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Midtrimester fetal heart rate variability and maternal hemodynamics in association with smoking
Midtrimester fetal heart rate variability and maternal hemodynamics in association with smoking M. Forss, Ph.D., P. Lehtovirta, M.D., I. Rauramo, M.D., and V. Kariniemi, M.D. HeL5inki, Finland Maternal heart rate (MHA), blood pressure (BP), the differential index (DI) describing the short-term component of fetal heart rate (FHA) variability, and the interval index (II) describing the long-term component were measured in eight subjects in the midtrimester before, during, and after the mothers smoked a standard cigarette. The analyses of FHA variability were performed by an "on-line" method with an abdominal fetal electrocardiogram used as a triggering signal and with a sample time of 1 minute. An increase of MHA, FHA, and BP with a concomitant decrease of II was observed. Unlike our findings regarding the third trimester, no significant change of Dl was observed. A correlation analysis revealed fetomaternal hemodynamic relationships different from those in the third trimester: There was a negative correlation between Dl and FHA (p < 0.01) and between Dl and MHA (p < 0.01). There was a positive correlation between FHA and MHA (p < 0.001). Unlike our findings regarding the third trimester, no correlation was found between Dl and BP or between II and MHA. We suggest that the midtrimester fetus shows the narcotic effect (decrease of II) of one cigarette, as does the term fetus, but fails to show the hypoxic effect (decrease of Dl), which has been observed in the term fetus. (AM. J. Ossrer. GYNECOL. 146:693, 1983.)
The acute effects of smoking during normal term pregnancy have been investigated thoroughly. Smoking one standard cigarette has been shown to elevate human maternal heart rate (MHR) and blood pressure (BP) 1• 2 and to decrease intervillous blood flow, 1 fetal heart rate (FHR) variability,:~ and fetal breathing movements!· s The opinions regarding the effects of smoking on basal FHR are somewhat contradictory. 1• 3 It has been shown in animal experiments that nicotine 6 and carbon monoxide 7 produce fetal hypoxia and that nicotine is responsible for decreased fetal breathing movementsa We have shown previously that smoking one cigarette provides an interesting model for investigating fetOmaternal hemodynamic interrelationshipsY In term fetuses the short-term variability of FHR (DI differential index) had a significant correlation with maternal BP, and the long-term variability of FHR (II = interval index) had a significant correlation with MHR. The present study was undertaken to find out whether the effects of smoking on midtrimester fetuses are similar to those on term fetuses and whether the aforementioned correlations exist as early as in the second trimester.
Material and methods Eight healthy women in their twenty-second to twenty-sixth weeks of pregnancy gave informed conFrom the Departments I and II of Obstetrics and Gynecology, Helsinki lJ ni:oersity Central Hospital. Received for publication May 28, 1982. Accepted February 2, 1983. Reprint requests: M. Forss, Ph.D., Department I and II of Obstetrics and Gynecology, Hel1inki University Central Hospital, Haartmaninkatu 2, SF-00290 Hel1inki 29, Finland.
sent and participated in the study. They all had smoking experience, and three of them were regular smokers (range, five to 20 cigarettes per day). The mothers were lying in a 15-degree left lateral retumbent position during the experiments. MHR was recorded bv maternal electrocardiogram and BP was recorded by sphygmomanometer at 2- to 5-minute intervals. Analyses of FHR variability were performed by a previously described rnethod 10 at !-minute intervals from an abdominal fetal electrocardiogram (aFECG) 10 minutes before, during, and 25 minutes after smoking. Before the onset of the actual test, a 5-minute analysis of FHR variability was performed to verify that the variability was normal. The mothers smoked one standard cigarette, inhaling for 5 minutes. The basal FHR was estimated visually from periods of the aFECG. coincident with measurements of MHR and BP. Mean indices of variability, basal FHR, MHR, and BP before, during, and after smoking were compared with Student's t test for statistical calculations. The correlations were calculated by least squares.
Results A transient elevation of MHR and systolic and diastolic BP occurred during smoking, and all values returned to the presmoking level in 10 minmes. A transient elevation of basal FHR and a decrease of II were observed 5 to 10 minutes after smoking, and both returned to the presmoking level in 15 minutes. D I did not change significantly during the experiment (Fig. l ). A correlation analysis (Table I) revealed negative exponential correlations between FHR and Dl (p < 0.01, Fig. 2.A) and between MHR and DI (p < O.Ql, Fig. 2,
693
694 Forss et al.
BP/HR
July 15, l!Jii:l Am. J. Obstet. Gynecol.
• • I I
150
0!
I
I
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I
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--1---1 I I
4
3
2
100
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0 FETAL HEART RATE
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4 2
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0 -10 -5
130
80
100
120
60
MATERNAL HEART RATE
SMOKING 5 10 TIME
15
20
25
MATERNAL HEART RATE
Fig. ~. Relations between maternal and fetal hemodynamic parameters in eight midtrimester pregnancies in association with maternal smoking. A, DI and basal FHR (y = 42.276 e· 0 ·01 "X, p < 0.01, r = 0.408, n = 61); B, DI and MHR (y = 5.597 e· 0 ·008X, p < 0.01, r -0.372, n 61 ); C, basal FHR and MHR (y = 85.796 x0 · 126 , p < 0.001, r = 0.429, n = 61).
Fig. 1. Effects of smoking on basal FHR, DI, II, systolic (S) and diastolic(D) maternal BP, and MHR in eight midtrimester pregnancies. Means were compared with the first values by paired t test. Asterisk: p < 0.01. Double asterisk: p < 0.001.
Table I. The correlation matrix of maternal and fetal hemodynamic parameters in association with smoking BP
Systolic BP Systolic Diastolic FHR MHR
Diastolic
FHR
MHR
II
Dl
0.816
0.156 0.256
0.224 0.271 0.429* I
0.102 0.041 -0.100 -0.010
0.250 0.158 -0.408t -0.372t 0.512
1
II
DI
I
1
1
*p < 0.001. tp < 0.01.
B). A pos1t1ve power correlation was found between MHR and FHR (p < 0.001, Fig. 2, C).
Comment The main finding of this study is the observation that responses of the midtrimester fetus to smoking are dif-
ferent from those of the third-trimester fetus. We have shown previously that both II and DI of the thirdtrimester fetus fall after the mother has smoked one cigarette. 3 We have suggested that these two indices describe two different reactions of the fetus: II describes the direct narcotic effect and DI, a hypoxic one
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mediated by decreased placental blood flow. The fall of II in the present study suggests that the midtrimester fetus shows the narcotic effect of smoking as does the third-trimester fetus. The lack of change in Dl, on the other hand, suggests that the midtrimester fetus does not suffer from hypoxia. Whether this is based on the lack of changes in uteroplacental blood flow or on fetal responses is being investigated. Another interesting finding of the present study is the fetomaternal hemodynamic relationships in the second trimester, which are also different from those in the third trimester. We have shown previously that in the third trimester II has a negative correlation with MHR and DI has a negative correlation with BP. 9 These significant correlations supported our concept that DI is correlated with placental blood flow and II is a reflection of the narcotic effect. Since DI did not change and had no correlation with BP in the present study, we presume that either there occurred no change of intervillous blood flow or the midtrimester fetus did not respond as measured by the DI. Instead, Dl had a methodologic correlation with basal FHR, as has also been reported previously. 11 The correlation of DI with MHR is explained by a strong correlation between MHR and FHR. The lack of correlation between II and MHR, although both change the same way as in the third trimester, is a curious phenomenon for which we have no explanation at present. REFERENCES I. Lehtovirta, P .. and Forss, M.: The acute effect of smoking on intervillous blood flow of the placenta, Br. ]. Obstet. Gynaecol. 85:i29, !9i8.
Hemodynamic effects ot smoking
695
2. Quigley, M.P., Sheehan, K. L., Wilkes, M. M., and Yen, S. S. C.: Effects of maternal smoking on circulating catecholamine levels and fetal heart rates, .\M . .J. OnsTET. GYNECOL. 73:808, 1979. 3. Lehtovirta, P., Forss, M., Kariniemi, V .. and Rauramo, 1.: Acute effects of smoking on fetal heart-rate variability, Br.]. Obstet. Gynaecol. 90:3, 19!:\:{. 4. Gennser, G., Mariial, K .. and Branrmark. B.: Maternal smoking and fetal breathing movement, AM.]. 0BSTET. GYNECOL. 1%3:861. 19i5. 5. Manning, F., and Feyerabend, C.: Cigarette smoking and fetal breathing movements, Br. J Obstet. Gvnaecol. 83: 262, 1976. 6. Suzuki, K., Horiguchi, T., Comas-l'rrutia, A.. C., MuellerHeubach, E., Morishima, H. 0., and Adamsons, K.: Placental transfer and distribution of nicotine in the pregnant rhesus monkey, AM.]. 0BSTET. Gna:cm .. ll9:25:l, 19i l. i. Socol, M. L, Manning, F. A., Murata, Y, and Druziu, M. L.: Maternal smoking causes fetal hypoxia: Experimental evidence, AM. j. 0BSTET. GYNECO!.. 142:214, 1982. 8. Manning, F., Walker, D., and Feyerabend. C.: The effect of nicotine on fetal breathing movements in conscious pregnant ewes, Obstet. Gynecol. 52:563, 1\liH. 9. Kariniemi, V., Forss, M., Lehtovirta, P., and Rauramo. 1.: Significant correlation between maternal hemodynamics and fetal heart rate variability, AM. J. Os~TRT. GYNF.COL. 144:43, 1982. 10. Kariniemi, \/., Katila, T., Laine, H., and Ammiilii, 1'.: On-line quantification of fetal heart rate variability, J. Perinat. Med. 9:248, 1980. II. van Geijn, H. P.,Jongsma, H. W., De Haan . .J., and Eskes, T. K. A. B.: Analysis of heart rate and beat-to-beat variability: Interval difference index, AM. J OnsTET. GYNt:coL. 138:246, 19RO.
The acute effects of smoking during normal term pregnancy have been investigated thoroughly. Smoking one standard cigarette has been shown to elevate human maternal heart rate (MHR) and blood pressure (BP) 1• 2 and to decrease intervillous blood flow, 1 fetal heart rate (FHR) variability,:~ and fetal breathing movements!· s The opinions regarding the effects of smoking on basal FHR are somewhat contradictory. 1• 3 It has been shown in animal experiments that nicotine 6 and carbon monoxide 7 produce fetal hypoxia and that nicotine is responsible for decreased fetal breathing movementsa We have shown previously that smoking one cigarette provides an interesting model for investigating fetOmaternal hemodynamic interrelationshipsY In term fetuses the short-term variability of FHR (DI differential index) had a significant correlation with maternal BP, and the long-term variability of FHR (II = interval index) had a significant correlation with MHR. The present study was undertaken to find out whether the effects of smoking on midtrimester fetuses are similar to those on term fetuses and whether the aforementioned correlations exist as early as in the second trimester.
Material and methods Eight healthy women in their twenty-second to twenty-sixth weeks of pregnancy gave informed conFrom the Departments I and II of Obstetrics and Gynecology, Helsinki lJ ni:oersity Central Hospital. Received for publication May 28, 1982. Accepted February 2, 1983. Reprint requests: M. Forss, Ph.D., Department I and II of Obstetrics and Gynecology, Hel1inki University Central Hospital, Haartmaninkatu 2, SF-00290 Hel1inki 29, Finland.
sent and participated in the study. They all had smoking experience, and three of them were regular smokers (range, five to 20 cigarettes per day). The mothers were lying in a 15-degree left lateral retumbent position during the experiments. MHR was recorded bv maternal electrocardiogram and BP was recorded by sphygmomanometer at 2- to 5-minute intervals. Analyses of FHR variability were performed by a previously described rnethod 10 at !-minute intervals from an abdominal fetal electrocardiogram (aFECG) 10 minutes before, during, and 25 minutes after smoking. Before the onset of the actual test, a 5-minute analysis of FHR variability was performed to verify that the variability was normal. The mothers smoked one standard cigarette, inhaling for 5 minutes. The basal FHR was estimated visually from periods of the aFECG. coincident with measurements of MHR and BP. Mean indices of variability, basal FHR, MHR, and BP before, during, and after smoking were compared with Student's t test for statistical calculations. The correlations were calculated by least squares.
Results A transient elevation of MHR and systolic and diastolic BP occurred during smoking, and all values returned to the presmoking level in 10 minmes. A transient elevation of basal FHR and a decrease of II were observed 5 to 10 minutes after smoking, and both returned to the presmoking level in 15 minutes. D I did not change significantly during the experiment (Fig. l ). A correlation analysis (Table I) revealed negative exponential correlations between FHR and Dl (p < 0.01, Fig. 2.A) and between MHR and DI (p < O.Ql, Fig. 2,
693
694 Forss et al.
BP/HR
July 15, l!Jii:l Am. J. Obstet. Gynecol.
• • I I
150
0!
I
I
-r--L--1.. I
I
1
I
5
I
--1---1 I I
4
3
2
100
0
0 FETAL HEART RATE
50
or
FHR
5
!60
Oil I I 4
5
~--·
3
OJ
I
!50
·:·:. ...<-~ .
4 2
3
140
2
0
0
60
••
0 -10 -5
130
80
100
120
60
MATERNAL HEART RATE
SMOKING 5 10 TIME
15
20
25
MATERNAL HEART RATE
Fig. ~. Relations between maternal and fetal hemodynamic parameters in eight midtrimester pregnancies in association with maternal smoking. A, DI and basal FHR (y = 42.276 e· 0 ·01 "X, p < 0.01, r = 0.408, n = 61); B, DI and MHR (y = 5.597 e· 0 ·008X, p < 0.01, r -0.372, n 61 ); C, basal FHR and MHR (y = 85.796 x0 · 126 , p < 0.001, r = 0.429, n = 61).
Fig. 1. Effects of smoking on basal FHR, DI, II, systolic (S) and diastolic(D) maternal BP, and MHR in eight midtrimester pregnancies. Means were compared with the first values by paired t test. Asterisk: p < 0.01. Double asterisk: p < 0.001.
Table I. The correlation matrix of maternal and fetal hemodynamic parameters in association with smoking BP
Systolic BP Systolic Diastolic FHR MHR
Diastolic
FHR
MHR
II
Dl
0.816
0.156 0.256
0.224 0.271 0.429* I
0.102 0.041 -0.100 -0.010
0.250 0.158 -0.408t -0.372t 0.512
1
II
DI
I
1
1
*p < 0.001. tp < 0.01.
B). A pos1t1ve power correlation was found between MHR and FHR (p < 0.001, Fig. 2, C).
Comment The main finding of this study is the observation that responses of the midtrimester fetus to smoking are dif-
ferent from those of the third-trimester fetus. We have shown previously that both II and DI of the thirdtrimester fetus fall after the mother has smoked one cigarette. 3 We have suggested that these two indices describe two different reactions of the fetus: II describes the direct narcotic effect and DI, a hypoxic one
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mediated by decreased placental blood flow. The fall of II in the present study suggests that the midtrimester fetus shows the narcotic effect of smoking as does the third-trimester fetus. The lack of change in Dl, on the other hand, suggests that the midtrimester fetus does not suffer from hypoxia. Whether this is based on the lack of changes in uteroplacental blood flow or on fetal responses is being investigated. Another interesting finding of the present study is the fetomaternal hemodynamic relationships in the second trimester, which are also different from those in the third trimester. We have shown previously that in the third trimester II has a negative correlation with MHR and DI has a negative correlation with BP. 9 These significant correlations supported our concept that DI is correlated with placental blood flow and II is a reflection of the narcotic effect. Since DI did not change and had no correlation with BP in the present study, we presume that either there occurred no change of intervillous blood flow or the midtrimester fetus did not respond as measured by the DI. Instead, Dl had a methodologic correlation with basal FHR, as has also been reported previously. 11 The correlation of DI with MHR is explained by a strong correlation between MHR and FHR. The lack of correlation between II and MHR, although both change the same way as in the third trimester, is a curious phenomenon for which we have no explanation at present. REFERENCES I. Lehtovirta, P .. and Forss, M.: The acute effect of smoking on intervillous blood flow of the placenta, Br. ]. Obstet. Gynaecol. 85:i29, !9i8.
Hemodynamic effects ot smoking
695
2. Quigley, M.P., Sheehan, K. L., Wilkes, M. M., and Yen, S. S. C.: Effects of maternal smoking on circulating catecholamine levels and fetal heart rates, .\M . .J. OnsTET. GYNECOL. 73:808, 1979. 3. Lehtovirta, P., Forss, M., Kariniemi, V .. and Rauramo, 1.: Acute effects of smoking on fetal heart-rate variability, Br.]. Obstet. Gynaecol. 90:3, 19!:\:{. 4. Gennser, G., Mariial, K .. and Branrmark. B.: Maternal smoking and fetal breathing movement, AM.]. 0BSTET. GYNECOL. 1%3:861. 19i5. 5. Manning, F., and Feyerabend, C.: Cigarette smoking and fetal breathing movements, Br. J Obstet. Gvnaecol. 83: 262, 1976. 6. Suzuki, K., Horiguchi, T., Comas-l'rrutia, A.. C., MuellerHeubach, E., Morishima, H. 0., and Adamsons, K.: Placental transfer and distribution of nicotine in the pregnant rhesus monkey, AM.]. 0BSTET. Gna:cm .. ll9:25:l, 19i l. i. Socol, M. L, Manning, F. A., Murata, Y, and Druziu, M. L.: Maternal smoking causes fetal hypoxia: Experimental evidence, AM. j. 0BSTET. GYNECO!.. 142:214, 1982. 8. Manning, F., Walker, D., and Feyerabend. C.: The effect of nicotine on fetal breathing movements in conscious pregnant ewes, Obstet. Gynecol. 52:563, 1\liH. 9. Kariniemi, V., Forss, M., Lehtovirta, P., and Rauramo. 1.: Significant correlation between maternal hemodynamics and fetal heart rate variability, AM. J. Os~TRT. GYNF.COL. 144:43, 1982. 10. Kariniemi, \/., Katila, T., Laine, H., and Ammiilii, 1'.: On-line quantification of fetal heart rate variability, J. Perinat. Med. 9:248, 1980. II. van Geijn, H. P.,Jongsma, H. W., De Haan . .J., and Eskes, T. K. A. B.: Analysis of heart rate and beat-to-beat variability: Interval difference index, AM. J OnsTET. GYNt:coL. 138:246, 19RO.