 ± 0.05 mgg1 versus 0.05 ± 0.03 mgg1, p ¼ 0.02). The detection rate of Cd in breast milk was higher among the mothers who delivered preterm infants ([2/8] 25% versus [8/99] 8.1%). The detection rate of Cd

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Table 2. Heavy metal levels and cases whose cord blood, breast milk and newborn hair Pb, Hg and Cd levels above the detection and the safe limits. Total Cord blood

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Breast milk mg L1

Newborn hair mg g

1

121

Levels

107

Cases above the detection limit n (%) Cases above the safe limit n (%) Levels

112

Cases above the detection limit n (%) Cases above the safe limit Levels Cases above the detection limit n (%) Cases above the safe limit n (%)

Lead

Mercury

Cadmium

1.66 ± 1.60* (5Dl–12.50)z (mg dL1) 120 (99.2)x1

5Dly (5Dl–5Dl)ô (5Dl–33.20)z (mg L1)

5Dly (5Dl–5Dl)ô (0–6.71)z (mg L1)

2 (1.7)jj2

24 (19.8)jj2

35 (29)yya

2 (1.7)zz

14.56 ± 12.13* (5Dl–46.14)z 89 (83.2)1x

1.36y (5Dl–5Dl)ô (5Dl–11.52)z 57 (53.3)jj2

& 2.72 ± 1.44* (1.01–8.01)z 112 (100)# &

&

& 0.23 ± 0.23* (0.01–1.43)z 112 (100)** &

5Dly (5Dl–5Dl)ô (5Dl–1.62)z 10 (9.3)jj2 & 0.07 ± 0.04* (0.01–0.22)z 112 (100)** &

& – No safe limit determined, Dl – detection limit. *Mean ± SD. yMedian. zRange. ôIQR. x40.03 mgL1. jj40.02 mgL1. #40.00003 mgg1. **40.00002 mgg1. yy 2 mg dL1. zz45.8 mgL1.

in cord blood was significantly higher in the mothers who consumed fish 2 times each week during pregnancy ([11/24] 45.8% versus [19/97] 19.6%, p ¼ 0.008). Maternal anthropometry, level of education, time between two pregnancies and parity, neonatal anthropometry, gender and the mode of delivery were not affected by Cd in the biological samples. No significant correlation was observed between three biological samples for the same heavy metal. There was a negative correlation between the level of Hg and Pb in breast milk (r ¼ 0.56, p50.0001), a positive correlation between the level of Pb and Cd in breast milk (r ¼ 0.31, p ¼ 0.001), a positive correlation between the level of Pb and Cd in umbilical cord blood (r ¼ 0.39, p50.0001), a positive correlation between the level of Pb and Hg in newborn hair (r ¼ 0.35, p50.0001) and a positive correlation between the level of Hg and Cd in newborn hair (r ¼ 0.20, p ¼ 0.033).

Discussion Women exposed to toxic heavy metals via absorption from the gastrointestinal tract, inhalation and skin exposure throughout life as well as during pregnancy can store these metals in their bodies [10–12]. Toxic metals that accumulate before and/or during pregnancy can be mobilized during pregnancy and cross the placental barrier, negatively affecting fetal development, depending on timing, dose and duration of exposure [3,11,13–15]. Fetal and neonatal

exposure is determined via detection of heavy metals in the maternal body, cord blood, infant hair, meconium and breast milk [16–18]. The Centers for Disease Control (CDC) lowered the predicted toxicity level of Pb in blood from 40 mg dL1 in 1975 to 10 mg dL1 in 1991 [19–22]. Currently, the CDC (2005) recommends that the level of Pb in blood should be 510 mg dL1; however, studies have reported that prenatal low level lead exposure (Pb level 55 mg dL1) is associated with impaired neurocognitive development during early childhood [22–25]. Gilbert and Wiess [8] suggested that the toxic level for Pb should be 2 mg dL1 instead of 10 mg dL1. In the present study, the mean Pb level in cord blood was 52 mg dL1 (1.66 ± 1.60 mg dL1); however, the level of Pb level in cord blood was 2 mg dL1 in 29% of the samples and 410 mg dL1 in only one (0.8%) sample. Between 1980 and 2011, the reported level of Pb in umbilical cord blood ranged from 0.67 to 13 mg dL1 [26– 31]. The mean Pb level in umbilical cord blood in the present study was lower than that reported by most other studies. The wide variation in the Pb level reported in umbilical cord blood may be due to differences in environmental conditions based on geography as well as environmental changes that occur over time. Leaded gasoline, lead-coated ceramics and lead-containing dyes are the most important sources of Pb exposure for the general population [32]. In Turkey, house paints do not contain lead and lead pipes are not used—the major source of Pb is leaded gasoline. The mean Pb level in umbilical

Maternal risk factors associated with Pb, Hg, and Cd levels in newborn

DOI: 10.3109/14767058.2015.1026255

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Table 3. Demographic findings, possible exposure routes and heavy metal levels. Cord blood

Breast milk

Pb

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n

mg dL

Newborn hair

Pb 1

n

Hg* 1

mg L

Maternal age 35 years 95 1.52 ± 1.31 89 14.26 ± 11.67 435 years 26 2.20 ± 2.34 19 15.96 ± 14.36 p 0.044 0.83 Matrenal working status Unemployed 57 1.74 ± 1.89 50 14.15 ± 12.47 Employed 64 1.59 ± 1.31 57 14.92 ± 11.93 p 0.6 0.75 Parity Primiparous 52 1.77 ± 1.99 48 15.58 ± 12.03 Multiparous 69 1.58 ± 1.24 59 13.74 ± 12.25 p 0.55 0.44 Gestational age 537 weeks 8 3.39 ± 3.96 7 10.77 ± 9.67 37 weeks 112 1.53 ± 1.25 99 14.62 ± 12.16 p 0.227 0.42 Gender Female 59 1.52 ± 1.21 52 14.56 ± 12.56 Male 62 1.80 ± 1.90 55 14.56 ± 11.83 p 0.33 1.00 Birth weight 53000 g 28 1.38 ± 1.34 22 11.48 ± 11.66 3000 g 93 1.75 ± 1.69 85 15.36 ± 12.19 p 0.16 0.16 Maternal ETS exposure during childhood period No 70 1.77 ± 1.91 61 15.35 ± 12.12 Yes 48 1.51 ± 1.06 44 13.62 ± 12.23 p 0.39 0.47 Maternal ETS exposure during pregnancy period No 30 1.74 ± 1.78 27 13.29 ± 12.32 Yes 91 1.64 ± 1.55 80 14.99 ± 12.11 p 0.79 0.54 Insecticide use Yes 56 1.54 ± 0. 96 51 17.03 ± 11.8 No 65 1.77 ± 0.99 56 12.31 ± 12.05 p 0.41 0.044 Fish consumption 2 meal/week 30 1.61 ± 1.67 28 15.43 ± 11.59 52 meal/week 91 1.82 ± 1.41 79 14.26 ± 12.37 p 0.55 0.66 Amalgam tooth feeling Exist 29 1.51 ± 1.42 27 13.54 ± 11.68 Absent 92 1.71 ± 1.66 81 14.89 ± 12.32 p 0.51 0.61

mg L

n

Pb 1

n

Hg 1

mg g

n

mg g

Cd 1

n

mg g1

89 19

1.30 (5Dl–7.32) 1.50 (5Dl–7.11) 0.92

87 25

2.72 ± 1.48 2.69 ± 1.34 0.82

87 25

0.24 ± 0.24 0.21 ± 0.20 0.62

87 25

0.07 ± 0.04 0.08 ± 0.05 0.78

50 58

1.36 (5Dl–6.73) 1.41 (5Dl–7.53) 0.73

51 61

3.15 ± 1.62 2.35 ± 1.18 0.003

51 61

0.29 ± 0.27 0.19 ± 0.20 0.03

51 61

0.07 ± 0.04 0.07 ± 0.04 0.96

49 59

5Dl (5Dl–7.20) 5.33 (5Dl–7.52) 0.09

48 64

2.64 ± 1.37 2.77 ± 1.51 0.64

48 64

0.26 ± 0.29 0.21 ± 0.20 0.28

48 64

0.07 ± 0.05 0.07 ± 0.04 0.91

7 100

1.41 (5Dl–7.27) 1.30 (5Dl–7.33) 0.90

8 103

1.93 ± 0.68 2.79 ± 1.47 0.10

8 103

0.27 ± 0.39 0.23 ± 0.23 0.64

8 103

0.06 ± 0.03 0.07 ± 0.04 0.57

52 56

2.89 (5Dl–7.58) 1.41 (5Dl–6.98) 0.53

52 60

2.80 ± 1.32 2.64 ± 1.55 0.57

52 60

0.23 ± 0.25 0.23 ± 0.23 0.96

52 60

0.07 ± 0.04 0.07 ± 0.04 0.59

22 86

6.69 (5Dl–7.99) 1.30 (5Dl–6.53) 0.17

25 87

2.42 ± 1.32 2.80 ± 1.47 0.19

25 87

0.23 ± 0.26 0.24 ± 0.23 0.68

25 87

0.07 ± 0.05 0.07 ± 0.04 0.98

62 44

5.74 (5Dl–7.27) 5Dl (5Dl–7.36) 0.08

64 45

2.97 ± 1.69 2.32 ± 0.91 0.02

64 45

0.23 ± 0.25 0.25 ± 0.23 0.59

64 45

0.08 ± 0.05 0.07 ± 0.04 0.34

27 80

1.29 (5Dl–7.99) 1.41 (5Dl–7.28) 0.48

25 87

2.71 ± 1.89 2.72 ± 1.31 0.99

25 87

0.21 ± 0.18 0.24 ± 0.25 0.46

25 87

0.05 ± 0.03 0.08 ± 0.05 0.02

51 56

0.60 (5Dl–7.13) 4.53 (5Dl–7.13) 0.65

52 60

2.59 ± 1.14 2.83 ± 1.67 0.38

52 60

0.24 ± 0.25 0.23 ± 0.22 0.43

52 60

0.07 ± 0.04 0.07 ± 0.04 0.88

28 79

1.46 (5Dl–7.24) 0.60 (5Dl–7.93) 0.83

28 84

2.94 ± 1.44 2.64 ± 1.45 0.35

28 84

0.27 ± 0.22 0.27 ± 0.45 0.53

28 84

0.07 ± 0.04 0.08 ± 0.05 0.10

27 81

1.41 (5Dl–7.27) 1.30 (5Dl–7.35) 0.94

25 87

2.85 ± 1.35 2.68 ± 1.48 0.58

25 87

0.25 ± 0.13 0.23 ± 0.25 0.67

25 87

0.07 ± 0.03 0.07 ± 0.05 0.56

ETS – environmental tobacco smoke. *Median (25–75 percentiles). Bold p values are statistically significant.

cord blood reported from Turkey drastically decreased from 15.36 ± 7.13 mg dL1 in 1994 to 1.65 ± 1.4 mg dL1 in 2011 [33–38], which is most likely indicative of the reduction in the use of leaded gasoline since 1998. The sale of leaded gasoline in Turkey was banned on 1 January 2006 (Law on the Quality of Petrol and Diesel Fuels, 11 June 2004, 25489 numbered Official Gazette). Subsequent to the reduction in the use of leaded gasoline mean Pb levels declined sharply [33–38]. Similar to Al-Jawadi et al.’s finding, in the present study the mean level of Pb in cord blood was lower in the mothers aged 35 years [39]. In the present study, the level of Pb in cord blood increased with maternal age; similarly Younes et al. reported that the Pb level in the breast milk of mothers aged 20 years (5.1 ± 1.4 mgL1) was lower than in those aged 36 years

(13.5 ± 6.5 mgL1) [40]. As expected, this may be due to an increase in the amount of Pb stored in the maternal body with age; however, the mean level of Pb in breast milk in the present study was similar in the mothers aged 35 years and 435 years, this might be due to absence of mothers aged 520 years in the present study. Pb in breast milk can be used as an indicator of both maternal and neonatal exposure [18]. The reported level of Pb in breast milk ranges from 51 to 4100 mg L1 [5,41–43]. To date, there is no defined safe level of Pb in breast milk. In the present study, the mean level of Pb in breast milk was 14.56 ± 12.13 mgL1 and was significantly higher in the mothers with a history of repeated insecticide exposure (mean level of Pb in breast milk: 17.03 ± 11.8 mgL1 versus 12.3 ± 12.0, p50.05). Interestingly, the mean level of Pb in

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breast milk was significantly higher in unemployed mothers than in those who were employed, which may have been due to high-level exposure from house dust among housewives during regular house cleaning while employed mothers mostly hire somebody else for this purpose [44]. Given a limited number of studies on Pb in newborn hair there is no defined safe level. Moro et al. reported that the geometric mean Pb level was 1.4 ± 0.2 mgkg1 in the hair of 141 newborns [45]. In the present study, the mean level of Pb in newborn hair was 2.72 ± 1.44 mgg1, indicating that there was continuous exposure during pregnancy. Razagui et al. reported that the mean Pb level was 4.56 mgg1 (4.39– 5.56 mgg1) in the hair of 82 newborns, and that cigarette smoking was associated with higher Cd and Pb concentrations [46]. Tobacco contains a wide variety of heavy metals, including Pb, Hg and Cd [47]. In the present study, maternal exposure to ETS was associated with detectable levels of Pb and Cd in newborn hair, indicating the importance of ETS exposure in chronic toxic heavy metal exposure. As it is observed in ban of leaded gasoline, tobacco smoking law may cause further decrease in chronic prenatal lead exposure. Smoking in indoor public spaces has also been prohibited in Turkey since 19 July 2009. Further studies could show the effect of this intervention. There are no barriers preventing transmission of Hg from mother to fetus. The primary sources of Hg exposure are consumption of contaminated fish and amalgam tooth fillings. The Food and Drug Administration (FDA) and the Environmental Protection Agency (EPA) advise pregnant women to avoid fish that contain high levels of Hg and eat up to two average meals a week [48]. Cord blood Hg levels 45.8 mgL1 are associated with low IQ [49,50]; therefore, most studies consider levels55.8 mgL1 as safe. In the present study, only two mothers had a detectable level of Hg in cord blood (15.74 mgL1 [3-fold greater than safe] and 33.20 mgL1 [6-fold greater than safe]). The first mother had three servings of fish each week during pregnancy and the other mother had amalgam tooth fillings (seven prior to pregnancy and two received during pregnancy); however, 53% of the mothers had a measurable level of Hg in breast milk, 28 of which had 2 servings of fish each week during pregnancy (41% of the consumed fish was anchovy—a very small, low fat content fish expected to have very low levels of Hg contamination). It is well known that nearly all fish contain traces of Hg and consumption of fish increases the Hg concentration in hair [51,52]. Neurodevelopment of the newborns in the present study is currently being followed-up and we intend to publish the data in the near future. WHO reported that the risk of fetal brain damage increases when the concentration of Hg in maternal scalp hair is 410–20 mg g1 [53]. Grandjean et al. [50,53] reported Hg-related neurodevelopmental dysfunction in children whose mother had Hg levels in their hair 510 mg g1 [50,51]. Recent epidemiological studies strongly suggest that long-term neurodevelopmental dysfunction results from fetal Hg exposure at doses as low as 1 ppm (mg g1) in maternal hair [51,54]; however, maternal hair was not analyzed in the present study—the Hg level in the newborn hair samples did not exceed 10 mg g1 and only two newborn hair samples had an Hg level 41 mg g1.

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Food and smoking are major sources of Cd exposure, and polluted air and water are other routes of exposure [55]. Cd is absorbed via the gut and lungs, and accumulates in the liver and kidneys (half-life: 6–38 years). Animal and human studies show that Cd exposure during pregnancy is associated with a decrease in birth weight, amelia, syringomyelia and delayed sternal rib ossification. High-level Cd exposure was reported to be carcinogenic, mutagenic and teratogenic in many animal studies [55–57]. There is no established safe level for Cd in cord blood, newborn hair or breast milk [56]. Maternal exposure to ETS is associated with higher fetal Cd exposure [58,59]. Ro¨llin et al. reported that the median Cd level in cord blood was 0.25 mg L1 (range: 0.05–0.89 mg L1) and that the Cd level in umbilical cord blood was higher in samples obtained from mothers who smoked [60]. Butler et al. reported that the level of Cd in the blood of mothers who were moderate smokers (1–8 cigarettes d1) and heavy smokers (48 cigarettes d1) was 7.4-fold higher and 12.5-fold higher, respectively, than in nonsmokers [28]. In addition, they detected Cd in 26% of all cord samples, with a geometric mean of 0.08 mgL1 [28]. Sorkun et al. reported that smoking ¨ ru¨n et al. increased the placental Cd concentration [61]. O reported that the level of Cd in breast milk increased in active and/or passive smokers during pregnancy (0.89 and 0.00 mg L1, respectively; p ¼ 0.023) [62]. Kutlu et al. studied a group of pregnant women (30 non-smokers and 90 smokers) and reported that the placental level of Cd and Pb was higher in the smokers than in the non-smokers [58]. In the present study, maternal exposure to ETS during pregnancy was associated with higher levels of Cd in newborn hair. Cd was detected in 19.8%, 9% and 100% of cord blood, breast milk and newborn hair samples, respectively, in the present study. The reported level of Cd in cord blood ranges between 0.08 and 0.78 mg L1 [31,59,60,63–65]. In the present study, the median level of Cd in cord blood was below the detection limit (range 5Dl–6.71 mg L1). Only one of the cord blood samples in the present study had a Cd level that was higher than safety cut-off value of 5 mg L1 used by American Occupational Safety and Health Administration (OSHA) [66]; however, this level is used for working adults— a safe Cd level for cord blood has not been defined. Al-Saleh et al. detected Cd in 94.8% of umbilical cord blood samples in their large series, but only five newborns had a Cd level 45 mg L1 [67]. The detection rate of Cd in cord blood was significantly higher among the mothers in the present study who consumed 2 servings of fish each week during pregnancy. Cd bioaccumulation in fish has been reported [68–71] and consumption of seafood is also accepted as one of the routes for human exposed to Cd [72]. The present findings indicate that Pb, Hg and Cd might cross the placental barrier prenatally and accumulate in breast milk postnatally, and that these toxic heavy metals might be a possible potential health hazard to fetuses and neonates. The primary toxic heavy metal exposure problem in the present study was Pb, which was detected in 80% of the three biological samples analyzed; however, a considerable number of infants were also exposed to Hg and Cd during prenatal life. Maternal exposure to ETS, especially household exposure, was also observed to increase the levels of Cd and Pb in

DOI: 10.3109/14767058.2015.1026255

Maternal risk factors associated with Pb, Hg, and Cd levels in newborn

the biological samples. This study also reflects that nationwide health promotion programs including prohibition of use of leaded gasoline and tobacco law would also decrease toxic heavy metal exposure of newborn infants. Lastly, we think that preventing/reducing household ETS exposure may decrease prenatal toxic heavy metal exposure.

Declaration of interest This work was funded by Hacettepe University research grant.

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Maternal risk factors associated with lead, mercury and cadmium levels in umbilical cord blood, breast milk and newborn hair.

Lead (Pb), mercury (Hg) and cadmium (Cd) are environmental pollutants that are wide spread throughout the world. The present study aimed to investigat...
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