Published online February 5, 2007
PEDIATRICS Vol. 119 No. 3 March 2007, pp. e610-e615 (doi:10.1542/peds.2006-2110)
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ARTICLE

Early Childhood Gender Differences in Anterior and Posterior Cerebral Blood Flow Velocity and Autoregulation

Nuj Tontisirin, MDa, Saipin L. Muangman, MDa, Pilar Suz, MDa, Catherine Pihoker, MDb, Dana Fisk, RNb, Anne Moore, RVTd, Arthur M. Lam, MDc,d and Monica S. Vavilala, MDa,b,c,d

a Anesthesiology
b Pediatrics
c Neurological Surgery, University of Washington, Seattle, Washington
d Cerebrovascular Laboratory, Harborview Medical Center, Seattle, Washington


   ABSTRACT
TOP
 ABSTRACT
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVE. We aimed to describe gender differences in blood flow velocity and autoregulation of the anterior and posterior cerebral circulations in prepubertal children.

METHODS. A prospective observational cohort study was performed at Harborview Medical Center's Cerebrovascular Laboratory after institutional review board approval, consent, and assent procedures. Children underwent measurement of middle cerebral and basilar artery flow velocities and cerebral autoregulation testing of the middle cerebral and basilar arteries. Cerebral autoregulation was quantified using the autoregulatory index, and estimated cerebrovascular resistance was calculated. Autoregulatory index <0.4 reflects impaired cerebral autoregulation. Data are presented as mean ± SD. Patients were healthy 4- to 8-year-old children.

RESULTS. Forty-eight children (24 boys and 24 girls) 4 to 8 years of age (mean: 6 ± 2 years) were enrolled. Middle cerebral artery flow velocity was higher than basilar artery flow velocity (96 ± 13 vs 65 ± 11 cm/s). Girls had higher middle cerebral artery flow velocity (99 ± 11 vs 91 ± 13 cm/s) and basilar artery flow velocity (70 ± 10 vs 61 ± 9 cm/s) than boys. Cerebral autoregulation was intact in all children. There was no gender difference in autoregulation between the middle cerebral artery (boys: 0.97 ± 0.07; girls: 0.94 ± 0.11) or basilar artery (boys: 0.94 ± 0.13; girls: 0.94 ± 0.11).

CONCLUSIONS. Similar to older children and adults, girls between 4 and 8 years of age had higher middle cerebral and basilar artery flow velocity than age-matched boys. This difference may reflect inherent differences in cerebral metabolic rate and/or estimated cerebrovascular resistance between the genders.

Key Words: cerebral blood flow velocity • pediatrics • cerebral autoregulation

Abbreviations: CBF—cerebral blood flow • CBFV—cerebral blood flow velocity • TCD—transcranial Doppler • Vmca—middle cerebral artery flow velocity • BA—basilar artery • Vbas—basilar artery flow velocity • MCA—middle cerebral artery • MAP—mean arterial pressure • MAPe—estimated mean arterial pressure • eCVR—estimated cerebrovascular resistance • CVR—cerebrovascular resistance • ARI—autoregulatory index • ARImca—autoregulatory index for the middle cerebral artery • ARIbas—autoregulatory index for the basilar artery • CMR—cerebral metabolic rate • RI—resistance index

In children, cerebral blood flow (CBV) velocity (CBFV) normally changes with age.1 It is low during infancy and increases during childhood before decreasing to adult levels during adolescence.1 Although normative age-related differences in CBFV are recognized in children, little is known about gender differences in either CBFV or cerebral autoregulation during early childhood.

Adult data indicate that middle cerebral artery flow velocity (Vmca) is higher in women ≥55 years of age than in age-matched men.2 In a recent pediatric study of 26 healthy 10- to 16-year-old pubertal adolescents, the investigators reported higher Vmca and basilar artery (BA) flow velocity (Vbas) in girls than in boys.3 In this study, girls had greater autoregulation of the BA compared with boys, whereas boys had greater autoregulation of the middle cerebral artery (MCA). Although the sample size in this study was small, and the significance of the reported differences in autoregulation remains unclear, these findings suggested that the observed gender-related cerebrovascular differences in adults are present during childhood and might be because of hormonal influences. However, whereas the authors used Tanner staging to document puberty, the age range of the children spanned 6 years, and no data from prepubertal children were included, thereby limiting the ability of the authors to define the age at which these potentially hormonally mediated changes occurred. Therefore, the purpose of the present study was to describe gender differences in anterior and posterior CBFV and autoregulation in prepubertal children during early childhood.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study Participants and Setting
This study was approved by the University of Washington's institutional review board. Healthy American Society of Anesthesiologists category I prepubertal children 4 to 8 years old were eligible. Children with a history of seizures, hypertension, syncope, dysautonomia, or neurologic/cardiac disorders were excluded. Children were recruited from well-child visits in the general pediatrics clinic at Harborview Medical Center. Informed consent for participation was obtained from the parent or guardian, and age-appropriate assent was obtained from each child. Physiologic testing was conducted at Harborview Medical Center's cerebrovascular laboratory.

Study Design and Protocol
Each subject was positioned on a bed with the head and back adjustable for elevation. An appropriately sized noninvasive blood pressure cuff was placed on 1 arm. Transcranial Doppler (TCD) ultrasonography (Multidop X; DWL Corp, Sipplingen, Germany) was used to measure flow velocities in the middle cerebral (Vmca) and basilar (Vbas) arteries (Figs 1 and 2). A hand-held 2-mHz ultrasound probe was used to insonate the desired vessel and positioned for sufficient time to achieve steady-state measurement. Previously established age-appropriate depths were used to insonate both the MCAs and BAs.4 During steady-state conditions, Vmca, Vbas, mean arterial pressure (MAP), heart rate, and respiratory rate were recorded in each position.


Figure 1
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  		FIGURE 1 Measurement of Vbas using TCD ultrasonography.

 

Figure 2
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  		FIGURE 2 Sample CBFV tracing from TCD ultrasonography. Peaks represent systolic flow velocities, and troughs represent diastolic flow velocities.

 
To examine cerebral autoregulation, change in position proceeded from the supine to sitting upright (90°) position. Five minutes was allowed between position changes before data collection. For the sitting upright position, the vertical distance between the noninvasive blood pressure cuff and the external auditory meatus was used to calculate the estimated MAP (MAPe) at the Circle of Willis. Because MAP decreases by 1 mmHg for every 1.36-cm increase in vertical height, the change in height from supine to sitting upright was divided by 1.36 cm to calculate the estimated MAPe in the sitting upright position. eCVR (estimated cerebrovascular resistance [CVR]) was calculated as the MAPe divided by Vmca or Vbas.

Briefly, cerebral autoregulation was quantified using the autoregulatory index (ARI) where ARI = % {Delta} eCVR/% {Delta} MAPe; eCVR is calculated as the ratio of MAP to Vmca or Vbas, as appropriate.5,6 Two ARIs were calculated for each subject: 1 for the MCA (ARImca) and 1 for the BA (ARIbas).

Sample Size Calculation and Statistical Analysis
Sample size calculation was based on previously published ARI data.7 We considered a 30% difference in mean ARI to be significant. Assuming {alpha} is .05 and β is .8, power analysis indicated that we needed 12 subjects in each group. The normal mean ARI in children without neurologic disease under general anesthesia is 0.75 to 0.90,7 and a mean ARI ≥0.4 reflects intact cerebral autoregulation.8 CBFV (Vmca and Vbas) and ARI were analyzed by gender. Two-factor analysis of variance was used to compare ARImca versus ARIbas and Vmca versus Vbas between boys and girls. All of the data are presented as mean ± SD.


   RESULTS
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Forty-eight children (24 boys and 24 girls) between the ages of 4 and 8 years (boys: mean: 6 ± 2 years; girls: mean: 6 ± 2 years; P = .85) were enrolled. There were no adverse events during testing, and all of the children completed the study procedure successfully. There was no overall difference in either blood pressure or respiratory rate during physiologic testing (Table 1).


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  		TABLE 1 Physiological Parameters (MAP and Respiratory Rate) During Examination of MCA and BA

 
For both boys and girls, Vmca was higher than Vbas (Vmca: 96 ± 13 cm/s vs Vbas 65 ± 11 cm/s; P = .002; Table 2). In both the supine and upright positions, girls had higher Vmca and Vbas than boys (Table 2). Girls had a lower CVRe of BA than boys (Tables 2 and 3), but there was no gender difference in MCA CVRe.


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  		TABLE 2 CBFV, MAP at MAPe, and CVRe of Healthy 4- to 8-Year-Old Children During Cerebral Autoregulation Testing

 

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  		TABLE 3 CVRe of MCA and BA by Age and Gender in the Supine Position

 
All of the study participants had intact cerebral autoregulation of the MCAs and BAs. There was no difference in the upright MAPe or percentage drop of MAPe between boys and girls (Table 1). There was no difference in either ARImca or ARIbas between boys and girls (Table 4).


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  		TABLE 4 Cerebral Autoregulation Data in 4- to 8-Year-Old Boys and Girls

 

   DISCUSSION
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 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The results of this study show that prepubertal 4- to 8-year-old girls have higher Vmca and Vbas than age-matched boys. This gender-related difference is similar to that described previously in older pubertal children (Table 5). 3 However, unlike in older children, we did not find any gender difference in cerebral autoregulation. This is the first study to document that the observed adult gender differences in CBFV are present during early childhood.


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  		TABLE 5 Vmca and Vbas by Age and Gender in the Supine Position

 
TCD ultrasonography is a noninvasive and bedside tool used to estimate CBF and measure CBFV. Clinically, TCD is used to determine CO2 reactivity and cerebral autoregulation, as well as to diagnose stroke, postoperative emboli, and cerebral vasospasm.9 It is used to prevent stroke in sickle cell disease.10,11 Referent age-related Vmca and Vbas data in children with and without disease using TCD ultrasonography are consistent with age-related CBF changes documented by other neuroimaging modalities, such as single photon emission computed tomography and positron emission tomography studies.12,13 However, there are no single photon emission computed tomography or positron emission tomography data examining gender differences in CBF in healthy children. This study used TCD ultrasonography to provide some estimate of gender-related differences in CBF of the MCA and BA in young boys and girls. Data from the present study indicate that the observed adult gender differences in Vmca are present in young children before puberty. In addition, gender differences in Vbas are also present during early childhood, suggesting that whatever factor may be responsible for the higher CBFV in young girls affects both the anterior and posterior cerebral circulations. This information in healthy children is important to our understanding of changes in disease states, such as traumatic brain injury14 and diabetic ketoacidosis,15 where cerebrovascular changes may account for neurologic complications, such as cerebral ischemia and/or cerebral edema. Examining normative data in healthy awake children is important, because sedatives, analgesics, and anesthetics may alter CBF. For example, hypnotics (barbiturates, etomidate, and propofol), benzodiazepines, opioids (fentanyl, alfentanil, and sufentanil), and {alpha}-2-adrenergic agonists (clonidine and dexmedetomidine) reduce CBF, whereas ketamine may cause variable regional changes.16

There are several potential explanations for the higher Vmca and Vbas observed in females, irrespective of age. These include gender differences in blood viscosity because of hematocrit, hormones, vessel (MCA or BA) size, cerebral metabolism, and/or CVR. Identifying which of these factors is the major reason for the observed finding is challenging, however, because comparative data of these factors between boys and girls are largely lacking. First, whereas girls age 12 to 18 years have a lower hematocrit than boys,17,18 the 1 study to examine hematocrit in prepubertal boys and girls 4 to 8 years of age reported no gender differences.19 We did not have permission to obtain hematocrit in our healthy prepubertal subjects, but this should not be problematic, because there are no gender differences in hematocrit in children in this age group. Second, we discussed previously the role of hormones as an explanation for our findings of higher Vmca and Vbas in 10- to 16-year-old girls because of the following reasons: (1) estrogen and testosterone levels change during this time and vary by gender, (2) animal data have demonstrated that estrogens improve vasodilatation via an enhancement of endothelial nitric oxide synthase,20 and (3) testosterone and/or its metabolites increased cerebral perfusion in healthy adults.21 However, sex steroid levels are normally very low in boys and girls before puberty, and with a reference range for estradiol of <10 ng/mL, reference range for testosterone of <10 ng/dL, and reference range for progesterone of <0.7 ng/mL for both genders,22 it is unlikely that hormonal differences account for the observed gender differences in Vmca and Vbas during early childhood. Third, although it is thought that internal carotid artery and MCA diameters typically reach adult size by 6 years,23 details of the increase in vessel diameter by age and gender are not available. In 1 study of 156 cerebral angiograms of 133 adults and children (72 males and 84 females), Gabrielsen and Greiz24 reported no relationship between age and vessel size but described smaller internal carotid artery and MCA in females compared with males. However, none of the angiograms were from children <10 years of age, and data from children were not analyzed separately. Therefore, it is unclear how cerebral vessel size influences the relationship between gender and CBF or CBFV in young children. Fourth, gender-related difference in Vmca and Vbas might be because of differences in cerebral metabolic rate (CMR).25 Although Kennedy and Sokoloff26 have shown that children have higher CMRs than adults, probably corresponding with the sharp rise in neuronal activity during this time,27 gender differences in CMR have not been examined. Finally, CVR may also impact CBF; Kennedy and Sokoloff26 also reported lower CVR in young children compared with adults. Describing similar findings, in 1988, Bode1 reported higher resistance indices (RIs) in newborns during the first days of life compared with after 1 year of life. After birth, RI slowly decreased reaching a nadir at 1 to 3 years of age before slightly increasing to adult levels between 10 and 16 years of age. However, gender was not considered, and he reported no difference in RI between the anterior and posterior cerebral circulations. In the present study, we estimated CVR from the MAP and CBFV and found that 4- to 8-year-old girls had lower CVRe of BA than age-matched boys (Table 2). Review of our previous CVRe data from older children shows that boys have higher CVRe of both anterior and posterior cerebral circulations than girls and that CVRe increases with age (Tables 3 and 6). Although we cannot separate the influence of cerebrovascular tone from vessel size on CVRe, these data suggest that a decrease in CVRe parallels the age- and gender-related increase in CBFV. We speculate that a higher CMR in girls might explain the noted lower CVRe and higher Vmca/Vbas in girls than in boys.


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  		TABLE 6 Vmca, Vbas, and CVRe MCA and BA by Age in Supine Position

 
In a previous study, we reported greater ARIbas in girls compared with boys, whereas boys were found to have greater autoregulation of MCA. In this study of younger children, we did not find any difference in ARI of either the anterior or posterior cerebral circulations. There are 2 possible explanations for this difference. First, gender differences in cerebral autoregulation may be hormonally mediated and coincide with puberty. Recent reports show that mechanisms involved in cerebral autoregulation may vary as a function of age. For example, experimental evidence derived from newborn piglets shows the prominent role of prostaglandins in the control cerebral autoregulation in the newborn period. On the other hand, the nitric oxide system is thought to have a less prominent role in the newborn but increases in importance with increasing age.28 Alternatively, given the small size of both studies, both type I and type II errors may have occurred, and larger number of subjects may be needed to detect potential gender differences in cerebral autoregulation.

Cerebral autoregulation can be evaluated by measuring changes in CBFV in response to changes in blood pressure using either the static or dynamic method of testing.8,29 We used the static cerebral autoregulation test (tilting test), because it is noninvasive, does not involve pharmacological intervention, and is well tolerated by children.30,31 We attempted to examine Vmca, Vbas, and cerebral autoregulation in children 2.5 to 3 years of age, but the lack of subject cooperation precluded obtaining quality data in these children. Therefore, obtaining such data in very young children may only be feasible while they are either sedated or anesthetized.

There are some limitations to this study. First, we measured CBFV using TCD ultrasonography and not CBF. However, TCD ultrasonography has been used to estimate CBF in children with various medical diseases, such as sickle cell disease,10,11 and the use of TCD data has allowed us to better understand the effects of pathologic conditions on cerebrovascular physiology, such as the hyperemic state in pediatric traumatic brain injury.14 We could not control the blood pressure to ensure an exact drop in MAPe to precipitate an autoregulatory response. However, all of the study participants achieved at or more than a 5-mmHg drop in MAPe with position change from supine to upright. We did not evaluate cerebral arteries other than the MCA and BA. Although we did not monitor end-tidal CO2 and cannot exclude the effect of changes in ventilation on CBF, we found no difference in respiratory rate in each position between boys and girls. We could not control CMR or flow metabolism coupling in our awake study participants. However, we recorded measurement under a steady-state condition by minimizing distraction during the study. We calculated CVRe from Vmca and MAPe data. Finally, because there are no significant differences in hormone concentrations observed normally between prepubertal boys and girls, we did not obtain hormone levels from our study participants.

Our small study shows that prepubertal girls 4 to 8 years of age have higher Vmca and Vbas than age-matched boys. This difference may reflect either the influence of CMR and/or CVRe on CBFV between the sexes. The lack of gender differences in ARI of both circulations during early childhood, in the presence of such differences in pubertal children, postulates a potential hormonal role in the control of cerebral autoregulation before adulthood. Our findings provide new information regarding gender differences in cerebrovascular physiology in healthy awake children. We have also demonstrated the feasibility of conducting such studies in children as young as 4 years of age.


   FOOTNOTES
 
Accepted Sep 27, 2006.

Address correspondence to Monica S. Vavilala, MD, Department of Anesthesiology, Harborview Medical Center, 325 Ninth Ave, Box 359724, Seattle, WA 98104. E-mail: vavilala{at}u.washington.edu

The authors have indicated they have no financial relationships relevant to this article to disclose.


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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics

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