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Fetal liver blood flow distribution: role in human developmental strategy to prioritize fat deposition versus brain development

Fetal liver blood flow distribution: role in human developmental strategy to prioritize fat deposition versus brain development
Fetal liver blood flow distribution: role in human developmental strategy to prioritize fat deposition versus brain development
Among primates, human neonates have the largest brains but also the highest proportion of body fat. If placental nutrient supply is limited, the fetus faces a dilemma: should resources be allocated to brain growth, or to fat deposition for use as a potential postnatal energy reserve? We hypothesised that resolving this dilemma operates at the level of umbilical blood distribution entering the fetal liver. In 381 uncomplicated pregnancies in third trimester, we measured blood flow perfusing the fetal liver, or bypassing it via the ductus venosus to supply the brain and heart using ultrasound techniques. Across the range of fetal growth and independent of the mother's adiposity and parity, greater liver blood flow was associated with greater offspring fat mass measured by dual-energy X-ray absorptiometry, both in the infant at birth (r = 0.43, P<0.001) and at age 4 years (r = 0.16, P = 0.02). In contrast, smaller placentas less able to meet fetal demand for essential nutrients were associated with a brain-sparing flow pattern (r = 0.17, p = 0.02). This flow pattern was also associated with a higher degree of shunting through ductus venosus (P = 0.04). We propose that humans evolved a developmental strategy to prioritize nutrient allocation for prenatal fat deposition when the supply of conditionally essential nutrients requiring hepatic inter-conversion is limited, switching resource allocation to favour the brain if the supply of essential nutrients is limited. Facilitated placental transfer mechanisms for glucose and other nutrients evolved in environments less affluent than those now prevalent in developed populations, and we propose that in circumstances of maternal adiposity and nutrient excess these mechanisms now also lead to prenatal fat deposition. Prenatal developmental influences play important roles in the human propensity to deposit fat
1932-6203
e41759
Godfrey, Keith M.
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Haugen, G.
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Kiserud, T.
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Inskip, H.M.
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Cooper, C.
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Harvey, N.C.
ce487fb4-d360-4aac-9d17-9466d6cba145
Crozier, S.R.
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Robinson, S.M.
ba591c98-4380-456a-be8a-c452f992b69b
Davies, L.
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Hanson, M.A.
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Godfrey, Keith M.
0931701e-fe2c-44b5-8f0d-ec5c7477a6fd
Haugen, G.
3cb2a509-d772-44e6-9ee9-80c9b692233c
Kiserud, T.
a68fe723-c8cf-49f6-9ea6-65c81f16ff31
Inskip, H.M.
5fb4470a-9379-49b2-a533-9da8e61058b7
Cooper, C.
e05f5612-b493-4273-9b71-9e0ce32bdad6
Harvey, N.C.
ce487fb4-d360-4aac-9d17-9466d6cba145
Crozier, S.R.
a97b1967-f6af-413a-8eb0-69fa25534d68
Robinson, S.M.
ba591c98-4380-456a-be8a-c452f992b69b
Davies, L.
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Hanson, M.A.
1952fad1-abc7-4284-a0bc-a7eb31f70a3f

Godfrey, Keith M., Haugen, G., Kiserud, T., Inskip, H.M., Cooper, C., Harvey, N.C., Crozier, S.R., Robinson, S.M., Davies, L. and Hanson, M.A. (2012) Fetal liver blood flow distribution: role in human developmental strategy to prioritize fat deposition versus brain development. PLoS ONE, 7 (8), e41759. (doi:10.1371/journal.pone.0041759). (PMID:22927915)

Record type: Article

Abstract

Among primates, human neonates have the largest brains but also the highest proportion of body fat. If placental nutrient supply is limited, the fetus faces a dilemma: should resources be allocated to brain growth, or to fat deposition for use as a potential postnatal energy reserve? We hypothesised that resolving this dilemma operates at the level of umbilical blood distribution entering the fetal liver. In 381 uncomplicated pregnancies in third trimester, we measured blood flow perfusing the fetal liver, or bypassing it via the ductus venosus to supply the brain and heart using ultrasound techniques. Across the range of fetal growth and independent of the mother's adiposity and parity, greater liver blood flow was associated with greater offspring fat mass measured by dual-energy X-ray absorptiometry, both in the infant at birth (r = 0.43, P<0.001) and at age 4 years (r = 0.16, P = 0.02). In contrast, smaller placentas less able to meet fetal demand for essential nutrients were associated with a brain-sparing flow pattern (r = 0.17, p = 0.02). This flow pattern was also associated with a higher degree of shunting through ductus venosus (P = 0.04). We propose that humans evolved a developmental strategy to prioritize nutrient allocation for prenatal fat deposition when the supply of conditionally essential nutrients requiring hepatic inter-conversion is limited, switching resource allocation to favour the brain if the supply of essential nutrients is limited. Facilitated placental transfer mechanisms for glucose and other nutrients evolved in environments less affluent than those now prevalent in developed populations, and we propose that in circumstances of maternal adiposity and nutrient excess these mechanisms now also lead to prenatal fat deposition. Prenatal developmental influences play important roles in the human propensity to deposit fat

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Published date: August 2012
Organisations: Faculty of Medicine, Faculty of Health Sciences

Identifiers

Local EPrints ID: 346628
URI: http://eprints.soton.ac.uk/id/eprint/346628
ISSN: 1932-6203
PURE UUID: 2fc56e61-7fd1-4c19-85f3-87e70b423d4e
ORCID for Keith M. Godfrey: ORCID iD orcid.org/0000-0002-4643-0618
ORCID for H.M. Inskip: ORCID iD orcid.org/0000-0001-8897-1749
ORCID for C. Cooper: ORCID iD orcid.org/0000-0003-3510-0709
ORCID for N.C. Harvey: ORCID iD orcid.org/0000-0002-8194-2512
ORCID for S.M. Robinson: ORCID iD orcid.org/0000-0003-1766-7269
ORCID for M.A. Hanson: ORCID iD orcid.org/0000-0002-6907-613X

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Date deposited: 04 Jan 2013 11:11
Last modified: 18 Feb 2021 17:02

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