Effects of fetal growth restriction on lung development before and after birth: A morphometric analysis
Abstract
Our aim was to determine the effects of fetal growth restriction (FGR) during late gestation on the structure of the lungs in the fetus near term and at 8 weeks after birth. The studies were performed using two groups of pregnant sheep and their offspring. In both groups, FGR was induced by umbilico‐placental embolisation (UPE); for fetal studies, UPE was performed from 120 days of gestation until 140 days (term, ∼146 days), when fetuses were killed for tissue analysis. For postnatal studies, UPE continued from 120 days until delivery at term; postnatal lambs were killed at 8 weeks after birth for tissue analysis. UPE led to a thicker pulmonary blood‐air barrier at 140 days of gestation and this difference, which was due to a thickened basement membrane, was still present at 8 weeks after birth. At 8 weeks, we also observed a smaller number of alveoli per respiratory unit, thicker interalveolar septa, and a greater volume density of lung tissue in FGR lambs compared to controls. These changes would be expected to impair gas exchange and alter the mechanical properties of the lungs. Our data show that structural alterations in the lungs induced by placental insufficiency were more evident at 8 weeks of postnatal age than near term, indicating that the effects of FGR on the lung may become more serious with age and may affect respiratory health later in life. Pediatr Pulmonol. 2001; 32:201–210. © 2001 Wiley‐Liss, Inc.
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A growth-restricted fetus has fewer insulin-producing beta cells and reduced vascularization in the pancreas, and compromised structure and maturation of the brain, lungs, and liver.
“In addition, the pancreas has fewer insulin-producing beta cells and reduced vascularization (159, 340, 473), and the structure and maturation of the brain (142), lungs (358, 359, 424, 460) and liver (209, 474) are compromised.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [358]
Cites
Weibel, E. R. (1963) · Springer eBooks · doi:10.1007/978-3-642-87553-3 · Cited by 3,378 · see citing works
Barker, D. J., Godfrey, K. M., Fall, C., Osmond, C., Winter, P. D., & Shaheen, S. O. (1991) · BMJ · doi:10.1136/bmj.303.6804.671 · Cited by 889 · see citing works
The Lung: Scientific Foundations
Guidotti, T. L. (1997) · JAMA · doi:10.1001/jama.1997.03550230093050 · Cited by 759 · see citing works
The basement membrane in pathology.
Martínez-Hernández, A., & Amenta, P. S. (1983) · PubMed · Cited by 659 · see citing works
Morphological effects of chronic tracheal ligation and drainage in the fetal lamb lung.
Alcorn, D., Adamson, T. M., Lambert, T. F., MALONEY, J. E., Ritchie, B. C., & Robinson, P. M. (1977) · Europe PMC (PubMed Central) · Cited by 473 · see citing works
Emery, J. L., & Mithal, A. (1960) · Archives of Disease in Childhood · doi:10.1136/adc.35.184.544 · Cited by 432 · see citing works
Blood gases, pH, and lactate in appropriate- and small-for-gestational-age fetuses
Nicolaides, K. H., Economides, D. L., & Soothill, P. W. (1989) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(89)90770-9 · Cited by 390 · see citing works
A MORPHOMETRIC STUDY ON THE THICKNESS OF THE PULMONARY AIR-BLOOD BARRIER
Weibel, E. R., & Knight, B. W. (1964) · The Journal of Cell Biology · doi:10.1083/jcb.21.3.367 · Cited by 374 · see citing works
Prenatal asphyxia, hyperlacticaemia, hypoglycaemia, and erythroblastosis in growth retarded fetuses.
Soothill, P. W., Nicolaides, K. H., & Campbell, S. (1987) · BMJ · doi:10.1136/bmj.294.6579.1051 · Cited by 371 · see citing works
The postnatal growth of the rat lung II. Autoradiography
Kauffman, S. L., Burri, P. H., & Weibel, E. R. (1974) · The Anatomical Record · doi:10.1002/ar.1091800108 · Cited by 367 · see citing works
The postnatal growth of the rat lung III. Morphology
Burri, P. H. (1974) · The Anatomical Record · doi:10.1002/ar.1091800109 · Cited by 343 · see citing works
Impact of Intrauterine Growth Retardation and Body Proportionality on Fetal and Neonatal Outcome
Kramer, M. S., Olivier, M., McLean, F. H., Willis, D. M., & Usher, R. H. (1990) · PEDIATRICS · doi:10.1542/peds.86.5.707 · Cited by 323 · see citing works
Effects of prematurity and intrauterine growth on respiratory health and lung function in childhood.
Rona, R. J., Gulliford, M. C., & Chinn, S. (1993) · BMJ · doi:10.1136/bmj.306.6881.817 · Cited by 274 · see citing works
The radial alveolar count method of Emery and Mithal: a reappraisal 1--postnatal lung growth.
Cooney, T. P., & Thurlbeck, W. M. (1982) · Thorax · doi:10.1136/thx.37.8.572 · Cited by 246 · see citing works
Trudinger, B., Stevens, D., Connelly, A., Hales, J. R. S., Alexander, G., Bradley, L., Fawcett, A., & Thompson, R. S. (1987) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(87)80241-7 · Cited by 245 · see citing works
The postnatal development and growth of the human lung. II. Morphology
Zeltner, T. B., & Burri, P. H. (1987) · Respiration Physiology · doi:10.1016/0034-5687(87)90058-2 · Cited by 221 · see citing works
Relation of fetal growth to adult lung function in south India.
Stein, C., Kumaran, K., Fall, C. H. D., Shaheen, S. O., Osmond, C., & Barker, D. J. P. (1997) · Thorax · doi:10.1136/thx.52.10.895 · Cited by 192 · see citing works
Influence of Postnatally Administered Glucocorticoids on Rat Lung Growth
Tschanz, S. A., Damke, B., & Burri, P. H. (2009) · Biology of the Neonate · doi:10.1159/000244241 · Cited by 186 · see citing works
Brumley, G. W., Chernick, V., Hodson, W. A., Normand, C., Fenner, A., & Avery, M. E. (1967) · Journal of Clinical Investigation · doi:10.1172/jci105586 · Cited by 174 · see citing works
Tyson, J. E., Kennedy, K., Broyles, S., & Rosenfeld, C. R. (1995) · PEDIATRICS · doi:10.1542/peds.95.4.534 · Cited by 167 · see citing works
Formation of Pulmonary Alveoli and Gas-Exchange Surface Area: Quantitation and Regulation
MASSARO, G. D., & Massaro, D. (1996) · Annual Review of Physiology · doi:10.1146/annurev.ph.58.030196.000445 · Cited by 157 · see citing works
Electromyographic activity of the nonpregnant and pregnant sheep uterus
Harding, R., Poore, E. R., Bailey, A., Thorburn, G. D., Jansen, C. A. M., & Nathanielsz, P. W. (1982) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(16)32389-4 · Cited by 111 · see citing works
Self-citationFetal Growth Restriction at Term: Myth or Reality?
MINIOR, V. K. (1998) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(98)00118-5 · Cited by 102 · see citing works
Ounsted, M., Moar, V. A., & Scott, W. (1981) · Early Human Development · doi:10.1016/0378-3782(81)90017-7 · Cited by 99 · see citing works
Fetal endocrine responses to chronic placental embolization in the late-gestation ovine fetus
Gagnon, R. J., Challis, J. R. G., Johnston, L., & Fraher, L. J. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(94)70309-4 · Cited by 97 · see citing works
Joyce, B. J., Louey, S., Davey, M. G., Cock, M. L., Hooper, S. B., & Harding, R. (2001) · Pediatric Research · doi:10.1203/00006450-200111000-00018 · Cited by 86 · see citing works
Self-citationCock, M. L., Albuquerque, C. A., Joyce, B. J., Hooper, S. B., & Harding, R. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.108858 · Cited by 85 · see citing works
Self-citationNikolajev, K., Heinonen, K., Hakulinen, A., & Länsimies, E. (1998) · Pediatric Pulmonology · doi:10.1002/(sici)1099-0496(199806)25:6 · Cited by 58 · see citing works
Renal and amniotic fluid responses to umbilicoplacental embolization for 20 days in fetal sheep
Cock, M. L., & Harding, R. (1997) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1997.273.3.r1094 · Cited by 54 · see citing works
Self-citationRelationship of mesenchymal changes to alveolar epithelial cell differentiation in fetal rat lung
Adamson, I. R. (1992) · Anatomy and Embryology · doi:10.1007/bf00211826 · Cited by 24 · see citing works
Wąsowicz, M., Biczysko, W., Marszałek, A., Yokoyama, S., & Nakayama, I. (1998) · PubMed · Cited by 16 · see citing works
Maritz, G. S., Scott, L., & Thomas, R. ‐. (1993) · Cell Biology International · doi:10.1006/cbir.1993.1041 · Cited by 10 · see citing works
Self-citationStages in the development of the rat lung: morphometric, light and electron microscopic studies.
Gomi, T., Kimura‐Ono, A., Adriaensen, D., Timmermans, J., Scheuermann, D. W., Mh, D. G.-L., Kitazawa, Y., Kikuchi, Y., Naruse, H., & Kishi, K. (1994) · PubMed · Cited by 9 · see citing works
van der Horst, G., Kitchin, R., Curry, P. T., & ATHERTON, R. W. (1989) · Journal of Electron Microscopy Technique · doi:10.1002/jemt.1060120109 · Cited by 9 · see citing works
Lipsett, J., Cool, J. C., Runciman, S., Kennedy, J. D., Martin, A. J., Byard, R. W., & Ford, W. D. A. (1997) · Pediatric Pathology & Laboratory Medicine · doi:10.1080/107710497174480 · Cited by 6 · see citing works
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Self-citationMonz, D., Tutdibi, E., Mildau, C., Shen, J., Kasoha, M., Laschke, M. W., Roolfs, T., Schmiedl, A., Tschernig, T., Bieback, K., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074740 · Cited by 46 · see citing works
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Joss‐Moore, L. A., Wang, Y., Yu, X., Campbell, M. S., Callaway, C. W., McKnight, R. A., Wint, A., Dahl, M. J., Dull, R. O., Albertine, K. H., et al. (2011) · Physiological Genomics · doi:10.1152/physiolgenomics.00183.2010 · Cited by 46 · see citing works
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Zana‐Taïeb, E., Pham, H., Franco‐Montoya, M., Jacques, S., Letourneur, F., Baud, O., Jarreau, P. H., & Vaiman, D. (2014) · The Journal of Pathology · doi:10.1002/path.4470 · Cited by 39 · see citing works
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Zana‐Taïeb, E., Butruille, L., Franco‐Montoya, M., López, E., Vernier, F., Grandvuillemin, I., Evain‐Brion, D., Deruelle, P., Baud, O., Delacourt, C., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078326 · Cited by 34 · see citing works
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Thangaratnarajah, C., Dinger, K., Vohlen, C., Klaudt, C., Nawabi, J., Garcia, E. L., Kwapiszewska, G., Dobner, J., Nüsken, K., Koningsbruggen-Rietschel, S. V., et al. (2017) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00432.2016 · Cited by 21 · see citing works
Peralta, G. P., Abellan, A., Montazeri, P., Basterrechea, M., Esplugues, A., González‐Palacios, S., Roda, C., Santa‐Marina, L., Sunyer, J., Vrijheid, M., et al. (2020) · European Respiratory Journal · doi:10.1183/13993003.00157-2020 · Cited by 21 · see citing works
Ventilation-induced lung injury is not exacerbated by growth restriction in preterm lambs
Allison, B. J., Hooper, S. B., Coia, E., Zahra, V. A., Jenkin, G., Malhotra, A. K., Sehgal, A., Kluckow, M. R., Gill, A. W., Sozo, F., et al. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00328.2015 · Cited by 20 · see citing works
Kurata, H., Ochiai, M., Inoue, H., Kusuda, T., Fujiyoshi, J., Ichiyama, M., Wakata, Y., & Takada, H. (2018) · Pediatrics & Neonatology · doi:10.1016/j.pedneo.2018.11.007 · Cited by 20 · see citing works
Magnus, M. C., Stigum, H., Håberg, S. E., Nafstad, P. H. J., London, S. J., & Nystad, W. (2015) · PLoS ONE · doi:10.1371/journal.pone.0116362 · Cited by 19 · see citing works
The need to differentiate between adults and children when treating severe asthma
Fainardi, V., & Saglani, S. (2015) · Expert Review of Respiratory Medicine · doi:10.1586/17476348.2015.1068693 · Cited by 19 · see citing works
Adverse early-life environment impairs postnatal lung development in mice
Lai, P. Y., Jing, X., Michalkiewicz, T., Entringer, B., Ke, X., Majnik, A. V., Kriegel, A. J., Liu, P., Lane, R. H., & Konduri, G. G. (2019) · Physiological Genomics · doi:10.1152/physiolgenomics.00016.2019 · Cited by 18 · see citing works
Wang, K. C. W., Morton, J. S., Davidge, S. T., Larcombe, A. N., James, A. L., Donovan, G. M., & Noble, P. B. (2017) · Respirology · doi:10.1111/resp.13071 · Cited by 17 · see citing works
Altered lung function at mid-adulthood in mice following neonatal exposure to hyperoxia
Sozo, F., Horvat, J. C., Essilfie, A., O’Reilly, M., Hansbro, P. M., & Harding, R. (2015) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2015.07.004 · Cited by 17 · see citing works
Self-citationDiaz, V., Lebras-Isabet, M.-N., & Denjean, A. (2005) · Pediatric Research · doi:10.1203/01.pdr.0000179398.62365.43 · Cited by 17 · see citing works
Fetal Growth Restriction and Asthma: Is the Damage Done?
Wang, K. C. W., James, A. L., & Noble, P. B. (2021) · Physiology · doi:10.1152/physiol.00042.2020 · Cited by 14 · see citing works
Environmental Pollution and the Developing Lung
Voynow, J. A., & Auten, R. L. (2015) · Clinical Pulmonary Medicine · doi:10.1097/cpm.0000000000000095 · Cited by 14 · see citing works
Nawabi, J., Vohlen, C., Dinger, K., Thangaratnarajah, C., Klaudt, C., Garcia, E. L., Hirani, D., Karakaya, P. H., Macheleidt, I. F., Odenthal, M., et al. (2018) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00413.2017 · Cited by 14 · see citing works
Clara cell protein in full-term pregnancies: The influence of intrauterine growth restriction
Briana, D. D., Gourgiotis, D., Boutsikou, M., Baka, S. G., Marmarinos, A., Liosi, S., Hassiakos, D., & Malamitsi‐Puchner, A. (2010) · Pediatric Pulmonology · doi:10.1002/ppul.21305 · Cited by 13 · see citing works
Briana, D. D., Gourgiotis, D., Baka, S. G., Boutsikou, M., Vraila, V., Boutsikou, Τ., Hassiakos, D., & Malamitsi‐Puchner, A. (2010) · Reproductive Sciences · doi:10.1177/1933719110366165 · Cited by 13 · see citing works
Harding, R., Snibson, K. J., Reilly, M. O. R., & Maritz, G. S. (2009) · KARGER eBooks · doi:10.1159/000221155 · Cited by 13 · see citing works
Self-citationLi, L., Guo, J., Wang, Y., Yuan, Y., Feng, X., Gu, X., Jiang, S., Chen, C., Cao, Y., Sun, J., et al. (2024) · The Italian Journal of Pediatrics/Italian journal of pediatrics · doi:10.1186/s13052-024-01747-1 · Cited by 11 · see citing works
The effects of low-moderate dose prenatal ethanol exposure on the fetal and postnatal rat lung
Probyn, M. E., Cuffe, J. S. M., Zanini, S., & Moritz, K. M. (2013) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174413000305 · Cited by 11 · see citing works
Effect of Antenatal Steroids on Haemodynamics in the Normally Grown and Growth Restricted Fetus
Miller, S., & Wallace, E. M. (2013) · Current Pediatric Reviews · doi:10.2174/1573396311309010014 · Cited by 11 · see citing works
The interdependence of cell volume and resting membrane potential
Fraser, J. A., & Huang, C. L.-H. (2005) · Physiology News · doi:10.36866/pn.58.21 · Cited by 10 · see citing works
Placental Findings and Effect of Prophylactic Hydrocortisone in Extremely Preterm Infants
Héneau, A., Guimiot, F., Mohamed, D., Novais, A. R. B., Alberti, C., Baud, O., & for the PREMILOC Trial study group (2018) · PEDIATRICS · doi:10.1542/peds.2017-1788 · Cited by 9 · see citing works
Intrauterine growth restriction affects diaphragm function in adult female and male mice
Francis, M. R., Pinniger, G. J., Noble, P. B., & Wang, K. C. W. (2019) · Pediatric Pulmonology · doi:10.1002/ppul.24519 · Cited by 9 · see citing works
The Influence of Nutrition on Lung Development before and after Birth
Harding, R., & Matteo, R. M. D. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-799941-8.00019-5 · Cited by 9 · see citing works
Self-citationPhysical, Endocrine, and Growth Factors in Lung Development
Wallace, M. J., Hooper, S. B., & McDougall, A. R. A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-799941-8.00008-0 · Cited by 9 · see citing works
Bajwa, R., Raju, M. N. P., Govande, V. P., Hemingway, M., Hammonds, K. A. P., & Vora, N. (2022) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2022.2086794 · Cited by 7 · see citing works
Valenzuela, I. J., Basurto, D., Regin, Y., Gie, A. G., der Veeken, L. V., Vergote, S., Muñoz‐Moreno, E., Leszczyński, B., Tielemans, B., Velde, G. V., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-22895-6 · Cited by 7 · see citing works
Mechanosensory transduction in the enteric nervous system
Smith, T. K., Spencer, N. J., & Hennig, G. W. (2005) · Physiology News · doi:10.36866/pn.58.23 · Cited by 7 · see citing works
Programmierung durch intrauterine Mangelversorgung
Alcazar, M. A. A., Nüsken, E., & Nüsken, K. (2015) · Monatsschrift Kinderheilkunde · doi:10.1007/s00112-015-3420-x · Cited by 5 · see citing works
Physiologic Mechanisms of Normal and Altered Lung Growth Before and After Birth
Wallace, M. J., Hooper, S. B., & Harding, R. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-35214-7.00063-9 · Cited by 5 · see citing works
Self-citationPhysiologic Mechanisms of Normal and Altered Lung Growth
Harding, R., & Hooper, S. B. (2004) · Elsevier eBooks · doi:10.1016/b978-0-7216-9654-6.50081-3 · Cited by 5 · see citing works
Self-citationDifferential Biomechanical Development of Elastic Tissues in the Bovine Fetus
Walter, E. J., & Wells, S. (2009) · Annals of Biomedical Engineering · doi:10.1007/s10439-009-9847-2 · Cited by 4 · see citing works
Prenatal Origins of Obstructive Airway Disease: Starting on the Wrong Trajectory?
Wang, K. C. W., James, A. L., Donovan, G. M., & Noble, P. B. (2024) · Comprehensive physiology · doi:10.1002/cphy.c230019 · Cited by 4 · see citing works
Changes in Neonatal Practice and Temporal Trends in Bronchopulmonary Dysplasia
Dickenson, G., Sikdar, O., Bhat, R., Nanjundappa, M., Harris, C., & Greenough, A. (2025) · American Journal of Perinatology · doi:10.1055/a-2672-2769 · Cited by 3 · see citing works
Sexual dimorphism in lung transcriptomic adaptations in fetal alcohol spectrum disorders
Naik, V. D., Millikin, D. J., Moussa, D. N., Jiang, H., Carabulea, A. L., Janeski, J. D., Ding, J., Chen, K., Rodríguez‐García, M., Jaiman, S., et al. (2025) · Respiratory Research · doi:10.1186/s12931-025-03094-z · Cited by 2 · see citing works
Impact of being small for gestational age in neonates born below 600 g birth weight
Jernej, R., Fuiko, R., Binder, J., Kiss, H., Klebermaß-Schrehof, K., Grill, A., Berger, A., & Goeral, K. (2025) · Pediatric Research · doi:10.1038/s41390-025-04202-x · Cited by 2 · see citing works
Retard de croissance intra-utérin et développement pulmonaire : approche expérimentale et clinique
Zana‐Taïeb, E., Aubelle, M., Ayoubi, M. E., López, E., & Jarreau, P. H. (2013) · Archives de Pédiatrie · doi:10.1016/j.arcped.2013.06.019 · Cited by 2 · see citing works
Effect of Environment and Aging on the Pulmonary Surfactant System
Orgeig, S., Morrison, J. L., & Daniels, C. B. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-799941-8.00026-2 · Cited by 2 · see citing works
Is Umbilical Cord Blood Therapy an Effective Treatment for Early Lung Injury in Growth Restriction?
Allison, B. J., Youn, H., Malhotra, A. K., McDonald, C. A., Castillo-Meléndez, M., Pham, Y., Sutherland, A. E., Jenkin, G., Polglase, G. R., & Miller, S. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00086 · Cited by 2 · see citing works
Epigenetics and the Developmental Origins of Lung Disease
Joss‐Moore, L. A., Lane, R. H., & Albertine, K. H. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-799941-8.00016-x · Cited by 2 · see citing works
Correani, A., Lanciotti, L., Giorgetti, C., Burattini, I., Fattore, S., Esposito, A., Costa, S., Tirone, C., Vento, G., & Carnielli, V. P. (2026) · European Journal of Pediatrics · doi:10.1007/s00431-025-06715-3 · Cited by 1 · see citing works
Glucocorticoids in pregnancy: a master-switch for fetal maturation
Tan, Y., Stark, M. J., Clifton, V. L., Wiese, M. D., Morrison, J. L., & Gatford, K. L. (2026) · Endocrine Reviews · doi:10.1210/endrev/bnag015 · Cited by 1 · see citing works
Restricted growth during early development: long-term effects on lung structure and function
Harding, R., & Sozo, F. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-91824-4.00002-2 · Cited by 1 · see citing works
Self-citationPulmonary Manifestations of Systemic Disorders
Inselman, L. S. (2008) · Elsevier eBooks · doi:10.1016/b978-032304048-8.50079-7 · Cited by 1 · see citing works
- Authors
- Maritz, G. S., Cock, M. L., Louey, S., Joyce, B. J., Albuquerque, C. A., & Harding, R.
- Affiliations
- University of the Western Cape (ZA)
- Monash University (AU)
- Corresponding author
- Maritz, G.S.
- Venue
- Pediatric Pulmonology
- Publisher
- Wiley
- Published
- 2001-08-28
- Volume
- 32
- Issue
- 3
- Pages
- 201-210
- ISSN
- 1099-0496 (ISSN-L)
- 8755-6863
- OpenAlex
- W1995602286
- Cited by
- 128
- References
- 35
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 8 · 2023: 2 · 2022: 4 · 2021: 1 · 2020: 4 · 2019: 4 · 2018: 6 · 2017: 5 · 2016: 4 · 2015: 12 · 2014: 8 · 2013: 8 · 2012: 6
- FWCI
- 3.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Pediatric Pulmonology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Neonatal Respiratory Health Research
- Keywords
- fetal growth restriction, lung development, placental insufficiency, basement membrane thickening, alveolar number, interalveolar septa, postnatal lung development, sheep model, respiratory health
- MeSH terms
- Animals, Animals, Newborn, Anthropometry, Female, Fetal Growth Retardation, Lung, Placental Insufficiency, Pregnancy, Pulmonary Alveoli, Sheep
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