Maternal Cigarette Smoking and Oxygen Diffusion Across the Placenta

doi:10.1053/plac.2000.0571

Placenta

Volume 21, Issue 8, November 2000, Pages 824-833

https://doi.org/10.1053/plac.2000.0571 Get rights and content

Abstract

The aim of this study was to test whether or not adaptations in partial, total and specific oxygen diffusive conductances occur in the placentae of women who smoke cigarettes during pregnancy and help to compensate for intrauterine fetal hypoxic stress. Tissue sections were randomly sampled from human term placentae divided into two groups (non-smokers and smokers) according to maternal smoking status. In smokers, status was expressed as either declared smoking rate or level of plasma cotinine (the major metabolite of nicotine). Sections were analysed stereologically to estimate key structural quantities (vascular volumes, exchange surface areas, tissue diffusion distances). These were combined with previously-published physicochemical quantities (oxygen-haemoglobin reaction rates and tissue oxygen diffusion coefficients) in order to estimate the partial conductances of six tissue compartments of the oxygen pathway: maternal erythrocytes and plasma, villous trophoblast, villous stroma (including fetal capillary wall), fetal plasma and erythrocytes. From partial conductances and birthweights, total and specific conductances were calculated for each placenta. Results were assessed statistically by analyses of variance andt -tests. Despite apparent improvements in the partial conductances of the maternal erythrocytes and plasma, total and specific conductances did not alter significantly in smoking groups. However, the relative biases affecting these estimates may be different in smokers and non-smokers. We conclude that total conductance does not increase in placentae associated with maternal smoking. However, given that the fetus suffers chronic hypoxic stress as a consequence of smoking (evidenced here by elevated haematocrits), even a constant diffusive conductance implies a reduced transplacental partial pressure gradient. This could be a contributory factor to the reduced birthweight.

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Citation Excerpt :
In any case, though, our results for MDA and for antioxidant amelioration are surprising in light of the clear-cut oxidative stress experienced in vivo with maternal smoking (Aycicek and Ipek, 2008; Fayol et al., 2005; Orhon et al., 2009; Rossner et al., 2009), and the protection by antioxidants against fetal lung damage caused by maternal tobacco exposure (McEvoy et al., 2014; Proskocil et al., 2005). In that regard, TSE does not include volatile tobacco-smoke chemicals like HCN and CO that interfere with fetal oxygen delivery and utilization (Carmines and Rajendran, 2008; Pettigrew et al., 1977; Robkin, 1997), nor does an in vitro model incorporate hypoxic stress resulting from uteroplacental vasoconstriction and reduced placental oxygen transfer, which are major contributors to fetal hypoxia in vivo (Albuquerque et al., 2004; Bush et al., 2000; Clark and Irion, 1992). Accordingly, the results seen here may underestimate the contribution played by oxidative stress for prenatal tobacco smoke exposure in vivo.
Tobacco smoke exposure is associated with neurodevelopmental disorders. We used neuronotypic PC12 cells to evaluate the mechanisms by which tobacco smoke extract (TSE) affects neurodifferentiation. In undifferentiated cells, TSE impaired DNA synthesis and cell numbers to a much greater extent than nicotine alone; TSE also impaired cell viability to a small extent. In differentiating cells, TSE enhanced cell growth at the expense of cell numbers and promoted emergence of the dopaminergic phenotype. Nicotinic receptor blockade with mecamylamine was ineffective in preventing the adverse effects of TSE and actually enhanced the effect of TSE on the dopamine phenotype. A mixture of antioxidants (vitamin C, vitamin E, N-acetyl-l-cysteine) provided partial protection against cell loss but also promoted loss of the cholinergic phenotype in response to TSE. Notably, the antioxidants themselves altered neurodifferentiation, reducing cell numbers and promoting the cholinergic phenotype at the expense of the dopaminergic phenotype, an effect that was most prominent for N-acetyl-l-cysteine. Treatment with methyl donors (vitamin B12, folic acid, choline) had no protectant effect and actually enhanced the cell loss evoked by TSE; they did have a minor, synergistic interaction with antioxidants protecting against TSE effects on growth. Thus, components of tobacco smoke perturb neurodifferentiation through mechanisms that cannot be attributed to the individual effects of nicotine, oxidative stress or interference with one-carbon metabolism. Consequently, attempted amelioration strategies may be partially effective at best, or, as seen here, can actually aggravate injury by interfering with normal developmental signals and/or by sensitizing cells to TSE effects on neurodifferentiation.

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^f1: To whom correspondence should be addressed at: School of Biomedical Sciences, University of Nottingham, Queen's Medical Centre, Nottingham NG7 2UH, UK. Fax +(0)115-970-9259; E-mail:[email protected]

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Regular ArticleMaternal Cigarette Smoking and Oxygen Diffusion Across the Placenta

Abstract

Am J Obstet Gynecol

Placenta

Placenta

Am J Obstet Gynecol

Pathol Res Pract

J Theor Biol

Placenta

Placenta

Placenta

Am J Obstet Gynecol

Placenta

J Steroid Biochem Mol Biol

Intern J Gynecol Obstet

Eur J Obstet Gynecol Reprod Biol

Placenta

Placenta

Placenta

Placenta

Am J Obstet Gynecol

Am J Obstet Gynecol

Am J Obstet Gynecol

Am J Obstet Gynecol

Am J Obstet Gynecol

Am J Obstet Gynecol

Placenta

Placenta

Placenta

Placenta

Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast, in vitro

J Cell Physiol

Placenta flow reduction in pregnant smokers

Acta Obstet Gynecol Scand

Ultrastructure of the human placenta at term. Observations on placentas from newborn children of smoking and non-smoking mothers

Acta Obstet Gynecol Scand

Ultrastructure of the villi and fetal capillaries in placentas from smoking and nonsmoking mothers

Br J Obstet Gynaecol

Human placental cytochrome P450 and quinone reductase enzyme induction in relation to maternal smoking

Reprod Fertil Dev

Autacoids and control of human placental blood flow

Clin Exp Pharmacol Physiol

Carboxyhemoglobin concentration in fetal cord blood and in blood of mothers who smoked during labor

Pediatrics

Maternal cigarette smoking and fetal oxygen transport: a study of P50, 2,3-diphosphoglycerate, total hemoglobin, hematocrit, and type F hemoglobin in fetal blood

Pediatrics

Capillary volume fraction is the principal determinant of villous membrane thickness in the normal human placenta at term

J Dev Physiol

Regular Article
Maternal Cigarette Smoking and Oxygen Diffusion Across the Placenta