The DOI matches its Crossref record; 36 of the 36 references it cites were found in a registry or an index.
Augmented uterine artery blood flow and oxygen delivery protect Andeans from altitude-associated reductions in fetal growth
Open accessAbstract
The effect of high altitude on reducing birth weight is markedly less in populations of high- (e.g., Andeans) relative to low-altitude origin (e.g., Europeans). Uterine artery (UA) blood flow is greater during pregnancy in Andeans than Europeans at high altitude; however, it is not clear whether such blood flow differences play a causal role in ancestry-associated variations in fetal growth. We tested the hypothesis that greater UA blood flow contributes to the protection of fetal growth afforded by Andean ancestry by comparing UA blood flow and fetal growth throughout pregnancy in 137 Andean or European residents of low (400 m; European n = 28, Andean n = 23) or high (3,100–4,100 m; European n = 51, Andean n = 35) altitude in Bolivia. Blood flow and fetal biometry were assessed by Doppler ultrasound, and maternal ancestry was confirmed, using a panel of 100 ancestry-informative genetic markers (AIMs). At low altitude, there were no ancestry-related differences in the pregnancy-associated rise in UA blood flow, fetal biometry, or birth weight. At high altitude, Andean infants weighed 253 g more than European infants after controlling for gestational age and other known influences. UA blood flow and O 2 delivery were twofold greater at 20 wk in Andean than European women at high altitude, and were paralleled by greater fetal size. Moreover, variation in the proportion of Indigenous American ancestry among individual women was positively associated with UA diameter, blood flow, O 2 delivery, and fetal head circumference. We concluded that greater UA blood flow protects against hypoxia-associated reductions in fetal growth, consistent with the hypothesis that genetic factors enabled Andeans to achieve a greater pregnancy-associated rise in UA blood flow and O 2 delivery than European women at high altitude.
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“However, in the majority of studies, the normal pregnancy-induced rise in uterine blood flow is blunted at high altitude in association with a reduced diameter of the uterine arteries and/or lower nitric oxide synthesis, regardless of ancestry (294, 295, 577, 603, 604).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [295]
In the citing paper
“Pregnant Tibetan women have higher uterine artery diameters and blood velocity than Han women at high altitude (107, 389), while Andean women have twice the increment in uterine artery diameter during pregnancy than European women at high altitude (295, 577, 604).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [295]
In the citing paper
“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 [295]
In the citing paper
“Indeed, in Andean women, the increase in uterine blood flow during pregnancy at high altitude can exceed that seen at low altitude (69, 295).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [295]
In the citing paper
“This results in differences in uterine blood flow between Andean and European women, which are detectable at 20 weeks of gestation before fetal growth slows (295).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [295]
In the citing paper
“In human infants near term, the diameters of the umbilical vein and artery are both smaller at high than low altitude, which results in a lower absolute blood flow in the umbilical circulation, irrespective of ethnicity (295, 443).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [295]
In the citing paper
“In human populations, the adverse consequences of high altitude on uterine artery diameter and uterine blood flow are less pronounced with long than short ancestry at high altitude (295, 387).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [295]
In the citing paper
“Thus, in some studies of Andeans, absolute oxygen delivery to the gravid uterus at high altitude is maintained or even increased above lowland values, despite the low maternal pO2, while in others the uterine oxygen supply is less at high than low altitude irrespective of ancestry (69, 295, 443, 604).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [295]
Citations
Cites
The Physiology of Reproduction
Legendre, M., & Jalabert, B. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-2-176_1 · Cited by 7,876
The Developmental Origins of Adult Disease
Barker, D. J. P. (2004) · Journal of the American College of Nutrition · doi:10.1080/07315724.2004.10719428 · Cited by 1,854
Villar, J., Valladares, E. C., WOJDYLA, D. M., Zavaleta, N., Carroli, G., Velazco, A., Shah, A., Campodónico, L., Bataglia, V., Faúndes, A., et al. (2006) · The Lancet · doi:10.1016/s0140-6736(06)68704-7 · Cited by 883
Fetal growth and perinatal viability in California.
Williams, R. L., Creasy, R. K., Cunningham, G. C., Hawes, W. E., Norris, F. D., & Tashiro, M. (1982) · PubMed · Cited by 807
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
Self-citationEDITORIAL: The developmental origins of adult disease
Barker, D. J. P. (2003) · European Journal of Epidemiology · doi:10.1023/a:1025388901248 · Cited by 407
Jensen, G. M., & MOORE, L. G. (1997) · American Journal of Public Health · doi:10.2105/ajph.87.6.1003 · Cited by 355
Self-citationPalmer, S. K., Zamudio, S., Coffin, C. T., Parker, S. B., Stamm, E. R., & MOORE, L. G. (1992) · PubMed · Cited by 267
Self-citationThe genomic distribution of population substructure in four populations using 8,525 autosomal SNPs
Shriver, M., Kennedy, G., Parra, E., Lawson, H. A., Sonpar, V. A., Huang, J., Akey, J., & Jones, K. (2004) · Human Genomics · doi:10.1186/1479-7364-1-4-274 · Cited by 253
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
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Go, H., Hashimoto, K., Kyozuka, H., Maeda, H., Nishigori, H., Satô, A., Ogata, Y., Kuse, M., Fujimori, K., Yasumura, S., et al. (2022) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2022.2130237 · Cited by 1
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Julian, C. G., Wilson, M. J., & MOORE, L. G. (2009)
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(2019) · Wiley eBooks · doi:10.1002/9781118768853.refs
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Baumgartner, E. (2018) · Springer eBooks · doi:10.1007/978-3-662-56396-0_9
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Toledo‐Jaldin, L., Gomez, R., Lazo‐Vega, L., Larrea, A., Vásquez, A., Ormachea-Orellana, W., Miranda‐Garrido, V., & Julian, C. G. (2025) · American Journal of Perinatology Reports · doi:10.1055/a-2689-2550
Self-citationLi, J., Zhang, G., Wang, X., Qiangba, C., Song, X., Lin, R., Huang, C., Yang, X., Ning, S., Zhang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24709038
Agüero, P., Elizabeth, R., Lomaglio, & Lomaglio, D. B. (2025) · International Journal of Pediatrics and Child Health · doi:10.12974/2311-8687.2025.13.08
Tang, X., Zhang, B., Jian, W., Zhou, K., Wang, P., Zhaxi, J., Wang, X., Wang, L., Wen, X., Zhao, L., et al. (2026) · European Journal of Nutrition · doi:10.1007/s00394-026-03911-1
Villamonte‐Calanche, W., Salazar-Zegarra, M. A., Miranda-Solís, F., & Jeri, M. (2026) · High Altitude Medicine & Biology · doi:10.1177/15578682261444625
Wang, X., Zhang, X., Juan, J., Gao, D., Yang, H., Zhang, M., Chen, X., Wang, X., Ma, Y., Teng, Y., et al. (2026) · Journal of Global Health · doi:10.7189/jogh.16.04168
Arenas, G. A., Herrera, E. A., Krause, B. J., Giussani, D. A., Julian, C. G., MOORE, L. G., & Lorca, R. A. (2026) · Physiological Reviews · doi:10.1152/physrev.00003.2026 · Cited by 1
Self-citation
Metadata
- Authors
- Julian, C. G., Wilson, M. J., Lopez, M., Yamashiro, H., Tellez, W., Rodriguez, A., Bigham, A. W., Shriver, M. D., Rodriguez, C., Vargas, E., & Moore, L. G.
- Affiliations
- University of Colorado Denver (US)
- Pennsylvania State University (US)
- Universidad Mayor de San Andrés (BO)
- Wake Forest University (US)
- ORCID
- Venue
- American Journal of Physiology-Regulatory, Integrative and Comparative Physiology
- Publisher
- American Physiological Society
- Published
- 2009-05
- Volume
- 296
- Issue
- 5
- Pages
- R1564-R1575
- ISSN
- 0363-6119 (ISSN-L)
- 1522-1490
- PMC
- PMC2689835
- OpenAlex
- W2139645408
- Cited by
- 141
- References
- 36
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 8 · 2023: 5 · 2022: 11 · 2021: 9 · 2020: 9 · 2019: 6 · 2018: 4 · 2017: 6 · 2016: 5 · 2015: 15 · 2014: 5 · 2013: 13 · 2012: 8
- FWCI
- 5.26
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal of Physiology-Regulatory, Integrative and Comparative Physiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service (HLBI-079647, HLBI-60131)
- Fogarty International Center (TW 01188, R03TW007957, R03TW001188)
- Topics
- Health Sciences › Medicine › Physiology (medical) › 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
- uterine artery blood flow, fetal growth, high altitude, birth weight, fetal oxygen delivery, hypoxia, fetal biometry, fetal head circumference, Indigenous American ancestry, maternal ancestry, pregnancy, Doppler ultrasound
- MeSH terms
- Adult, Altitude, Arteries, Biological Transport, Birth Weight, Bolivia, Europe, Female, Humans, Oxygen, Pregnancy, Regional Blood Flow, Uterus, Case-Control Studies, White People, American Indian or Alaska Native, Fetal Development
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