Do Traumatic Brain Contusions Increase in Size after Decompressive Craniectomy?

Abstract

Hemorrhagic contusions (HC) represent a common consequence of traumatic brain injury (TBI) and usually evolve during the first 12 h after trauma. The relationship between decompressive craniectomy (DC) and evolution of the post-traumatic HC is still unclear. The aim of the present study was to evaluate the impact of DC on HC evolution. Fifty-seven patients with the evidence of at least one HC at admission CT scan were analyzed. Twenty-five patients (Group 1) underwent DC and 32 patients underwent medical therapy alone (Group 2). Fisher's exact test was used to compare categorical variables. Logistic regression model was used to assess the independent contribution of predictive factors (age, ≤50 years; treatment received, DC vs. medical; anticoagulant/antiplatelet drugs intake; Rotterdam CT score, 1–3 vs. 4–6) to the evolution/new appearance of an HC. A significant increase (≥2 cc) of any HC during the observation period was detected in 8 patients (14%): 4/25 patients (16%) of Group 1 and 4/32 patients (12.5%) of Group 2 (Fisher exact test two-sided p=0.72). Univariate and multivariate analyses showed that none of the analyzed factors was associated with increased or de novo appearance of any HC. DC does not seem to constitute a risk factor for the evolution of HC.

Introduction

H emorrhagic contusions (HC) represent a common consequence of traumatic brain injury (TBI). A retrospective series of serial CT scan studies of patients with TBI has found that the expansion of HC is inherent in the injury process, and usually occurs within the first 12 h after injury.¹ The outcome of patients with TBI is also influenced by the presence of post-traumatic HC and their possible increase during the days following trauma.^1,2 In the series by Chang et al., 86 out of 229 (38%) initially unoperated patients with TBI showed an HC increasing from the first to the second head CTscan.³ Other authors reported a post-traumatic increase of HC in a higher percentage of cases (ranging from 42% to 59%), especially within the first 6–12 h post-injury.^1,4,5

Decompressive craniectomy (DC) can be a lifesaving procedure to relieve critically increased, not otherwise controllable, intracranial pressure (ICP) in patients with TBI. However, the relationship between DC and evolution of post-traumatic HC is still unclear. In 2003, Zweckberger et al. studied the influence of craniotomy on ICP, contusion volume, and functional outcome in a model of traumatic brain injury in mouse. They found that 24 h after trauma, the contusion volume was 40% smaller in craniotomized mice than in controls.⁶ On the other hand, in several clinical series, the rate of HC increasing after DC ranged from 5% to 6%^7
–9 to 16%.¹⁰ In contrast, Flint et al. found a very high incidence (58% of cases) of new or expanded HC following DC, explaining those findings with the loss of a “tamponade effect” after bone removal.¹¹ Moreover, these authors correlated the increase in volume of post-traumatic HC after DC with a higher mortality. No further studies have been published to date to explore if the evolution of a HC is a common consequence of surgery or if it is part of the natural history of the brain contusion, especially during the first 6–12 h after trauma. In view of these considerations, the timing of both radiological investigations and surgery seem to be important issues.

The aim of the present study was to evaluate the impact of DC on HC evolution.

Methods

Patient population and management

From January 2010 to June 2011, 164 adults with severe (Glasgow Coma Score [GCS] ≤8) closed head injury were admitted to our center. For the purposes of this study, we only included 57 patients with the evidence of at least one HC on admission CT scan.

Patients were initially admitted to the Intensive Care Unit and were treated according to the guidelines for the management of severe brain injury.^12,13 Medical management included intubation, ventilation, oxygenation, 30 degree head elevation, fluid resuscitation, sedation (propofol 2–5 mg/kg/h, remifentanyl 0.1–0.2 μg/kg/min), mild hyperventilation (pCO² 30–33 mm Hg), normothermia (36–36.5°C), and normoglycemia. Osmotherapy with mannitol (1–2 g/kg/daily) and hypertonic saline solution administration were the next step.

Of the 57 patients analyzed in this study, 21 underwent DC immediately after the admission CT scan (because of diffuse brain swelling associated with rapid clinical deterioration, massive brain swelling with obliteration of the subarachnoid spaces especially in the basal cisterns, and uncal herniation), and 4 underwent DC within 6–12 h after trauma (because of uncontrollable intracranial hypertension – ICP>20 mmHg – despite maximal medical therapy) (Group 1). Early signs of brainstem injury, such as bilaterally fixed and dilated pupils, were contraindications to DC. The remaining 32 patients underwent medical therapy alone (Group 2). An intraventricular catheter for ICP monitoring was placed in 36 patients after admission, including patients belonging to Group 2 and the 4 patients who underwent DC within 6–12 h after trauma. Controlled ventricular drainage was used, when possible, as second-line treatment when maximal medical management was not able to control ICP elevation.

DC was performed as we described in a previous article,¹⁴ through the removal of the fronto-temporo-parietal calvarium until the level of the zygoma, and expansive duroplasty. A subdural catheter for postoperative ICP monitoring was placed in all patients.

Neuroradiological monitoring and radiological assessment

According to our institutional protocol, all patients underwent a head CT scan every 6–12 h during the first day after trauma, then every 24–48 h. The four patients who underwent DC within 6–12 h after trauma underwent a head CT scan immediately before surgery.

All available CT scan studies on an “electronic picture archiving and communication system” (PACS) were analyzed. Particularly, we focused on: 1) the admission CT scan (or the last preoperative CT scan for the four patients who underwent DC after initial failure of medical therapy) (time zero), 2) the 12–24 h CT scan (time one), and 3) a late CT scan performed from 4 to 6 days after trauma (time two). CT scans were independently analyzed by two neuroradiologists and the average of the relative measurements was calculated. CT scans were compared with each other and the difference in volume of HC was recorded during the three different stages. In addition to the main HC, any further smaller HC was also measured, and its evolution along the observation span was compared.

The volume of the brain contusion was measured on axial nonenhanced CT images. All hemorrhagic foci volumes were estimated by drawing regions of interest (ROIs) around the boundary of each lesion using the MRIcroN v1.0 software (Rorden, 2008; http://www.mricro.com). Boundaries of contusions only included the volume of frank hemorrhage, not the surrounding edema. The areas of hemorrhagic increased attenuation were assessed using the same window parameters for each patient (width, 76; level, 35) and the resulting ROIs areas were multiplied by the section thickness plus gap and summed together to estimate the total volume. Contusion volume was considered significantly increased if an enlargement ≥2 cc was measured at postoperative CT scans. Rotterdam CT score was finally calculated.

Statistical analysis

The statistical package used for analyses was SPSS for Windows Version 13.0. Means were compared using one-way ANOVA. Fisher's exact test was used to compare categorical variables. Logistic regression model was used to assess the independent contribution of predictive factors (age ≤50 years; treatment received, DC vs. medical; anticoagulant/antiplatelet drugs intake; Rotterdam CT score, 1–3 vs. 4–6) to the evolution/new appearance of an HC. Variables with p values<0.05 were considered statistically significant.

Results

There were 38 men and 19 women (mean age 45.9±21.5 years, age range: 16–87 years). For patients who underwent DC, the mean anteroposterior diameter of the bone flap was 15 cm (range 14–16.5 cm) and the mean area of hemicraniectomy was 168 cm² (range 145–220 cm²). Median Rotterdam score was 3 both for Group 1 and for Group 2.

In Group 1, the mean volume of the main HC at diagnosis was 12.6±17 cc, ranging from 0.4 to 66 cc. In Group 2, the mean volume of the main HC at diagnosis was 7.3±11 cc, ranging from 0.4 to 36.5 cc (p=0.16). At least another secondary HC was present in 9/25 patients (36%) of Group 1 and in 17/32 patients (53%) of Group 2.

Overall, there was no significant modification of the mean volume of main HC, both for Group 1 (time zero: 12.6±17 cc, time one: 11.9±16 cc, time two: 11.1±15.4 cc, p=1) and for Group 2 (time zero: 7.3±11 cc, time one: 7.2±9.3, time two: 6.2±8.9 cc, p=1).

Overall, a significant increase (≥2 cc) of any HC (ranging from 2.5 to 22 cc) during the observation period was detected in eight patients (14%). None of these patients required surgical treatment of the HC. In particular, a significant increase of any HC was present in 4/25 patients (16%) of Group 1 and 4/32 patients (12.5%) of Group 2 (Fisher exact test two-sided p=0.72). Univariate analysis also showed that the presence of antiplatelet/anticoagulant drugs intake, age, and Rotterdam CT score were not significantly correlated with the evolution of any HC.

Logistic regression analysis confirmed that none of the analyzed factors was independently associated with increased or de novo appearance of any HC (Table 1).

Table 1.

Logistic Regression Analysis Showing that None Among the Analyzed Factors was Independently Associated with Evolution of Any HC

			95% CI for HR
Factor	Sig.	HR	Lower	Upper
Age (<50 vs, ≥50 years)	0.627	1.567	0.256	9.575
Treatment (Group 1 vs, Group 2)	0.792	1.286	0.198	8.373
Antiplatelet/anticoagulant drugs intake	0.690	1.503	0.203	11.116
Rotterdam CT score 1–3 vs 4–6	0.458	0.507	0.084	3.043

HC, hemorrhagic contusions; HR,

Discussion

Several investigators previously found that post-traumatic HC may spontaneously increase in size during the first hours after TBI.^15

–20 Potential risk factors for HC evolution include abnormalities in coagulation, ethanol intoxication, body temperature (both hypothermia and hyperthermia may potentially influence the coagulation), post-injury hypotension and hypoxia.⁵ Delayed development (within few days) of HC after DC has also been reported after TBI.^21

–24 Moreover, other authors found that the presence of associated subarachnoid hemorrhage and large size of the HC on admission are powerful predictors of HC evolution.^3,4,25 Nonetheless, the relationship between DC and HC evolution is not yet elucidated. Few studies revealed that the patients who underwent craniotomy for evacuation of a traumatic intracranial mass may develop a second hematoma at the operation site¹⁵ or in contralateral hemisphere.²⁶ Bullock et al. found an incidence of ∼7% of postoperative hematomas that required a second operation,¹⁵ although most of them were located in the extradural compartment. Yang et al. reported that 7.4% of patients who underwent DC for TBI presented the appearance of an HC contralateral to DC.²⁶ It is important not to confuse the contusion evolution with the presence of hemorrhagic infarction at the bone edges of the decompression, caused by herniation of the swollen hemisphere through the craniectomy defect with kinking of the cerebral veins and laceration of the cerebral cortex.^26,27 This is particularly true in cases of too small decompression.²⁶ The influence of DC on development and evolution of HC was also emphasized by Flint et al.¹¹ These authors discussed the incidence and the clinical significance of new or expanding HC following DC. Comparing pre- and postoperative head CT scans, they found that new or expanded HC of ≥5 cc were observed after DC in 25/40 patients (62%), more frequently in the ipsilateral hemisphere (81.5%). They also found that the severity of findings on first CT scan, as measured by the Rotterdam Score, was associated with the risk of postoperative HC evolution.¹¹ In our series, we observed significant new or expanded contusions in the minority of cases: in 16% of patients who underwent DC and in 12.5% of patients who did not undergo DC. Moreover, we preferred to use a smaller cutoff to define a significant increase of HC (2 cc compared with 5 cc in the Flint series). It is interesting to underline that this percentage is much lower than that (38–59%) reported by other authors who analyzed the natural history of post-traumatic contusions in patients who did not undergo DC,^1,3
–5 and is comparable to other published series of patients who underwent DC (5–16%).^7

–10

In our series, we observed that none of the analyzed factors (age, therapy [medical alone vs. DC], anticoagulant/antiplatelet drugs intake, or Rotterdam score) was significantly associated with increased postoperative contusion at logistic regression analysis.

Our retrospective study presents several potential sources of bias. Only a prospective controlled trial of DC in TBI would definitely be able to ascertain whether DC itself may increase the risk of expanding contusions. Finally, we acknowledge that the total number of patients is limited, although it is comparable to most neurosurgical series published of this topic.^7,10,11

Conclusion

In conclusion our results show that expanding HCs are not common in patients undergoing DC. Moreover, no statistically significant risk factors associated with HC expansion were identified in this series.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

References

Servadei

, Nanni

, Nasi

M.T.

, Zappi

, Vergoni

, Giuliani

, Arista

1995. Evolving brain lesions in the first 12 hours after head injury: analysis of 37 comatose patients. Neurosurgery, 37:899–906.

Bullock

, Golek

, Blake

. 1989. Traumatic intracerebral hematoma - which patients should undergo surgical evacuation? CT scan features and ICP monitoring as a basis for decision making. Surg. Neurol., 32:181–187.

Chang

E.F.

, Meeker

, Holland

M.C.

2007. Acute traumatic intraparenchymal hemorrhage: risk factors for progression in the early post-injury period. Neurosurgery, 61,Suppl. 1:222–230.

Chieregato

, Fainardi

, Morselli–Labate

A.M.

, Antonelli

, Compagnone

, Targa

, Kraus

, Servadei

. 2005. Factors associated with neurological outcome and lesion progression in traumatic subarachnoid hemorrhage patients. Neurosurgery, 56:671–680.

Oertel

, Kelly

D.F.

, McArthur

, Boscardin

W.J.

, Glenn

T.C.

, Hong Lee

, Gravori

, Obukhov

, McBride

D.Q.

, Martin

N.A.

2002. Progressive hemorrhage after head trauma: predictors and consequences of the evolving injury. J. Neurosurg., 96:109–116.

Zweckberger

, Stoffel

, Baethmann

, Plesnila

2003. Effect of decompression craniotomy on increase of contusion volume and functional outcome after controlled cortical impact in mice. J. Neurotrauma, 20:1307–1314.

Chibbaro

, Tacconi

2007. Role of decompressive craniectomy in the management of severe head injury with refractory cerebral edema and intractable intracranial pressure. Our experience with 48 cases. Surg. Neurol., 68:632–638.

Huang

A.P.

, Tu

Y.K.

, Tsai

Y.H.

, Chen

Y.S.

, Hong

W.C.

, Yang

C.C.

, Kuo

L.T.

, Su

I.C.

, Huang

S.H.

, Huang

S.J.

2008. Decompressive craniectomy as the primary surgical intervention for hemorrhagic contusion. J. Neurotrauma, 25:1347–1354.

Polin

R.S.

, Shaffrey

M.E.

, Bogaev

C.A.

, Tisdale

, Germanson

, Bocchicchio

, Jane

J.A.

1997. Decompressive bifrontal craniectomy in the treatment of severe refractory posttraumatic cerebral edema. Neurosurgery, 41:84–92.

10.

Aarabi

, Hesdorffer

D.C.

, Ahn

E.S.

, Aresco

, Scalea

T.M.

, Eisemberg

H.M.

2006. Outcome following decompressive craniectomy for malignant swelling due to severe head injury. J. Neurosurg., 104:469–479.

11.

Flint

A.C.

, Manley

G.T.

, Gean

A.D.

, Hemphlill

J.C.

III , Rosenthal

2008. Post-operative expansion of hemorrhagic contusions after unilateral decompressive hemicraniectomy in severe traumatic brain injury. J. Neurotrauma, 25:503–512.

12.

Brain Trauma Foundation, American Association of Neurological Surgeons, Joint Section on Neurotrauma and Critical Care. 2000. Guidelines for cerebral perfusion pressure. J. Neurotrauma., 17:507–511.

13.

Bullock

, Chesnut

R.M.

, Clifton

, Ghajar

, Marion

D.W.

, Narayan

R.K.

, Newell

D.W.

, Pitts

L.H.

, Rosner

M.J.

, Wilberger

J.W.

1996. Guidelines for the management of severe head injury. Brain Trauma Foundation. Eur. J. Emerg. Med., 3:109–127.

14.

Pompucci

, De Bonis

, Pettorini

, Petrella

, Di Chirico

, Anile

. 2007. Decompressive craniectomy for traumatic brain injury: patient age and outcome. J. Neurotrauma, 24:1182–1188.

15.

Bullock

, Hanemann

C.O.

, Murray

, Teasdale

G.M.

1990. Recurrent hematomas following craniotomy for traumatic intracranial mass. J. Neurosurg., 72:9–14.

16.

Diaz

F.G.

, Yock

D.H.

Jr , Larson

, Rockswold

G.L.

1979. Early diagnosis of delayed posttraumatic intracerebral hematomas. J. Neurosurg., 50:217–223.

17.

Doughty

R.G.

1938. Posttraumatic delayed intracerebral hemorrhage. South Med J., 31:254–256.

18.

Jaimovich

, Monges

J.A.

1991–1992. Delayed posttraumatic intracranial lesions in children. Pediatr. Neurosurg., 17:25–29.

19.

Lobato

R.D.

, Rivas

J.J.

, Gomez

P.A.

, Castañeda

, Cañizal

J.M.

, Sarabia

, Cabrera

, Muñoz

M.J.

1991. Head-injured patients who talk and deteriorate into coma. Analysis of 221 cases studied with computerized tomography. J. Neurosurg., 75:256–261.

20.

Touho

, Hirakawa

, Hino

, Karasawa

, Ohno

1986. Relationship between abnormalities of coagulation and fibrinolysis and postoperative intracranial hemorrhage in head injury. Neurosurgery, 19:523–531.

21.

Gudeman

S.K.

, Kishore

P.R.

, Miller

J.D.

, Girevendulis

A.K.

, Lipper

M.H.

, Becker

D.P.

1979. The genesis and significance of delayed traumatic intracerebral hematoma. Neurosurgery, 5:309–313.

22.

Mertol

, Guner

, Acar

, Aatbay

, Kirisoglu

1991. Delayed traumatic intracerebral hematoma. Br J Neurosurg., 5:491–498.

23.

Soloniuk

, Pitts

L.H.

, Lovely

, Bartkowski

1986. Traumatic intracerebral hematomas: timing of appearance and indications for operative removal. J. Trauma, 26:787–794.

24.

Young

H.A.

, Gleave

J.R.

, Schmidek

H.H.

, Gregory

1984. Delayed traumatic intracerebral hematoma: report of 15 cases operatively treated. Neurosurgery, 14:22–25.

25.

Alahmadi

, Vachhrajani

, Cusimano

M.D.

2010. The natural history of brain contusion: an analysis of radiological and clinical progression. J. Neurosurg., 112:1139–1145.

26.

Yang

X.F.

, Wen

, Shen

, Li

, Lou

, Liu

W.G.

, Zhan

R.Y.

2008. Surgical complications secondary to decompressive craniectomy in patients with a head injury: a series of 108 consecutive cases. Acta. Neurochir. (Wien), 150:1241–1247.

27.

Csókay

, Nagy

, Novoth

2001. Avoidance of vascular compression in decompressive surgery for brain edema caused by trauma and tumor ablation. Neurosurg. Rev., 24:209–213.