The placental lipidome of maternal antenatal depression predicts socio-emotional problems in the offspring
The placental lipidome of maternal antenatal depression predicts socio-emotional problems in the offspring
While maternal mental health strongly influences neurodevelopment and health in the offspring, little is known about the determinants of inter-individual variation in the mental health of mothers. Likewise, the in utero biological pathways by which variation in maternal mental health affects offspring development remain to be defined. Previous studies implicate lipids, consistent with a known influence on cognitive and emotional function, but the relevance for maternal mental health and offspring neurodevelopment is unclear. This study characterizes the placental and circulatory lipids in antenatal depression, as well as socio-emotional outcomes in the offspring. Targeted liquid chromatography-mass spectrometry covering 470 lipid species was performed on placenta from 186 women with low (n = 70) or high (n = 116) levels of antenatal depressive symptoms assessed using the Edinburgh Postnatal Depression Scale at 26 weeks’ gestation. Child socio-emotional outcomes were assessed from the Child Behavior Check List (CBCL) at 48 months. Seventeen placental lipid species showed an inverse association with antenatal EPDS scores. Specifically, lower levels of phospholipids containing LC-PUFAs: omega-3 docosapentaenoic acid (DPA), eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), and omega-6 arachidonic acid (AA) were significantly associated with depressive symptoms. Additional measurement of LC-PUFA in antenatal plasma samples at mid-gestation confirmed the reduced circulation of these specific fatty acids in mothers. Reduced concentration of the placental phospholipids also predicted poorer socio-emotional outcomes in the offspring. This study provides new insights into the role of the materno-fetal lipid cross-talk as a mechanism linking maternal mental health to that of the offspring. These findings show the potential utility of nutritional approaches among pregnant women with depressive symptoms to reduce offspring risk for later socio-emotional problems.
Wong, Gerard
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Weir, Jacquelyn M.
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Mishra, Priti
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Huynh, Kevin
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Nijagal, Brunda
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Gupta, Varsha
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Broekman, Birit F.P.
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Chong, Mary Foong-Fong
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Chan, Shiao-Yng
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Tan, Kok Hian
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Tull, Dedreia
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McConville, Malcolm
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Calder, Philip
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Godfrey, Keith
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Chong, Yap-Seng
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Gluckman, Peter D.
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Meaney, Michael J.
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Meikle, Peter J.
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Karnani, Neerja
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4 February 2021
Wong, Gerard
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Weir, Jacquelyn M.
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Mishra, Priti
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Huynh, Kevin
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Nijagal, Brunda
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Gupta, Varsha
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Broekman, Birit F.P.
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Chong, Mary Foong-Fong
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Chan, Shiao-Yng
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Tan, Kok Hian
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Tull, Dedreia
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McConville, Malcolm
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Calder, Philip
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Godfrey, Keith
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Chong, Yap-Seng
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Gluckman, Peter D.
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Meaney, Michael J.
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Meikle, Peter J.
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Karnani, Neerja
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Wong, Gerard, Weir, Jacquelyn M., Mishra, Priti, Huynh, Kevin, Nijagal, Brunda, Gupta, Varsha, Broekman, Birit F.P., Chong, Mary Foong-Fong, Chan, Shiao-Yng, Tan, Kok Hian, Tull, Dedreia, McConville, Malcolm, Calder, Philip, Godfrey, Keith, Chong, Yap-Seng, Gluckman, Peter D., Meaney, Michael J., Meikle, Peter J. and Karnani, Neerja
(2021)
The placental lipidome of maternal antenatal depression predicts socio-emotional problems in the offspring.
Translational Psychiatry, 11 (1), [107].
(doi:10.1038/s41398-021-01208-x).
Abstract
While maternal mental health strongly influences neurodevelopment and health in the offspring, little is known about the determinants of inter-individual variation in the mental health of mothers. Likewise, the in utero biological pathways by which variation in maternal mental health affects offspring development remain to be defined. Previous studies implicate lipids, consistent with a known influence on cognitive and emotional function, but the relevance for maternal mental health and offspring neurodevelopment is unclear. This study characterizes the placental and circulatory lipids in antenatal depression, as well as socio-emotional outcomes in the offspring. Targeted liquid chromatography-mass spectrometry covering 470 lipid species was performed on placenta from 186 women with low (n = 70) or high (n = 116) levels of antenatal depressive symptoms assessed using the Edinburgh Postnatal Depression Scale at 26 weeks’ gestation. Child socio-emotional outcomes were assessed from the Child Behavior Check List (CBCL) at 48 months. Seventeen placental lipid species showed an inverse association with antenatal EPDS scores. Specifically, lower levels of phospholipids containing LC-PUFAs: omega-3 docosapentaenoic acid (DPA), eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), and omega-6 arachidonic acid (AA) were significantly associated with depressive symptoms. Additional measurement of LC-PUFA in antenatal plasma samples at mid-gestation confirmed the reduced circulation of these specific fatty acids in mothers. Reduced concentration of the placental phospholipids also predicted poorer socio-emotional outcomes in the offspring. This study provides new insights into the role of the materno-fetal lipid cross-talk as a mechanism linking maternal mental health to that of the offspring. These findings show the potential utility of nutritional approaches among pregnant women with depressive symptoms to reduce offspring risk for later socio-emotional problems.
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Accepted/In Press date: 11 January 2021
e-pub ahead of print date: 4 February 2021
Published date: 4 February 2021
Additional Information:
Funding Information:
We thank the GUSTO study group, which includes Allan Sheppard, Amutha Chinnadurai, Anne Eng Neo Goh, Anne Rifkin-Graboi, Anqi Qiu, Arijit Biswas, Bee Wah Lee, Birit F.P. Broekman, Boon Long Quah, Borys Shuter, Chai Kiat Chng, Cheryl Ngo, Choon Looi Bong, Christiani Jeyakumar Henry, Cornelia Yin Ing Chee, Yam Thiam Daniel Goh, Doris Fok, Fabian Yap, George Seow Heong Yeo, Helen Chen, Hugo P S van Bever, Iliana Magiati, Inez Bik Yun Wong, Ivy Yee-Man Lau, Jeevesh Kapur, Jenny L. Richmond, Jerry Kok Yen Chan, Joanna D. Holbrook, Joshua J. Gooley, Keith M. Godfrey, Kenneth Kwek, Kok Hian Tan, Krishnamoorthy Niduvaje, Leher Singh, Lin Lin Su, Lourdes Mary Daniel, Lynette P Shek, Marielle V. Fortier, Mark Hanson, Mary Foong-Fong Chong, Mary Rauff, Mei Chien Chua, Michael Meaney, Mya Thway Tint, Neerja Karnani, Ngee Lek, Oon Hoe Teoh, P. C. Wong, Peter D. Gluckman, Pratibha Agarwal, Rob M. van Dam, Salome A. Rebello, Seang-Mei Saw, Shang Chee Chong, Shirong Cai, Shu-E Soh, Sok Bee Lim, Chin-Ying Stephen Hsu, Victor Samuel Rajadurai, Walter Stunkel, Wee Meng Han, Wei Wei Pang, Yap-Seng Chong, Yin Bun Cheung, Yiong Huak Chan and Yung Seng Lee. This work was supported by the Translational Clinical Research (TCR) Flagship Program on Developmental Pathways to Metabolic Disease funded by the National Research Foundation (NRF) and administered by the National Medical Research Council (NMRC), Singapore - NMRC/TCR/004-NUS/2008. Additional funding is provided by Strategic Positioning Fund (SPF) awarded by Agency for Science, Technology and Research (A*STAR), Singapore, available to NK. KMG is supported by the National Institute for Health Research through the NIHR Southampton Biomedical Research Centre and by the European Union’s Seventh Framework Programme (FP7/2007–2013), projects EarlyNutrition and ODIN under grant agreement numbers 289346 and 613977. MJM is supported by funding from the Hope for Depression Research Foundation (USA). The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.
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© 2021, The Author(s).
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Local EPrints ID: 446391
URI: http://eprints.soton.ac.uk/id/eprint/446391
PURE UUID: 9c3fd359-ed66-4ddb-960d-606ec70ffe31
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Date deposited: 05 Feb 2021 17:33
Last modified: 17 Mar 2024 05:59
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Contributors
Author:
Gerard Wong
Author:
Jacquelyn M. Weir
Author:
Priti Mishra
Author:
Kevin Huynh
Author:
Brunda Nijagal
Author:
Varsha Gupta
Author:
Birit F.P. Broekman
Author:
Mary Foong-Fong Chong
Author:
Shiao-Yng Chan
Author:
Kok Hian Tan
Author:
Dedreia Tull
Author:
Malcolm McConville
Author:
Yap-Seng Chong
Author:
Peter D. Gluckman
Author:
Michael J. Meaney
Author:
Peter J. Meikle
Author:
Neerja Karnani
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