Early lung development: lifelong effect on respiratory health and disease

Stocks, Janet; Hislop, Alison; Sonnappa, Samatha

doi:10.1016/s2213-2600(13)70118-8

Cited by 390Asthma and respiratory diseasesChronic Obstructive Pulmonary Disease (COPD) ResearchBirth, Development, and Health

Early lung development: lifelong effect on respiratory health and disease

Stocks, Janet, Hislop, Alison, Sonnappa, Samatha·2013·The Lancet Respiratory Medicine

DOI 10.1016/s2213-2600(13)70118-8

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Abstract

Interest in the contribution of changes in lung development during early life to subsequent respiratory morbidity is increasing. Most evidence of an association between adverse intrauterine factors and structural effects on the developing lung is from animal studies. Such evidence has been augmented by epidemiological studies showing associations between insults to the developing lung during prenatal and early postnatal life and adult respiratory morbidity or reduced lung function, and by physiological studies that have elucidated mechanisms underlying these associations. The true effect of early insults on subsequent respiratory morbidity can be understood only if the many prenatal and postnatal factors that can affect lung development are taken into account. Adverse factors affecting lung development during fetal life and early childhood reduce the attainment of maximum lung function and accelerate lung function decline in adulthood, initiating or worsening morbidity in susceptible individuals. In this Review, we focus on factors that adversely affect lung development in utero and during the first 5 years after birth, thereby predisposing individuals to reduced lung function and increased respiratory morbidity throughout life. We focus particularly on asthma and COPD.

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Tobacco exposure during pregnancy reduces pulmonary function.
“Maternal smoking during pregnancy has adverse effects outside the central nervous system, most notably on lung development, causing lifelong decreases in pulmonary function.”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [199]
Maternal smoking during pregnancy causes lifelong decreases in pulmonary function.
“Maternal smoking during pregnancy has adverse effects outside the central nervous system, most notably on lung development, causing lifelong decreases in pulmonary function.”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [199]

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Self-citation
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Tomato juice protects the lungs of the offspring of female rats exposed to nicotine during gestation and lactation
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Vitamin A deficiency disturbs collagen IV and laminin composition and decreases matrix metalloproteinase concentrations in rat lung. Partial reversibility by retinoic acid
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Maternal allergen exposure reprograms the developmental lung transcriptome in atopic and normoresponsive rat pups
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Does Breastfeeding Impact Lung Function and Asthma Risk?
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Can asthma be predicted from an early age?
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COPD in Non-smokers
Lam, H. K. B., Kurmi, O., & Ayres, J. G. (2012) · Humana Press eBooks · doi:10.1007/978-1-62703-149-3_14 · Cited by 1 · see citing works

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Lung-Function Trajectories Leading to Chronic Obstructive Pulmonary Disease
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Mesenchymal Stromal Cell Exosomes Ameliorate Experimental Bronchopulmonary Dysplasia and Restore Lung Function through Macrophage Immunomodulation
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Childhood predictors of lung function trajectories and future COPD risk: a prospective cohort study from the first to the sixth decade of life
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Airway remodeling in asthma: what really matters
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Preterm Birth and Childhood Wheezing Disorders: A Systematic Review and Meta-Analysis
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Understanding the Short- and Long-Term Respiratory Outcomes of Prematurity and Bronchopulmonary Dysplasia
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Post-Tuberculosis Lung Disease: Clinical Review of an Under-Recognised Global Challenge
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Post-tuberculosis lung health: perspectives from the First International Symposium
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Pulmonary Effects of Maternal Smoking on the Fetus and Child: Effects on Lung Development, Respiratory Morbidities, and Life Long Lung Health
McEvoy, C. T., & Spindel, E. R. (2016) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2016.08.005 · Cited by 262 · see citing works
Respiratory effects of air pollution on children
Goldizen, F. C., Sly, P. D., & Knibbs, L. D. (2015) · Pediatric Pulmonology · doi:10.1002/ppul.23262 · Cited by 217 · see citing works
Two-Year Follow-Up Outcomes of Premature Infants Enrolled in the Phase I Trial of Mesenchymal Stem Cells Transplantation for Bronchopulmonary Dysplasia
Ahn, S. Y., Chang, Y. S., Kim, J. H., Sung, S. I., & Park, W. S. (2017) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2017.02.061 · Cited by 202 · see citing works
A Distinct Low Lung Function Trajectory from Childhood to the Fourth Decade of Life
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Clinical standards for the assessment, management and rehabilitation of post-TB lung disease
Migliori, G. B., Marx, F. M., Ambrosino, N., Zampogna, E., Schaaf, H. S., van der Zalm, M. M., Allwood, B., Byrne, A., Mortimer, K. J., Wallis, R. S., et al. (2021) · The International Journal of Tuberculosis and Lung Disease · doi:10.5588/ijtld.21.0425 · Cited by 195 · see citing works
The Presence of Chronic Mucus Hypersecretion across Adult Life in Relation to Chronic Obstructive Pulmonary Disease Development
Allinson, J. P., Hardy, R., Donaldson, G. C., Shaheen, S. O., Kuh, D. J., & Wedzicha, J. A. (2015) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201511-2210oc · Cited by 192 · see citing works
Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products
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Early-life exposome and lung function in children in Europe: an analysis of data from the longitudinal, population-based HELIX cohort
Agier, L., Basagaña, X., Maître, L., Granum, B. B., Bird, P. K., Casas, M., Oftedal, B., Wright, J., Andrušaitytė, S., de Castro, M., et al. (2019) · The Lancet Planetary Health · doi:10.1016/s2542-5196(19)30010-5 · Cited by 162 · see citing works
A Systematic Review of the Prevalence and Pattern of Imaging Defined Post-TB Lung Disease
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Investigating the psychosocial determinants of child health in Africa: The Drakenstein Child Health Study
Stein, D. J., Koen, N., Donald, K. A., Adnams, C. M., Koopowitz, S., Lund, C., Marais, A., MYERS, B. J., Roos, A., Sorsdahl, K. R., et al. (2015) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2015.03.016 · Cited by 150 · see citing works
The role of nicotine in the effects of maternal smoking during pregnancy on lung development and childhood respiratory disease. Implications for dangers of e-cigarettes
Spindel, E. R., & McEvoy, C. T. (2016) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201510-2013pp · Cited by 154 · see citing works
Effects of Long-Term Exposure to Traffic-Related Air Pollution on Lung Function in Children
Schultz, E. S., Litonjua, A. A., & Melén, E. (2017) · Current Allergy and Asthma Reports · doi:10.1007/s11882-017-0709-y · Cited by 154 · see citing works
Early-Life Exposure to Traffic-related Air Pollution and Lung Function in Adolescence
Schultz, E. S., Hallberg, J., Bellander, T., Bergström, A., Bottai, M., Chiesa, F., Gustafsson, P., Gruzieva, O., Thunqvist, P., Pershagen, G., et al. (2015) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201505-0928oc · Cited by 151 · see citing works
Post-TB health and wellbeing
Nightingale, R., Carlin, F., Meghji, J. Z., McMullen, K., Evans, D. H., van der Zalm, M. M., Anthony, M. G., Bittencourt, M. S., Byrne, A., Preez, K. D., et al. (2023) · The International Journal of Tuberculosis and Lung Disease · doi:10.5588/ijtld.22.0514 · Cited by 155 · see citing works
Expiratory airflow in late adolescence and early adulthood in individuals born very preterm or with very low birthweight compared with controls born at term or with normal birthweight: a meta-analysis of individual participant data
Doyle, L. W., ANDERSSON, S. M., Bush, A., Cheong, J. L. Y., Clemm, H. H., Evensen, K. A. I., Gough, A., Halvorsen, T., Hovi, P., Kajantie, E., et al. (2019) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(18)30530-7 · Cited by 145 · see citing works
Combined Impact of Smoking and Early-Life Exposures on Adult Lung Function Trajectories
Allinson, J. P., Hardy, R., Donaldson, G. C., Shaheen, S. O., Kuh, D. J., & Wedzicha, J. A. (2017) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201703-0506oc · Cited by 144 · see citing works
The health and social implications of household air pollution and respiratory diseases
Simkovich, S. M., Goodman, D., Roa, C., Crocker, M. E., Gianella, G. E., Kirenga, B. J., Wise, R. A., & Checkley, W. (2019) · npj Primary Care Respiratory Medicine · doi:10.1038/s41533-019-0126-x · Cited by 139 · see citing works
Increasing airway obstruction from 8 to 18 years in extremely preterm/low-birthweight survivors born in the surfactant era
Doyle, L. W., Adams, A., ROBERTSON, C. F., Ranganathan, S., Davis, N. M., Lee, K. J., & Cheong, J. L. Y. (2016) · Thorax · doi:10.1136/thoraxjnl-2016-208524 · Cited by 136 · see citing works
Early-life origins of chronic respiratory diseases: understanding and promoting healthy ageing
Carraro, S., Scheltema, N. M., Bont, L., & Baraldi, E. (2014) · European Respiratory Journal · doi:10.1183/09031936.00084114 · Cited by 137 · see citing works
Early childhood lower respiratory tract infection and premature adult death from respiratory disease in Great Britain: a national birth cohort study
Allinson, J. P., Chaturvedi, N., Wong, A., Shah, I., Donaldson, G. C., Wedzicha, J. A., & Hardy, R. (2023) · The Lancet · doi:10.1016/s0140-6736(23)00131-9 · Cited by 135 · see citing works
Lung growth and pulmonary function after prematurity and bronchopulmonary dysplasia
Moschino, L., Bonadies, L., & Baraldi, E. (2021) · Pediatric Pulmonology · doi:10.1002/ppul.25380 · Cited by 116 · see citing works
The Epidemiology of Chronic Suppurative Lung Disease and Bronchiectasis in Children and Adolescents
McCallum, G. B., & Binks, M. (2017) · Frontiers in Pediatrics · doi:10.3389/fped.2017.00027 · Cited by 115 · see citing works
Exposure to urban greenspace and pathways to respiratory health: An exploratory systematic review
Mueller, W., Milner, J., Loh, M. M., Vardoulakis, S., & Wilkinson, P. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.154447 · Cited by 106 · see citing works
Outdoor Air Pollution and Childhood Respiratory Disease: The Role of Oxidative Stress
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Nutrition and Lung Growth
Arigliani, M., Spinelli, A. M., Liguoro, I., & Cogo, P. E. (2018) · Nutrients · doi:10.3390/nu10070919 · Cited by 102 · see citing works
Noncommunicable Lung Disease in Sub-Saharan Africa. A Community-based Cross-Sectional Study of Adults in Urban Malawi
Meghji, J. Z., Nadeau, G. A., Davis, K. J., Wang, D., Nyirenda, M., Gordon, S. B., & Mortimer, K. J. (2016) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201509-1807oc · Cited by 97 · see citing works
Untargeted Metabolomic Analysis of Amniotic Fluid in the Prediction of Preterm Delivery and Bronchopulmonary Dysplasia
Baraldi, E., Giordano, G., Stocchero, M., Moschino, L., Zaramella, P., Tran, M. R., Carraro, S., Romero, R. J., & Gervasi, M. T. (2016) · PLoS ONE · doi:10.1371/journal.pone.0164211 · Cited by 88 · see citing works
Mesenchymal stromal cell‐derived small extracellular vesicles restore lung architecture and improve exercise capacity in a model of neonatal hyperoxia‐induced lung injury
Willis, G. R., Fernandez‐Gonzalez, A., Reis, M., Yeung, V., Liu, X., Ericsson, M., Andrews, N. A., Mitsialis, S. A., & Kourembanas, S. (2020) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2020.1790874 · Cited by 91 · see citing works
Bronchopulmonary dysplasia: what are its links to COPD?
McGrath‐Morrow, S. A., & Collaco, J. M. (2019) · Therapeutic Advances in Respiratory Disease · doi:10.1177/1753466619892492 · Cited by 88 · see citing works
The special vulnerability of children
Etzel, R. A. (2020) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2020.113516 · Cited by 88 · see citing works
Lung Function at 8 and 16 Years After Moderate-to-Late Preterm Birth: A Prospective Cohort Study
Thunqvist, P., Gustafsson, P., Schultz, E. S., Bellander, T., Berggren-Broström, E., Norman, M., Wickman, M. C., Melén, E., & Hallberg, J. (2016) · PEDIATRICS · doi:10.1542/peds.2015-2056 · Cited by 86 · see citing works
Longitudinal study of maternal body mass index, gestational weight gain, and offspring asthma
Dumas, O., Varraso, R., Gillman, M. W., Field, A. E., & Camargo, C. A. (2016) · Allergy · doi:10.1111/all.12876 · Cited by 83 · see citing works
Distinguishing adult-onset asthma from COPD: a review and a new approach
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Tobacco Use and Smoke Exposure in Children: New Trends, Harm, and Strategies to Improve Health Outcomes
Makadia, L. D., Roper, P. J., Andrews, J. O., & Tingen, M. S. (2017) · Current Allergy and Asthma Reports · doi:10.1007/s11882-017-0723-0 · Cited by 82 · see citing works
Tobacco smoke exposure in early life and adolescence in relation to lung function
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Bronchopulmonary Dysplasia: An Update of Current Pharmacologic Therapies and New Approaches
Michael, Z., Spyropoulos, F., Ghanta, S., & Christou, H. A. (2018) · Clinical Medicine Insights Pediatrics · doi:10.1177/1179556518817322 · Cited by 75 · see citing works
Health-related quality of life and risk factors associated with spirometric restriction
Guerra, S., Carsin, A., Keidel, D., Sunyer, J., Leynaert, B., Janson, C., Jarvis, D., Stolz, D., Rothe, T., Pons, M., et al. (2017) · European Respiratory Journal · doi:10.1183/13993003.02096-2016 · Cited by 74 · see citing works
“Good things come in small packages”: application of exosome-based therapeutics in neonatal lung injury
Willis, G. R., Mitsialis, S. A., & Kourembanas, S. (2017) · Pediatric Research · doi:10.1038/pr.2017.256 · Cited by 74 · see citing works
The Effect of Extended Continuous Positive Airway Pressure on Changes in Lung Volumes in Stable Premature Infants: A Randomized Controlled Trial
Lam, R., Schilling, D., Scottoline, B. P., Platteau, A., Niederhausen, M., Lund, K. C., Schelonka, R. L., MacDonald, K. D., & McEvoy, C. T. (2019) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2019.07.074 · Cited by 74 · see citing works
Distinctive lung function trajectories from age 10 to 26 years in men and women and associated early life risk factors – a birth cohort study
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Retinoic Acid: A Key Regulator of Lung Development
Fernandes-Silva, H., Araújo-Silva, H., Correia‐Pinto, J., & Moura, R. S. (2020) · Biomolecules · doi:10.3390/biom10010152 · Cited by 71 · see citing works
The disappearing Salton Sea: A critical reflection on the emerging environmental threat of disappearing saline lakes and potential impacts on children's health
Johnston, J., Razafy, M., Lugo, H., Olmedo, L., & Farzan, S. F. (2019) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2019.01.365 · Cited by 70 · see citing works
The association of early-life exposure to air pollution with lung function at ~17.5 years in the “Children of 1997” Hong Kong Chinese Birth Cohort
He, B., Huang, J. V., Kwok, M. K., Yeung, S. L. A., Hui, L. L., Li, A. M., Leung, G. M., & Schooling, C. M. (2019) · Environment International · doi:10.1016/j.envint.2018.11.073 · Cited by 71 · see citing works
Airway obstruction in young adults born extremely preterm or extremely low birth weight in the postsurfactant era
Doyle, L. W., Irving, L. B., Haikerwal, A., Lee, K. J., Ranganathan, S., & Cheong, J. L. Y. (2019) · Thorax · doi:10.1136/thoraxjnl-2019-213757 · Cited by 70 · see citing works
Asthma and COPD overlap pathophysiology of ACO
Hikichi, M., Hashimoto, S., & Gon, Y. (2018) · Allergology International · doi:10.1016/j.alit.2018.01.001 · Cited by 72 · see citing works
The global burden of respiratory infections in indigenous children and adults: A review
Basnayake, T. L., Morgan, L. C., & Chang, A. B. (2017) · Respirology · doi:10.1111/resp.13131 · Cited by 68 · see citing works
Childhood Origins of Adult Lung Disease as Opportunities for Prevention
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Reduced Lung Function and Health-Related Quality of Life after Treatment for Pulmonary Tuberculosis in Gambian Children: A Cross-Sectional Comparative Study
Nkereuwem, E., Agbla, S. C., Sallahdeen, A., Owolabi, O., Sillah, A. K., Genekah, M., Tunkara, A., Kandeh, S., Jawara, M., Saidy, L., et al. (2022) · Thorax · doi:10.1136/thorax-2022-219085 · Cited by 66 · see citing works
Bridging Lung Development with Chronic Obstructive Pulmonary Disease. Relevance of Developmental Pathways in Chronic Obstructive Pulmonary Disease Pathogenesis
Boucherat, O., Morissette, M. C., Provencher, S., Bonnet, S., & Maltais, F. (2015) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201508-1518pp · Cited by 66 · see citing works
Post-tuberculosis sequelae in children and adolescents: a systematic review
Igbokwe, V., Ruby, L. C., Sultanli, A., & Bélard, S. (2023) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(23)00004-x · Cited by 65 · see citing works
Antioxidative effects of caffeine in a hyperoxia-based rat model of bronchopulmonary dysplasia
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Prenatal and Perinatal Determinants of Lung Health and Disease in Early Life
Manuck, T. A., Levy, P. T., Gyamfi‐Bannerman, C., Jobe, A. H., & Blaisdell, C. J. (2016) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2015.4577 · Cited by 59 · see citing works
Chronic Lung Disease of Prematurity: Long-Term Respiratory Outcome
Mazloum, D. E., Moschino, L., Bozzetto, S., & Baraldi, E. (2014) · Neonatology · doi:10.1159/000360651 · Cited by 58 · see citing works
Disparities in Pulmonary Function in Healthy Children across the Indian Urban–Rural Continuum
Sonnappa, S., Lum, S., Kirkby, J. C., Bonner, R., Wade, A. M., Subramanya, V., Lakshman, P. T., Rajan, B., Nooyi, S. C., & Stocks, J. (2014) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201406-1049oc · Cited by 56 · see citing works
Self-citation
Determinants of early life immune responses to RSV infection
Ruckwardt, T. J., Morabito, K. M., & Graham, B. S. (2016) · Current Opinion in Virology · doi:10.1016/j.coviro.2016.01.003 · Cited by 58 · see citing works
Child Poverty and the Promise of Human Capacity: Childhood as a Foundation for Healthy Aging
Wise, P. H. (2016) · Academic Pediatrics · doi:10.1016/j.acap.2016.01.014 · Cited by 55 · see citing works
Trajectories of Lung Function in Infants and Children: Setting a Course for Lifelong Lung Health
Jordan, B. K., & McEvoy, C. T. (2020) · PEDIATRICS · doi:10.1542/peds.2020-0417 · Cited by 54 · see citing works
Epigenetic impacts of maternal tobacco and e-vapour exposure on the offspring lung
Zakarya, R., Adcock, I. M., & Oliver, B. G. G. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0631-3 · Cited by 53 · see citing works
The respiratory impacts of air pollution in children: Global and domestic (Taiwan) situation
Wu, I.-P., Liao, S., Lai, S., & Wong, K.-S. (2021) · Biomedical Journal · doi:10.1016/j.bj.2021.12.004 · Cited by 52 · see citing works
Linking bronchopulmonary dysplasia to adult chronic lung diseases: role of WNT signaling
Ota, C., Baarsma, H. A., Wagner, D. E., Hilgendorff, A., & Königshoff, M. (2016) · Molecular and Cellular Pediatrics · doi:10.1186/s40348-016-0062-6 · Cited by 51 · see citing works
Lung Development Genes and Adult Lung Function
Portas, L., Pereira, M., Shaheen, S., Wyss, A., London, S., Burney, P., Hind, M., Dean, C. H., & Minelli, C. (2020) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201912-2338oc · Cited by 34 · see citing works
Long-term effects of pneumonia in young children
Grimwood, K., & Chang, A. B. (2015) · Pneumonia · doi:10.15172/pneu.2015.6/621 · Cited by 52 · see citing works
Oral Vitamin C (500 mg/d) to Pregnant Smokers Improves Infant Airway Function at 3 Months (VCSIP). A Randomized Trial
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Authors: Stocks, J., Hislop, A., & Sonnappa, S.
Affiliations: University College London (GB)
Corresponding author: Stocks, Janet
ORCID: Sonnappa, Samatha
Venue: The Lancet Respiratory Medicine
Publisher: Elsevier BV
Published: 2013-11
Volume: 1
Issue: 9
Pages: 728-742
ISSN: 2213-2600 (ISSN-L)
DOI: 10.1016/s2213-2600(13)70118-8
OpenAlex: W2153070821
Cited by: 390
References: 184
Citations by year: 2026: 22 · 2025: 43 · 2024: 48 · 2023: 33 · 2022: 28 · 2021: 26 · 2020: 42 · 2019: 30 · 2018: 20 · 2017: 32 · 2016: 26 · 2015: 27 · 2014: 13
FWCI: 2.43
Type: journal article
Language: en
Open access: closed
Locations: The Lancet Respiratory Medicine (publishedVersion)
PubMed (publishedVersion)
UCL Discovery (University College London) (submittedVersion)
Topics: Health Sciences › Medicine › Physiology › Asthma and respiratory diseases
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Chronic Obstructive Pulmonary Disease (COPD) Research
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Keywords: lung development, fetal lung development, early postnatal life, reduced lung function, lung function decline, respiratory morbidity, asthma, chronic obstructive pulmonary disease, developmental origins of health and disease
MeSH terms: Environmental Exposure, Humans, Lung, Morbidity, Respiratory Tract Diseases, Global Health, Disease Progression

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Early lung development: lifelong effect on respiratory health and disease

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