a community study of smoking in pregnancy

The Journal of 0 bstetrics and Gynaecology of the British Commonwealth

VOL. 79 No. 12 NEW SERIES DECEMBER 1972

A COMMUNITY STUDY OF SMOKING IN PREGNANCY

BY

*JOAN ANDREWS, Consultant Obstetrician

AND

*JOHN M. MCGARRY, Lecturer in Obstetrics University Hospital of Wales, Cardiff

Summary A comprehensive study has been made of all pregnant women in the city of Cardiff. One aspect has been to review the habit of smoking during pregnancy in relation to maternal and fetal wellbeing. Some suggestions are made as to the mode of action of cigarette smoke in producing these effects.

SINCE the introduction of tobacco into European society there have been reports of potential ill effects. Sontag and Wallace (1935) showed that the fetus too could be affected and it was demonstrated that the fetal heart rate increased shortly after an expectant mother smoked a cigarette. The first definitive studies by Simpson (1957) and by Lowe (1959) linked a decrease in the average birth weight of infants with the maternal smoking habit. Since then, many studies have shown an association between maternal smoking and both fetal and maternal complications, including abortion, perinatal death, premature labour and toxaemia of pregnancy.

The present study has been made in an attempt to review some of the conflicting reports and by analysis of the smoking habits and results in a complete community to avoid error due to sampling and small numbers. The large numbers involved also allow possibly correlated factors to be studied to assess the partial effect of each on the final result.

*Present address: J.A.-St. Davids Hospital, Cardiff; J.M.McG.-Department of Obstetrics, University Hospi- tal of Wales, Cardiff.

1057

35

METHOD OF STUDY

Obstetric and social data relating to all women normally resident in the city of Cardiff have been recorded. The Cardiff Births Survey started in 1965. Originally transcription sheets were completed partly by medical and partly by clerical staff, but since 1968 the coding has been done entirely by clerical workers since their accuracy has been shown to be superior to that of the frequently changing medical officer.

During the puerperium the patient’s smoking habit was enquired into and recorded. In the majority of cases the enquiry was made by one of the Birth Survey clerks but where the mother was delivered at home, this information and some other social data not already recorded in domiciliary records was obtained by the district midwife. The coded data was programmed in Multiple Variate Counter for computer analysis at the Atlas Computer Laboratory, Chilton.

It may be that some women knowing of a climate of opinion against smoking may claim to smoke less than in fact they do, and certainly in this Cardiff study women tended to give a lower estimate of their smoking habits if asked while in hospital than when the same question

1058 ANDREWS AND MCGARRY

TABLE I Prematurity and smoking

Source of study

~ ~

Average weight Prematurity rate Author reduction among

infants of mothers Smokers Non-smokers who smoke (g.) (per cent) (per cent)

Birmingham-1 958 California-1 957 Perinatal mortality survey-1958 Baltimore- 1 96 1 (Negro) Aberdeen-1962 San Francisco-1964 (white)

Lancashire-1964 California-1 967 Dublin-1 968 Cardiff-1965-1 968

(Negro)

Lowe (1959) W. J. Simpson (1957)

Frazier et nl. (1961) Herriott et al. (1962) Yerushalmy (1964)

Simpson (1964) Underwood et al. (1967) Mulcahy (1968)

170 12.1 6.1

170 156 18.6 11.2 160

6 . 4 3.5 13.4 4.9

255 7.0 3.3 115 to 333

300 170 10.4 6.1

* Smoking 5 cigarettes

was asked in their own home by a district midwife.

The total number of maternities recorded during the years 1965-1968 was 18,631 although the numbers analysed in different tables vary depending on whether all births, all live births, or only maternities are considered.

RESULTS 1. Infant Weight

There seems no doubt that smoking by the mother during pregnancy leads to a reduction in infant weight, and a concomitant increase in the prematurity rate. Lowe (1959) found an average reduction of 170 g. in the weight of infants born to mothers who smoked. Since then other workers have found similar reductions (Table I)

In the present study the average weight reduction of single living infants born to mothers who smoked was 170 g. This figure was based on those cases in which the mother went into labour spontaneously and was delivered of a single liveborn infant. The prematurity rate among smokers (including all births) rose to 10.4 per cent. compared with 6 - 1 per cent in non-smokers. There was a progressive fall in average infant weight with the number of cigarettes smoked by the mother and an average weight for infants of ex-smokers which was between that of non-smokers and light smokers. The term ‘ex-smoker’ in the Cardiff Survey

relates to those women who gave up smoking either before or during the early part of the pregnancy (Table 11).

Neither Lowe (1959) nor Frazier et al. (1961) demonstrated any change in the average weight of those infants born to women who gave up smoking during pregnancy and suggested that the effect of smoking was a short term one acting only while the smoking habit persisted and particularly if it was continued throughout pregnancy.

The explanation for this weight reduction may be that the babies of women who smoke

TABLE I1 Birth Weight and Cigurettes Smoked (Single livebirths)

Mean Incidence Birth of infants

weight weighing

(g.) (per cent.) i 1 S.D. 2500 g. cr less

Non-smokers 3390+562 4 - 1 Ex-smokers 33101 536 4.9 Smokers

1 4 cigarettes/day 3331 i 5 7 5 5.9 5-9 cigarettes/day 321 6 i 577 7.3

1C19 cigaretteslday 3171 +610 8.8 20 or more cigarettes/

day 31 66A656 9 . 2 All smokers 8.1

Fratio = 85.13; xz = 133.3: Significant at 1 percent. level; p = <0.001.

SMOKING i~ PREGNANCY 1059

TABLE 111 Premnfirre delivery and smoking

Average Incidence of pregnancy lasting

period of gestation Smokers Non-smokers

Source of study Author shortening of less than 37 weeks (per cent)

Perinatal mortality survey-19% Butler and Bonham 6 .1 4 .3

Baltimore-I 961 Frazier et al. (1961) 0 . 3 weeks San Francisco-1964 (white) Yerushalmy (1964) 0.19 weeks 6 . 5 5 . 9

(Negro) 0.2 weeks 16.7 13.4 Cardiff * 9 . 2 6 . 7

(1963)

Duration of gestation defined as lasting less than 266 days or 37 completed weeks. * Includes only single liveborn infants following spontaneous onset of labour.

during pregnancy are born early, are born small for dates or alternatively that their lower weight is a reflection of some other influence also associated with smoking.

2. Premature Labour The question of premature delivery has been

studied with conflicting results. OLane (1963), and Duffus and MacGillivray (1968) failed to find a relationship between maternal smoking habit and premature delivery but other studies (Table 111) have shown smoking to be associated with a shorter period of gestation. Buncher (1969), on the basis of average expected weight gain, calculated that 10 per cent of the weight difference of children of smoking and non- smoking mothers was due to shortened gestation and that the remaining 90 per cent was associated with other characteristics acting independently of the duration of gestation. Allowance needs to be made for artificial premature induction of labour as Lowe (1959) has shown 8 reduced incidence of surgical induction in women who smoke regularly.

Amongst the Cardiff women 6 . 6 per cent of non-smokers delivered before the beginning of the 38th week whilst 8 .6 per cent of all smokers did so. Table IV shows the progressive increase of premature delivery associated with smoking for those women who had a spontaneous onset of labour and were delivered of a single child.

Many factors other than smoking are associated with early delivery. Women of lower social class smoke more heavily and also tend to be anaemic, yet have an additional incidence

TABLE IV Incidence of premafrire delivery (37 weeks or less)

Incidence of single, liveborn infants born following spontaneous onset of labour before 37 completed weeks of pregnancy

Number Per cent.

Non-smokers 482 out of 7176 6 . 7 Ex-smokers 65 out of 869 7 -47 Smokers 572 out of 6238 9.17

of premature delivery apparently related to smoking (Table V, VI, and VII). The test of significance used in these and subsequent tables is designed to assess the effect of two variables such as maternal weight and smoking habit on the incidence of a third factor such as infant weight.

In the present study there was no increase of premature rupture of membranes among women who smoked. It has been suggested that smoking is associated with increased myometrial activity (Kumar and Pantelis, 1963), which may account for the increase in premature labour.

3. ‘Small for Dates’ To determine the extent of retardation of

fetal growth related to smoking only those cases were studied in which labour started spontaneously, a single live child was delivered and in which the date of the last menstrual period was known with some certainty (Fig. 1).


TABLE V Smoking habit related to social class

-

Social class Incidence of smoking in pregnancy Incidence of ex-smokers (Registrar General's classifi- cation of occupations, 1960) Number Per cent Number Per cent

I and I1 I11 IV V

606 out of 2339 25.9 171 out of 2339 7.3 3864 out of 9292 41 * 6 599 out of 9292 6 .4 1029 out of 2150 47.9 115 out of 2150 5.3 991 out of 1942 51 .O 107 out of 1942 5.5

TABLE VI Incidence of delivery at 37 weeks or less smoking habit and social class (all maternities)

Non-smokers Smokers Social class

Number Per cent Number Per cent

I and I1 108 out of 1579 6.8 42 out of 619 6-8 111 354 out of 4892 7.2 356 out of 3920 9.1 IV 84 out of 1018 8.3 107 out of 1038 10.3 V 77 out of 852 9 .0 91 out of lo00 9.1 All classes 623 out of 8341 7.5 596 out of 6577 9.1

Significance x2 Difference in ,y2 P All factors 21.7378 Social class 13.7378 8.0841 <0.01 >0.001 Smoking 4.1536 9.5001 t0.01 >0.001 Interaction 3.8932 0.2604 >0.05 (i.e. effect of change of social class which also

affects smoking habit) degree of freedom = 1

TABLE VII Incidence of delivery at 37 weeks or less, smoking habit and anaemia in early pregnancy

Anaemia (Haemoglobin more than 70 per cent

when tested before 24 weeks gestation) No anaemia


Non-smo kers Ex-smokers Smokers

1-4 cigarettes 5-9 cigarettes 10-19 cigarettes 20+ cigarettes

All smokers

17 out of 191 8.9 440 out of 6777 6.5 *2 out of 26 7.7 64 out of 820 7.8

4 out of 25 16.0 46 out of 737 6.2 6-5 *2 out of 46 4.3

10 out of 88 11.4 189 out of 2244 8.4 4 out of 32 12.5 89 out of 817 10.9

20 out of 191 10.5 397 out of 4921 8.1

73 out of 1123

* Only 2 cases.

Smoking Anaemia Interaction

x" 33.71 11.46 7 ' 8292 7.6811

Difference in $ P

22.2417 3.6391 0-1482

to-001 <0.01 >0.001

>0*05

SMOKING IN PREGNANCY 1061

T

3500

3oM)

M E A N BIRTH 2m

W E I G H T

(9.1

deviat ion tstondard 2000

1500

1000

;URE I .

j i I

i A

I J.

I I I I A

Smoking1 Non-srnoki ng 1

J i :I i i I

28 30 32 34 36 38 40 42 U

WEEKS G E S T A T I O N FIG. 1

Mean birth weight, duration of gestation and smoking habit.

It can be demonstrated that there is diminution in fetal weight additional to any effect due to social class or maternal anaemia (Table VIII and IX).

In contradiction to the findings of O'Lane (1 963) and Buncher (1969) the lighter weight women smoked more heavily and smoking had an effect on birth weight additional to that of maternal weight (Table X). The increase of smoking habit in the lighter woman was inde- pendent of her height (Table XI).

Maternal weight gain in pregnancy which was excessive in 36 per cent of non-smokers and in 30 per cent of smokers had considerably less influence on infant weight than did the smoking habit (Table XII).

Whether low maternal weight and excessive smoking are both related to a third factor such as social class or poor nutrition or whether smoking either reduces maternal appetite or has some direct inhibitory effect on fetal

metabolism is open to discussion. A study on fetal growth retardation in rats (Younoszai, et al., 1969) showed that a reduction in food intake was associated with cigarette smoke. However, in addition to this, growth retardation was greatest in those fetuses in which the pregnant rats were exposed to actual cigarette smoke as against exposure to either pure nicotine or simple smoke. This suggested that tobacco smoke contained factors other than nicotine which were responsible for fetal growth retardation, and which were additional to the reduction of maternal appetite.

The question of a direct inhibitory effect of smoking on fetal metabolism has been studied by various workers. It has been shown (Heron, 1962) that carboxyhaemoglobin is increased in the mother who smokes and in her infant: 5 to 10 per cent of haemoglobin was changed to carboxyhaemoglobin by fairly continuous smoking. Monte11 (1964) demonstrated that


TABLE VIII Infant weight, maternal social class and smoking habit

Infants weighing 2500 g. or less a t birth

Non-smokers Smokers Ex-smokers All Cases Social class -

Number Per cent Number Per cent Number Per cent Number Per cent

I and I1 47 out of 1547 3.03 27 out of 603 4.47 5 out of 160 3.12 84 out of 2306 3.64 111 185 out of 4169 3.87 285 out of 3805 7.49 30 out of 589 5.09 514 Out of 9403 5.46 IV 38 out of 992 3.83 96 out of 1010 9.50 8 O U ~ of 112 7.14 146 out of 2167 6.73 V 43 out of 831 5.17 79 out of977 8.08 5 Out of 105 4.76 132 out of 1969 6.70

x” Difference in x2 P 114.8008

Social class 93.0412 21.7596 <0.001 Smoking 8.4213 84.6 199 <0.001 Interaction 8.4194 1.9161 X lo-’ >0.05

TABLE IX Infant weight, smoking habit and anaemia in early pregnancy

Infants weighing 2500 g. or less at birth

Maternal anaemia No anaemia (Hb less than 70 per cent when tested

before 24 weeks gestation) during pregnancy

Number Per cent Number

Non-smokers Smokers

11 out of 191 5.7 293 out of 6777 4-3 17 out of 191 8.9 398 out of 4521 8.1

Anaemia Smoking Interaction

X2 Dierence in x2 P 70.7143 69.6754 1.0389 0.2174 69.4580 5.1396 x 0.0

TABLE X Infant weight, maternal weight and smoking habit (single liveborn infants born ajier spontaneous onset of labour)


Light weight mothers Moderate weight mothers Heavy weight mothers (50 t o 69 kg.) (less than 50 kg.) (70 kg. or more)

Number Per cent Number Per cent Number Per cent

Non-smokers 41 out of 437 9.4 Ex-smokers 5 out of 52 9.6 Smokers 110 out of 593 20.3

x2 58,8104

Weight 9.8594 Smoking 3.2881 Interaction 2.3272

161 out of 4722 3.4 23 out of 1208 1.9 30 out of 549 5.5 5 out of 139 3.6

230 out of 3782 6.1 26 out of 840 3.1

Difference in xp P

48.95 10 6.5713 0.9609


TABLE XI Smoking Habit, maternal weight and height

Incidence of smoking

Short mothers Medium size mothers Tall mothers (5 ft. 1 in. to 5 ft. 3 in.) (less than 5 ft. 1 in.) (5 ft. 4 in. or more)

~ ~~~


Light weight mothers 50 kg. 308 out of 633 48.7 300 out of 543 55.2 34 O U ~ of 43 46.6

Heavy weight mothers 70 kg. 73 out of 227 32.2 387 out of 1011 35.1 602 O U ~ of 1659 36.3 All weights 1269 out of 3073 41.3 3489 out of 8277 42.4 2500 Out of 6186 40.4

Moderate weight mothers 50 to 69 kg. 685 out of 1856 36-9 2301 out of 5571 41.3 1488 out of 3781 39.4

Height Weight Interaction

XB 76.0051 74 * 7078 30 * 2765 29.8864

Difference in ,ye P

1.2973 44.4313 0.3901

TABLE XI1 Infant weight, maternal weight gain and smoking habit (single liveborn infants born after spontaneous onset of labour)


Maternal excess weight gain Normal maternal weight gain


Non-smokers Ex-smokers Smokers

64 out of 2241 2 .9 133 out of 3968 3.4 56 out of 1575 3.6 231 out of 3164 7.3 14 out of 306 4 - 6 21 out of 449 4.7

* Excess weight gain is defined as a gain of 0 . 7 kg. per week in any 4 week period after the 20th week of gestation.

x” Direrence in 2 P 5.3876

Weight gain 4.6306 0.7570 >0.05 Smoking 0.1302 4.5004 <0.05 >0.01 Interaction 0.0 0.0 >0.05

the enzyme carbonic anhydrase was diminished in amount in the cord blood of infants of women who smoke. Mosier and Armstrong (1964) demonstrated that the administration of nicotine solution to pregnant rats caused a decrease in fetal weight and in the lipid content of the fetal liver.

Another possible effect on fetal nutrition is the part played by the increased cyanide intake of smokers. The effect of smoking on thiocyanate and B,, metabolism has been investigated (McGarry and Andrews, 1972). Further factors

which may affect fetal growth are either diminution of placental circulation or placental separation. In this study both accidental antepartum haemorrhage and antepartum haemorrhage of uncertain origin occurred more frequently among those women smoking during pregnancy (Table XIII). If the cause of prematurity is studied antepartum haemorrhage was thought to be the cause in 1 -2 per cent of those patients who smoked in pregnancy compared with only 0.5 per cent among non-smokers. Russell el al. (1966) similarly found an increase


TABLE XI11 Incidence of anteparturn haemorrhage

Abruptio placentae or ‘other’ forms of APA

Infants weighing Infants weighing All infant weights more than 2500 g. 2500 g. or less

Number Per cent Number Per cent Number Per cent --

Non-smokers 75 out of 536 14.0 316 out of 9224 3 .4 391 out of 9760 4 . 0 Smokers 131 out of 807 16.2 284 out of 7345 3.9 415 out of 8152 5 . 1

Maturity Smoking Interaction

x2 Difference in x2 P 384.4220 3.2473 381 .I747 <0.001 6.7491 x 3,1798 <0.01 >0,001 1.2939 X 0.0 >0.05

in vaginal bleeding during early pregnancy among women who smoked.

The ratio of male to female infants was not affected by the maternal smoking habit.

Factors other than smoking during pregnancy certainly affect fetal growth, and some like maternal age and parity are clearly inter-related with smoking.

In the present series 45 per cent of young women under the age of 25 smoke, compared with 38.8 per cent of those over the age of 25 years. If these figures are compared with those for 1958 from the Perinatal Mortality Survey there would seem to have been at least a 50 per cent increase in the smoking habit over ten years. Within each age group the effect of smoking on infant weight persists (Table XIV).

The smoking habit appeared to increase with maternal parity but if each age/parity group is considered (Table XV) it is seen that young multipara and particularly grande multiparae in their twenties and early thirties smoked most heavily.

4. PerinutuI Mortality Of primary importance is whether, as well

as influencing fetal size, maternal smoking increases perinatal mortality. Schoeneck (1941), in a study of rabbits exposed to cigarette smoke found a ten-fold increase in stillbirths and a three-fold increase in neonatal deaths. Differ- ences in mortality described in various human studies (Table XVI) may be because some reported series include abortions as part of the

TABLE XIV Maternal age, smoking habit and infant weight


Maternal age in years Non-smokers Smokers


19 or less 20 to 24 25 to 34 More than 35 All ages

71 out of 977 7 .3 97 out of 1026 9.5 1 12 out of 2864 3.9 288 out of 2839 8 . 0 144 out of 4133 3 . 5 191 out of 2883 6 .6 42 out of 933 4 .5 88 out of 7031 2 .5

369 out of 8916 4.1 601 out of 7454 8.7

Maternal age Smoking Interaction

x” 371 * 9299 165.6004 143 .2038 135.79 17

Diyerence in J P

206.329 22 * 3966

7.4121

<0.001 t0.001 <0.01 >0.001


TABLE XV Efect of age and parity on smoking habit

Incidence of smoking (per cent)

Parity Age in years

19 or less 20 to 24 25 to 34 35 or more All ages

0 1, 2, and 3 4, 5, and 6 7 or more All parities

45.8 40.5 32.0 35.0 39.9 50.1 50.9 38.3 35.2 42.7 - 57.9 52.6 50.2 52.0 - - 55.0 45.5 48.9

46.7 46.2 39.0 40.4 42-7

N.B. These total figures differ slightly from those in tables considering age or parity alone, as only patients in whom age, parity and smoking habit were known are included in this table.

Source of study

Perinatal Mortality Survey

California 1967 Dublin 1968

1958

Sheffield 1968

Cardiff

TABLE XVI Perinatal mortality and maternal smoking habit

Perinatal mortality Author Types of fetal loss counted

Smokers Non-smokers ~ ~ ~~

Stillbirths and neonatal deaths 4.48 3.24

Underwood et al. (1967) ‘Perinatal’ deaths 2.08 1.97 Mulcahy (1968) Stillbirths, neonatal deaths and 15-20 14.0

Russell et al. (1968) Stillbirths, neonatal deaths and 7.9 4.1

Stillbirths and neonatal deaths 3.1 2.5

abortions

abortions

total mortality while others are not representa- tive of a community.

premature infants (weight 2500 g. or less) born

to those mothers who smoked was shown by Underwood et al. (1967) and by Yerushalmy

A decrease in perinatal mortality among (1964) and this finding was confirmed in the Cardiff series (Table XVII). The overall small

TABLE XVII Perinatal mortality (stillbirths and all neonatal deaths) related to infant weight and smoking habit

Perinatal deaths

In infants In infants In infants weighing 2500 g. or less weighing more than 2500 g. of all weights


Non-smokers 114 out of 436 26.1 101 out of 8597 1.2 215 out of 9033 2.4 Ex-smokers 21 out of 62 33.9 12 out of 1081 1 . 1 33 out of 1143 2.9

1 to 4 cigarettes 19 out of 71 26.8 8 out of 1003 0.8 27 out of 1074 2.5

10 to 19 cigarettes 64 out of 332 19.3 47 out of 3109 1 .5 111 out of 3441 3.2 20 or more cigarettes 28 out of 137 20.4 20 out of 1183 I .7 48 out of 1320 3.6

All smokers 133 out of 678 19.6 87 out of 6892 1.3 220 out of 7570 2.9

Smokers

5 to 9 cigarettes 22 out of 138 15.9 12 out of 1597 0.8 34 out of 1735 2.0


TABLE XVIII Length of gestation related to mortality of single liveborn infants born following spontaneous onset of labour

Neonatal deaths Length of

gestation in weeks Non-smokers Smokers


28 28 to 31 32 to 35 36 to 37 38 to 39 40 41 42 to 43 44 or more

8 out of 11 15 out of 31 4 out of 96 2 out of 339 9 out of 1799

13 out of 2904 6 out of 1311 7 out of 619 1 out of 51

72.7 48.4 4.2 0.6 0.5 0.5 0.5 1.1 2.0


11 out of 1477 7 out of 2519 3 out of 1003 4 out of 578 0 out of 82

76.9 50-0 7.9 1.1 0.7 0.3 0.3 0.7

but significant increase in mortality of infants was greater for infants born to those women born to mothers who smoke may be due to who smoked (Table XVIII). The increase in other adverse factors which are also associated perinatal mortality occurred among smokers with smoking. regardless of maternal age or parity (Table XIX).

The probable cause of death is shown in 39th week of gestation the neonatal death rate Tables XX and XXI and among stillbirths

Maturity certainly plays a part as up to the

TABLE XIX Stillbirths and neonatal deaths, maternal age and parity

Perinatal deaths

Non-smokers Smokers


Age 19 Para 0 Para 1, 2, 3 Para 4 t

Age 20 to 24 Para 0 Para 1, 2, 3 Para 4+

Age 25 to 34 Para 0 Para 1, 2, 3 Para 4

Age 35 or more Para 0 Para 1, 2, 3 Para 4+

24 out of 780 2 out of 208

-

42 out of 1433 26 out of 1442 1 out of 30


6 out of 83 8 out of 568

12 out of 297

3.07 0.96 -

2.93 1.80 3.33

2.24 1.99 3.92

7.22 1.4

4.04

27 out of 801 10 out of 240

-




3.37 4.16 -

2.36 2.02 2.27

*Only two cases

2.27 2.6 3.94

12.00 4.0 5.79


maternal smoking appeared to increase the death rate associated with antepartum haemorrhage. Among neonatal deaths, pneumonia, respiratory distress syndrome and gross immaturity were more frequently found to be con- tributory causes in the infants of mothers who smoked than in the infants of those who did not.

TABLE XX Cause of stillbirth related to smoking habit

Percentage incidence

Non-smokers Smokers Cause of stillbirth

Maternal disease Maternal hypertension Difficult labour Antepartum haemorrhage Congenital malformation Haemolytic disease Infection Anoxia (without obvious

cause) Other cause stillbirth Macerated stillbirth (with-

out obvious cause)

0.01 0.19 0.09 0.11 0.32

0.01

0.24

0.29

0.17 0.05 0-39 0.27 0.13

0.23 0.02

0.23

Total stillbirths 1.30 1.54

5 . Congenital Malformation Both Mulcahy (1968) and Yerushalmy (1964)

studied the incidence of malformation of infants

TABLE XXI Cause of neonatal death related to smoking habit

~~ ~

Percentage incidence

Non-smokers Smokers Cause of neonatal death

Immaturity (no other cause) Congenital malformation Pneumonia Asphyxia-atalectasis Birth injury Infection Haemolytic disease Respiratory distress

Other

Total neonatal deaths

syndrome

0.25 0.33 0.06 0.17 0.03 0.03 0.01

0.09 0.11

1.10

0.36 0.31 0.19 0.12 0.09

0.03

0.16 0.12

-

1.4

among mothers smoking in pregnancy and found no differences unaccounted for by maternal age or parity. The findings of the present study are presented in Table XXII. The numbers were too small to sub-divide by age and parity.

6. Surgical Induction of Lubour Lowe (1959) showed a reduced incidence of

induction of labour among women who smoked and this finding has been confirmed by Herriot et al. (1962) and again in the present study

TABLE XXII Incidence of congenital abnormality (all single births)

Non-smokers Smokers


Total abnormal infants Type of abnormality

Anencephaly 18 Spina bifida 20 Other C.N.S. abnormality 38 CVS abnormality 34 Gut abnormality 21 Genito-urinary abnormality 39 Bone abnormality 65 Cleft palate and/or hare lip 10

Other abnormality 19

,ye (all abnormalities) = 2.22, p = > 0.05. x2 (cleft palate and hare lip) = 5.36, p = <0.05 >0.01.

2.37

0 . 2 0.22 0-42 0.37 0.23 0.43 0.72 0.11 0.21

15 23 36 32 24 25 52 20 18

~

2.73

0 . 2 0 .3 0.47 0.42 0.32 0.33 0.68 0.26 0.24


(Table XXII1). It seems unlikely to be due to smaller infant size with consequently less inductions for possible disproportion, as this practice is no longer common. Table XXIV demonstrates that the reduction of induction of labour among those who smoked was not due to a decrease in the incidence of postmaturity nor to less inductions for postmaturity. Age and parity should have a reverse effect on induction as the older primagravida who might be expected to need the most inductions, nevertheless smoked less than any other age/parity group.

TABLE XXIll Incidence of induction of labour (Single liveborn infants)

Labour induced

Number Per cent.

Non-smokers 1736 out of 8912 19.4 Ex-smokers 257 out of 1126 22.0 Smokers 1226 out of 7452 16.4

x2 = 26.814; p = <0.001.

The main reason for the reduction of the need for surgical induction among those who smoked appeared to be the lower incidence of toxaemia (Table XXV).

7. Pre-eclamptic toxaemia Underwood et al. (1967) first noted the lowered

incidence of pre-eclamptic toxaemia among women smoking during pregnancy. Duffus and MacGillivray (1 968) pointed out that despite the fewer number of cases, those women who smoked and developed albuminuric pre-eclampsia had a higher associated perinatal mortality. Russell el al. (1968), and also the Perinatal Mortality Survey team confirmed the association between smoking and a decreased incidence of toxaemia.

In this study, mild or moderate pre-eclamptic toxaemia was recorded when, after the 20th week of pregnancy, the diastolic blood pressure rose above 90 mm.Hg on at least two occasions and there was clinical oedema andlor proteinuria of less than 1 g./litre. Severe pre-eclampsia was recorded when the above findings were associated with proteinuria of 1 g./litre. Hypertension was defined and recorded when a diastolic blood pressure of 90 mm.Hg or a systolic blood pressure of 150 mm.Hg was found on at least two occasions before pregnancy or before the 20th week.

This present study revealed a decrease in hypertension and in pre-eclamptic toxaemia

TABLE XXIV Incidence of induction of labour .for ‘postmaturity’ (single liveborn infants)

Non-smokers Smokers


Incidence postmaturity 955 out of 8912 10.7 927 out of 7452 12.4

maturity 1451 out of 8912 16.2 959 out of 7452 12.8 Cases induced other than for post-

Cases induced for postmaturity

Total cases induced 1736 out of 8912 19.4 1226 out of 7452 16.3 42 or more weeks gestation 285 out of 8912 3.2 267 out of 7452 3 . 5

TABLE XXV Incidence of induction of labour for ‘toxaemia of pregnancy’

Cases induced other Cases induced for Total cases induced than for toxaemia toxaemia


Non-smokers 1016 out of 9142 1 1 . 1 1054 out of 9142 11.5 2081 out of 9142 22.8 Smokers 887 out of 7661 11.6 544 out of 7661 7 .1 1444 out of 7661 18.8


TABLE XXVI Hypertension, sociaI class and smoking habit

Hypertension Mild P.E.T. and moderate P.E.T. Severe P.E.T. Social class

Per cent Number Per cent Number Per cent Number

Non-smokers I and I1 111 IV V

All classes

Smokers I and I1 111 IV V

All classes


1196 out of 8174

74 out of 601 366 out of 3819

87 out of 1007 86 out of 974

613 out of 6401

15.3 15.0 1 3 . 7 12.6 14.6

12.3 9 . 6 8 .6 8 . 8 9 .6


471 out of 8174


265 out of 6401

4 . 2 6.3 5.7 5 . 4 5 . 8

4.3 4 . 4 3 .2 3.9 4.1

15 out of 1554 1.0 37 out of 4793 0.8

3 out of 996 0 .3 3 out of 831 0 . 4

58 out of 8174 0 .7

1 out of 601 0 .2 12 out of 3819 0 .3

5 out of 1007 0.5 4 out of 974 0 - 4

22 out of 6401 0 . 3

Hypertension

Social class Smoking Interaction

X2 83.1207 69.2533 2.7366 2.5708

Diyerence in x2 P

13.8674 66.5168 0.1657

which occurred regardless of social class (Table XXVI).

Various explanations have been given as to the reduced incidence of pre-eclamptic toxaemia in women who smoke during pregnancy. The explanation cannot lie solely with the age or parity of the patient as it is just the young primigravida who tends to be the one who smokes most heavily who is known clinically to be most prone to develop pre-eclampsia.

The evidence of Coffman and Javett (1963) that nicotine dilates the muscle capillaries may offer one explanation for the lowered incidence of pre-eclampsia among smokers despite previous suggestions that cigarette smoking caused peri- pheral vasoconstriction and mild hypertension. Volle and Koelle (1970) drew attention to the complex action of nicotine.

The association between smoking and maternal weight and weight gain in pregnancy was studied by Duffus and MacGillivray (l968), who found no difference between smokers and non-smokers. Contrary to their findings, Table XXVIL demonstrates that heavy smokers had a lesser incidence of excessive weight gain.

It can also be shown (Table XXVIII and XXrX) that despite the lower initial weight and

TABL~. XXVII Maternal weight gain and smoking habit

Excess weight gain*

Number Per cent. -__ Non-smokers 2827 out of 7762 36.4 Ex-smokers 415 out of 989 42.0 Smokers

1-4 cigarettes 334 out of 829 40.3 5-9 cigarettes 496 out of 1327 37-4 10-19 cigarettes 831 out of 2632 31.6 20+ cigarettes 267 out of 956 27.9

All smokers 1928 Out of 5744 33.6

* Excessive weight gain is defined as a gain of 0 . 7 kg. per week in any 4 week period after the 20th week of gestation.

reduced weight gain of the woman who smoked during pregnancy, the incidence of toxaemia remained lower in the smoker regardless of her initial weight or weight gain. This suggested that lack of weight gain was not the only explanation for the lowered incidence of toxaemia.

It may be that it is not nicotine but one of the other active constituents of tobacco smoke which is responsible for the lower incidence of pre- eclamptic toxaemia among smokers. Cyanide


TABLE XXVIII Hypertension, maternal weight and smoking habit

Incidence of hypertension

Maternal weight Non-smokers Smokers Total


Low weight 87 out of 522 16.66 63 out of 652 9.66 150 out of 1174 12.77 Moderate weight 1265 Out of 6603 19.16 671 out of 5092 13.17 1936 out of 11695 16.55 Heavy weight 356 Out of 938 37.95 165 out of 584 28.25 521 out of 1522 34.23 All weights 1708 out of 8063 21.18 899 out of 6328 14.20

Maternal weight Smoking Interaction

x2 335.7194 1 15.3671 33.2878 33.2653

Difference in x2 P

220.3523 t0.001 82.0792 <0.001

2 -2 >0.05

is present in tobacco (Darby and Wilson, 1967) and is detoxicated in the body to thiocyanate. Thiocyanate has been shown to be present in higher concentrations in both blood and urine of the smoker than in the non-smoker. Thio- cyanate has a known hypotensive effect and it is possible that this is the active agent in reducing the incidence of both hypertension and pre- eclampsia in the woman who smokes.

Despite the favourable effect of smoking on the incidence of hypertension in pregnancy the present study confirmed the findings of Duffus and MacGillivray (1968) that there was an increased perinatal mortality if hypertension

was present in a woman who smoked during her pregnancy (Table XXX). It may be that when hypertension does occur there is already an element of poor fetal growth which, if associated with smoking during pregnancy, contributes to the higher perinatal mortality.

8. Hypertension It is appreciated that many cases defined as

mild pre-eclampsia may in fact be cases of hypertension unrecognized in early pregnancy. Although the separation of ‘hypertension of pregnancy’ into hypertension and pre-eclamptic toxaemia is necessarily a rather arbitrary one,

TABLE XXIX Hypertension, weight gain and smoking habit

Incidence ‘hypertension’

Maternal weight gain Non-smokers Smokers All cases


No excess weight gain 1033 out of 4971 20.78 492 out of 3859 12.74 1525 out of 8830 17.27 Excess weight gain 666 Out of 2862 23.27 369 out of 1952 18.90 1035 out of 4814 21.49 All weight gains 1699 out of 7833 21.67 861 out of 5811 14.81

X2 Difference in x2 P 116.1732

Excess weight gain 91 -4261 24.7471 t0.001 Smoking 9.5917 81.8344 <0.001 Interaction 2 -20 9.5917 <0.01 >0*001


TABLE XXX Hypertension, perinatal mortality and smoking habit

Incidence of perinatal deaths

Non-smokers Smokers All cases ~~ ~


With hypertension 59 out of 1899 3 . 1 0 52 out of 1029 5.05 111 out of2928 3.79 No hypertension 142 out of 7043 2.01 153 out of 6403 2.38 295 out of 13446 2.19 All cases 201 out of 8942 2.24 205 out of 7432 2.75

Smoking Hypertension Interaction

X2 36.8155 30.7245

Difference in x2 P

6.0911 t0.05 >0.01 2.0793 28.6451

2-20 2,0793

the lower incidence of hypertension among those who smoked may be explained differently than the lower incidence of pre-eclampsia. The hyper- tensive patient is very often the older, prima- gravid, higher social class patient who has been shown to smoke little.

9. Antepartum haemorrhage Placental separation has been shown to be

more common in those women who smoke and Table XXXI demonstrates that this was not just an effect of parity.

10. Thrombo-embolism A further maternal condition which has been

discussed in relation to smoking is that of thrombo-embolism. Interest has centred mainly

around oral contraceptive users and Kay et a/ . (1969) showed that the smoking habit was increased among oral contraceptive users.

Daniel et al. (1967), basing their report on the same community as this present survey, showed that suppression of lactation with oestrogen is associated with a higher incidence of puerperal thrombo-embolism.

In the Cardiff survey the incidence of cigarette smoking was shown not to effect the incidence of puerperal thrombo-embolism (Table XXXII). Millar and Littlepage (1970) made the suggestion that smoking might be a further causative factor in puerperal thrombo-embolism but to judge by our study this seemed merely to be an association between lower social class, increased smoking habit and a low incidence of breast

TABLE XXXI Accidental haemorrhage, parity and smoking habit

Incidence of accidental haemorrhage

Para 0 ~ _ _ _ _ _ ~ ~

Para I , 2 and 3 Para 4 or more


Non-smokers 65 out of 3174 2.04 84 out of 519 1.61 13 out of 776 1.67 Smokers 71 out of 2459 2.88 103 out of 4289 2 . 4 29 out of 917 3.16

Parity Smoking Interaction

X2 Direrences in x2 P 319.3232 304.2561 15.0671 t0.001 232,5728 71,6834 <0.001 2149 6994 17.8734 <0.001


TABLE XXXII Smoking and puerperal thrombo-embolism

Incidence of thrombo-embolism

Breast feeding Lactation suppressed with oestrogen


Non-smokers Smokers

8 out of 3134 0.25 26 out of 5536 0.46 5 out of 1784 0.28 27 out of 5487 0 .49

x” Difference in 2 P 3.8998

Method of feeding 5 -2 3.8441 <0,05 >0.01 Smoking 5 -3 5 -2 >0.05

5 -3 >0.05 Interact ion 5 -21

feeding (Table XXXIII). It seems possible that similar inter-related factors may account for the increase of cigarette smoking among oral contraceptive users.

CONCLUSIONS The baby born to the mother who continued

to smoke during pregnancy was born small. A minor influence on infant weight was a small increase in premature labour among those women who smoked. An increased incidence of placental separation may have led to premature labour and placental insufficiency. There was also a correlation between the lighter women, who not only smoked more heavily but produced

smaller babies. In addition there appeared to be some direct adverse influence of maternal smoking on fetal nutrition, which was indepen- dent of other factors such as maternal weight or social class.

The woman who smoked during pregnancy was also more likely to lose that baby. There was a small but significant increase in perinatal mortality for any period of gestation. The improved mortality of the baby who was premature by weight was artificial and was due to the increased number of mature but small babies in this group. The mortality was associated with immaturity and respiratory distress syndrome and infection and occurred independently of maternal age and parity.

TABLE XXXIII Smoking, social class and lactation suppression

Incidence of breast feeding on the 7th day

Social class Non-smokers Smokers


I and I1 667 out of 1563 42.7 187 out of 616 30.4 III 1505 out of 4831 31.2 893 out of 3859 23.1 IV 296 out of 1004 29.5 198 out of 1019 19.4 V 208 out of 838 24.8 196 out of 986 19.7

2 Difference in ,$ 223.076

P

Social class 118.1531 104.9229 <0.001 Smoking 22.2727 95.8804 <0*001 Interaction 19.3911 2.8815 >0.05


In this series the mother who smoked during pregnancy appeared to be more at risk of having an infant with cleft palate and hare lip, although inevitably the affected numbers were small.

At first sight the effects of smoking upon the mother were advantageous: there is less surgical induction with less associated hypertension and pre-eclamptic toxaemia. There was, however, a higher incidence of placental separation if the mother smoked.

A satisfactory explanation is still required to account for the reduction in infant size and blood pressure levels found in association with maternal smoking. Poor maternal nutrition, reduced appetite and placental separation may all play a part, but there appears to be some additional adverse effect of smoking on fetal nutrition. Nicotine has been the one element in cigarette smoke which has been largely incrimi- nated, although an increase in carboxyhaemoglobin has also been reported.

An alternative hypothesis is that cigarettes by virtue of their cyanide content have an adverse effect on maternal and fetal vitamin B,, metabolism and possibly also, by detoxication of cyanide to thiocyanate, reduce maternal blood pressure.

ACKNOWLEDGEMENTS We thank Professor A. S . Duncan and Profes-

sor C. R. Lowe for their original work in initiat- ing the survey. Professor H. Campbell has throughout been a source of stimulation and encouragement. The Atlas Computer Labora- tory, Chilton, and in particular Mrs. J. Lay, have made available and advised on computer facilities. Mr. Tweedie of the University of Liverpool designed and programmed the multi- factorial test of significance used in many tables.

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a community study of smoking in pregnancy

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