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Open Access 23-01-2024 | Bronchial Asthma | Original Article

Fetal lung growth predicts the risk for early-life respiratory infections and childhood asthma

Authors: Dimitra E. Zazara, Olympia Giannou, Steven Schepanski, Mirja Pagenkemper, Anastasios D. Giannou, Maike Pincus, Ioannis Belios, Stefan Bonn, Ania C. Muntau, Kurt Hecher, Anke Diemert, Petra Clara Arck

Published in: World Journal of Pediatrics

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Abstract

Background

Early-life respiratory infections and asthma are major health burdens during childhood. Markers predicting an increased risk for early-life respiratory diseases are sparse. Here, we identified the predictive value of ultrasound-monitored fetal lung growth for the risk of early-life respiratory infections and asthma.

Methods

Fetal lung size was serially assessed at standardized time points by transabdominal ultrasound in pregnant women participating in a pregnancy cohort. Correlations between fetal lung growth and respiratory infections in infancy or early-onset asthma at five years were examined. Machine-learning models relying on extreme gradient boosting regressor or classifier algorithms were developed to predict respiratory infection or asthma risk based on fetal lung growth. For model development and validation, study participants were randomly divided into a training and a testing group, respectively, by the employed algorithm.

Results

Enhanced fetal lung growth throughout pregnancy predicted a lower early-life respiratory infection risk. Male sex was associated with a higher risk for respiratory infections in infancy. Fetal lung growth could also predict the risk of asthma at five years of age. We designed three machine-learning models to predict the risk and number of infections in infancy as well as the risk of early-onset asthma. The models’ R2 values were 0.92, 0.90 and 0.93, respectively, underscoring a high accuracy and agreement between the actual and predicted values. Influential variables included known risk factors and novel predictors, such as ultrasound-monitored fetal lung growth.

Conclusion

Sonographic monitoring of fetal lung growth allows to predict the risk for early-life respiratory infections and asthma.

Graphical abstract

Appendix
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Literature
1.
go back to reference GBD 2015 LRI Collaborators. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory tract infections in 195 countries: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Infect Dis. 2017;17:1133–61. GBD 2015 LRI Collaborators. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory tract infections in 195 countries: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Infect Dis. 2017;17:1133–61.
4.
go back to reference Avendaño Carvajal L, Perret Pérez C. Epidemiology of respiratory infections. Pediatr Respir Dis. 2020:263–72. Avendaño Carvajal L, Perret Pérez C. Epidemiology of respiratory infections. Pediatr Respir Dis. 2020:263–72.
5.
go back to reference Mulholland K. Global burden of acute respiratory infections in children: implications for interventions. Pediatr Pulmonol. 2003;36:469–74.PubMedCrossRef Mulholland K. Global burden of acute respiratory infections in children: implications for interventions. Pediatr Pulmonol. 2003;36:469–74.PubMedCrossRef
6.
go back to reference Chen J, Hu P, Zhou T, Zheng T, Zhou L, Jiang C, et al. Epidemiology and clinical characteristics of acute respiratory tract infections among hospitalized infants and young children in Chengdu, West China, 2009–2014. BMC Pediatr. 2018;18:216.PubMedPubMedCentralCrossRef Chen J, Hu P, Zhou T, Zheng T, Zhou L, Jiang C, et al. Epidemiology and clinical characteristics of acute respiratory tract infections among hospitalized infants and young children in Chengdu, West China, 2009–2014. BMC Pediatr. 2018;18:216.PubMedPubMedCentralCrossRef
7.
go back to reference Mameli C, Picca M, Buzzetti R, Pace ME, Badolato R, Cravidi C, et al. Incidence of acute respiratory infections in preschool children in an outpatient setting before and during Covid-19 pandemic in Lombardy Region, Italy. Ital J Pediatr. 2022;48:18.PubMedPubMedCentralCrossRef Mameli C, Picca M, Buzzetti R, Pace ME, Badolato R, Cravidi C, et al. Incidence of acute respiratory infections in preschool children in an outpatient setting before and during Covid-19 pandemic in Lombardy Region, Italy. Ital J Pediatr. 2022;48:18.PubMedPubMedCentralCrossRef
8.
go back to reference Nair H, Simões EA, Rudan I, Gessner BD, Azziz-Baumgartner E, Zhang JSF, et al. Global and regional burden of hospital admissions for severe acute lower respiratory infections in young children in 2010: a systematic analysis. Lancet. 2013;381:1380–90.PubMedPubMedCentralCrossRef Nair H, Simões EA, Rudan I, Gessner BD, Azziz-Baumgartner E, Zhang JSF, et al. Global and regional burden of hospital admissions for severe acute lower respiratory infections in young children in 2010: a systematic analysis. Lancet. 2013;381:1380–90.PubMedPubMedCentralCrossRef
9.
go back to reference Abu-Raya B, Viñeta Paramo M, Reicherz F, Lavoie PM. Why has the epidemiology of RSV changed during the COVID-19 pandemic? EClinicalMedicine. 2023;61:102089.PubMedPubMedCentralCrossRef Abu-Raya B, Viñeta Paramo M, Reicherz F, Lavoie PM. Why has the epidemiology of RSV changed during the COVID-19 pandemic? EClinicalMedicine. 2023;61:102089.PubMedPubMedCentralCrossRef
10.
go back to reference Li Y, Wang X, Blau DM, Caballero MT, Feikin DR, Gill CJ, et al. Global, regional, and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in children younger than 5 years in 2019: a systematic analysis. Lancet. 2022;399:2047–64.PubMedPubMedCentralCrossRef Li Y, Wang X, Blau DM, Caballero MT, Feikin DR, Gill CJ, et al. Global, regional, and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in children younger than 5 years in 2019: a systematic analysis. Lancet. 2022;399:2047–64.PubMedPubMedCentralCrossRef
11.
go back to reference Asher MI, Rutter CE, Bissell K, Chiang C-Y, El Sony A, Ellwood E, et al. Worldwide trends in the burden of asthma symptoms in school-aged children: Global Asthma Network Phase I cross-sectional study. Lancet. 2021;398:1569–80.PubMedPubMedCentralCrossRef Asher MI, Rutter CE, Bissell K, Chiang C-Y, El Sony A, Ellwood E, et al. Worldwide trends in the burden of asthma symptoms in school-aged children: Global Asthma Network Phase I cross-sectional study. Lancet. 2021;398:1569–80.PubMedPubMedCentralCrossRef
12.
go back to reference Meghji J, Mortimer K, Agusti A, Allwood BW, Asher I, Bateman ED, et al. Improving lung health in low-income and middle-income countries: from challenges to solutions. Lancet. 2021;397:928–40.PubMedCrossRef Meghji J, Mortimer K, Agusti A, Allwood BW, Asher I, Bateman ED, et al. Improving lung health in low-income and middle-income countries: from challenges to solutions. Lancet. 2021;397:928–40.PubMedCrossRef
13.
go back to reference Zhang D, Zheng J. The burden of childhood asthma by age group, 1990–2019: a systematic analysis of Global Burden of Disease 2019 data. Front Pediatr. 2022;10:823399.PubMedPubMedCentralCrossRef Zhang D, Zheng J. The burden of childhood asthma by age group, 1990–2019: a systematic analysis of Global Burden of Disease 2019 data. Front Pediatr. 2022;10:823399.PubMedPubMedCentralCrossRef
14.
go back to reference Bønnelykke K, Vissing NH, Sevelsted A, Johnston SL, Bisgaard H. Association between respiratory infections in early life and later asthma is independent of virus type. J Allergy Clin Immunol. 2015;136:81–6.e4.PubMedPubMedCentralCrossRef Bønnelykke K, Vissing NH, Sevelsted A, Johnston SL, Bisgaard H. Association between respiratory infections in early life and later asthma is independent of virus type. J Allergy Clin Immunol. 2015;136:81–6.e4.PubMedPubMedCentralCrossRef
15.
go back to reference Achten NB, van Rossum AMC, Bacharier LB, Fitzpatrick AM, Hartert TV. Long-term respiratory consequences of early-life respiratory viral infections: a pragmatic approach to fundamental questions. J Allergy Clin Immunol Pract. 2022;10:664–70.PubMedCrossRef Achten NB, van Rossum AMC, Bacharier LB, Fitzpatrick AM, Hartert TV. Long-term respiratory consequences of early-life respiratory viral infections: a pragmatic approach to fundamental questions. J Allergy Clin Immunol Pract. 2022;10:664–70.PubMedCrossRef
16.
go back to reference Dumas O, Erkkola R, Bergroth E, Hasegawa K, Mansbach JM, Piedra PA, et al. Severe bronchiolitis profiles and risk of asthma development in Finnish children. J Allergy Clin Immunol. 2022;149:1281–5.e1.PubMedCrossRef Dumas O, Erkkola R, Bergroth E, Hasegawa K, Mansbach JM, Piedra PA, et al. Severe bronchiolitis profiles and risk of asthma development in Finnish children. J Allergy Clin Immunol. 2022;149:1281–5.e1.PubMedCrossRef
17.
go back to reference van Meel ER, Mensink-Bout SM, den Dekker HT, Ahluwalia TS, Annesi-Maesano I, Arshad SH, et al. Early-life respiratory tract infections and the risk of school-age lower lung function and asthma: a meta-analysis of 150 000 European children. Eur Respir J. 2022;60:2102395.PubMedPubMedCentralCrossRef van Meel ER, Mensink-Bout SM, den Dekker HT, Ahluwalia TS, Annesi-Maesano I, Arshad SH, et al. Early-life respiratory tract infections and the risk of school-age lower lung function and asthma: a meta-analysis of 150 000 European children. Eur Respir J. 2022;60:2102395.PubMedPubMedCentralCrossRef
18.
go back to reference Moore HC, Hall GL, de Klerk N. Infant respiratory infections and later respiratory hospitalisation in childhood. Eur Respir J. 2015;46:1334–41.PubMedCrossRef Moore HC, Hall GL, de Klerk N. Infant respiratory infections and later respiratory hospitalisation in childhood. Eur Respir J. 2015;46:1334–41.PubMedCrossRef
20.
go back to reference Broughton S, Bhat R, Roberts A, Zuckerman M, Rafferty G, Greenough A. Diminished lung function, RSV infection, and respiratory morbidity in prematurely born infants. Arch Dis Child. 2006;91:26–30.PubMedCrossRef Broughton S, Bhat R, Roberts A, Zuckerman M, Rafferty G, Greenough A. Diminished lung function, RSV infection, and respiratory morbidity in prematurely born infants. Arch Dis Child. 2006;91:26–30.PubMedCrossRef
21.
go back to reference Stocks J, Hislop A, Sonnappa S. Early lung development: lifelong effect on respiratory health and disease. Lancet Respir Med. 2013;1:728–42.PubMedCrossRef Stocks J, Hislop A, Sonnappa S. Early lung development: lifelong effect on respiratory health and disease. Lancet Respir Med. 2013;1:728–42.PubMedCrossRef
22.
go back to reference Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK. Estimation of fetal weight with the use of head, body, and femur measurements-a prospective study. Am J Obstet Gynecol. 1985;151:333–7.PubMedCrossRef Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK. Estimation of fetal weight with the use of head, body, and femur measurements-a prospective study. Am J Obstet Gynecol. 1985;151:333–7.PubMedCrossRef
23.
go back to reference Warsof SL, Gohari P, Berkowitz RL, Hobbins JC. The estimation of fetal weight by computer-assisted analysis. Am J Obstet Gynecol. 1977;128:881–92.PubMedCrossRef Warsof SL, Gohari P, Berkowitz RL, Hobbins JC. The estimation of fetal weight by computer-assisted analysis. Am J Obstet Gynecol. 1977;128:881–92.PubMedCrossRef
24.
go back to reference Tang Y, Jin XD, Xu L, Deng Y, Chang Z, Li Q, et al. The value of ultrasonography in assessing fetal lung maturity. J Comput Assist Tomogr. 2020;44:328–33.PubMedCrossRef Tang Y, Jin XD, Xu L, Deng Y, Chang Z, Li Q, et al. The value of ultrasonography in assessing fetal lung maturity. J Comput Assist Tomogr. 2020;44:328–33.PubMedCrossRef
25.
go back to reference van der Zalm MM, Uiterwaal CSPM, Wilbrink B, de Jong BM, Verheij TJM, Kimpen JLL, et al. Respiratory pathogens in respiratory tract illnesses during the first year of life: a birth cohort study. Pediatr Infect Dis J. 2009;28:472–6.PubMedCrossRef van der Zalm MM, Uiterwaal CSPM, Wilbrink B, de Jong BM, Verheij TJM, Kimpen JLL, et al. Respiratory pathogens in respiratory tract illnesses during the first year of life: a birth cohort study. Pediatr Infect Dis J. 2009;28:472–6.PubMedCrossRef
26.
go back to reference Asher MI, Keil U, Anderson HR, Beasley R, Crane J, Martinez F, et al. International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J. 1995;8:483–91.PubMedCrossRef Asher MI, Keil U, Anderson HR, Beasley R, Crane J, Martinez F, et al. International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J. 1995;8:483–91.PubMedCrossRef
27.
go back to reference Gough H, Grabenhenrich L, Reich A, Eckers N, Nitsche O, Schramm D, et al. Allergic multimorbidity of asthma, rhinitis and eczema over 20 years in the German birth cohort MAS. Pediatr Allergy Immunol. 2015;26:431–7.PubMedPubMedCentralCrossRef Gough H, Grabenhenrich L, Reich A, Eckers N, Nitsche O, Schramm D, et al. Allergic multimorbidity of asthma, rhinitis and eczema over 20 years in the German birth cohort MAS. Pediatr Allergy Immunol. 2015;26:431–7.PubMedPubMedCentralCrossRef
28.
go back to reference Lommatzsch M, Criée CP, de Jong CCM, Gappa M, Geßner C, Gerstlauer M, et al. Diagnosis and treatment of asthma: a guideline for respiratory specialists 2023-published by the German Respiratory Society (DGP) e. V. Pneumologie. 2023;77:461–543 (in German)PubMed Lommatzsch M, Criée CP, de Jong CCM, Gappa M, Geßner C, Gerstlauer M, et al. Diagnosis and treatment of asthma: a guideline for respiratory specialists 2023-published by the German Respiratory Society (DGP) e. V. Pneumologie. 2023;77:461–543 (in German)PubMed
29.
go back to reference Abdulhameed AF, Memon QA. An improved trapezoidal rule for numerical integration. J Phys Conf Ser. 2021;2090:012104.CrossRef Abdulhameed AF, Memon QA. An improved trapezoidal rule for numerical integration. J Phys Conf Ser. 2021;2090:012104.CrossRef
30.
go back to reference Kianifard F, Gallo PP. Poisson regression analysis in clinical research. J Biopharm Stat. 1995;5:115–29. Kianifard F, Gallo PP. Poisson regression analysis in clinical research. J Biopharm Stat. 1995;5:115–29.
31.
go back to reference Cover T, Hart P. Nearest neighbor pattern classification. IEEE Trans Inf Theory. 1967;13:21–7.CrossRef Cover T, Hart P. Nearest neighbor pattern classification. IEEE Trans Inf Theory. 1967;13:21–7.CrossRef
34.
go back to reference Chen T, Guestrin C. XGBoost: a scalable tree boosting system. Proceedings of the 22nd ACM SIGKDD International Conference on Knowledge Discovery and Data Mining. San Francisco, California, USA: Association for Computing Machinery; 2016. p. 785–94. Chen T, Guestrin C. XGBoost: a scalable tree boosting system. Proceedings of the 22nd ACM SIGKDD International Conference on Knowledge Discovery and Data Mining. San Francisco, California, USA: Association for Computing Machinery; 2016. p. 785–94.
35.
go back to reference Chicco D, Warrens MJ, Jurman G. The coefficient of determination R-squared is more informative than SMAPE, MAE, MAPE, MSE and RMSE in regression analysis evaluation. PeerJ Comput Sci. 2021;7:e623.PubMedPubMedCentralCrossRef Chicco D, Warrens MJ, Jurman G. The coefficient of determination R-squared is more informative than SMAPE, MAE, MAPE, MSE and RMSE in regression analysis evaluation. PeerJ Comput Sci. 2021;7:e623.PubMedPubMedCentralCrossRef
36.
go back to reference Lundberg SM, Lee SI. A unified approach to interpreting model predictions. ArXiv. 2017. abs/1705.07874. Lundberg SM, Lee SI. A unified approach to interpreting model predictions. ArXiv. 2017. abs/1705.07874.
37.
go back to reference Khourdifi Y, Bahaj M. Applying best machine learning algorithms for breast cancer prediction and classification. 2018 International Conference on Electronics, Control, Optimization and Computer Science (ICECOCS). 2018. p. 1–5. Khourdifi Y, Bahaj M. Applying best machine learning algorithms for breast cancer prediction and classification. 2018 International Conference on Electronics, Control, Optimization and Computer Science (ICECOCS). 2018. p. 1–5.
38.
go back to reference Marne S, Churi S, Marne M. Predicting breast cancer using effective classification with decision tree and K means clustering technique. 2020 International Conference on Emerging Smart Computing and Informatics (ESCI). 2020. p. 39–42. Marne S, Churi S, Marne M. Predicting breast cancer using effective classification with decision tree and K means clustering technique. 2020 International Conference on Emerging Smart Computing and Informatics (ESCI). 2020. p. 39–42.
39.
go back to reference Albrecht M, Pagenkemper M, Wiessner C, Spohn M, Lütgehetmann M, Jacobsen H, et al. Infant immunity against viral infections is advanced by the placenta-dependent vertical transfer of maternal antibodies. Vaccine. 2022;40:1563–71.PubMedCrossRef Albrecht M, Pagenkemper M, Wiessner C, Spohn M, Lütgehetmann M, Jacobsen H, et al. Infant immunity against viral infections is advanced by the placenta-dependent vertical transfer of maternal antibodies. Vaccine. 2022;40:1563–71.PubMedCrossRef
40.
go back to reference American College of Obstetricians and Gynecologists’ Committee on Clinical Consensus-Obstetrics, Gantt A, Society for Maternal-Fetal Medicine, Metz TD, Kuller JA, Louis JM, et al. Obstetric care consensus #11, pregnancy at age 35 years or older. Am J Obstet Gynecol. 2023;228:B25–40. American College of Obstetricians and Gynecologists’ Committee on Clinical Consensus-Obstetrics, Gantt A, Society for Maternal-Fetal Medicine, Metz TD, Kuller JA, Louis JM, et al. Obstetric care consensus #11, pregnancy at age 35 years or older. Am J Obstet Gynecol. 2023;228:B25–40.
42.
go back to reference Van Putte-Katier N, Uiterwaal CS, De Jong BM, Kimpen JL, Verheij TJ, Van Der Ent CK, et al. The influence of maternal respiratory infections during pregnancy on infant lung function. Pediatr Pulmonol. 2007;42:945–51.PubMedCrossRef Van Putte-Katier N, Uiterwaal CS, De Jong BM, Kimpen JL, Verheij TJ, Van Der Ent CK, et al. The influence of maternal respiratory infections during pregnancy on infant lung function. Pediatr Pulmonol. 2007;42:945–51.PubMedCrossRef
43.
go back to reference McEvoy CT, Spindel ER. Pulmonary effects of maternal smoking on the fetus and child: effects on lung development, respiratory morbidities, and life long lung health. Paediatr Respir Rev. 2017;21:27–33.PubMed McEvoy CT, Spindel ER. Pulmonary effects of maternal smoking on the fetus and child: effects on lung development, respiratory morbidities, and life long lung health. Paediatr Respir Rev. 2017;21:27–33.PubMed
44.
go back to reference Meyer KF, Krauss-Etschmann S, Kooistra W, Reinders-Luinge M, Timens W, Kobzik L, et al. Prenatal exposure to tobacco smoke sex dependently influences methylation and mRNA levels of the Igf axis in lungs of mouse offspring. Am J Physiol Lung Cell Mol Physiol. 2017;312:L542–55.PubMedCrossRef Meyer KF, Krauss-Etschmann S, Kooistra W, Reinders-Luinge M, Timens W, Kobzik L, et al. Prenatal exposure to tobacco smoke sex dependently influences methylation and mRNA levels of the Igf axis in lungs of mouse offspring. Am J Physiol Lung Cell Mol Physiol. 2017;312:L542–55.PubMedCrossRef
45.
go back to reference Zazara DE, Arck PC. Developmental origin and sex-specific risk for infections and immune diseases later in life. Semin Immunopathol. 2019;41:137–51.PubMedCrossRef Zazara DE, Arck PC. Developmental origin and sex-specific risk for infections and immune diseases later in life. Semin Immunopathol. 2019;41:137–51.PubMedCrossRef
46.
go back to reference Zazara DE, Perani CV, Solano ME, Arck PC. Prenatal stress challenge impairs fetal lung development and asthma severity sex-specifically in mice. J Reprod Immunol. 2018;125:100–5.PubMedCrossRef Zazara DE, Perani CV, Solano ME, Arck PC. Prenatal stress challenge impairs fetal lung development and asthma severity sex-specifically in mice. J Reprod Immunol. 2018;125:100–5.PubMedCrossRef
47.
go back to reference Zazara DE, Wegmann M, Giannou AD, Hierweger AM, Alawi M, Thiele K, et al. A prenatally disrupted airway epithelium orchestrates the fetal origin of asthma in mice. J Allergy Clin Immunol. 2020;145:1641–54.PubMedCrossRef Zazara DE, Wegmann M, Giannou AD, Hierweger AM, Alawi M, Thiele K, et al. A prenatally disrupted airway epithelium orchestrates the fetal origin of asthma in mice. J Allergy Clin Immunol. 2020;145:1641–54.PubMedCrossRef
48.
go back to reference Martinez FD. Early-life origins of chronic obstructive pulmonary disease. N Engl J Med. 2016;375:871–8.PubMedCrossRef Martinez FD. Early-life origins of chronic obstructive pulmonary disease. N Engl J Med. 2016;375:871–8.PubMedCrossRef
49.
go back to reference Silva GE, Sherrill DL, Guerra S, Barbee RA. Asthma as a risk factor for COPD in a longitudinal study. Chest. 2004;126:59–65.PubMedCrossRef Silva GE, Sherrill DL, Guerra S, Barbee RA. Asthma as a risk factor for COPD in a longitudinal study. Chest. 2004;126:59–65.PubMedCrossRef
50.
51.
go back to reference Ubags NDJ, Alejandre Alcazar MA, Kallapur SG, Knapp S, Lanone S, Lloyd CM, et al. Early origins of lung disease: towards an interdisciplinary approach. Eur Respir Rev. 2020;29:200191.PubMedPubMedCentralCrossRef Ubags NDJ, Alejandre Alcazar MA, Kallapur SG, Knapp S, Lanone S, Lloyd CM, et al. Early origins of lung disease: towards an interdisciplinary approach. Eur Respir Rev. 2020;29:200191.PubMedPubMedCentralCrossRef
52.
go back to reference Holgate ST. The sentinel role of the airway epithelium in asthma pathogenesis. Immunol Rev. 2011;242:205–19.PubMedCrossRef Holgate ST. The sentinel role of the airway epithelium in asthma pathogenesis. Immunol Rev. 2011;242:205–19.PubMedCrossRef
53.
go back to reference Blume C, Swindle EJ, Dennison P, Jayasekera NP, Dudley S, Monk P, et al. Barrier responses of human bronchial epithelial cells to grass pollen exposure. Eur Respir J. 2013;42:87–97.PubMedCrossRef Blume C, Swindle EJ, Dennison P, Jayasekera NP, Dudley S, Monk P, et al. Barrier responses of human bronchial epithelial cells to grass pollen exposure. Eur Respir J. 2013;42:87–97.PubMedCrossRef
54.
go back to reference Swindle EJ, Collins JE, Davies DE. Breakdown in epithelial barrier function in patients with asthma: Identification of novel therapeutic approaches. J Allergy Clin Immunol. 2009;124:23–34.PubMedCrossRef Swindle EJ, Collins JE, Davies DE. Breakdown in epithelial barrier function in patients with asthma: Identification of novel therapeutic approaches. J Allergy Clin Immunol. 2009;124:23–34.PubMedCrossRef
55.
go back to reference American College of Obstetricians and Gynecologists. ACOG practice bulletin No. 97: fetal lung maturity. Obstet Gynecol. 2008;112:717–26. American College of Obstetricians and Gynecologists. ACOG practice bulletin No. 97: fetal lung maturity. Obstet Gynecol. 2008;112:717–26.
56.
go back to reference Besnard AE, Wirjosoekarto SA, Broeze KA, Opmeer BC, Mol BW. Lecithin/sphingomyelin ratio and lamellar body count for fetal lung maturity: a meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2013;169:177–83.PubMedCrossRef Besnard AE, Wirjosoekarto SA, Broeze KA, Opmeer BC, Mol BW. Lecithin/sphingomyelin ratio and lamellar body count for fetal lung maturity: a meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2013;169:177–83.PubMedCrossRef
57.
go back to reference Prakash KN, Ramakrishnan AG, Suresh S, Chow TW. Fetal lung maturity analysis using ultrasound image features. IEEE Trans Inf Technol Biomed. 2002;6:38–45.PubMedCrossRef Prakash KN, Ramakrishnan AG, Suresh S, Chow TW. Fetal lung maturity analysis using ultrasound image features. IEEE Trans Inf Technol Biomed. 2002;6:38–45.PubMedCrossRef
58.
go back to reference Bonet-Carne E, Palacio M, Cobo T, Perez-Moreno A, Lopez M, Piraquive JP, et al. Quantitative ultrasound texture analysis of fetal lungs to predict neonatal respiratory morbidity. Ultrasound Obstet Gynecol. 2015;45:427–33.PubMedCrossRef Bonet-Carne E, Palacio M, Cobo T, Perez-Moreno A, Lopez M, Piraquive JP, et al. Quantitative ultrasound texture analysis of fetal lungs to predict neonatal respiratory morbidity. Ultrasound Obstet Gynecol. 2015;45:427–33.PubMedCrossRef
59.
go back to reference Palacio M, Bonet-Carne E, Cobo T, Perez-Moreno A, Sabria J, Richter J, et al. Prediction of neonatal respiratory morbidity by quantitative ultrasound lung texture analysis: a multicenter study. Am J Obstet Gynecol. 2017;217:e1–14. Palacio M, Bonet-Carne E, Cobo T, Perez-Moreno A, Sabria J, Richter J, et al. Prediction of neonatal respiratory morbidity by quantitative ultrasound lung texture analysis: a multicenter study. Am J Obstet Gynecol. 2017;217:e1–14.
61.
go back to reference Anadkat JS, Kuzniewicz MW, Chaudhari BP, Cole FS, Hamvas A. Increased risk for respiratory distress among white, male, late preterm and term infants. J Perinatol. 2012;32:780–5.PubMedPubMedCentralCrossRef Anadkat JS, Kuzniewicz MW, Chaudhari BP, Cole FS, Hamvas A. Increased risk for respiratory distress among white, male, late preterm and term infants. J Perinatol. 2012;32:780–5.PubMedPubMedCentralCrossRef
63.
go back to reference Sonnenschein-van der Voort AM, Gaillard R, de Jongste JC, Hofman A, Jaddoe VW, Duijts L. Foetal and infant growth patterns, airway resistance and school-age asthma. Respirology. 2016;21:674–82. Sonnenschein-van der Voort AM, Gaillard R, de Jongste JC, Hofman A, Jaddoe VW, Duijts L. Foetal and infant growth patterns, airway resistance and school-age asthma. Respirology. 2016;21:674–82.
64.
go back to reference Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med. 2008;178:667–72.PubMedPubMedCentralCrossRef Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med. 2008;178:667–72.PubMedPubMedCentralCrossRef
65.
go back to reference Kusel MM, de Klerk NH, Kebadze T, Vohma V, Holt PG, Johnston SL, et al. Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J Allergy Clin Immunol. 2007;119:1105–10.PubMedPubMedCentralCrossRef Kusel MM, de Klerk NH, Kebadze T, Vohma V, Holt PG, Johnston SL, et al. Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J Allergy Clin Immunol. 2007;119:1105–10.PubMedPubMedCentralCrossRef
66.
go back to reference Gómez Real F, Burgess JA, Villani S, Dratva J, Heinrich J, Janson C, et al. Maternal age at delivery, lung function and asthma in offspring: a population-based survey. Eur Respir J. 2018;51:1601611.PubMedCrossRef Gómez Real F, Burgess JA, Villani S, Dratva J, Heinrich J, Janson C, et al. Maternal age at delivery, lung function and asthma in offspring: a population-based survey. Eur Respir J. 2018;51:1601611.PubMedCrossRef
67.
go back to reference Laerum BN, Svanes C, Wentzel-Larsen T, Gulsvik A, Torén K, Norrman E, et al. Young maternal age at delivery is associated with asthma in adult offspring. Respir Med. 2007;101:1431–8.PubMedCrossRef Laerum BN, Svanes C, Wentzel-Larsen T, Gulsvik A, Torén K, Norrman E, et al. Young maternal age at delivery is associated with asthma in adult offspring. Respir Med. 2007;101:1431–8.PubMedCrossRef
68.
go back to reference Raby BA, Celedón JC, Litonjua AA, Phipatanakul W, Sredl D, Oken E, et al. Low-normal gestational age as a predictor of asthma at 6 years of age. Pediatrics. 2004;114:e327–32.PubMedCrossRef Raby BA, Celedón JC, Litonjua AA, Phipatanakul W, Sredl D, Oken E, et al. Low-normal gestational age as a predictor of asthma at 6 years of age. Pediatrics. 2004;114:e327–32.PubMedCrossRef
69.
go back to reference Maritz GS, Harding R. Life-long programming implications of exposure to tobacco smoking and nicotine before and soon after birth: evidence for altered lung development. Int J Environ Res Public Health. 2011;8:875–98.PubMedPubMedCentralCrossRef Maritz GS, Harding R. Life-long programming implications of exposure to tobacco smoking and nicotine before and soon after birth: evidence for altered lung development. Int J Environ Res Public Health. 2011;8:875–98.PubMedPubMedCentralCrossRef
70.
go back to reference Walsh K, McCormack CA, Webster R, Pinto A, Lee S, Feng T, et al. Maternal prenatal stress phenotypes associate with fetal neurodevelopment and birth outcomes. Proc Natl Acad Sci U S A. 2019;116:23996–4005.PubMedPubMedCentralCrossRef Walsh K, McCormack CA, Webster R, Pinto A, Lee S, Feng T, et al. Maternal prenatal stress phenotypes associate with fetal neurodevelopment and birth outcomes. Proc Natl Acad Sci U S A. 2019;116:23996–4005.PubMedPubMedCentralCrossRef
71.
go back to reference Montgomery S, Bahmanyar S, Brus O, Hussein O, Kosma P, Palme-Kilander C. Respiratory infections in preterm infants and subsequent asthma: a cohort study. BMJ Open. 2013;3:e004034.PubMedPubMedCentralCrossRef Montgomery S, Bahmanyar S, Brus O, Hussein O, Kosma P, Palme-Kilander C. Respiratory infections in preterm infants and subsequent asthma: a cohort study. BMJ Open. 2013;3:e004034.PubMedPubMedCentralCrossRef
72.
go back to reference Sánchez García L, Calvo C, Casas I, Pozo F, Pellicer A. Viral respiratory infections in very low birthweight infants at neonatal intensive care unit: prospective observational study. BMJ Paediatr Open. 2020;4:e000661.PubMedPubMedCentralCrossRef Sánchez García L, Calvo C, Casas I, Pozo F, Pellicer A. Viral respiratory infections in very low birthweight infants at neonatal intensive care unit: prospective observational study. BMJ Paediatr Open. 2020;4:e000661.PubMedPubMedCentralCrossRef
73.
go back to reference Carraro S, Scheltema N, Bont L, Baraldi E. Early-life origins of chronic respiratory diseases: understanding and promoting healthy ageing. Eur Respir J. 2014;44:1682–96.PubMedCrossRef Carraro S, Scheltema N, Bont L, Baraldi E. Early-life origins of chronic respiratory diseases: understanding and promoting healthy ageing. Eur Respir J. 2014;44:1682–96.PubMedCrossRef
74.
75.
go back to reference Rasmussen M, Reddy M, Nolan R, Camunas-Soler J, Khodursky A, Scheller NM, et al. RNA profiles reveal signatures of future health and disease in pregnancy. Nature. 2022;601:422–7.PubMedPubMedCentralCrossRef Rasmussen M, Reddy M, Nolan R, Camunas-Soler J, Khodursky A, Scheller NM, et al. RNA profiles reveal signatures of future health and disease in pregnancy. Nature. 2022;601:422–7.PubMedPubMedCentralCrossRef
Metadata
Title
Fetal lung growth predicts the risk for early-life respiratory infections and childhood asthma
Authors
Dimitra E. Zazara
Olympia Giannou
Steven Schepanski
Mirja Pagenkemper
Anastasios D. Giannou
Maike Pincus
Ioannis Belios
Stefan Bonn
Ania C. Muntau
Kurt Hecher
Anke Diemert
Petra Clara Arck
Publication date
23-01-2024
Publisher
Springer Nature Singapore
Published in
World Journal of Pediatrics
Print ISSN: 1708-8569
Electronic ISSN: 1867-0687
DOI
https://doi.org/10.1007/s12519-023-00782-y