CRANIOCEREBRAL DISPROPORTION IN CHILDREN WITH TRAUMATIC BRAIN INJURY

CRANIOCEREBRAL DISPROPORTION IN CHILDREN WITH TRAUMATIC BRAIN INJURY

Larkin V.I., Koval R.P., Novokshonov A.V., Dolzhenko D.A.

Omsk State Medical University,
City Pediatric Clinical Hospital No.3, Omsk, Russia,
Regional Clinical Center of Miners’ Health Protection, Leninsk-Kuznetsky, Russia,
Regional Clinical Hospital, Barnaul, Russia

The problem of traumatic brain injury (TBI) is still significant. Cranial and cerebral injuries are most common in children (30-50 %) [1, 2]. Moreover, severe pediatric TBI is 4-20 % [1, 3]. The mass effect (ME) of TBI is the cause of disorder of intracranial volumetric relationships with development of craniocerebral disproportion [4]. The first response to appearance and expansion of additional “traumatic” volume is the use of reserved elasticity of the medullary substance and free spaces inside the brainpan.
The specific mildness and dynamicity of manifestation of the signs of focal cerebral lesion, tendency to generalized cerebral reactions and rapid change in clinical conditions are often the basis for diagnostic difficulties.
Currently, there is a differential approach to surgical treatment of brain compression. One should prefer the active surgical management for recovery of cerebral tissue functioning [5, 6]. One of the existing reserves of decreasing mortality and improving outcomes of surgical treatment of severe TBI with brain compression is conduction of surgical intervention before development of dislocation syndrome or at least at the initial phases [7, 8]. V.V. Krylov et al. determined the maximal volume of non-operated meningeal hematomas with favorable outcomes [8].
In the current study we made the following tasks: determination of individual craniometrical data of a child (the volume of cranial cavity, brain volume, the volume of reserve liquor spaces), ME in different types of injuries, estimation of dependence of clinical manifestations of traumatic brain injury on the ME degree in children.
The objective of the study – to develop the way of the calculation of the optimum volume of decompressive trepanation of the skull in children with different mass-effect of the trauma with consideration of the individual craniometrical parameters.

MATERIALS AND METHODS

The features of the syndrome of acute craniocerebral disproportion (CCD) were investigated in Omsk diagnostic center. The main intracranial components were investigated with CT-morphometry in 182 children with TBI of various severity (the age from 3 months to 15 years).
The inclusion criteria were the following: children at the age of 1-15 years with dense bones of the cranial vault and absent opened fontanels, ossification defects and posttrepanation defects; presence of middle or severe TBI; acute course of the process (up to 72 hours after injury); presence of intracranial traumatic focus, traumatic structural disorders of cranial bones, signs of cerebral edema; written informed consent from the children’s parents.
The exclusion criteria were intracranial hematoma in the postcranial fossa; presence of a concurrent nervous system disease influencing on the clinical manifestation of TBI (organic lesion and cerebral malformations).
CT-morphometry was used for investigation of the intracranial relationships in five subgroups: 115 children with mild TBI, 14 children with middle or severe TBI, 12 children with severe brain contusions, 6 children with intracranial hematoma. The recurrent measurements allowed clarifying the total changes in the brain volume and its perfusion over time. The dependence of clinical manifestations of TBI on ME intensity was examined in 35 children with single middle-severe and severe TBI in the groups IA, IB, IC, ID. Surgical interventions were conducted in 32 cases.
All children received the clinical and neurological examination: estimation of consciousness (with GCS), brainstem and hemispheric symptoms, vital functions. CT-morphometry was used for measuring the cranial cavity volume (the total volume of all intracranial components), the cerebrospinal fluid volume and the liquor-cranial index (LCI). Realization of recurrent measurements allowed clarifying the total changes in the volume of the brain and its perfusion over time.
The statistical analysis was conducted with NCSS 2004, STATISTICA 6, MS Excel 2007. The incidence of the clinical symptoms was investigated with chi-square test with Yates correction for little groups and Student’s test. The statistical significance of the clinical efficiency of treatment was estimated with non-parametrical Wilcoxon’s test and Mann-Whitney test. The analysis of the clinical efficiency of the offered technique was conducted according to Sacket D.L.

RESULTS

The sum mass effect of injury in children with mild traumatic brain injury

The group 1 included 115 children (41 girls and 74 boys) with the clinical manifestations of mild traumatic brain injury who were included into the comparison group [9]. CT did not identify any traumatic changes in this group. It corresponded to the literature data (Kornienko V.N., 1997).
The results of CT-morphometry allow concluding that the volume of liquor spaces in children with normal conditions is determined with the parameters of physical development and gender. The volume of the cranial cavity was measured according to the head circumference (the table 1). The mean parameters of the brain were estimated in the different age groups (the table 2). The volume of the brain increases with age, with the highest increase during the first year of child’s life. The normal LCI varies within 1.73 ± 0.6 % to 2.7 ± 0.72 %. The morphometric findings were accepted as the normal rate.

Table 1. The  dependence of the skull volume on its circumference

Head circumference (cm)

Number of observed cases (n)

Mean volume of skull М ± m (cm3)
1 2 3
65 1 2586
60 2 1841 ± 148
59 2 1672 ± 140
58 6 1591 ± 142
57 9 1558 ± 198
56 16 1354 ± 109
55 15 1323 ± 124
54 25 1388 ± 149
53 21 1250 ± 116
52 30 1278 ± 114
51 20 1112 ± 99
50 12 1091 ± 67
49 20 1054 ± 86
48 6 1063 ± 97
47 13 951 ± 108
46 2 871 ± 119
45 6 882 ± 138
44 7 852 ± 68
43 4 835 ± 105
42 3 699 ± 19
41 3 724 ± 82
40 5 602 ± 62
36 3 432 ± 58

Table 2. The size of the  brain of the  children according CT data

Age of children

 Brain volume М ± m (cm3)

1

 2

up to 1 month
n = 2

  421.1 ± 44.23

1-3 months
n = 4

  579.3 ± 51.57

4-6 months
n = 6

  794.7 ± 54.25

7-9 months
n = 2

  884.2 ± 117.34

10-12 months
n = 3

  990.8 ± 55.63

2 years
n = 7

 1034.4 ± 56.67

3 years
n = 6

 1102.8 ± 45.71

4 years
n = 5

 1122.2 ± 78.16

5 years
n = 7

 1145.5 ± 164.33

6 years
n = 10

 1172.1 ± 191.22

7 years
n = 11

 1178.6 ± 193.92

8 years
n = 12

 1185.4 ± 127.51

9 years
n = 8

 1189.3 ± 146.43

10 years
n = 9

 1194.3 ± 136.17

11 years
n = 10

 1213.8 ± 98.12

12 years
n = 10

 1219.9 ± 74.73

13 years
n = 5

 1236.6 ± 65.87

14 years
n = 12

 1281.3 ± 139.22

N = 129

  

The total mass effect of injury in children with middle-severe traumatic brain injury

The second group included 14 patients with the clinical forms of contusion with mild or middle severity. CT identified the contusion foci of the type 1-3, with the type 2 as the most common foci of contusion; their features were absence of tomodensitometric signs of rude destructive changes and signs of diffuse lesion of the brain in view of moderate increase or decrease in density (4-6 HU) of the meningeal substance. The mass effect of the middle-severe injury was insignificant (2.5 ± 1.3 %) and was similar with the volume of reserve liquor spaces.

The total mass effect of injury in children with severe traumatic brain injury

The group 3 included 12 children with clinical manifestations of severe cerebral contusion with absence of intracranial hematoma at the moment of the examination. The foci of hemorrhagic contusions of the types 3-4 were complicated by perifocal or lobar edema with tendency to increasing on the days 3-10. It manifested itself as the decrease in the density in the perifocal region of contusion (about 18 HU), edema transforming to lobar form or extension to two subjacent lobes with increase in the volumetric effect. Besides the total narrowing of the ventricular system, we identified other signs of decrease in reserve intracranial spaces. The clinical course and outcomes were favorable in this group. The mass effect of severe TBI was significant (13 ± 9.1 %).

The total mass effect of injury in children with intracranial hematoma

In many studied cases the patients with severe TBI had the evident signs of intracranial hematoma at the moment of admission to the neurosurgery unit. They received the emergency surgery within the first hour. ME of intracranial hematomas was 10.7 ± 4 %. A small hematoma can be a hematoma with ME, which could be compensated by individual reserve spaces of the craniocerebral system in a certain child. Therefore, the mass effect increases with increasing severity of TBI (the table 3).

Table 3. The data of  mass-effect of TBI of various severity

Patients

LKI-1

LKI-2

 (V1-V2) (см³)

M-effect (%)

Mild TBI

 - - - -

Middle severity TBI

 2.1 ± 1.03 1.75 ± 0.85 26.4 ± 14.9 2.5 ± 1.32

Intracranial hematoma

 2.5 ± 0.42 5.2 ± 0.38 106.5 ± 22.72 10.7 ± 4.31

Severe TBI

 3.9 ± 0.81 4.9 ± 3.13 162 ± 98.46  13 ± 9.13
ANOVA p = 0.113 p = 0.093 p = 0.003 p = 0.002

The clinical manifestations of traumatic brain injury

The clinical manifestations of TBI with mass effect < 5 %

7 boys and 4 girls were included into the subgroup IA during dynamic CT examination. The total ME of the injury was 0.3-3.9 %.
The clinical manifestations were characterized by the compensated course and were estimated according to GCS > 8 in 10 cases. There were some mild stem and pyramid symptoms with the manifestations in view of horizontal nystagmus, moderate sunsetting, asymmetry of deep reflexes, Babinski's symptom, absent disorders of vital function and absent dislocation of the midline structures of the brain. CT examination identified some signs of diffuse lesion of the brain such as moderate increase or decrease in density of the meningeal substance. The volume of hematomas was 2-10 cm3.
The surgical treatment consisted in removal of hematoma through the cutting hole and the surgical preparation of a depressed fracture.

The clinical manifestations of TBI with mass effect of 5-12 %

The subgroup IB included 7 boys and 2 girls. The total ME was 5.1-10.8 %.
The clinical picture manifested itself as the moderate and rude decompensated course of the injury estimated with GCS from 8 to 3 points in 7 cases. The moderate stem and pyramid symptoms were in view of absence of the corneal reflexes, sunsetting, Hertwig-Magendie symptom, presence of the pathological foot signs, appearance of Bogolepov’s symptom. The tendency to bradycardia and hypotension was determined by the presence of dislocation of the midline structures of the brain in all patients in this subgroup. The CT examination identified the contusion foci of the types 1 and 2, intracranial hematomas of various location (30-136 cm3), the signs of cerebral edema.
The surgical technique was determined by the phase of the clinical course of the injury. The moderate decompensated course was treated with bone plastic trepanation, the rude decompensated course – 8 decompressive trepanations.

The clinical manifestations of TBI with mass effect of 12-20 %

The subgroup IC included 3 boys and 5 girls. ME was 12.5-19.9 %.
The clinical picture showed the decompensated course of the injury with GCS = 3-8 in 7 cases (coma 1, 2), presence of rude signs of dislocation of the stem structures of the brain with manifestations in view of absent corneal reflexes, Hertwig-Magendie symptom, paresis, the pathological foot signs, bradycardia, increasing arterial pressure. The absence of increasing transverse displacement of the midline structures of the brain was determined by appearance of the signs of axial dislocation. The CT examination identified the contusion foci of the types 2 and 3 with massive hemorrhagic contusions of the types 3 and 4 appearing by the mechanism of countercoup. The volume of hematomas was 84-166 cm3.
The surgical technique consisted in unilateral decompressive skull trepanation in 6 patients and bilateral one in 2 patients.

The clinical manifestations of TBI with mass effect > 20 %

The subgroup ID included 4 boys and 3 girls. ME was 20.3-37.4 %.
The clinical manifestations were the rude decompensated course and the terminal phase (GCS = 4-3). The consciousness level varied from sopor to coma III. There were some rude stem (absence of corneal reflexes, Hertwig-Magendie syndrome, uni- or bilateral mydriasis) and semispheric (rude paresis, pathologic foot signs) symptoms, disordered vital functions (tachycardia and hypotension, pathologic breathing). The absence of displacement in the midline structures of the brain did not allow even indirect estimating the sizes of the pathologic processes. The CT examination showed the dominance of the contusion foci of the types 4 and 5, the intracranial hematomas of various location (the mean volume of 22-120 cm3), lobar or diffuse edema. The main treatment technique was bilateral decompressive trepanation in 4 and unilateral one in 3 patients.

The comparative estimation of the clinical manifestations of TBI in the subgroups IA, IB, IC and ID

The intensity of ME of the injury was the determining parameter of the disease course, methods and results of the treatment and outcomes of TBI. The intensity and the expression of the general cerebral syndrome were characterized by the quantitative estimation with GCS: the lower amount of points, the higher injury ME.

Figure 1. The rate of symptoms of brain stem lesion in patients with different mass-effect of injury

Figure 1


The injury ME with 12 % was associated with absence of clear consciousness. The presence of coma testifies the increase in ME exceeding 12 %. Coma III indicates ME > 20 %.
The moderate sunsetting indicated ME < 12 %, but the combination of Hertwig-Magendie symptom and absent corneal reflexes – ME > 12 %. The presence of paresis, Bogolepov and Babinski symptoms are common for ME > 12 %. Spasms are the sign of intracranial hemorrhage. Hypotension and concurrent bradycardia show the increase in ME > 5 %. The disorder of vital functions (bradycardia and hypotension) testify ME > 5 %. Therefore, the statistically significant (p < 0.05) symptoms of the increase in the volume of the intracranial components were absence of corneal reflexes, Parino symptom, Hertwig-Magendie symptom, Bogolepov’s symptom, Babinski’s symptom, bradycardia, pathological breathing, spasms.
The mathematical models have been created. These models are used for estimation of the intracranial components (the brain, cerebrospinal fluid, cranial cavity) in dependence on the craniometrical parameters (head circumference, cranial and longitudinal diameter of the skull) (the table 4).

Table 4. The relationships between volumes of the intracranial components and the craniometric parameters (linear regression analysis)

Calcuated value

Calculation technique

Designations

Cranial cavity volume

 V1 = (L – 21.71)*38.43 V1 – cranial cavity volume, cm3

Volume of cerebrospinal fluid

 V2 = (L – 41.08)*2.08 V2 – volume of cerebrospinal fluid, cm3

Brain volume

 V3 = 36.35*L-748.84. V3 – brain volume, cm3

Head circumference

 L = 2.08A + 1.26B + 1.58 L – head circumference, cm
    А – longitudinal internal cranial diameter, cm
    В – transverse internal cranial diameter, cm

The developed formulae were used for calculation of the necessary size of uni- or bilateral decompressive trepanation, which allows creating the necessary reserve space in estimation of ME.
The size of trepanation was calculated with dependence on the longitudinal and transverse diameters of the head measured in CT examination. The multiple linear regression analysis was conducted. The head circumference L (cm) was considered as the dependent variable.
The independent variables were:

1. The longitudinal diameter of the head A (cm) measured in the CT examination (p < 0.00001).
2. The transverse diameter B (cm) measured in the CT examination (p < 0.00001).
The diameter of the trepanation hole was determined with the degree of the injury mass effect and with the individual craniometric parameters with use of the formulae:                                                               

 D1 = 2 ((5.8L – 119.2) × W)1/2, D2 = 2 ((2.9L – 59.6) × W)1/2

D1 – the diameter of the trepanation hole for unilateral trepanation, cm; D2 – the diameter of the trepanation hole for bilateral trepanation, cm; L – the head circumference, cm; A – the longitudinal internal diameter of the head, cm; B – the transverse internal diameter of the head, cm; W – the value of mass effect %.

Figure 2. For the same ME of injury, the volume of trepanation increases with the increase in longitudinal and transverse cranial diameters and, as result, head circumference

Figure 2


DISCUSSION

The intensity of injury ME was the parameter of TBI, which determines the course, and results of the treatment.
For ME < 5 % it is appropriate to perform the conservative treatment. The requirement for the surgical intervention appears in a life threatening injury (a depressed fracture, increasing intracranial hematoma, the clinical picture of increasing compression of the brain etc.) and the high probability of increasing ME of the injury. Intracranial hematoma is removed by means of the low invasive surgical interventions. For a fracture it is sufficiently to use the surgical preparation and removal of an intracranial traumatic mass without use of extensive decompressive trepanation. The approach highly depends on the individual features of the patient, particularly, the individual volume of reserve spaces.
For ME > 5 %, the danger of irreversible cerebral changes is possible, but the removal of pathologic components of the craniocerebral system or increase in its capacity is indicated regardless of the individual craniometrical parameters. Bone plastic trepanation with obligatory dura mater plastics is possible in the compensated condition and absent tendency to increasing ME. In case of increasing ME it is necessary to perform the surgery with decompressive orientation.
The surgical technique for an injury with ME > 12 % includes uni- or bilateral decompressive trepanation with formation of the trepanation hole (holes) of the optimal size.

Figure 3
a) acute period of severe TBI with evident traumatic edema, ME 15 %; b) trepanation volume corresponds to the calculated value; c) outcome of  surgical treatment – edema  regression

Figure 3


The main technique for treating TBI with ME > 20 % is bilateral decompressive trepanation with sizes of the holes which are equal or exceeding the calculated sizes. The use of all available curative techniques with extensive decompressive trepanation does not warrant a favorable outcome.
The size of decompressive trepanation as the main operation favoring the removal of craniocerebral disproportion in increasing intracranial pressure for improving the functional state of the brain is usually calculated empirically and is conducted without consideration of ME of an injury or the individual craniometrical parameters.
The concept of craniocerebral disproportion, which was implemented into the neurosurgery department in 1999, allowed achieving the significant decrease in the mortality after severe TBI in 289 children.
The concept is still actual in the modern conditions of the use of the transducers for measuring ICP. In actual practice, with the decompensated condition of the patient, one can observe the time lacking during installation of ICP transducer. The close neurological examination with estimating the consciousness (GCS), the stem and hemispheric symptoms and vital disorders can help to make a decision.
Decompressive trepanation increases the volume of cranial cavity and prevents or decreases the impaction of the secondary injuring factors, i.e. it is the main curative technique for severe traumatic brain injury in children. The use of the developed technique for choice of trepanation sizes on the basis of a degree of injury ME and the individual craniometrical parameters improves the outcomes of surgical treatment of traumatic brain injury.

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