- Email: [email protected]
Current Perspectives in the Surgical Treatment of Severe Traumatic Brain Injury
Literature Review
Current Perspectives in the Surgical Treatment of Severe Traumatic Brain Injury Lorenzo Giammattei1, Mahmoud Messerer1, Iype Cherian2, Daniele Starnoni1, Rodolfo Maduri1, Ekkehard M. Kasper3, Roy T. Daniel1
Key words Cisternostomy - Decompressive craniectomy - External ventricular drain - Traumatic brain injury -
Abbreviations and Acronyms aSAH: Aneurysmal subarachnoid hemorrhage CSF: Cerebrospinal fluid DC: Decompressive craniectomy EVD: External ventricular drain ICP: Intracranial pressure SAH: Subarachnoid hemorrhage TBI: Traumatic brain injury From the 1Department of Neurosurgery, Lausanne University Hospital, Lausanne, Switzerland; 2Department of Neurosurgery, College of Medical Sciences, Bharatpur, Nepal; and 3Division of Neurosurgery, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA To whom correspondence should be addressed: Lorenzo Giammattei, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018) 116:322-328. https://doi.org/10.1016/j.wneu.2018.05.176 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
INTRODUCTION Traumatic brain injury (TBI) remains a leading cause of death and disability for people of all ages1 and has a significant economic impact because of the financial resources needed to take care of such patients in the acute care setting as well as in a long-term setting. The pathogenesis of TBI includes a primary injury that is directly related to the physical impact on the brain (mostly related to the kinetic energy of the trauma) and a delayed secondary injury that is caused by the subsequent molecular, chemical, and inflammatory cascades. This situation can result in intracranial hypertension and/or cerebral ischemia. An uncontrolled increase in intracranial pressure (ICP) can occur immediately or after a certain delay and confers a poor prognosis.2 Therefore, control of intracranial hypertension is imperative in patients with severe TBI. In
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- BACKGROUND:
The available surgical options to control increased intracranial pressure and to limit secondary brain damage in the setting of severe traumatic brain injury (TBI) include decompressive craniectomy, cisternostomy, and other methods to divert cerebrospinal fluid (CSF) such as placement of an external ventricular drain.
- METHODS:
We discuss the rationale and the limitations of these surgical techniques based on preclinical and clinical evidence. A detailed description of the differences between ventricular CSF drainage and cisternal drainage is added based on recent hypotheses on TBI physiopathology and CSF circulation.
- RESULTS:
Cisternostomy seems a more physiological approach to the treatment of brain swelling, with the potential of effectively controlling intracranial pressure and reducing the effects of secondary brain damage.
- CONCLUSIONS:
Further clinical studies need to be performed to validate the efficacy of this emerging surgical procedure for severe TBI.
this report, we focus on available surgical options to control increased ICP and to limit secondary brain damage in the setting of severe TBI. To this end, we discuss decompressive craniectomy (DC), cisternostomy, and other methods to divert cerebrospinal fluid (CSF) such as placement of an external ventricular drain (EVD) and we elaborate on their respective rationale and possible controversies. Decompressive Craniectomy DC is an effective surgical procedure to control increased ICP and was first described in 1901 by Kocher.3 Surgical intervention consists of 2 steps: first, to remove a sizable portion of the calvarium and second, to open the dura mater with the aim of creating more space for the swollen brain, thereby reducing ICP. The 2 most popular versions of DC are hemicraniectomy and bifrontal craniectomy and their respective use is based on the topography of the cerebral insult.4 The patient population with TBI who may benefit from DC can be divided into 3 main groups: 1) Patients presenting with a circumscript hemorrhagic lesion exerting a mass
effect. Suitable patients can undergo craniotomy and evacuation of the hematoma,5 and in cases of intraoperative brain swelling, the bone flap is not replaced. Alternatively, the bone flap is not replaced as a precautionary measure if there is a high chance that the patient may develop further brain swelling (prophylactic DC).6 2) Patients with a traumatic mass lesion can undergo craniotomy with the bone flap being placed back at the end of surgery because of a lax brain; failure of ICP control despite maximal medical therapy in this patient group can later lead to the decision to remove the bone flap in a second setting. 3) Patients who present without a predominantly focal mass lesion after severe TBI (e.g., patients with multiple cerebral contusions and diffuse axonal injury, usually bilateral). In this patient population, neuromonitoring has traditionally been the mainstay of care. Here, DC could be performed as a rescue procedure in cases of refractory ICP despite maximal medical treatment. Maximal medical treatment for such patients usually includes sedation,
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hyperventilation, and osmotherapy7 and in certain cases, also hypothermia. In this patient group, DC is often performed before (or instead of) the institution of barbiturate coma. Preclinical Studies of DC. Results of DC in animal models remain controversial. Some studies8 have reported positive effects of intervention, whereas others9 have reported a significant procedural association with brain edema and contusions undergoing hemorrhagic transformation leading to increased functional impairment. A recent mathematical model confirmed an intuitive finding that DC successfully reduces global ICP measures, but does so at the expense of inducing local anatomic zones of extreme tissue strain and stretch.10 The latter concept has been corroborated by a radiographic study that showed focally increased strain levels and increased water content after DC.11 In particular, von Holst et al.11 found areas sustaining a high level of strain and especially in regions in which the brain tissue was close to the edges of the postsurgical skull defect, possibly resulting in physiologic brain dysfunction. These findings have raised concerns regarding the appropriate use of DC and have contributed to the uncertainties surrounding the clinical indications and technical demands for performing adequate DC. So over years of clinical practice, DC has gone through several periods of favor and despair.12,13 Clinical Outcome After DC: Review of the Available Evidence. The 2 largest randomized clinical trials that have investigated the role of DC in the setting of severe TBI are the Decompressive Craniectomy (DECRA) trial14 and the subsequently performed Randomised Evaluation of Surgery with Craniectomy for Uncontrollable Elevation of Intracranial Pressure (RESCUEicp) trial.7 The DECRA trial14 investigated the role of early bifrontal DC in cases of diffuse brain swelling without lesion with mass effect. The patients were randomly assigned to DC or medical treatment if they developed intracranial hypertension (defined as ICP >20 mm Hg for >15 minutes in a 1-hour period) despite optimized first-tier interventions. The DECRA trial showed that early DC was an effective measure in reducing ICP and shortened the duration of mechanical ventilation and
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length of stay in the intensive care unit but was associated with more unfavorable outcomes. In particular, the number of patients scoring a value of 1e4 on the Extended Glasgow Outcome Scale was higher in patients in the surgical arm compared with patients in the medical arm (70% vs. 51%, respectively). However, this difference concerning outcome vanished after adjusting the results for the baseline covariates such as pupillary reactivity.15 Some criticisms have been brought forward regarding this trial especially with respect to patient randomization, and it was opined that the ICP threshold used does not reflect current clinical practice. Other critical points raised were the high crossover rate from the medical to the surgical arm16 and the unusual surgical technique (bifrontal craniectomy without division of the sagittal sinus and the falx).6 Despite these criticisms, the DECRA trial was important in establishing that there is no role for early DC, thus confirming that it is appropriate to proceed with second-tier and third-tier medical therapies, maintaining a role for DC as a last-tier treatment.6 Based on these premises, the RESCUEicp trial7 was designed to assess the effectiveness of DC as a last-tier treatment for patients with refractory ICP increase. The 2 most important differences with DECRA with respect to patients’ enrolment were a higher ICP threshold (>25 mm Hg for 1e12 hours despite maximal medical treatment, except barbiturates), which reflects a more widely accepted definition of refractory ICP,6 and inclusion of patients with intracranial hematoma evacuated. This study aimed to depict a more realistic application of DC considering that most neurosurgeons and intensivists would not resort to DC in cases of ICP >20 mm Hg for 15 minutes but would instead increment medical therapy.17 The RESCUEicp trial showed that DC resulted in lower mortality but at the cost of higher rates of patients who remained in a vegetative state and/or with severe disability. The investigators of that trial argued that at their 6-month follow-up point, a favorable outcome occurred in 42.8% of patients who had undergone DC, whereas this was observed in only 34.6% of patients who were medically treated. However, their definition of a favorable outcome also included patients who were left with
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severe disability, which is of some concern.18 Moreover, some criticisms have been raised about the relatively high crossover rate from the medical to the surgical arm and the choice of surgical technique (unilateral frontotemporoparietal or bifrontal craniectomy), which was based on imaging interpretations and surgeon’s discretion.18 This study has confirmed that reduction of mortality is associated with a higher risk of surviving with severe disability, raising important ethical issues.19 When considering DC, another argument brought forward is that the subsequent procedure of cranioplasty also carries a not insignificant rate of complications that cannot be ignored (including a high rate of infections, reoperations, intracranial hemorrhage, extra-axial fluid collection, hydrocephalus, seizures, and subsequent bone flap resorptions, with a total complication rate that ranges from 10% to as high as 40%).20
Cisternostomy The controversies surrounding DC prompted the neurosurgical community to seek surgical solutions other than DC for suitable treatment of severe TBI. New perspectives have evolved as a result of the innovative contributions of Cherian et al.,21 who introduced the concept of performing a cisternostomy in the setting of severe TBI. This procedure is defined by opening the cisternal compartments surrounding the base of the brain and leaving a drain behind in the cistern, allowing the compartment to stay open to atmospheric pressure. The procedure requires 1 surgical step in addition to a classic frontotemporal trauma flap, which involves epidural drilling to provide an access corridor to the basal cisterns. An inferior lateral frontal dural opening is performed to access the basal cisterns. The opticocarotid cistern is first reached and CSF is drained to achieve immediate brain relaxation, after which the lamina terminalis and even the posterior fossa cisterns are opened. Subarachnoid blood is drained and the cisterns are left in communication to one another. At the end of the procedure, a drain is left in the cisternal compartment, which remains in place for approximately 5e6 days. Once the brain is relaxed, the dura can be opened over the convexity in a conventional manner to also address subdural or
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intraparenchymatous hemorrhage, should there be a need to do so. The underlying rationale of this procedure lies in the emerging recognition of the pivotal role of the paravascular Virchow-Robin spaces (the so-called glymphatic system) and their relevance for CSF circulation,22-24 as represented in Figure 1. In the setting of severe TBI, there is almost always a significant amount of associated subarachnoid hemorrhage (SAH). It is believed that this SAH leads to an increase in pressure in the basal cisterns (by clogging the natural CSF drainage pathways), thus producing an outflow congestion or shift of fluid toward the brain, which then leads to brain swelling via the development of CSF shift edema. The procedure of opening the basal cisterns can hence reduce the development of CSF shift edema by reopening the fluid pathways from the brain toward the basal cisterns via the Virchow-Robin spaces.21 The surgical technique of opening the basal cisterns to release additional CSF to relax the brain and to facilitate intracranial surgery was popularized by Yasargil et al.25 and forms one of the mainstays of surgical techniques in vascular and skull base surgery. The idea of continued cisternal CSF drainage is also not new and has previously been used in the setting of acute
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aneurysmal SAH (aSAH) surgery.21 The surgical procedure in itself (although new in trauma surgery) is a standard procedure that forms an integral part of skull base and vascular surgery. In cases of aSAH surgery, this procedure seems to be of paramount importance and the necessary steps of this surgical technique are similar to those of proposed cisternostomy in cases of severe TBI. However, cisternostomy in the setting of severe TBI has faced some controversial arguments: 1) The pathophysiologic rationale involving the glymphatic system and paravascular pathways and their respective impairment by traumatic SAH is relatively new and some discrepancies exist in the literature concerning the various structures involved. Central to the concept is the ability to reverse CSF shift edema. Despite preclinical evidence,22,26,27 the existence and reversal of CSF shift edema need to be validated by clinicoradiologic data. Clinical evidence for direction of fluid flow and interstitial waste clearance caused by cisternostomy needs to be assessed.28 2) One of the main criticisms of cisternostomy is the fact that its effect could be solely related to the greater amount of CSF drainage. With this
technique, the rate of CSF drained is higher than that of an EVD. This situation comes about primarily because this drain allows, at the same time, the removal of CSF in the basal cisterns and in the ventricular compartment as a result of the opening of the lamina terminalis. The effect of this significant drainage on ICP and cerebral perfusion pressure control cannot be overstated. Moreover, the cisternal drain does not have the technical and procedural limitations in cannulating the ventricles in cases of brain swelling, which is often the case with ventricular drains. However, the effects of cisternostomy, besides those previously mentioned, need to be proved. 3) Clinical experience has been limited to only a few centers that have embarked on studying this surgical approach29-31 and its impact on clinical outcome, including the optimal timing, needs to be investigated. 4) The surgical procedure in itself requires training in basic vascular and skull base surgery and has a learning curve. This factor needs to be considered, because cisternal opening in cases of extremely swollen brains cannot be performed by inexperienced surgeons. Elevation of the frontal lobe in cases of brain swelling is challenging and carries the risk of iatrogenic contusions. However, the complications related to this procedure can be minimized if the following surgical steps are followed: Performing a craniotomy that includes the removal of the sphenoid ridge at least until the superior orbital fissure Performing a small basal durotomy to avoid brain herniation and to limit the area of frontal lobe exposed to iatrogenic contusions Removing the associated subdural hematoma or contusions to reduce brain herniation
Figure 1. The current pathways recognized for the exchange of fluid within the intracranial compartment. According to a new hypothesis,21 the fluid exchange between the cisterns and the brain parenchyma, through the paravascular Virchow-Robin spaces, may be of greater importance than the traditionally recognized transfer of fluid within the ventricular system and its absorption at the level of the sinuses.
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In cases of severe brain swelling that cannot be managed by removal of hematomas, resection of the temporal pole32 through a small basal durotomy (which is often a part of a burst temporal lobe) gives early
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access to the cisterns. It is usually the first cistern that is difficult to reach. Once this cistern is opened, the subsequent cisternal openings are easier because the brain becomes lax. 5) Severe TBI can be an extremely heterogeneous entity (acute subdural hematoma, multiple intraparenchymal contusions, diffuse post-traumatic SAH, brain swelling without mass effect) and only multicentric clinical trials would elucidate the proper indications for cisternostomy. In a preliminary phase, cisternostomy should probably be considered as an adjuvant surgical strategy complementary rather than alternative to DC.21 Once its safety, feasibility and effects on outcome are well studied, we could then decide on its applicability as an alternative to DC. In clinical practice, the surgical indications for cisternostomy are comparable to those established for DC. In particular, cisternostomy can be considered in 3 distinct clinical scenarios: 1) Severe TBI with concomitant acute subdural hematoma when the brain is expected to be swollen after evacuation of the hematoma. In this case, cisternostomy is to be considered as an adjunct to the primary procedure. 2) Severe TBI with multiple cerebral contusion developing refractory intracranial hypertension despite maximal medical treatment. In this scenario, cisternostomy is considered as a lasttier treatment. 3) Severe TBI with a significant SAH burden, in which the development of increased ICP is predictable. This is a scenario that lends itself to a prospective randomized trial of prophylactic cisternostomy versus cisternostomy after demonstration of increased ICP. Preclinical Studies Constituting the Rationale of Cisternostomy. The classic theory of CSF circulation presupposes that CSF is produced in the choroid plexus and then circulates from the ventricles along the subarachnoid spaces to be reabsorbed at the level of the dural sinuses by a distinct mechanism involving the pacchionian
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granulations. However, more recently, a different model has been proposed according to which the CSF is continuously produced and absorbed in the entire CSF system, with a pivotal role for the paravascular Virchow-Robin spaces for CSF circulation.24,33 This model has been further supported by molecular studies in an animal model.34 These paravascular pathways that seem to assume great relevance for CSF circulation have been extensively characterized by Iliff et al.22,26,27 These studies22,27 also showed that the fluid exchange between cisterns and brain parenchyma was significantly more intense than the exchange between the ventricles and brain parenchyma. Other investigators found that CSF enters the brain parenchyma along para-arterial spaces where it mixes with interstitial fluid and its solutes before it is removed through paravenous spaces.28 The investigators26,27 found that perivascular CSF circulation was mediated by the astroglial water channel aquaporin 4, thus leading to the term glial-lymphatic or glymphatic system. Since this description, further studies have explored the glymphatic system and its role in metabolic waste clearance, immune surveillance, distribution of nutrients to the brain, paracrine signaling, and probably other functionality.35 The study by Iliff et al.26 also showed that after TBI, there was an impairment in the function of the glymphatic system, with a subsequent decrease in the drainage of interstitial fluid. According to these findings, it is reasonable to propose that such a shift of fluid back toward the brain could significantly contribute to brain swelling after severe TBI. Cisternostomy addresses this outflow obstruction and CSF shift edema and aims at reversing the shift by draining the fluid from the cisterns to the exterior. Another aspect that deserves consideration is the fact that some factors (such as oxygen free radicals, histamine, kinins, and glutamate) are released during brain trauma and that these metabolites can enhance both vasogenic and cytotoxic edema.36 It can be assumed that leaving a cisternal drainage in place for some days thus facilitates the washout of such toxic metabolites. However, further studies are needed to better characterize the role of the glymphatic system in solute
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clearance. Understanding its natural role will help to resolve the controversies that exist regarding the anatomic substrates involved in the fluid exchange and the sequence of events for TBI. Clinical Outcome After Cisternostomy. The clinical experience is largely based on a study comparing 3 groups of patients with severe TBI undergoing conventional DC (284 patients), DC plus cisternostomy (272 patients), and cisternostomy alone (476 patients).29 In this large cohort study, the investigators found a significantly better clinical outcome score (mean Glasgow Outcome Scale of 3.9, 3.7, and 2.8), lower mortality (15.6%, 26.4% and 34.8%), and fewer days of assisted ventilation (2.4, 3.2, and 6.3) in the group treated with cisternostomy compared with the groups treated with either cisternostomy plus DC or DC alone. However, this study has some important limitations: It is a nonrandomized clinical study. No baseline clinical (Glasgow Coma Scale score, pupillary status) and radiologic information were provided and, thus, the homogeneity of the analyzed groups cannot be verified. Results were not supported by a statistical analysis. Follow-up is limited to 6 weeks after surgery, whereas most TBI studies report outcome at 6e12 months after treatment.7,14 Apart from this pilot study, the current literature on cisternostomy consists only of case reports.30,31 Other Techniques for CSF Diversion Placement of an EVD is a basic neurosurgical procedure and is one of the most common methods to assess and relieve increased ICP.2 It is therefore reasonable to propose this procedure as a secondtier therapy in cases of refractory intracranial hypertension.2 How Does EVD Placement Compare with Cisternal CSF Drainage? Physiological Remarks. CSF in the central nervous system is distributed as follows: approximately 30 mL is located within in the
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4 ventricles and another 110 mL resides in the subarachnoid spaces.37 The amount of CSF that can be drained from the cisterns is therefore larger. In cases of severe TBI with refractory hypertension, even after accurate EVD positioning, the result is usually a collapsed ventricular system with subsequent failure of any EVD drainage. The procedure of cisternostomy, which includes lamina terminalis fenestration, on the other hand, enables both compartments (ventricular and subarachnoid space) to be drained, resulting in more efficient drainage. A cisternal drain, as opposed to a ventricular drain, enables the reversal of the CSF shift edema and facilitates interstitial solute clearance,27 thus directly addressing the problem posed by worsening brain edema. This is a scenario commonly seen after a certain delay after severe TBI. The technique of opening (and cleaning out) the cisterns with continuous drainage then allows fluids to move more rapidly from the interstitial compartment of the brain toward the cisterns and then to the outside (into a CSF diversion system). This concept needs further preclinical and clinical studies to be confirmed because it could be argued that cisternostomy, instead of reversing CSF shift edema, simply addresses a larger amount of CSF and thus better ICP control. From a speculative point of view, the cisternal drain could also be used as an EVD to assess ICP. The technique of cisternostomy presupposes leaving the drain in the prepontine cistern and this, when coupled with a standard intraparenchymal ICP monitor, allows exploration of pressure distribution within the cisternal compartment, leading to interesting future research.38 Delayed post-traumatic hydrocephalus is a common complication after TBI and it is probably caused by CSF circulatory obstruction and/or problems with CSF absorption. A recent study39 showed that severe SAH or intraventricular hemorrhage is a strong and significant predictor for the development of post-traumatic hydrocephalus. Similarly, in aSAH, blood and blood products can obstruct CSF circulation, hinder absorption, or create aseptic inflammation causing hydrocephalus. A recent study by the group of Lawton40 showed that opening of the lamina
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terminalis and membrane of Lillequist significantly reduced the rates of shuntdependent hydrocephalus after aSAH. However, aSAH and traumatic SAH are different etiopathologies. The mechanisms triggering the development of subsequent hydrocephalus are probably the same. The technique of cisternostomy that includes evacuation of subarachnoid blood, opening of the lamina terminalis, and continuous cisternal drainage can reduce the rate of development of delayed post-traumatic hydrocephalus, although this needs to be corroborated by further clinical studies. Vasospasm, although well recognized after aSAH, is an underestimated entity in severe TBI.41 Several investigators have tried to assess the clinical value of removing blood clot burden and irrigating the cisterns in aSAH with the intention of reducing the rates for vasospasm, but results have been discordant.42-44 Future studies in trauma are needed to see if the procedure of cisternostomy, including removal of subarachnoid blood clots and washing the cisterns, has additional positive effects in the prevention of posttraumatic vasospasm. Clinical Experience with EVD. Liu et al.45 in their prospective observational study on severe TBI reported a significantly lower rate of refractory intracranial hypertension (and consequently, fewer decompressive craniectomies) and better outcome in patients managed with EVD compared with patients managed with intraparenchymal pressure monitors. However, controversy exists about the feasibility of using EVD to monitor ICP, namely difficulties in cannulating the ventricles in cases of brain swelling and frequent failure of the system caused by blood clots, infections, and hemorrhages.46 Another important issue is reliability of ICP signal from an open EVD, which has been recently investigated by Hockel et al.47 These investigators concluded that if CSF drainage is needed (according to the clinical situation), patients should receive an EVD with an integrated ICP probe or EVD line plus a separate ICP probe; the common practice of assessing ICP via open EVD with frequent clamping of the catheter is suitable only for overall ICP trend assessment. These factors have contributed to the widespread use of intraparenchymal ICP
monitors, which seems to be associated with fewer complications at the expense of high costs and inability to drain CSF, with the consequent necessity of heavier sedation, osmotherapy, hyperventilation, and barbiturates.48 Despite these controversies ventricular fluidecoupled ICP monitoring is still considered the gold standard of ICP monitoring.49 The literature concerning the efficacy of this method (EVD placement in the setting of severe TBI) remains poor (level of recommendation III according to the guidelines for the management of severe traumatic brain injury).50 Timofeev et al.51 described their experience with EVD placement to control increased ICP in cases in which ventricular size was deemed appropriate by the neurosurgeon. Ventricular size is one of the most important factors limiting the impact of this surgical maneuver because in cases of very small or collapsed ventricles, the amount of CSF that can be drained is often insufficient.2 The investigators achieved a rapid decrease of ICP in their patients but initial ICP reduction was followed by gradual or rapid re-increase to values exceeding 20 mm Hg by the end of a 24hour period in almost half of their patient population. Bhargava et al.52 described their experience in achieving good control of ICP in a group of patients with refractory increased ICP, although a selection bias cannot be excluded considering that the patients undergoing EVD or DC were not randomly selected. However, in cases of compressed ventricles or with major midline shift, adequate EVD positioning can be challenging and may require the use of neuronavigation.53 In severe TBI, there is often significant associated intraventricular hemorrhage, which potentially leads to drain failure with the necessity of repeated access to the system for flushing of the catheter, which then carries an increased risk for possible infection.2 CONCLUSIONS Current recommendations for the surgical treatment of ICP in severe TBI have focused on DC (as the primary or secondary procedure of choice) with or without EVD.50 However, the recently introduced concept of cisternostomy
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seems to offer a more physiologic approach to the treatment of brain swelling, with the potential for effectively controlling ICP and reducing the effects of secondary brain damage. Other potential benefits such as reducing rates of vasospasm and hydrocephalus also need to be considered. This brief overview based on current knowledge of the surgical treatment of severe TBI aims to stimulate a debate within the neurosurgical community on the relative merits of DC and cisternostomy with a view to proposing a multicentric randomized clinical study. REFERENCES 1. Weiner GM, Lacey MR, Mackenzie L, Shah DP, Frangos SG, Grady MS, et al. Decompressive craniectomy for elevated intracranial pressure and its effect on the cumulative ischemic burden and therapeutic intensity levels after severe traumatic brain injury. Neurosurgery. 2010;66:1111-1118 [discussion: 1118-1119]. 2. Li LM, Timofeev I, Czosnyka M, Hutchinson PJ. Review article: the surgical approach to the management of increased intracranial pressure after traumatic brain injury. Anesth Analg. 2010;111: 736-748. 3. T Kocher. Hirnerschütterung, Hirndruck und chirurgische Eingriffe bei Hirnerkrankungen. In: Nothnagel H, ed. Specielle Pathologie und Therapie. Wien: A Hölder. 1901;9(pt. 3: 81e290):325e367 [in German]. 4. Galgano M, Toshkezi G, Qiu X, Russell T, Chin L, Zhao LR. Traumatic brain injury: current treatment strategies and future endeavors. Cell Transplant. 2017;26:1118-1130. 5. Mendelow AD, Gregson BA, Rowan EN, Francis R, McColl E, McNamee P, et al. Early surgery versus initial conservative treatment in patients with traumatic intracerebral hemorrhage (STITCH[Trauma]): the first randomized trial. J Neurotrauma. 2015;32:1312-1323.
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8. Zweckberger K, Eros C, Zimmermann R, Kim SW, Engel D, Plesnila N. Effect of early and delayed decompressive craniectomy on secondary brain damage after controlled cortical impact in mice. J Neurotrauma. 2006;23:1083-1093.
23. Oreskovic D, Klarica M. A new look at cerebrospinal fluid movement. Fluids Barriers CNS. 2014;11:16.
9. Szczygielski J, Mautes AE, Muller A, Sippl C, Glameanu C, Schwerdtfeger K, et al. Decompressive craniectomy increases brain lesion volume and exacerbates functional impairment in
24. Oreskovic D, Klarica M. The formation of cerebrospinal fluid: nearly a hundred years of interpretations and misinterpretations. Brain Res Rev. 2010;64:241-262. 25. Yasargil MG, Kasdaglis K, Jain KK, Weber HP. Anatomical observations of the subarachnoid
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27. Iliff JJ, Goldman SA, Nedergaard M. Implications of the discovery of brain lymphatic pathways. Lancet Neurol. 2015;14:977-979. 28. Bacyinski A, Xu M, Wang W, Hu J. The paravascular pathway for brain waste clearance: current understanding, significance and controversy. Front Neuroanat. 2017;11:101. 29. Cherian I, Yi G, Munakomi S. Cisternostomy: Replacing the age old decompressive hemicraniectomy? Asian J Neurosurg. 2013;8:132-138. 30. Giammattei L, Messerer M, Oddo M, Borsotti F, Levivier M, Daniel RT. Cisternostomy for refractory posttraumatic intracranial hypertension. World Neurosurg. 2018;109:460-463. 31. Masoudi MS, Rezaee E, Hakiminejad H, Tavakoli M, Sadeghpoor T. Cisternostomy for management of intracranial hypertension in severe traumatic brain injury; case report and literature review. Bull Emerg Trauma. 2016;4:161-164. 32. Oncel D, Demetriades D, Gruen P, Salim A, Inaba K, Rhee P, et al. Brain lobectomy for severe head injuries is not a hopeless procedure. J Trauma. 2007;63:1010-1013. 33. Bulat M, Klarica M. Recent insights into a new hydrodynamics of the cerebrospinal fluid. Brain Res Rev. 2011;65:99-112. 34. Igarashi H, Tsujita M, Kwee IL, Nakada T. Water influx into cerebrospinal fluid is primarily controlled by aquaporin-4, not by aquaporin-1: 17O JJVCPE MRI study in knockout mice. Neuroreport. 2014;25:39-43. 35. Plog BA, Nedergaard M. The glymphatic system in central nervous system health and disease: past, present, and future. Annu Rev Pathol. 2018;13: 379-394. 36. Unterberg AW, Stover J, Kress B, Kiening KL. Edema and brain trauma. Neuroscience. 2004;129: 1021-1029. 37. Weller RO, Galea I, Carare RO, Minagar A. Pathophysiology of the lymphatic drainage of the central nervous system: implications for pathogenesis and therapy of multiple sclerosis. Pathophysiology. 2010;17:295-306. 38. Moyse E, Ros M, Marhar F, Swider P, Schmidt EA. Characterisation of supra- and infratentorial ICP profiles. Acta Neurochir Suppl. 2016;122:37-40. 39. Chen H, Yuan F, Chen SW, Guo Y, Wang G, Deng ZF, et al. Predicting posttraumatic hydrocephalus: derivation and validation of a risk scoring system based on clinical characteristics. Metab Brain Dis. 2017;32:1427-1435. 40. Winkler EA, Burkhardt JK, Rutledge WC, Rick JW, Partow CP, Yue JK, et al. Reduction of shunt dependency rates following aneurysmal subarachnoid
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hemorrhage by tandem fenestration of the lamina terminalis and membrane of Liliequist during microsurgical aneurysm repair. J Neurosurg. 2017:1-7. https:// doi.org/10.3171/2017.5.JNS163271. [Epub ahead of print].
45. Liu H, Wang W, Cheng F, Yuan Q, Yang J, Hu J, et al. External ventricular drains versus intraparenchymal intracranial pressure monitors in traumatic brain injury: a prospective observational study. World Neurosurg. 2015;83:794-800.
41. Oertel M, Boscardin WJ, Obrist WD, Glenn TC, McArthur DL, Gravori T, et al. Posttraumatic vasospasm: the epidemiology, severity, and time course of an underestimated phenomenon: a prospective study performed in 299 patients. J Neurosurg. 2005;103:812-824.
46. Valadka AB. Are external ventricular drains better than parenchymal intracranial pressure monitors in trauma patients? World Neurosurg. 2015;84: 211-213.
42. Nakagomi T, Furuya K, Nagashima H, Tanaka J, Ishii T, Takanashi S, et al. Surgical procedure and results of cisternal washing therapy for the prevention of cerebral vasospasm following SAH. Acta Neurochir Suppl. 2011;110:105-109. 43. Yamamoto T, Mori K, Esaki T, Nakao Y, Tokugawa J, Watanabe M. Preventive effect of continuous cisternal irrigation with magnesium sulfate solution on angiographic cerebral vasospasms associated with aneurysmal subarachnoid hemorrhages: a randomized controlled trial. J Neurosurg. 2016;124:18-26. 44. Kodama N, Sasaki T, Kawakami M, Sato M, Asari J. Cisternal irrigation therapy with urokinase and ascorbic acid for prevention of vasospasm after aneurysmal subarachnoid hemorrhage. Outcome in 217 patients. Surg Neurol. 2000;53: 110-117 [discussion: 117-118].
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47. Hockel K, Schuhmann MU. ICP monitoring by open extraventricular drainage: common practice but not suitable for advanced neuromonitoring and prone to false negativity. Acta Neurochir Suppl. 2018;126:281-286. 48. Aiolfi A, Khor D, Cho J, Benjamin E, Inaba K, Demetriades D. Intracranial pressure monitoring in severe blunt head trauma: does the type of monitoring device matter? J Neurosurg. 2018;128: 828-833. 49. Akbik OS, Krasberg M, Nemoto EM, Yonas H. Effect of cerebrospinal fluid drainage on brain tissue oxygenation in traumatic brain injury. J Neurotrauma. 2017;34:3153-3157.
51. Timofeev I, Dahyot-Fizelier C, Keong N, Nortje J, Al-Rawi PG, Czosnyka M, et al. Ventriculostomy for control of raised ICP in acute traumatic brain injury. Acta Neurochir Suppl. 2008;102:99-104. 52. Bhargava D, Alalade A, Ellamushi H, Yeh J, Hunter R. Mitigating effects of external ventricular drain usage in the management of severe head injury. Acta Neurochir (Wien). 2013;155:2129-2132. 53. AlAzri A, Mok K, Chankowsky J, Mullah M, Marcoux J. Placement accuracy of external ventricular drain when comparing freehand insertion to neuronavigation guidance in severe traumatic brain injury. Acta Neurochir (Wien). 2017;159: 1399-1411.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 1 April 2018; accepted 24 May 2018 Citation: World Neurosurg. (2018) 116:322-328. https://doi.org/10.1016/j.wneu.2018.05.176 Journal homepage: www.WORLDNEUROSURGERY.org
50. Carney N, Totten AM, O’Reilly C, Ullman JS, Hawryluk GW, Bell MJ, et al. Guidelines for the management of severe traumatic brain injury, fourth edition. Neurosurgery. 2017;80:6-15.
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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Current Perspectives in the Surgical Treatment of Severe Traumatic Brain Injury Lorenzo Giammattei1, Mahmoud Messerer1, Iype Cherian2, Daniele Starnoni1, Rodolfo Maduri1, Ekkehard M. Kasper3, Roy T. Daniel1
Key words Cisternostomy - Decompressive craniectomy - External ventricular drain - Traumatic brain injury -
Abbreviations and Acronyms aSAH: Aneurysmal subarachnoid hemorrhage CSF: Cerebrospinal fluid DC: Decompressive craniectomy EVD: External ventricular drain ICP: Intracranial pressure SAH: Subarachnoid hemorrhage TBI: Traumatic brain injury From the 1Department of Neurosurgery, Lausanne University Hospital, Lausanne, Switzerland; 2Department of Neurosurgery, College of Medical Sciences, Bharatpur, Nepal; and 3Division of Neurosurgery, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA To whom correspondence should be addressed: Lorenzo Giammattei, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018) 116:322-328. https://doi.org/10.1016/j.wneu.2018.05.176 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
INTRODUCTION Traumatic brain injury (TBI) remains a leading cause of death and disability for people of all ages1 and has a significant economic impact because of the financial resources needed to take care of such patients in the acute care setting as well as in a long-term setting. The pathogenesis of TBI includes a primary injury that is directly related to the physical impact on the brain (mostly related to the kinetic energy of the trauma) and a delayed secondary injury that is caused by the subsequent molecular, chemical, and inflammatory cascades. This situation can result in intracranial hypertension and/or cerebral ischemia. An uncontrolled increase in intracranial pressure (ICP) can occur immediately or after a certain delay and confers a poor prognosis.2 Therefore, control of intracranial hypertension is imperative in patients with severe TBI. In
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- BACKGROUND:
The available surgical options to control increased intracranial pressure and to limit secondary brain damage in the setting of severe traumatic brain injury (TBI) include decompressive craniectomy, cisternostomy, and other methods to divert cerebrospinal fluid (CSF) such as placement of an external ventricular drain.
- METHODS:
We discuss the rationale and the limitations of these surgical techniques based on preclinical and clinical evidence. A detailed description of the differences between ventricular CSF drainage and cisternal drainage is added based on recent hypotheses on TBI physiopathology and CSF circulation.
- RESULTS:
Cisternostomy seems a more physiological approach to the treatment of brain swelling, with the potential of effectively controlling intracranial pressure and reducing the effects of secondary brain damage.
- CONCLUSIONS:
Further clinical studies need to be performed to validate the efficacy of this emerging surgical procedure for severe TBI.
this report, we focus on available surgical options to control increased ICP and to limit secondary brain damage in the setting of severe TBI. To this end, we discuss decompressive craniectomy (DC), cisternostomy, and other methods to divert cerebrospinal fluid (CSF) such as placement of an external ventricular drain (EVD) and we elaborate on their respective rationale and possible controversies. Decompressive Craniectomy DC is an effective surgical procedure to control increased ICP and was first described in 1901 by Kocher.3 Surgical intervention consists of 2 steps: first, to remove a sizable portion of the calvarium and second, to open the dura mater with the aim of creating more space for the swollen brain, thereby reducing ICP. The 2 most popular versions of DC are hemicraniectomy and bifrontal craniectomy and their respective use is based on the topography of the cerebral insult.4 The patient population with TBI who may benefit from DC can be divided into 3 main groups: 1) Patients presenting with a circumscript hemorrhagic lesion exerting a mass
effect. Suitable patients can undergo craniotomy and evacuation of the hematoma,5 and in cases of intraoperative brain swelling, the bone flap is not replaced. Alternatively, the bone flap is not replaced as a precautionary measure if there is a high chance that the patient may develop further brain swelling (prophylactic DC).6 2) Patients with a traumatic mass lesion can undergo craniotomy with the bone flap being placed back at the end of surgery because of a lax brain; failure of ICP control despite maximal medical therapy in this patient group can later lead to the decision to remove the bone flap in a second setting. 3) Patients who present without a predominantly focal mass lesion after severe TBI (e.g., patients with multiple cerebral contusions and diffuse axonal injury, usually bilateral). In this patient population, neuromonitoring has traditionally been the mainstay of care. Here, DC could be performed as a rescue procedure in cases of refractory ICP despite maximal medical treatment. Maximal medical treatment for such patients usually includes sedation,
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hyperventilation, and osmotherapy7 and in certain cases, also hypothermia. In this patient group, DC is often performed before (or instead of) the institution of barbiturate coma. Preclinical Studies of DC. Results of DC in animal models remain controversial. Some studies8 have reported positive effects of intervention, whereas others9 have reported a significant procedural association with brain edema and contusions undergoing hemorrhagic transformation leading to increased functional impairment. A recent mathematical model confirmed an intuitive finding that DC successfully reduces global ICP measures, but does so at the expense of inducing local anatomic zones of extreme tissue strain and stretch.10 The latter concept has been corroborated by a radiographic study that showed focally increased strain levels and increased water content after DC.11 In particular, von Holst et al.11 found areas sustaining a high level of strain and especially in regions in which the brain tissue was close to the edges of the postsurgical skull defect, possibly resulting in physiologic brain dysfunction. These findings have raised concerns regarding the appropriate use of DC and have contributed to the uncertainties surrounding the clinical indications and technical demands for performing adequate DC. So over years of clinical practice, DC has gone through several periods of favor and despair.12,13 Clinical Outcome After DC: Review of the Available Evidence. The 2 largest randomized clinical trials that have investigated the role of DC in the setting of severe TBI are the Decompressive Craniectomy (DECRA) trial14 and the subsequently performed Randomised Evaluation of Surgery with Craniectomy for Uncontrollable Elevation of Intracranial Pressure (RESCUEicp) trial.7 The DECRA trial14 investigated the role of early bifrontal DC in cases of diffuse brain swelling without lesion with mass effect. The patients were randomly assigned to DC or medical treatment if they developed intracranial hypertension (defined as ICP >20 mm Hg for >15 minutes in a 1-hour period) despite optimized first-tier interventions. The DECRA trial showed that early DC was an effective measure in reducing ICP and shortened the duration of mechanical ventilation and
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length of stay in the intensive care unit but was associated with more unfavorable outcomes. In particular, the number of patients scoring a value of 1e4 on the Extended Glasgow Outcome Scale was higher in patients in the surgical arm compared with patients in the medical arm (70% vs. 51%, respectively). However, this difference concerning outcome vanished after adjusting the results for the baseline covariates such as pupillary reactivity.15 Some criticisms have been brought forward regarding this trial especially with respect to patient randomization, and it was opined that the ICP threshold used does not reflect current clinical practice. Other critical points raised were the high crossover rate from the medical to the surgical arm16 and the unusual surgical technique (bifrontal craniectomy without division of the sagittal sinus and the falx).6 Despite these criticisms, the DECRA trial was important in establishing that there is no role for early DC, thus confirming that it is appropriate to proceed with second-tier and third-tier medical therapies, maintaining a role for DC as a last-tier treatment.6 Based on these premises, the RESCUEicp trial7 was designed to assess the effectiveness of DC as a last-tier treatment for patients with refractory ICP increase. The 2 most important differences with DECRA with respect to patients’ enrolment were a higher ICP threshold (>25 mm Hg for 1e12 hours despite maximal medical treatment, except barbiturates), which reflects a more widely accepted definition of refractory ICP,6 and inclusion of patients with intracranial hematoma evacuated. This study aimed to depict a more realistic application of DC considering that most neurosurgeons and intensivists would not resort to DC in cases of ICP >20 mm Hg for 15 minutes but would instead increment medical therapy.17 The RESCUEicp trial showed that DC resulted in lower mortality but at the cost of higher rates of patients who remained in a vegetative state and/or with severe disability. The investigators of that trial argued that at their 6-month follow-up point, a favorable outcome occurred in 42.8% of patients who had undergone DC, whereas this was observed in only 34.6% of patients who were medically treated. However, their definition of a favorable outcome also included patients who were left with
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severe disability, which is of some concern.18 Moreover, some criticisms have been raised about the relatively high crossover rate from the medical to the surgical arm and the choice of surgical technique (unilateral frontotemporoparietal or bifrontal craniectomy), which was based on imaging interpretations and surgeon’s discretion.18 This study has confirmed that reduction of mortality is associated with a higher risk of surviving with severe disability, raising important ethical issues.19 When considering DC, another argument brought forward is that the subsequent procedure of cranioplasty also carries a not insignificant rate of complications that cannot be ignored (including a high rate of infections, reoperations, intracranial hemorrhage, extra-axial fluid collection, hydrocephalus, seizures, and subsequent bone flap resorptions, with a total complication rate that ranges from 10% to as high as 40%).20
Cisternostomy The controversies surrounding DC prompted the neurosurgical community to seek surgical solutions other than DC for suitable treatment of severe TBI. New perspectives have evolved as a result of the innovative contributions of Cherian et al.,21 who introduced the concept of performing a cisternostomy in the setting of severe TBI. This procedure is defined by opening the cisternal compartments surrounding the base of the brain and leaving a drain behind in the cistern, allowing the compartment to stay open to atmospheric pressure. The procedure requires 1 surgical step in addition to a classic frontotemporal trauma flap, which involves epidural drilling to provide an access corridor to the basal cisterns. An inferior lateral frontal dural opening is performed to access the basal cisterns. The opticocarotid cistern is first reached and CSF is drained to achieve immediate brain relaxation, after which the lamina terminalis and even the posterior fossa cisterns are opened. Subarachnoid blood is drained and the cisterns are left in communication to one another. At the end of the procedure, a drain is left in the cisternal compartment, which remains in place for approximately 5e6 days. Once the brain is relaxed, the dura can be opened over the convexity in a conventional manner to also address subdural or
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intraparenchymatous hemorrhage, should there be a need to do so. The underlying rationale of this procedure lies in the emerging recognition of the pivotal role of the paravascular Virchow-Robin spaces (the so-called glymphatic system) and their relevance for CSF circulation,22-24 as represented in Figure 1. In the setting of severe TBI, there is almost always a significant amount of associated subarachnoid hemorrhage (SAH). It is believed that this SAH leads to an increase in pressure in the basal cisterns (by clogging the natural CSF drainage pathways), thus producing an outflow congestion or shift of fluid toward the brain, which then leads to brain swelling via the development of CSF shift edema. The procedure of opening the basal cisterns can hence reduce the development of CSF shift edema by reopening the fluid pathways from the brain toward the basal cisterns via the Virchow-Robin spaces.21 The surgical technique of opening the basal cisterns to release additional CSF to relax the brain and to facilitate intracranial surgery was popularized by Yasargil et al.25 and forms one of the mainstays of surgical techniques in vascular and skull base surgery. The idea of continued cisternal CSF drainage is also not new and has previously been used in the setting of acute
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aneurysmal SAH (aSAH) surgery.21 The surgical procedure in itself (although new in trauma surgery) is a standard procedure that forms an integral part of skull base and vascular surgery. In cases of aSAH surgery, this procedure seems to be of paramount importance and the necessary steps of this surgical technique are similar to those of proposed cisternostomy in cases of severe TBI. However, cisternostomy in the setting of severe TBI has faced some controversial arguments: 1) The pathophysiologic rationale involving the glymphatic system and paravascular pathways and their respective impairment by traumatic SAH is relatively new and some discrepancies exist in the literature concerning the various structures involved. Central to the concept is the ability to reverse CSF shift edema. Despite preclinical evidence,22,26,27 the existence and reversal of CSF shift edema need to be validated by clinicoradiologic data. Clinical evidence for direction of fluid flow and interstitial waste clearance caused by cisternostomy needs to be assessed.28 2) One of the main criticisms of cisternostomy is the fact that its effect could be solely related to the greater amount of CSF drainage. With this
technique, the rate of CSF drained is higher than that of an EVD. This situation comes about primarily because this drain allows, at the same time, the removal of CSF in the basal cisterns and in the ventricular compartment as a result of the opening of the lamina terminalis. The effect of this significant drainage on ICP and cerebral perfusion pressure control cannot be overstated. Moreover, the cisternal drain does not have the technical and procedural limitations in cannulating the ventricles in cases of brain swelling, which is often the case with ventricular drains. However, the effects of cisternostomy, besides those previously mentioned, need to be proved. 3) Clinical experience has been limited to only a few centers that have embarked on studying this surgical approach29-31 and its impact on clinical outcome, including the optimal timing, needs to be investigated. 4) The surgical procedure in itself requires training in basic vascular and skull base surgery and has a learning curve. This factor needs to be considered, because cisternal opening in cases of extremely swollen brains cannot be performed by inexperienced surgeons. Elevation of the frontal lobe in cases of brain swelling is challenging and carries the risk of iatrogenic contusions. However, the complications related to this procedure can be minimized if the following surgical steps are followed: Performing a craniotomy that includes the removal of the sphenoid ridge at least until the superior orbital fissure Performing a small basal durotomy to avoid brain herniation and to limit the area of frontal lobe exposed to iatrogenic contusions Removing the associated subdural hematoma or contusions to reduce brain herniation
Figure 1. The current pathways recognized for the exchange of fluid within the intracranial compartment. According to a new hypothesis,21 the fluid exchange between the cisterns and the brain parenchyma, through the paravascular Virchow-Robin spaces, may be of greater importance than the traditionally recognized transfer of fluid within the ventricular system and its absorption at the level of the sinuses.
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In cases of severe brain swelling that cannot be managed by removal of hematomas, resection of the temporal pole32 through a small basal durotomy (which is often a part of a burst temporal lobe) gives early
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access to the cisterns. It is usually the first cistern that is difficult to reach. Once this cistern is opened, the subsequent cisternal openings are easier because the brain becomes lax. 5) Severe TBI can be an extremely heterogeneous entity (acute subdural hematoma, multiple intraparenchymal contusions, diffuse post-traumatic SAH, brain swelling without mass effect) and only multicentric clinical trials would elucidate the proper indications for cisternostomy. In a preliminary phase, cisternostomy should probably be considered as an adjuvant surgical strategy complementary rather than alternative to DC.21 Once its safety, feasibility and effects on outcome are well studied, we could then decide on its applicability as an alternative to DC. In clinical practice, the surgical indications for cisternostomy are comparable to those established for DC. In particular, cisternostomy can be considered in 3 distinct clinical scenarios: 1) Severe TBI with concomitant acute subdural hematoma when the brain is expected to be swollen after evacuation of the hematoma. In this case, cisternostomy is to be considered as an adjunct to the primary procedure. 2) Severe TBI with multiple cerebral contusion developing refractory intracranial hypertension despite maximal medical treatment. In this scenario, cisternostomy is considered as a lasttier treatment. 3) Severe TBI with a significant SAH burden, in which the development of increased ICP is predictable. This is a scenario that lends itself to a prospective randomized trial of prophylactic cisternostomy versus cisternostomy after demonstration of increased ICP. Preclinical Studies Constituting the Rationale of Cisternostomy. The classic theory of CSF circulation presupposes that CSF is produced in the choroid plexus and then circulates from the ventricles along the subarachnoid spaces to be reabsorbed at the level of the dural sinuses by a distinct mechanism involving the pacchionian
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granulations. However, more recently, a different model has been proposed according to which the CSF is continuously produced and absorbed in the entire CSF system, with a pivotal role for the paravascular Virchow-Robin spaces for CSF circulation.24,33 This model has been further supported by molecular studies in an animal model.34 These paravascular pathways that seem to assume great relevance for CSF circulation have been extensively characterized by Iliff et al.22,26,27 These studies22,27 also showed that the fluid exchange between cisterns and brain parenchyma was significantly more intense than the exchange between the ventricles and brain parenchyma. Other investigators found that CSF enters the brain parenchyma along para-arterial spaces where it mixes with interstitial fluid and its solutes before it is removed through paravenous spaces.28 The investigators26,27 found that perivascular CSF circulation was mediated by the astroglial water channel aquaporin 4, thus leading to the term glial-lymphatic or glymphatic system. Since this description, further studies have explored the glymphatic system and its role in metabolic waste clearance, immune surveillance, distribution of nutrients to the brain, paracrine signaling, and probably other functionality.35 The study by Iliff et al.26 also showed that after TBI, there was an impairment in the function of the glymphatic system, with a subsequent decrease in the drainage of interstitial fluid. According to these findings, it is reasonable to propose that such a shift of fluid back toward the brain could significantly contribute to brain swelling after severe TBI. Cisternostomy addresses this outflow obstruction and CSF shift edema and aims at reversing the shift by draining the fluid from the cisterns to the exterior. Another aspect that deserves consideration is the fact that some factors (such as oxygen free radicals, histamine, kinins, and glutamate) are released during brain trauma and that these metabolites can enhance both vasogenic and cytotoxic edema.36 It can be assumed that leaving a cisternal drainage in place for some days thus facilitates the washout of such toxic metabolites. However, further studies are needed to better characterize the role of the glymphatic system in solute
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clearance. Understanding its natural role will help to resolve the controversies that exist regarding the anatomic substrates involved in the fluid exchange and the sequence of events for TBI. Clinical Outcome After Cisternostomy. The clinical experience is largely based on a study comparing 3 groups of patients with severe TBI undergoing conventional DC (284 patients), DC plus cisternostomy (272 patients), and cisternostomy alone (476 patients).29 In this large cohort study, the investigators found a significantly better clinical outcome score (mean Glasgow Outcome Scale of 3.9, 3.7, and 2.8), lower mortality (15.6%, 26.4% and 34.8%), and fewer days of assisted ventilation (2.4, 3.2, and 6.3) in the group treated with cisternostomy compared with the groups treated with either cisternostomy plus DC or DC alone. However, this study has some important limitations: It is a nonrandomized clinical study. No baseline clinical (Glasgow Coma Scale score, pupillary status) and radiologic information were provided and, thus, the homogeneity of the analyzed groups cannot be verified. Results were not supported by a statistical analysis. Follow-up is limited to 6 weeks after surgery, whereas most TBI studies report outcome at 6e12 months after treatment.7,14 Apart from this pilot study, the current literature on cisternostomy consists only of case reports.30,31 Other Techniques for CSF Diversion Placement of an EVD is a basic neurosurgical procedure and is one of the most common methods to assess and relieve increased ICP.2 It is therefore reasonable to propose this procedure as a secondtier therapy in cases of refractory intracranial hypertension.2 How Does EVD Placement Compare with Cisternal CSF Drainage? Physiological Remarks. CSF in the central nervous system is distributed as follows: approximately 30 mL is located within in the
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4 ventricles and another 110 mL resides in the subarachnoid spaces.37 The amount of CSF that can be drained from the cisterns is therefore larger. In cases of severe TBI with refractory hypertension, even after accurate EVD positioning, the result is usually a collapsed ventricular system with subsequent failure of any EVD drainage. The procedure of cisternostomy, which includes lamina terminalis fenestration, on the other hand, enables both compartments (ventricular and subarachnoid space) to be drained, resulting in more efficient drainage. A cisternal drain, as opposed to a ventricular drain, enables the reversal of the CSF shift edema and facilitates interstitial solute clearance,27 thus directly addressing the problem posed by worsening brain edema. This is a scenario commonly seen after a certain delay after severe TBI. The technique of opening (and cleaning out) the cisterns with continuous drainage then allows fluids to move more rapidly from the interstitial compartment of the brain toward the cisterns and then to the outside (into a CSF diversion system). This concept needs further preclinical and clinical studies to be confirmed because it could be argued that cisternostomy, instead of reversing CSF shift edema, simply addresses a larger amount of CSF and thus better ICP control. From a speculative point of view, the cisternal drain could also be used as an EVD to assess ICP. The technique of cisternostomy presupposes leaving the drain in the prepontine cistern and this, when coupled with a standard intraparenchymal ICP monitor, allows exploration of pressure distribution within the cisternal compartment, leading to interesting future research.38 Delayed post-traumatic hydrocephalus is a common complication after TBI and it is probably caused by CSF circulatory obstruction and/or problems with CSF absorption. A recent study39 showed that severe SAH or intraventricular hemorrhage is a strong and significant predictor for the development of post-traumatic hydrocephalus. Similarly, in aSAH, blood and blood products can obstruct CSF circulation, hinder absorption, or create aseptic inflammation causing hydrocephalus. A recent study by the group of Lawton40 showed that opening of the lamina
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terminalis and membrane of Lillequist significantly reduced the rates of shuntdependent hydrocephalus after aSAH. However, aSAH and traumatic SAH are different etiopathologies. The mechanisms triggering the development of subsequent hydrocephalus are probably the same. The technique of cisternostomy that includes evacuation of subarachnoid blood, opening of the lamina terminalis, and continuous cisternal drainage can reduce the rate of development of delayed post-traumatic hydrocephalus, although this needs to be corroborated by further clinical studies. Vasospasm, although well recognized after aSAH, is an underestimated entity in severe TBI.41 Several investigators have tried to assess the clinical value of removing blood clot burden and irrigating the cisterns in aSAH with the intention of reducing the rates for vasospasm, but results have been discordant.42-44 Future studies in trauma are needed to see if the procedure of cisternostomy, including removal of subarachnoid blood clots and washing the cisterns, has additional positive effects in the prevention of posttraumatic vasospasm. Clinical Experience with EVD. Liu et al.45 in their prospective observational study on severe TBI reported a significantly lower rate of refractory intracranial hypertension (and consequently, fewer decompressive craniectomies) and better outcome in patients managed with EVD compared with patients managed with intraparenchymal pressure monitors. However, controversy exists about the feasibility of using EVD to monitor ICP, namely difficulties in cannulating the ventricles in cases of brain swelling and frequent failure of the system caused by blood clots, infections, and hemorrhages.46 Another important issue is reliability of ICP signal from an open EVD, which has been recently investigated by Hockel et al.47 These investigators concluded that if CSF drainage is needed (according to the clinical situation), patients should receive an EVD with an integrated ICP probe or EVD line plus a separate ICP probe; the common practice of assessing ICP via open EVD with frequent clamping of the catheter is suitable only for overall ICP trend assessment. These factors have contributed to the widespread use of intraparenchymal ICP
monitors, which seems to be associated with fewer complications at the expense of high costs and inability to drain CSF, with the consequent necessity of heavier sedation, osmotherapy, hyperventilation, and barbiturates.48 Despite these controversies ventricular fluidecoupled ICP monitoring is still considered the gold standard of ICP monitoring.49 The literature concerning the efficacy of this method (EVD placement in the setting of severe TBI) remains poor (level of recommendation III according to the guidelines for the management of severe traumatic brain injury).50 Timofeev et al.51 described their experience with EVD placement to control increased ICP in cases in which ventricular size was deemed appropriate by the neurosurgeon. Ventricular size is one of the most important factors limiting the impact of this surgical maneuver because in cases of very small or collapsed ventricles, the amount of CSF that can be drained is often insufficient.2 The investigators achieved a rapid decrease of ICP in their patients but initial ICP reduction was followed by gradual or rapid re-increase to values exceeding 20 mm Hg by the end of a 24hour period in almost half of their patient population. Bhargava et al.52 described their experience in achieving good control of ICP in a group of patients with refractory increased ICP, although a selection bias cannot be excluded considering that the patients undergoing EVD or DC were not randomly selected. However, in cases of compressed ventricles or with major midline shift, adequate EVD positioning can be challenging and may require the use of neuronavigation.53 In severe TBI, there is often significant associated intraventricular hemorrhage, which potentially leads to drain failure with the necessity of repeated access to the system for flushing of the catheter, which then carries an increased risk for possible infection.2 CONCLUSIONS Current recommendations for the surgical treatment of ICP in severe TBI have focused on DC (as the primary or secondary procedure of choice) with or without EVD.50 However, the recently introduced concept of cisternostomy
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LITERATURE REVIEW LORENZO GIAMMATTEI ET AL.
seems to offer a more physiologic approach to the treatment of brain swelling, with the potential for effectively controlling ICP and reducing the effects of secondary brain damage. Other potential benefits such as reducing rates of vasospasm and hydrocephalus also need to be considered. This brief overview based on current knowledge of the surgical treatment of severe TBI aims to stimulate a debate within the neurosurgical community on the relative merits of DC and cisternostomy with a view to proposing a multicentric randomized clinical study. REFERENCES 1. Weiner GM, Lacey MR, Mackenzie L, Shah DP, Frangos SG, Grady MS, et al. Decompressive craniectomy for elevated intracranial pressure and its effect on the cumulative ischemic burden and therapeutic intensity levels after severe traumatic brain injury. Neurosurgery. 2010;66:1111-1118 [discussion: 1118-1119]. 2. Li LM, Timofeev I, Czosnyka M, Hutchinson PJ. Review article: the surgical approach to the management of increased intracranial pressure after traumatic brain injury. Anesth Analg. 2010;111: 736-748. 3. T Kocher. Hirnerschütterung, Hirndruck und chirurgische Eingriffe bei Hirnerkrankungen. In: Nothnagel H, ed. Specielle Pathologie und Therapie. Wien: A Hölder. 1901;9(pt. 3: 81e290):325e367 [in German]. 4. Galgano M, Toshkezi G, Qiu X, Russell T, Chin L, Zhao LR. Traumatic brain injury: current treatment strategies and future endeavors. Cell Transplant. 2017;26:1118-1130. 5. Mendelow AD, Gregson BA, Rowan EN, Francis R, McColl E, McNamee P, et al. Early surgery versus initial conservative treatment in patients with traumatic intracerebral hemorrhage (STITCH[Trauma]): the first randomized trial. J Neurotrauma. 2015;32:1312-1323.
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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 1 April 2018; accepted 24 May 2018 Citation: World Neurosurg. (2018) 116:322-328. https://doi.org/10.1016/j.wneu.2018.05.176 Journal homepage: www.WORLDNEUROSURGERY.org
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