Maternal oxygen delivery is not related to altitude‐ and ancestry‐associated differences in human fetal growth
Open accessAbstract
Fetal growth is reduced at high altitude, but the decrease is less among long‐resident populations. We hypothesized that greater maternal uteroplacental O 2 delivery would explain increased fetal growth in Andean natives versus European migrants to high altitude. O 2 delivery was measured with ultrasound, Doppler and haematological techniques. Participants (n= 180) were pregnant women of self‐professed European or Andean ancestry living at 3600 m or 400 m in Bolivia. Ancestry was quantified using ancestry‐informative single nucleotide polymorphims. The altitude‐associated decrement in birth weight was 418 g in European versus 236 g in Andean women (P< 0.005). Altitude was associated with decreased uterine artery diameter, volumetric blood flow and O 2 delivery regardless of ancestry. But the hypothesis was rejected as O 2 delivery was similar between ancestry groups at their respective altitudes of residence. Instead, Andean neonates were larger and heavier per unit of O 2 delivery, regardless of altitude (P< 0.001). European admixture among Andeans was negatively correlated with birth weight at both altitudes (P< 0.01), but admixture was not related to any of the O 2 transport variables. Genetically mediated differences in maternal O 2 delivery are thus unlikely to explain the Andean advantage in fetal growth. Of the other independent variables, only placental weight and gestational age explained significant variation in birth weight. Thus greater placental efficiency in O 2 and nutrient transport, and/or greater fetal efficiency in substrate utilization may contribute to ancestry‐ and altitude‐related differences in fetal growth. Uterine artery O 2 delivery in these pregnancies was 99 ± 3 ml min−1, ∼5‐fold greater than near‐term fetal O 2 consumption. Deficits in maternal O 2 transport in third trimester normal pregnancy are unlikely to be causally associated with variation in fetal growth.
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In some studies, the protective effect of Andean ancestry on uterine artery haemodynamics is only seen at high altitude while in others, the ethnic differences are also evident at sea level.
“In some studies, the protective effect of Andean ancestry on uterine artery haemodynamics is only seen at high altitude while in others, the ethnic differences are also evident at sea level (295, 604).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [604]
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 [604]
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Cites
Genetic conflicts in human pregnancy
Haig, D. (1993) · The Quarterly Review of Biology · doi:10.1086/418300 · Cited by 1,253 · see citing works
Regulation of Human Placental Development by Oxygen Tension
Genbačev, O., Zhou, Y., Ludlow, J. W., & Fisher, S. J. (1997) · Science · doi:10.1126/science.277.5332.1669 · Cited by 914 · see citing works
Placental oxidative stress: from miscarriage to preeclampsia
Burton, G. J., & Jauniaux, E. (2004) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2004.03.003 · Cited by 673 · see citing works
Development of the placental villous tree and its consequences for fetal growth
Kingdom, J. C., Huppertz, B., Seaward, G. R., & Kaufmann, P. (2000) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00423-1 · Cited by 591 · see citing works
Skin pigmentation, biogeographical ancestry and admixture mapping
Shriver, M. D., Parra, E. J., Dios, S., Bonilla, C., Norton, H., Jovel, C., Pfaff, C., Jones, C., Massac, A., Cameron, N., et al. (2003) · Human Genetics · doi:10.1007/s00439-002-0896-y · Cited by 549 · see citing works
Molecular Evidence of Placental Hypoxia in Preeclampsia
Soleymanlou, N., Jurišica, I., Nevo, O., Ietta, F., Zhang, X., Zamudio, S., Post, M., & Caniggia, I. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-0078 · Cited by 394 · see citing works
Self-citationJensen, G. M., & MOORE, L. G. (1997) · American Journal of Public Health · doi:10.2105/ajph.87.6.1003 · Cited by 355 · see citing works
Human Genetic Adaptation to High Altitude
MOORE, L. G. (2001) · High Altitude Medicine & Biology · doi:10.1089/152702901750265341 · Cited by 335 · see citing works
Comparative primate energetics and hominid evolution
Leonard, W. R., & Robertson, M. L. (1997) · American Journal of Physical Anthropology · doi:10.1002/(sici)1096-8644(199702)102:2 · Cited by 297 · see citing works
Palmer, S. K., Zamudio, S., Coffin, C. T., Parker, S. B., Stamm, E. R., & MOORE, L. G. (1992) · PubMed · Cited by 267 · see citing works
Self-citationPalmer, S. K., Moore, L. G., Young, D. A., Cregger, B., Berman, J. C., & Zamudio, S. (1999) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(99)70611-3 · Cited by 244 · see citing works
Self-citationEffects of Altitude versus Economic Status on Birth Weight and Body Shape at Birth
Giussani, D. A., Phillips, P. S., Anstee, S., & Barker, D. J. P. (2001) · Pediatric Research · doi:10.1203/00006450-200104000-00009 · Cited by 230 · see citing works
Moore, L. G., Young, D., McCullough, R. E., Droma, T., & Zamudio, S. (2001) · American Journal of Human Biology · doi:10.1002/ajhb.1102 · Cited by 194 · see citing works
Self-citationTorroni, A., Miller, J. A. O., MOORE, L. G., Zamudio, S., Zhuang, J., Droma, T., & Wallace, D. C. (1994) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330930204 · Cited by 190 · see citing works
Self-citationEffect of altitude on uterine artery blood flow during normal pregnancy
Zamudio, S., Palmer, S. K., Droma, T., Stamm, E. R., Coffin, C. T., & MOORE, L. G. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.79.1.7 · Cited by 186 · see citing works
Self-citationYip, R. (1987) · The Journal of Pediatrics · doi:10.1016/s0022-3476(87)80209-3 · Cited by 167 · see citing works
Bonilla, C., Parra, E. J., Pfaff, C., Dios, S., Marshall, J. A., Hamman, R. F., Ferrell, R. E., Hoggart, C., McKeigue, P., & Shriver, M. (2004) · Annals of Human Genetics · doi:10.1046/j.1529-8817.2003.00084.x · Cited by 164 · see citing works
Liu, D., Moberg, E., Kollind, M., Lins, P. E., Adamson, U., & Macdonald, I. A. (1992) · Diabetologia · doi:10.1007/bf00400932 · Cited by 162 · see citing works
Zamudio, S. (2003) · High Altitude Medicine & Biology · doi:10.1089/152702903322022785 · Cited by 161 · see citing works
Self-citationLarge-scale SNP analysis reveals clustered and continuous patterns of human genetic variation
Shriver, M. D., Mei, R., Parra, E. J., Sonpar, V. A., Halder, I., Tishkoff, S. A., Schurr, T. G., Zhadanov, S. I., Osipova, L. P., Brutsaert, T. D., et al. (2005) · Human Genomics · doi:10.1186/1479-7364-2-2-81 · Cited by 150 · see citing works
Altitude, Low Birth Weight, and Infant Mortality in Colorado
Unger, C. A. (1988) · JAMA · doi:10.1001/jama.1988.03720230037027 · Cited by 146 · see citing works
Human PaCO2 and standard base excess compensation for acid-base imbalance
Schlichtig, R., Grogono, A. W., & Severinghaus, J. W. (1998) · Critical Care Medicine · doi:10.1097/00003246-199807000-00015 · Cited by 144 · see citing works
Konje, J. C., Howarth, E. S., Kaufmann, P., & Taylor, D. J. (2003) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1046/j.1471-0528.2003.t01-1-02163.x · Cited by 134 · see citing works
Fetal biometry at 4300 m compared to sea level in Peru
Krampl, E., LEES, C. C., Bland, M., Dorado, J. E., Moscoso, G. J., & Campbell, S. C. (2000) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2000.00156.x · Cited by 128 · see citing works
Merriwether, D. A., Hall, W. W., Vahlne, A. G., & Ferrell, R. E. (1996) · PubMed Central · Cited by 127 · see citing works
Protection from intrauterine growth retardation in Tibetans at high altitude
Zamudio, S., Droma, T., Norkyel, K. Y., Acharya, G., Zamudio, J. A., Niermeyer, S., & MOORE, L. G. (1993) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330910207 · Cited by 125 · see citing works
Self-citationMaternal responses to long-term hypoxemia in sheep
Kitanaka, T., Gilbert, R. D., & Longo, L. D. (1989) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1989.256.6.r1340 · Cited by 125 · see citing works
Altitude, ethnic and sex differences in birth weight and length in Bolivia.
Jd, H., Ea, F., Stepick, C. D., Beard, J., & Hurtado, L. (1980) · PubMed · Cited by 114 · see citing works
Effects of chronic hypoxia in vivo on the expression of human placental glucose transporters
Zamudio, S., Baumann, M. U., & Illsley, N. P. (2006) · Placenta · doi:10.1016/j.placenta.2004.12.010 · Cited by 114 · see citing works
Self-citationAssociation of African Genetic Admixture with Resting Metabolic Rate and Obesity Among Women
Fernández, J. R., Shriver, M. D., Beasley, T. M., Rafla‐Demetrious, N., Parra, E. J., Albu, J., Nicklas, B. J., Ryan, A. S., McKeigue, P., Hoggart, C., et al. (2003) · Obesity Research · doi:10.1038/oby.2003.124 · Cited by 107 · see citing works
Melting curve analysis of SNPs (McSNP): a gel-free and inexpensive approach for SNP genotyping.
Akey, J., Sosnoski, D., Parra, E., Dios, S., Hiester, K., Su, B., Bonilla, C., Jin, L., & Shriver, M. (2001) · BioTechniques · doi:10.2144/01302tt05 · Cited by 106 · see citing works
Genetic conflicts in human pregnancy
Haig, D. (2007) · The biomedical & life sciences collection. · doi:10.69645/ivjc2529 · Cited by 98 · see citing works
High-altitude hypoxia and preeclampsia
Zamudio, S. (2007) · Frontiers in Bioscience · doi:10.2741/2286 · Cited by 97 · see citing works
Self-citationFactors affecting gas transfer across the placenta and the oxygen supply to the fetus.
Carter, A. M. (1989) · PubMed · Cited by 82 · see citing works
Ovine placentome morphology: Effect of high altitude, long-term hypoxia
Penninga, L., & Longo, L. D. (1998) · Placenta · doi:10.1016/s0143-4004(98)90008-x · Cited by 82 · see citing works
Brutsaert, T. D., Parra, E. J., Shriver, M. D., Gamboa, A. C., Rivera, M. C., & Lèon‐Velarde, F. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00105.2005 · Cited by 82 · see citing works
Fetal responses to long-term hypoxemia in sheep
Kitanaka, T., Alonso, J. G., Gilbert, R. D., Siu, B. L., Clemons, G. K., & Longo, L. D. (1989) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1989.256.6.r1348 · Cited by 81 · see citing works
Transepithelial Glucose Transport and Metabolism in BeWo Choriocarcinoma Cells
Vardhana, P. A., & Illsley, N. P. (2002) · Placenta · doi:10.1053/plac.2002.0857 · Cited by 78 · see citing works
Self-citationRegulation of placental metabolism by glucose supply
Hay, W. (1995) · Reproduction Fertility and Development · doi:10.1071/rd9950365 · Cited by 76 · see citing works
Blood volume expansion, preeclampsia, and infant birth weight at high altitude
Zamudio, S., Palmer, S. K., Dahms, T. E., Berman, J. C., McCullough, R. G., McCullough, R. E., & MOORE, L. G. (1993) · Journal of Applied Physiology · doi:10.1152/jappl.1993.75.4.1566 · Cited by 74 · see citing works
Self-citationUse of arterialized venous blood sampling during incremental exercise tests
McLoughlin, P., Popham, P., Linton, R. A. F., et al. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.73.3.937 · Cited by 68 · see citing works
Mitochondrial DNA analysis of ancient Peruvian highlanders
Shinoda, K., Adachi, N., Guillén, S. E., & Shimada, I. (2006) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20408 · Cited by 68 · see citing works
Placental Villus Morphology in Relation to Maternal Hypoxia at High Altitude
Espinoza, J., Sebire, N. J., McAuliffe, F., Krampl, E., & Nicolaides, K. H. (2001) · Placenta · doi:10.1053/plac.2001.0696 · Cited by 67 · see citing works
Rupert, J. L., & Hochachka, P. W. (2001) · High Altitude Medicine & Biology · doi:10.1089/152702901750265332 · Cited by 56 · see citing works
Brutsaert, T. D., Parra, E. J., Shriver, M. D., et al. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01088.2002 · Cited by 56 · see citing works
Uterine artery hemodynamic adaptations through the menstrual cycle into early pregnancy
Bernstein, I. M. (2002) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(01)01787-2 · Cited by 51 · see citing works
Martı́nez-Laso, J., Siles, N., Moscoso, J., Zamora, J., Serrano-Vela, J. I., R-A-Cachafeiro, J. I., Castro, M. J., Serrano‐Ríos, M., & Arnaiz‐Villena, A. (2005) · European Journal of Medical Genetics · doi:10.1016/j.ejmg.2005.04.005 · Cited by 50 · see citing works
Brutsaert, T. D., Parra, E. J., Shriver, M. D., et al. (2003) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10319 · Cited by 49 · see citing works
Ethnicity determination by names among the Aymara of Chile and Bolivia.
Chakraborty, R., Barton, S. A., Ferrell, R. E., & Schull, W. J. (1989) · PubMed · Cited by 48 · see citing works
Wehrenberg, W. B., Chaichareon, D. P., Dierschke, D. J., Rankin, J. H. G., & Ginther, O. J. (1977) · Biology of Reproduction · doi:10.1095/biolreprod17.1.148 · Cited by 38 · see citing works
Heavy birthweight in Native Indians of British Columbia.
Thomson, M. (1991) · PubMed · Cited by 36 · see citing works
Tripathy, V., & Gupta, R. (2005) · American Journal of Human Biology · doi:10.1002/ajhb.20400 · Cited by 34 · see citing works
Munroe, M., Shah, C. P., Badgley, R. F., & Bain, H. W. (1984) · Europe PMC (PubMed Central) · Cited by 32 · see citing works
Cellular life histories and bow tie biology
Lampl, M. (2004) · American Journal of Human Biology · doi:10.1002/ajhb.20094 · Cited by 27 · see citing works
Pathophysiology, cellular and molecular mechanisms of foetal growth retardation
Han, V. K. M. (1993) · Equine Veterinary Journal · doi:10.1111/j.2042-3306.1993.tb04802.x · Cited by 26 · see citing works
Nance, W. E. (1976) · Acta geneticae medicae et gemellologiae · doi:10.1017/s0001566000013933 · Cited by 25 · see citing works
Maternal endocrine adaptations to placental hormones in houmans
Evain‐Brion, D. (1999) · Acta Paediatrica · doi:10.1111/j.1651-2227.1999.tb14345.x · Cited by 23 · see citing works
Genetic and environmental adaptation in high altitude natives
Brutsaert, T. D. (2001) · Advances in experimental medicine and biology · doi:10.1007/978-1-4757-3401-0_10 · Cited by 13 · see citing works
Regulation of Fetal Amino Acid Metabolism: Substrate or Hormonal Regulation? ,
Liechty, E. A., & Denne, S. C. (1998) · Journal of Nutrition · doi:10.1093/jn/128.2.342s · Cited by 12 · see citing works
Uterine artery hemodynamic adaptations through the menstrual cycle into early pregnancy
Dickey, R. P. (2002) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(02)02110-5 · Cited by 10 · see citing works
Kuzawa, C. W. (1998) · doi:10.1002/(sici)1096-8644(1998)107:27+
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- Authors
- Zamudio, S., Postigo, L., Illsley, N. P., Rodriguez, C., Heredia, G., Brimacombe, M., Echalar, L., Torricos, T., Tellez, W., Maldonado, I., Balanza, E., Alvarez, T., Ameller, J., & Vargas, E.
- Affiliations
- Rutgers New Jersey Medical School (US)
- Universidad Mayor de San Andrés (BO)
- Corresponding author
- Zamudio, Stacy
- ORCID
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2007-07-05
- Volume
- 582
- Issue
- 2
- Pages
- 883-895
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC2075336
- OpenAlex
- W2128835155
- Cited by
- 97
- References
- 61
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 2 · 2023: 4 · 2022: 2 · 2021: 10 · 2020: 6 · 2019: 3 · 2018: 4 · 2017: 2 · 2016: 4 · 2015: 10 · 2014: 2 · 2013: 7 · 2012: 5
- FWCI
- 3.94
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD042737, HD 42737)
- 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 growth, high altitude, European immigrants, birth weight, uterine artery blood flow, European admixture, placental weight, gestational age
- MeSH terms
- Altitude, Arteries, Biological Availability, Birth Weight, Cross-Sectional Studies, Female, Humans, Indians, South American, Oxygen, Placenta, Pregnancy, Prospective Studies, Regional Blood Flow, Uterus, Ultrasonography, Prenatal, White People, Fetal Development
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