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Keywords:

  • Transplacental transfer;
  • Beluga;
  • Partitioning;
  • PCBs;
  • PBDEs

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. Acknowledgements
  7. REFERENCES

This study found that arctic beluga whales (Delphinapterus leucas) transferred, on average, 11.4% (7.5 mg) and 11.1% (0.1 mg) of their polychlorinated biphenyl (PCB) and polybrominated diphenyl ether (PBDE) blubber burden to their near-term fetuses. A single physicochemical parameter, log KOW, largely explained this transplacental transfer for PCBs (r2 = 0.79, p < 0.00001) and PBDEs (r2 = 0.37, p = 0.007), with congeners having a log KOW < 6.5 preferentially transferred to the fetus. Blubber concentrations of 257 ng/g lipid weight (lw) PCBs and 3.8 ng/g (lw) PBDEs in beluga fetuses highlights the exposure to endocrine-disrupting compounds during a critical developmental stage. The implications of detecting these levels of legacy PCBs and the flame retardant PBDEs in unborn arctic beluga are unclear. Environ. Toxicol. Chem. 2012;31:296–300. © 2011 SETAC


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. Acknowledgements
  7. REFERENCES

Persistent organic pollutants (POPs) such as polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) are ubiquitous in the environment and have a well-documented propensity to biomagnify in marine food webs 1. Many marine mammals accumulate high levels of POPs, reflecting their often long lives, high trophic levels within aquatic food webs, and inability to readily eliminate these compounds. Exposure to lipophilic contaminants has been linked to immune dysfunction and neurotoxicity as well as disruption of endocrine and reproductive systems in marine mammals 2, 3.

Persistent organic pollutants are transferred from females to their offspring during gestation and lactation, thus exposing neonates to some of the highest levels of these endocrine-disrupting compounds they will encounter during their lifetime 4. While considerable variability occurs in the degree to which POPs are transferred from female to offspring among species, lactational transfer in mammals during nursing commonly accounts for more than 80% of the total reproductive transfer 5, 6. Nevertheless, POPs readily traverse placental membranes and may present a particular risk during gestation, because thresholds for adverse effects are lowered during critical stages of fetal development 7.

The lactational transfer of POPs has been described well in marine mammals, but in utero exposure has rarely been documented because of difficulties in obtaining fetal samples from healthy pregnant females. Reports of prenatal exposure are almost exclusively for PCBs and organochlorine pesticides 7–10, with only one report on transplacental transfer for PBDEs 11. Furthermore, these studies often rely on opportunistic sampling of stranded and/or bycaught animals of varying quality and consider a limited dataset of congeners. Regardless, results from these reports indicate an inverse relationship between the degree of halogenation of contaminants and the mother-fetus transfer efficiency.

Through collaboration with Inuvialuit community subsistence hunters, we were able to take advantage of a unique opportunity to examine PCB and PBDE transfer dynamics in free-ranging healthy arctic beluga whales (Delphinapterus leucas) during a critical juncture that is otherwise impossible to study in protected animals. The objective of the present study was to characterize the transplacental transfer of a full suite of PCB and PBDE congeners in two matched mother-fetus beluga pairs from arctic Canada and to characterize the processes governing this partitioning.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. Acknowledgements
  7. REFERENCES

Beluga samples were collected in 2008 and 2009 during the traditional harvest by Inuvialuit hunters at Hendrickson Island near the community of Tuktoyaktuk, in the Northwest Territories, Canada (69°30′N, 133°58′W). Full-depth blubber samples were taken from sites slightly dorsal of the pectoral flipper from the mothers and their near-term fetuses. Samples were wrapped in solvent-rinsed foil, frozen at −20°C on site, stored in portable freezers, and shipped to Fisheries and Oceans Canada, where they were stored at −80°C within two weeks of collection. Subsamples were taken to include all blubber layers, and approximately 300 mg were analyzed for 205 PCB and 78 PBDE congeners by the Laboratory of Expertise in Aquatic Chemical Analysis (Fisheries and Oceans Canada) within 30 d of field collection. Ross et al. 12 described extraction and clean-up procedures, instrumental analysis and conditions, and quality assurance/quality control criteria used for PCBs and PBDEs. Because of varying degrees of moderate background contamination, all PBDE data were blank-corrected. Due to analytical difficulties of measuring highly brominated PBDEs reliably, measurements of nona to deca congeners were not included. The percentage of lipid was determined from the remaining extract after drying under nitrogen flow. Congeners were quantified after resuspension in 1:1 dichloromethane-hexane by high-resolution gas chromatography/high-resolution mass spectrometry.

The mass of beluga whales and the blubber mass as percentage of total body weight was estimated from relationships described in Ryg et al. 13. The total contaminant blubber burden, expressed in mg, was calculated by multiplying the body weight, the relative blubber mass (to total body weight), lipid content, and contaminant concentration 7. The contaminant transfer rate was defined as the ratio of fetal blubber burden to the combined fetal and maternal burden. Relationships between variables were determined by a linear regression analysis (Sigma Plot Ver 10.0).

RESULTS AND DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. Acknowledgements
  7. REFERENCES

Analyzing these mother and near-term fetus pairs enabled us to evaluate the transplacental transfer of POPs prior to nursing during the beluga's 10.5-month gestation period. Between 135 to 157 PCB congeners and 23 to 27 PBDE congeners were detected in the four beluga samples. Polychlorinated biphenyls and PBDE concentration profiles were similar in all belugas; thus, the highest concentrated congeners were averaged and are displayed in Table 1. The top 10 PCB congeners represented more than 50% of the total concentration in the mother and fetus pairs. Similarly, BDE 47, 99, 100, 154, 49, 28/33, 66, and 71 accounted for more than 95% of total PBDEs.

Table 1. Average blubber concentration (ng/g lipid weight [lw]), estimated blubber burden (mg), and percentage of transfer from mother to fetus of the top ten PCB and PBDE congeners in two mother-fetus pairs of Arctic beluga whales (Delphinapterus leucas) sampled near Hendrickson Island, Northwest Territories, Canada
  Mother concentration (ng/g lw)Fetus concentration (ng/g lw)Mother blubber burden (mg)Fetus blubber burden (mg)Transfera (%)
  • a

    Transfer is defined as the ratio of fetal burden to the combined fetal and mother burden.

    PCB = polychlorinated biphenyl; PBDE = polybrominated diphenyl ether.

PCBsPCB 5215.617.43.10.514.6
 PCB 9511.712.12.30.413.9
 PCB 9913.612.22.70.412.2
 PCB 10116.617.73.30.514.0
 PCB 1109.99.51.50.316.4
 PCB 11813.513.72.60.413.6
 PCB 138/16323.716.84.60.59.8
 PCB 14912.110.12.40.311.3
 PCB 15329.419.15.70.69.2
 PCB 18711.43.62.20.14.6
 ΣPCB310257617.511.4
PBDEsBDE 28/330.10.10.020.00312.8
 BDE 473.42.50.70.0713.4
 BDE 490.10.20.030.00618.4
 BDE 660.090.060.020.00210.7
 BDE 710.080.060.020.00211.7
 BDE 990.70.40.30.027.7
 BDE 1000.50.30.090.0076.2
 BDE 1530.050.010.0090.00031.8
 BDE 1540.20.050.040.0012.9
 BDE 1550.070.020.010.00053.8
 ΣPBDE5.53.81.10.111.1

The total concentration of PCBs and PBDEs were similar in the females and their prenatal offspring, with average values of 310 and 257 ng/g (lw) for PCBs and 5.5 and 3.8 ng/g (lw) for PBDEs in the mothers and fetuses, respectively (Table 1). Brominated diphenyl ether-47 represented 43 to 64% and 58 to 68% of ΣPBDE in the mothers and fetuses, respectively, consistent with the dominance of this congener in aquatic biota 14. The concentration of top PCB and PBDE congeners in the mothers and fetuses differed by less than 10 ng/g (lw) in most cases (Table 1). Total PCB and PBDE concentrations in the mothers were considerably lower than the average level in six apparently nonreproductive adult females sampled during the same trip. Average female ΣPCB and ΣPBDE were 842 ± 503 and 21 ± 6.8 ng/g (lw), respectively (L. Loseto, Fisheries and Oceans Canada, Winnipeg, Canada, personal communication), with our beluga females representing on average 37 and 26% of these values. The lower values in these two females were consistent with their reproductive status, suggesting considerable transfer to their offspring; however, age cannot be ruled out as a driving factor, because the mothers were considerably younger than the average age (23 and 30 vs 44). The ΣPBDE concentrations from the present study were similar to those found in western (9.3 ng/g) and eastern (12 ng/g) Canadian Arctic belugas, but far less than for belugas from St. Lawrence (535 ng/g) and Norway (72 ng/g) 15, 16.

While congener-specific PCB and PBDE patterns appeared basically similar between mother and fetus, notable differences became evident when these concentrations were plotted as a function of the ratio of fetus to mother (Fig. 1). Because the partition trend was the same for both pairs, the values were averaged. The trends were similar for both PCBs and PBDEs, with a lower proportion of the heavier congeners appearing in the fetus. For PCBs, congeners with five or fewer chlorine atoms were preferentially transferred to the fetus. The trend in the transfer rates calculated from total blubber burden clearly demonstrated the more ready transfer of lower weight congeners to the fetus compared to heavier congeners (Table 1). The transfer was highest for di-CBs (41%) and tri-BDEs (26%) and declined to low (1.2%) and null levels for nona-CBs and hepta- to octa-BDEs, respectively (results not shown). We calculated the overall average transfer rate as 11.4% for ΣPCBs and 11.1% for ΣPBDEs (Table 1).

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Figure 1. Polychlorinated biphenyl (PCB) and polybrominated diphenyl ether (PBDE) congener profile and partition ratios between mother and fetus beluga whales (Delphinapterus leucas). Top panels show concentrations of PCB and PBDE congeners for beluga pair 1. Bottom panels show the average partition ratios between the two mother–fetus pairs. Partition ratios were calculated as the blubber concentration in the fetus divided by that in the mother and were logarithmically transformed. The high partition ratio calculated for BDE-101 may be an artifact of the near detection limit quantification of this congener.

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To explore the transfer dynamics between mother and fetus further, partition ratios were plotted against octanol-water partition coefficients (KOW) (Fig. 2). We observed a significant negative correlation between log KOW and the average partition ratio for PCBs (r2 = 0.79, p < 0.00001) and PBDEs (r2 = 0.37, p = 0.007). Greig et al. 10 found a similar log KOW-based partitioning between mother and fetus for 11 PCBs and 3 DDT isomers in California sea lions (Zalophus californianus). Our results indicate a similar mechanism of transfer of less lipophilic and lower molecular weight congeners to the fetus for both PCBs and PBDEs, with physicochemical characteristics governing this transfer. Additionally, the point at which congener ratios diverged (i.e., at zero between mother and fetus) was log KOW approximately 6.5 (corresponding to a molecular weight of ∼350 Da), above which congeners were preferentially retained by the mother, while congeners below this value were readily transferred to the fetus.

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Figure 2. Average partition ratios plotted against logarithmic octanol-water partition coefficients (log KOW) for polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in two beluga (Delphinapterus leucas) mother–fetus pairs. Partition ratios were calculated as the blubber concentration in the fetus divided by that in the mother and were logarithmically transformed. The dashed line represents partition parity. Octanol-water partition coefficients were taken from Patil 25, Makino 26, and Papa et al. 27. Higher than average partition ratios at low log KOW occurred for PCB congeners 7/9, 12/13, and 21 are likely because of the volatile nature and more variable recovery of these lighter congeners in the laboratory. A high value was also found for BDE-101, likely because of quantification of this congener measured near detection limits.

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This relationship supports previous reports of a more efficient transplacental transfer of lighter congeners to the fetus as compared to high-molecular weight and more lipophilic congeners 7–9. In gray seals (Halichoerus grypus), a barrier between blubber and circulatory lipids was proposed, where transfer efficiency was inversely related to the degree of chlorination in PCBs 4. Tanabe et al. 9 described the transplacental transfer of organochlorines as being regulated by partitioning between mother and fetus blubber, whereby blood acts as a carrier. In this scenario, the lower affinity of high molecular weight congeners to polar lipids in the blood and placenta, compared to nonpolar lipids (triglycerides) in blubber, generates the partitioning trend observed between mother and fetus. These studies, as well as others describing blubber–blood or lactational transfer 17–19, highlight the importance of basic physicochemical properties in shaping the pharmacokinetics of POP partitioning in marine mammals.

While the transplacental transfer dynamics have been reported for PCBs in several marine mammals, to our knowledge, a study of the melon-headed whale (Peponocephala electra) is the only other that describes the transfer of PBDEs in a cetacean 11. The results from that study agree with our findings describing the more efficient placental transfer of lower brominated PBDEs and complete resistance to transfer of hepta- to octa-BDEs. Our results add to the limited number of published reports on transplacental transfer of POPs; this information, together with lactational transfer, is useful in modeling the bioaccumulation of POPs in marine mammals. Because few studies are available, models of POP bioaccumulation often use nonspecies-specific transfer characteristics. Our results for transfer efficiency from mother to fetus for POPs are higher than those estimated in a St. Lawrence beluga model, which adapted placental transfer characteristics from Dalli-type Dall's porpoise (Phocoenoides dalli) 20. This highlights the importance of continued research into species-specific reproductive offloading of organic contaminants for the proper modeling of POP bioaccumulation in marine mammal populations.

Although the transport and fate of PCBs in the environment are reasonably well understood, PBDEs remain the subject of considerable attention. Lower-brominated PBDEs have been shown to exhibit similar long-range transport potential to PCBs; however, a full understanding of the bioavailability and trophic transfer of PBDEs remains elusive 14, 21. Our observation of the common governing role of log KOW for the transfer of both PCBs and PBDEs provides clear insight into the lipid-based transfer across cetacean placenta, an important component of the fate of persistent contaminants in marine mammals. This complements those reports that describe the role of log KOW in shaping the bioaccumulation and biomagnification of contaminants in marine food webs 14, 22.

The toxicological implications of the ready transplacental transfer of organic contaminants in the present study are unclear. Non-ortho PCBs (77, 126, and 169) and mono-ortho PCBs (105, 114, 118, 123, 156, 157, 167, and 189) were detected in the beluga fetuses, indicating potential toxicological risks through activation of the aryl-hydrocarbon receptor pathway 12. Although the ΣPCB toxic equivalents were below levels for adverse health effects as determined in harbor seal studies 12, perinatally exposed mammals are at a heightened risk of harmful effects compared to adults 23, 24. This prenatal exposure to endocrine-disrupting contaminants, at concentrations that are similar to those observed in adults, underscores the potential vulnerability of young arctic beluga whales prior to exposure by way of nursing and subsequent feeding.

Acknowledgements

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. Acknowledgements
  7. REFERENCES

Funding for the present study was provided by the Northern Contaminants Program of Aboriginal Affairs and Northern Development Canada, the Fisheries Joint Management Committee, and the Ecosystem Research Initiative of Fisheries and Oceans Canada (Central and Arctic Region). The present study also received support from the Natural Sciences and Engineering Research Council of Canada through awards to L. Loseto and J.P. Desforges. We thank F. Pokiak, N. Pokiak, N. Dangerfield, K. Felix, M. Noël, J. Noksana, S. Ostertag, R. Walker, and the Inuvik-area staff of Fisheries and Oceans Canada. We thank the Tuktoyaktuk Hunters and Trappers Committee and local hunters of Tuktoyaktuk.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS AND DISCUSSION
  6. Acknowledgements
  7. REFERENCES
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