Constrictive-Stenotic Arteriopathy in Traumatic Subarachnoid Hemorrhage

Svistov D.V., Savchuk A.N.

Chair of Neurosurgery, Medicomilitary Academy, Saint Petersburg, Russia

Introduction

Profound and detailed studies in the field of severe craniocerebral trauma, carried out during the last decade, led to marked improvement of results of treatment, characterized by reduction of mortality in leading clinics and better long-term outcomes. It has been achieved due to introduction of new highly informative diagnostic methods and the so-called aggressive intensive care [4,  9, 13]. However, the rate of unfavorable outcomes in patients with traumatic subarachnoid hemorrhage and intracranial hematomas is still very high [5, 6]. One of the factors, affecting a course and outcome of severe craniocerebral trauma, is constrictive-stenotic arteriopathy (CSA) [1, 2, 8].

Diagnostic methods, a rate and clinical significance of CSA in severe craniocerebral trauma, accompanied by subarachnoid hemorrhage, are described in medical literature rather poorly [14, 15].

Thus, a goal of the present study consisted in working out an algorithm of treatment of patients with severe craniocerebral trauma, complicated by CSA, against a background of subarachnoid hemorrhage.

Material and Methods

The study is based on results of clinical-instrumental examination of 106 cases with severe craniocerebral trauma, accompanied by traumatic SAH. We selected patients, admitted to a hospital on the 1st-3rd day after trauma. We did not include into our research cases, who died during the first three days, as well as those patients, who were admitted in more than three days after trauma. Retrospective analysis of examination results made it possible to divide all patients into two groups: casualties without CSA manifestations (group I) and those with diagnosed CSA (group II or the main group).

There was no reliable difference in sex and age indices. A number of male patients was bigger (72-76%), a mean age was 35-39 years.

Subarachnoid hemorrhage was verified with the help of CSF studies in all casualties. It was done on admission in 56 cases (52.8%) and after coping with brain compression in 50 patients (47.2%). Liquor was estimated visually; its pressure, cellular and protein composition were studied and a number of erythrocytes was counted.

Transcranial dopplerography (TCD) was a basic method of estimating cerebral circulation. Examination was carried out with TC 2-64 (EME, Germany), Angiodin (Bioss, Russia) and Sonoline Elegra (Siemens, Germany). Standard approaches and algorithms were used for location of blood flow in basal arteries [3].

CSA was diagnosed with the help of a hemispheric index of blood flow (HIBF), being a ratio between mean linear blood flow velocity in the ipsilateral MCA and an analogous parameter in the ICA's extracranial segment (HIBF = VMCA / VICA). HIBF of less than 3.0 was considered to be a normal value. CSA was spoken about, when levels of VMCA and HIBF were higher than 120 cm/s and 3.0 respectively. Kaech's classification was used for estimating a degree of MCA constriction, dependent on velocity indices [12]. The criteria were as follows: normal values of VMCA - less than 80 cm/c, nonspecific acceleration - 80-120 cm/s, moderate constriction - 120-150 cm/s, marked constriction - 150-200 cm/s, critical constriction - more than 200 cm/s.

Cerebral angiography was applied in 40 casualties (22 of them had CSA). Examination was carried out in an X-ray operating room with Polystar-II (Siemens, Germany), having the Fluorospot H system and a syringe for administration of Angiomat 6000 contrast substance. Angiograms were used for measuring a diameter of intracranial arteries (gauging). Angiographic examination was repeated in 7 cases (6.6%) with application of transluminal angioplasty. In case of detection of constricted areas in intracranial arteries and absence of contraindications, transluminal chemoangioplasty (TCA) was performed by intracarotid administration of papaverine. If it was ineffective, we used balloon angioplasty (TBA). In TCA papaverine (320 mg) was diluted in 0.9% NaCl solution (up to 150 ml). The drug was administered with an automatic syringe during 20 min. TCA was performed 18 times. When TBA was necessary, a balloon-catheter was applied. It was placed into a stenosed segment and dilated during 3-5 sec with a pressure of 0.5-1 atmospheres. A positive effect was supplemented by repeated administration of papaverine (320 mg).

CT- examination was carried out on the first day (73 patients - 69%), the second day (21 cases - 20%) and the third day (12 casualties - 11%). CT findings helped to estimate severity of traumatic SAH and to diagnose intracranial hematomas, contusion foci and blood in the ventricular system, hydrocephalus and brain edema. An amount of blood in a subarachnoid space was assessed according to Fisher C.M. [11].

Results and Discussion

CSA was diagnosed in 32 out 106 casualties. It made 30.2% out of a number of cases with diagnosed traumatic SAH. The analysis of various clinical-instrumental indices in the groups of patients showed, that biomechanics, a type of craniocerebral trauma and a character of lesions, presence and a character of accompanying pathology had no effect on CSA development.

More often it developed in patients with severe cerebral lesions. Cases with CSA had grosser disturbances of consciousness (p<0.005) on admission (Fig.1).

Severity of traumatic SAH, watched in the groups, was reliably different. It was found out, that difference in erythrocytes' amount in lumbar liquor, was statistically reliable in both groups (p<0.05). Patients, in whom this amount exceeded 100 000 in 1 mm3 during the first three days, developed CSA more often (p<0.05). The analysis of CT findings was indicative of more frequent development of CSA in massive basal traumatic SAH of the IIIrd-IVth degrees, localized in basal cisterns and lateral fissure (p<0.05). It allowed to determine a cause-and-reason relationship between traumatic SAH and CSA, verified during CT examination (Fig.2). CSA was much more frequent in cases with fractures of the skull fornix and base (p<0.05). The same phenomenon was typical of casualties with multiple intracranial lesions, including epi-, subdural and intracerebral hematomas, contusion and crush foci (p<0.05).

The analysis of outcomes of severe craniocerebral trauma in both groups revealed, that favorable and unfavorable outcomes were watched in 66 (89.2%) and 8 (10.8%) of patients without CSA respectively. As for cases with CSA, favorable and unfavorable outcomes were observed in 19 (59.4%; p<0.05) and 13 (40.6%; p<0.05) of them respectively. Thus, the rate of unfavorable outcomes of craniocerebral trauma in patients with CSA was 3.8 higher than in casualties without it (p<0.005).

According to TCD examinations, signs of CSA appeared on the 3rd-5th day. VMCA reached its maximum values on the 5-7th day after craniocerebral injury, i.e. a little bit earlier than in aneurysmal SAH. Dynamics of VMCA and HIBF in casualties of both groups is presented in Table 1.

Table 1

Dynamics of VMCA (cm/s) and HIBF in Casualties of Both Groups.

 

A Day after Severe Craniocerebral Trauma

 

1

3

5

6

7

9

11

Gr. I (n=74)
VMCA(cm/s)

50±10

88±13

100±12

90±10

75±13

65±8

60±10

Gr. I (n=74)
HIBF

1.7±0.3

1.8±0.6

2±0.3

1.3±0.2

1.4±0.4

1.6±0.5

1.7±0.2

Gr. II (n=32)
VMCA(cm/s)

43±8

92±12

136±18

157±26

152±17

130±13

96±7

Gr. II (n=32)
HIBF

1.3±0.4

3.1±0.1

3.9±0.5

4.3±0.6

4.1±0.4

3.0±0.3

2.6±0.2

 

³0.05

<0.05

<0.05

<0.05

<0.05

<0.05

<0.05

An absolute value of VMCA was considered to be the most important prognostic index. According to it there were 16 cases (50%) with moderate CSA (120-149 cm/s), 10 casualties (31%) with marked CSA (150-199 cm/s) and 6 patients (19%) with critical CSA (200 cm/s and more).

A dopplerographic picture of CSA was watched during not more than 10 days in 30 patients (96%). While comparing data of angiography and TCD, we revealed correlation between blood flow velocity indices in MCA and its caliber. Increase of linear blood flow velocity in MCA up to 170-200 cm/s in HIBF of more than 5 corresponded to an angiographic picture of marked CSA. When VMCA and HIBF were above 220 cm/s and 6 respectively, an angiographic picture was indicative of critical CSA too. Dynamics of VMCA and HIBF, dependent on a degree of MCA's constriction, diagnosed during angiographic examination, is shown in Table 2.

Table 2

Correlation between VMCA and HIBF and a Degree of Artery Constriction According to Data of Angiographic Examinations.

A Degree of Artery Constriction

VMCA(cm/s)

HIBF

< 50% (n=11)

146±24

3.5±0.9

50-75% (n=5)

185±32

4.9±1.1

> 75% (n=6)

220±39

6.8±1.3

Analyzing a clinical picture of an early period of traumatic SAH in our patients, we tried to determine factors, which would allow to prognosticate development of CSA and cerebral ischemia, conditioned by it. All casualties of group II were retrospectively divided into two subgroups in compliance with a type of a clinical course of CSA (progradient or apoplectiform) [7]. There were no clinical manifestations of secondary cerebral ischemia due to CSA in 17 casualties (53%). It allowed to distinguish the third (asymptomatic) type of a clinical course of CSA.

An asymptomatic type of a clinical course is the most favorable one. According to data of TCD, patients with this type were characterized by moderate CSA. Maximum VMCA during a follow-up period did not exceed 150 cm/s (136±12) in 16 patients. An increase of VMCA up to 165 cm/s was watched only in one case. Autoregulation was preserved or slightly impaired, overshoot coefficient (OC) was not less than 1.17 (1.21±0.01), HIBF was not more than 4.4 (3.5±0.5). Not a single patient had CSA, which involved two or more vascular regions. Repeated CT and/or MRI examinations in cases with this type of a clinical course of CSA did not show hypodense areas in a zone of blood supply of stenosed arteries.

A progradient type of a clinical course was diagnosed in 9 patients with CSA (28%). It was more severe in comparison with an asymptomatic type. According to indices of VMCA, cases with a progradient type had a clinical picture of marked CSA on the 4-8th day. Linear blood flow velocity was not more than 200 cm/s (175±13). Autoregulation was impaired, OC was not less than 1.11 (1.16±0.03). HIBF did not exceed 5.3 (4.1±0.9). CSA involved two vascular regions and affected 3-4 segments in 8 patients. Symptoms of secondary ischemia appeared on the 6th (1 case), 7th (3 cases) and 8th (5 cases) day after traumatic SAH. These symptoms included development or progression of mono- or hemiparesis, aphasic disorders, clouded consciousness. Regress of symptoms of secondary ischemia was watched on the 4th, 5th and 7th day since their onset in 5 (67%), 2 (22%) and 1 (11%) patients respectively. There were no stem symptoms. Repeated CT and/or MRI examinations, carried out on the 7th (5 cases) and 8th (4 cases) day were indicative of appearance of hypodense areas in a zone of blood supply of arteries with marked CSA, diagnosed earlier. They were classified as zones of regional ischemia (8 patients) and zones of ischemia in regions, responsible for adjacent blood supply (1 case). One patient with a progradient type of a clinical course died. A vegetative state and unfavorable outcomes were watched in 1 and 2 casualties respectively.

An apoplectiform type of a clinical course of CSA was observed in 6 patients (19%) and manifested itself in thier decompensated state. Data of TCD were indicative of critical CSA with VMCA of more than 200 cm/s (228±17). There was rapid increase of VMCA by 100 cm/s and more, watched during the 3rd-4th day after traumatic SAH. CSA manifestations were typical of both hemispheres. It involved more than 4 segments. Reactivity and autoregulation were absent (OC=1.05±0.06). Reduction of VMCA at the end of a compression test (an inverted or perverted response) was observed in 4 patients (67%). HIBF reached 8 (6.8±1.2).

One could watch clinical manifestations of secondary ischemia on the 6-7th day. First and foremost it was characterized by stem lesions, i.e. deep coma, mioses turning into mydriasis, inhibited light reflex, divergent squint along the vertical line, decerebrate rigidity, tachy- or bradycardia, arterial hyper-or hypotension, central disorders of breathing. Repeated CT and/or MRI examinations of all 6 cases demonstrated, that zones of secondary ischemia were present not only in regions of blood supply of arteries with critical CSA and areas of adjacent blood supply, but also in stem structures. Severe invalidism and fatal outcomes were watched in 1 and 5 cases respectively.

Table 3, based on CT data, illustrates correlation between three types of a clinical course and severity of traumatic SAH. Table 4, compiled on the basis of dopplerographic results, reflects correlation between types of a clinical course and severity of CSA.

Table 3

Correlation between Severity of Traumatic SAH and Versions of a Clinical Course of CSA.

Severity of Traumatic SAH

A Type of Its Course

 

Asymptomatic

Progradient

Apoplectiform

I (n=1)

1

-

-

II (n=2)

2

-

-

III-IV (n=29)

14 (82%)

9 (100%)

6 (100%)

Table 4

Correlation between Severity and Versions of a Clinical Course of CSA According to Data of Dopplerographic Examinations.

A degree of CSA

A Type of Its Course

 

Asymptomatic

Progradient

Apoplectiform

Moderate

16

1

-

Marked

1

8

-

Critical

-

-

6

Clinical manifestations of CSA developed on the 5-8th day after craniocerebral trauma and traumatic SAH. They were in compliance with symptoms of ischemia in the region of large cerebral and perforating arteries, participating in blood supply of the stem and subcortical structures of the brain. Taking into account that dopplerographic signs, indicative of constriction of arterial lumens, take the lead over clinical manifestations of CSA, one can state, that TCD is an effective method of diagnosis and prognostication of a CSA course in traumatic SAH. Monitoring of an individual course of CSA in each patient helps to take timely measures, aimed at optimization of cerebral perfusion before development of secondary ischemia. From this point of view it is inadmissible to use TCD only for diagnosis of CSA as a cause of cerebral ischemia. This modality should be applied for prognostication of its development and course. It demands carrying out dynamic examinations, beginning with the very first day. It should be noted, that information on blood flow in both MCA and ICA, registered on the neck, is quite sufficient for verification of CSA. It can be done by trained paramedical personnel, in particular anesthetists, who know how to operate monitoring systems perfectly well.

Severity of signs of secondary ischemia was dependent on a degree of its spread and localization of constricted cerebral vessels, diagnosed with the help of TCD. They varied from mild, transient up to gross focal symptoms, accompanied by common cerebral disorders. In case of critical bilateral CSA secondary ischemia was characterized by both focal and marked common cerebral disorders. It was conditioned by involvement of perforating arteries.

Dynamic CT and/or MRI examinations, carried out in casualties with a progradient type of a clinical course on the 7-8th day, demonstrated areas of secondary ischemia in regions of arteries, affected by CSA, and zones of adjacent blood circulation. The same findings were typical of cases with an apoplectiform type of a clinical course, but at the same time there were areas of secondary ischemia in stem structures, caused by spread of CSA on short branches of cerebral arteries.

Dymnamics of VMCA changes within the 3rd-5th day after traumatic SAH can be used for prognostication of a further course of CSA, development and outcome of secondary ischemia, conditioned by it. As for development and outcome of this ischemia, rapid increase of VMCA (by 100 cm/s during 72 hours) in both carotid regions within the 3rd-5th day after traumatic SAH, as well as disappearance of reactivity and autoregulation, were unfavorable prognostic signs. This fact reflects similarity of manifestations of CSA in traumatic and aneurysmal SAH. CSA does not result in a fatal ischemic lesion in all cases, but it is sure to aggravate severity of a course and duration of an acute period of severe craniocerebral trauma.

We studied possibility of applying transluminal angioplasty for correction of symptomatic CSA, watched in traumatic SAH. There were 7 patients; 4 of them had a progradient type of a clinical course of marked CSA; an apoplectiform type of critical CSA was present in 3 cases. Symptoms of secondary cerebral ischemia, conditioned by CSA, appeared on the 6th, 7th and 8th day after traumatic SAH in 3 (43%), 3 (43%) and 1(14%) patients respectively.

Transluminal angioplasty was effective in 5 out of 7 casualties with symptoms of secondary ischemia. Poor results of this procedure (no regress of neurologic symptoms) were conditioned by its late application, development of irreversible ischemic changes of the brain substance, impaired blood supply mainly in the region of perforating arteries.

Transluminal balloon angioplasty was used by us in segmental constriction of basal arteries. As for chemoangioplasty with papaverine, it was applied as the first stage of intervention treatment or in diffuse CSA. Chemoangioplasty allowed to increase a diameter of constricted segments by 20-30%, but a dopplerographic picture of CSA was watched again in all patients in a day after the procedure. It became a cause of repeated chemoangioplasty (2-4 procedures). Dynamics of indices of cerebral blood flow after chemoangioplasty is demonstrated in Table 5 and (Fig.3). Transcranial balloon angioplasty made it possible to normalize a caliber of arteries, affected by CSA. It gave a stable result and there was no need of repeated manipulations (Fig.4), (Fig.5).

Table 5

Dynamics of Mean Indices of Blood Flow in Performing TCA According to Data of TCD-Examinations.

 

Before TCA

After TCA

VMCA (cm/s)

175±15

131±12

VICA (cm/s)

33±4

52±6

OC

1.08±0.05

1.19±0.02

HIBF

4.4±0.5

2.5±0.4

The obtained data allowed to propose an algorithm of diagnostic and therapeutic measures in CSA, caused by traumatic SAH (Fig.6).

When consciousness disturbances in craniocerebral trauma are characterized by the score of 12 and less (Glasgow Coma Score), CT of the brain is indicated. If there are signs of basal traumatic SAH, TCD screening should be carried out from the very first day. As for the rest patients, TCD examination is carried out on the 5-7th day in order either to confirm absence of CSA or to diagnose this pathology (approximately in 3% of cases). Patients with CT-positive traumatic SAH are subject to prevention of CSA with the help of drugs. Cases with dopplerographic signs of CSA are classified in compliance with a level of VMCA. A risk of secondary ischemia is maximum in casualties with the IInd-IVth degree of traumatic SAH according to Fisher and marked and critical CSA according to data of TCD. In case of developing symptoms of secondary ischemia and inefficacy of conservative measures angiography, combined with transluminal angioplasty, is used. Absence of regress of neurologic symptoms and angiographic manifestations of CSA is the basis for performing transluminal balloon angioplasty.

Conclusions

  1. CSA develops in 1/3 of patients with traumatic SAH and is complicated by a secondary ischemic lesion of the brain in a half of cases with CT-verified basal SAH.
  2. Growth of linear blood flow velocity in cerebral arteries, indicative of constriction of their lumen, is registered on the 3rd-5th day after traumatic SAH and reaches its maximum by the 5-7th day. As a rule, clinical manifestations of CSA develop on the 7-9th day after traumatic SAH. Dopplerographic signs of CSA appear 3-4 days earlier, than clinical manifestations of secondary cerebral ischemia.
  3. In case of development of marked and critical CSA with a progradient or apoplectiform course, it is possible to use transluminal chemoangioplasty, based on selective administration of myotropic antispasmodics. If it ineffective, transluminal balloon angioplasty is performed.

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