Maternal cigarette smoking and oxygen diffusion across the placenta.

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 and t -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.

[1]  T. Mayhew,et al.  A quantitative study on the effects of maternal smoking on placental morphology and cadmium concentration. , 2000, Placenta.

[2]  T. Mayhew,et al.  Proliferation, differentiation and apoptosis in villous trophoblast at 13-41 weeks of gestation (including observations on annulate lamellae and nuclear pore complexes). , 1999, Placenta.

[3]  C Salafia,et al.  Cigarette smoking and pregnancy II: vascular effects. , 1999, Placenta.

[4]  C. Salafia,et al.  Cigarette smoking and pregnancy I: ovarian, uterine and placental effects. , 1999, Placenta.

[5]  B. Ottesen,et al.  Stem villous arteries from the placentas of heavy smokers: functional and mechanical properties. , 1999, American journal of obstetrics and gynecology.

[6]  J. Kingdom,et al.  Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta , 1998, Histochemistry and Cell Biology.

[7]  T. Mayhew Thinning of the intervascular tissue layers of the human placenta is an adaptive response to passive diffusion in vivo and may help to predict the origins of fetal hypoxia. , 1998, European journal of obstetrics, gynecology, and reproductive biology.

[8]  Kimya,et al.  Acute Effects of Maternal Smoking on the Uterine and Umbilical Artery Blood Velocity Waveforms , 1998, Journal of maternal-fetal investigation : the official journal of French Society of Ultrasound in Medicine and Biology ... [et al.].

[9]  J. Andrade,et al.  A morphometric study of maternal smoking on apoptosis in the syncytiotrophoblast , 1998, International journal of gynaecology and obstetrics: the official organ of the International Federation of Gynaecology and Obstetrics.

[10]  W. Spellacy,et al.  Umbilical cord plasma erythropoietin levels in pregnancies complicated by maternal smoking. , 1998, American journal of obstetrics and gynecology.

[11]  V. Howard,et al.  Unbiased Stereology: Three-Dimensional Measurement in Microscopy , 1998 .

[12]  J. Kingdom,et al.  Oxygen and placental villous development: origins of fetal hypoxia. , 1997, Placenta.

[13]  G. Lindmark,et al.  Hemoconcentration in smoking mothers is associated with impaired fetal growth , 1997, Acta obstetricia et gynecologica Scandinavica.

[14]  G. Burton,et al.  Stereology and its impact on our understanding of human placental functional morphology , 1997, Microscopy research and technique.

[15]  T. Mayhew Recent applications of the new stereology have thrown fresh light on how the human placenta grows and develops its form , 1997, Journal of microscopy.

[16]  J. Guibourdenche,et al.  Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast, in vitro , 1996, Journal of cellular physiology.

[17]  C. Rodeck,et al.  Maternal smoking and fetal carboxyhaemoglobin and blood gas levels , 1996, British journal of obstetrics and gynaecology.

[18]  Tsuguyoshi Suzuki,et al.  Toxicology of metals , 1996 .

[19]  G. Burton,et al.  Stereological evaluation of vascular adaptations in human placental villi to differing forms of hypoxic stress. , 1996, Placenta.

[20]  T. Mayhew,et al.  Human placental cytochrome P450 and quinone reductase enzyme induction in relation to maternal smoking. , 1995, Reproduction, fertility, and development.

[21]  G. Burton,et al.  Placental histomorphometry and morphometric diffusing capacity of the villous membrane in pregnancies complicated by maternal iron-deficiency anemia. , 1995, American journal of obstetrics and gynecology.

[22]  G. Burton,et al.  Effects of hypobaric hypoxia on the fetoplacental unit: the morphometric diffusing capacity of the villous membrane at high altitude. , 1994, American journal of obstetrics and gynecology.

[23]  W. Walters,et al.  AUTACOIDS AND CONTROL OF HUMAN PLACENTAL BLOOD FLOW , 1994, Clinical and experimental pharmacology & physiology.

[24]  R. Demir,et al.  Structural changes in placental barrier of smoking mother. A quantitative and ultrastructural study. , 1994, Pathology, research and practice.

[25]  F. B. Sørensen,et al.  The effects of mode of delivery and sex of newborn on placental morphology in control and diabetic pregnancies. , 1993, Journal of anatomy.

[26]  Y. Osawa,et al.  Cigarette smoking during pregnancy lowers aromatase cytochrome P-450 in the human placenta , 1993, The Journal of Steroid Biochemistry and Molecular Biology.

[27]  L. Platt,et al.  Cigarette Smoking During Pregnancy: Acute Effects on Uterine Flow Velocity Waveforms , 1993, Obstetrics and gynecology.

[28]  T. Mayhew,et al.  Changes in oxygen diffusive conductances of human placentae during gestation (10-41 weeks) are commensurate with the gain in fetal weight. , 1993, Placenta.

[29]  T. Mayhew,et al.  Quantitative description of the elaboration and maturation of villi from 10 weeks of gestation to term. , 1992, Placenta.

[30]  T M Mayhew,et al.  A review of recent advances in stereology for quantifying neural structure , 1992, Journal of neurocytology.

[31]  E. Jauniaux,et al.  The Effect of Smoking in Pregnancy on Early Placental Morphology , 1992, Obstetrics and gynecology.

[32]  G. Burton,et al.  Capillary volume fraction is the principal determinant of villous membrane thickness in the normal human placenta at term. , 1992, Journal of developmental physiology.

[33]  J. Livesey,et al.  High-performance liquid-chromatographic method compared with a modified radioimmunoassay of cotinine in plasma. , 1991, Clinical chemistry.

[34]  Mayhew Tm,et al.  The new stereological methods for interpreting functional morphology from slices of cells and organs , 1991, Experimental physiology.

[35]  T. Mayhew,et al.  Oxygen diffusive conductances of human placentae from term pregnancies at low and high altitudes. , 1990, Placenta.

[36]  R. Demir,et al.  Ultrastructural investigation of the effects of cigarette smoking on the human placenta , 1990 .

[37]  K J Dalton,et al.  Morphometric differences between the placental vasculature of non‐smokers, smokers and ex‐smokers , 1989, British journal of obstetrics and gynaecology.

[38]  F. Teasdale,et al.  Morphological changes in the placentas of smoking mothers: a histomorphometric study. , 1989, Biology of the neonate.

[39]  S. Bull,et al.  Maternal cigarette smoking: the effects on umbilical and uterine blood flow velocity. , 1988, American journal of obstetrics and gynecology.

[40]  L. Beaulac-Baillargeon,et al.  Caffeine-cigarette interaction on fetal growth. , 1987, American journal of obstetrics and gynecology.

[41]  H J Gundersen,et al.  The efficiency of systematic sampling in stereology and its prediction * , 1987, Journal of microscopy.

[42]  T. Mayhew,et al.  Morphometric studies on villi in human term placentae and the effects of altitude, ethnic grouping and sex of newborn. , 1987, Placenta.

[43]  T. Mayhew,et al.  The volumetric composition of human term placentae: altitudinal, ethnic and sex differences in Bolivia. , 1987, Journal of anatomy.

[44]  T. Mayhew,et al.  Microscopical morphology of the human placenta and its effects on oxygen diffusion: a morphometric model. , 1986, Placenta.

[45]  G. Eklund,et al.  Smoking, Maternal Age, and Fetal Growth , 1985, Obstetrics and gynecology.

[46]  J. James,et al.  Basal lamina thickening in the placentae of smoking mothers. , 1985, Placenta.

[47]  T. Mayhew,et al.  Stereological studies on the true thickness of the villous membrane in human term placentae: a study of placentae from high-altitude pregnancies. , 1985, Placenta.

[48]  T. Mayhew,et al.  Structure-function correlation in the human placenta: the morphometric diffusing capacity for oxygen at full term. , 1984, Journal of anatomy.

[49]  J. Whitfield,et al.  Carboxyhemoglobin, cotinine, and thiocyanate assay compared for distinguishing smokers from non-smokers. , 1984, Clinical chemistry.

[50]  T. Maruo,et al.  Effects of smoking on fetoplacental-maternal system during pregnancy. , 1984, American journal of obstetrics and gynecology.

[51]  K. V. Andersen,et al.  Placenta flow Reduction in Pregnant Smokers , 1984, Acta obstetricia et gynecologica Scandinavica.

[52]  Y. Berthiaume,et al.  Maternal cigarette smoking and fetal oxygen transport: a study of P50, 2,3-diphosphoglycerate, total hemoglobin, hematocrit, and type F hemoglobin in fetal blood. , 1983, Pediatrics.

[53]  J. C. Peereboom-Stegeman,et al.  Structural changes in the placenta of smoking mothers: a quantitative study. , 1983, Placenta.

[54]  R. K. Miller,et al.  Placental toxicity of cadmium in the rat: an ultrastructural study. , 1983, Placenta.

[55]  M A Hofman,et al.  Evolution of brain size in neonatal and adult placental mammals: a theoretical approach. , 1983, Journal of theoretical biology.

[56]  Y. Berthiaume,et al.  Carboxyhemoglobin concentration in fetal cord blood and in blood of mothers who smoked during labor. , 1982, Pediatrics.

[57]  J. Haas Human adaptability approach to nutritional assessment: a Bolivian example. , 1981, Federation proceedings.

[58]  I. Asmussen ULTRASTRUCTURE OF THE VILLI AND FETAL CAPILLARIES IN PLACENTAS FROM SMOKING AND NONSMOKING MOTHERS , 1980, British journal of obstetrics and gynaecology.

[59]  P. Lehtovirta,et al.  THE ACUTE EFFECT OF SMOKING ON INTERVILLOUS BLOOD FLOW OF THE PLACENTA , 1978, British journal of obstetrics and gynaecology.

[60]  R. Østerby,et al.  Distribution of Membrane Thickness Determined By Lineal Analysis , 1978, Journal of microscopy.

[61]  B. Pirani Smoking during pregnancy. , 1978, Obstetrical & gynecological survey.

[62]  J. Tonascia,et al.  Maternal smoking, pregnancy complications, and perinatal mortality. , 1977, American journal of obstetrics and gynecology.

[63]  L. Misiewicz [Cigarette smoking and pregnancy]. , 1977, Wiadomosci lekarskie.

[64]  I. Asmussen Ultrastructure of the Human Placenta at Term: Observations on Placentas from Newborn Children of Smoking and Non‐Smoking Mothers , 1977, Acta obstetricia et gynecologica Scandinavica.

[65]  G. Mau SMOKING AND THE FETUS , 1976, The Lancet.

[66]  H. Munro,et al.  Quantitative studies of human placenta. I. Morphometry. , 1973, Biology of the neonate.

[67]  P. Cole,et al.  SMOKING DURING PREGNANCY AND ITS EFFECTS ON THE FETUS , 1972, The Journal of obstetrics and gynaecology of the British Commonwealth.

[68]  H. Goldstein,et al.  Cigarette Smoking in Pregnancy: Its Influence on Birth Weight and Perinatal Mortality , 1972, British medical journal.

[69]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[70]  R. Mulcahy Effect of age, parity, and cigarette smoking on outcome of pregnancy. , 1968, American Journal of Obstetrics and Gynecology.

[71]  J. Metcalfe,et al.  Gas exchange in the pregnant uterus. , 1967, Physiological reviews.