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Effects of maternal cigarette smoking on fetal breathing and fetal movements
Effects of maternal cigarette smoking on fetal breathing and fetal movements I. THALER, M.D.
J.
D. S. GOODMAN, M.B., M.R.C.O.G.
G. S. DAWES, D.M., F.R.C.O.G., F.R.S. Oxford, England The effect of cigarette smoking on fetal breathing and fetal movements was studied in 10 women with low-risk pregnancy of 34 to 38 weeks' gestation. A continuous Doppler ultrasound method was used to measure fetal breath intervals. Smoking two cigarettes caused a small increase in the rate of fetal breathing (p < 0.01 ), which persisted for 60 minutes; the proportion of time the fetus spent breathing was not changed. There was a decrease in the number of fetal movements felt by the mother. These findings are discussed in relation to the alleged pathophysiologic effects of tobacco smoking on the fetus. (AM. J. 0BSTET. GYNECOL. 138:282, 1980.)
S r N c E the first report on human fetal breathing in utero with the use of an ultrasound method, 1 a large body of literature has appeared 2 which concentrates on the incidence of breathing (i.e., the proportion of time that fetai breathing movements are present) rather than its pattern. Yet observations on sheep have shown that the pattern of breathing, whenever present. is of importance as a diagnostic index of fetal health.a Recently, it has become possible to record fetal breath intervals quantitatively by means of the continuous Doppler ultrasound method. Therefore, we have taken the opportunity to study the effects of maternal cigarette smoking on fetal breath intervals and on fetal body movements and to reexamine the effect of smoking on the incidence of breathing in low-risk pregnancy. The original reports on the effects of smoking on fetal breathing, with use of the A-scan ultrasound method to foiiow movements of the chest waii, described a reduction in the incidence of fetal breathing that lasted an hour or more."· 5 There are three reasons
for treating this evidence with reserve. First, although injection or infusion of nicotine into the descending aorta of the pregnant ewe caused a decrease in fetal breathing accompanied by, and attributed to, hypoxemia, only doses of nicotine that were larger than those anticipated from human smoking were effective. 6 Second, observations on human fetal breathing activity by real-time B-scan and/or by continuous Doppler ultrasound showed an incidence of breathing substantially less than that reported with the A-scan method. It seemed likely that the A-scan method recorded both breathing and body movements. And third, measurements in sheep showed that movements of the chest wall do not give a direct, reliable measure of fetal breathing. 7 The present study showed that cigarette smoking does not reduce the incidence of fetal breathing, but does alter the frequency distribution of breath intervals, the mean rate of breathing, and the number of fetal body movements recorded by the mother.
Material and methods From the 1'·./ufJield Institute for 1\ledical Research,
University of Oxford. Supported by grants from the Medical Research Council, the Tobacco Advisory Council, and Action Research for the Crippled Child. Received for publication September 12, 1979. Rev~'ed
March 19, 1980.
Acceptedjune 11, 1980. Reprint requests: Dr. Israel Thaler, Department of Obstetrics and Gynecology, Rambam Medical Centre, Haifa, Israel.
282
Ten women volunteered for the study. They 1·anged in age from 20 to 34 years, had uncomplicated pregnancies of 34 to 3"8 weeks' gestation, and smoked 8 to 25 cigarettes (of a middle tar yield) a day. Observations were made after the women had abstained from smoking for 12 hours or more, and after they had eaten a breakfast that contained at least 55 gm of carbohydrate and 345 calories (average, 80 and 482, respectively). Measurements were started between 0930 and 1000 hours, 60 to 90 minutes after breakfast, with the 0002-9378/801190282+06$00.60/0
©
1980 The C. V. Mosby Co.
Maternal smoking effects on fetal breathing and movements
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women in a semirecumbent position. Within the hrst 30 to 40 minutes (the control period). each woman was given a light snack. which supplied, on the average, 2:l gm of carbohvdralt' and 250 calories. Each woman was monitored on 2 successive days, at the same time of dav and after the same breakfast. This procedure \\
Fig. 2. Rate of fetal breathing (±SE) on the control day (•) and on the day when two cigarettes were smoked (beginning at zero time, u).
on a tape recorder (Sony TC l.'i:EiO) and were later replaved into a peak frequency follower and analyzer'' The intervals between successive peaks were displayed on a multichannel recorder (MX-·! Devices Instruments. England). Fig. I demonstrates the' mtput signal from rhe peak frequency follower, together with the corresponding breath intervals measured to within 100 msec. Artifact~ due to fetal or maternal movement were readily identified and were excluded. Mean breathing intervals and the root mean square (RMS) values were calculated for each 5-minute epoch; only segments that contained at least :Hl breaths were used for further analysis. The proportion of time the fetus spent breathing was also calculated for each ,'i-minute epoch. Statistical significance was determined by analvsis of variance and paired t test, with each fetus serving as its own control. Validation
Simultaneous visual real-time B-scan (I\ udear Enterprise Sector Scanner) and audible continuous Doppler ultrasound records of fetal breathing movements were made on a video-recorder. Over :l,t100 breaths were identified by independent observers, with the usc of visual signals and/or audible. Each obserl'er pressed a key whenever he identified a breath, and the proportion of coincidences within 0.25 second was recorded. There was good agreement, but when both lhe audibk signal~ were compared. the agreemelll was suhsta ntially betrer, 95% versus 92% for visual-vi:mal and for
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visual-audible comparisons. We concluded that it was easier to identify a fetal breath with certainty with the continuous Doppler method, which was also better repeatable than visualization of the chest wall with the real-time method. Results
The effect of smoking two cigarettes on fetal breathing rate is shown in Fig. 2. The mean breathing rates in the control periods of both the smoking and the nonsmoking days were similar. 46.2 ± 1.8 (SE) min-• and 46.5 ± i.5 min-•· respeeiiveiy. The mean frequency distributions of breath intervals were almost identical during the control period of the two days (Fig. 3), and showed evidence of a bimodal distribution.
Within the first 5 minutes from the start of smoking, there was an increase in fetal breathing rate, which reached 54.2 ± 3 min- 1 at 10 minutes (Fig. 2) and rose to a peak of 57.1 ± 3.9 min-• between 20 and 25 minutes. There was a shift to the left in the frequency distribution of breath intervals, the peak of which became higher. The shift was maximal between 15 and 30 minutes (Fig. 4). Over the next 30 minutes the rate of fetal breathing declined. At 60 minutes it was still above the control level (50.4 ± 3.3 min-•, Fig. 2), and the frequency distribution was still somewhat to the left of that in the control period. An analysis of variance W
Maternal smoking effects on fetal breathing and movements
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women. On the smoking clay there were significant differences between the mean rates of breathing in the live epochs tp < 0.02:1). A paired t test between the mean rates of breathing in the control period and each of the f(JJiowing 15-minute epochs showed a significant increase in breathing rate in the hrst and second 15minute epochs after smoking started ( p < 0.0 1). The rate of breathing on the control day is shown in Fig. 2. Anahsis of ,·ariance did not show a significant difference between the mean rates of breathing in the five epochs (p < (J.05). Table I shows the mean breath intervals for 1he control periods and the following two :W-minute epochs for each day. The variability of breath intervals was determined as the R.'\fS value of the differences from the mean. The R.\fS value for both the control periods was 397 msec. It declined slightlv on both the smoking and nonsmoking davs during the studv period, to an average of ~15~ msec. In order to determine whether the variability was related to the rate of breathing, regression analysis between breath intervals and RMS values in 5-minute epochs was performed. A highly significant correlation was found between the two (r = 0.45, p < 0.001), thereby showing that variability increased as breaths slowed. This relationship held both before and after smoking. However, the regression lines obtained from all the 5-minute epochs on the control day and in the
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Fig. 6. Numbers of fetal movements (per :SO minutes, ±SE) recorded hy the mothers with (cc) or without (•) smokin~ two cigarettes.
Table I. Mean values ± SE of breath intervals (sec) in 10 human fetuses in the absence and presence of maternal smoking .Yo smoking
Control period 0-30 min 0-60 min
1.29 ± 0.006 (4,375) !.27 ± 0.005 ( 4,227\ 1.:~9 ± 0.006 (3,492)
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control period of the smoking dav and that obtained after smoking started were not signihcmtlv diftcrenl. The mean incidences of fetal breathing during the control period of the smoking Cia) ~tnd 011 the cmHrol day were h·!.W.k ± ':2.7 and :'i·Uifi; .:!: H.O . respeniveh. Smoking had no significant effect on tht· incidence ot breathing. There was also no change 011 the co!llrol dav, and no signilficant difference ht·tw(Til I he two da\s (Fig.:·>). The number of fetal movements telt t)\ the mother was signihcanth reduced dming the tirst :ll1 minute' after smoking started (p < 0.0 1). The numher was stili reduced during the next 30 minutes, but returned to the control level between 60 and 90 rninutt's (Fig. 6). ;\Jo significant change was observed on the 1ontrol cia\. Outcome of pregnancy. All 10 women were deli\·erecl of inhmts \·aginally. Seven had spomaneous deliveries and three required fi>rceps deliven. two because of signs of fetal distress and one J,ct.1use ol thick
286 Thaler, Goodman, and Dawes Am.
meconium liquor (the fetal pH and heart rate pattern were normal). Seven deliveries were at term, and the average weight of the newborn neonates in this group was 3.21 kg (0.13 SD). One delivery was at 38 weeks' gestation (2.7 kg), one at 37 weeks (2.83 kg), and one at 36 weeks ( 1.93 kilograms). Apgar scores (I and 5 minutes) were normal in nine babies. The premature baby born at 36 weeks required an immediate intubation because of apnea, but was extubated at 5 minutes with an Apgar score of 5.
Comment It has been suggested that there is a long-term association between maternal cigarette smoking and fetal growth retardation, premature birth, and increased risk of stillbirth or neonatal death. 10 Both human studies11. 1'1 and animal experiments 14- 16 have been interpreted as suggesting that fetal hypoxia, induced by nicotine or carbon monoxide in tobacco smoke, may be responsible. However, there is as yet no direct proof of these hypotheses. Our latest f1ndings serve to set straight the previous record and present a paradox. The A-scan ultrasound method is liable to misinterpretation on several counts, including bidirectional movement of the fetal chest with each breath. The Doppler method of identifying fetal breathing has been well validated in both sheep and man/· 17 · 1" and has the advantage over real-time B-scans that breath intervals can be measured objectively to an acceptable degree of accuracy. The new findings show that the rate of fetal breathing is enhanced after cigarette smoking, with no change in incidence. The difference from the previous f1ndings reported from this and other institutions is attributed to the difference in methods. The paradox arises from the fact that maternal cigarette smoking is associated with a reduction in fetal
J
Onober I, 19HO Obstet. Gvrwrol
movements (as perceived bv the mother) without a concomitant decrease in the incidence of breathing and with a decrease in mean breath interval. The formn observation needs verification bv an objective method. Let us for the sake of argument assume that it is true. At the present moment, the onlv mechanism bY which fetal body or limb movements are reduced is belieYed to be hypoxia. However, hypoxia is known to be associated with prolonged apnea in fetal lambs or monkeys, and this was not observed in our study. It is possible, then, that additional factors other than hypoxia mav inlluence fetal body movements. Indeed, no adequate studies have been executed to discriminate between hypoxemia, acidemia, and hypoglycemia as a cause of the disappearance of fetal movements prior to death in utero. Yet all three are known to be associated with prolonged apnea in fetal lambs. The simplest explanation for the paradox is multifactorial, that the decrease in mean breath inten·al is attributed to, for instance, hypercapnia, whereas the decrease in perceived movements is due to some other cause, at present unknown. Two points may be made, first that it is unlikely on present evidence that the fetus is subject, as a result of maternal smoking, to hypoxemia sufficient to reduce bodv and limb movements, since breathing is maintB.ined and the rate is increased. Second, it is unlikely that nicotine, which certainly crosses the placenta in man, 19 has a direct action on the carotid bodies. The latter are relativelv insensitive to pharmacologic stimuli in fetal lambs near term,Z 0 · ~· and maternal infusion of large closes does not appear to affect fetal breathing. We are grateful for the help of Professor A. C. Turnbull and the consultants who made their patients available, and to the patients themselves who gave so much of their time and interest to the study.
REFERENCES I. Boddy. K., and Robinson, J. S.: External method for detection of fetal breathing in utero, Lancet 2: 1231, 1971. 2. Wilds, P. L.: Observations of intrauterine fetal breathing movements, AM. J. OssTET. GYNECOL. 131:315, 1978. 3. Chapman, R. L. K., Dawes, G. S., Rurak, D. W., and Wilds, P. L.: Intermittent breathing before death in fetal lambs, AM. J. OssTET. GYNECOL. 125:73, 1978. 4. Gennser, G., Marsal, K., and Lindstrom, K.: Maternal smoking and fetal breathing movements, AM. J. 0BSTET. GYNECOL. 123:861, 1975. 5. Manning, F. A., and Feyerabend, C. I.: Cigarette smoking and fetai breathing movements, Br. j. Obstet. Gynaecoi. 83:262, 1976. 6. Manning, F., Walker, D., and Feyerabend, C.: The effect of nicotine on fetal breathing movements in conscious pregnant ewes, Obstet. Gynecol. 52:563, 1978.
7. Poore, E. R.: The relationship between fetal breathing movements as measured by thoracic pressure changes and the movement of the chest measured directly in vivo. Presented at the Fifth Conference on Fetal Breathing. Nijmegen, Holland, 1978. 8. Boyce, E. S., Dawes, G. S., Gough,]. D., and Poore, E. R.: Doppler ultrasound method for detecting human fetal breathing in utero, Br. Med. J. 2: 17, 1976. 9. Gough, J. D., and Poore, E. R.: A continuous Doppler ultrasound method for recording foetal breathing in utero, Ultrasound Med. Bioi. In press.
10. Pirani, B. B.: Smoking during ptegnancy, Obstet. Gynecol. Surv. 33:1, 1978. 11. Quigley, M. E., Sheehan, K. L., Wilkes, M. M., and Yen, S. S. C.: Elucidation of mechanisms for the deleterious effects of maternal smoking on fetal well-being. Pre-
\' olum e I :IH
Number :1
12.
~~~-
14.
15.
16.
sen ted at the Twenty-fifth Annual Meeting of the Society for Gvnecologic Investigation, Atlanta, Georgia, March 15-18. 1978. Cole. P. V .. Hawkins. L. V., and Roberts. D.: Smoking during pregnancy and its effect on the fetus. J. Obstet. Gynaecol. Br. Commonw. 79:782, 1972. Longo, L. D.: 1~hc biological effects of carbon monoxide on the pregnant woman, fetus, and newborn infant, AM. J. 0BSTET. GYNECOL. 129:69, 1977. Sumki, K., Horigucht, T .. Comas-Urrutia, A. C., Mueller-Heubach, E., .\forishima, H. 0., and Adamsons, K.: Pharmacologic effects of nicotine upon the fetus and mother in the rhesus monkev, AM. J. 0BSTET. GYNECOL. lll:l092. 1971. Resnik. R., Brink, G. W., and Wilkes, M. M.: Catecholamine-mediated reduction in uterine blood flow followmg nicotine infusion in the pregnant ewe. Presented at the Twentv-fifth Annual Meeting of the Society for Gynecologic Investigation. Atlanta, Georgia, March 15-18, 1978. Kirschbaum,J. H., Dilts, P. V .. Jr., and Brinkman, C. R.:
Maternal smoking effects on fetal breathing anrl movements
287
Some acute effects of smoking in sheq• and their fetuses. Obstet. Gvnecol. 35:527, 1970. 17. Gough, J.D., and Poore, E. R.: Directi<•nal Doppler measurements of fetal breath in!!. I. Ph\sinl tl.ond.) 272: 121', 197i.
"-·
18. Goodman, J D. S., and Mantell. C· ll
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D. S. GOODMAN, M.B., M.R.C.O.G.
G. S. DAWES, D.M., F.R.C.O.G., F.R.S. Oxford, England The effect of cigarette smoking on fetal breathing and fetal movements was studied in 10 women with low-risk pregnancy of 34 to 38 weeks' gestation. A continuous Doppler ultrasound method was used to measure fetal breath intervals. Smoking two cigarettes caused a small increase in the rate of fetal breathing (p < 0.01 ), which persisted for 60 minutes; the proportion of time the fetus spent breathing was not changed. There was a decrease in the number of fetal movements felt by the mother. These findings are discussed in relation to the alleged pathophysiologic effects of tobacco smoking on the fetus. (AM. J. 0BSTET. GYNECOL. 138:282, 1980.)
S r N c E the first report on human fetal breathing in utero with the use of an ultrasound method, 1 a large body of literature has appeared 2 which concentrates on the incidence of breathing (i.e., the proportion of time that fetai breathing movements are present) rather than its pattern. Yet observations on sheep have shown that the pattern of breathing, whenever present. is of importance as a diagnostic index of fetal health.a Recently, it has become possible to record fetal breath intervals quantitatively by means of the continuous Doppler ultrasound method. Therefore, we have taken the opportunity to study the effects of maternal cigarette smoking on fetal breath intervals and on fetal body movements and to reexamine the effect of smoking on the incidence of breathing in low-risk pregnancy. The original reports on the effects of smoking on fetal breathing, with use of the A-scan ultrasound method to foiiow movements of the chest waii, described a reduction in the incidence of fetal breathing that lasted an hour or more."· 5 There are three reasons
for treating this evidence with reserve. First, although injection or infusion of nicotine into the descending aorta of the pregnant ewe caused a decrease in fetal breathing accompanied by, and attributed to, hypoxemia, only doses of nicotine that were larger than those anticipated from human smoking were effective. 6 Second, observations on human fetal breathing activity by real-time B-scan and/or by continuous Doppler ultrasound showed an incidence of breathing substantially less than that reported with the A-scan method. It seemed likely that the A-scan method recorded both breathing and body movements. And third, measurements in sheep showed that movements of the chest wall do not give a direct, reliable measure of fetal breathing. 7 The present study showed that cigarette smoking does not reduce the incidence of fetal breathing, but does alter the frequency distribution of breath intervals, the mean rate of breathing, and the number of fetal body movements recorded by the mother.
Material and methods From the 1'·./ufJield Institute for 1\ledical Research,
University of Oxford. Supported by grants from the Medical Research Council, the Tobacco Advisory Council, and Action Research for the Crippled Child. Received for publication September 12, 1979. Rev~'ed
March 19, 1980.
Acceptedjune 11, 1980. Reprint requests: Dr. Israel Thaler, Department of Obstetrics and Gynecology, Rambam Medical Centre, Haifa, Israel.
282
Ten women volunteered for the study. They 1·anged in age from 20 to 34 years, had uncomplicated pregnancies of 34 to 3"8 weeks' gestation, and smoked 8 to 25 cigarettes (of a middle tar yield) a day. Observations were made after the women had abstained from smoking for 12 hours or more, and after they had eaten a breakfast that contained at least 55 gm of carbohydrate and 345 calories (average, 80 and 482, respectively). Measurements were started between 0930 and 1000 hours, 60 to 90 minutes after breakfast, with the 0002-9378/801190282+06$00.60/0
©
1980 The C. V. Mosby Co.
Maternal smoking effects on fetal breathing and movements
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Time in seconds Fig. 1. Records of Doppler shift frequencies before and after filtering (a!HJl'l'i from an ultrasound transducer on the maternal abdomen, showing the rise in frequency with increased velotitv of few! inferior vena caval blood flow on inspiration. The lowe't reund shows the breath interval derived instant
women in a semirecumbent position. Within the hrst 30 to 40 minutes (the control period). each woman was given a light snack. which supplied, on the average, 2:l gm of carbohvdralt' and 250 calories. Each woman was monitored on 2 successive days, at the same time of dav and after the same breakfast. This procedure \\
Fig. 2. Rate of fetal breathing (±SE) on the control day (•) and on the day when two cigarettes were smoked (beginning at zero time, u).
on a tape recorder (Sony TC l.'i:EiO) and were later replaved into a peak frequency follower and analyzer'' The intervals between successive peaks were displayed on a multichannel recorder (MX-·! Devices Instruments. England). Fig. I demonstrates the' mtput signal from rhe peak frequency follower, together with the corresponding breath intervals measured to within 100 msec. Artifact~ due to fetal or maternal movement were readily identified and were excluded. Mean breathing intervals and the root mean square (RMS) values were calculated for each 5-minute epoch; only segments that contained at least :Hl breaths were used for further analysis. The proportion of time the fetus spent breathing was also calculated for each ,'i-minute epoch. Statistical significance was determined by analvsis of variance and paired t test, with each fetus serving as its own control. Validation
Simultaneous visual real-time B-scan (I\ udear Enterprise Sector Scanner) and audible continuous Doppler ultrasound records of fetal breathing movements were made on a video-recorder. Over :l,t100 breaths were identified by independent observers, with the usc of visual signals and/or audible. Each obserl'er pressed a key whenever he identified a breath, and the proportion of coincidences within 0.25 second was recorded. There was good agreement, but when both lhe audibk signal~ were compared. the agreemelll was suhsta ntially betrer, 95% versus 92% for visual-vi:mal and for
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visual-audible comparisons. We concluded that it was easier to identify a fetal breath with certainty with the continuous Doppler method, which was also better repeatable than visualization of the chest wall with the real-time method. Results
The effect of smoking two cigarettes on fetal breathing rate is shown in Fig. 2. The mean breathing rates in the control periods of both the smoking and the nonsmoking days were similar. 46.2 ± 1.8 (SE) min-• and 46.5 ± i.5 min-•· respeeiiveiy. The mean frequency distributions of breath intervals were almost identical during the control period of the two days (Fig. 3), and showed evidence of a bimodal distribution.
Within the first 5 minutes from the start of smoking, there was an increase in fetal breathing rate, which reached 54.2 ± 3 min- 1 at 10 minutes (Fig. 2) and rose to a peak of 57.1 ± 3.9 min-• between 20 and 25 minutes. There was a shift to the left in the frequency distribution of breath intervals, the peak of which became higher. The shift was maximal between 15 and 30 minutes (Fig. 4). Over the next 30 minutes the rate of fetal breathing declined. At 60 minutes it was still above the control level (50.4 ± 3.3 min-•, Fig. 2), and the frequency distribution was still somewhat to the left of that in the control period. An analysis of variance W
Maternal smoking effects on fetal breathing and movements
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Fig. 5. Incidence (proportion of time ± SE) of fetal breathing with (below) or without (abm•e) smoking two cigarettes.
women. On the smoking clay there were significant differences between the mean rates of breathing in the live epochs tp < 0.02:1). A paired t test between the mean rates of breathing in the control period and each of the f(JJiowing 15-minute epochs showed a significant increase in breathing rate in the hrst and second 15minute epochs after smoking started ( p < 0.0 1). The rate of breathing on the control day is shown in Fig. 2. Anahsis of ,·ariance did not show a significant difference between the mean rates of breathing in the five epochs (p < (J.05). Table I shows the mean breath intervals for 1he control periods and the following two :W-minute epochs for each day. The variability of breath intervals was determined as the R.'\fS value of the differences from the mean. The R.\fS value for both the control periods was 397 msec. It declined slightlv on both the smoking and nonsmoking davs during the studv period, to an average of ~15~ msec. In order to determine whether the variability was related to the rate of breathing, regression analysis between breath intervals and RMS values in 5-minute epochs was performed. A highly significant correlation was found between the two (r = 0.45, p < 0.001), thereby showing that variability increased as breaths slowed. This relationship held both before and after smoking. However, the regression lines obtained from all the 5-minute epochs on the control day and in the
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Smoking
-30
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il)
1...--...i t : - - - - = - - - ' - - - - - ' - - - - ' 45 30 15 0 -30 60
30
t ',i
E
0
E
..... c(I)
T
25r
mmute~
Fig. 6. Numbers of fetal movements (per :SO minutes, ±SE) recorded hy the mothers with (cc) or without (•) smokin~ two cigarettes.
Table I. Mean values ± SE of breath intervals (sec) in 10 human fetuses in the absence and presence of maternal smoking .Yo smoking
Control period 0-30 min 0-60 min
1.29 ± 0.006 (4,375) !.27 ± 0.005 ( 4,227\ 1.:~9 ± 0.006 (3,492)
1HatRmal smoking
uo
± 0.006 (5,205)
1.1:\ :±. 0.005 (5,676\* I IH .!: O.OO!l (6,407)
The number of breaths analvzed are gi\en in paren~ \~ ~- " " "
LHC.')C~.
*Two cigarettes were smoked during the fir,r on the average.
1.~.3
minutes,
control period of the smoking dav and that obtained after smoking started were not signihcmtlv diftcrenl. The mean incidences of fetal breathing during the control period of the smoking Cia) ~tnd 011 the cmHrol day were h·!.W.k ± ':2.7 and :'i·Uifi; .:!: H.O . respeniveh. Smoking had no significant effect on tht· incidence ot breathing. There was also no change 011 the co!llrol dav, and no signilficant difference ht·tw(Til I he two da\s (Fig.:·>). The number of fetal movements telt t)\ the mother was signihcanth reduced dming the tirst :ll1 minute' after smoking started (p < 0.0 1). The numher was stili reduced during the next 30 minutes, but returned to the control level between 60 and 90 rninutt's (Fig. 6). ;\Jo significant change was observed on the 1ontrol cia\. Outcome of pregnancy. All 10 women were deli\·erecl of inhmts \·aginally. Seven had spomaneous deliveries and three required fi>rceps deliven. two because of signs of fetal distress and one J,ct.1use ol thick
286 Thaler, Goodman, and Dawes Am.
meconium liquor (the fetal pH and heart rate pattern were normal). Seven deliveries were at term, and the average weight of the newborn neonates in this group was 3.21 kg (0.13 SD). One delivery was at 38 weeks' gestation (2.7 kg), one at 37 weeks (2.83 kg), and one at 36 weeks ( 1.93 kilograms). Apgar scores (I and 5 minutes) were normal in nine babies. The premature baby born at 36 weeks required an immediate intubation because of apnea, but was extubated at 5 minutes with an Apgar score of 5.
Comment It has been suggested that there is a long-term association between maternal cigarette smoking and fetal growth retardation, premature birth, and increased risk of stillbirth or neonatal death. 10 Both human studies11. 1'1 and animal experiments 14- 16 have been interpreted as suggesting that fetal hypoxia, induced by nicotine or carbon monoxide in tobacco smoke, may be responsible. However, there is as yet no direct proof of these hypotheses. Our latest f1ndings serve to set straight the previous record and present a paradox. The A-scan ultrasound method is liable to misinterpretation on several counts, including bidirectional movement of the fetal chest with each breath. The Doppler method of identifying fetal breathing has been well validated in both sheep and man/· 17 · 1" and has the advantage over real-time B-scans that breath intervals can be measured objectively to an acceptable degree of accuracy. The new findings show that the rate of fetal breathing is enhanced after cigarette smoking, with no change in incidence. The difference from the previous f1ndings reported from this and other institutions is attributed to the difference in methods. The paradox arises from the fact that maternal cigarette smoking is associated with a reduction in fetal
J
Onober I, 19HO Obstet. Gvrwrol
movements (as perceived bv the mother) without a concomitant decrease in the incidence of breathing and with a decrease in mean breath interval. The formn observation needs verification bv an objective method. Let us for the sake of argument assume that it is true. At the present moment, the onlv mechanism bY which fetal body or limb movements are reduced is belieYed to be hypoxia. However, hypoxia is known to be associated with prolonged apnea in fetal lambs or monkeys, and this was not observed in our study. It is possible, then, that additional factors other than hypoxia mav inlluence fetal body movements. Indeed, no adequate studies have been executed to discriminate between hypoxemia, acidemia, and hypoglycemia as a cause of the disappearance of fetal movements prior to death in utero. Yet all three are known to be associated with prolonged apnea in fetal lambs. The simplest explanation for the paradox is multifactorial, that the decrease in mean breath inten·al is attributed to, for instance, hypercapnia, whereas the decrease in perceived movements is due to some other cause, at present unknown. Two points may be made, first that it is unlikely on present evidence that the fetus is subject, as a result of maternal smoking, to hypoxemia sufficient to reduce bodv and limb movements, since breathing is maintB.ined and the rate is increased. Second, it is unlikely that nicotine, which certainly crosses the placenta in man, 19 has a direct action on the carotid bodies. The latter are relativelv insensitive to pharmacologic stimuli in fetal lambs near term,Z 0 · ~· and maternal infusion of large closes does not appear to affect fetal breathing. We are grateful for the help of Professor A. C. Turnbull and the consultants who made their patients available, and to the patients themselves who gave so much of their time and interest to the study.
REFERENCES I. Boddy. K., and Robinson, J. S.: External method for detection of fetal breathing in utero, Lancet 2: 1231, 1971. 2. Wilds, P. L.: Observations of intrauterine fetal breathing movements, AM. J. OssTET. GYNECOL. 131:315, 1978. 3. Chapman, R. L. K., Dawes, G. S., Rurak, D. W., and Wilds, P. L.: Intermittent breathing before death in fetal lambs, AM. J. OssTET. GYNECOL. 125:73, 1978. 4. Gennser, G., Marsal, K., and Lindstrom, K.: Maternal smoking and fetal breathing movements, AM. J. 0BSTET. GYNECOL. 123:861, 1975. 5. Manning, F. A., and Feyerabend, C. I.: Cigarette smoking and fetai breathing movements, Br. j. Obstet. Gynaecoi. 83:262, 1976. 6. Manning, F., Walker, D., and Feyerabend, C.: The effect of nicotine on fetal breathing movements in conscious pregnant ewes, Obstet. Gynecol. 52:563, 1978.
7. Poore, E. R.: The relationship between fetal breathing movements as measured by thoracic pressure changes and the movement of the chest measured directly in vivo. Presented at the Fifth Conference on Fetal Breathing. Nijmegen, Holland, 1978. 8. Boyce, E. S., Dawes, G. S., Gough,]. D., and Poore, E. R.: Doppler ultrasound method for detecting human fetal breathing in utero, Br. Med. J. 2: 17, 1976. 9. Gough, J. D., and Poore, E. R.: A continuous Doppler ultrasound method for recording foetal breathing in utero, Ultrasound Med. Bioi. In press.
10. Pirani, B. B.: Smoking during ptegnancy, Obstet. Gynecol. Surv. 33:1, 1978. 11. Quigley, M. E., Sheehan, K. L., Wilkes, M. M., and Yen, S. S. C.: Elucidation of mechanisms for the deleterious effects of maternal smoking on fetal well-being. Pre-
\' olum e I :IH
Number :1
12.
~~~-
14.
15.
16.
sen ted at the Twenty-fifth Annual Meeting of the Society for Gvnecologic Investigation, Atlanta, Georgia, March 15-18. 1978. Cole. P. V .. Hawkins. L. V., and Roberts. D.: Smoking during pregnancy and its effect on the fetus. J. Obstet. Gynaecol. Br. Commonw. 79:782, 1972. Longo, L. D.: 1~hc biological effects of carbon monoxide on the pregnant woman, fetus, and newborn infant, AM. J. 0BSTET. GYNECOL. 129:69, 1977. Sumki, K., Horigucht, T .. Comas-Urrutia, A. C., Mueller-Heubach, E., .\forishima, H. 0., and Adamsons, K.: Pharmacologic effects of nicotine upon the fetus and mother in the rhesus monkev, AM. J. 0BSTET. GYNECOL. lll:l092. 1971. Resnik. R., Brink, G. W., and Wilkes, M. M.: Catecholamine-mediated reduction in uterine blood flow followmg nicotine infusion in the pregnant ewe. Presented at the Twentv-fifth Annual Meeting of the Society for Gynecologic Investigation. Atlanta, Georgia, March 15-18, 1978. Kirschbaum,J. H., Dilts, P. V .. Jr., and Brinkman, C. R.:
Maternal smoking effects on fetal breathing anrl movements
287
Some acute effects of smoking in sheq• and their fetuses. Obstet. Gvnecol. 35:527, 1970. 17. Gough, J.D., and Poore, E. R.: Directi<•nal Doppler measurements of fetal breath in!!. I. Ph\sinl tl.ond.) 272: 121', 197i.
"-·
18. Goodman, J D. S., and Mantell. C· ll