Hypoglycemia and the Origin of Hypoxia-Induced Reduction in Human Fetal Growth
Open accessAbstract
BACKGROUND: The most well known reproductive consequence of residence at high altitude (HA >2700 m) is reduction in fetal growth. Reduced fetoplacental oxygenation is an underlying cause of pregnancy pathologies, including intrauterine growth restriction and preeclampsia, which are more common at HA. Therefore, altitude is a natural experimental model to study the etiology of pregnancy pathophysiologies. We have shown that the proximate cause of decreased fetal growth is not reduced oxygen availability, delivery, or consumption. We therefore asked whether glucose, the primary substrate for fetal growth, might be decreased and/or whether altered fetoplacental glucose metabolism might account for reduced fetal growth at HA. METHODS: Doppler and ultrasound were used to measure maternal uterine and fetal umbilical blood flows in 69 and 58 residents of 400 vs 3600 m. Arterial and venous blood samples from mother and fetus were collected at elective cesarean delivery and analyzed for glucose, lactate and insulin. Maternal delivery and fetal uptakes for oxygen and glucose were calculated. PRINCIPAL FINDINGS: The maternal arterial - venous glucose concentration difference was greater at HA. However, umbilical venous and arterial glucose concentrations were markedly decreased, resulting in lower glucose delivery at 3600 m. Fetal glucose consumption was reduced by >28%, but strongly correlated with glucose delivery, highlighting the relevance of glucose concentration to fetal uptake. At altitude, fetal lactate levels were increased, insulin concentrations decreased, and the expression of GLUT1 glucose transporter protein in the placental basal membrane was reduced. CONCLUSION/SIGNIFICANCE: Our results support that preferential anaerobic consumption of glucose by the placenta at high altitude spares oxygen for fetal use, but limits glucose availability for fetal growth. Thus reduced fetal growth at high altitude is associated with fetal hypoglycemia, hypoinsulinemia and a trend towards lactacidemia. Our data support that placentally-mediated reduction in glucose transport is an initiating factor for reduced fetal growth under conditions of chronic hypoxemia.
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Measurements of absolute rates of uterine and umbilical glucose uptake suggest that the placenta may be using up to 60% more glucose at high altitude.
“Measurements of absolute rates of uterine and umbilical glucose uptake suggest that the placenta may be using up to 60% more glucose at high altitude (605).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [605]
This is greater than the 13-15% reduction in absolute uterine oxygen delivery observed between these high- and low-altitude populations of pregnant women.
“This is greater than the 13-15% reduction in absolute uterine oxygen delivery observed between these high-and low-altitude populations of pregnant women (604, 605).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [605]
Since the percentage decrease in fetal glucose delivery appears to be greater than the percentage reduction in net fetal glucose consumption measured as umbilical glucose uptake at high altitude, there may also be activation of gluconeogenesis from lactate and amino acids by the high-altitude fetus near term.
“Since the percentage decrease in fetal glucose delivery appears to be greater than the percentage reduction in net fetal glucose consumption measured as umbilical glucose uptake at high altitude (605), there may also be activation of gluconeogenesis from lactate and amino acids by the high-altitude fetus near term.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [605]
In Bolivian women, oxygen consumption by the utero-placental tissues near term appears to be about 20% less at high than low altitude in the absence of any change in placental weight.
“In Bolivian women, oxygen consumption by the utero-placental tissues near term appears to be about 20% less at high than low altitude in the absence of any change in placental weight (605).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [605]
The proposed metabolic switch in the high altitude placenta will have consequences for fetal metabolism because, although fetal oxygen consumption is maintained on a weight specific basis, the fetus has lower than normal glucose concentrations and uses less glucose per kg body weight measured as umbilical glucose uptake.
“The proposed metabolic switch in the high altitude placenta will have consequences for fetal metabolism because, although fetal oxygen consumption is maintained on a weight specific basis, the fetus has lower than normal glucose concentrations and uses less glucose per kg body weight measured as umbilical glucose uptake (605).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [605]
Per kg of fetus, placental oxygen delivery to the human fetus and its rate of oxygen consumption near term are normal at high altitude, although the fetuses are smaller.
“Indeed, per kg of fetus, placental oxygen delivery to the human fetus and its rate of oxygen consumption near term are normal at high altitude, although the fetuses are smaller (443, 605).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [605]
There is an increase in the fetal arterial concentration of lactate in these fetuses, but little is known about their rate of lactate consumption or about the rates of placental production and delivery of lactate at high altitude.
“There is an increase in the fetal arterial concentration of lactate in these fetuses, but little is known about their rate of lactate consumption or about the rates of placental production and delivery of lactate at high altitude (534, 605).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [605]
In the high-altitude human placenta, GLUT1 is reduced at the basal but not the microvillous membranes, consistent with the decreased placental transfer of glucose to the fetus in conditions of chronic maternal hypoxia.
“By contrast, in the high-altitude human placenta, GLUT1 is reduced at the basal but not the microvillous membranes, consistent with the decreased placental transfer of glucose to the fetus in conditions of chronic maternal hypoxia (601, 605).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [605]
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- Authors
- Zamudio, S., Torricos, T., Fik, E., Oyala, M., Echalar, L., Pullockaran, J., Tutino, E., Martin, B., Belliappa, S., Balanza, E., & Illsley, N. P.
- Affiliations
- University of Medicine and Dentistry of New Jersey (US)
- Universidad Mayor de San Andrés (BO)
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- Zamudio, Stacy
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- 5
- Issue
- 1
- Pages
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- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2797307
- OpenAlex
- W2026644865
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- 141
- References
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- Figshare (submittedVersion, cc-by)
- Funders
- National Science Foundation (TW007444, 0309142)
- National Institutes of Health
- Fogarty International Center (TW007444, R03TW007444)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD042737, HD046982, R01HD046982, HD042737)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › High Altitude and Hypoxia
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- fetal hypoglycemia, fetal growth restriction, high altitude, hypoxia, umbilical blood flow, fetal lactate, hypoinsulinemia, GLUT1 glucose transporter, placental glucose transport, preeclampsia
- MeSH terms
- Adult, Hypoxia, Female, Glucose, Humans, Infant, Newborn, Maternal-Fetal Exchange, Pregnancy, Regional Blood Flow, Ultrasonography, Doppler, Fetal Development
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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