British Journal of Obstetrics and Gynaecology October 1918. Vol85. pp 132-137
EFFECTS OF MATERNAL CIGARETTE SMOKING ON THE FETUS AND PLACENTA BY
R. L. NAEYE,Department of Pathology The Pennsylvania State University College of Medicine Hershey, Pennsylvania, USA 17033 Summary In a large, prospective study, mothers who smoked during one pregnancy but not another had smaller infants in the pregnancy in which they smoked, irrespective of birth order and many other factors that affect fetal growth. Light cigarette smokers gained an average 90 g less at term than non-smokers, entirely due to the smaller size of the light smokers’ newborn infants. Heavy smokers gained 533 g less than non-smokers, only one-third of which was due to the smaller size of the heavy smokers’ newborn infants. As smoking increased, placentas enlarged and developed microscopic lesions characteristic of underperfusion from the uterus. This underperfusion was probably periodic rather than continuous because the smokers’ decidua had few of the arterial lesions that are characteristic of chronic low blood flow. Pregnancies were a mean I . 5 days shorter in smokers than in non-smokers, due to more frequent amniotic fluid infections in the smokers.
‘THE newborn infants of mothers who smoke cigarettes reportedly weigh 150 to 400 g less than newborn infants of non-smokers due to growth retardation and shorter gestations in the offspring of the smokers (Russel et al, 1968: Mulcahy et al, 1970: Yerushalmy, 1971). Rush (1974) and Davies et a1 (1976) have suggested that lower pregnancy weight gains by smokers mean less food intake and that this lower intake is responsible for the growth retardation. Reduced fetal oxygenation is another possible cause of the growth retardation since pregnant women who smoke have increased levels of carboxyhaemoglobin and nicotine may reduce uteroplacental perfusion (Cole et al, 1972; Suzuke et al, 1971). Placentas have been reported t o be enlarged in cigarette smokers but to have no lesions that would explain retarded fetal growth (Mulcahy et al, 1970; Wingerd et al, 1976). In the present study I searched for placental and other causes of the fetal growth retardation and shorter
gestations associated with maternal cigarette smoking during pregnancy. PATIENTS AND METHODS The Collaborative Perinatal Project of the National Institute of Neurological and Communicative Disorders and Stroke provides a valuable opportunity to analyze the possible effects of cigarette smoking on the fetus, placenta and decidua. It prospectively followed the course of 53 518 pregnancies in 12 hospitals in different regions of the United States between 1959 to 1966 and recorded events of gestation, labour, delivery and the neonatal period (Niswander and Gordon, 1972). Data on mothers’ smoking habits during pregnancy and well-preserved placentas were available from 46 754 single born infants. Four specially trained technicians reviewed microscopic sections from the placentas. Non-routine abnormalities were checked by the author. Birth weights, the weights of placentas and 132
EFFECTS OF SMOKING ON FETUS AND PLACENTA
maternal pregnancy weight gains were recorded from clinical charts and pathologists’ records. A large number of factors were analyzed that might contribute t o the fetal growth retardation and shorter gestations associated with maternal cigarette smoking. These factors included : duration of pregnancy, maternal weight gain and its partition between the mother, fetus and placenta, birth order, mother’s age, race, her prepregnancy weight, height, socioeconomic status, interval between pregnancies, anaemia in either the mother or the infant and sex of the infant. Chi square and Student’s ‘t’ test were used for the statistical analyses.
RESULTS At each gestational age birth weights were significantly less and from 33 weeks onwards placental weights were greater in heavy smokers than in light smokers and non-smokers (Table I). Light smokers who were delivered between 38 to 42 weeks gestation gained an average 90 g less during pregnancy than non-smokers, entirely due to the smaller size of the infants
733
born to the light smokers. The values at individual gestational ages can be found in Table 11. Heavy smokers gained 533 g less than non-smokers, only one-third of which was due to the smaller size of the heavy smokers’ newborn infants. Some mothers smoked in one but not another of their pregnancies included in the study making possible analyses that controlled for many maternal and paternal constitutional and environmental factors. Pregnancy weight gains were smalIer in a mother’s second pregnancy in the study than in the first, no matter what her smoking habits (Table 111). These second pregnancy weight gains had their greatest decrease from first pregnancy weight gains in mothers who smoked only in the second pregnancy. Mothers had smaller infants in the pregnancy in which they smoked, irrespective of birth order (Table 111). There were no significant differences in the ratio of male to female offspring, haemoglobin levels in newborn infants, maternal age, maternal haemoglobin levels, prepregnancy body weights, interval between pregnancies or socioeconomic
TABLE I Birth weights and placental weights in gestations of various durations in smokers and non-smokers
--
Birth weight (g) Gestation (weeks)
__
31 32 33 34 35 36 37 38 39 40 41 42 43
Placental weight (9) Cigarettes/day
Cigarettes/day Non-smoker 2624 2584 2640 2798 2893 2940 3007 3093 3208 3341 3447 3479 3438
Non-smoker 1-20
Over 20
Z415d 2395e 250Ie 2615ie 27 1 Oe 2803e 284Se 2926e 3072e 3189e 328ge 3335e 3274e
1887e 1 944e 2591 248ge 2675e 2697e 2816e 2909e 3070e 3188e 3279e 3267e 3346b
385 386 386 398 408 42 I 419 427 430 443 454 45 5 457
1-20
Over 20
374 380 387 392 407 417 417 420 43 1 44 1 45 I 459 45 1
355 350 406 399 420 422 430a 443c 450e 45s 464b 465b 479
No. of patients
370 507 608 1001 1418 1854 2803 4935 8454 10300 8128 4379 1997
P
EFFECTS OF MATERNAL CIGARETTE SMOKING ON THE FETUS AND PLACENTA BY
R. L. NAEYE,Department of Pathology The Pennsylvania State University College of Medicine Hershey, Pennsylvania, USA 17033 Summary In a large, prospective study, mothers who smoked during one pregnancy but not another had smaller infants in the pregnancy in which they smoked, irrespective of birth order and many other factors that affect fetal growth. Light cigarette smokers gained an average 90 g less at term than non-smokers, entirely due to the smaller size of the light smokers’ newborn infants. Heavy smokers gained 533 g less than non-smokers, only one-third of which was due to the smaller size of the heavy smokers’ newborn infants. As smoking increased, placentas enlarged and developed microscopic lesions characteristic of underperfusion from the uterus. This underperfusion was probably periodic rather than continuous because the smokers’ decidua had few of the arterial lesions that are characteristic of chronic low blood flow. Pregnancies were a mean I . 5 days shorter in smokers than in non-smokers, due to more frequent amniotic fluid infections in the smokers.
‘THE newborn infants of mothers who smoke cigarettes reportedly weigh 150 to 400 g less than newborn infants of non-smokers due to growth retardation and shorter gestations in the offspring of the smokers (Russel et al, 1968: Mulcahy et al, 1970: Yerushalmy, 1971). Rush (1974) and Davies et a1 (1976) have suggested that lower pregnancy weight gains by smokers mean less food intake and that this lower intake is responsible for the growth retardation. Reduced fetal oxygenation is another possible cause of the growth retardation since pregnant women who smoke have increased levels of carboxyhaemoglobin and nicotine may reduce uteroplacental perfusion (Cole et al, 1972; Suzuke et al, 1971). Placentas have been reported t o be enlarged in cigarette smokers but to have no lesions that would explain retarded fetal growth (Mulcahy et al, 1970; Wingerd et al, 1976). In the present study I searched for placental and other causes of the fetal growth retardation and shorter
gestations associated with maternal cigarette smoking during pregnancy. PATIENTS AND METHODS The Collaborative Perinatal Project of the National Institute of Neurological and Communicative Disorders and Stroke provides a valuable opportunity to analyze the possible effects of cigarette smoking on the fetus, placenta and decidua. It prospectively followed the course of 53 518 pregnancies in 12 hospitals in different regions of the United States between 1959 to 1966 and recorded events of gestation, labour, delivery and the neonatal period (Niswander and Gordon, 1972). Data on mothers’ smoking habits during pregnancy and well-preserved placentas were available from 46 754 single born infants. Four specially trained technicians reviewed microscopic sections from the placentas. Non-routine abnormalities were checked by the author. Birth weights, the weights of placentas and 132
EFFECTS OF SMOKING ON FETUS AND PLACENTA
maternal pregnancy weight gains were recorded from clinical charts and pathologists’ records. A large number of factors were analyzed that might contribute t o the fetal growth retardation and shorter gestations associated with maternal cigarette smoking. These factors included : duration of pregnancy, maternal weight gain and its partition between the mother, fetus and placenta, birth order, mother’s age, race, her prepregnancy weight, height, socioeconomic status, interval between pregnancies, anaemia in either the mother or the infant and sex of the infant. Chi square and Student’s ‘t’ test were used for the statistical analyses.
RESULTS At each gestational age birth weights were significantly less and from 33 weeks onwards placental weights were greater in heavy smokers than in light smokers and non-smokers (Table I). Light smokers who were delivered between 38 to 42 weeks gestation gained an average 90 g less during pregnancy than non-smokers, entirely due to the smaller size of the infants
733
born to the light smokers. The values at individual gestational ages can be found in Table 11. Heavy smokers gained 533 g less than non-smokers, only one-third of which was due to the smaller size of the heavy smokers’ newborn infants. Some mothers smoked in one but not another of their pregnancies included in the study making possible analyses that controlled for many maternal and paternal constitutional and environmental factors. Pregnancy weight gains were smalIer in a mother’s second pregnancy in the study than in the first, no matter what her smoking habits (Table 111). These second pregnancy weight gains had their greatest decrease from first pregnancy weight gains in mothers who smoked only in the second pregnancy. Mothers had smaller infants in the pregnancy in which they smoked, irrespective of birth order (Table 111). There were no significant differences in the ratio of male to female offspring, haemoglobin levels in newborn infants, maternal age, maternal haemoglobin levels, prepregnancy body weights, interval between pregnancies or socioeconomic
TABLE I Birth weights and placental weights in gestations of various durations in smokers and non-smokers
--
Birth weight (g) Gestation (weeks)
__
31 32 33 34 35 36 37 38 39 40 41 42 43
Placental weight (9) Cigarettes/day
Cigarettes/day Non-smoker 2624 2584 2640 2798 2893 2940 3007 3093 3208 3341 3447 3479 3438
Non-smoker 1-20
Over 20
Z415d 2395e 250Ie 2615ie 27 1 Oe 2803e 284Se 2926e 3072e 3189e 328ge 3335e 3274e
1887e 1 944e 2591 248ge 2675e 2697e 2816e 2909e 3070e 3188e 3279e 3267e 3346b
385 386 386 398 408 42 I 419 427 430 443 454 45 5 457
1-20
Over 20
374 380 387 392 407 417 417 420 43 1 44 1 45 I 459 45 1
355 350 406 399 420 422 430a 443c 450e 45s 464b 465b 479
No. of patients
370 507 608 1001 1418 1854 2803 4935 8454 10300 8128 4379 1997
P
