In aquatic mammals, maternal transfer is the movement of contaminants from mother to offspring, typically of lipophilic contaminants while in utero or through the mother's milk. This has become important with the increase in usage of persistent organic pollutants (POPs). POPs biomagnify due to their lipophilic nature and become accumulated in the lipid tissues of aquatic mammals. These lipids are used as energy for the mother during the development of offspring, which releases the POPs into the circulatory fluid. This leads to a transfer of the toxicants into the developing embryos during gestation as well as into milk that an aquatic mammal produces during lactation.

History and background

Marine mammals are exposed to a variety of chemicals throughout their life, mostly through their diet. Once the chemicals are accumulated in the body tissues of the mammals, a portion of these chemicals in the female mammals are transferred to their offspring during gestation and lactation.

The degree of maternal-fetal transfer of chemical pollutants is affected by chemical and physical properties of those compounds. Lipophilicity, protein binding, and active transport mechanisms all influence the absorption and distribution of such chemicals in maternal tissues.[1] Lipophilic chemicals, such as many POPs, can be transferred through the fatty portion of milk, while hydrophilic components can be transferred along with the liquid portion of the milk. The placenta provides a barrier to some contaminants, but is partially permeable to others, including many organics and certain heavy metals such as lead, mercury and cadmium, particularly when combined with organic molecules.[2]

Mechanisms of Maternal Transfer

Lactation

The transfer of contaminants from mother to pup through lactation is most likely the largest mass transfer of contaminants, greater than that of in-utero transfers.[3] When the mother begins lactation, blubber lipids are converted into milk lipids to feed her offspring. During this process, toxicants that were stored in blubber lipids are moved into the milk and subsequently are transferred to the nursing pup.

The transfer of toxicants through lactation is driven by the log Kow of the toxicants. Chemical compounds with a high affinity for lipids (a higher log Kow) will more readily be transferred through lactation due to the high lipid content of milk.[4] The transfer of toxicants from blubber to milk is not fully understood, and selective transfer of contaminants has been observed.

Mass balance of toxicants is difficult during lactation due to milk lipids originating from blubber lipids as well as being synthesized locally in mammary tissue. The change in toxicant solubility between blubber and circulatory fluid as well as the breakdown and resynthesis of blubber lipids and circulatory lipids also contributes to the difficulties of mass balance of toxicants between blubber, circulatory, and milk lipids.[5]

However, even with difficulties of mass balancing, it has generally been observed in grey seals and harbor porpoises that residues in pup blubber lipids are generally similar or slightly higher than in maternal milk lipids, and are approximately half of the residues in maternal blubber lipids.[3][6]

Placental Transfer

The transfer of POPs from mother to fetus via the placenta is less than that of lactation but can still cause adverse effects.[7] Fatty acids from the mother's plasma are transported either through diffusion or active transport through the placenta to be used in important processes such as brain development.[8] Sources of fatty acids are mainly derived from blubber in seals, porpoises, and whales.

Lipophilic chemicals such as PCBs previously stored within the mother's fatty tissue can be transferred to the fetus via the circulatory fluid. Some lipophilic chemicals can be metabolized by the fetus using mostly CYP enzymes, but others are quickly incorporated into developing fetal adipose tissue.[9][10] The storage and release of these chemicals within the fetus can lead to endocrine disruption, immunosuppression, thyroid disruption, and neurotoxicity in seals and orcas.[11]

Implications

Offspring Vulnerability

In mammals, maternal factors can be transferred via the placenta, in the colostrum, and in normal milk during lactation. Marine mammal offspring are especially vulnerable during the time when their own immune systems have not yet matured. When females provide milk to their young, they can have a dramatic impact on offspring fitness during ontogeny, as well as when the offspring matures into an adult.[12] Female marine mammals pass on most of their POP burden to their first-born offspring, while the calf is in utero and afterwards during lactation. The large amount of POPs transferred to the offspring as well as the fast rate of transfer, can sometimes prove fatal.[13]

Male vs. Female

The POP burden carried by male and female marine mammals tends to increase with time until they reach the age of sexual maturity. After that point, the burden in males continues to grow, as they continue to absorb POPs from their food. However, with female marine mammals, the POP burden carried decreases after birth but can then increase until the next reproductive cycle.[13]

References

  1. ↑ Aylward, L. L.; Hays, S. M.; Kirman, C. R.; Marchitti, S. A.; Kenneke, J. F.; English, C.; Mattison, D. R.; Becker, R. A. (2014-01-01). "Relationships of chemical concentrations in maternal and cord blood: a review of available data". Journal of Toxicology and Environmental Health Part B: Critical Reviews. 17 (3): 175–203. doi:10.1080/10937404.2014.884956. ISSN 1521-6950. PMID 24749481. S2CID 21505371.
  2. ↑ Sparling, Donald W. (2016-04-18). Ecotoxicology Essentials: Environmental Contaminants and Their Biological Effects on Animals and Plants. Academic Press. ISBN 9780128019610.
  3. 1 2 Addison, R. F.; Brodie, P. F. (1977-07-01). "Organochlorine Residues in Maternal Blubber, Milk, and Pup Blubber from Grey Seals (Halichoerus grypus) from Sable Island, Nova Scotia". Journal of the Fisheries Research Board of Canada. 34 (7): 937–941. doi:10.1139/f77-146. ISSN 0015-296X.
  4. ↑ Frouin, Héloïse; Lebeuf, Michel; Hammill, Mike; Fournier, Michel (2012-02-15). "Transfer of PBDEs and chlorinated POPs from mother to pup during lactation in harp seals Phoca groenlandica". Science of the Total Environment. 417–418: 98–107. Bibcode:2012ScTEn.417...98F. doi:10.1016/j.scitotenv.2011.11.084. PMID 22239965.
  5. ↑ Addison, R. F.; Brodie, P. F. (1987-04-01). "Transfer of Organochlorine Residues from Blubber through the Circulatory System to Milk in the Lactating Grey Seal Halichoerus grypus". Canadian Journal of Fisheries and Aquatic Sciences. 44 (4): 782–786. doi:10.1139/f87-095. ISSN 0706-652X.
  6. ↑ Heppleston, P. B. (1973-03-01). "Organochlorines in British grey seals". Marine Pollution Bulletin. 4 (3): 44–45. doi:10.1016/0025-326X(73)90305-6.
  7. ↑ Ren, Aiguo; Qiu, Xinghua; Jin, Lei; Ma, Jin; Li, Zhiwen; Zhang, Le; Zhu, Huiping; Finnell, Richard H.; Zhu, Tong (2011-08-02). "Association of selected persistent organic pollutants in the placenta with the risk of neural tube defects". Proceedings of the National Academy of Sciences. 108 (31): 12770–12775. Bibcode:2011PNAS..10812770R. doi:10.1073/pnas.1105209108. ISSN 0027-8424. PMC 3150927. PMID 21768370.
  8. ↑ Lager, Susanne; Powell, Theresa (2012). "Regulation of Nutrient Transport across the Placenta". Journal of Pregnancy. 2012: 179827. doi:10.1155/2012/179827. PMC 3523549. PMID 23304511.
  9. ↑ Prouillac, Caroline; Lecoeur, Sylvaine (2010-10-01). "The role of the placenta in fetal exposure to xenobiotics: importance of membrane transporters and human models for transfer studies". Drug Metabolism and Disposition. 38 (10): 1623–1635. doi:10.1124/dmd.110.033571. ISSN 1521-009X. PMID 20606001. S2CID 8134538.
  10. ↑ Szabo, AndrewJ.; Szabo, Olga (1974-08-31). "Originally published as Volume 2, Issue 7879PLACENTAL FREE-FATTY-ACID TRANSFER AND FETAL ADIPOSE-TISSUE DEVELOPMENT: AN EXPLANATION OF FETAL ADIPOSITY IN INFANTS OF DIABETIC MOTHERS". The Lancet. 304 (7879): 498–499. doi:10.1016/S0140-6736(74)92020-0. PMID 4137108.
  11. ↑ Krahn, Margaret M.; Hanson, M. Bradley; Baird, Robin W.; Boyer, Richard H.; Burrows, Douglas G.; Emmons, Candice K.; Ford, John K. B.; Jones, Linda L.; Noren, Dawn P. (2007-12-01). "Persistent organic pollutants and stable isotopes in biopsy samples (2004/2006) from Southern Resident killer whales". Marine Pollution Bulletin. 54 (12): 1903–1911. doi:10.1016/j.marpolbul.2007.08.015. PMID 17931664.
  12. ↑ "SeaWeb - Ocean Briefing Book". www.seaweb.org. Archived from the original on 2016-06-02. Retrieved 2016-05-23.
  13. 1 2 "Marine Chemical Pollution". WDC, Whale and Dolphin Conservation. Retrieved 2016-05-23.
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