DSpace at VNU: Kinetic differences of legacy organochlorine pesticides and polychlorinated biphenyls in Vietnamese human breast milk

Chemosphere 81 (2010) 1006–1011 Contents lists available at ScienceDirect Chemosphere journal homepage: www.elsevier.com/locate/chemosphere Kinetic differences of legacy organochlorine pesticides and polychlorinated biphenyls in Vietnamese human breast milk Nguyen Minh Tue a, Agus Sudaryanto b, Tu Binh Minh c, Bui Hong Nhat c, Tomohiko Isobe b, Shin Takahashi a, Pham Hung Viet c, Shinsuke Tanabe a,⇑ a b c Center for Marine Environmental Studies, Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japan Senior Research Fellow Center, Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japan Centre for Environmental Technology and Sustainable Development, Hanoi University of Science, 334 Nguyen Trai, Hanoi, Viet Nam a r t i c l e i n f o Article history: Received February 2010 Received in revised form 28 July 2010 Accepted September 2010 Available online 25 September 2010 Keywords: Breast milk Depuration POPs Temporal trend Vietnam a b s t r a c t The present study investigated the current contamination status and evaluated several kinetic-related features of organochlorine pesticides (OCPs) and PCBs in human breast milk collected from northern Vietnam The variation in the levels of these contaminants was found to be strongly associated with total lactation time and dietary habits OCPs exhibited the characteristics of steadily declining compounds: the overall levels of DDTs and HCHs in the population decreased with a half-time of only years and it can be suggested that OCPs depurated relatively fast with breastfeeding (5% per month) PCBs were slower in both regards, with a temporal decrease half-time of 12 years and a suggested depuration rate via breastfeeding of 2.5% per month, indicating that the exposure level was still high relative to the human body burden It was found that the PCB exposure levels of infant from breastfeeding exceeded the reference dose, and this situation may continue for the next two or three decades Knowledge of these kinetic-related characteristics not only is useful for risk assessment and prediction of future trends of legacy contaminants but also may provide insight regarding similar kinetic processes of emerging persistent pollutants Ó 2010 Elsevier Ltd All rights reserved Introduction Worldwide production and intensive use of organochlorine compounds (OCs), including organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs), has resulted in their widespread contamination These compounds have received considerable attention in the late decades of the last century with regard to their persistence, bioaccumulative characteristics, long-range transport and long-term toxic effects to human (ATSDR, 2000, 2002) Despite the global declining trends of OCs in recent years (Norén and Meironyté, 2000; Schecter et al., 2005; Jaraczewska et al., 2006; Kunisue et al., 2006; Lignell et al., 2009), elevated levels of OCPs were still observed in human breast milk from Asian developing countries due to a later phase-out than in developed countries, suggesting further monitoring is necessary (Kunisue et al., 2004; Minh et al., 2004; Sudaryanto et al., 2006; Subramanian et al., 2007) Vietnam was reported to be among the countries with the highest levels of dichlorodiphenyltrichloroethane and its metabolites (DDTs) and unlike other Asian developing countries also had relatively high levels of PCBs (Minh et al., 2004) because of the extensive use of ⇑ Corresponding author Tel./fax: +81 89 927 8171 E-mail address: shinsuke@agr.ehime-u.ac.jp (S Tanabe) 0045-6535/$ - see front matter Ó 2010 Elsevier Ltd All rights reserved doi:10.1016/j.chemosphere.2010.09.013 OCPs in agriculture and imported PCB-contaminated transformer oil before their ban in 1995 (Minh et al., 2008) Breast milk is a convenient matrix for monitoring persistent organic pollutants (POPs) in human The advantages include simple and non-invasive sample collection, suitability for determination of lipophilic POPs due to the relatively rich lipid content, and relevance with regard to the exposure of breastfeeding infants, who are at the early stage of development and vulnerable to toxic contaminants However, due to the transfer of the mother’s body burden to the infant through breastfeeding (Carrizo et al., 2007; Shen et al., 2007; Trapp et al., 2008), the contamination levels in female donors may vary with lactation time Indeed, the levels of legacy POPs such as OCs in mother’s milk have been reported to decrease with the number of children (Minh et al., 2004; Fürst, 2006; Kunisue et al., 2006; Sudaryanto et al., 2006) Recent monitoring studies have been designed to avoid the variation by sampling milk from only primiparae within 3–8 weeks post-partum (WHO, 2005) With this approach, it is difficult however to make a direct comparison with data from past references and the survey is also more difficult to coordinate, especially in developing countries where health assessment frameworks are scarce There have been studies aiming to quantify the variation due to lactation, either by temporal monitoring of the compounds in individual donors (Schecter et al., 1998; N.M Tue et al / Chemosphere 81 (2010) 1006–1011 Hooper et al., 2007) or by using mathematical models (Trapp et al., 2008) Together, these studies indicate that the observed depuration kinetic of POPs during the lactation period varies for different compounds and suggest an important influence of human intake level This influence may explain the lack of significant difference in the breast milk levels of emerging POPs such as polybrominated diphenyl ethers (PBDEs) between primiparae and multiparae mothers (Schecter et al., 2003; Tue et al., 2010) Consequently, while the depuration kinetics of legacy and emerging POPs through breastfeeding may be similar, investigating the former has the advantage because their human intake levels are low relative to the body burden The present study investigated the current contamination status of legacy OCPs and PCBs in northern Vietnamese human breast milk and assessed their different kinetic-related characteristics, specifically the relationship between OC levels and lactation time as well as the connection of this relationship to the declining trend of the compound An up-to-date assessment of infant health risk from OCs in mother’s milk was also conducted Material and methods 2.1 Sample collection Breast milk samples (n = 33) were collected between August and September 2007 from Hanoi, the capital city of Vietnam and its surrounding suburban and rural areas All donors were nonsmokers, non-drinkers and appeared healthy The samples were collected by the donors or with the help of a midwife and placed in solvent-pre-cleaned analytical-grade glass containers with Teflon-lined screw caps and kept in gel ice Informed consents were obtained from all donors Questionnaires were also used to acquire information on age, height and weight measurements, number of deliveries, detailed history of breastfeeding, occupation and dietary habit General information on the donors are summarised in Table After collection the samples were kept with ice and sent within h to the Centre for Environmental Technology and Sustainable Development (Hanoi University of Science, Hanoi, Vietnam) to store at À20 °C The frozen samples were later air-transported with gel ice to the Environmental Specimen Bank (es-BANK, Ehime University, Japan) and stored at À25 °C until analysis Table General characteristics of the donors of breast milk Parameters Urban (n = 14) Suburban/rural (n = 19) Age (year) Weight (kg) Height (cm) BMI (kg mÀ2) 23–35 (28.0) 46–62 (53.0) 155–167 (160) 16.4–25.4 (19.9) 1–2 (1.6) 0.57–12 (4.5) 4.5–25 (10.0) 18–35 (25.5) 40–52 (45.0) 150–159 (155) 16.7–21.6 (19.1) 4–14 (8) 2–14 (6) 1–7 (3) 2.3–7.3 (4.4) 86% office worker 14% housewife 0–14 (6) 0–8 (3) 0–1 (0) 1.2–6.4 (3.1) 37% farmer, 26% housewife 37% other Number of children Nursing period (last child, month) Total nursing period (all children, month) Food consumption (servings per week) Meat and meat products Fish Milk and dairy products Breast milk lipid content (%) Occupation Values between parentheses are medians 1–4 (1.8) 0.43–12 (7.3) 1.3–57 (18.6) 1007 2.2 Chemical analyses Analysis of OCs followed the method described by Minh et al (2004) Briefly, approximately 10 g of sample was applied to a glass column containing 10 g of pre-cleaned diatomaceous earth (EXtrelutÒ NT, Merck, Germany), kept for 30 and then extracted with 250 ml diethyl ether The extract was dried over anhydrous sodium sulphate then concentrated and solvent-exchanged into hexane A portion of this extract (25% in volume) was used for gravimetric determination of lipid content The remaining extract was subjected to gel permeation chromatography (packed Bio-Bead S-X 3, Bio-Rad Laboratories, USA) for lipid removal using a dichloromethane (DCM)/hexane mixture (1:1 v/v) as eluant The lipid-free extract was then concentrated and passed through a 12 g of activated Florisil (Florisil PR, Wako, USA) packed in a glass column for final clean-up and separation The first fraction, eluted with hexane, contained PCBs, hexachlorobenzene (HCB), trans-nonaclor and p,p0 -DDE while the second fraction, eluted with 20% DCM in hexane, contained hexachlorocyclohexane isomers (HCHs), chlordane compounds (CHLs: oxychlordane, trans- and cis-chlordanes, trans- and cis-nonachlors) and DDTs (p,p0 -DDT, -DDE and -DDD) Quantification with external standards was carried out using a GC-ECD (Agilent 6890 series) equipped with an auto-injector (Agilent 7683 series) and a DB-1 fused silica capillary column (0.25 mm i.d  0.25 lm film thickness  30 m length, J&W Scientific, USA) The external standard for PCBs was an equivalent mixture of 62 PCB congeners (BP-MS, Wellington Laboratories, Canada) A procedural blank was analysed simultaneously with every series of five samples to check for interference and contamination Recoveries throughout the procedure (n = 5) were 99.1 ± 5.5% for DDTs, 95.7 ± 5.5% for PCBs, 94.1 ± 3.7% for HCHs, 92.6 ± 7.2% for HCB and 98.6 ± 6.5% for CHLs Relative standard deviations (n = 3) for the analysis of a pooled milk sample were less than 15% for HCHs and less than 10% for other OCs Further details on quantification and quality assurance have been described previously (Minh et al., 2004) Concentrations were not recovery-corrected and were expressed on a lipid weight basis unless otherwise specified 2.3 Data analyses The Wilcoxon rank sum test was used for assessing whether the contaminant levels between groups were significantly different For this analysis, non-detectable levels were set to zero Possible associations between levels of contaminants and sociodemographic parameters were examined using multiple linear regressions Compounds detected in less than 80% of the samples were not examined Non-detectable levels were set to half of the detection limit and then all levels were log-transformed (base 10) to bring the data distribution closer to normality The parameters used as independent variables included age, body mass index (BMI), total lactation time, and consumption of food from animal origin (total frequency for meat, fish and dairy products) Parity was not included in the models due to a strong correlation with lactation time (Spearman’s q = 0.86, p < 0.001) Parameters with a p-value of more than 0.1 were removed from the model; those with p < 0.05 were considered as having significant relationship with level of the contaminant All calculations were performed using the statistical software package R (R Foundation for Statistical Computing, Vienna, Austria) version 2.9.2 First-order kinetics were assumed for both the depuration of OCs in individual mother’s milk through breastfeeding and the long-term decline of OCs in the population This kinetic can be expressed using the following logarithmic equation: log10 C ẳ log10 C kt 1ị 1008 N.M Tue et al / Chemosphere 81 (2010) 1006–1011 where C1 and C2 are the OC levels at the beginning and the end of the time interval t, respectively and k is the first-order decrease rate constant A decrease half-time can be derived as tdec1/2 = log102/k Results and discussion 3.1 Contamination levels and patterns DDT compounds were the predominant organochlorine contaminants in Vietnamese human breast milk The total levels of p,p0 -DDT and its metabolites were an order of magnitude higher than total PCB levels (Table 2) Other OCPs followed a pattern of HCHs > HCB > CHLs The levels of CHLs were low; oxychlordane, trans- and cis-nonachlor were not detected in 27%, 39% and 21% of the samples, respectively These results may reflect the usage pattern of OCPs in Vietnam, as the usage of HCB and CHLs was very limited compared with other countries (Minh et al., 2004) As seen in Table 2, donors living in the city had significantly higher levels of OCs than those living in suburban and rural areas Specifically, only p,p0 -DDE, b-HCH and several highly chlorinated PCB congeners (CB-138, -153 and -180) accumulated at substantially higher levels in urban donors These compounds are the predominant and more persistent of their respective groups Thus their elevated relative abundance suggests a long accumulation history rather than a recent exposure Indeed, the proportions of the main ingredients of pesticides technical mixtures, p,p0 -DDT and a-HCH, within their groups of compounds were only 1.3– 8.5% (median 3.1%) and