The impact of maternal asthma during pregnancy on offspring retinal microvascular structure and its relationship to placental growth factor production in utero.


Journal

Microcirculation (New York, N.Y. : 1994)
ISSN: 1549-8719
Titre abrégé: Microcirculation
Pays: United States
ID NLM: 9434935

Informations de publication

Date de publication:
08 2020
Historique:
received: 10 02 2020
revised: 17 04 2020
accepted: 20 04 2020
pubmed: 25 4 2020
medline: 20 8 2021
entrez: 25 4 2020
Statut: ppublish

Résumé

Asthma is a common chronic disease in pregnancy that affects placental function and fetal growth and associated with cardio-metabolic disorders in the offspring but the mechanisms are unknown. This study explored whether maternal asthma in pregnancy is associated with the development of offspring microvascular structure and whether it was related to biomarkers of angiogenesis in utero. Children aged 4 to 6 years, born to either asthmatic mothers (n = 38) or healthy controls (n = 25), had their retinal microvascular structure examined. Maternal plasma PlGF concentrations at 18 and 36 weeks' gestation were measured. There was a significant global difference in all retinal microvascular measures between children of asthmatic mothers relative to controls and increased retinal venular tortuosity in children born to asthmatic mothers (7.1 (95% CI 0.7-13.5); P = .031). A rise in plasma PlGF from 18 to 36 weeks' gestation was observed in the control population which was significantly lower in the asthma group by 190.9 pg/mL. PlGF concentrations were correlated with microvascular structure including arteriolar branching and venular tortuosity. These exploratory findings indicate that exposure to maternal asthma during pregnancy is associated with persistent changes in microvascular structure in childhood that may be driven by alterations to angiogenic mechanisms in utero.

Identifiants

pubmed: 32330353
doi: 10.1111/micc.12622
doi:

Substances chimiques

Placenta Growth Factor 144589-93-5

Types de publication

Clinical Trial Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e12622

Informations de copyright

© 2020 John Wiley & Sons Ltd.

Références

Grzeskowiak LE, Smith B, Roy A, Dekker GA, Clifton VL. Patterns, predictors and outcomes of asthma control and exacerbations during pregnancy: a prospective cohort study. ERJ Open Res. 2016;2(1):00054-2015.
Hodyl NA, Stark MJ, Scheil W, Grzeskowiak LE, Clifton VL. Perinatal outcomes following maternal asthma and cigarette smoking during pregnancy. Eur Respir J. 2014;43(3):704-716.
Barker DJ. Birth weight and hypertension. Hypertension. 2006;48(3):357-358.
Tegethoff M, Olsen J, Schaffner E, Meinlschmidt G. Asthma during pregnancy and clinical outcomes in offspring: a national cohort study. Pediatrics. 2013;132(3):483.
Lin S, Herdt-Losavio M, Gensburg L, Marshall E, Druschel C. Maternal asthma, asthma medication use, and the risk of congenital heart defects. Birth Defects Res A Clin Mol Teratol. 2009;85(2):161-168.
Visentin S, Grumolato F, Nardelli GB, Di Camillo B, Grisan E, Cosmi E. Early origins of adult disease: low birth weight and vascular remodeling. Atherosclerosis. 2014;237(2):391-399.
Mayhew TM, Jenkins H, Todd B, Clifton VL. Maternal asthma and placental morphometry: effects of severity, treatment and fetal sex. Placenta. 2008;29(4):366-373.
Clifton V, Giles W, Smith R, et al. Alterations of placental vascular function in asthmatic pregnancies. Am J Respir Crit Care Med. 2001;164(4):546-553.
Khaliq A, Dunk C, Jiang J, et al. Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: molecular evidence for "placental hyperoxia" in intrauterine growth restriction. Lab Invest. 1999;79(2):151-170.
Crispi F, Dominguez C, Llurba E, Martin-Gallan P, Cabero L, Gratacos E. Placental angiogenic growth factors and uterine artery Doppler findings for characterization of different subsets in preeclampsia and in isolated intrauterine growth restriction. Am J Obstet Gynecol. 2006;195(1):201-207.
Poon LC, Zaragoza E, Akolekar R, Anagnostopoulos E, Nicolaides KH. Maternal serum placental growth factor (PlGF) in small for gestational age pregnancy at 11(+0) to 13(+6) weeks of gestation. Prenat Diagn. 2008;28(12):1110-1115.
Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol. 2003;188(1):177-182.
Sherrell H, Clifton V, Kumar S. Predicting intrapartum fetal compromise at term using the cerebroplacental ratio and placental growth factor levels (PROMISE) study: randomised controlled trial protocol. BMJ Open. 2018;8(8):e022567.
Luna RL, Kay VR, Rätsep MT, et al. Placental growth factor deficiency is associated with impaired cerebral vascular development in mice. Mol Hum Reprod. 2016;22(2):130-142.
Cheung CY, Ikram MK, Sabanayagam C, Wong TY. Retinal microvasculature as a model to study the manifestations of hypertension. Hypertension. 2012;60(5):1094-1103.
Smith W, Wang JJ, Wong TY, et al. Retinal arteriolar narrowing is associated with 5-year incident severe hypertension: the Blue Mountains Eye Study. Hypertension. 2004;44(4):442-447.
Mitchell P, Liew G, Rochtchina E, et al. Evidence of arteriolar narrowing in low-birth-weight children. Circulation. 2008;118(5):518-524.
Gishti O, Jaddoe VWV, Duijts L, et al. Influence of breastfeeding on retinal vessel calibers in school-age children. the Generation R Study. Eur J Clin Nutr. 2016;70(1):72-77.
Grzeskowiak LE, Smith B, Roy A, Dekker GA, Clifton VL. An observational study of the impact of an antenatal asthma management service on asthma control during pregnancy. Eur J Obstet Gynecol Reprod Biol. 2016;197:48-53.
McNamara H, Barclay P, Sharma V. Accuracy and precision of the ultrasound cardiac output monitor (USCOM 1A) in pregnancy: comparison with three-dimensional transthoracic echocardiography. Br J Anaesth. 2014;113(4):669-676.
Jatoi NA, Mahmud A, Bennett K, Feely J. Assessment of arterial stiffness in hypertension: comparison of oscillometric (Arteriograph), piezoelectronic (Complior) and tonometric (SphygmoCor) techniques. J Hypertens. 2009;27(11):2186-2191.
Kandasamy Y, Smith R, Wright IM. Retinal microvasculature measurements in full-term newborn infants. Microvasc Res. 2011;82(3):381-384.
Cheung N, Saw SM, Liew G, et al. Childhood vascular risk factors and retinal vessel caliber. Asia Pacific J Ophthalmol. 2012;1(4):193-197.
Li LJ, Ikram MK, Wong TY. Retinal vascular imaging in early life: insights into processes and risk of cardiovascular disease. J Physiol. 2016;594(8):2175-2203.
Hellstrom A, Hard AL, Svensson E, Niklasson A. Ocular fundus abnormalities in children born before 29 weeks of gestation: a population-based study. Eye (London, England). 2000;14(Pt 3A):324-329.
Hussain SM, Kähönen M, Raitakari OT, et al. Impact of fetal growth and preterm birth on the retinal microvasculature in mid-adulthood. Microcirculation. 2015;22(4):285-293.
Brodszki J, Lanne T, Marsal K, Ley D. Impaired vascular growth in late adolescence after intrauterine growth restriction. Circulation. 2005;111(20):2623-2628.
Kandasamy Y, Smith R, Wright Ian MR. Retinal microvascular changes in low-birth-weight babies have a link to future health. J Perinat Med. 2012;209.
Hellstrom A, Dahlgren J, Marsal K, Ley D. Abnormal retinal vascular morphology in young adults following intrauterine growth restriction. Pediatrics. 2004;113(2):e77-e80.
Cheung CY, Tay WT, Mitchell P, et al. Quantitative and qualitative retinal microvascular characteristics and blood pressure. J Hypertens. 2011;29(7):1380-1391.
Ahmed A, Dunk C, Ahmad S, Khaliq A. Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble Flt-1 by oxygen-a review. Placenta. 2000;21(Suppl A):S16-S24.
Gishti O, Jaddoe VWV, Felix JF, et al. Influence of maternal angiogenic factors during pregnancy on microvascular structure in school-age children. Hypertension. 2015;65(4):722-728.
Nishimoto F, Sakata M, Minekawa R, et al. Metal transcription factor-1 is involved in hypoxia-dependent regulation of placenta growth factor in trophoblast-derived cells. Endocrinology. 2009;150(4):1801-1808.
Osei-Kumah A, Smith R, Jurisica I, Caniggia I, Clifton VL. Sex-specific differences in placental global gene expression in pregnancies complicated by asthma. Placenta. 2011;32(8):570-578.
Meakin AS, Saif Z, Jones AR, Aviles PFV, Clifton VL. Review: Placental adaptations to the presence of maternal asthma during pregnancy. Placenta. 2017;54:17-23.
Tegethoff M, Greene N, Olsen J, Schaffner E, Meinlschmidt G. Inhaled glucocorticoids during pregnancy and offspring pediatric diseases: a national cohort study. Am J Respir Crit Care Med. 2012;185(5):557-563.
Hodyl NA, Stark MJ, Osei-Kumah A, Bowman M, Gibson P, Clifton VL. Fetal glucocorticoid-regulated pathways are not affected by inhaled corticosteroid use for asthma during pregnancy. Am J Respir Crit Care Med. 2011;183(6):716-722.
Murphy VE, Gibson PG, Giles WB, et al. Maternal asthma is associated with reduced female fetal growth. Am J Respir Crit Care Med. 2003;168(11):1317-1323.
Clifton VL, Moss TJM, Wooldridge AL, et al. Development of an experimental model of maternal allergic asthma during pregnancy. J Physiol. 2016;594(5):1311-1325.
Enninga EA, Nevala WK, Creedon DJ, Markovic SN, Holtan SG. Fetal sex-based differences in maternal hormones, angiogenic factors, and immune mediators during pregnancy and the postpartum period. Am J Reprod Immunol. 2015;73(3):251-262.
Regitz-Zagrosek V, Kararigas G. Mechanistic pathways of sex differences in cardiovascular disease. Physiol Rev. 2017;97(1):1-37.

Auteurs

Ailee R Jones (AR)

Mater Medical Research Institute, University of Queensland, Brisbane, QLD, Australia.

Christine Tuckwell (C)

Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia.

Ian M R Wright (IMR)

Illawarra Health and Medical Research Institute and School of Medicine, The University of Wollongong, Wollongong, NSW, Australia.

Janna L Morrison (JL)

Early Origins of Adult Health Research Group, School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA, Australia.

Yogavijayan Kandasamy (Y)

Department of Neonatology, Townsville Hospital, Douglas, QLD, Australia.

Melanie R Wittwer (MR)

Lyell McEwin Hospital, University of Adelaide, Adelaide, SA, Australia.

Margaret A Arstall (MA)

Lyell McEwin Hospital, University of Adelaide, Adelaide, SA, Australia.

Michael J Stark (MJ)

Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia.

Michael Davies (M)

Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia.

Cameron Hurst (C)

Statistics Unit, QIMR Berghofer Medical Research Institute, Herston, QLD, Australia.

Satomi Okano (S)

Statistics Unit, QIMR Berghofer Medical Research Institute, Herston, QLD, Australia.

Vicki L Clifton (VL)

Mater Medical Research Institute, University of Queensland, Brisbane, QLD, Australia.
Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH