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ORIGINAL RESEARCH |
From the Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas, and the Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, University Of Utah, Salt Lake City, Utah.
Address reprint requests to: Shlomit Riskin-Mashiah, MD, 18 Freud Street, Haifa, 34753, Israel; e-mail: asriskin{at}newmail.net.
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ABSTRACT |
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METHODS: Transcranial Doppler ultrasound was used to measure peak, end-diastolic, and mean velocities in the middle cerebral arteries of 34 normotensive and 17 mild chronic hypertensive women in the third trimester of pregnancy. Measurements were performed in the left lateral position at baseline, during 5% CO2 inhalation, and during an isometric handgrip test. Mean pulsatility index, resistance index, and cerebral perfusion pressure at each time were compared using 2-way repeated measures analysis of variance. Using an alpha error of 5%, the statistical power to identify differences in middle cerebral artery indices in response to the two maneuvers was at least 90% and 50% in comparison between the two groups. Significance was P < .05.
RESULTS: Pregnant women with mild chronic hypertension had higher baseline mean blood pressure but similar pulsatility index (0.73 versus 0.75), resistance index (0.50 versus 0.50), and cerebral perfusion pressure (59.9 versus 61.8 mm Hg) compared with normotensive pregnant women. Both maneuvers caused a significant reduction in pulsatility index and resistance index and higher cerebral perfusion pressure. No significant differences were noted in the response to either 5% CO2 inhalation or isometric handgrip test between the two groups.
CONCLUSION: Pregnant women with mild chronic hypertension show normal cerebral vasomotor reactivity to CO2 breathing and isometric handgrip. This suggests that the abnormal cerebrovascular autoregulation in preeclampsia is not directly linked to the elevated blood pressure but rather is determined by a separate pathophysiologic pathway.
LEVEL OF EVIDENCE: II-2
Using these tests we have previously shown that preeclamptic women demonstrate cerebral hyperperfusion and reduced cerebrovascular reactivity.5 We also demonstrated that normotensive pregnant women who later developed preeclampsia experience cerebral hemodynamic changes that predate the development of overt preeclampsia symptoms.6
Women with chronic hypertension are at increased risk to develop obstetric complications during pregnancy, including superimposed preeclampsia, eclampsia, and intrauterine growth retardation. There are only scant and conflicting data in the literature regarding cerebral hemodynamics in pregnant women with chronic hypertension.7,8 Our objective was to evaluate and compare the cerebrovascular hemodynamics and reactivity in normotensive and mild chronic hypertensive pregnant women without preeclampsia using both the 5% CO2 stimulation test and the isometric handgrip test.
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MATERIALS AND METHODS |
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Between September 1997 and June 2000, 17 women with mild chronic hypertensive had a transcranial Doppler study during the third trimester. Women were considered as having mild chronic hypertension if they had a known history of hypertension before pregnancy with blood pressure of 140/90 or higher9 who were on no medication or on only low doses of alpha-methyldopa. The control group consisted of 34 normotensive pregnant women who had a transcranial Doppler study at similar gestational age and parity. All women in both groups had an uneventful pregnancy and delivery; specifically, they delivered at term, and none developed preeclampsia (defined as proteinuria greater than or equal to 300 mg/24 hours and worsening blood pressure9). Five pregnant women with chronic hypertension who developed superimposed preeclampsia after the transcranial Doppler scan were excluded from this study.
A transcranial Doppler ultrasound (Medasonics Cerebrovascular Diagnostic System, Fremont, CA) with a pulsed, range-gated, 2-MHz transducer was used for middle cerebral artery velocity measurements. The M1 portion of the middle cerebral artery (initial 2-cm segment) was insonated via the transtemporal approach, and the depth of interrogation was adjusted to obtain an optimal velocity signal. The middle cerebral artery velocity waveform was recorded on both sides of the head if possible, and the average value was then used in the analysis. A minimum of 6 waveforms was averaged for each of the following parameters: systolic, end diastolic, and mean velocities. The cerebral velocity data were recorded directly from the Medasonics system.
Heart rate and the systolic, diastolic, and mean arterial systemic blood pressure (BP) were measured automatically (Dinamap, Criticon Inc, Tampa, FL). Peripheral oxygen saturation and the expired end-tidal partial pressure of CO2 were also recorded (Nellcor N300; Nellcor Inc, Pleasanton, CA).
For the isometric handgrip test, we used a bulb dynamometer (Fabrication Enterprises Inc, Irvington, NY). The women were instructed to hold the ball in their dominant hand and to exert maximal compressive force on 3 separate occasions. Each squeezing period was followed by a rest period of 1 minute. The average value of the 3 was calculated as the maximal voluntary contraction.
According to the study protocol, all pregnant women were first placed in the left lateral recumbent position and rested for 10 minutes in a quiet room before being studied. At that time, baseline measurements of systemic BP, heart rate, O2 saturation, end-tidal CO2, and bilateral middle cerebral artery velocities were recorded. The patients were then asked to breathe air with a 5% CO2 concentration (Ready mixed gas supplied in a cylinder, Tri-Gas Industrial Gases Inc, Irving, TX) through a nonrebreathing face mask. Maternal oxygen saturation and end tidal CO2 concentrations were continuously measured during this phase of the study. The same set of measurements was repeated once a new steady state of end-tidal CO2 was achieved (usually within 1–2 minutes). Carbon dioxide inhalation was then stopped, and the patient was allowed to rest. She was monitored until her end-tidal CO2 returned to baseline.
After 5 minutes of recovery, the patients were asked to maintain handgrip contraction at 30% of the predetermined maximal voluntary contraction force. Handgrip was maintained for up to a maximum of 2 minutes and the measurement set was repeated.
Clinical information from the patients’ prenatal and delivery records, along with the BP, heart rate, cerebral blood flow velocity, and other test data were entered into a computerized database (Access database, Microsoft, Seattle, WA).
The derived middle cerebral artery parameters were calculated as follows:
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Aaslid et al10 have previously validated a noninvasive method for cerebral perfusion pressure measurement using transcranial Doppler ultrasound of the middle cerebral artery. We used the above modification of this formula, which has been previously reported and validated in pregnant women.11
Cerebrovascular reactivity in the middle cerebral artery distribution was assessed by the effect of the challenge maneuvers (CO2 and handgrip) on each of the calculated parameters. Based on the data in the literature, the inter- and intraobserver variation for pulsatility index and resistance index are about 1%12,13and less than 10% for the cerebral perfusion pressure.8
All data were tested for normal distribution (Kolmogorov-Smirnov test, SigmaStat 2.03, Chicago, IL). Appropriate parametric (Student t test) and nonparametric (Mann-Whitney Rank test) tests for unpaired data were than used in the analysis. The 2 groups were compared at baseline and in response to the 2 maneuvers using 2-way repeated measures analysis of variance with multiple comparison procedures by Tukey test (SigmaStat). A post hoc power analysis was performed to evaluate the primary measures of the study, the middle cerebral artery indices: pulsatility index, resistance index, and cerebral perfusion pressure. Using an alpha error of 5%, the statistical power to identify differences in response to the 2 maneuvers was at least 90% and 50% in comparison between the two groups. Data are reported as mean ± SE or median and range, and statistical significance was set at P < .05.
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RESULTS |
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). Gestational age at delivery and neonatal birth weight were similar in both groups (Table 1).
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Isometric handgrip force was similar in both groups (P = .3), and there were no significant changes in mean blood pressure, heart rate, or O2 saturation in either group during the test. In both groups, the isometric handgrip test caused reduction in middle cerebral artery pulsatility and resistance indices and increase in cerebral perfusion pressure (Table 2).
Using baseline values as covariates, no significant differences were noted in the response to either hypercapnia or isometric handgrip test between normotensive and chronic hypertensive pregnant women (Table 2).
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DISCUSSION |
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However, Belfort et al8 found that most of the pregnant women with chronic hypertension have cerebral perfusion pressure within normal limits, whereas pregnant women with superimposed preeclampsia have significantly higher cerebral perfusion pressure.
This study shows that pregnant women with uncomplicated mild chronic hypertension have normal baseline cerebral perfusion pressure, pulsatility index and resistance index, and normal vasodilatory response to both provocative tests. Furthermore, we have previously shown6 that women with preeclampsia behave differently with markedly elevated cerebral perfusion pressure and reduced vasodilatory response to provocative tests.
Some of the discrepancies found between the different studies are probably related to differences in severity and chronicity of the hypertension and the treatment that those women got. Both Sugimori14 and Maeda et al15 have found that chronic hypertension affects the cerebral vasculature even before frank cerebral injury occurs. However, these changes depend on the severity14 and chronicity15 of the disease.
The women included in this study had only mild chronic hypertension, and the rest5 were treated with only low doses of alpha-methyldopa to control their blood pressure. The fact that some of the patients were taking antihypertensive medication is a potential confounding influence in this study. Alpha-methyldopa is not thought to have any significant effect on cerebral perfusion pressure but little is known on the effect of this drug on the cerebrovascular autoregulation. Serra-Serra et al16 have found that it had only modest effect on middle cerebral artery mean velocity. Based on the present data, it is not possible to comment on cerebrovascular autoregulation in pregnant women with severe uncontrolled chronic hypertension.
The pulsatility index and resistance index were used for assessment of arterial resistance because absolute velocity measurements rely on an accurate measurement of the angle of incidence of the Doppler ultrasound beam. In studies where multiple measurements are required, it is impossible to ensure that the identical angle of incidence will be used at all measurement times. The resistance index and pulsatility index are ratios and as such are reproducible and are independent of the angle of incidence. This allows accurate repeat measurements that are comparable and not affected by measurement bias. The cerebral perfusion pressure measurement has the same advantage.
In summary, our study demonstrates that pregnant women with mild chronic hypertension without superimposed preeclampsia have normal cerebrovascular indices and normal vasomotor response to hypercapnia and isometric handgrip. The abnormality in cerebrovascular autoregulation that we have previously described in preeclamptic women appears to be specific to preeclampsia and is not related to hypertension per se.
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Footnotes |
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doi: 10.1097/01.AOG.0000110250.48579.21
Received September 4, 2003. Received in revised form October 25, 2003. Accepted November 6, 2003.
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REFERENCES |
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2. Hartl WH, Furst H. Application of transcranial Doppler sonography to evaluate cerebral hemodynamics in carotid artery disease. Comparative analysis of different hemodynamic variables. Stroke 1995;26:2293–7.
3. Linkis P, Jorgensen LG, Olesen HL, Madsen PL, Lassen NA, Secher NH. Dynamic exercise enhances regional cerebral artery mean flow velocity. J Appl Physiol 1995;78: 12–6.
4. Imms FJ, Russo F, Iyawe VI, Segal MB. Cerebral blood flow velocity during and after sustained isometric skeletal muscle contractions in man. Clin Sci 1998;94:353–8.[Medline]
5. Riskin-Mashiah S, Belfort MA, Saade GR, Herd JA. Transcranial Doppler measurement of cerebral velocity indices as a predictor of preeclampsia. Am J Obstet Gynecol 2002;187:1667–72.[Medline]
6. Riskin-Mashiah S, Belfort MA, Saade GR, Herd JA. Cerebrovascular Reactivity is Different in Normal Pregnancy and Preeclampsia. Obstet Gynecol 2001;98:827–32.
7. Williams KP, Wilson S. Variation in cerebral perfusion pressure with different hypertensive states in pregnancy. Am J Obstet Gynecol 1998;179:1200–3.[Medline]
8. Belfort MA, Tooke-Miller C, Allen JC Jr, Varner MA, Grunewald C, Nisell H, et al. Pregnant women with chronic hypertension and superimposed preeclampsia have higher cerebral perfusion pressure. BJOG 2001;108: 1141–7.[Medline]
9. Report of the National High Blood Pressure Education Program Working Group Report on High Blood Pressure in Pregnancy. Am J Obstet Gynecol 2000;183:S1–22.
10. Aaslid R, Lundar T, Lindegaard KF, Nornes H, Estimation of cerebral perfusion pressure from arterial blood pressure and transcranial Doppler recording. In: Miller JD, Teasdale GM, Rowan JO, editors. Intracranial pressure VI. Berlin: Heidelberg, Springer-Verlag; 1986. p. 226–9.
11. Belfort MA, Tooke-Miller C, Varner M, Saade G, Grunewald C, Nisell H, et al. Evaluation of a noninvasive transcranial Doppler and blood pressure-based method for the assessment of cerebral perfusion pressure in pregnant women. Hypertens Pregnancy 2000;19:331–40.[Medline]
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14. Sugimori H, Ibayashi S, Irie K, Ooboshi H, Nagao T, Fujii K, et al. Cerebral hemodynamics in hypertensive patients compared with normotensive volunteers. A transcranial Doppler study. Stroke 1994;25:1384–9.[Abstract]
15. Maeda H, Matsumoto M, Handa N, Hougaku H, Ogawa S, Itoh T, et al. Reactivity of cerebral blood flow to carbon dioxide in hypertensive patients: evaluation by the transcranial Doppler method [see comments]. J Hypertens 1994;12:191–7.[Medline]
16. Serra-Serra V, Kyle PM, Chandran R, Redman CW. The effect of nifedipine and methyldopa on maternal cerebral circulation. Br J Obstet Gynaecol 1997;104:532–7.[Medline]
This article has been cited by other articles:
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  S. Riskin-Mashiah and M. A. Belfort Preeclampsia is Associated With Global Cerebral Hemodynamic Changes Reproductive Sciences, May 1, 2005; 12(4): 253 - 256. [Abstract] [PDF]
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S. Riskin-Mashiah and M. A. Belfort Cerebrovascular Hemodynamics in Chronic Hypertensive Pregnant Women Who Later Develop Superimposed Preeclampsia Reproductive Sciences, January 1, 2005; 12(1): 28 - 32. [Abstract] [PDF]
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