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The blood flow velocity waveform in the fetal internal carotid artery in the presence of hydrocephaly
Early Humon Development, 18 (1988) 95-99 Elsevier Scientific Publishers Ireland Ltd.
95
EHDO0917
The blood flow velocity waveform in the fetal internal carotid artery in the presence of hydrocephaly J.A.G.W. van den Wijngaard,
A. Reuss and J.W. Wladimiroff
Deportment of Obstetrics and Gynoecology, Erasmus University Rotterdom, The Netherlands Accepted for publication
15 February 1988
Summary The pulsatility index in the fetal internal carotid artery was studied in the presence of bilateral symmetrical hydrocephaly (n = 9) and unilateral hydrocephaly (n = 4). An elevated pulsatility index was demonstrated in five cases (38.5%) suggesting increased resistance to cerebral blood flow. In unilateral hydrocephaly a marked difference in pulsatility index was established between the normal and affected side. No relation could be established between the pulsatility index level and severity of ventriculomegaly or postnatal outcome. Both ventriculomegaly and increased intracranial pressure may play a role in the observed rise in pulsatility index. fetal cerebral blood flow; fetal internal carotid artery; pulsatility index; blood flow velocity waveform; hydrocephaly
Introduction Recently, a pulsed Doppler method for recording the flow velocity waveform in the fetal internal carotid artery in the human fetus was introduced [l 11. It was demonstrated that also in the human fetus a brain-sparing effect may occur in the presence of chronic fetal hypoxia [12]. The present study represents an investigation into the characteristics of the flow velocity waveform in the fetal internal carotid artery in the presence of congenital hydrocephaly. Subjects After parental informed consent, a total of 13 hydrocephalic fetuses was studied. Gestational age at the time of the study varied between 27 and 38 0378-3782/88/$03.50 0 1988 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland
96
weeks (mean: 32 weeks). The time interval between the Doppler ultrasound measurement and delivery varied between 2 days and 9 weeks (mean: 4 weeks). The diagnosis of hydrocephaly was based on a ventriculo-hemisphere ratio of the anterior and/or posterior horn of the lateral ventricle [2] above the upper confidence limit according to the normogram by van Egmond-Linden et al. [3]. ratio: Ventriculomegaly was graded as “mild” (raised ventriculo-hemisphere “moderate” (raised ventriculo< 2 x upper confidence limit) in three cases; hemisphere ratio: < 3 x upper confidence limit) in two cases and “severe” (raised ventriculo-hemisphere ratio: > 3 x upper confidence limit) in eight cases. In nine cases the ventriculo-hemisphere ratio was symmetrically raised. In the remaining four cases there was only a one-sided rise of the ventriculo-hemisphere ratio indicating unilateral ventriculomegaly. Isolated hydrocephaly was established in seven fetuses, hydrocephaly in combination with spina bifida in four fetuses and hydrocephaly in combination with multiple structural defects (polycystic kidneys, palatoschizis, encephalocele, skeletal deformations) in two fetuses. All pregnancies were tested for TORCHinfections, results were negative. Fetal birthweight was always above the tenth percentile for weight of gestation according to the Kloosterman Tables [8] corrected for maternal parity and fetal sex. Methods A Diasonics CV 400 mechanical sector scanner (carrier frequency: 3.5 MHz was used to locate the internal carotid artery at the level of the bifurcation into the middle and anterior cerebral artery as described previously by Wladimiroff et al. [l 11. After placing the sample gate of the Diasonics CV 400 pulsed Dop pler (carrier frequency: 3 MHz; depth of sample gate: variable; sample size: 4 mm) over the internal carotid artery, a maximum flow velocity waveform was recorded. In all cases measurements on either side of the midline were performed. From hard copies of the video-taped measurements the ,degree of pulsatility of the waveform was quantified by calculating the pulsatility index according to Gosling and Ring [4] using a microcomputer (Apple III). The pulsatility index merely reflects peripheral vascular resistance [9]. Each measurement included on average 16 cardiac cycles (min, 12; max, 23). All flow velocity waveform recordings were obtained during fetal apnea. Comparison was made with the normogram relating the pulsatility index in the internal carotid artery to gestational age as described by Wladimiroff et al. [12]. Results Figure 1 represents the pulsatility index values in the fetal internal carotid artery from nine fetuses with bilateral symmetrical hydrocephaly (nos. l-9) and from four fetuses with unilateral hydrocephaly (nos. 10-13) relative to the normogram by Wladimiroff et al. [12].
91
In the presence of bilateral symmetrical hydrocephaly, the difference in pulsatility index between the left and right internal carotid artery only varied between 0.02 and 0.11 (2-6070). For every bilateral symmetrical hydrocephalic fetus therefore, a mean pulsatility index was calculated for further use in the study, which ranged between 1.25 and 2.50. In the presence of unilateral hydrocephaly the pulsatility index on the affected side ranged between 1.55 and 2.58, whereas on the non-affected side the index varied between 1.OO and 1.95. The absolute difference in pulsatility index between the two sides ranged between 0.43 and 0.63. 2.6
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I 26-27
I 28-29
I 30-31
GESTATIONAL
I 32-33
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I 34-35
I 36-37
I 36 -39
(WEEKS)
Fig. 1. Pulsatility index values from 13 hydrocephaiic fetuses relative to the normogram for the internal carotid artery [12]. 0, indicates normal ventricular size on the non-affected side in the presence of unilateral hydrocephaly (nos. 10-13); 0, indicates mild ventricular dilatation; A, indicates moderate ventricular dilatation; H, indicates severe ventricular dilatation.
98
Considering all values together, the pulsatility index was situated between the mean and lower limit in two cases (15.5%), between the mean and upper limit in six cases (46Vo), and above the upper limit in the remaining five cases (38.5%). No relation could be established between the severity of the ventriculomegaly as expressed by the ventriculo-hemisphere ratio and pulsatility index level. Fetal outcome was poor: seven infants died within the first week following delivery (nos. 2-4, 9, 10, 12 and 13; Fig. l), five infants demonstrated a variable degree of mental and physical handicap (nos. 1, 5-8; Fig. I), only one infant (no. 11; Fig. 1) seems to be developing normally at the age of 1 year. There was no relation between pulsatility index and fetal outcome. Discussion The raised pulsatility index values in the fetal internal carotid artery in the presence of hydrocephaly suggest increased resistance to cerebral blood flow [7]. This rise in pulsatility index may be attributed to stretching, displacement, deformation or even compression of the fetal internal carotid arteries by the enlarged ventricles [ 131. A further rise in the pulsatility index value can be expected in the presence of increased intracranial pressure because of a concomitant rise in cerebrovascular resistance [l]. This may explain the wide distribution in pulsatility index around the upper limit of the normogram in the present study as well as the lack of correlation between the severity of the ventriculomegaly and pulsatility index. The impact of ventriculomegaly on the flow velocity waveform in the fetal internal carotid artery is demonstrated in the unilateral cases of hydrocephaly, in which the pulsatility index in this vessel on the affected side exhibited a 29-55% rise as compared with the pulsatility index in the non-affected hemisphere. The question arises as to how these data compare with the results obtained in newborns. A decrease in pulsatile flow and corresponding rise in resistance index was described in the anterior cerebral arteries in the presence of infantile hydrocephaly [6]. A significant correlation between the degree of ventricular enlargement and elevation of this index was established. It was suggested that ventriculomegaly is a more critical factor than elevated intracranial pressure in the pathogenesis of impaired flow. Furthermore, it was demonstrated that unilateral ventriculomegaly was accompanied by an asymmetrical elevation of resistance index in the sylvian arteries [lo]. Corrective intervention resulted in a significant improvement of cerebral blood flow. A recent study [5], however, failed to show any change in cerebral flow characteristics in the presence of hydrocephaly. The discrepancy between the previous two studies [6,10] and latter study [5] may be attributed to population differences, particularly with respect to the nature of the hydrocephaly (congenital/acquired) and level of intracranial pressure (normal/elevated). We found a clear indication of elevated pulsatility index in part of our
99
population of congenital hydrocephalic fetuses. However, the impossibility of in-utero intracranial pressure assessment does not allow many statements on the underlying reasons as to why there was not a more uniform vascular response to hydrocephaly. No correlation could be established between the level of the pulsatility index in the fetal internal carotid artery and severity or postnatal outcome of congenital hydrocephaly. The latter is not surprising taking into account the nature and severity of associated structural anomalies present in six out of 15 fetuses. References 1
6 7
8 9
10 11 12
13
Bada, H.S., Miller, J.E. and Menke, J.A. (1982): Intracranial pressure and cerebral arterial pulsatile flow measurements in neonatal intraventricular hemorrhage. J. Pediatr. 100, 2912%. Campbell, S. (1979): Diagnosis of the fetus and infant. In: Genetic disorders and the fetus, pp. 431-467. Editor: A. Milunsky. Plenum, New York. Egmond-Linden, A. van, Wladimiroff, J.W. and Niermeijer, M.F. (1986): Fetal hydrocephaly: diagnosis, prognosis and management. Ultrasound Med. Biol., 12, 939-944. Gosling, R.G. and King, D.H. (1975): Ultrasound angiology. In: Arteries and Veins, pp. 61-98. Editors: A.W. Marcus and L. Adamson. Churchill Livingstone, Edinburgh. Grant, E.G., White, E.M. and Schellinger, D. (1987): Cranial duplex sonography of the infant. Radiology, 163, 177-185. Hill, A. and Volpe, J.J. (1982): Decrease in pulsatile flow in the anterior cerebral arteries in infantile hydrocephalus. Pediatrics, 69, 4-7. Jonkman, E.J. and Mosmans, P.C.M. (1982): Basic anatomy, physiology and pathology of human cerebral circulation. In: Doppler ultrasound in the diagnosis of cerebrovascular disease, pp. l-28. Editors: R.S. Reneman and A.P.G. Hoeks. Research Studies Press, Chichester. Kloosterman, G. (1970): On intrauterine growth. Int. J. Gynaecol. Obstet., 8, 895-912. Noordam, M.J., Wladimiroff, J.W., Lotgering, F.K., Struijk, P.C. and Tonge, H.M. (1987): Fetal blood flow velocity waveforms in relation to changing peripheral vascular resistance. Early Hum. Dev., 15, 119-127. Santini, J.J., Saliba, E. and Arbeille, Ph. (1985): Mesure non invasive du flux sanguin cerebral chez le noveau-nt hydrocephale. Neurochirurgia, 3 1,7- 13. Wladimiroff, J.W., Tonge, H.M. and Stewart, P.A. (1986): Doppler ultrasound assessment of cerebral blood flow in the human fetus. Br. J. Obstet. Gynaecol., 93, 471-475. Wladimiroff, J.W., Wijngaard, J.A.G.W. van den, Degani, S., Noordam, M.J., Eyck, J. van and Tonge, H.M. (1987): Cerebral and umbilical arterial blood flow velocity waveforms in normal and growth-retarded pregnancies; a comparative study. Obstet. Gynecol., 69, 705-769. Wozniak, M., McLane, D.G. and Raimondi, A.J. (1975): Micro- and macrovascular changes as the direct cause of congenital murine hydrocephalus. J. Neurosurg., 43, 535-539.
95
EHDO0917
The blood flow velocity waveform in the fetal internal carotid artery in the presence of hydrocephaly J.A.G.W. van den Wijngaard,
A. Reuss and J.W. Wladimiroff
Deportment of Obstetrics and Gynoecology, Erasmus University Rotterdom, The Netherlands Accepted for publication
15 February 1988
Summary The pulsatility index in the fetal internal carotid artery was studied in the presence of bilateral symmetrical hydrocephaly (n = 9) and unilateral hydrocephaly (n = 4). An elevated pulsatility index was demonstrated in five cases (38.5%) suggesting increased resistance to cerebral blood flow. In unilateral hydrocephaly a marked difference in pulsatility index was established between the normal and affected side. No relation could be established between the pulsatility index level and severity of ventriculomegaly or postnatal outcome. Both ventriculomegaly and increased intracranial pressure may play a role in the observed rise in pulsatility index. fetal cerebral blood flow; fetal internal carotid artery; pulsatility index; blood flow velocity waveform; hydrocephaly
Introduction Recently, a pulsed Doppler method for recording the flow velocity waveform in the fetal internal carotid artery in the human fetus was introduced [l 11. It was demonstrated that also in the human fetus a brain-sparing effect may occur in the presence of chronic fetal hypoxia [12]. The present study represents an investigation into the characteristics of the flow velocity waveform in the fetal internal carotid artery in the presence of congenital hydrocephaly. Subjects After parental informed consent, a total of 13 hydrocephalic fetuses was studied. Gestational age at the time of the study varied between 27 and 38 0378-3782/88/$03.50 0 1988 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland
96
weeks (mean: 32 weeks). The time interval between the Doppler ultrasound measurement and delivery varied between 2 days and 9 weeks (mean: 4 weeks). The diagnosis of hydrocephaly was based on a ventriculo-hemisphere ratio of the anterior and/or posterior horn of the lateral ventricle [2] above the upper confidence limit according to the normogram by van Egmond-Linden et al. [3]. ratio: Ventriculomegaly was graded as “mild” (raised ventriculo-hemisphere “moderate” (raised ventriculo< 2 x upper confidence limit) in three cases; hemisphere ratio: < 3 x upper confidence limit) in two cases and “severe” (raised ventriculo-hemisphere ratio: > 3 x upper confidence limit) in eight cases. In nine cases the ventriculo-hemisphere ratio was symmetrically raised. In the remaining four cases there was only a one-sided rise of the ventriculo-hemisphere ratio indicating unilateral ventriculomegaly. Isolated hydrocephaly was established in seven fetuses, hydrocephaly in combination with spina bifida in four fetuses and hydrocephaly in combination with multiple structural defects (polycystic kidneys, palatoschizis, encephalocele, skeletal deformations) in two fetuses. All pregnancies were tested for TORCHinfections, results were negative. Fetal birthweight was always above the tenth percentile for weight of gestation according to the Kloosterman Tables [8] corrected for maternal parity and fetal sex. Methods A Diasonics CV 400 mechanical sector scanner (carrier frequency: 3.5 MHz was used to locate the internal carotid artery at the level of the bifurcation into the middle and anterior cerebral artery as described previously by Wladimiroff et al. [l 11. After placing the sample gate of the Diasonics CV 400 pulsed Dop pler (carrier frequency: 3 MHz; depth of sample gate: variable; sample size: 4 mm) over the internal carotid artery, a maximum flow velocity waveform was recorded. In all cases measurements on either side of the midline were performed. From hard copies of the video-taped measurements the ,degree of pulsatility of the waveform was quantified by calculating the pulsatility index according to Gosling and Ring [4] using a microcomputer (Apple III). The pulsatility index merely reflects peripheral vascular resistance [9]. Each measurement included on average 16 cardiac cycles (min, 12; max, 23). All flow velocity waveform recordings were obtained during fetal apnea. Comparison was made with the normogram relating the pulsatility index in the internal carotid artery to gestational age as described by Wladimiroff et al. [12]. Results Figure 1 represents the pulsatility index values in the fetal internal carotid artery from nine fetuses with bilateral symmetrical hydrocephaly (nos. l-9) and from four fetuses with unilateral hydrocephaly (nos. 10-13) relative to the normogram by Wladimiroff et al. [12].
91
In the presence of bilateral symmetrical hydrocephaly, the difference in pulsatility index between the left and right internal carotid artery only varied between 0.02 and 0.11 (2-6070). For every bilateral symmetrical hydrocephalic fetus therefore, a mean pulsatility index was calculated for further use in the study, which ranged between 1.25 and 2.50. In the presence of unilateral hydrocephaly the pulsatility index on the affected side ranged between 1.55 and 2.58, whereas on the non-affected side the index varied between 1.OO and 1.95. The absolute difference in pulsatility index between the two sides ranged between 0.43 and 0.63. 2.6
11 0
urn 2.1
=A ,
0
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,/
\
m
/- \
\,/
\
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\ ’ +2SQ
1.0 ,\ /
\ 0.8
’
/L
-2SD
1’
\ /’ \/
I 26-27
I 28-29
I 30-31
GESTATIONAL
I 32-33
AGE *
I 34-35
I 36-37
I 36 -39
(WEEKS)
Fig. 1. Pulsatility index values from 13 hydrocephaiic fetuses relative to the normogram for the internal carotid artery [12]. 0, indicates normal ventricular size on the non-affected side in the presence of unilateral hydrocephaly (nos. 10-13); 0, indicates mild ventricular dilatation; A, indicates moderate ventricular dilatation; H, indicates severe ventricular dilatation.
98
Considering all values together, the pulsatility index was situated between the mean and lower limit in two cases (15.5%), between the mean and upper limit in six cases (46Vo), and above the upper limit in the remaining five cases (38.5%). No relation could be established between the severity of the ventriculomegaly as expressed by the ventriculo-hemisphere ratio and pulsatility index level. Fetal outcome was poor: seven infants died within the first week following delivery (nos. 2-4, 9, 10, 12 and 13; Fig. l), five infants demonstrated a variable degree of mental and physical handicap (nos. 1, 5-8; Fig. I), only one infant (no. 11; Fig. 1) seems to be developing normally at the age of 1 year. There was no relation between pulsatility index and fetal outcome. Discussion The raised pulsatility index values in the fetal internal carotid artery in the presence of hydrocephaly suggest increased resistance to cerebral blood flow [7]. This rise in pulsatility index may be attributed to stretching, displacement, deformation or even compression of the fetal internal carotid arteries by the enlarged ventricles [ 131. A further rise in the pulsatility index value can be expected in the presence of increased intracranial pressure because of a concomitant rise in cerebrovascular resistance [l]. This may explain the wide distribution in pulsatility index around the upper limit of the normogram in the present study as well as the lack of correlation between the severity of the ventriculomegaly and pulsatility index. The impact of ventriculomegaly on the flow velocity waveform in the fetal internal carotid artery is demonstrated in the unilateral cases of hydrocephaly, in which the pulsatility index in this vessel on the affected side exhibited a 29-55% rise as compared with the pulsatility index in the non-affected hemisphere. The question arises as to how these data compare with the results obtained in newborns. A decrease in pulsatile flow and corresponding rise in resistance index was described in the anterior cerebral arteries in the presence of infantile hydrocephaly [6]. A significant correlation between the degree of ventricular enlargement and elevation of this index was established. It was suggested that ventriculomegaly is a more critical factor than elevated intracranial pressure in the pathogenesis of impaired flow. Furthermore, it was demonstrated that unilateral ventriculomegaly was accompanied by an asymmetrical elevation of resistance index in the sylvian arteries [lo]. Corrective intervention resulted in a significant improvement of cerebral blood flow. A recent study [5], however, failed to show any change in cerebral flow characteristics in the presence of hydrocephaly. The discrepancy between the previous two studies [6,10] and latter study [5] may be attributed to population differences, particularly with respect to the nature of the hydrocephaly (congenital/acquired) and level of intracranial pressure (normal/elevated). We found a clear indication of elevated pulsatility index in part of our
99
population of congenital hydrocephalic fetuses. However, the impossibility of in-utero intracranial pressure assessment does not allow many statements on the underlying reasons as to why there was not a more uniform vascular response to hydrocephaly. No correlation could be established between the level of the pulsatility index in the fetal internal carotid artery and severity or postnatal outcome of congenital hydrocephaly. The latter is not surprising taking into account the nature and severity of associated structural anomalies present in six out of 15 fetuses. References 1
6 7
8 9
10 11 12
13
Bada, H.S., Miller, J.E. and Menke, J.A. (1982): Intracranial pressure and cerebral arterial pulsatile flow measurements in neonatal intraventricular hemorrhage. J. Pediatr. 100, 2912%. Campbell, S. (1979): Diagnosis of the fetus and infant. In: Genetic disorders and the fetus, pp. 431-467. Editor: A. Milunsky. Plenum, New York. Egmond-Linden, A. van, Wladimiroff, J.W. and Niermeijer, M.F. (1986): Fetal hydrocephaly: diagnosis, prognosis and management. Ultrasound Med. Biol., 12, 939-944. Gosling, R.G. and King, D.H. (1975): Ultrasound angiology. In: Arteries and Veins, pp. 61-98. Editors: A.W. Marcus and L. Adamson. Churchill Livingstone, Edinburgh. Grant, E.G., White, E.M. and Schellinger, D. (1987): Cranial duplex sonography of the infant. Radiology, 163, 177-185. Hill, A. and Volpe, J.J. (1982): Decrease in pulsatile flow in the anterior cerebral arteries in infantile hydrocephalus. Pediatrics, 69, 4-7. Jonkman, E.J. and Mosmans, P.C.M. (1982): Basic anatomy, physiology and pathology of human cerebral circulation. In: Doppler ultrasound in the diagnosis of cerebrovascular disease, pp. l-28. Editors: R.S. Reneman and A.P.G. Hoeks. Research Studies Press, Chichester. Kloosterman, G. (1970): On intrauterine growth. Int. J. Gynaecol. Obstet., 8, 895-912. Noordam, M.J., Wladimiroff, J.W., Lotgering, F.K., Struijk, P.C. and Tonge, H.M. (1987): Fetal blood flow velocity waveforms in relation to changing peripheral vascular resistance. Early Hum. Dev., 15, 119-127. Santini, J.J., Saliba, E. and Arbeille, Ph. (1985): Mesure non invasive du flux sanguin cerebral chez le noveau-nt hydrocephale. Neurochirurgia, 3 1,7- 13. Wladimiroff, J.W., Tonge, H.M. and Stewart, P.A. (1986): Doppler ultrasound assessment of cerebral blood flow in the human fetus. Br. J. Obstet. Gynaecol., 93, 471-475. Wladimiroff, J.W., Wijngaard, J.A.G.W. van den, Degani, S., Noordam, M.J., Eyck, J. van and Tonge, H.M. (1987): Cerebral and umbilical arterial blood flow velocity waveforms in normal and growth-retarded pregnancies; a comparative study. Obstet. Gynecol., 69, 705-769. Wozniak, M., McLane, D.G. and Raimondi, A.J. (1975): Micro- and macrovascular changes as the direct cause of congenital murine hydrocephalus. J. Neurosurg., 43, 535-539.