Original Article
5
Decompressive Craniectomy after Severe Traumatic Brain Injury in Children: Complications and Outcome Astrid Pechmann1 Constantin Anastasopoulos1 Janbernd Kirschner1
Rudolf Korinthenberg1
1 Division of Neuropediatrics and Muscle Disorders, University Medical
Center Freiburg, Freiburg, Germany 2 Department of Neurosurgery, University Medical Center Freiburg, Freiburg, Germany
Vera van Velthoven-Wurster2
Address for correspondence Janbernd Kirschner, MD, Division of Neuropediatrics and Muscle Disorders, University Medical Center Freiburg, Mathildenstr.1, 79106 Freiburg, Germany (e-mail: [email protected]).
Abstract
Keywords
► traumatic brain injury ► decompressive craniectomy ► children ► complications ► outcome
Decompressive craniectomy (DC) is a controversially discussed neurosurgical procedure to reduce elevated intracranial pressure after severe traumatic brain injury (TBI). In contrast to adults, several studies could show a benefit for the pediatric population, but still DC is considered as an emergency procedure only. The aim of our study was to identify secondary complications and long-term sequelae of the procedure. All children presenting to the University Medical Center Freiburg between 2005 and 2013 who underwent DC after severe TBI were retrospectively reviewed with respect to complications and outcome. Twelve children were included with a mean Glasgow Coma Scale of 4.5 1.7. The most frequent complications after TBI and DC were formation of hygroma (83%), aseptic bone resorption of the reimplanted bone flap (50%), posttraumatic hydrocephalus (42%), secondary infection or dysfunction of ventriculoperitoneal shunt (25%) or cranioplasty (33%), and epilepsy (33%). Because of these complications, 75% of patients required further surgery in addition to cranioplasty with up to eight interventions. At follow-up, mean Glasgow Outcome Scale was 3.3 1.2. Within our patient population, we demonstrated high incidence of complications after DC, leading to further surgical procedures and longer hospitalization. These potential complications have to be considered in any decision about DC as an emergency procedure.
Introduction An increasing intracranial pressure (ICP) is a severe complication after traumatic brain injury (TBI) due to mass lesions, hemorrhage, or diffuse cerebral edema. High ICP correlates with a reduced cerebral perfusion pressure (CPP) and, therefore, carries the risk of secondary brain damage1 involving high grade of morbidity and mortality. Accordingly, TBI ranks among the most frequent cause of death in children.2 Guidelines for the management of intracranial hypertension in severe TBI in children include mainly conservative procedures, such as analgosedation, hyperosmolar therapy, mild hyperventilation, temperature control, cerebrospinal fluid drainage, or barbiturates to lower ICP.3
received April 10, 2014 accepted after revision July 15, 2014 published online October 24, 2014
Decompressive craniectomy (DC) is a controversially discussed neurosurgical method to reduce elevated ICP by removing a variable amount of skull bone.4 In adults, DC is approved as potent treatment of refractory high ICP. But a benefit of functional outcome of survivors after DC is not evident as adverse effects, such as brain edema, subdural collections, hydrocephalus, or brain infarction, affect the outcome.4,5 In contrast, several studies have now shown that in the pediatric population DC has a positive effect on the long-term outcome of children with severe TBI.6–13 Among those, Taylor at al performed the only randomized study demonstrating a significant difference in outcome between children who underwent DC and children who were given medical
© 2015 Georg Thieme Verlag KG Stuttgart · New York
DOI http://dx.doi.org/ 10.1055/s-0034-1393707. ISSN 0174-304X.
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Neuropediatrics 2015;46:5–12.
Craniectomy after Severe TBI in Children: Complications and Outcome treatment only.13 But despite these promising results, possible complications following DC should also be considered in children before indicating the surgical procedure. Thus, current treatment guidelines still consider DC only as a rescue therapy when medical treatment has failed to control elevated ICP.3,14 The aim of our study was to identify and characterize the possible complications in relation to the long-term outcome in children after severe TBI to make a contribution for better consideration of DC.
Materials and Methods We retrospectively reviewed all medical charts of children who presented to the Department of Pediatrics and Adolescent Medicine of the University Medical Center Freiburg between January 2005 and February 2013, and underwent DC after severe TBI. To classify our patient population, we focused on age, sex, cause of injury, initial clinical examination, initial Glasgow Coma Scale (GCS), pupil size and reactivity, cerebral imaging, ICP, and timing and indication for DC. On admission, all children received a comprehensive examination by a multidisciplinary team and a computed tomographic (CT) scan of the brain was initiated immediately. The indication for emergency DC was based on CT findings, clinical signs for cerebral herniation, or preexisting anisocoria. Without an emergency indication for DC, children underwent a conservative treatment according to the treatment guidelines for TBI.3 DC was then performed when ICP was refractory to the medical treatment. Cranioplasty was performed approximately 3 months after DC. Complications after DC were identified by follow-ups in our neuropediatric outpatient clinic or additionally required surgical or nonsurgical treatments in hospital. To measure the long-term outcome, we used the Glasgow Outcome Scale (GOS) which was first described by Jennett and Bond in 1975.15 Although it has been criticized for being insufficiently sensitive, still it is the most widely used and accepted instrument particularly for patients’ outcome after rehabilitation.16 As favorable outcome we considered a score of 5 (good recovery) or 4 (moderate disability) and a score of 3 (severe disability), 2 (vegetative state), or 1 (death) as unfavorable outcome. In addition, we also focused on motor residual symptoms and behavioral abnormalities. Follow-up time varied from 3 to 83 months after the trauma with a median of 29.4 27.4 months.
Results Patient Population Twelve children were included in this study: eight boys (67%) and four girls (33%). One girl had to be excluded for not fulfilling the explicit criteria of severe TBI with an initial GSC of 15. Age ranged from 2 to 14 years (mean, 8.5 4.3 years). The major causes of TBI were car accident (42%), fall from height > 2 m (17%), and toboggan accident (17%). The preliminary examination showed a mean GCS of 4.5 1.7. In six children (50%), the GCS score was 3 before intubation and Neuropediatrics
Vol. 46
No. 1/2015
Pechmann et al.
sedation. The highest GCS was 8 at initial presentation. Six children (50%) presented initial anisocoria. In one child, grand mal seizures were observed immediately after the trauma. On admission at our emergency unit, all children were intubated and sedated. Key features and outcome of all 12 children are shown in ►Table 1. CT findings were as follows: skull fracture (92%), contusion hemorrhage (67%), subarachnoidal hemorrhage (SAH) (59%), subdural hemorrhage (SDH) (33%), brain midline shift (33%), intraventricular hemorrhage (33%), cerebral herniation (17%), and epidural hemorrhage (EDH) (8%).
Indication and Timing for Craniectomy Overall patients’ median time to DC was 53.2 69.8 hours. In 10 children ICP was monitored before surgery: mean ICP was 43.7 18.0 mm Hg. The two remaining children showed clinical signs of cerebral herniation initially so that an emergency DC was performed without measuring ICP. Within our population we could identify two subgroups according to the timing of DC: Six patients underwent emergency surgery based on CT findings, clinical signs of cerebral herniation, or initial anisocoria. Median time to surgery was 2.7 0.9 hours and the mean ICP among these children was 49.8 15.9 mm Hg. The other six patients were initially treated conservatively. DC was performed when ICP was refractory to medical therapy. Median time to surgery was 95.3 71.1 hours and mean ICP was 39.7 19.5 mm Hg.
Clinical Course after Surgery In all children, DC achieved an initial decrease of ICP less than 20 mm Hg. Three patients showed secondary brain swelling with a new increase of ICP: one girl underwent contralateral craniectomy within the next day, whereas the other two were treated conservatively with medical therapy or insertion of external ventriculostomy. The most frequent complication after surgery was the formation of subdural hygroma in 10 children (83%) (►Fig. 1). Half of them (in total 42%) developed posttraumatic hydrocephalus with consecutive implantation of ventriculoperitoneal (VP) shunt. In three children (25%), the incidence of myoclonia or Jackson seizures required medical treatment. Seven children (58%) showed a transient diabetes insipidus and eight children (67%) developed pneumonia under ventilation. Severe complications included meningitis in two children (17%) and sinus venous thrombosis in one child (8%). Two children (17%) required tracheotomy and in four children (33%) a gastrostomy was performed. In seven children (58%), a magnetic resonance imaging scan was performed after DC. Diffuse axonal injury lesion occurred in five of them. Median time to extubation was 11.7 5.8 days and the median length of stay at our intensive care unit was 16.6 7.8 days.
Cranioplasty In 10 children (83%), the cryopreserved autologous bone flap was reimplanted. Due to severe skull fractures in one child with bilateral hemicraniectomy, a prosthesis on one side was necessary in addition to the bone flap on the other side. Two
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
6
Pupil reactivity
Anisocoria
Normal
Normal
Normal
Pupils fixed, mydriasis
Anisocoria
Pupils fixed, miosis
Patient
♂, 13 y, fall (6 m)
♀, 2 y, kick by a horse
♂, 14 y, fall (5 m)
♂, 11 y, car accident
♂, 12 y, knocked by a swing set
♀, 10 y, car accident
♀, 11 y, car accident
1
2
3
4
5
6
7
6
3
3
3
8
3
6
GCS
Initial findings
50
20
nm
65
19
40
nm
ICP
Fixed pupils, cerebral herniation, ICP > 50 mm Hg
Increasing cerebral edema, cerebral herniation
Cerebral herniation
Refractory high ICP, cerebral herniation, pupils fixed and dilated
Refractory high ICP, acute dilated right pupil
Refractory high ICP
Clinical signs of cerebral herniation
Indication for DC
0
1
0
8
3
1
0
Time to DC (day)
Hygroma, hydrocephalus, VP shunt, infection of VP shunt, dislocation of cranioplasty,
Hygroma
Hygroma, hydrocephalus, VP shunt, infection of VP shunt, aseptic bone resorption, cerebrospinal fluid fistula
Hygroma, aseptic bone resorption of reimplanted bone flap
Aseptic bone resorption of reimplanted bone flap
Hygroma, hydrocephalus, VP shunt, dislocation of cranioplasty, woundhealing disturbances
Hygroma, infection of cranioplasty
Long-term complication after DC
Complications
6
0
8
1
1
2
2
Surgery in addition to DC and cranioplasty
Mesencephalic syndrome, tetraspasticity
Chronified headache, lack of concentration, learning disability
Apallic syndrome, tetraspasticity
Insecure gait, facial nerve paresis left, problems with fine motor skills, reduced memory retention
Lack of concentration
Hemiparesis left, developmental delay, reduced memory retention
Epilepsy, mild mental retardation, learning disabilities, reduced memory retention, lack of concentration
Outcome
Outcome
2
5
2
4
5
4
4
GOS
Neuropediatrics
Vol. 46
(Continued)
3
83
14
18
37
7
30
Follow-up (month)
Pechmann et al.
No. 1/2015
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Skull fracture, contusion hemorrhage
SDH, contusion hemorrhage, intraventricular hemorrhage
Skull fracture, EDH, SAH, intraventricular hemorrhage, cerebral herniation
Skull fracture
Skull fracture, contusion hemorrhage, SAH
Skull fracture, brain shift, SAH, contusion hemorrhage
Skull fracture, contusion hemorrhage, brain shift, SAH
CT findings
Decompressive craniectomy
Table 1 Patient population, indication for decompressive craniectomy, long-term complications and outcome
Craniectomy after Severe TBI in Children: Complications and Outcome 7
Neuropediatrics
Vol. 46
Normal
Normal
Normal
Anisocoria
♂, 7 y, car accident
♂, 7 y, toboggan accident
♂, 2 y, knocked by wardrobe
♀, 3 y, toboggan accident
9
No. 1/2015
10
11
12
3
6
5
5
3
GCS
Skull fracture, SDH, minimal brain shift, contusion hemorrhage, cerebral herniation
Skull fracture, SDH, contusion hemorrhage
Skull fracture, SAH, contusion hemorrhage
Skull fracture, SAH, intraventricular hemorrhage
Skull fracture, SAH, SDH, intraventricular hemorrhage, brain shift
CT findings
60
34
30
50
69
ICP
Refractory increasing ICP
Refractory increasing ICP
Refractory increasing ICP
Increasing cerebral edema, fixed and dilated pupils
Dilated left pupil, refractory elevated ICP
Indication for DC
7
5
0
0
0
Time to DC (day)
Decompressive craniectomy
Hygroma, partial aseptic bone resorption
Hygroma
Aseptic bone resorption, dislocation of cranioplasty
Hygroma, aseptic bone resorption, hydrocephalus, VP shunt
Hygroma, hydrocephalus, VP shunt, dysfunction of VP shunt
wound-healing disturbances
Long-term complication after DC
Complications
0
0
2
1
3
Surgery in addition to DC and cranioplasty
Ataxia, aphasia, developmental delay, attention-deficit disorder
Epilepsy, hemiparesis right, developmental delay, attention-deficit disorder
Epilepsy, reduced fine motor skills, attention-deficit disorder, learning disability
Dysarthria, nystagmus, tetraparesis, mental retardation
Apallic syndrome, epilepsy, death 4.5 years after trauma
Outcome
Outcome
4
3
4
3
1
GOS
3
11
47
70
Follow-up (month)
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Craniectomy after Severe TBI in Children: Complications and Outcome
Abbreviations: ♀, girl; ♂, boy; CT, computed tomography; DC, decompressive craniectomy; EDH, epidural hemorrhage; GCS, Glasgow coma scale; GOS, Glasgow outcome scale; ICP, intracranial pressure; nm, not measured; SAH, subarachnoidal hemorrhage; SDH, subdural hemorrhage; VP, ventriculoperitoneal; y, year.
Anisocoria
♂, 10 y, car accident
Pupil reactivity
Initial findings
8
Patient
Table 1 (Continued)
8 Pechmann et al.
Pechmann et al.
Fig. 1 Magnetic resonance imaging scan of patient no. 2 showing the development of hygroma and dislocation of cranioplasty 6 months after decompressive craniectomy.
Fig. 2 Computed tomographic scan of patient no. 5 showing aseptic bone resorption 12 months after reimplantation of the bone flap.
children (17%) underwent cranioplasty using a prosthesis primary. Mean time to cranioplasty was 3.7 1.9 months. Both the autologous bone flap and the prosthesis were fixed by titanium clamps and additionally with nonabsorbable sutures in some cases.
(25%), reduced memory retention (25%), attention-deficit disorder (25%), mild mental retardation (17%), or delayed development (25%) depending on the age at injury.
Long-Term Complications Long-term complications after DC, which led to additional surgical procedures, were observed in the majority of the patients: Six children (50%) underwent aseptic bone resorption after reimplantation of the preserved bone flap (►Fig. 2). In five of those a secondary cranioplasty was necessary. The incidence of infection or dislocation of cranioplasty was 33%. In three children (25%), infection or dysfunction of VP shunt after cranioplasty was observed. Other complications making surgical procedures necessary were wound-healing disturbances in two children (17%) and the development of a cerebrospinal fluid fistula in one child (8%). As a consequence, nine children (75%) underwent further surgery in addition to cranioplasty ranging from one to eight interventions.
Follow-Up Mean GOS within our patient population was 3.3 1.2 at a follow-up time ranging from 3 to 83 months (median, 29.4 27.4 months). Seven children reached favorable outcome (58%) while three children in vegetative status required total care (25%). One of them died through pulmonary complications 4.5 years after DC. Four children (33%) developed symptomatic epilepsy. Motor residual symptoms were as follows: hemiparesis or gait problems in five children (42%), tetraspasticity in three children (25%), and problems with fine motor skills in two children (17%). Only three children (25%) had no motor residual symptoms. Despite the three children with GOS < 3, the remaining nine children had mild to moderate behavioral abnormalities after TBI: learning disabilities (25%), lack of concentration
Discussion DC is a controversially discussed surgical procedure for the treatment of refractory intracranial hypertension. A few studies have shown a positive impact on the long-term outcome in children after severe TBI.6–13 But the establishment of explicit criteria for the indication of DC failed due to overall small number of cases, heterogeneous indication for craniectomy, and the lack of a detailed randomized control trial.17 The main aim of our study was to describe possible complications following DC and subsequent cranioplasty as these have to be considered when DC is performed as an emergency procedure. The most frequent complications within our patient population after DC were the formation of hygroma, posttraumatic hydrocephalus requiring implantation of a VP shunt, and symptomatic epilepsy. After cranioplasty aseptic bone resorption, infection or dislocation of either VP shunt or cranioplasty led to further surgical procedures. Concerning the long-term outcome using the GOS, our results with a favorable outcome in 7 out of the 12 children are comparable to previous studies.7–9,12 As the GOS is a nonspecific score to characterize the outcome in children, we also studied the incidence of motor residual symptoms and behavioral abnormalities, which showed the prevalence of motor problems in 75% and behavioral problems in all children. This might be associated with the severity of the trauma but also with the complications following DC, which might cause delayed or even poorer recovery after TBI.
Hygroma and Posttraumatic Hydrocephalus The incidence of hygroma after TBI is high but the underlying mechanism and the correlation with DC is not completely Neuropediatrics
Vol. 46
No. 1/2015
9
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Craniectomy after Severe TBI in Children: Complications and Outcome
Craniectomy after Severe TBI in Children: Complications and Outcome understood. One possible explanation is damage to the arachnoid–dura interface layer caused primarily by shearing stress due to the trauma but also possibly due to the intraoperative opening of the dura, which might cause subgaleal or subdural effusion.18,19 As another mechanism a blood–brain barrier failure with consecutive increased permeability of blood capillaries and elevated osmotic pressure is discussed.20 A third consideration is that an altered circulation of cerebrospinal fluid due to the primary trauma or due to DC increases the occurrence of hygroma and hydrocephalus.18,21,22 In adults, a correlation between CT findings and the incidence of hygroma was observed: in the group with subdural hygroma midline shift, SAH, tearing of the arachnoid membrane, and compression of basal cisterns were most frequent.21 Further, a higher risk for patients after DC with diffuse brain injury or high dynamic accident has been described.18 Giza et al studied the pathophysiological characteristics of children after severe TBI and found a higher risk for subdural hematoma and diffuse cerebral edema compared with adults.23 This might implicate that even children have a higher risk for hygroma due to the diffuse brain swelling. In summary, the incidence of hygroma depends on the mechanism of the primary trauma and the CT findings but after DC an altered circulation of the cerebrospinal fluid or the intraoperative opening of the dura may increase the risk for the formation of hygroma. Furthermore, in several studies subdural hygroma is discussed as a high risk factor for posttraumatic hydrocephalus.21,22 In addition, Shi et al showed that patients with low GCS and a large decompression defect tend to develop a posttraumatic hydrocephalus after DC.24 Although there are also studies describing no correlation between hygroma and the development of hydrocephalus,18 our results show that all children with posttraumatic hydrocephalus had a preexisting hygroma and both children who underwent bilateral decompression developed hydrocephalus within 2 months. The indication for the implantation of a VP shunt within our cohort was a progressive hydrocephalus with an increase of the ventricular size. In one girl, dislocation of cranioplasty occurred and in two children a cerebrospinal fluid leakage was the overriding symptom. After implantation of the VP shunt, further complications, such as infection, dysfunction of the VP shunt, or dislocation of the reimplanted bone flap, were observed in four of the five children with hydrocephalus.
Cranioplasty To repair the craniotomy defect a secondary cranioplasty is necessary. If possible, the preserved autologous bone flap is reused; otherwise a prosthesis has to be implanted. The use of the bone flap has, in general, a lower risk for infection25 and the advantage of a potential reincorporation particularly in children.26 But aseptic bone resorption is one common complication after cranioplasty.7,17,26,27 We observed aseptic bone resorption in 50% of the children following reimplantation of the autologous bone flap. This is similar to the findings of Grant et al26 but shows higher incidence compared with other studies.6,17,27 Grant et al postulated that the risk of Neuropediatrics
Vol. 46
No. 1/2015
Pechmann et al.
aseptic bone resorption increases with the size of the skull defect,26 which can be a possible explanation for our results. Here, no correlation between time to cranioplasty and bone resorption could be found.26 A significant lower rate of aseptic bone resorption after early cranioplasty was demonstrated by Piedra et al. They classified their cohort on the basis of the criteria of early (< 6 weeks) and late cranioplasty (> 6 weeks) and could reduce the rate of bone resorption from 42% in the late cohort to 14.3% in the early cohort.27 Figaji et al even described a reimplantation of the bone flap during the initial DC in the attempt of reducing the rate of bone resorption.7 In our cohort, time to cranioplasty was 3.7 1.9 months ranging from 2 to 9.5 months. None of the children underwent cranioplasty within 6 weeks; therefore, we cannot evaluate a potential benefit of early cranioplasty with our data. Another aspect being controversially discussed as a potential risk factor for aseptic bone resorption is the presence of a permanent VP shunt or hygroma.26–29 The hypothesis is that reduced ICP fluctuations caused by VP shunt may negatively affect the skull growth and, therefore, facilitate aseptic bone resorption.28,29 Within our cohort, four children with aseptic bone resorption had preexisting hygroma and two of them had a permanent VP shunt. Our small case series does not allow naming a tendency toward higher rates of aseptic bone resorption with preexisting hygroma or VP shunt. The fixation of the bone flap may also play a role for aseptic bone resorption. Within our cohort, autologous bone flap and cranioplasty were fixed with titanium clamps and in some additional cases with nonabsorbable sutures. No difference between the techniques could be detected. This result is comparable to other studies.25,29 Five children with aseptic bone resorption underwent further surgical procedure to repair the skull defect with a prosthesis. We observed a dislocation or infection of the implanted prosthesis in four children and wound-healing disturbances in one girl after cranioplasty in combination with a distinctive hygroma and consecutive posttraumatic hydrocephalus. Because of the earlier-described complications, there was an average number of surgical procedures in addition to DC and cranioplasty of 3.2 2.5 (ranging from one to eight interventions).
Epilepsy The incidence of posttraumatic epilepsy is well described and associated with the severity of the brain injury. Compared with adults, children have an increased risk for seizures after TBI.30,31 Annegers et al identified brain contusion with subdural hematoma, skull fracture, or loss of consciousness as specific risk factors for late seizures.30 In fact, all children with posttraumatic epilepsy in our series suffered from skull fractures, SDH, or contusion hemorrhage and a GCS < 6. The development of posttraumatic epilepsy in 33% of our population coincides with previous results.30,32 Our data do not indicate that DC increases the risk for epilepsy after TBI.
Behavioral Abnormalities Behavioral abnormalities are a frequently observed complication after severe TBI. In our study, all children
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
10
Craniectomy after Severe TBI in Children: Complications and Outcome
2 Kraus JF, Rock A, Hemyari P. Brain injuries among infants, children,
adolescents, and young adults. Am J Dis Child 1990;144(6):684–691 3 Kochanek PM, Carney N, Adelson PD, et al; American Academy of
Timing of Decompressive Craniectomy and Outcome Another aspect being discussed in regard to DC is the timing of the surgical procedure. Some authors hypothesize that early DC has a positive impact on long-term outcome6,11,13 whereas others could not observe a strong correlation between timing and outcome.8,9 Within our patient population, six children underwent emergency surgery. However, this subgroup was clinically different from the group with later DC with higher preoperative ICP and higher prevalence of clinical signs of cerebral herniation, so comparison between the two groups does not allow any conclusion about the timing of DC.
Conclusion Despite the potential benefit of DC in children after severe TBI, this case series demonstrates a high incidence of complications following DC that lead to a significant number of neurosurgical interventions associated with additional burden for patients and families and possible impact on the longterm outcome. Although, this case series without a control group does not allow direct conclusions about the causal relationship between DC and the observed postoperative complications, we feel that awareness about the high rate of complications and the need of additional neurosurgical interventions is very important. Therefore, any discussion about the indication for DC after TBI in children, even though it is performed as an emergency procedure, should not only include potential benefits from ICP release, but also risks and potential sequelae of the procedure. In addition, further research is needed to reduce secondary complications in those cases where DC is unavoidable. This includes management of hygroma and timing of cranioplasty.
Conflict of Interest The authors have no conflicts of interest to disclose.
4
5
6
7
8
9
10
11
12
13
14
15
Funding The authors have no financial relationships relevant to this article to disclose. No external funding was secured for this study.
References
16 17
18
1 Mehta A, Kochanek PM, Tyler-Kabara E, et al. Relationship of
intracranial pressure and cerebral perfusion pressure with outcome in young children after severe traumatic brain injury. Dev Neurosci 2010;32(5-6):413–419
11
19
Pediatrics-Section on Neurological Surgery; American Association of Neurological Surgeons/Congress of Neurological Surgeons; Child Neurology Society; European Society of Pediatric and Neonatal Intensive Care; Neurocritical Care Society; Pediatric Neurocritical Care Research Group; Society of Critical Care Medicine; Paediatric Intensive Care Society UK; Society for Neuroscience in Anesthesiology and Critical Care; World Federation of Pediatric Intensive and Critical Care Societies. Guidelines for the acute medical management of severe traumatic brain injury in infants, children, and adolescents—second edition. Pediatr Crit Care Med 2012;13(Suppl 1):S1–S82 Sahuquillo J, Arikan F. Decompressive craniectomy for the treatment of refractory high intracranial pressure in traumatic brain injury. Cochrane Database Syst Rev 2006;(1):CD003983 Cooper DJ, Rosenfeld JV, Murray L, et al; DECRA Trial Investigators; Australian and New Zealand Intensive Care Society Clinical Trials Group. Decompressive craniectomy in diffuse traumatic brain injury. N Engl J Med 2011;364(16):1493–1502 Adamo MA, Drazin D, Waldman JB. Decompressive craniectomy and postoperative complication management in infants and toddlers with severe traumatic brain injuries. J Neurosurg Pediatr 2009;3(4):334–339 Figaji AA, Fieggen AG, Peter JC. Early decompressive craniotomy in children with severe traumatic brain injury. Childs Nerv Syst 2003; 19(9):666–673 Jagannathan J, Okonkwo DO, Dumont AS, et al. Outcome following decompressive craniectomy in children with severe traumatic brain injury: a 10-year single-center experience with long-term follow up. J Neurosurg 2007;106(4, Suppl):268–275 Kan P, Amini A, Hansen K, et al. Outcomes after decompressive craniectomy for severe traumatic brain injury in children. J Neurosurg 2006;105(5, Suppl):337–342 Ruf B, Heckmann M, Schroth I, et al. Early decompressive craniectomy and duraplasty for refractory intracranial hypertension in children: results of a pilot study. Crit Care 2003;7(6):R133–R138 Rutigliano D, Egnor MR, Priebe CJ, et al. Decompressive craniectomy in pediatric patients with traumatic brain injury with intractable elevated intracranial pressure. J Pediatr Surg 2006; 41(1):83–87, discussion 83–87 Cambra FJ, Palomeque A, Muñoz-Santanach D, Segura Matute S, Navarro Balbuena R, García Fructuoso G. Use of decompressive craniectomy in the management of refractory intracranial hypertension in paediatric patients [in Spanish]. An Pediatr (Barc) 2010; 73(1):12–18 Taylor A, Butt W, Rosenfeld J, et al. A randomized trial of very early decompressive craniectomy in children with traumatic brain injury and sustained intracranial hypertension. Childs Nerv Syst 2001;17(3):154–162 Maas AI, Dearden M, Teasdale GM, et al; European Brain Injury Consortium. EBIC-guidelines for management of severe head injury in adults. Acta Neurochir (Wien) 1997;139(4):286–294 Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet 1975;1(7905):480–484 Shukla D, Devi BI, Agrawal A. Outcome measures for traumatic brain injury. Clin Neurol Neurosurg 2011;113(6):435–441 Pérez Suárez E, Serrano González A, Pérez Díaz C, García Salido A, Martínez de Azagra Garde A, Casado Flores J. Decompressive craniectomy in 14 children with severe head injury: clinical results with long-term follow-up and review of the literature. J Trauma 2011;71(1):133–140 Aarabi B, Chesler D, Maulucci C, Blacklock T, Alexander M. Dynamics of subdural hygroma following decompressive craniectomy: a comparative study. Neurosurg Focus 2009;26(6):E8 Haines DE, Harkey HL, al-Mefty O. The “subdural” space: a new look at an outdated concept. Neurosurgery 1993;32(1):111–120 Neuropediatrics
Vol. 46
No. 1/2015
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
presented mild to moderate behavioral problems, which is comparable with other results. 8,17 The incidence of behavioral abnormalities has to be attributed to the severity of TBI and thus, behavioral abnormalities are probably no explicit complication following DC. But long hospitalization due to DC and the following complications can lead to a delayed or even poorer recovery33 and might have an impact on cognitive and behavioral development.
Pechmann et al.
Craniectomy after Severe TBI in Children: Complications and Outcome
Pechmann et al.
20 Liu Y, Gong J, Li F, Wang H, Zhu S, Wu C. Traumatic subdural
27 Piedra MP, Thompson EM, Selden NR, Ragel BT, Guillaume DJ.
hydroma: clinical characteristics and classification. Injury 2009; 40(9):968–972 Jeon SW, Choi JH, Jang TW, Moon SM, Hwang HS, Jeong JH. Risk factors associated with subdural hygroma after decompressive craniectomy in patients with traumatic brain injury: a comparative study. J Korean Neurosurg Soc 2011;49(6):355–358 Honeybul S, Ho KM. Incidence and risk factors for post-traumatic hydrocephalus following decompressive craniectomy for intractable intracranial hypertension and evacuation of mass lesions. J Neurotrauma 2012;29(10):1872–1878 Giza CC, Mink RB, Madikians A. Pediatric traumatic brain injury: not just little adults. Curr Opin Crit Care 2007;13(2):143–152 Shi SS, Zhang GL, Zeng T, Lin YF. Posttraumatic hydrocephalus associated with decompressive cranial defect in severe braininjured patients. Chin J Traumatol 2011;14(6):343–347 Chang V, Hartzfeld P, Langlois M, Mahmood A, Seyfried D. Outcomes of cranial repair after craniectomy. J Neurosurg 2010; 112(5):1120–1124 Grant GA, Jolley M, Ellenbogen RG, Roberts TS, Gruss JR, Loeser JD. Failure of autologous bone-assisted cranioplasty following decompressive craniectomy in children and adolescents. J Neurosurg 2004;100(2, Suppl Pediatrics):163–168
Optimal timing of autologous cranioplasty after decompressive craniectomy in children. J Neurosurg Pediatr 2012;10(4): 268–272 Bowers CA, Riva-Cambrin J, Hertzler DA II, Walker ML. Risk factors and rates of bone flap resorption in pediatric patients after decompressive craniectomy for traumatic brain injury. J Neurosurg Pediatr 2013;11(5):526–532 Martin KD, Franz B, Kirsch M, et al. Autologous bone flap cranioplasty following decompressive craniectomy is combined with a high complication rate in pediatric traumatic brain injury patients. Acta Neurochir (Wien) 2014;156(4):813–824 Annegers JF, Hauser WA, Coan SP, Rocca WA. A population-based study of seizures after traumatic brain injuries. N Engl J Med 1998; 338(1):20–24 Frey LC. Epidemiology of posttraumatic epilepsy: a critical review. Epilepsia 2003;44(Suppl 10):11–17 Hahn YS, Fuchs S, Flannery AM, Barthel MJ, McLone DG. Factors influencing posttraumatic seizures in children. Neurosurgery 1988;22(5):864–867 Honeybul S, Ho KM. Long-term complications of decompressive craniectomy for head injury. J Neurotrauma 2011;28(6): 929–935
21
22
23 24
25
26
Neuropediatrics
Vol. 46
No. 1/2015
28
29
30
31 32
33
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
12
Copyright of Neuropediatrics is the property of Georg Thieme Verlag Stuttgart and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
5
Decompressive Craniectomy after Severe Traumatic Brain Injury in Children: Complications and Outcome Astrid Pechmann1 Constantin Anastasopoulos1 Janbernd Kirschner1
Rudolf Korinthenberg1
1 Division of Neuropediatrics and Muscle Disorders, University Medical
Center Freiburg, Freiburg, Germany 2 Department of Neurosurgery, University Medical Center Freiburg, Freiburg, Germany
Vera van Velthoven-Wurster2
Address for correspondence Janbernd Kirschner, MD, Division of Neuropediatrics and Muscle Disorders, University Medical Center Freiburg, Mathildenstr.1, 79106 Freiburg, Germany (e-mail: [email protected]).
Abstract
Keywords
► traumatic brain injury ► decompressive craniectomy ► children ► complications ► outcome
Decompressive craniectomy (DC) is a controversially discussed neurosurgical procedure to reduce elevated intracranial pressure after severe traumatic brain injury (TBI). In contrast to adults, several studies could show a benefit for the pediatric population, but still DC is considered as an emergency procedure only. The aim of our study was to identify secondary complications and long-term sequelae of the procedure. All children presenting to the University Medical Center Freiburg between 2005 and 2013 who underwent DC after severe TBI were retrospectively reviewed with respect to complications and outcome. Twelve children were included with a mean Glasgow Coma Scale of 4.5 1.7. The most frequent complications after TBI and DC were formation of hygroma (83%), aseptic bone resorption of the reimplanted bone flap (50%), posttraumatic hydrocephalus (42%), secondary infection or dysfunction of ventriculoperitoneal shunt (25%) or cranioplasty (33%), and epilepsy (33%). Because of these complications, 75% of patients required further surgery in addition to cranioplasty with up to eight interventions. At follow-up, mean Glasgow Outcome Scale was 3.3 1.2. Within our patient population, we demonstrated high incidence of complications after DC, leading to further surgical procedures and longer hospitalization. These potential complications have to be considered in any decision about DC as an emergency procedure.
Introduction An increasing intracranial pressure (ICP) is a severe complication after traumatic brain injury (TBI) due to mass lesions, hemorrhage, or diffuse cerebral edema. High ICP correlates with a reduced cerebral perfusion pressure (CPP) and, therefore, carries the risk of secondary brain damage1 involving high grade of morbidity and mortality. Accordingly, TBI ranks among the most frequent cause of death in children.2 Guidelines for the management of intracranial hypertension in severe TBI in children include mainly conservative procedures, such as analgosedation, hyperosmolar therapy, mild hyperventilation, temperature control, cerebrospinal fluid drainage, or barbiturates to lower ICP.3
received April 10, 2014 accepted after revision July 15, 2014 published online October 24, 2014
Decompressive craniectomy (DC) is a controversially discussed neurosurgical method to reduce elevated ICP by removing a variable amount of skull bone.4 In adults, DC is approved as potent treatment of refractory high ICP. But a benefit of functional outcome of survivors after DC is not evident as adverse effects, such as brain edema, subdural collections, hydrocephalus, or brain infarction, affect the outcome.4,5 In contrast, several studies have now shown that in the pediatric population DC has a positive effect on the long-term outcome of children with severe TBI.6–13 Among those, Taylor at al performed the only randomized study demonstrating a significant difference in outcome between children who underwent DC and children who were given medical
© 2015 Georg Thieme Verlag KG Stuttgart · New York
DOI http://dx.doi.org/ 10.1055/s-0034-1393707. ISSN 0174-304X.
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Neuropediatrics 2015;46:5–12.
Craniectomy after Severe TBI in Children: Complications and Outcome treatment only.13 But despite these promising results, possible complications following DC should also be considered in children before indicating the surgical procedure. Thus, current treatment guidelines still consider DC only as a rescue therapy when medical treatment has failed to control elevated ICP.3,14 The aim of our study was to identify and characterize the possible complications in relation to the long-term outcome in children after severe TBI to make a contribution for better consideration of DC.
Materials and Methods We retrospectively reviewed all medical charts of children who presented to the Department of Pediatrics and Adolescent Medicine of the University Medical Center Freiburg between January 2005 and February 2013, and underwent DC after severe TBI. To classify our patient population, we focused on age, sex, cause of injury, initial clinical examination, initial Glasgow Coma Scale (GCS), pupil size and reactivity, cerebral imaging, ICP, and timing and indication for DC. On admission, all children received a comprehensive examination by a multidisciplinary team and a computed tomographic (CT) scan of the brain was initiated immediately. The indication for emergency DC was based on CT findings, clinical signs for cerebral herniation, or preexisting anisocoria. Without an emergency indication for DC, children underwent a conservative treatment according to the treatment guidelines for TBI.3 DC was then performed when ICP was refractory to the medical treatment. Cranioplasty was performed approximately 3 months after DC. Complications after DC were identified by follow-ups in our neuropediatric outpatient clinic or additionally required surgical or nonsurgical treatments in hospital. To measure the long-term outcome, we used the Glasgow Outcome Scale (GOS) which was first described by Jennett and Bond in 1975.15 Although it has been criticized for being insufficiently sensitive, still it is the most widely used and accepted instrument particularly for patients’ outcome after rehabilitation.16 As favorable outcome we considered a score of 5 (good recovery) or 4 (moderate disability) and a score of 3 (severe disability), 2 (vegetative state), or 1 (death) as unfavorable outcome. In addition, we also focused on motor residual symptoms and behavioral abnormalities. Follow-up time varied from 3 to 83 months after the trauma with a median of 29.4 27.4 months.
Results Patient Population Twelve children were included in this study: eight boys (67%) and four girls (33%). One girl had to be excluded for not fulfilling the explicit criteria of severe TBI with an initial GSC of 15. Age ranged from 2 to 14 years (mean, 8.5 4.3 years). The major causes of TBI were car accident (42%), fall from height > 2 m (17%), and toboggan accident (17%). The preliminary examination showed a mean GCS of 4.5 1.7. In six children (50%), the GCS score was 3 before intubation and Neuropediatrics
Vol. 46
No. 1/2015
Pechmann et al.
sedation. The highest GCS was 8 at initial presentation. Six children (50%) presented initial anisocoria. In one child, grand mal seizures were observed immediately after the trauma. On admission at our emergency unit, all children were intubated and sedated. Key features and outcome of all 12 children are shown in ►Table 1. CT findings were as follows: skull fracture (92%), contusion hemorrhage (67%), subarachnoidal hemorrhage (SAH) (59%), subdural hemorrhage (SDH) (33%), brain midline shift (33%), intraventricular hemorrhage (33%), cerebral herniation (17%), and epidural hemorrhage (EDH) (8%).
Indication and Timing for Craniectomy Overall patients’ median time to DC was 53.2 69.8 hours. In 10 children ICP was monitored before surgery: mean ICP was 43.7 18.0 mm Hg. The two remaining children showed clinical signs of cerebral herniation initially so that an emergency DC was performed without measuring ICP. Within our population we could identify two subgroups according to the timing of DC: Six patients underwent emergency surgery based on CT findings, clinical signs of cerebral herniation, or initial anisocoria. Median time to surgery was 2.7 0.9 hours and the mean ICP among these children was 49.8 15.9 mm Hg. The other six patients were initially treated conservatively. DC was performed when ICP was refractory to medical therapy. Median time to surgery was 95.3 71.1 hours and mean ICP was 39.7 19.5 mm Hg.
Clinical Course after Surgery In all children, DC achieved an initial decrease of ICP less than 20 mm Hg. Three patients showed secondary brain swelling with a new increase of ICP: one girl underwent contralateral craniectomy within the next day, whereas the other two were treated conservatively with medical therapy or insertion of external ventriculostomy. The most frequent complication after surgery was the formation of subdural hygroma in 10 children (83%) (►Fig. 1). Half of them (in total 42%) developed posttraumatic hydrocephalus with consecutive implantation of ventriculoperitoneal (VP) shunt. In three children (25%), the incidence of myoclonia or Jackson seizures required medical treatment. Seven children (58%) showed a transient diabetes insipidus and eight children (67%) developed pneumonia under ventilation. Severe complications included meningitis in two children (17%) and sinus venous thrombosis in one child (8%). Two children (17%) required tracheotomy and in four children (33%) a gastrostomy was performed. In seven children (58%), a magnetic resonance imaging scan was performed after DC. Diffuse axonal injury lesion occurred in five of them. Median time to extubation was 11.7 5.8 days and the median length of stay at our intensive care unit was 16.6 7.8 days.
Cranioplasty In 10 children (83%), the cryopreserved autologous bone flap was reimplanted. Due to severe skull fractures in one child with bilateral hemicraniectomy, a prosthesis on one side was necessary in addition to the bone flap on the other side. Two
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
6
Pupil reactivity
Anisocoria
Normal
Normal
Normal
Pupils fixed, mydriasis
Anisocoria
Pupils fixed, miosis
Patient
♂, 13 y, fall (6 m)
♀, 2 y, kick by a horse
♂, 14 y, fall (5 m)
♂, 11 y, car accident
♂, 12 y, knocked by a swing set
♀, 10 y, car accident
♀, 11 y, car accident
1
2
3
4
5
6
7
6
3
3
3
8
3
6
GCS
Initial findings
50
20
nm
65
19
40
nm
ICP
Fixed pupils, cerebral herniation, ICP > 50 mm Hg
Increasing cerebral edema, cerebral herniation
Cerebral herniation
Refractory high ICP, cerebral herniation, pupils fixed and dilated
Refractory high ICP, acute dilated right pupil
Refractory high ICP
Clinical signs of cerebral herniation
Indication for DC
0
1
0
8
3
1
0
Time to DC (day)
Hygroma, hydrocephalus, VP shunt, infection of VP shunt, dislocation of cranioplasty,
Hygroma
Hygroma, hydrocephalus, VP shunt, infection of VP shunt, aseptic bone resorption, cerebrospinal fluid fistula
Hygroma, aseptic bone resorption of reimplanted bone flap
Aseptic bone resorption of reimplanted bone flap
Hygroma, hydrocephalus, VP shunt, dislocation of cranioplasty, woundhealing disturbances
Hygroma, infection of cranioplasty
Long-term complication after DC
Complications
6
0
8
1
1
2
2
Surgery in addition to DC and cranioplasty
Mesencephalic syndrome, tetraspasticity
Chronified headache, lack of concentration, learning disability
Apallic syndrome, tetraspasticity
Insecure gait, facial nerve paresis left, problems with fine motor skills, reduced memory retention
Lack of concentration
Hemiparesis left, developmental delay, reduced memory retention
Epilepsy, mild mental retardation, learning disabilities, reduced memory retention, lack of concentration
Outcome
Outcome
2
5
2
4
5
4
4
GOS
Neuropediatrics
Vol. 46
(Continued)
3
83
14
18
37
7
30
Follow-up (month)
Pechmann et al.
No. 1/2015
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Skull fracture, contusion hemorrhage
SDH, contusion hemorrhage, intraventricular hemorrhage
Skull fracture, EDH, SAH, intraventricular hemorrhage, cerebral herniation
Skull fracture
Skull fracture, contusion hemorrhage, SAH
Skull fracture, brain shift, SAH, contusion hemorrhage
Skull fracture, contusion hemorrhage, brain shift, SAH
CT findings
Decompressive craniectomy
Table 1 Patient population, indication for decompressive craniectomy, long-term complications and outcome
Craniectomy after Severe TBI in Children: Complications and Outcome 7
Neuropediatrics
Vol. 46
Normal
Normal
Normal
Anisocoria
♂, 7 y, car accident
♂, 7 y, toboggan accident
♂, 2 y, knocked by wardrobe
♀, 3 y, toboggan accident
9
No. 1/2015
10
11
12
3
6
5
5
3
GCS
Skull fracture, SDH, minimal brain shift, contusion hemorrhage, cerebral herniation
Skull fracture, SDH, contusion hemorrhage
Skull fracture, SAH, contusion hemorrhage
Skull fracture, SAH, intraventricular hemorrhage
Skull fracture, SAH, SDH, intraventricular hemorrhage, brain shift
CT findings
60
34
30
50
69
ICP
Refractory increasing ICP
Refractory increasing ICP
Refractory increasing ICP
Increasing cerebral edema, fixed and dilated pupils
Dilated left pupil, refractory elevated ICP
Indication for DC
7
5
0
0
0
Time to DC (day)
Decompressive craniectomy
Hygroma, partial aseptic bone resorption
Hygroma
Aseptic bone resorption, dislocation of cranioplasty
Hygroma, aseptic bone resorption, hydrocephalus, VP shunt
Hygroma, hydrocephalus, VP shunt, dysfunction of VP shunt
wound-healing disturbances
Long-term complication after DC
Complications
0
0
2
1
3
Surgery in addition to DC and cranioplasty
Ataxia, aphasia, developmental delay, attention-deficit disorder
Epilepsy, hemiparesis right, developmental delay, attention-deficit disorder
Epilepsy, reduced fine motor skills, attention-deficit disorder, learning disability
Dysarthria, nystagmus, tetraparesis, mental retardation
Apallic syndrome, epilepsy, death 4.5 years after trauma
Outcome
Outcome
4
3
4
3
1
GOS
3
11
47
70
Follow-up (month)
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Craniectomy after Severe TBI in Children: Complications and Outcome
Abbreviations: ♀, girl; ♂, boy; CT, computed tomography; DC, decompressive craniectomy; EDH, epidural hemorrhage; GCS, Glasgow coma scale; GOS, Glasgow outcome scale; ICP, intracranial pressure; nm, not measured; SAH, subarachnoidal hemorrhage; SDH, subdural hemorrhage; VP, ventriculoperitoneal; y, year.
Anisocoria
♂, 10 y, car accident
Pupil reactivity
Initial findings
8
Patient
Table 1 (Continued)
8 Pechmann et al.
Pechmann et al.
Fig. 1 Magnetic resonance imaging scan of patient no. 2 showing the development of hygroma and dislocation of cranioplasty 6 months after decompressive craniectomy.
Fig. 2 Computed tomographic scan of patient no. 5 showing aseptic bone resorption 12 months after reimplantation of the bone flap.
children (17%) underwent cranioplasty using a prosthesis primary. Mean time to cranioplasty was 3.7 1.9 months. Both the autologous bone flap and the prosthesis were fixed by titanium clamps and additionally with nonabsorbable sutures in some cases.
(25%), reduced memory retention (25%), attention-deficit disorder (25%), mild mental retardation (17%), or delayed development (25%) depending on the age at injury.
Long-Term Complications Long-term complications after DC, which led to additional surgical procedures, were observed in the majority of the patients: Six children (50%) underwent aseptic bone resorption after reimplantation of the preserved bone flap (►Fig. 2). In five of those a secondary cranioplasty was necessary. The incidence of infection or dislocation of cranioplasty was 33%. In three children (25%), infection or dysfunction of VP shunt after cranioplasty was observed. Other complications making surgical procedures necessary were wound-healing disturbances in two children (17%) and the development of a cerebrospinal fluid fistula in one child (8%). As a consequence, nine children (75%) underwent further surgery in addition to cranioplasty ranging from one to eight interventions.
Follow-Up Mean GOS within our patient population was 3.3 1.2 at a follow-up time ranging from 3 to 83 months (median, 29.4 27.4 months). Seven children reached favorable outcome (58%) while three children in vegetative status required total care (25%). One of them died through pulmonary complications 4.5 years after DC. Four children (33%) developed symptomatic epilepsy. Motor residual symptoms were as follows: hemiparesis or gait problems in five children (42%), tetraspasticity in three children (25%), and problems with fine motor skills in two children (17%). Only three children (25%) had no motor residual symptoms. Despite the three children with GOS < 3, the remaining nine children had mild to moderate behavioral abnormalities after TBI: learning disabilities (25%), lack of concentration
Discussion DC is a controversially discussed surgical procedure for the treatment of refractory intracranial hypertension. A few studies have shown a positive impact on the long-term outcome in children after severe TBI.6–13 But the establishment of explicit criteria for the indication of DC failed due to overall small number of cases, heterogeneous indication for craniectomy, and the lack of a detailed randomized control trial.17 The main aim of our study was to describe possible complications following DC and subsequent cranioplasty as these have to be considered when DC is performed as an emergency procedure. The most frequent complications within our patient population after DC were the formation of hygroma, posttraumatic hydrocephalus requiring implantation of a VP shunt, and symptomatic epilepsy. After cranioplasty aseptic bone resorption, infection or dislocation of either VP shunt or cranioplasty led to further surgical procedures. Concerning the long-term outcome using the GOS, our results with a favorable outcome in 7 out of the 12 children are comparable to previous studies.7–9,12 As the GOS is a nonspecific score to characterize the outcome in children, we also studied the incidence of motor residual symptoms and behavioral abnormalities, which showed the prevalence of motor problems in 75% and behavioral problems in all children. This might be associated with the severity of the trauma but also with the complications following DC, which might cause delayed or even poorer recovery after TBI.
Hygroma and Posttraumatic Hydrocephalus The incidence of hygroma after TBI is high but the underlying mechanism and the correlation with DC is not completely Neuropediatrics
Vol. 46
No. 1/2015
9
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Craniectomy after Severe TBI in Children: Complications and Outcome
Craniectomy after Severe TBI in Children: Complications and Outcome understood. One possible explanation is damage to the arachnoid–dura interface layer caused primarily by shearing stress due to the trauma but also possibly due to the intraoperative opening of the dura, which might cause subgaleal or subdural effusion.18,19 As another mechanism a blood–brain barrier failure with consecutive increased permeability of blood capillaries and elevated osmotic pressure is discussed.20 A third consideration is that an altered circulation of cerebrospinal fluid due to the primary trauma or due to DC increases the occurrence of hygroma and hydrocephalus.18,21,22 In adults, a correlation between CT findings and the incidence of hygroma was observed: in the group with subdural hygroma midline shift, SAH, tearing of the arachnoid membrane, and compression of basal cisterns were most frequent.21 Further, a higher risk for patients after DC with diffuse brain injury or high dynamic accident has been described.18 Giza et al studied the pathophysiological characteristics of children after severe TBI and found a higher risk for subdural hematoma and diffuse cerebral edema compared with adults.23 This might implicate that even children have a higher risk for hygroma due to the diffuse brain swelling. In summary, the incidence of hygroma depends on the mechanism of the primary trauma and the CT findings but after DC an altered circulation of the cerebrospinal fluid or the intraoperative opening of the dura may increase the risk for the formation of hygroma. Furthermore, in several studies subdural hygroma is discussed as a high risk factor for posttraumatic hydrocephalus.21,22 In addition, Shi et al showed that patients with low GCS and a large decompression defect tend to develop a posttraumatic hydrocephalus after DC.24 Although there are also studies describing no correlation between hygroma and the development of hydrocephalus,18 our results show that all children with posttraumatic hydrocephalus had a preexisting hygroma and both children who underwent bilateral decompression developed hydrocephalus within 2 months. The indication for the implantation of a VP shunt within our cohort was a progressive hydrocephalus with an increase of the ventricular size. In one girl, dislocation of cranioplasty occurred and in two children a cerebrospinal fluid leakage was the overriding symptom. After implantation of the VP shunt, further complications, such as infection, dysfunction of the VP shunt, or dislocation of the reimplanted bone flap, were observed in four of the five children with hydrocephalus.
Cranioplasty To repair the craniotomy defect a secondary cranioplasty is necessary. If possible, the preserved autologous bone flap is reused; otherwise a prosthesis has to be implanted. The use of the bone flap has, in general, a lower risk for infection25 and the advantage of a potential reincorporation particularly in children.26 But aseptic bone resorption is one common complication after cranioplasty.7,17,26,27 We observed aseptic bone resorption in 50% of the children following reimplantation of the autologous bone flap. This is similar to the findings of Grant et al26 but shows higher incidence compared with other studies.6,17,27 Grant et al postulated that the risk of Neuropediatrics
Vol. 46
No. 1/2015
Pechmann et al.
aseptic bone resorption increases with the size of the skull defect,26 which can be a possible explanation for our results. Here, no correlation between time to cranioplasty and bone resorption could be found.26 A significant lower rate of aseptic bone resorption after early cranioplasty was demonstrated by Piedra et al. They classified their cohort on the basis of the criteria of early (< 6 weeks) and late cranioplasty (> 6 weeks) and could reduce the rate of bone resorption from 42% in the late cohort to 14.3% in the early cohort.27 Figaji et al even described a reimplantation of the bone flap during the initial DC in the attempt of reducing the rate of bone resorption.7 In our cohort, time to cranioplasty was 3.7 1.9 months ranging from 2 to 9.5 months. None of the children underwent cranioplasty within 6 weeks; therefore, we cannot evaluate a potential benefit of early cranioplasty with our data. Another aspect being controversially discussed as a potential risk factor for aseptic bone resorption is the presence of a permanent VP shunt or hygroma.26–29 The hypothesis is that reduced ICP fluctuations caused by VP shunt may negatively affect the skull growth and, therefore, facilitate aseptic bone resorption.28,29 Within our cohort, four children with aseptic bone resorption had preexisting hygroma and two of them had a permanent VP shunt. Our small case series does not allow naming a tendency toward higher rates of aseptic bone resorption with preexisting hygroma or VP shunt. The fixation of the bone flap may also play a role for aseptic bone resorption. Within our cohort, autologous bone flap and cranioplasty were fixed with titanium clamps and in some additional cases with nonabsorbable sutures. No difference between the techniques could be detected. This result is comparable to other studies.25,29 Five children with aseptic bone resorption underwent further surgical procedure to repair the skull defect with a prosthesis. We observed a dislocation or infection of the implanted prosthesis in four children and wound-healing disturbances in one girl after cranioplasty in combination with a distinctive hygroma and consecutive posttraumatic hydrocephalus. Because of the earlier-described complications, there was an average number of surgical procedures in addition to DC and cranioplasty of 3.2 2.5 (ranging from one to eight interventions).
Epilepsy The incidence of posttraumatic epilepsy is well described and associated with the severity of the brain injury. Compared with adults, children have an increased risk for seizures after TBI.30,31 Annegers et al identified brain contusion with subdural hematoma, skull fracture, or loss of consciousness as specific risk factors for late seizures.30 In fact, all children with posttraumatic epilepsy in our series suffered from skull fractures, SDH, or contusion hemorrhage and a GCS < 6. The development of posttraumatic epilepsy in 33% of our population coincides with previous results.30,32 Our data do not indicate that DC increases the risk for epilepsy after TBI.
Behavioral Abnormalities Behavioral abnormalities are a frequently observed complication after severe TBI. In our study, all children
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
10
Craniectomy after Severe TBI in Children: Complications and Outcome
2 Kraus JF, Rock A, Hemyari P. Brain injuries among infants, children,
adolescents, and young adults. Am J Dis Child 1990;144(6):684–691 3 Kochanek PM, Carney N, Adelson PD, et al; American Academy of
Timing of Decompressive Craniectomy and Outcome Another aspect being discussed in regard to DC is the timing of the surgical procedure. Some authors hypothesize that early DC has a positive impact on long-term outcome6,11,13 whereas others could not observe a strong correlation between timing and outcome.8,9 Within our patient population, six children underwent emergency surgery. However, this subgroup was clinically different from the group with later DC with higher preoperative ICP and higher prevalence of clinical signs of cerebral herniation, so comparison between the two groups does not allow any conclusion about the timing of DC.
Conclusion Despite the potential benefit of DC in children after severe TBI, this case series demonstrates a high incidence of complications following DC that lead to a significant number of neurosurgical interventions associated with additional burden for patients and families and possible impact on the longterm outcome. Although, this case series without a control group does not allow direct conclusions about the causal relationship between DC and the observed postoperative complications, we feel that awareness about the high rate of complications and the need of additional neurosurgical interventions is very important. Therefore, any discussion about the indication for DC after TBI in children, even though it is performed as an emergency procedure, should not only include potential benefits from ICP release, but also risks and potential sequelae of the procedure. In addition, further research is needed to reduce secondary complications in those cases where DC is unavoidable. This includes management of hygroma and timing of cranioplasty.
Conflict of Interest The authors have no conflicts of interest to disclose.
4
5
6
7
8
9
10
11
12
13
14
15
Funding The authors have no financial relationships relevant to this article to disclose. No external funding was secured for this study.
References
16 17
18
1 Mehta A, Kochanek PM, Tyler-Kabara E, et al. Relationship of
intracranial pressure and cerebral perfusion pressure with outcome in young children after severe traumatic brain injury. Dev Neurosci 2010;32(5-6):413–419
11
19
Pediatrics-Section on Neurological Surgery; American Association of Neurological Surgeons/Congress of Neurological Surgeons; Child Neurology Society; European Society of Pediatric and Neonatal Intensive Care; Neurocritical Care Society; Pediatric Neurocritical Care Research Group; Society of Critical Care Medicine; Paediatric Intensive Care Society UK; Society for Neuroscience in Anesthesiology and Critical Care; World Federation of Pediatric Intensive and Critical Care Societies. Guidelines for the acute medical management of severe traumatic brain injury in infants, children, and adolescents—second edition. Pediatr Crit Care Med 2012;13(Suppl 1):S1–S82 Sahuquillo J, Arikan F. Decompressive craniectomy for the treatment of refractory high intracranial pressure in traumatic brain injury. Cochrane Database Syst Rev 2006;(1):CD003983 Cooper DJ, Rosenfeld JV, Murray L, et al; DECRA Trial Investigators; Australian and New Zealand Intensive Care Society Clinical Trials Group. Decompressive craniectomy in diffuse traumatic brain injury. N Engl J Med 2011;364(16):1493–1502 Adamo MA, Drazin D, Waldman JB. Decompressive craniectomy and postoperative complication management in infants and toddlers with severe traumatic brain injuries. J Neurosurg Pediatr 2009;3(4):334–339 Figaji AA, Fieggen AG, Peter JC. Early decompressive craniotomy in children with severe traumatic brain injury. Childs Nerv Syst 2003; 19(9):666–673 Jagannathan J, Okonkwo DO, Dumont AS, et al. Outcome following decompressive craniectomy in children with severe traumatic brain injury: a 10-year single-center experience with long-term follow up. J Neurosurg 2007;106(4, Suppl):268–275 Kan P, Amini A, Hansen K, et al. Outcomes after decompressive craniectomy for severe traumatic brain injury in children. J Neurosurg 2006;105(5, Suppl):337–342 Ruf B, Heckmann M, Schroth I, et al. Early decompressive craniectomy and duraplasty for refractory intracranial hypertension in children: results of a pilot study. Crit Care 2003;7(6):R133–R138 Rutigliano D, Egnor MR, Priebe CJ, et al. Decompressive craniectomy in pediatric patients with traumatic brain injury with intractable elevated intracranial pressure. J Pediatr Surg 2006; 41(1):83–87, discussion 83–87 Cambra FJ, Palomeque A, Muñoz-Santanach D, Segura Matute S, Navarro Balbuena R, García Fructuoso G. Use of decompressive craniectomy in the management of refractory intracranial hypertension in paediatric patients [in Spanish]. An Pediatr (Barc) 2010; 73(1):12–18 Taylor A, Butt W, Rosenfeld J, et al. A randomized trial of very early decompressive craniectomy in children with traumatic brain injury and sustained intracranial hypertension. Childs Nerv Syst 2001;17(3):154–162 Maas AI, Dearden M, Teasdale GM, et al; European Brain Injury Consortium. EBIC-guidelines for management of severe head injury in adults. Acta Neurochir (Wien) 1997;139(4):286–294 Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet 1975;1(7905):480–484 Shukla D, Devi BI, Agrawal A. Outcome measures for traumatic brain injury. Clin Neurol Neurosurg 2011;113(6):435–441 Pérez Suárez E, Serrano González A, Pérez Díaz C, García Salido A, Martínez de Azagra Garde A, Casado Flores J. Decompressive craniectomy in 14 children with severe head injury: clinical results with long-term follow-up and review of the literature. J Trauma 2011;71(1):133–140 Aarabi B, Chesler D, Maulucci C, Blacklock T, Alexander M. Dynamics of subdural hygroma following decompressive craniectomy: a comparative study. Neurosurg Focus 2009;26(6):E8 Haines DE, Harkey HL, al-Mefty O. The “subdural” space: a new look at an outdated concept. Neurosurgery 1993;32(1):111–120 Neuropediatrics
Vol. 46
No. 1/2015
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
presented mild to moderate behavioral problems, which is comparable with other results. 8,17 The incidence of behavioral abnormalities has to be attributed to the severity of TBI and thus, behavioral abnormalities are probably no explicit complication following DC. But long hospitalization due to DC and the following complications can lead to a delayed or even poorer recovery33 and might have an impact on cognitive and behavioral development.
Pechmann et al.
Craniectomy after Severe TBI in Children: Complications and Outcome
Pechmann et al.
20 Liu Y, Gong J, Li F, Wang H, Zhu S, Wu C. Traumatic subdural
27 Piedra MP, Thompson EM, Selden NR, Ragel BT, Guillaume DJ.
hydroma: clinical characteristics and classification. Injury 2009; 40(9):968–972 Jeon SW, Choi JH, Jang TW, Moon SM, Hwang HS, Jeong JH. Risk factors associated with subdural hygroma after decompressive craniectomy in patients with traumatic brain injury: a comparative study. J Korean Neurosurg Soc 2011;49(6):355–358 Honeybul S, Ho KM. Incidence and risk factors for post-traumatic hydrocephalus following decompressive craniectomy for intractable intracranial hypertension and evacuation of mass lesions. J Neurotrauma 2012;29(10):1872–1878 Giza CC, Mink RB, Madikians A. Pediatric traumatic brain injury: not just little adults. Curr Opin Crit Care 2007;13(2):143–152 Shi SS, Zhang GL, Zeng T, Lin YF. Posttraumatic hydrocephalus associated with decompressive cranial defect in severe braininjured patients. Chin J Traumatol 2011;14(6):343–347 Chang V, Hartzfeld P, Langlois M, Mahmood A, Seyfried D. Outcomes of cranial repair after craniectomy. J Neurosurg 2010; 112(5):1120–1124 Grant GA, Jolley M, Ellenbogen RG, Roberts TS, Gruss JR, Loeser JD. Failure of autologous bone-assisted cranioplasty following decompressive craniectomy in children and adolescents. J Neurosurg 2004;100(2, Suppl Pediatrics):163–168
Optimal timing of autologous cranioplasty after decompressive craniectomy in children. J Neurosurg Pediatr 2012;10(4): 268–272 Bowers CA, Riva-Cambrin J, Hertzler DA II, Walker ML. Risk factors and rates of bone flap resorption in pediatric patients after decompressive craniectomy for traumatic brain injury. J Neurosurg Pediatr 2013;11(5):526–532 Martin KD, Franz B, Kirsch M, et al. Autologous bone flap cranioplasty following decompressive craniectomy is combined with a high complication rate in pediatric traumatic brain injury patients. Acta Neurochir (Wien) 2014;156(4):813–824 Annegers JF, Hauser WA, Coan SP, Rocca WA. A population-based study of seizures after traumatic brain injuries. N Engl J Med 1998; 338(1):20–24 Frey LC. Epidemiology of posttraumatic epilepsy: a critical review. Epilepsia 2003;44(Suppl 10):11–17 Hahn YS, Fuchs S, Flannery AM, Barthel MJ, McLone DG. Factors influencing posttraumatic seizures in children. Neurosurgery 1988;22(5):864–867 Honeybul S, Ho KM. Long-term complications of decompressive craniectomy for head injury. J Neurotrauma 2011;28(6): 929–935
21
22
23 24
25
26
Neuropediatrics
Vol. 46
No. 1/2015
28
29
30
31 32
33
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
12
Copyright of Neuropediatrics is the property of Georg Thieme Verlag Stuttgart and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
