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Necessity to measure PCBs and organochlorine pesticide concentrations in human umbilical cords for fetal exposure assessment.

Three types of tissue samples--umbilical cord (UC), umbilical cord serum (CS), and maternal serum (MS)--have often been used to assess fetal exposure to chemicals. In order to know the relationship of contamination between mothers and fetuses, we measured persistent chemicals in comparable sets of the three tissue samples. Also, we analyzed the association between the chemicals in maternal and fetal tissues to know which tissue is the best sample for fetal exposure assessment. On a wet basis, the chemical concentrations were of the order MS > CS > UC, except for some chemicals such as cis-chlordane and endosulfan. On a lipid basis, the concentrations in UC were nearly equal or often higher than in MS, but the concentrations in CS were usually lower than in others. Hexachlorocyclohexanes and penta-, hexa-, and heptachlorinated biphenyls showed an association between the concentrations in UC versus MS, and UC versus CS. These chemicals also showed high correlation coefficients between the chemical concentrations in UC of first babies and maternal age. These chemicals were dosely related to each other when grouped on the basis of their concentrations using cluster analysis. In conclusion, we insist that UC is the best sample to assess fetal contamination status of persistent chemicals. There is a possibility that the assessment based on the contamination levels in CS result in an underestimation. Key words: cord blood, maternal blood, organochlorine pesticides, polychlorinated biphenyls (PCBs), umbilical cord. doi:10.1289/ehp.7330 available via http://dx.doLorg/[Online 14 December 2004]

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It is believed that humans are exposed to multiple chemicals from food, air, water, and so forth, including natural products; industrial products, such as polychlorinated biphenyls (PCBs), pesticides, and pharmaceuticals; and nonintentional products, such as dioxins. Human fetuses are exposed to multiple chemicals through placenta in Japan (Mori 2001; Mori et al. 2003; Todaka and Mori 2002), and infants are exposed to these chemicals through milk (Borgert et al. 2003). A number of persistent organochlorine pollutants have been detected in human follicular fluid (De Felip et al. 2004) and amniotic fluid (Foster et al. 2000). Because human fetuses and infants are considered significantly more sensitive to a variety of environmental toxicants compared with adults (Branum et al. 2003; Charnley and Putzrath 2001; Needham and Sexton 2000), the adverse effects of chemicals on these fetuses and infants are of concern.

Three types of tissue samples--umbilical cord (UC), umbilical cord serum (CS), and maternal serum (MS)--have often been used to assess fetal exposure to chemicals. There are several reports indicating that the chemical concentrations were higher in maternal blood than in cord blood (Sarcinelli et al. 2003; Waliszewski et al. 2000; Walker et al. 2003). The assessments using cord blood have suggested fetal contamination. However, the chemical concentrations in fetal tissues are still unclear. There are only a few reports using fetal tissues such as UC (Covaci et al. 2002; Grandjean et al. 2001).

In order to know the relationship of contamination between mothers and fetuses, we measured persistent chemicals in comparable sets of the three tissue samples (UC, CS, and MS). Also, we analyzed the association between the chemicals in maternal and fetal tissues to know which tissue is the best sample for fetal exposure assessment.

Materials and Methods

Sample. Thirty-two pregnant women who were general citizens and lived in the cities of Chiba and Yamanashi, near Tokyo, Japan, were surveyed in 2002 and 2003. UC (- 20 cm), maternal blood (10 mL), and cord blood (10 mL) were collected from the cases delivered by cesarean section. The deliveries were conducted at least 12 hr after the last meal. UC without cord blood and MS and CS were stored at -20[degrees]C until use in glassware that had been checked to be without contamination. In the whole-study subjects, 20 mothers had complete samples (MS, CS, and UC), and their average age at delivery was 32.8 [+ or -] 4.0 years. There were 12 mothers without CS samples, and their average age was 31.9 [+ or -] 4.9 years. In total, 32 cases were used for the analysis of correlation between maternal age and chemical concentrations. This study has been approved by the Congress of Medical Bioethics of Chiba University and the University of Yamanashi, and all the samples were obtained after receipt of written informed consent.

Chemicals measured. We measured 19 organochlorine pesticides: dichlorodiphenyltrichloroethane (DDT) and its metabolites [dichlorodiphenyldichloroethylene (DDE) and dichlorodiphenyldichloroethane (DDD): p,p'-DDT, o,p'-DDT, p,p'-DDE, o,p'-DDE, p,p'-DDD, o,p'-DDD], chlordane and its metabolites (cis-chlordane, trans-chlordane, trans-nonachlor, oxychlordane), heptachlor and its metabolites (heptachlor, heptachlor epoxide), methoxychlor, "drins" (dieldrin, aldrin, endrin), endosulfan isomers (mixture of [alpha]- and [beta]-endosulfan), hexachlorobenzene (HCB), and hexachlorocyclohexane (HCH) isomers (mixture of [alpha]-, [beta]-, [gamma]-, and [delta]-HCH). We also measured 10 groups of PCB congeners grouped by their number of chlorines from 1 to 10.

Pretreatment. MS (4-5 mL), CS (3-4 mL), and UC (17-27 g) were used for the preparation of samples for gas chromatography-mass spectrometry. The details were revealed to the public through the homepage of the Ministry of Environment of the Government of Japan (2002). Briefly, the UC samples were homogenized with ethanol/hexane (1:3) and sodium sulfuric anhydride by a Polytron PT3100 (Kinematica AG, Littau-Lucerne, Switzerland) after 13C12-labeled PCB, [sup.13][C.sub.6]-labeled [beta]-HCH, [sup.13][C.sub.6]-labeled HCB, 13C9-1abeled endosulfan-I, [sup.13][C.sub.12]-labeled pentaCB, and [sup.13][C.sub.12]-1abeled p,p'-DDT had been added as quantitative standards. After filtration, the filtrate and an additional filtrate of the rehomogenate of the residue were washed with water twice. The resulting hexane extract was dehydrated using sodium sulfuric anhydride and concentrated by evaporation. One-sixth of the concentrated extract was used for measurement of PCBs, another sixth for that of organochlorine pesticides, and half for the gravimetric fat determination.

The MS and CS samples were extracted twice using an ether/hexane (3:1) mixture after addition of the quantitative standards. The resulting ether/hexane extract was dehydrated using sodium sulfuric anhydride and concentrated by evaporation (crude extract). A fourth the crude extract was used for measurement of PCBs, and another fourth for organochlorine pesticides.

Measurement of PCBs. After the crude extract was treated with 1 mol/L KOH/ethanol for 18 hr, it was extracted using hexane three times and was concentrated with nitrogen. The concentrate was then eluted through a silica gel 60 column (70-230 ASTM-mesh; Merck, Darmstadt, Germany) with 10 mL hexane, evaporated to a final volume of 0.1 mL, and analyzed after the addition of [sup.13][C.sub.12]-labeled PCB.

PCBs were quantitated by gas chromatography-mass spectrometry. Gas chromatography was performed using a Hewlett Packard HP6800 series equipped with a Micromass AutoSpec Ultima mass spectrometer (Micromass Ltd., Manchester UK). An HT8 fused silica capillary column [0.25 mm inner diameter (i.d.) x 25 m with a 0.33-mm film thickness; SGE International Pty Ltd., Austin, TX, USA] was used to separate each PCB congener. The column temperature was maintained at 100[degrees]C for 2 min, raised to 180[degrees]C at a rate of 5[degrees]C/min, maintained at 180[degrees]C for 0.5 min, raised to 270[degrees]C at a rate of 20[degrees]C/min, then to 300[degrees]C at a rate of 5[degrees]C/min, and finally maintained at 300[degrees]C for 2 rain. The carrier gas (helium) flow rate was 1 mL/min. The ionizing current was 600 [micro]A, the ionizing energy was 38 eV, and the accelerating voltage was 8 kV. The resolution of the mass spectrometer was maintained at approximately > 10,000 (10% valley) throughout, and the analysis was carried out according to selected ion monitoring.

Measurement of organochlorine pesticides. The crude extract was evaporated to a final volume of 0.5 mL and extracted twice with hexane-saturated acetonitrile. The resulting acetonitrile extract was added to water and extracted with hexane twice, then dehydrated using sodium sulfuric anhydride, and evaporated with nitrogen. The concentrate was eluted through a Florisil column (1 g/6 cc, Sep-pak Vac Florisil; Waters, Milford, MA, USA) using 10 mL hexane, evaporated to a final volume of 0.1 mL, and analyzed after the addition of fluoranthene-d10.

Organochlorine pesticides were quantitated by gas chromatography-mass spectrometry in the same manner as for PCBs, except that the column was a BPX-25 fused silica capillary column, 0.22 mm i.d. x 30 m with a 0.25-mm film thickness (SGE International Pty Ltd.). The column temperature was maintained at 60[degrees]C for 1 min, raised to 300[degrees]C at a rate of 10[degrees]C/min, and finally maintained at 300[degrees]C for 10 min.

Lipid contents. Lipid contents in the UC samples were determined gravimetrically, and lipid contents in MS and CS were determined enzymatically as the sum of the total cholesterol, triglycerides, and phospholipids.

Statistical analysis. The statistical analysis was performed using Microsoft Excel 2002 (Microsoft, Redmond, WA, USA). Cluster analysis was performed by the cosine correlation method using GeneMaths software (version 1.50; Applied Maths BVBA, Sint-MartensLatem, Belgium).

Results

Detection rate. Tables 1-4 show the concentration of organochlorine pesticides (Tables 1 and 2) and PCBs (Tables 3 and 4) in the three types of tissues (MS, CS, and UC). It became clear that human fetuses were contaminated with multiple chemicals in Japan. However, o,p'-DDE, o,p'-DDD, aldrin, endrin, and methoxychlor were not detected in any of the tissues in this study. Other chemicals were detected in MS and/or UC, but the detection rate was very low in the CS (Tables 1 and 2). In particular, cis-chlordane, endosulfan, p,p'-DDT, dieldrin, p,p'-DDD, and heptachlor were not detected in CS; however, both were detected in MS (detection rate > 70%) and UC. PCB congeners with five to seven chlorines were detected in all samples, whereas other congeners showed a relatively low detection rate in CS (Tables 3 and 4).

Contamination levels. The highest concentrations found were p,p'-DDE, HCHs, and HCB in all three tissues both on a lipid basis (Table 1) and wet basis (Table 2). Generally, the chemical concentrations on a wet basis were of the order MS > CS > UC. This is due to the difference in lipid content. Lipid content in MS, CS, and UC (20 complete samples) was 0.76 [+ or -] 0.13%, 0.23 [+ or -] 0.04%, and 0.11 [+ or -] 0.02%, respectively. Remarkably, the concentrations of some chemicals in UC on a wet basis, such as cis-chlordane and endosulfan, were almost equal to those in MS (Table 2). On the other hand, on a lipid basis, the concentrations of the following chemicals in UC were nearly equal or often higher than in MS: HCHs, p,p'-DDT, cis-chlordane, trans-chlordane, endosulfan, and heptachlor epoxide (p < 0.001, paired t-test; Table 1). The chemical concentrations in CS were usually lower than in other tissues.

PCB congeners grouped on the basis of their number of chlorines showed different patterns of distribution depending on the number of chlorines. TetraCB and pentaCB concentrations were higher in MS than in UC (p < 0.05, paired t-test), whereas hexaCB and heptaCB concentrations were higher in UC than in MS (p < 0.001, paired t-test) on a lipid basis (Table 3); particularly, heptaCBs and octaCBs showed a high UC:MS ratio. The UC:MS ratio varied according to the number of chlorines in the range of 3-8: UC < MS for congeners with 3-5 chlorines, and UC > MS for congeners with 6-8 chlorines (Table 3). The detection rates of congeners with 1 or 2 chlorines were higher in UC than in MS, whereas those with of 9 or 10 chlorines were higher in MS than in UC. The concentrations (average and median, on a lipid basis) of congeners with 9 or 10 chlorines were higher than those with 1 or 2 chlorines in MS, whereas concentrations of congeners with 1 or 2 chlorines were higher than those with 9 or 10 chlorines in UC. These facts suggest that the accumulation of PCBs in UC is different depending on the number of chlorines; PCB congeners with 1, 2, 6, 7 and 8 chlorines easily accumulate in UC compared with other congeners.

Association between the chemical concentrations among chemicals. We reported that correlation existed between total PCBs and other persistent chemicals, such as p,p'-DDE, HCB, and HCHs, in human UC (Mori et al. 2003). To confirm our previous findings, we applied a cluster analysis technique in the present study. We used the cluster analysis to discover "natural" groupings of objects that reflect evolutionary or functional relationships among the objects; some of the cluster analyses often done in toxicogenomics research have this objective (Immermann and Huang 2003). The cluster analysis was performed using cosine correlation matrix for chemical concentrations in UC for UC, and the clustering results were represented in the dendrogram (Figure 1). Consequently, we found that PCBs with 5-8 chlorines and some organochlorines, such as p,p'-DDE, HCB, and HCHs, were closely related to each other (Figure 1).

[FIGURE 1 OMITTED]

Association between the chemical concentrations among the three types of tissues. Correlation of organochlorine pesticide concentrations among the three types of tissues is shown in Table 5. Some organochlorine pesticides showed no association between MS versus CS and/or between CS versus UC. Between MS versus CS, HCB, HCHs, heptachlor epoxide, and PCBs with chlorines showed a relatively high correlation coefficient (r > 0.7). Between CS versus UC, HCHs, p,p'-DDE, and PCBs with 5-8 chlorines showed relatively high correlation (r > 0.7). Comparing MS and UC, HCHs and PCBs with 4-7 chlorines showed a relatively high correlation coefficient (r > 0.7).

Association between the chemical concentrations in UC and maternal age. Several studies have reported that chemical concentrations were dependent upon maternal age at delivery (Mori et al. 2003; Rhainds et al. 1999). Our present results confirmed that HCHs, pentaCBs, hexaCBs, heptaCBs, and octaCBs showed such correlation (Table 5). A significant correlation was found between CS versus UC and age versus UC (r = 0.75; Table 5). Also, relatively significant correlation was found between MS versus UC and age versus UC (r = 0.64; Table 5). However, we found no correlation between MS versus CS and age versus UC (r = 0.04; Table 5). That is, HCHs, pentaCBs, hexaCBs, and heptaCBs tended to show relatively high association of concentrations in CS versus UC and MS versus UC. Also, these chemicals showed high correlation coefficients between the chemical concentrations in UC of first babies and maternal age.

Discussion

We investigated the distribution of organochlorine pesticides and PCBs in three types of tissues (UC, CS, and MS). We analyzed the chemical contamination status mainly on a lipid basis because the liposolubility rate is thought to be a major factor influenced by rates of accumulation and elimination from tissues and organs (Parham et al. 1997) and because the existing differences depend principally on lipid content of the tissues (Henriksen et al. 1998). Several studies have reported that the concentration levels of persistent chemicals showed association between cord blood and maternal blood (Sala et al. 2001; Waliszewski et al. 2000; Walker et al. 2003). In our study, we found strong correlation between MS versus CS (Table 5) in some organochlorine pesticides and PCB congeners. Also, Grandjean et al. (2001) showed high associations between cord blood and UC. The tendency was confirmed in our study of HCHs, p,p'-DDE, and some PCB congeners (Table 5). However, we found no report that compared the concentration levels among UC, CS, and MS. Hence, we compared the data among these three tissues.

In the present study, we found that the chemical concentrations were often higher in UC than in CS on a lipid basis, and the detection rates and the concentrations in CS were often lower than in MS and UC. In past studies, chemical concentrations were higher in adipose tissues than in serum (Lopez-Carrillo et al, 1999; Pauwels et al. 2000), and in other studies, concentrations were higher in serum lipid than in breast tissues (Waliszewski et al. 2003). Moreover, as suggested by Pauwels et al. (2000), the concentration levels of persistent chemicals varied dramatically depending on the tissues (Tables 1 and 3). One of the reasons for the confusion may be the pharmacokinetics of chemicals in blood. Mohammed et al. (1990) and Noren et al. (1999) reported that chemicals in blood are bound to lipoproteins and albumin rather than being dissolved in lipid, and the distribution in plasma vary according to the chemicals. It is possible that a free form of chemicals is distributed by simple equilibrium, but distribution or transport of bound form of chemicals to protein in blood is more complicated, so the chemical concentration in CS might be lower than in MS and UC. Further studies on the distribution of contaminants in different body tissues and fetal tissues are required.

In conclusion, we believe that UC is the best sample to assess fetal contamination status of persistent chemicals. There is a possibility that assessment based on the contamination levels in CS result in an underestimation.
Table 1. Organochlorine pesticide concentrations (pg/g-lipid) in three
types of tissue.

Organochlorine Detection (a)
pesticide, tissue (%) Mean [+ or -] SD

HCB
 MS 100 15,500 [+ or -] 6,220
 CS 100 10,900 [+ or -] 3,680 **
 UC 95 17,700 [+ or -] 6,360 (##)
HCHs
 MS 100 27,400 [+ or -] 10,630
 CS 100 33,800 [+ or -] 19,300
 UC 100 36,200 [+ or -] 14,920 **
p,p'-DDT
 MS 80 3,380 [+ or -] 3,240
 CS 0 --
 UC 50 5,550 [+ or -] 7,160 **
o,p'-DDT
 MS 15 38 [+ or -] 104
 CS 0 --
 UC 0 --
p,p'-DDE
 MS 100 89,700 [+ or -] 33,600
 CS 100 33,000 [+ or -] 16,500 **
 UC 100 79,600 [+ or -] 26,200 (##)
p,p'-DDD
 MS 85 766 [+ or -] 982
 CS 0 --
 UC 15 215 [+ or -] 527
cis-Chlordane
 MS 100 240 [+ or -] 165
 CS 0 --
 UC 70 1,220 [+ or -] 1,230 **
trans-Chlordane
 MS 95 320 [+ or -] 257
 CS 20 198 [+ or -] 449
 UC 55 644 [+ or -] 848 **
Oxychlordane
 MS 85 2,640 [+ or -] 4,160
 CS 40 978 [+ or -] 1,630
 UC 60 2,120 [+ or -] 2,100
trans-Nonachlor
 MS 100 7,230 [+ or -] 2,840
 CS 80 3,780 [+ or -] 6,470
 UC 100 7,660 [+ or -] 2,580
Dieldrin
 MS 70 495 [+ or -] 454
 CS 0 --
 UC 45 1,970 [+ or -] 3,170 *
Endosulfan
 MS 90 380 [+ or -] 267
 CS 0 --
 UC 70 2,090 [+ or -] 2,440 **
Heptachlor --
 MS 25 150 [+ or -] 272
 CS 0 --
 UC 10 505 [+ or -] 1,620
Heptachlor epoxide
 MS 100 142 [+ or -] 729
 CS 95 1,580 [+ or -] 844
 UC 100 2,790 [+ or -] 1,280 **,(##)

Organochlorine 25th
pesticide, tissue Minimum percentile Median

HCB
 MS 3,600 10,000 16,000
 CS 5,200 8,800 11,000
 UC ND 16,000 18,000
HCHs
 MS 13,000 22,000 26,000
 CS 12,000 24,000 28,000
 UC 18,000 26,000 30,000
p,p'-DDT
 MS ND 1,000 2,400
 CS
 UC ND ND 1,100
o,p'-DDT
 MS ND ND ND
 CS -- -- --
 UC -- -- --
p,p'-DDE
 MS 19,000 71,000 93,000
 CS 14,000 22,000 28,000
 UC 29,000 64,000 78,000
p,p'-DDD
 MS ND 200 360
 CS -- --
 UC ND ND ND
cis-Chlordane
 MS 63 110 200
 CS -- --
 UC ND ND 1,200
trans-Chlordane
 MS ND 160 240
 CS ND ND ND
 UC ND ND 290
Oxychlordane
 MS ND 620 1,200
 CS ND ND ND
 UC ND ND 1,900
trans-Nonachlor
 MS 2,000 5,600 7,000
 CS ND 1,400 1,900
 UC 2,500 6,200 6,700
Dieldrin
 MS ND ND 440
 CS -- -- --
 UC ND ND ND
Endosulfan
 MS ND 280 340
 CS -- -- --
 UC ND ND 1,600
Heptachlor
 MS ND ND ND
 CS -- --
 UC ND ND ND
Heptachlor epoxide
 MS 310 950 1,200
 CS ND 1,100 1,500
 UC 160 2,000 2,700

Organochlorine 75th
pesticide, tissue percentile Maximum

HCB
 MS 17,800 31,000
 CS 12,000 18,000
 UC 20,000 28,000
HCHs
 MS 30,000 55,000
 CS 39,000 100,000
 UC 45,000 69,000
p,p'-DDT
 MS 5,100 11,000
 CS
 UC 9,300 19,000
o,p'-DDT
 MS ND 340
 CS -- --
 UC -- --
p,p'-DDE
 MS 110,000 150,000
 CS 42,000 75,000
 UC 90,000 140,000
p,p'-DDD
 MS 950 3,800
 CS -- --
 UC ND 1,600
cis-Chlordane
 MS 330 660
 CS -- --
 UC 1,700 4,400
trans-Chlordane
 MS 430 1,200
 CS ND 1,400
 UC 1,200 3,000
Oxychlordane
 MS 3,900 19,000
 CS 1,600 6,300
 UC 3,700 6,100
trans-Nonachlor
 MS 9,000 14,000
 CS 3,800 30,000
 UC 8,300 14,000
Dieldrin
 MS 770 1,600
 CS -- --
 UC 2,200 9,600
Endosulfan
 MS 460 1,100
 CS -- --
 UC 2,900 9,400
Heptachlor
 MS 100 700
 CS -- --
 UC ND 6,500
Heptachlor epoxide
 MS 1,700 3,000
 CS 1,900 3,400
 UC 3,500 6,000

ND, not detected.

* Detection rate is shown as a percentage (n = 20). * p < 0.05 and
** p < 0.001 compared with MS. (##) p < 0.001 compared with CS.

Table 2. Organochlorine pesticide concentrations (pg/g-wet) in three
types of tissue.

Organochlorine Detection (a)
pesticide, tissue (%) Mean [+ or -] SD

HCB
 MS 100 120 [+ or -] 55.2
 CS 100 23.9 [+ or -] 8.42 **
 UC 95 19.6 [+ or -] 6.52 **
HCHs
 MS 100 208 [+ or -] 84.7
 CS 100 74.5 [+ or -] 39.3 **
 UC 100 39.8 [+ or -] 7.8 **,(##)
pp'-DDT
 MS 80 26.40 [+ or -] 26.5
 CS 0 --
 UC 50 5.76 [+ or -] 7.53 *
op'-DDT
 MS 15 0.32 [+ or -] 0.89
 CS 0 --
 UC 0 --
pp'-DDE
 MS 100 680.0 [+ or -] 277
 CS 100 71.9 [+ or -] 30.7 **
 UC 100 86.5 [+ or -] 26.1 **,(#)
pp'-DDD
 MS 85 6.11 [+ or -] 7.99
 CS 0 --
 UC 15 0.26 [+ or -] 0.63
cis-Chlordane
 MS 100 1.81 [+ or -] 1.25
 CS 0 --
 UC 70 1.20 [+ or -] 1.19
trans-Chlordane
 MS 95 2.46 [+ or -] 2.45
 CS 20 0.41 [+ or -] 0.90
 UC 55 0.68 [+ or -] 0.91 *
Oxychlordane
 MS 85 22.80 [+ or -] 45.4
 CS 40 2.19 [+ or -] 3.45
 UC 60 2.48 [+ or -] 2.50
trans-Nonachlor
 MS 100 55.00 [+ or -] 23.2
 CS 80 8.02 [+ or -] 12.1 **
 UC 100 8.52 [+ or -] 3.17 **
Dieldrin
 MS 70 3.75 [+ or -] 3.30
 CS 0 --
 UC 45 2.02 [+ or -] 3.01
Endosulfan
 MS 90 2.90 [+ or -] 2.07
 CS 0 --
 UC 70 2.83 [+ or -] 2.61
Heptachlor
 MS 25 1.44 [+ or -] 2.58
 CS 0 --
 UC 10 0.57 [+ or -] 1.82
Heptachlor epoxide
 MS 100 10.70 [+ or -] 5.67
 CS 95 3.51 [+ or -] 1.80 **
 UC 100 2.89 [+ or -] 1.03 **

Organochlorine 25th
pesticide, tissue Minimum percentile Median

HCB
 MS 20 81 120
 CS 13 20 23
 UC ND 17 20
HCHs
 MS 100 160 190
 CS 33 49 70
 UC 17 29 35
pp'-DDT
 MS ND 8.0 17
 CS -- -- --
 UC ND ND 1.0
op'-DDT
 MS ND ND ND
 CS -- -- --
 UC -- -- --
pp'-DDE
 MS 190 480 640
 CS 26 50 72
 UC 31 76 88
pp'-DDD
 MS ND 1.6 2.7
 CS -- -- --
 UC ND ND ND
cis-Chlordane
 MS 0.54 0.70 1.3
 CS -- -- --
 UC ND ND 1.1
trans-Chlordane
 MS ND 1.2 1.9
 CS ND ND ND
 UC ND ND 0.25
Oxychlordane
 MS ND 4.9 11
 CS ND ND ND
 UC ND ND 2.3
trans-Nonachlor
 MS 15 38 53
 CS ND 3.1 4.3
 UC 2.9 6.8 7.9
Dieldrin
 MS ND ND 3.4
 CS -- -- --
 UC ND ND 2.7
Endosulfan
 MS ND 2 2.6
 CS -- -- --
 UC ND ND 1.9
Heptachlor
 MS ND ND ND
 CS -- -- --
 UC ND ND ND
Heptachlor epoxide
 MS 2.3 6.9 9
 CS ND 2.4 3.3
 UC 0.3 2.2 3.1

Organochlorine 75th
pesticide, tissue percentile Maximum

HCB
 MS 140 230
 CS 25 46
 UC 23 33
HCHs
 MS 240 430
 CS 82 190
 UC 48 95
pp'-DDT
 MS 42 90
 CS -- --
 UC 11 27
op'-DDT
 MS ND 3
 CS -- --
 UC -- --
pp'-DDE
 MS 900 1,200
 CS 95 130
 UC 94 150
pp'-DDD
 MS 7.1 30
 CS -- --
 UC ND 2.1
cis-Chlordane
 MS 2.6 4.8
 CS -- --
 UC 2.0 4.4
trans-Chlordane
 MS 3.1 12
 CS ND 2.9
 UC 1.1 2.9
Oxychlordane
 MS 24 210
 CS 3.6 12
 UC 4.5 6.9
trans-Nonachlor
 MS 68 100
 CS 9.7 56
 UC 10.3 17
Dieldrin
 MS 5.9 10
 CS -- --
 UC 2.6 8.5
Endosulfan
 MS 3.9 8.4
 CS -- --
 UC 3.3 10
Heptachlor
 MS 1.2 7.2
 CS -- --
 UC ND 7.2
Heptachlor epoxide
 MS 13 24
 CS 4.2 7.3
 UC 3.5 5.1

ND, not detected.

(a) Detection rate is shown as a percentage (n = 20). * p < 0.05
and ** p < 0.001 compared with MS. (#) p < 0.05 and (##) p < 0.001
compared with CS.

Table 3. PCB concentrations (pg/g-lipid) in three types of tissue.

 Detection (a)
PCB, tissue (%) Mean [+ or -] SD Minimum

MonoCBs
 MS 25 8.4 [+ or -] 30.5 ND
 CS 0 -- --
 UC 95 480 [+ or -] 405 * ND
DiCBs
 MS 70 44 [+ or -] 37 ND
 CS 0 -- --
 UC 80 354 [+ or -] 276 ** ND
TriCBs
 MS 100 1,630 [+ or -] 639 720
 CS 65 1,630 [+ or -] 1770 ND
 UC 90 1,210 [+ or -] 977 ND
TetraCBs
 MS 100 7,000 [+ or -] 2120 4,000
 CS 95 4,360 [+ or -] 3750 ** ND
 UC 95 3,190 [+ or -] 2,200 ** ND
PentaCBs
 MS 100 15,000 [+ or -] 4,630 7,700
 CS 100 12,700 [+ or -] 6,080 ** 3,700
 UC 100 13,200 [+ or -] 6,100 * 5,100
HexaCBs
 MS 100 25,600 [+ or -] 8,410 11,000
 CS 100 31,200 [+ or -] 11,000 ** 14,000
 UC 100 32,600 [+ or -] 12,000 ** 13,000
HeptaCBs
 MS 100 9,640 [+ or -] 3,610 3,900
 CS 100 12,300 [+ or -] 5,420 ** 3,500
 UC 100 15,200 [+ or -] 5,860 **,(##) 7,700
OctaCBs
 MS 100 1,750 [+ or -] 718 590
 CS 75 1,700 [+ or -] 1,380 ND
 UC 100 3,130 [+ or -] 1,360 **,(##) 1,700
NonaCBs
 MS 70 212 [+ or -] 174 ND
 CS 35 146 [+ or -] 291 ND
 UC 50 148 [+ or -] 221 ND
DecaCBs
 MS 85 114 [+ or -] 65 ND
 CS 35 130 [+ or -] 257 ND
 UC 55 148 [+ or -] 173 * ND
Total PCBs
 MS 100 61,500 [+ or -] 18,400 29,000
 CS 100 63,800 [+ or -] 23,300 31,000
 UC 100 70,000 [+ or -] 26,100 *,(#) 34,000

 25th 75th
PCB, tissue percentile Median percentile Maximum

MonoCBs
 MS ND ND 28 110
 CS -- -- -- --
 UC 100 470 640 1,400
DiCBs
 MS ND 44 67 120
 CS -- -- -- --
 UC 220 370 450 1,200
TriCBs
 MS 1200 1400 2,000 2,900
 CS ND 1,500 2,200 6,700
 UC 560 1100 1,800 3,900
TetraCBs
 MS 7,400 7,100 8,000 12,000
 CS 1,800 3,300 5,600 14,000
 UC 2,100 3,000 4,000 10,000
PentaCBs
 MS 11,000 15,000 18,000 25,000
 CS 8,000 13,000 17,000 24,000
 UC 7,900 12,000 18,000 25,000
HexaCBs
 MS 20,000 26,000 30,000 42,000
 CS 23,000 31,000 38,000 51,000
 UC 24,000 35,000 40,000 53,000
HeptaCBs
 MS 7,400 8,600 12,000 17,000
 CS 8,000 12,000 13,500 23,000
 UC 11,000 14,000 20,000 29,000
OctaCBs
 MS 1,500 1,800 2,500 3,100
 CS 830 1,400 2,600 4,400
 UC 2,100 2,700 3,900 5,900
NonaCBs
 MS ND 220 290 530
 CS ND ND 200 1,200
 UC ND 60 210 910
DecaCBs
 MS 91 115 150 240
 CS ND ND 220 1,100
 UC ND 96 255 570
Total PCBs
 MS 46,000 61,000 72,000 96,000
 CS 44,000 63,000 77,000 110,000
 UC 47,000 73,000 88,000 130,000

ND, not detected.

(a) Detection rate is shown as a percentage (n = 20). * p < 0.05
and ** p < 0.001 compared with MS. (#) p < 0.05 and (##) p < 0.001
compared with CS.

Table 4. PCB concentrations (a) (pg/g-wet) in three types of tissue.

 Detection (a)
PCB, tissue (%) Mean [+ or -] SD Minimum

MonoCBs
 MS 25 0.10 [+ or -] 0.21 ND
 CS 0 -- --
 UC 95 0.52 [+ or -] 0.47 ND
DiCBs
 MS 70 8.65 [+ or -] 0.28 ND
 CS 0 -- --
 UC 80 0.38 [+ or -] 0.30 ND
TriCBs
 MS 100 13.0 [+ or -] 6.14 6.1
 CS 65 3.78 [+ or -] 4.42 ** ND
 UC 90 1.38 [+ or -] 1.15 **, (#) ND
TetraCBs
 MS 100 53.2 [+ or -] 17.75 22
 CS 95 9.59 [+ or -] 8.32 ** ND
 UC 95 3.69 [+ or -] 3.13 **, (##) ND
PentaCBs
 MS 100 115 [+ or -] 42.3 51
 CS 100 27.5 [+ or -] 12.8 ** 8.6
 UC 100 14.6 [+ or -] 7.54 **, (##) 5.2
HexaCBs
 MS 100 195 [+ or -] 68.4 90
 CS 100 69.3 [+ or -] 25.9 ** 26
 UC 100 36.1 [+ or -] 15.3 **, (##) 16
HeptaCBs
 MS 100 73.3 [+ or -] 26.7 34
 CS 100 27.9 [+ or -] 13.8 ** 6.2
 UC 100 17.1 [+ or -] 8.26 **, (##) 8.6
OctaCBs
 MS 100 14.5 [+ or -] 5.57 4.6
 CS 75 4.03 [+ or -] 3.96 ** ND
 UC 100 3.57 [+ or -] 1.86 **, (#) 1.4
NonaCBs
 MS 70 1.54 [+ or -] 1.26 ND
 CS 35 0.32 [+ or -] 0.64 ND
 UC 50 0.17 * [+ or -] 0.27 * ND
DecaCBs
 MS 85 0.87 [+ or -] 0.50 ND
 CS 35 0.29 [+ or -] 0.58 ND
 UC 55 0.18 [+ or -] 0.23 ** ND
Total PCBs
 MS 100 467 [+ or -] 154 220
 CS 100 139 [+ or -] 56.4 ** 56
 UC 100 77.4 [+ or -] 35.5 **, (##) 35

 25th 75th
PCB, tissue percentile Median percentile Maximum

MonoCBs
 MS ND ND 0.02 0.68
 CS -- -- -- --
 UC 0.16 0.36 0.82 1.7
DiCBs
 MS ND 0.35 0.52 0.89
 CS -- -- -- --
 UC 0.24 0.36 0.50 1.2
TriCBs
 MS 8.5 10 15 31
 CS ND 3.6 4.8 17
 UC 0.45 1.3 1.8 4.4
TetraCBs
 MS 40 50 65 91
 CS 4.2 6.9 13 35
 UC 2.4 2.9 4.5 15
PentaCBs
 MS 81 110 140 190
 CS 19 26 34 54
 UC 10 13 18 37
HexaCBs
 MS 140 210 240 340
 CS 51 68 88 130
 UC 26 35 43 78
HeptaCBs
 MS 55 73 94 120
 CS 19 26 32 61
 UC 12 16 20 43
OctaCBs
 MS 11 15 18 26
 CS 1.4 3.4 5.1 16
 UC 2.1 3.4 4.3 8.3
NonaCBs
 MS ND 1.6 2.5 3.8
 CS ND ND 0.52 2.7
 UC ND 0.065 0.26 1.1
DecaCBs
 MS 0.73 0.86 1.0 1.7
 CS ND ND 0.49 2.5
 UC ND 0.094 0.33 0.85
Total PCBs
 MS 340 490 570 780
 CS 100 130 180 270
 UC 57 73 91 190

ND, not detected.

(a) Detection rate is shown as a percentage (n = 20).
* p < 0.05 and ** p < 0.001 compared with MS.
(#) p < 0.05 and (##) p < 0.001 compared with CS.

Table 5. Correlation coefficients (r) of chemicals among tissues
and between maternal age and chemical concentrations in UC of
first babies.

 Between
 maternal
 age and
 concentrations
 Among tissues (a) in UC of first
 babies
 MS vs. CS CS vs. UC MS vs. UC (age vs. UC)

HCB 0.73 0.30 0.39 -0.16
HCHs 0.72 0.76 0.80 0.83
p,p'-DDE 0.46 0.76 0.29 0.28
cis-Chlordane -- -- 0.03 -0.02
trans-Nonachlor 0.18 0.20 0.11 0.47
Endosulfan -- -- 0.19 -0.20
Heptachlor epoxide 0.72 0.22 0.02 0.10
TriCBs -- -- 0.35 -0.03
TetraCBs 0.51 0.41 0.73 0.37
PentaCBs 0.83 0.89 0.84 0.75
HexaCBs 0.87 0.87 0.82 0.76
HeptaCBs 0.68 0.85 0.72 0.85
OctaCBs 0.32 0.70 0.47 0.81
NonaCBs -- -- -0.25 --
DecaCBs -- -- 0.40 --
Total PCBs 0.82 0.82 0.81 0.80
Correlation 0.04 0.75 0.64 --
 coefficients
 (r) (b)
 between "among
 tissues" and
 age vs. UC

--, not calculated.

(a) The values shown were calculated when the detection rate
in the tissue was [greater than or equal to] 70%.
(b) Total PCBs were excluded from this calculation.


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Hideki Fukata, (1,2) Mariko Omori, (1,2,3,4) Hisao Osada, (2,5) Emiko Todaka, (2,4,6) and Chisato Mori (2,4)

(1) Department of Environmental Medical Science, (2) Environmental Health Science Project for Future Generations, (3) Department of Reproductive Medicine, and (4) Department of Bioenvironmental Medicine, Graduate School of Medicine, Chiba University, Chiba, Japan; (5) Department of Obstetrics and Gynecology, Chiba University Hospital, Chiba, Japan; (6) Center for Environment, Health and Field Sciences, Chiba University, Kashiwa, Japan

Address correspondence to C. Mori, Department of Bioenvironmental Medicine, Graduate School of Medicine, Chiba University, Chiba 260-8670 Japan. Telephone: 81-43-226-2017. Fax: 81-43-226-2018. E-mail: cmori@faculty.chiba-u.jp

This work was supported by grants from the Ministry of the Environment (Government of Japan) and the Ministry of Education, Culture, Sports, Science and Technology (Government of Japan).

Received 16 June 2004; accepted 14 December 2004.
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Date:Mar 1, 2005
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