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Doppler Sonographic Screening of the Flow in the Basilar Artery during Head Rotation Reduces the Risk for Sudden Infant Death Dopplersonografisches Screening der Blutströmung in der Arteria basilaris während Kopfrotation reduziert das Risiko für den plötzlichen Säuglingstod Authors

K.-H. Deeg, A. Reisig

Affiliation

Sozialstiftung Bamberg, Klinik für Kinder und Jugendliche

Key words

Zusammenfassung

Abstract

!

!

Ziel: Eine möglicher Risikofaktor des plötzlichen Säuglingstods ist eine Minderperfusion des Hirnstamms während Kopfrotation. Material und Methoden: Von 1998 – 2009 wurde die Blutströmung in der A. basilaris bei 18194 Neugeborenen, 9322 Jungen und 8872 Mädchen, dopplersonografisch gemessen. Die Flussmessungen erfolgten in 5 verschiedenen Positionen: in Rückenlage mit Kopf in Mittelposition (Neutralposition) sowie nach Rotation zur linken und rechten Seite und zwar in Rücken- und Bauchlage. Aus dem Flussspektrum wurde die maximale und mittlere Flussgeschwindigkeit ermittelt. Die Flussgeschwindigkeiten während der Kopfrotation wurden in Prozent der Neutralposition angegeben. Ein Abfall der Flussgeschwindigkeiten unter 50% wurde als abnorm, eine biphasische, negative oder um die Nulllinie oszillierende Blutströmung wurde als pathologisch angesehen. Bei Kindern mit abnormem oder pathologischem Fluss während der Kopfrotation wurden gefährliche Kopfrotationen durch entsprechende Lagerungsmaßnahmen vermieden. Die Inzidenz von SID in unserer Studiengruppe wurde mit der SID-Inzidenz von 3519 Neugeborenen ohne Screening verglichen. Ergebnisse: Bei 17 929 Neugeborenen (98,54%) war die Blutströmung in der A. basilaris unabhängig von Kopfrotation und Körperposition. 204 Neugeborenen (1,12 %) zeigten einen abnormen Abfall der Flussgeschwindigkeiten unter 50 %. Pathologische Blutströmungen konnten nur bei 61 Kindern (0,33 %) gefunden werden. Die Inzidenz von SID in der Studiengruppe war 0,055 ‰ (1:18 194), in der Kontrollgruppe 1,14 ‰ (4:3519). Der statistische Vergleich der SID-Inzidenz beider Gruppen zeigte eine signifikant niedrigere SID-Inzidenz in der Screeninggruppe (p < 0,0030). Schlussfolgerung: Die Hypoperfusion des Hirnstamms ist ein möglicher Risikofaktor von SID.

Purpose: Position-dependent hypoperfusion of the brain stem may be a risk factor of sudden infant death. Materials and Methods: From 1998 to 2009 we performed Doppler sonographic flow measurements in the basilar artery of 18194 newborns, 9322 boys and 8872 girls, in five different positions: the neutral position with the head in the midline and during head rotation to the left and right in a supine or prone position. The peak systolic and the time average flow velocity were measured from the flow profile. The flow velocities during head rotation were converted to % of the flow in the neutral position. A decrease in the velocities during head rotation below 50 % was thought to be abnormal. Biphasic flow, flow oscillating around the zero line or retrograde flow during rotation was considered to be pathological. Head rotations, which had caused abnormal and pathological flow, were avoided. The incidence of SIDS in our study group was evaluated and compared with the incidence in a control group of 3519 newborns. Results: In 17 929 newborns (98.54 %) the blood flow in the basilar artery was independent of head rotation and body position. In 204 newborns (1.12 %) we found an abnormal decrease under 50 %. Pathological flow alterations could be found in 61 patients (0.33 %). The overall incidence rate of SIDS in the study group was 0.055 ‰ (1:18 194). The incidence rate of SIDS in the control group was 1.14 ‰ (4:3519). The comparison of both groups showed a statistically significant (p < 0.0030) lower incidence rate in the study group. Conclusion: Hypoperfusion of the brain stem may be a significant risk factor of SIDS.


▶ sudden infant death ● ▶ position-dependent blood ● ▶ ● ▶ ● ▶ ●

flow Doppler sonography basilar artery vertebral arteries

received accepted

28.10.2009 14.12.2009

Bibliography DOI http://dx.doi.org/10.1055/ s-0029-1245144 Published online March 16, 2010 Ultraschall in Med 2010; 31: 506 – 514 © Georg Thieme Verlag KG Stuttgart ∙ New York ∙ ISSN 0172-4614

Correspondence Prof. Dr. Karl-Heinz Deeg Sozialstiftung Bamberg, Klinik für Kinder und Jugendliche Buger Str. 80 96049 Bamberg Germany Tel.: ++ 49/9 51/50 31 27 00 Fax: Sekr : ++ 49/9 51/50 31 27 09 [email protected]

Deeg KH, Reisig A. Doppler Sonographic Screening… Ultraschall in Med 2010; 31: 506 – 514

Originalarbeit

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Fig. 1 Doppler sonographic flow measurement in the basilar artery in the coronal section. Normal forward flow during systole and diastole. Normal flow profile with normal flow velocities. Abb. 1 Dopplersonografische Flussmessung in der A. basilaris im Koronarschnitt. Normaler systolisch-diastolischer Vorwärtsfluss. Normales Flussprofil mit normalen Flussgeschwindigkeiten.

Fig. 2 a Normal flow profile in neutral position with a peak systolic flow velocity of 44 cm/sec. b Abnormal fall of the blood flow velocities during head rotation to the right in prone position although a normal forward flow can be shown. The peak systolic flow velocity decreased from 44 cm/sec to 16 cm/sec during head rotation.

We assumed that position-dependent hypoperfusion of the brain stem may be a risk factor for the sudden infant death syndrome [7, 8]. For the evaluation of this hypothesis, we performed Doppler sonographic flow measurements in the basilar artery of healthy newborns and investigated the dependency on head and body position.

Patients and methods !

From 1998 to 2009 we performed a Doppler sonographic screening program of the flow in the basilar artery in 18,194 healthy newborns born in the department of gynecology and obstetrics of our hospital. Preterm infants and ill newborns were not included in our investigation. 9322 (51.2 %) newborns were boys and 8872 (48.8 %) were girls. The infants were born with a gestational age of 38.6 ± 2.1 weeks and a mean birth weight of 3293 ± 597 g. Doppler sonographic flow measurements were performed in the neonatal period (mean: 8 ± 14 days). All investigations were performed by experienced assistant sonographers of our unit. Each sonographer conducted the investigations exclusively for more than 6 months (about 1000 Doppler sonographic studies). All investigations were performed with informed consent of the parents. The study was approved and accepted by the ethics committee of the university of Erlangen-Nuremberg. The study was performed with the computer sonographic units Acuson 128 Art and Sequoia (Siemens). Our investigations were carried out with a 5 and 7.5 MHz sector or curved array transducer with the possibility of color and spectral Doppler. Investigations of the basilar artery were performed in sagittal ▶ Fig. 1) [9]. In all newborns flow in the and coronal sections (● basilar artery was measured in five different head and body positions as shown previously [7, 8]: 1. Supine position with head in the midline (neutral position)

Abb. 2 a In Neutralposition normales Flussprofil mit einer maximalen systolischen Flussgeschwindigkeit von 44 cm/s. b Abnormer Abfall der Flussgeschwindigkeiten in Bauchlage und Kopfrotation zur rechten Seite, obwohl noch ein systolisch-diastolischer Vorwärtsfluss nachweisbar ist. Die maximale systolische Flussgeschwindigkeit fällt während der Rotation des Kopfes von 44 auf 16 cm/s.



Sudden infant death syndrome (SIDS) is the most common cause of death in the first year of life beyond the neonatal period. The global incidence rate is between 0.5 and 5‰ [1, 2]. Due to different prevention campaigns, the incidence rate in Europe has dropped to 0.5 to 1 ‰ in recent years [2]. Although many theories have been published in recent decades, the causes of SIDS are still unknown. Pathological-anatomical investigations of the brain of SIDS victims have shown gliosis of the brain stem [3, 4]. Gliosis may be the result of recurrent injury of the brain stem such as frequent or longer lasting ischemia. The most important risk factor found in SIDS victims is the prone position [1, 2, 5]. 83 % of infants who die of SIDS are found in a prone position [5, 6].

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Fig. 4 Flow measurement in the basilar artery during head rotation. Till rotation of 80° normal forward flow. Between 80 and 85° marked reduction of the flow velocities, although normal forward flow can be shown. Between 85° and 90° flow reverse with missing diastolic flow occurs.


Abb. 4 Flussmessungen in der A. basilaris während Kopfrotation. Bis zu 80° normaler Vorwärtsfluss. Zwischen 80 und 85° deutlicher Abfall der Flussgeschwindigkeiten bei erhaltenem Vorwärtsfluss. Zwischen 85 und 90° retrograder Fluss mit fehlender diastolischer Komponente.

Fig. 3 a Coronal scan: Pathological retrograde systolic flow and missing diastolic flow during head rotation. Very low time average flow velocity. b Sagittal scan through the midline: Pathological biphasic flow with retrograde systolic and antegrade diastolic flow in the basilar artery during head rotation. c Sagittal scan through the midline: Pathological flow oscillating around the zero line. Very low time average flow velocities in all cases. Abb. 3 a Koronarschnitt: pathologisch retrograder systolischer Fluss und fehlender diastolischer Fluss während Kopfrotation. Sehr niedrige mittlere Flussgeschwindigkeit. b Sagittalschnitt in der Mittellinie: während Kopfrotation pathologisch biphasischer Fluss in der A. basilaris mit retrogradem systolischem Fluss und antegradem diastolischem Fluss. c Sagittalschnitt in der Mittellinie: pathologischer, um die Nulllinie oszillierender Fluss. Sehr niedrige mittlere Fließgeschwindigkeiten in allen 3 Fällen.

2. Supine position with head rotation to the right and left 3. Prone position with head rotation to the right and left The peak systolic and time average flow velocities were mea▶ Fig. 1). sured from the flow profile (●

The flow velocities in the neutral position (supine with head in the midline) served as the individual point of reference assumed to be 100 %. The flow velocities in the other positions were converted to a flow percentage in the neutral position. We assumed that the flow in the basilar artery does not change significantly during head rotation and changes in body position ▶ Fig. 2a). (● A drop in the flow velocities during head rotation to less than 50 % of the initial value in the neutral position was thought to ▶ Fig. 2b). be abnormal (● A biphasic flow with diastolic flow reversal, flow oscillating around the zero line or systolic retrograde flow, with missing ▶ Fig. 3, 4). diastolic component was considered pathological (● All infants with an abnormal and pathological flow during the screening program underwent a thorough second investigation with additional flow measurement in the vertebral arteries one day later. Abnormal flow measurements (abnormal or pathological flow) were always reproducible. In 213 infants with abnormal (156) and pathological (57) flow in the basilar artery, the flow in both vertebral arteries was additionally investigated in coronal sections [7, 8]. Measurements in the vertebral arteries were performed 5 mm below the confluence of both vertebral arteries in the above ▶ Fig. 5a). mentioned positions similar to the basilar artery (● In the neutral position the anatomical size of the vertebral arteries was judged. Both arteries have usually a similar size. In these cases the flow velocities are similar. If the peak or time average flow velocity of one vertebral artery was less than 50 % of the other, the artery was considered to be hypo▶ Fig. 5b, c). If only one artery could be shown by colplastic (● or Doppler, although low flow settings were chosen, unilateral ▶ Fig. 5 d). vertebral aplasia was diagnosed (● Flow measurements in the vertebral arteries during head rotation were performed in 73 infants with an abnormal flow decrease and in 39 infants with a pathological flow decrease during head rotation. Flow alterations were considered abnor-


b

Fig. 5 a Normal confluence of the vertebral arteries (coronal scan through the base of the skull). BA = basilar artery; PCA = posterior cerebral artery; VAr and VAl = right and left vertebral artery. b Doppler sonographic flow measurement in the right vertebral artery shows a normal flow profile with normal flow velocities (time average flow velocity 13.9 cm/sec). c Dopplersonographic flow measurement in the left vertebral artery shows an antegrade flow profile with low flow velocities in comparison to the right side (time average velocity 5.9 cm/sec). d Unilateral vertebral artery aplasia on the right side of the image (arrow) in an infant with mild ventricular dilation. Normal basilar artery and left vertebral artery on the left side of the image. e Unilateral vertebral artery hypoplasia on the right side of the image. The left vertebral artery (VA li) and the basilar artery show normal antegrade flow displayed in red. The hypoplastic right artery (VA re) shows retrograde flow during head rotation. It is therefore displayed in blue.

Abb. 5 a Normaler vertebro-basilärer Konfluenz (Koronarschnitt durch die Schädelbasis). BA = A. basilaris; PCA = A. cerebri posterior; VAr and VAl = rechte und linke Arteria Vertebralis. b Dopplersonografische Flussmessung in der rechten Vertebralarterie. Normales Flussprofil mit normalen Flussgeschwindigkeiten (mittlere Flussgeschwindigkeit 13,9 cm/s). c Dopplersonografische Flussmessung in der linken Vertebralarterie zeigt einen antegraden Fluss mit niedrigen Flussgeschwindigkeiten im Vergleich zur rechten Seite (mittlere Flussgeschwindigkeit 5,9 cm/s). d Einseitige Aplasie der A. vertebralis auf der rechten Bildseite (Pfeil) bei einem Kind mit leichter Ventrikulomegalie. Normale A. basilaris und linke Vertebralarterie auf der linken Bildseite. e Einseitige Hypoplasie der Vertebralarterie auf der rechten Bildseite. Die linke Vertebralarterie (VA li) und die A. basilaris zeigen einen normalen Vorwärtsfluss, der sich rot darstellt. Die hypoplastische rechte Vertebralarterie (VA re) zeigt einen retrograden Fluss während Kopfrotation, der sich blau darstellt.

mal (< 50% of the initial value) or pathological if they were retrograde, biphasic or oscillating around the zero line ▶ Fig. 5e) [7, 8]. (● The parents of infants with an abnormal decrease in the flow velocities or pathological flow during head rotation were instructed to avoid the head rotations that caused the drop in the flow velocities. Additionally these infants were provided with a monitor that controlled heart and breathing rate during sleep. In collaboration with the board of health and the public prosecution department, all SIDS cases of our district were registered and analyzed.

The incidence rate of SIDS in our study group was evaluated and compared with the incidence rate in a control group of 3,519 newborns, born between 1998 and 2009 at our institution, that were not investigated. The parents of these newborns elected not to participate in our voluntary screening program. Statistical analysis of the incidence rate of SIDS in both groups was performed with Fishers’ exact test.


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Table 1 Peak systolic flow velocities and flow percentage in neutral position with standard deviation in different head and body positions. position

peak systolic flow

%

velocity (cm/s)

neutral: supine with head in the midline

42.5 ± 10.8

100

supine with head rotation to the right

40.6 ± 10.8

96.14 ± 13.6

supine with head rotation to the left

40.4 ± 10.6

95.59 ± 13.1

prone with head rotation to the right

39.4 ± 10.7

93.29 ± 15.3

prone with head rotation to the left

40.0 ± 10.5

94.78 ± 14.2

Table 2 Time average flow velocities and percentage of flow velocities in neutral position in different head and body positions. position

time average flow

%

neutral: supine with head in the midline

13.0 ± 4.0

100

supine with head rotation to the right

12.5 ± 4.0

98.94 ± 27.41

supine with head rotation to the left

12.5 ± 3.9

99.30 ± 27.17

prone with head rotation to the right

12.5 ± 4.0

99.23 ± 28.95

prone with head rotation to the left

12.8 ± 4.1

101.18 ± 28.65


velocity (cm/s)

Fig. 6 Box plots of the peak systolic flow velocities in percentage of the flow in neutral position. The graphic shows that the flow velocities during head rotation usually do not fall below 50 % of the initial value. Abb. 6 Box plots der maximalen systolischen Flussgeschwindigkeiten bezogen auf die Flussgeschwindigkeiten in Neutralposition. Die Abbildung zeigt, dass die Flussgeschwindigkeiten während der Kopfrotation nicht unter 50% des Ausgangswerts abfallen.

Results !

Basilar artery

According to possible flow changes during head rotation, we divided the infants into three groups: ▶ Group I: Infants without considerable changes in the flow in the basilar artery during head rotation ▶ Group II: Infants with a decrease in flow velocities to less than 50 % of the value measured in the neutral position ▶ Group III: Infants with retrograde or biphasic flow or flow fluctuating around the zero line during head rotation

Group I: Normal flow

In 17981 newborns (98.83 %) a systolic-diastolic forward flow ▶ Fig. 1). The peak systolic could be found in all positions (● flow velocities in this group did not fall below 50% of the initial values in the neutral position. The blood flow in the basilar artery was independent of head rotation and body position. The mean peak systolic and mean time average flow ▶ Table 1, 2. velocities in the different positions are listed in ● The box plots of the changes in the peak systolic and time average flow velocities in the different positions are shown in ▶ Fig. 6, 7. ●

Infants with an abnormal or pathological flow during head rotation

In 213 infants (1.17 %) head rotation caused an abnormal or pathological flow. In 156 infants we found an abnormal decrease to less than 50% of the initial value, and in 57 infants we found a pathological flow. Abnormal and pathological

Fig. 7 Box plots of the time average flow velocities in percentage of the flow in neutral position. The graphic shows that the flow velocities do not decrease below 50 % of the initial value in neutral position. Abb. 7 Box plots der mittleren, über die Zeit gewichteten Flussgeschwindigkeiten im Vergleich zur Normalposition. Die Abbildung zeigt, dass die mittleren Flussgeschwindigkeiten während Kopfrotation nicht unter 50 % des Ausgangswerts abfallen.

flow measurements could be reproduced during repeated investigations. In 144 infants (67.6%) abnormal flow occurred during rotation to the right, and in 74 infants (34.7%) during rotation to the left. In 9 infants (4.2 %) flow decrease was identified during rotation to both sides. In 4 infants the side of flow alteration was not registered.


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In 156 newborns (0.86%) we found a decrease in the peak systolic and/or the time average flow velocity to less than 50 % of the individual normal value measured in the neutral position ▶ Fig. 2). In contrast to group III, a normal forward flow dis(● ▶ Fig. 2b). played over the baseline could be found (● Abnormal flow alterations could be shown in a prone and supine position, although the alterations in a prone position were more pronounced.

Group III: Pathological flow during head rotation

Pathological flow alterations could be found in 57 patients (0.31 %). Pathological flow alterations during head rotation were as follows: ▶ Retrograde flow in the basilar artery either systolic- diastolic or only during systole was found in 26 infants (0.14 %) ▶ Fig. 3a) (● ▶ Biphasic flow with systolic retrograde and diastolic forward ▶ Fig. 3b) flow was found in 26 infants (0.14 %) (● ▶ Oscillating flow fluctuating around the zero line was seen in ▶ Fig. 3c) 5 infants (0.03 %) (● Pathological flow alterations were found in both a supine and prone position. Flow changes in a prone position were more pronounced than in a supine position. Slight head rotations of up to approximately 70° did not cause flow alterations in any infant (the exact angles were estimated but not measured). Pathological flow occurred only during maximum rotation of approximately 80 to 90°, characteristic of prone body position. Successive head rotation first caused flow deceleration at a rotation of about 80°. Further rotation of up to approximately 85 to 90° caused pathological biphasic ▶ Fig. 4). Pathological flow was aggravated or retrograde flow (● during additional reclination of the head, which is typical for prone sleeping.

Flow measurements in the vertebral arteries in a neutral position

In 213 infants with abnormal or pathological flow during head rotation, the flow was measured in both vertebral arteries in a ▶ Fig. 5a). In 208 infants systolic-diastolic forneutral position (● ward flow could be shown in the vertebral arteries (one or two). 5 infants showed retrograde flow in the right vertebral artery in the neutral position. The cause of the retrograde flow in the neutral position was not further evaluated. 151 infants (70%) had similar flow velocities in two vertebral arteries. The rest of the patients (30%) showed abnormal flow in one vertebral artery: 43 infants (20.2%) had unilateral vertebral hypopla▶ Fig. 5c, d). sia, and 14 (6.6%) had unilateral vertebral aplasia (● Anatomical abnormalities occurred twice as often on the right side (41 infants) than on the left side (21 infants).

Flow measurements in the vertebral arteries during head rotation

In 73 patients with an abnormal flow decrease under 50% of the initial value and in 39 patients with a pathological flow decrease during head rotation, flow measurements were additionally performed in the vertebral arteries during head rotation.

Flow changes in the vertebral arteries in 73 patients with an abnormal flow in the basilar artery during head rotation In 73 patients with an abnormal flow in the basilar arteries during head rotation, an abnormal or pathological retrograde or biphasic flow could be found in the contralateral vertebral artery during head rotation. Abnormal or pathological flow occurred in 43 (59%) infants during rotation to the right and in 24 infants (33%) during rotation to the left. Abnormal flow alterations during rotation to both sides could be found in 6 infants (8%).

Flow changes in the vertebral arteries in 39 patients with a pathological flow during head rotation In 39 patients with a pathological flow in the basilar arteries during head rotation, a pathological (retrograde or biphasic) flow could be found in the contralateral vertebral artery during head rotation. A pathological flow during head rotation occurred in 21 infants during rotation to the right and in 16 infants during rotation to the left. Bilateral flow alterations could be found in 2 infants.

Approach in infants with an abnormal and pathological flow Abnormal and pathological flow alterations were considered dangerous for the development of brain stem hypoperfusion and SIDS. Therefore prevention methods were implemented: ▶ Parents were instructed to avoid head rotations to the potentially dangerous side on which flow decrease occurred. ▶ The infants were provided with a monitor to control heart and breathing rate until normalization of the blood flow in the basilar artery during head rotation. Prevention of head rotation to the problematic side (where pathological flow occurred) prevented acute life threatening events with apnea and bradycardia in all infants.

Doppler sonographic controls of patients with an abnormal or pathological flow Serial Doppler sonographic controls were performed until normalization of the flow occurred. Flow alterations decreased in severity as the infant aged. Normalization of flow occurred within 11 months with a mean of 4.5 ± 2.8 months. The flow often normalized already within the first six months of life. Monitoring was stopped after normalization of the basilar artery flow (no decrease to less than 50% of the initial value during head rotation).

SIDS incidence rate

The incidence rate of SIDS in the study group was compared to ▶ Table 3). the SIDS incidence rate in the control group (● ▶ 1 infant in group I (17981 infants with no flow alteration) died at the age of 6 months of SIDS. Pathological-anatomical investigation showed no obvious cause of death.

Table 3 Frequency of SIDS in the screening group (n: 18,194) in comparison with a control group (n: 3519) without screening.1 SID

screening

no

yes

sum

yes

18 193

1

18 194

no

3 515

4

3 519

21 708

5

21 713

total

1

Exact Fishers’ test: p-value < 0.0030.



Group II: Abnormal decrease to less than 50% during head rotation

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▶ No infant in group II (156 infants with abnormal flow decrease

< 50%) and in group III (57 infants with pathological flow) died of SIDS. ▶ The overall incidence rate of SIDS in the study group was 0.055 ‰ (1 infant from 18194) ▶ 4 infants in the control group (3 519 infants) died of SIDS. The incidence rate of SIDS in the control group was 1.14 ‰. ▶ The comparison of the SIDS incidence rate in the study group and the control group with Fishers’ exact test showed a statistically significant (p < 0.0030) lower incidence rate in the ▶ Table 3). study group (●

Discussion


!

Sudden infant death syndrome is the most frequent cause of death in the first year of life. The United States have a SIDS rate of 0.57‰ [1]. Due to recent back to sleep intervention campaigns the incidence rate of SIDS in Germany has decreased to 0.5 ‰ in the last several years. The causes of SIDS are still unclear. Pathological-anatomical investigations of SIDS victims showed gliosis of the brain stem, which may have been the result of frequent or longer lasting ischemic events [3, 4]. Since most SIDS victims are found in a prone position [1, 2, 6], we assumed that position-dependent hypoperfusion of the brain stem may be a major risk factor of SIDS [7, 8]. Color-coded Doppler sonography allows the measurement and quantification of blood flow velocities in all intracranial arteries through the open anterior fontanelle [9, 10]. Alterations in flow during head rotation and changes in body position can be registered. Since the diameter of the great intracranial arteries at the base of the skull is constant, alterations in the volume flow correlate well with changes in the time average flow velocity. A significant decrease in the time average flow velocities causes a reduction in the volume flow in the measured artery and leads to a significant decrease in the blood supply to certain areas of the brain. Very low forward flow and especially biphasic flow or flow oscillating around the zero line may cause low time average flow velocities and volume flow. If these flow alterations occur in the basilar artery they may lead to hypoperfusion of the brain stem. Biphasic flow and flow oscillating around the zero line are extremely dangerous for the perfusion of the brain or parts of the brain since they are associated with a very low volume flow. If they are found in all intracranial arteries, they are characteristic of intravital brain death [11, 12]. If they are found in the blood supply of the brain stem, this may lead to hypoperfusion of the brain stem and may cause malfunction of the brain stem. The influence of head position on the flow within the vertebro-basilar system in vivo has been described in a preliminary note by Rotteveel and Colon [13]. In three out of five patients with near sudden infant death, they found ‘blocking’ of the contralateral vertebral artery with a unidirectional Doppler device [13]. Unidirectional Doppler systems, however, do not allow flow measurements in defined intracranial arteries. With duplex Doppler systems, flow measurements in defined intracranial arteries are possible [9, 10]. Flow measurements in the basilar artery are of special interest since the brain stem is perfused by arteries originating from the basilar artery. Our previous investigations have shown that the flow velocities in the internal carotid and anterior cerebral arteries are

Fig. 8 a MR angiogram of the vertebral arteries in neutral position (Olga Hospital, Stuttgart, Prof. Winkler). VAl and VAr = left and right vertebral artery. ICAl and ICAr = left and right carotid artery. b MR angiogram of the vertebral arteries during head rotation to the left (Olga Hospital, Stuttgart, Prof. Winkler). The image shows compression of the right vertebral artery at the cranio-cerebral junction (arrows). Abb. 8 a MR Angiogramm der Vertebralarterien in Neutralposition (Olga Hospital, Stuttgart, Prof. Winkler). VAl und VAr = linke und rechte Vertebralarterie. ICAl und ICAr = linke und rechte A. carotis. b MR-Angiogramm der Vertebralarterien während Kopfrotation nach links (Olga Hospital, Stuttgart, Prof. Winkler). Kompression der rechten Vertebralarterie im Bereich des kraniozervikalen Übergangs (Pfeile).

independent of head rotation and body position [7, 8, 14]. Pathological flow alterations were found in 20 % of patients with apparent life-threatening events who have an increased risk of SIDS [7, 8, 14]. In our screening collective the flow in the basilar artery was independent of the head rotation and body position in 98.83% of infants. Pathological flow alterations could only be found in a very low percentage of 0.31 %. The decrease in blood flow in the basilar artery was caused by blockage of the contralateral vertebral artery at the cranio-cervical junction during head votation [7, 8]. This could clearly be shown by MR angiography, which was performed in some pa▶ Fig. 8). tients with pathological flow during head rotation (● Since head rotation in a prone position is more pronounced than in a supine position, flow alterations in a prone position were more distinct. This correlates with the fact that most SIDS victims were found in a prone position [1, 5]. Flow alterations were aggravated (transition of abnormal to pathological flow) if rotation was associated with additional reclination of the head. Predisposing locations for the compression of the vertebral arteries are the cranio-cervical junction, especially the exit from the transverse foramen of the atlas, the course around the lateral mass of the atlas and the penetration through the atlanto▶ Fig. 8). occipital membrane (● The compression of the vertebral arteries at the cranio-cervical junction may reduce the flow in the contralateral vertebral artery and in the basilar artery of vulnerable infants. If the contralateral vertebral artery is blocked, the brain stem is exclusively perfused by the other vertebral artery. However, if this artery is hypoplastic or aplastic, compensatory mechanisms are limited. The flow in the hypoplastic artery may not be suf-


b

ficient and cause oscillating or biphasic flow in the basilar artery. If complete obstruction of the flow at the cranio-cervical occurs, the only compensating mechanism is perfusion by the posterior communicating branches of the circle of Willis. In these cases retrograde flow in the basilar artery can be found. However, the collateral circulation through the posterior communicating arteries is limited. Pathological-anatomical investigations by Pamphlett demonstrated that the small posterior communicating arteries of young infants cannot sufficiently compensate blockage of vertebral artery flow. In 81% of infants the conductance through the communicating arteries is less than 25 % of the basilar artery conductance [15]. The conductance in one vertebral artery is less than half of the contralateral artery in 41 % of 68 infants [15]. Previous Doppler sonographic investigations of the flow in the vertebral arteries of 2,737 newborns showed anatomical differences in 8 % of the vertebral arteries [16]: 6 % of the infants had unilateral hypoplasia of one vertebral artery (right side 3.7 % left side 2.3 %). In 2% of the infants, unilateral aplasia of the vertebral arteries could be found (right side 1.3 % left side 0.7 %). The percentage of unilateral aplasia or hypoplasia of the vertebral arteries in the screening group with abnormal or pathological flow in the basilar artery was higher (30%). If the leading (larger) vertebral artery is blocked during head rotation, the hypoplastic vertebral artery and the small posterior communicating arteries can no longer supply enough blood flow to the brain stem [15, 16]. For the blood supply to the brain stem it makes no difference whether the artery is perfused in an antegrade or retrograde fashion as long as the time average flow velocity does not drop significantly. The time average flow velocity is responsible for the volume flow and perfusion. Biphasic flow profiles and a flow which oscillates around the zero line are problematic. In these cases time average flow velocities may fall under a critical limit. A subsequent decrease in volume flow may cause life threatening hypoperfusion of the brain stem. This may lead to lethal brain stem ischemia, induce central apnea and bradycardia and cause sudden infant death [15]. Our hypothesis is confirmed by postmortem angiograms performed by Saternus in infants who died of SIDS [17 – 20]. He found a dramatic flow reduction in both vertebral arteries during head rotation, caused by mechanic compression at the cranio-cervical junction [18, 19]. Rotation of 90° induced a reduction in the average flow volume to less than 5% of the initial value [18]. Additional reclination or flexion of the head associated with rotation aggravated the situation [19]. Wald et al. calculated the vascular resistance in the vertebral arteries of 10 sudden infant death victims by measuring the intravascular peak pressure in different head positions [21]. Position-induced pressure changes occurred in the vertebral arteries of all children. In 3 infants head rotation increased the vascular resistance in the contralateral vertebral artery, in one infant ipsilaterally. In 3 other infants the combined movement of rotation and extension caused an increase in resistance ipsilaterally and contralaterally. Arterial compression during neck movement has been demonstrated directly by Pamphlett [21]. He performed pathologicalanatomical investigations of the cranio-cervical junction in SIDS victims [21]. He found compression of the vertebral arteries during head rotation and extension [21]. The arteries were

compressed between the transverse process of the atlas and the occipito-cervical membrane [21]. Pamphlett concludes that compression of the vertebral arteries during head movement could induce lethal brain stem ischemia [21]. In patients with inadequate collateral flow, it may cause hypoperfusion of the brain stem and be a cause of SIDS [21]. In summary blockage of the vertebral arteries during head rotation could be shown by post-mortem angiographic studies and by pathological-anatomical investigations of SIDS victims [17 – 21]. Blockage of the vertebral arteries is caused by several anatomical abnormalities at the cranio-cervical transition in newborns and young infants [22, 23]. Gilles could show instability in the region of the atlanto-occipital articulation post-mortem, which caused compression of the vertebral arteries [22]. Anatomical disproportion of the ring of atlas and the width of the foramen occipitale magnum leads to protrusion of the dorsal ring of atlas through the foramen magnum into the posterior cranial fossa during extreme head rotation [22]. This may cause compression of the spinal cord on one side and the vertebral arteries on the other side [22]. The abnormal narrow spinal canal in young infants may be compressed by reclination of the head to less than 50 % of the initial value [18]. Additionally the posterior portions of the occipital condyles are hypoplastic and allow compression of the vertebral arteries [22]. The superior articular facet of the atlas is relatively short and flat posterior. The vertebral arteries lie exposed on the surface and are not protected by a groove as in older infants and adults [22]. Good formation of the posterior condyles in older children on the other hand protects the vertebral arteries from compression [22]. The artery in young infants, however, is vulnerable to compression on the flat surface of the atlas [22]. Extension and rotation of the head may compress the vertebral artery and the neighboring soft tissue between two adjacent bony structures (posterior arch of atlas and occipital bone). A thick atlanto-occipital membrane, which runs directly above the vertebral artery, may aggravate compression [21]. Pamphlett and Gilles speculate that this compression may reduce vertebral perfusion in certain risk patients and cause life-threatening events [21, 22]. Another aggravating fact is the bad head control of young infants which tolerates extreme head rotations. In the first months of life sleeping in a prone position and the bad tonus of the neck muscles may lead to pronounced head rotation. Infants with the above mentioned anatomical abnormalities have an increased risk for compression or complete obstruction of the flow in the vertebral arteries. Simultaneous decrease of the blood flow in the basilar artery may cause lifethreatening hypoperfusion of the brain stem and cause central bradycardia and apnea. With increasing age, beginning upright positions and better head control of infants (necessary for sitting!), extreme head rotations occur less frequently. Other positive influencing factors are anatomical alterations in the region of the cranio-cervical region with increasing growth. This may be the reason why the risk of hypoperfusion of the brain stem gradually disappears. Our speculations are supported by recurrent Doppler sonographic flow measurements during the first year of life. These Doppler sonographic controls showed normalization of blood flow during the second half of the first year of life. This is in accordance with epidemiologic data which show a peak inci-


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dence rate of SIDS at 3 months and a marked decrease after the age of 9 months [1, 5].

Conclusion !

▶ Hypoperfusion of the brain stem may be a significant risk factor of SIDS.


▶ Pulsed Doppler sonography is a noninvasive method for the

evaluation of the hypoperfusion theory of SIDS in vivo [18, 19, 21 – 24]. Doppler sonographic screening of the flow in the basilar artery can detect infants with an increased risk for SIDS. ▶ Our Doppler sonographic screening programme and the prevention of dangerous head rotations in patients with an abnormal and pathological flow caused a significant reduction in the incidence rate of SIDS (0.055‰) in our area in comparison with a control group (1.14 ‰). ▶ A general screening of the flow in the basilar artery could detect patients with an increased risk of hypoperfusion of the brain stem. ▶ General neonatal Doppler sonographic screening of the flow in the basilar artery during head rotation could further reduce the incidence rate of SIDS.

Acknowledgement !

The MRI investigations were performed in the Department of Pediatric Radiology of the Olga Hospital in Stuttgart (Chief: Prof. Dr. P. Winkler).

References

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