Environmental Science and Pollution Research https://doi.org/10.1007/s11356-018-1535-z
RESEARCH ARTICLE
Quantification of polychlorinated biphenyl contamination using human placenta as biomarker from Punjab Province, Pakistan Anber Naqvi 1 & Abdul Qadir 1 & Adeel Mahmood 2 & Mujtaba Baqar 3 & Iqra Aslam 1 & Farhan Sajid 4 & Mehvish Mumtaz 5 & Jun Li 6 & Gan Zhang 6 Received: 30 October 2017 / Accepted: 13 February 2018 # Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract The present study biomonitored the placental polychlorinated biphenyl (PCB) concentrations in women from Punjab Province, Pakistan, that provides the pioneer data for occurrence and body burden of PCBs in placental tissues from South Asian women. The ∑34PCB concentrations in placental tissues were ranged from 20.2 to 115.98 ng/g lipid weight (lip. wt.), with predominance of tetra-PCB (54.67%). The levels of ∑8DL-PCBs and ∑6-indicator PCBs were ranged from 2.03 to 27.64 ng/g (lip. wt.) and 1.71 to 30.8 ng/g (lip. wt.), respectively. The WHO-TEQ2005 values for DL-PCBs were ranged from 1.18 × 10−5 to 0.067 ng/g (lip. wt.), with highest value evaluated for CB-126. The estimated daily intake (EDI) for DL-PCBs was ranged from 9.27 × 10−8 to 5.25 × 10−4 pg WHO-TEQ/kg body weight (bw), which was within the tolerable daily intake (TDI) values established by international organizations. The spatial distribution patterns of Σ34PCB concentrations from study area have shown relative higher concentrations in samples from urban and industrial cities than rural areas, and industrial and urban releases along with e-waste handling were recognized as vital PCB sources in the environment. In order to ascertain the transplacental transfer of PCBs, the fetal growth parameters were correlated with the ∑34PCB concentrations in placental tissues. The relationship between ∑34PCB concentrations in placental tissues and infant’s anthropometric measures through multiple linear regression showed a negative correlation of infant’s body weight (R2 = 0.0728), crown to heel length (R2 = 0.068), head circumference (R2 = 0.0342), chest circumference (R2 = 0.0001), and mid arm circumference (R2 = 0.0096) that noticeably highlights the inhibited fetal anthropometric development associated with maternal PCB bioaccumulation. Hence, an immediate elimination of ongoing PCB addition in the studied area has been emphasized and further investigations are suggested to appropriately manage the public and neonatal health risks in the region. Keywords PCBs . Dioxin-like PCBs . Placental transfer . Neonatal health
Responsible editor: Hongwen Sun Electronic supplementary material The online version of this article (https://doi.org/10.1007/s11356-018-1535-z) contains supplementary material, which is available to authorized users. * Abdul Qadir
[email protected]
3
Sustainable Development Study Centre, Government College University, Lahore 54000, Pakistan
* Mujtaba Baqar
[email protected]
4
District Headquarters Hospital Khanewal, Department of Primary and Secondary Health Care, Government of the Punjab, Lahore 58270, Pakistan
5
School of Environment, Tsinghua University, Beijing 100084, China
6
State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China
1
2
College of Earth and Environmental Sciences, University of the Punjab, Lahore 54590, Pakistan Department of Environmental Sciences, Government College Women University, Sialkot 51310, Pakistan
Environ Sci Pollut Res
Introduction Polychlorinated biphenyls (PCBs) are industrial chemicals that are of great global concern, owing to their persistent, lipophilic, bioaccumulative, and toxicity in various biological and environmental media (Kodavanti et al. 2017).On the basis of in vivo and in vitro studies, the International Agency for Research on Cancer (IARC) has placed PCBs into group 1 compounds, i.e., carcinogenic to humans (IARC 2016). Besides their carcinogenic characteristics, the PCB exposure has been established to cause reproductive, endocrinal, neurological, and immunological disorders (Letcher et al. 2010). In recognition to the PCBs’ adverse environmental effects, its production and usage was prohibited globally under the Stockholm Convention on Persistent Organic Pollutants, 2001 (UNEP 2001). However, the easier availability, adaptability, and low-cost of PCBs sustain its usage in developing countries, including Pakistan (Baqar et al. 2017a). Subsequently, they have been released from manufacturing and repairing of electric wares, industrial wastewater discharges, and unsafe waste disposal techniques (Eqani et al. 2013; Kim and Yoon 2014; Syed et al. 2014). Besides, a vast human population in Pakistan has limited earnings to purchase advanced electronic devices, which broadens the consumer market for reconditioned and used outdated devices, predominantly imported from developed countries and possibly contains PCBs. These end-of-life products produce e-waste that undergone open burning and other hazardous recycling techniques to recover metals (Iqbal et al. 2015; Baqar et al. 2017b) and subsequently increases the atmospheric PCB concentrations in Asian countries (Li et al. 2007; Eqani et al. 2012b; Ali et al. 2013). In humans, principal exposure route to PCBs is the dietary intake that accounts 90% of the total exposure (Chovancová et al. 2012); other sources include dermal exposure, ingestion, and inhalation from ambient environment (Ullah et al. 2016).Once entered the human body, they persist and bioaccumulate in the body lipids (Hites 2004), and can be traced out in the blood streams and tissues (Lopez-Espinosa et al. 2007). Nevertheless, studies have suggested that the PCBs exposure originates in the uterine stage of life through placental transfer (Vizcaino et al. 2014; Nanes et al. 2014). The placenta is considered to be the lifeline to fetus in utero, supplying oxygen and nutrients, and waste removal from fetal environment (Leino et al. 2013; Nanes et al. 2014). However, the persistent and bioaccumulative compounds, including PCBs have been reported to reach the fetus by crossing the placental barrier through blood circulation (Covaci et al. 2002; Wang et al. 2006). The prenatal exposure to PCBs may lead to preterm birth, reduced birth weight, and intrauterine growth retardation; along with some latent effects, such as disturbed levels of thyroid hormone, reproductive impairments, cognitive deficits, altered perceptual development, and adverse neurobehavioral impacts (Covaci et al. 2002; Bergonzi et al.
2009; Kodavanti et al. 2017). The PCBs’ exposure at early developmental stages may lead to health risks in fetuses and infants, who are more susceptible to the impacts of these environmental toxins as their detoxification mechanisms are partially developed than adults (Vizcaino et al. 2014). In recent years, studies had effectively biomonitored the PCB levels in human placental tissues worldwide (Myllynen et al. 2005; Gómara et al. 2012; Leino et al. 2013; Tsukimori et al. 2013; Nanes et al. 2014; Vizcaino et al. 2014). In contrast, though high PCB concentrations have been reported from various environmental compartments in Pakistan (Eqani et al. 2012a,b, 2013; Syed et al. 2013, 2014; Mahmood et al. 2014b; Mumtaz et al. 2016; Yasmeen et al. 2017); to date, no study has undertaken to assess placental transfer of PCBs. The present study was conducted for quantitative screening of PCB levels in the placental tissue samples from Punjab Province, Pakistan and its correlation with maternal characteristics and neonatal anthropometric measures. The objectives of the study include occurrence, spatial distribution and source apportionment, comparative analysis, toxicity equivalency (TEQ), and estimated daily intake (EDI) assessment for dioxin-like PCBs (DL-PCBs) that provides baseline data on the maternal and prenatal exposure levels of PCBs from Pakistan as well as South Asia that could be significantly valuable in future epidemiological and human health risk studies.
Materials and methods Study area and sampling strategy The study area encompasses five districts of Punjab province (Pakistan) viz. Lahore, Sialkot, Khanewal, Okara, and Chakwal (Fig. 1). The Punjab is the most populated province of Pakistan that is considered to be the life-line for the country; as it contains the most intensively cultivated areas, i.e., Rechna Doab, Jech Doab, and Bari Doab, and most number of industrial units. Urban expansion and industrialization in the province have caused an increase in environmental pollution due to vehicular emission, coal combustion, industrial emissions and effluents discharges, and municipal solid waste burning in open dumps. Besides, the e-waste burning to recover valuables is also a common practice observed in most parts of the province. However, despite of the fact that Pakistan ratifies the Stockholm Convention, 2001, yet, the country is experiencing PCB environmental release (Eqani et al. 2012a; Syed et al. 2014) that led to PCB contamination in various environmental media of the Punjab province. Site selection criterion was based on the industrial and agricultural activities and spatial diversity within these districts. The study area was further subdivided into two zones, viz., urban and rural to make the cross-comparison between them.
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Fig. 1 Map of the study area showing sampling sites within five districts of the Punjab Province, Pakistan
The rural women were those who purely belonged from areas with agricultural activities. Women (n = 43) (rural = 18 and urban = 25) with a cesarean section at public sector hospitals, located in the study area were selected as subjects (Table S1). The inclusion criteria included those who were born and currently residing in Punjab province, age ranging between 18 and 45 years, with no previous history of cardiac disease (Thomas et al. 2006) and maternal or fetal anomalies (Nanes et al. 2014). Prior to sampling, the approval of the present study was obtained from Advanced Studies and Research Board (ASRB), University of the Punjab, Pakistan, and written consent was obtained from the subjects, after they were briefed about the purpose of the research.
Sample and data collection Placental tissues (~ 20 g each) were collected with the assistance of paramedical staff from the villous parenchyma, excluding the decidua basalis and chorionic plate, within 10–15 min after the delivery, in sterilized glass jars, pre-rinsed with dichloromethane. The collected samples were sealed and labeled immediately after the collection and kept in an ice-box with dry ice, and followed by their transfer to Ecotoxicology Laboratory at the College of Earth and Environmental Sciences, University of the Punjab, Pakistan; where the samples were stored till further analysis (Dewan et al. 2013; Nanes et al. 2014). In order to obtain information about maternal and neonatal anthropometric characteristics, lifestyle
and socio-demographic conditions of the subjects, a selfadministered questionnaire was used. The descriptive statistical results of the questionnaire are summarized in Table S2.
Sample preparation Each frozen placenta sample was thawed, finely chopped, weighed to 1 g, transferred to 30 mL glass vial, and spiked with the surrogate standards, i.e., 2,4,5,6-tetrachloro-m-xylene (TCmX) and Decachlorobiphenyl (CB-209). The spiked sample was then vortexed, stirred, and sonicated for 20 min and kept overnight at 4 °C (Covaci and Voorspoels 2005; Vizcaino et al. 2014). PCB residues were then extracted using previously described method by Bergonzi et al. (2009) and Dewan et al. (2013). Briefly, sonicated-spiked samples were extracted with n-hexane (6 mL) and acetone (3 mL), and equilibrated by ultrasonic treatment for 1 h at 3 °C, followed by their centrifugation for 10 min at 2000 revolution per minute (rpm). The clear upper layer of n-hexane, containing PCBs was then separated into another glass vial and repeating the process twice to obtain maximum extract, with no PCB residual left. The extract was then cleaned and purified through 12mm diameter silica-alumina packed column, containing sodium sulphate, anhydrous(1 cm), sulfuric acid-silica, 50% (4 cm), neutral silica, 3% deactivated (4 cm), and neutral alumina, 3% deactivated (4 cm), and eluted with n-hexane (10 mL) and dichloromethane (5 mL). The purified extract
Environ Sci Pollut Res
was then concentrated through gentle nitrogen streaming, until 0.2 mL of the extract obtained, followed by addition of isooctane (50 μl) and 13C–PCB 141 as solvent keeper and internal standard, respectively (Vizcaino et al. 2014).
Chromatographic analysis In total 34 PCB congeners (IUPAC No. 30, 37, 44, 49, 52, 54, 60, 66, 70, 74, 77, 82, 87, 99, 101, 105, 114, 118, 126, 128, 138, 153, 156, 158, 166, 169, 170, 179, 180, 183, 187, 189, 198, and 209) were analyzed at the State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, China, using a Triple Quadrupole GC/MS (Agilent 7000A) connected with Gas Chromatograph (Agilent 7890A) and autosampler (Agilent 7693) having CP-8 capillary column (CP7481, CP-Sil 8, 50 m × 0.25 mm × 0.12 μm from Netherlands). The temperature of the injector was adjusted to 280 °C and temperature of the oven was set initially at 100 °C (for 3 min), which was later increased to 160 °C at the rate of 20.0 °C per min and ultimately to 296 °C at 8 °C per min, with holding time of 5.5 min. The electron impact spectrometry per three fragment ions in selected-ion monitoring mode was employed to identify the PCB congeners. The mass selective detector (MSD) source and quadruple temperatures were set at 230 and 150 °C, respectively. The identification of analyte was based upon their respective retentions time and ion chromatographs against the standards. Quantification was done by creating (multi-level) calibration curves and for all the concentration ranges detected in the samples, a good linearity of R2 > 0.99 was achieved.
Lipid determination Placental lipids were measured gravimetrically by taking placenta tissue (1 g), and thrice homogenizing it in 5-mL solution of chloroform: methanol: hydrochloric acid (20:10:0.1 v/v/v), followed by the addition of 0.1 N HCl (10 mL) and centrifugation for 10 min at 3000 rpm. Organic phase containing lipids was then collected and the process was repeated to obtain maximum lipids. The extract was then concentrated under nitrogen stream and dry lipids were measured gravimetrically (Vizcaino et al. 2014).
Quality control and quality assurance Quality assurance and controls were firmly followed for the entire analysis. The glassware was thoroughly rinsed with double-distilled water and later baked in muffle furnace for 4 h at 450 °C before their usage, to prevent any contamination to the samples. All the chemicals/reagents consumed were purchased from Merck KGaA (Germany) and were of HPLC grade. The internal and surrogate standards were
purchased from Dr. Ehrenstorfer GmbH (Germany) and CPA chem Ltd. (Bulgaria), respectively. For instrumental calibration, standards were run every day and solvent blanks were analyzed after every 15 samples (a batch) to avoid any repeatability and cross-contamination in chemical analysis. For PCB peak integration, the Agilent MassHunter Workstation Software Quantitative Analysis was used. The prescribed procedure by Syed et al. (2014) was used to calculate method detection limit (MDL) and instrumental detection limit (IDL). The determination of congeners below the IDL was referred as not detected (ND). The MDLs were calculated as thrice to the standard deviation (SD) of the blank (Mahmood et al. 2014a). The calibration standards were used on daily basis to compute the calibration curves. Mean recovery values were79 ± 8% for TCmX and 82 ± 9% for CB-209, respectively and all the results were adjusted to the blanks and standards recovery ratios; for determination of CB-209 was only used as surrogate standard (Baqar et al. 2017b).
Statistical analysis The Statistical Package for the Social Sciences (SPSS) version 16.0 was used to test basic descriptive statistic and multiple regression analysis of PCBs with maternal and neonatal physiological data. The Arc GIS version 10.2.2 was employed to display PCB spatial distribution patterns in the study area.
Results and discussion PCB congeners and homologs profile Descriptive statistics of 34 PCB congeners and 7 PCB homologs in placental tissues from Pakistanare summarized inTable S3 and Table 1, respectively. The placental lipids values were ranged from 0.7% to 3.0% (mean: 1.8%). The ∑34PCB concentrations in placental tissues were measured between 20.2 and 115.98 ng/g lipid weight (lip. wt.) with mean concentration of 80.26 ± 19.87 ng/g (lip. wt.). All the studied PCB congeners were detected from placental samples. The PCB congener-specific profile highlighted the CB-70 (mean: 6.63 ng/g (lip. wt.) as most dominant PCB congener, followed by CB-66 and CB-52, and least concentration was depictedbyCB-166 (mean0.21ng/g(lip. wt.). The PCB homologs profile revealed the dominance of tetra-PCB with 54.67% contribution of the total PCBs. The overall PCB homologs distribution trend in placental tissues from Pakistan were in magnitude as; tetra-CB > penta-CB > hexa-CB > triCB > hepta-CB > octa-CB > deca-CB. In Pakistan, PCBs are primarily used as a technical mixture of tetra-CB, penta-CB and tri-CB (Syed et al. 2014; Baqar et al. 2017b) which has been validated by the prevalence of tetra-CB and penta-CB in placental tissue samples from the study area. The dominance of tetra-CB and penta-CB in placental tissues were in consistent to previous
4.97 39.94 19.24 15.69 4.84 0.11 0.07 84.82 5.48 ± 1.56 45.34 ± 10.12 20.65 ± 7.36 15.27 ± 7.14 6.24 ± 2.54 0.19 ± 0.23 0.26 ± 0.44 93.43 ± 46.17 6.1–11.72 36.11–61.54 6.16–23.16 3.04–13.15 0.55–3.74 0.03–1.06 0.02–2.44 25.79–158.22 8.91 51.05 14.15 7.89 2.88 0.46 0.31 85.65 4.02 ± 1.44 34.35 ± 10.08 17.75 ± 6.25 12.32 ± 5.36 3.3 ± 2.07 2.68 ± 7.66 0.24 ± 0.18 74.66 ± 47.55 1.26–8.97 12.65–66.05 3.11–23.74 1.2–9.22 0.77–3.64 0.01–0.92 0.07–1.46 12.54–149.18
CB 198 only
CB 209 only g
f
Sum of CB 128, 138, 153, 156, 158, 166, and 169
Sum of CB 82, 87, 99, 101, 105, 114, 118, and 126
Sum of CB 44, 49, 52, 54, 60, 66. 70, 74, and 77
Sum of CB 30 and 37
Sum of CB 170, 179, 180, 183, 187, and 189 e
d
c
b
a
tri-PCBa tetra-PCBb penta-PCBc hexa-PCBd hepta-PCBe octa-PCBf deca-PCBg ∑34PCBs
7.8 ± 2.34 48.12 ± 10.16 17.19 ± 5.96 7.96 ± 4.75 4.46 ± 2.43 1.14 ± 1.37 1.14 ± 1.46 87.80 ± 55.39
7.81 52.24 18.25 6.84 4.11 0.60 0.77 6.84
4.38–12.92 32.59–60.56 8.9–24.91 3.1–18.71 1.67–8.48 0.08–4.2 0.03–4.89 19.18–193.25
4.69 ± 2.01 42.18 ± 17.2 12.89 ± 7.56 5.33 ± 2.69 1.53 ± 0.84 0.45 ± 0.33 0.4 ± 0.56 67.47 ± 43.06
4.23 42.31 12.32 6.15 1.35 0.36 0.11 66.83
Range Median Mean ± SD Range Median Mean ± SD
3.95 32.97 16.16 12.44 3.02 0.20 0.19 68.94
2.04–6.62 22.2–52.17 10.85–30.57 5.97–22.54 0.49–7.4 0.13–24.48 0.02–0.55 27.16–174.04
8.82 ± 2.08 50.14 ± 7.72 14.1 ± 5.32 7.67 ± 3.22 2.66 ± 1.05 0.58 ± 0.39 0.57 ± 0.74 84.54 ± 43.92
Mean ± SD Mean ± SD
Median
Range
Sialkot Okara Khanewal Lahore Homologs
Table 1
Descriptive statistics of PCBs in placental tissues (ng/g (lip. wt.)) samples from five districts of the Punjab Province, Pakistan
Median
Range
Chakwal
Mean ± SD
Median
Range
4.03–8.11 37.57–61.45 13.26–30.56 6.19–23.48 4.3–10.43 0.02–0.6 0.01–1.04 43.29–155.90
Environ Sci Pollut Res
findings of Nanes et al. (2014) from the USA. Moreover, the degree of chlorination has also been highlighted to affect the placental PCB concentrations (Vizcaino et al. 2014) that is dominated by higher chlorinated congeners due to their longer halflives and greater bioaccumulation capacity in humans (Leino et al. 2013). However, the predominance of less chlorinated PCBs in placental tissues was reported in some previous studies (Fernandez et al. 2012; Ma et al. 2012; Needham et al. 2011). Among the 34 PCB congeners, six indicator (or marker) PCB congeners (i.e., CB-52, CB-101, CB-118, CB-138, CB153, and CB-180) were also evaluated. The ∑6PCB (sum of six indicator PCBs) mean concentrations was measured as 17.69 ng/g (lip. wt.). The CB-52 has shown the highest mean concentration (6.01 ng/g (lip. wt.)) among indicator PCB congeners, followed by CB-101 and CB-153. Previously, Nanes et al. (2014) and Gómara et al. (2012) highlighted that the dominance of CB-52, followed by the CB-101 in placental tissue samples from United States and Spanish mothers. Some studies have shown abundance of CB-153 in placental tissue samples (Porpora et al. 2013; Vizcaino et al. 2014). Though CB-52 and CB-101 are rapidly metabolized in living organisms, so their high levels are occasional in humans; indicating recent human exposure to low chlorinated PCB congeners (Gómara et al. 2012). Similarly, the occurrence of non-persistent congeners (i.e., CB-52, CB-66, CB-74, CB-101, CB-105, and CB-128) at high concentrations indicated the recent and local exposure of the subjects to PCBs (Covaci et al. 2001). Despite of the fact that few studies have attempted to quantify the PCB accumulation levels in placental tissues; a comparative analysis of ∑PCB concentrations in placental tissues from current study with other studies across the world was performed (Table 2). The comparison revealed that ∑PCB levels in placental tissues from present study were found to be slightly higher or comparable to those reported from Finnish (median: 48.5 ng/g lip. wt.) (Leino et al. 2013), Italian (92.5 ng/g lip. wt.) (Bergonzi et al. 2009), and Spanish mothers (40 ng/g lip. wt.) Vizcaino et al. 2014). However, the current placental PCB levels were much higher than the findings from China (Ma et al., 2012), the USA (Nanes et al. 2014), and Spain (Gómara et al. 2012). In past, the placental PCB levels in Asian mothers were reported to be lower than those from North American and European mothers (Nanes et al. 2014), reflecting the fact that 80% of the global PCB production occurred in these industrialized regions (Breivik et al. 2002). Nevertheless, soon after the global prohibition on the production and use of PCB under the Stockholm Convention (2001), the PCB production and usage was strategically eliminated in developed countries (Fiedler et al. 2013). However, the ongoing usage of PCBs is being reported from Pakistan along with its release from uncontrolled e-waste recycling (Mahmood et al. 2014a; Iqbal et al. 2015) which is also validated by PCB concentrations in placental tissue samples from Pakistan.
10–230 –
Vizcaino et al. (2014)
0.943–4.331 Gomara et al. (2012) 2.546 –
CB-28, 52, 101, 118, 153, 138, and 180 49 Spain
7
17 Spain
15
42 USA
32
130 Finland
37
40
0.076–0.856 Nanes et al. (2014) 0.371 –
Leino et al. (2013) 48.5 –
–
Ma et al. (2012)
Bergonzi et al. (2009)
ND-9.8
–
0.89
92.5
– 08 130
70
China
Italy
30
CB-28, 31, 52, 74, 99, 101, 105, 114, 118, 123, 128, 138, 146, 153, 156, 157, 167, 170, 172, 177, 180, 183, 187, 189, 194, 196, 201, 203, 206, and 209 CB-18, 28, 33, 47, 49, 51, 52, 60, 66, 74, 77, 81, 99, 101, 105, 110, 114, 118, 122, 123, 126, 128, 138, 141, 153, 156, 157, 167, 169, 170, 180, 183, 187, 189, 194, 206, and 209 CB-8, 28, 37, 44, 49, 52, 60, 66, 70, 74, 77, 82, 87, 99, 101, 105, 114, 118, 126, 128, 138, 153, 156, 158, 166, 169, 170, 179, 180, 183, 187, and 189 CB-28, 52, 101, 118, 146, 153, 105, 138, 187, 183, 128, 156, 180, 170, and 189
–
20.2–115.98 Present study
Mean Median Range
80.26 67.08
CB-30, 37, 44, 49, 52, 54, 60, 66, 70, 74, 77, 82, 87, 99, 101, 105, 114, 118, 126, 128, 138, 153, 156, 158, 166, 169, 170, 179, 180, 183, 187, 189, 198, and 209 CB-105, 118, 156, 157, 167, 189, 206, and 209 34
Number of samples Number of congeners PCB congeners studied Country
Pakistan 43
Comparison of PCBs concentrations (ng/g (lip. wt.)) in placental tissues with previous studies from other countries Table 2
Concentration
Reference
Environ Sci Pollut Res
Spatial distribution and source apportionment of PCBs The PCBs’ spatial distribution in placental tissues from the Punjab, Pakistanis is illustrated in Fig. 2. The mean Σ34PCB concentration-based spatial profile followed the order as: Chakwal > Lahore > Sialkot > Okara > Khanewal. Relatively higher Σ34PCB concentrations were detected in placental samples from urban and industrial cities, i.e., Chakwal (93.43 ± 46.17 ng/g (lip. wt.)), Lahore (87.80 ± 55.39 ng/g (lip. wt.)), and Sialkot (84.54 ± 43.92 ng/g (lip. wt.)) than those from the rural towns of Okara (74.66 ± 47.55 ng/g (lip. wt.)), and Khanewal (67.47 ± 43.06 ng/g (lip. wt.)). The relative higher spatial levels of PCBs associated with urban and industrial areas have also been established in previous studies from the Punjab province (Ali et al. 2014; Mumtaz et al. 2016), and other parts of the world (Toan and Quy 2015). High levels of PCBs in placental tissues from industrial and urban cities reflect their continual exposure to PCB sources in the urban environment (Diamond et al. 2010). Among the PCB homologs in placental tissues, the tetra-PCB was the most dominated homolog, with highest mean concentration observed in samples from Sialkot (50.14 ± 7.72 ng/g (lip. wt.)), followed by Lahore (48.12 ± 10.16 ng/g (lip. wt.)), and Chakwal (45.34 ± 10.12 ng/g (lip. wt.)). Similar distribution pattern was observed for tri-PCB, where Sialkot (8.82 ± 2.08 ng/g (lip. wt.)) and Lahore (7.8 ± 2.34 ng/g (lip. wt.)) have exhibited the highest levels of contamination. However, in the case of penta-PCB, hepta-PCB, and hexaPCB concentrations, the Chakwal has shown the utmost levels of contamination (Fig. 2). In the study area, the Sialkot and Lahore are urban as well as industrial cities having steel production and recycling, surgical tool manufacturing, transformer repairing, old equipment dismantling and maintenance, and metal recovery from e-waste, pigment, and PVC (polyvinyl chloride) industries (Farooq et al. 2011; Eqani et al. 2012a; Syed et al. 2014; Mahmood et al. 2014b; Iqbal et al. 2015), these are possible sources of PCB environmental release. Besides that, coal combustion, oil spills from industrial sites, volatilization from PCB-containing building materials, incineration emissions, and open burning of municipal solid and industrial waste (Chi et al. 2007; Syed et al. 2013; Chakraborty et al. 2016) are also possible sources of PCB human exposure, leading to placental accumulation in mothers from Sialkot and Lahore (Mahmood et al. 2014b). Despite the fact that Chakwal is not an urban city, yet the district hosts large number of cement factories, supplying a substantial portion of the regional cement requirement and the widespread energy crisis in the country encouraged the cement industries to use the tire-derived fuels (TDF) and refusedderived fuels (RDFs) (Cheema and Badshah 2013), possibly emitting the PCBs in the local environment in the absence of any legislative mechanism for PCB emissions control. People
Environ Sci Pollut Res
Fig. 2 Spatial patterns of PCB homologs in placental tissues from five districts of Punjab Province, Pakistan
dwelling adjacent to the cement plants and incinerators are categorized by Agency for Toxic Substances and Disease Registry (ASTDR) as Bspecial population^ which are vulnerable to high level exposure to PCBs as compared to general population (ASTDR 2014). Moreover, in the recent times, co-processing of solid waste and sewage sludge, fly ash and tires in cement industries have been recognized as key sources of PCB environmental emissions (Jin et al. 2017; Richards and Agranovski 2017). At the same time, the area has also been highlighted with traffic congestion by thousands of diesel-operated trucks passing through the Chakwal district each day (Aziz et al. 2014) that may lead to PCB emissions associated with heavy duty vehicular emissions (Laroo et al. 2012). All of these sources exert synergistic effect to local PCB exposure that is also evident from the highest concentrations of certain PCB homologs in placental samples from Chakwal. Whereas, the presence of PCBs in
placental samples from Khanewal and Okara (rural areas) are apparently attributed to semi-volatile nature of PCBs, diffusive gaseous transport and their tendency to travel long distances in the environment which might lead to their abrupt occurrence in rural areas from study area (Gasic et al. 2010; Mahmood et al. 2014b; Syed et al. 2013).
Dioxin-like PCBs Profile distribution of dioxin-like PCBs In total, eight DL-PCBs, including three non-ortho (CB77, 126, and 169) and five mono-ortho (CB-105, 114, 118, 156, and 189) were determined in this study (Table 3). The DL-PCBs exhibit various similar toxicological characteristics as of polychlorinated dibenzo-p-dioxins
Environ Sci Pollut Res Table 3 Mean concentrations of eight dioxin-like and six indicator PCBs in human placental samples (ng/g (lip. wt.)) from five districts of the Punjab Province, Pakistan
PCB congener/class
Lahore
Khanewal
Okara
Sialkot
Chakwal
CB-77 CB-126 CB-169 ∑non-ortho CB-105 CB-114 CB-118 CB-156 CB-189 ∑mono-ortho ∑8DL-PCBs CB-52 CB-101 CB-118 CB-138 CB-153 CB-180 ∑6-indicator PCBs
2.96 0.94 0.84 4.75 1.70 1.48 1.32 0.49 0.72 5.71 10.45 6.88 4.67 1.32 1.55 2.50 1.66 18.59
7.91 0.39 0.44 8.73 0.76 0.56 1.25 0.37 0.21 3.15 11.88 5.86 3.20 1.25 1.11 1.71 0.32 13.45
0.74 0.42 0.21 1.37 2.10 0.30 1.82 0.21 0.27 4.70 6.07 4.12 6.59 1.82 3.30 5.19 0.54 21.55
3.20 0.88 0.56 4.64 1.37 1.13 1.04 0.58 0.54 4.67 9.31 7.22 3.52 1.04 2.08 1.64 0.32 15.82
1.17 0.77 0.75 2.69 3.01 0.99 2.53 0.24 0.47 7.24 9.93 5.86 1.65 2.53 4.32 4.56 1.48 20.40
(PCDDs) and polychlorinated dibenzofurans (PCDFs) due to their structural similarities. The levels of ∑8DL-PCBs in placenta tissues ranged from 2.03 to 27.64 ng/g (lip. wt.), with mean concentration of 9.48 ± 10.9 ng/g (lip. wt.); exhibiting a considerable 11.82% contribution of the total PCBs in placenta tissues. The DL-PCB distribution profile was dominated by CB-77, followed in abundance by CB105 and CB-118. The non-ortho DL-PCBs in placenta contributed prominently in total DL-PCBs with 45.91% of the ∑8DL-PCBs. The noticeable occurrence of non-ortho DLPCB congeners in placental tissues from the region is alarming due to their carcinogenicity; as they possess similar characteristics to the tetrachlorodienzo-p-dioxin (TCDD) (Mahmood et al. 2014a).Similarly, the occurrence of CB-105 and CB-156 indicates the ongoing environmental release of commercial PCBs as both of these congeners are vital ingredients of technical Aroclor mixtures/products (Kim et al. 2009; Malik et al. 2014).
CB-126 and least for CB-156 in maternal placenta tissues. The WHO-TEQ value for ∑ 8 PCBs was calculated as 0.083 ng/g (lip. wt.). The WHO-TEQ values in placental tissues from present study were found to be higher than those from maternal placental samples in Taiwan (0.00291 ng/g (lip. wt.)) and Japan (0.0012 ng/g (lip. wt.)) (Suzukiet al. 2005; Wang et al. 2004).
Estimation of human daily intake of dioxin-like PCBs The magnitude of the maternal health risk associated to body burden of the DL-PCBs exposure was evaluated as estimated daily intake (EDI) using the Eq. (2), established by WHO (1998) and later followed Japanese Environmental Health Committee of the Central Environment Council (EHCCEC 1999) and Finish Department of Environmental Health Table 4 Toxicity equivalency (TEQ) and estimated daily intake (EDI) of dioxin-like PCBs in maternal placental samples
Toxicity equivalency (TEQ) of dioxin-like PCBs
Compound
The toxicological similarities of the DL-PCBs to PCDDs were evaluated through assessment of toxicity equivalence (TEQs) for dioxins using Eq. (1), where BC^ is the DL-PCB congener’s concentration and BTEF^ is the toxicity equivalence factor established by the World Health Organization, International Programme on Chemical Safety (WHO-IPCS) in 2005 (Van den Berg et al. 2006). TEQ ¼ C TEF
ð1Þ
The calculated WHO-TEQs values of three non-ortho and five mono-ortho PCBs are summarized in Table 4. The WHOTEQ values for DL-PCBs were ranged from 1.18 × 10−5 to 0.067 ng/g (lip. wt.), with the highest value evaluated for
WHO 2005– TEF
Non-ortho substituted CB-77 0.0001 CB-126 0.1 CB-169 0.03 Mono-ortho substituted CB-105 0.00003 CB-114 0.00003 CB-118 0.00003 CB-156 0.00003 CB-189 0.00003 ∑8PCBs –
WHO-TEQs (ng/g)
EDI (pg WHOTEQ/kg bw)
3.43 × 10−4
2.69 × 10−6
0.067 0.0162
5.25 × 10−4 1.27 × 10−4
4.96 × 10−5 2.64 × 10−5 4.47 × 10−5 1.18 × 10−5 1.32 × 10−5 0.083
3.90 × 10−7 2.07 × 10−7 3.51 × 10−7 9.27 × 10−8 1.04 × 10−7 6.56 × 10−4
*WHO 2005–TEFs (Van den Berg et al. 2006)
Environ Sci Pollut Res
Infant's Body Weight (Pounds)
8
Products and Environment (COT) (2 pg TEQ/kg bw) (Van Leeuwen et al. 2000; European Commission 2001; WHO/ FAO, 2001; USEPA 2000).
y = -0.0168x + 5.8716 R² = 0.0728
7 6 5
Correlation between placental PCB levels and neonatal anthropometric measures
4 3 2 1 0 0.00
20.00
40.00
60.00
80.00
100.00
120.00
140.00
PCB Concentration (ng/g lip. wt)
Fig. 3 Simple linear regression showing relationship between PCBs in maternal placenta and infants body weight
(Kiviranta 2005). EDI ðng=kg=dayÞ ¼
Body Burden ðng=kg Þ x lnð2Þ ðhalf −lifeÞ x f
ð2Þ
where f is the absorption factor (assumed to be 50%), ln(2) = 0.693, and half-life is assumed to be 7.5 years (EHCCEC 1999). The calculated EDI for DL-PCBs was ranged from 9.27 × −8 10 to 5.25 × 10−4 pg WHO-TEQ/kg bw (body weight); with highest and lowest EDI computed for CB-126 and CB-156, respectively. The mean EDI of ∑8dl-PCBs was found to be 6.56 × 10−4 pg WHO-TEQ/kg bw. The current EDI results were found to be much lower than the tolerable daily intake (TDI) values established by WHO (1–4 pg TEQ/kg bw), The European Union Scientific Committee on Food (EU SCF) (2 pg TEQ/kg bw), Joint FAO/WHO Expert Committee on Food Additives (JECFA) (2.3 pg TEQ/kg bw), United States Environmental Protection Agency (USEPA) (0.001–0.01 pg TEQ/ kg bw), and the UK Committee on Toxicity of Chemicals in Food, Consumer
Conclusions The occurrence, congeners profile, spatial variations, source apportionment, toxicity equivalence (WHO-TEQ), and estimated daily intake (EDI) associated to maternal exposure of PCBs from five districts of Punjab Province, Pakistan, were
60.00 y = -0.0618x + 47.364 R² = 0.068 Infant anthropometric measures (cm)
Fig. 4 Multiple linear regressions showing relationship between PCBs in maternal placenta and infants anthropometric measures
A prenatal POPs exposure had been reported to inhibit fetal growth, resulting in reduced birth weight, crown to heel length, head, mid-arm, and chest circumferences (Dewan et al. 2013; Vafeiadi et al. 2014). The relationship between ∑34PCB concentrations in placental tissues and infant’s anthropometric measures through multiple linear regression (Table S4) have shown a negative correlation of infant’s body weight (R2 = 0.0728) (Fig. 3), crown to heel length (R2 = 0.068), head circumference (R2 = 0.0342), chest circumference (R 2 = 0.0001), and mid arm circumference (R2 = 0.0096) (Fig. 4). These negative correlation findings have reflected neonatal and fetal health effects associated with maternal PCB exposure and its subsequent bioaccumulation. The current decrements in fetal and neonatal growth associated with maternal or/and neonatal PCB concentrations were in consistent to the findings of the previous studies conducted in the USA (Sagivet al. 2007), Europe (Govarts et al. 2012), China (Wu et al. 2011), India (Dewan et al. 2013), Saudi Arabia (Al-Saleh et al. 2012), and Singapore (Tan et al. 2009).
50.00
40.00
y = -0.0219x + 35.026 R² = 0.0342
Crown to Heel Length Head Circumference Chest Circumference
30.00
Mid Arm Circumference
y = -0.0012x + 31.853 R² = 0.0001
Linear (Crown to Heel Length)
20.00
10.00
0.00 0.00
Linear (Head Circumference) Linear (Chest Circumference)
y = -0.0073x + 10.467 R² = 0.0096
20.00
40.00
Linear (Mid Arm Circumference)
60.00
80.00
100.00
PCB Concentration (ng/g lip. wt.)
120.00
140.00
Environ Sci Pollut Res
assessed that they provide a pioneer data for PCBs in placental tissues from South Asian women. Among the PCB congeners, the CB-70 was the most dominant PCB congener, followed in abundance by CB-66 and CB-52. The overall PCB homolog distribution trend in placental tissues from Pakistan were in descending order as tetra-PCB > penta-PCB > hexa-PCB > tri-PCB > hepta-PCB > octa-PCB > deca-PCB. The placental PCB levels from study area were found to be comparable or higher than those assessed in similar studies. The mean Σ34PCB concentration-based spatial profile followed the order as Chakwal > Lahore > Sialkot > Okara > Khanewal, representing relatively higher levels of contamination in urban and industrial cities than the rural towns. The multi-regression analysis has shown reduction in neonatal anthropometric measurements associated with maternal PCB body burden. Thus, at present, the maternal exposure to PCBs in Pakistan exerts risks to neonatal health and detailed human biomonitoring and risk assessment studies are needed to be conducted in the region. The present study also suggests the best pollution control practices and rigid legislative actions to be opted on emergency grounds to prevent PCB future environmental releases to safeguard human health risks. Acknowledgements We express our sincere gratitude to the State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, China for providing support for laboratory analysis.
Compliance with ethical standards The approval of the present study was obtained from Advanced Studies and Research Board (ASRB), University of the Punjab, Pakistan, and written consent was obtained from the subjects, after they were briefed about the purpose of the research.
References Agency for Toxic Substances and Disease Registry (ASTDR) (2014) Case studies in environmental medicine, polychlorinated biphenyls (PCBs) toxicity. Agency for Toxic Substances and Disease Registry, US Department of Health and Human Services, pp 1–90 Ali N, Eqani SAMAS, Malik RN, Neels H, Covaci A (2013) Organohalogenated contaminants (OHCs) in human serum of mothers and children from Pakistan with urban and rural residential settings. Sci Total Environ 461-462:655–662 Ali N, Mehdi T, Malik RN, Eqani SAMAS, Kamal A, Dirtu AC, Neels H, Covaci A (2014) Levels and profile of several classes of organic contaminants in matched indoor dust and serum samples from occupational settings of Pakistan. Environ Pollut 193:269–276 Al-Saleh I, Al-Doush I, Alsabbaheen A, Mohamed GED, Rabbah A (2012) Levels of DDT and its metabolites in placenta, maternal and cord blood and their potential influence on neonatal anthropometric measures. Sci Total Environ 416:62–74 AzizF,SyedJH,MalikRN,KatsoyiannisA,MahmoodA,LiJ,ZhangG,Jones KC (2014) Occurrence of polycyclic aromatic hydrocarbons in the Soan River, Pakistan: insights into distribution, composition, sources and ecological risk assessment. Ecotoxicol Environ Saf 109:77–84
Baqar M, Arslan M, Sadef Y, Mahmood A, Qadir A, Ahmad SR (2017a) Persistent organic pollutants: potential threat to ecological integrities in term of geno-toxicity and oxidative stress. Hum Ecol Risk Assess 23:1249–1271 Baqar M, Mahmood A, Sadef Y, Mahmood A, Ahmad SR, Li J, Zhang G (2017b) Occurrence, ecological risk assessment and spatio-temporal variation of polychlorinated biphenyls (PCBs) in water and sediments along River Ravi and its northern tributaries, Pakistan. Environ Sci Pollut Res 24:27913–27930. https://doi.org/10.1007/ s11356-017-0182-0 Bergonzi R, Specchia C, Dinolfo M, Tomasi C, De Palma G, Frusca T, Apostoli P (2009) Distribution of persistent organochlorine pollutants in maternal and foetal tissues: data from an Italian polluted urban area. Chemosphere 76:747–754 Breivik K, Sweetman A, Pacyna JM, Jones KC (2002) Towards a global historical emission inventory for selected PCB congeners—a mass balance approach: 1. Global production and consumption. Sci Total Environ 290:181–198 Chakraborty P, Zhang G, Li J, Selvaraj S, Breivik K, Jones KC (2016) Soil concentrations, occurrence, sources and estimation of air-soil exchange of polychlorinated biphenyls in Indian cities. Sci Total Environ 562:928–934 Cheema, K., and Badshah, S. (2013) Cement industry, Alternate Fuel and Environmental Benefits. Paper presented at the International Journal of Engineering Research and Technology Chi KH, Chang MB, Kao SJ (2007) Historical trends of PCDD/Fs and dioxin-like PCBs in sediments buried in a reservoir in Northern Taiwan. Chemosphere 68:1733–1740 Chovancová J, Čonka K, Fabišiková A, Sejáková ZS, Dömötörová M, Drobná B, Wimmerová S (2012) PCDD/PCDF, DL-PCB and PBDE serum levels of Slovak general population. Chemosphere 88:1383–1389 Covaci A, Voorspoels S (2005) Optimization of the determination of polybrominateddiphenyl ethers in human serum using solid-phase extraction and gas chromatography-electron capture negative ionization mass spectrometry. J Chromatogr B 827(2):216–223 Covaci A, Hura C, Schepens P (2001) Selected persistent organochlorine pollutants in Romania. Sci Total Environ 280:143–152 Covaci A, Jorens P, Jacquemyn Y, Schepens P (2002) Distribution of PCBs and organochlorine pesticides in umbilical cord and maternal serum. Sci Total Environ 298(1–3):45–53 Dewan P, Jain V, Gupta P, Banerjee BD (2013) Organochlorine pesticide residues in maternal blood, cord blood, placenta, and breastmilk and their relation to birth size. Chemosphere 90:1704–1710 Diamond ML, Melymuk L, Csiszar SA, Robson M (2010) Estimation of PCB stocks, emissions, and urban fate: will our policies reduce concentrations and exposure. Environ Sci Technol 44:2777–2783 Eqani SAMAS, Malik RN, Katsoyiannis A, Zhang G, Chakraborty P, Mohammad A, Jones KC (2012a) Distribution and risk assessment of organochlorine contaminants in surface water from River Chenab, Pakistan. J Environ Monit 14:1645–1654 Eqani SAMAS, Malik RN, Zhang G, Mohammad A, Chakraborty P (2012b) Polychlorinated biphenyls (PCBs) in the sediments of the River Chenab, Pakistan. Chem Ecol 28:327–339 Eqani SAMAS, Malik RN, Zhang G, Cincinelli A, Rasheed A, Qadir A, Bokhari H, Mohammad A, Jones KC, Katsoyiannis A (2013) Uptake of organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) by river water fish: the case of River Chenab. Sci Total Environ 450–451:83–91 European Commission. (2001) Scientific committee on food. Opinion of the scientific committee on food on the risk assessment of dioxins and dioxin-like PCBs in food. Update based on new scientific information available since the adoption of the SCF opinion of 22nd November 2000. CS/CNTM/DIOXIN/20 final, Adopted on 30 May 2001 Farooq S, Eqani SAMAS, Malik RN, Katsoyiannis A, Zhang G, Zhang Y, Li J, Xiang L, Jones KC, Shinwari ZK (2011) Occurrence, finger printing
Environ Sci Pollut Res and ecological risk assessment of polycyclic aromatic hydrocarbons (PAHs) in the Chenab River, Pakistan. J Environ Monit 13:3207–3215 Fernandez MF, Parera J, Arrebola JP, Marina LS, Vrijheid M, Llop S, Abalos M, Tardon A, Castaño A, Abad E, Olea N (2012) Levels of polychlorinated dibenzo-p-dioxins, dibenzofurans and dioxin-like polychlorinated biphenyls in placentas from the Spanish INMA birth cohort study. Sci Total Environ 441:49–56 Fiedler H, Abad E, van Bavel B, de Boer J, Bogdal C, Malisch R (2013) The need for capacity building and first results for the Stockholm Convention Global Monitoring Plan. Trends Anal Chem 46:72–84 Gasic B, MacLeod M, Klanova J, Scheringer M, Ilic P, Lammel G, Pajovic A, Breivik K, Holoubek I, Hungerbühler K (2010) Quantification of sources of PCBs to the atmosphere in urban areas: a comparison of cities in North America, Western Europe and former Yugoslavia. Environ Pollut 158:3230–3235 Gómara B, Athanasiadou M, Quintanilla-López JE, González MJ, Bergman A (2012) Polychlorinated biphenyls and their hydroxylated metabolites in placenta from Madrid mothers. Environ Sci Pollut Res 19:139–147 Govarts E, Nieuwenhuijsen M, Schoeters G, Ballester F, Bloemen K, De Boer M, Chevrier C, Eggesbø M, Guxens M, Krämer U (2012) Birth weight and prenatal exposure to polychlorinated biphenyls (PCBs) and dichlorodiphenyldichloroethylene (DDE): a meta-analysis within 12 European birth cohorts. Environ Health Perspect 120:162–170 Hites RA (2004) Polybrominateddiphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environmental Science & Technology 38:945–956 International Agency for Research on Cancer (IARC) (2016). IARC monographs on the evaluation of carcinogenic risks to humans; polychlorinated biphenyls and polybrominated biphenyls, Volume 107 (2016). International Agency for Research on Cancer, Lyon Iqbal M, Breivik K, Syed JH, Malik RN, Li J, Zhang G, Jones KC (2015) Emerging issue of e-waste in Pakistan: a review of status, research needs and data gaps. Environ Pollut 207:308–318 Japanese Environmental Health Committee of the Central Environment Council (1999). Report on Tolerable Daily Intake (TDI) of Dioxins and Related Compounds (Japan). Available at: https://www.env.go. jp/en/chemi/dioxins/tdi_report.pdf (Accessed on 03-06-2017) Jin R, Zhan J, Liu G, Zhao Y, Zheng M, Yang L, Wang M (2017) Profiles of polychlorinated biphenyls (PCBs) in cement kilns co-processing solid waste. Chemosphere 174:165–172 Kim KS, Lee SC, Kim KH, Shim WJ, Hong SH, Choi KH, Yoon JH, Kim JG (2009) Survey on organochlorine pesticides, PCDD/Fs, dioxinlike PCBs and HCB in sediments from the Han River, Korea. Chemosphere 75:580–587 Kim SK, Yoon J (2014) Chronological trends of emission, environmental level and human exposure of POPs over the last 10 years (1999– 2010) in Korea: implication to science and policy. Sci Total Environ 470–471:1346–1361 Kiviranta, H. (2005). Exposure and human PCDD/F and PCB body burden in Finland. Department of Environmental Health, National Public Health Institute, Kuopio, Finland. Available at: https://core. ac.uk/download/pdf/15167498.pdf (Accessed on 21-07-2017) Kodavanti, P.R.S., Valdez, J., Yang, J.H., Curras-Collazo, M., and Loganathan, B.G. (2017). Chapter 39—polychlorinated biphenyls, polybrominated biphenyls, polychlorinated dibenzo-p-dioxins, and polychlorinated dibenzofurans A2-Gupta, Ramesh C reproductive and developmental toxicology (second edition) (pp. 711–743): Academic Press Laroo CA, Schenk CR, Sanchez LJ, McDonald J, Smith PL (2012) Emissions of PCDD/Fs, PCBs, and PAHs from legacy on-road heavy-duty diesel engines. Chemosphere 89:1287–1294 Leino O, Kiviranta H, Karjalainen AK, Kronberg-Kippilä C, Sinkko H, Larsen EH, Virtanen S, Tuomisto JT (2013) Pollutant concentrations in placenta. Food Chem Toxicol 54:59–69
Letcher RJ, Bustnes JO, Dietz R, Jenssen BM, Jørgensen EH, Sonne C, Verreault J, Vijayan MM, Gabrielsen GW (2010) Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci Total Environ 408:2995–3043 Li J, Zhang G, Guo L, Xu W, Li X, Lee CS, Ding A, Wang T (2007) Organochlorine pesticides in the atmosphere of Guangzhou and Hong Kong: regional sources and long-range atmospheric transport. Atmos Environ 41:3889–3903 Lopez-Espinosa MJ, Granada A, Carreno J, Salvatierra M, Olea-Serrano F, Olea N (2007) Organochlorine pesticides in placentas from southern Spain and some related factors. Placenta 28:631–638 Ma J, Qiu X, Ren A, Jin L, Zhu T (2012) Using placenta to evaluate the polychlorinated biphenyls (PCBs) and polybrominateddiphenyl ethers (PBDEs) exposure of fetus in a region with high prevalence of neural tube defects. Ecotoxicol Environ Saf 86:141–146 Mahmood A, Malik RN, Li J, Zhang G (2014a) Levels, distribution profile, and risk assessment of polychlorinated biphenyls (PCBs) in water and sediment from two tributaries of the River Chenab, Pakistan. Environ Sci Pollut Res 21:7847–7855 Mahmood A, Syed JH, Malik RN, Zheng Q, Cheng Z, Li J, Zhang G (2014b) Polychlorinated biphenyls (PCBs) in air, soil, and cereal crops along the two tributaries of River Chenab, Pakistan: concentrations, distribution, and screening level risk assessment. Sci Total Environ 481:596–604 Malik RN, Mehboob F, Ali U, Katsoyiannis A, Schuster JK, Moeckel C, Jones KC (2014) Organo-halogenated contaminants (OHCs) in the sediments from the Soan River, Pakistan: OHCs (adsorbed TOC) burial flux, status and risk assessment. Sci Total Environ 481:343–351 Mumtaz, M., Mehmood, A., Qadir, A., Mahmood, A., Malik, R.N., Sabir, A.M., Li, J., and Zhang, G. (2016). Polychlorinated biphenyl (PCBs) in rice grains and straw; risk surveillance, congener specific analysis, distribution and source apportionment from selected districts of Punjab Province, Pakistan. Science of the Total Environment, 543, Part A, 620–627 Myllynen P, Pasanen M, Pelkonen O (2005) Human placenta: a human organ for developmental toxicology research and biomonitoring. Placenta 26:361–371 Nanes JA, Xia Y, Dassanayake RMAPS, Jones RM, Li A, Stodgell CJ, Walker C, Szabo S, Leuthner S, Durkin MS, Moye J, Miller RK (2014) Selected persistent organic pollutants in human placental tissue from the United States. Chemosphere 106:20–27 Needham, L.L., Grandjean, P., Heinzow, B., Jørgensen, P.J., Nielsen, F., Patterson, D.G. Jr, Sjödin, A., Turner, W.E., and Weihe, P. (2011). Partition of environmental chemicals between maternal and fetal blood and tissues. Environmental Science Technology, 45, 1121–1126 Porpora MG, Lucchini R, Abballe A, Ingelido AM, Valentini S, Fuggetta E, Cardi V, Ticino A, Marra V, Fulgenzi AR (2013) Placental transfer of persistent organic pollutants: a preliminary study on mothernewborn pairs. Int J Environ Res Public Health 10:699–711 Richards G, Agranovski IE (2017) Dioxin-like PCB emissions from cement kilns during the use of alternative fuels. J Hazard Mater 323: 698–709 Sagiv KS, Tolbert PE, Altshul LM, Korrick SA (2007) Organochlorine exposures during pregnancy and infant size at birth. Epidemiology 18:120–129 Suzuki G, Nakano M, Nakano S (2005) Distribution of PCDDs/PCDFs and Co-PCBs in human maternal blood, cord blood, placenta, milk, and adipose tissue: dioxins showing high toxic equivalency factor accumulate in the placenta. Biosci Biotechnol Biochem 69:1836–1847 Syed JH, Malik RN, Li J, Zhang G, Jones KC (2013) Levels, distribution and air–soil exchange fluxes of polychlorinated biphenyls (PCBs) in the environment of Punjab Province, Pakistan. Ecotoxicol Environ Saf 97:189–195 Syed JH, Malik RN, Li J, Chaemfa C, Zhang G, Jones KC (2014) Status, distribution and ecological risk of organochlorines (OCs) in the
Environ Sci Pollut Res surface sediments from the Ravi River, Pakistan. Sci Total Environ 472:204–211 Tan J, Loganath A, Chong YS, Obbard JP (2009) Exposure to persistent organic pollutants in utero and related maternal characteristics on birth outcomes: a multivariate data analysis approach. Chemosphere 74:428–433 Thomas GO, Wilkinson M, Hodson S, Jones KC (2006) Organohalogen Chemicals in Human Blood from the United Kingdom. Environ Pollut 141:30–41 Toan VD, Quy NP (2015) Residues of polychlorinated biphenyls (PCBs) in sediment from CauBay River and their impacts on agricultural soil, human health risk in KieuKy Area, Vietnam. Bull Environ Contam Toxicol 95:177–182 Tsukimori K, Morokuma S, Hori T, Takahashi K, Hirata T, Otera Y, Fukushima K, Kawamoto T, Wake N (2013) Characterization of placental transfer of polychlorinated dibenzo-p-dioxins, dibenzofurans and polychlorinated biphenyls in normal pregnancy. J Obstet Gynaecol Res 39:83–90 Ullah R, Malik RN, Muhammad A, Ahad K, Tariq M, Asghar R, Qadir A (2016) Higher concentrations and ecological risks of selected persistent organic pollutants in Macrobrachium Lamarrei from the streams of Sialkot, Pakistan. J Agric Sci Technol 6:27–34 United States Environmental Protection Agency (USEPA). (2000). Exposure and human health reassessment of 2,3,7,8tetrachlorodibenzo-p-dioxin and related compounds. Draft final. N a t i o na l Cen t e r f or e nv i r o nm e nt a l a s ses sm e nt , U. S . Environmental Protection Agency, Washington, DC United Nations Environmental Programme (UNEP) (2001) Final act of the conference of plenipotentiaries on the Stockholm convention on persistent organic pollutant. United Nations Environment Program, Geneva http://www.pops.int/default.htm Vafeiadi M, Vrijheid M, Fthenou E, Chalkiadaki G, Rantakokko P, Kiviranta H, Kyrtopoulos SA, Chatzi L, Kogevinas M (2014) Persistent organic pollutants exposure during pregnancy, maternal
gestational weight gain, and birth outcomes in the mother–child cohort in Crete, Greece (RHEA study). Environ Int 64:116–123 Van den Berg M, Birnbaum LS, Denison M, De Vito M, Farland W, Feeley M, Fiedler H, Hakansson H, Hanberg A, Haws L, Rose M, Safe S, Schrenk D, Tohyama C, Tritscher A, Tuomisto J, Tysklind M, Walker N, Peterson RE (2006) The 2005 World Health Organization reevaluation of human and mammaliantoxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 93:223–241 Van Leeuwen FX, Feeley M, Schrenk D, Larsen JC, Farland W, Younes M (2000) Dioxins: WHO’s tolerable daily intake (TDI) revisited. Chemosphere 40:1095–1101 Vizcaino E, Grimalt JO, Fernández-Somoano A, Tardon A (2014) Transport of persistent organic pollutants across the human placenta. Environ Int 65:107–115 Wang SL, Chang YC, Chao HR, Li CM, Li LA, Lin LY, Päpke O (2006) Body burdens of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls and their relations to estrogen metabolism in pregnant women. Environ Health Perspect 114:740–745 Wang SL, Lin CY, Leon Guo Y, Lin LY, Chou WL, Chang LW (2004) Infant exposure to polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls (PCDD/Fs, PCBs)—correlation between prenatal and postnatal exposure. Chemosphere 54:1459–1473 WHO/FAO. 2001. Joint FAO/WHO Expert Committee on Food Additives. Fifty-seventh meeting. Rome, 5–14 June, 2001 World Health Organization (WHO) (1998) Assessment of the health risk of dioxins: reevaluation of the tolerable daily intake TDI. World Health Organization, Geneva, pp 25–29 Wu K, Xu X, Liu J, Guo Y, Huo X (2011) In utero exposure to polychlorinated biphenyls and reduced neonatal physiological development from Guiyu, China. Ecotoxicol Environ Saf 74:2141–2147 Yasmeen H, Qadir A, Mumtaz M, Eqani SAMAS, Syed JH, Mahmood A, Jamil N, Nazar F, Ali H, Ahmad MS, Tanveer ZI, Ahmad MS (2017) Risk profile and health vulnerability of female workers who pick cotton by organanochlorine pesticides from southern Punjab, Pakistan. Environ Toxicol Chem 36:1193–1201
