Allometric studies on growth and development of the human placenta: growth of tissue compartments and diffusive conductances in relation to placental volume and fetal mass
Open accessAbstract
Correlations between placental size and fetal mass during gestation fail to account for changes in composition that accompany placental growth and maturation. This study uses stereological data on the sizes of different tissue compartments in human placentas from 10 weeks of gestation to term and relates them to placental volume and to fetal mass by means of allometric analysis. In addition, tissue dimensions are used to calculate a physiological transport measure (diffusive conductance) for the villous membrane. Histological sections randomly sampled from placentas and analysed stereologically provided estimates of structural quantities (volumes, exchange surface areas, lengths, numbers of nuclei, diffusion distances). These data were combined with a physicochemical quantity (Krogh's diffusion coefficient) in order to estimate oxygen diffusive conductances for the villous membrane and its two components (trophoblast and stroma). Allometric relationships between these quantities and placental volume or fetal mass were obtained by linear regression analyses after log‐transformation. Placental tissues had different growth trajectories: most grew more rapidly than placental volume and all grew more slowly than fetal mass. Diffusion distances were inversely related to placental and fetal size. Differential growth impacted on diffusive conductances, which, again, did not improve commensurately with placental volume but did match exactly growth of the fetus. Findings show that successful integration between supply and demand can be achieved by differential tissue growth. Allometric analysis of results from recent studies on the murine placenta suggest further that diffusive conductances may also be matched to fetal mass during gestation and to fetal mass at term across species.
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The theoretical diffusing capacity for oxygen expressed per kg of fetal weight remains constant across gestational age.
“It is notable that the theoretical diffusing capacity for oxygen expressed per kg of fetal weight remains constant across gestational age (364, 368), suggesting placental development determines the rate of fetal growth or that the two are closely co-regulated.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [364]
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Cites
The efficiency of systematic sampling in stereology and its prediction *
Gundersen, H., & Jensen, E. B. V. (1987) · Journal of Microscopy · doi:10.1111/j.1365-2818.1987.tb02837.x · Cited by 3,586 · see citing works
The Pathology of the Human Placenta
Benirschke, K., & Driscoll, S. G. (1967) · Springer eBooks · doi:10.1007/978-1-4612-9809-0 · Cited by 2,123 · see citing works
Unbiased Stereology: Three-Dimensional Measurement in Microscopy
Howard, C. V., & Reed, M. (1998) · Cited by 1,149 · see citing works
Unbiased Stereology. Three‐Dimensional Measurement in Microscopy.
Sandau, K. (1999) · Journal of Microscopy · doi:10.1046/j.1365-2818.1999.0429a.x · Cited by 890 · see citing works
Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy.
Rodesch, F., Simon, P., Donner, C., & Jauniaux, E. R. M. (1992) · PubMed · Cited by 753 · 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
Oxygen and placental villous development: Origins of fetal hypoxia
Kingdom, J. C., & Kaufmann, P. (1997) · Placenta · doi:10.1016/s0143-4004(97)90000-x · Cited by 581 · see citing works
Aspects of Human Fetoplacental Vasculogenesis and Angiogenesis. II. Changes During Normal Pregnancy
Kaufmann, P., Mayhew, T. M., & Jones, D. S. (2003) · Placenta · doi:10.1016/j.placenta.2003.10.009 · Cited by 437 · see citing works
Self-citationPathology of the Human Placenta
Benirschke, K., & Kaufmann, P. (2000) · Springer eBooks · doi:10.1007/978-1-4757-4199-5 · Cited by 400 · see citing works
Aspects of Human Fetoplacental Vasculogenesis and Angiogenesis. I. Molecular Regulation
Jones, D. S., Kaufmann, P., & Mayhew, T. M. (2003) · Placenta · doi:10.1016/j.placenta.2003.10.004 · Cited by 359 · see citing works
Self-citationA review of recent advances in stereology for quantifying neural structure
Mayhew, T. M. (1992) · Journal of Neurocytology · doi:10.1007/bf01191700 · Cited by 330 · see citing works
Self-citationMayhew, T. M., Jones, D. S., & Kaufmann, P. (2003) · Placenta · doi:10.1016/j.placenta.2003.10.010 · Cited by 328 · see citing works
Self-citationJauniaux, E. R. M., Watson, A. L., & Burton, G. J. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.111935 · Cited by 316 · see citing works
Developmental Dynamics of the Definitive Mouse Placenta Assessed by Stereology1
Coan, P. M., Ferguson-Smith, A. C., & Burton, G. J. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.024166 · Cited by 296 · see citing works
Effect of nutrient intake during pregnancy on fetal and placental growth and vascular development
Redmer, D. A., Wallace, J. M., & Reynolds, L. P. (2004) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2004.06.006 · Cited by 294 · see citing works
The new stereological methods for interpreting functional morphology from slices of cells and organs
Mayhew, T. (1991) · Experimental Physiology · doi:10.1113/expphysiol.1991.sp003533 · Cited by 273 · see citing works
Self-citationSOOTHILL, P. W., Nicolaides, K. H., Rodeck, C. H., & Campbell, S. C. (1986) · Fetal Diagnosis and Therapy · doi:10.1159/000262264 · Cited by 265 · see citing works
SOOTHILL, P. W., Nicolaides, K. H., Rodeck, C. H., & Campbell, S. C. (1988) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-198843010-00005 · Cited by 227 · see citing works
Jackson, M., Mayhew, T. M., & Boyd, P. A. (1992) · Placenta · doi:10.1016/0143-4004(92)90060-7 · Cited by 158 · see citing works
Self-citationBurton, G. J., Reshetnikova, O. S., Milovanov, A. P., & Teleshova, O. V. (1996) · Placenta · doi:10.1016/s0143-4004(05)80643-5 · Cited by 149 · cited 1× · see citing works
“They are maintained in maternal anaemia and preeclampsia (Reshetnikova et al. 1995; Burton et al. 1996) and increased at high altitude (Mayhew et al. 1990; Reshetnikova et al. 1994) and during maternal diabetes (Mayhew et al. 1993b).”
BackgroundSimpson, R. A., Mayhew, T. M., & Barnes, P. (1992) · Placenta · doi:10.1016/0143-4004(92)90055-x · Cited by 141 · see citing works
Self-citationBush, P. G., Mayhew, T. M., Abramovich, D. R., Aggett, P. J., Burke, M. D., & Page, K. (2000) · Placenta · doi:10.1053/plac.1999.0470 · Cited by 138 · see citing works
Self-citationStereologic examination of placentas from mothers who smoke during pregnancy
Larsen, L. G., Clausen, H. V., & Jönsson, L. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.120481 · Cited by 136 · see citing works
Gas exchange in the pregnant uterus
Metcalfe, J., Bartels, H., & Moll, W. (1967) · Physiological Reviews · doi:10.1152/physrev.1967.47.4.782 · Cited by 135 · see citing works
Mayhew, T. M. (2002) · Placenta · doi:10.1053/plac.2002.0865 · Cited by 132 · see citing works
Self-citationReshetnikova, O. S., Burton, G. J., & Milovanov, A. P. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(94)90402-2 · Cited by 127 · see citing works
Distribution of Membrane Thickness Determined By Lineal Analysis
Gundersen, H. J. G., Jensen, T. B., & Østerby, R. (1978) · Journal of Microscopy · doi:10.1111/j.1365-2818.1978.tb00091.x · Cited by 127 · see citing works
Quantitative Studies of Human Placenta I.
Laga, E. M., Driscoll, S. G., & Munro, H. N. (2009) · Biology of the Neonate · doi:10.1159/000240605 · Cited by 117 · see citing works
Jackson, M. R., Mayhew, T. M., & Haas, J. D. (1987) · Placenta · doi:10.1016/0143-4004(87)90077-4 · Cited by 112 · see citing works
Self-citationVentilatory Thresholds during a Graded Exercise Test
BHAMBHANI, Y. N., & Singh, M. (2009) · Respiration · doi:10.1159/000194758 · Cited by 103 · see citing works
Ruminant models of prenatal growth restriction
Anthony, R., Scheaffer, A., Wright, C., & Regnault, T. R. H. (2019) · Bioscientifica Proceedings · doi:10.1530/biosciprocs.5.014 · Cited by 98 · see citing works
Maternal Cigarette Smoking and Oxygen Diffusion Across the Placenta
Bush, P. G., Mayhew, T. M., Abramovich, D. R., Aggett, P. J., Burke, M. D., & Page, K. (2000) · Placenta · doi:10.1053/plac.2000.0571 · Cited by 83 · see citing works
Self-citationMayhew, T. M., Jackson, M. R., & Haas, J. D. (1986) · Placenta · doi:10.1016/s0143-4004(86)80003-0 · Cited by 83 · see citing works
Self-citationReshetnikova, O. S., Burton, G. J., & Васильевна, Т. О. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)90330-5 · Cited by 82 · see citing works
Mayhew, T. M., Jackson, M. R., & Boyd, P. A. (1993) · Placenta · doi:10.1016/s0143-4004(05)80248-6 · Cited by 80 · see citing works
Self-citationEvolution of brain size in neonatal and adult placental mammals: A theoretical approach
Hofman, M. A. (1983) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(83)80011-3 · Cited by 80 · see citing works
Oxygen diffusive conductances of human placentae from term pregnancies at low and high altitudes
Mayhew, T. M., Jackson, M. R., & Haas, J. D. (1990) · Placenta · doi:10.1016/s0143-4004(05)80195-x · Cited by 77 · see citing works
Self-citationJackson, M., Mayhew, T. M., & Haas, J. D. (1987) · PubMed · Cited by 72 · see citing works
Self-citationMayhew, T. M., Joy, C. F., & Haas, J. D. (1984) · PubMed · Cited by 65 · see citing works
Self-citationJackson, M. R., Joy, C. F., Mayhew, T. M., & Haas, J. D. (1985) · Placenta · doi:10.1016/s0143-4004(85)80054-0 · Cited by 65 · see citing works
Self-citationEstimation of human fetal-placental unit metabolic rate by application of the Bohr principle.
Bonds, D. R., Lo, C., Cheek, T. G., Hägerdal, M., Bb, G., & Sg, G. (1986) · PubMed · Cited by 60 · see citing works
Mayhew, T. M., Wadrop, E., & Simpson, R. A. (1994) · PubMed · Cited by 51 · see citing works
Self-citationOxygen diffusive conductance in placentae from control and diabetic women
Mayhew, T. M., Sørensen, F. B., Klebe, J. G., & Jackson, M. (1993) · Diabetologia · doi:10.1007/bf02374479 · Cited by 46 · see citing works
Self-citationQuantitative Studies of Human Placenta II.
Laga, E. M., Driscoll, S. G., & Munro, H. N. (2009) · Biology of the Neonate · doi:10.1159/000240606 · Cited by 39 · see citing works
Ansari, T. (2003) · Placenta · doi:10.1016/s0143-4004(03)00044-4 · Cited by 29 · see citing works
Relationship between Metabolic Rate and Body Size in Fetal Life
Bell, A. W., Battaglia, F. C., Makowski, E. L., & Meschia, G. (2009) · Biology of the Neonate · doi:10.1159/000242100 · Cited by 25 · see citing works
Mayhew, T. M. (1991) · PubMed · Cited by 22 · see citing works
Self-citationAnsari, T., Gillan, J., Condell, D., et al. (2003) · Early Human Development · doi:10.1016/j.earlhumdev.2003.11.004 · Cited by 10 · see citing works
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Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
- Authors
- Mayhew, T. M.
- Affiliations
- University of Nottingham (GB)
- Corresponding author
- Mayhew, Terry M.
- Venue
- Journal of Anatomy
- Publisher
- Wiley
- Published
- 2006-05-26
- Volume
- 208
- Issue
- 6
- Pages
- 785-794
- ISSN
- 0021-8782 (ISSN-L)
- 1469-7580
- PMC
- PMC2100236
- OpenAlex
- W1987030937
- Cited by
- 31
- References
- 48
- Citations by year
- 2026: 3 · 2024: 2 · 2021: 1 · 2020: 4 · 2019: 2 · 2018: 1 · 2017: 1 · 2016: 1 · 2015: 3 · 2013: 1 · 2012: 1
- FWCI
- 4.26
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Anatomy (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- human placenta, placental development, allometry, placental volume, oxygen diffusion, trophoblast, placental stroma, diffusion distance, stereology, placental maturation, fetal oxygenation
- MeSH terms
- Biological Transport, Female, Fetal Blood, Fetus, Hemoglobins, Humans, Oxyhemoglobins, Placenta, Placentation, Pregnancy, Pregnancy Trimesters, Regression Analysis, Trophoblasts, Placental Circulation, Fetal Development
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