The basal cisternostomy for management of severe traumatic brain injury: A retrospective study

Abstract

Purpose

Traumatic brain injury (TBI) is a significant public health issue that impacts individuals all over the world and is one of the main causes of mortality and morbidity. Decompressive craniectomy is the usual course of treatment. Basal cisternostomy has been shown to be highly effective as an alternative procedure to decompressive craniectomy.

Methods

We conducted a retrospective cohort of patients who received surgery for severe TBI between January 2019 and March 2023. Inclusion criterias were patients between the ages of 18 and 70 years who met the diagnostic criteria for severe TBI at first presentation and who underwent surgical intervention. The exclusion criteria were patients who have severe multiple injuries at the time of admission; preoperative intracranial pressure > 60 mmHg; cognitive impairment before the onset of the disease; hematologic disorders; or impaired functioning of the heart, liver, kidneys, or other visceral organs. Depending on the surgical approach, the patients were categorized into decompressive craniectomy group as well as basal cisternostomy group. General data and postoperative indicators, including Glasgow coma scale, intracranial pressure, etc., were recorded for both groups of patients. Among them, the Glasgow outcome scale extended assessment at 6 months served as the primary outcome. After that, the data were statistically analyzed using SPSS software.

Results

The trial enrolled 41 patients (32 men and 9 women) who met the inclusion criteria. Among them, 25 patients received decompressive decompressive craniectomy, and 16 patients received basal cisternostomy. Three days postoperative intracranial pressure levels were 10.07 ± 2.94 mmHg and 17.15 ± 14.65 mmHg (p = 0.013), respectively. The 6 months following discharge Glasgow outcome scale extended of patients was 4.73 ± 2.28 and 3.14 ± 2.15 (p = 0.027), respectively.

Conclusion

Our study reveals that basal cisternostomy in patients with surgically treated severe TBI has demonstrated significant efficacy in reducing intracranial pressure as well as patient prognosis follow-up and avoids removal of the bone flap. The efficacy of cisternostomy has to be studied in larger, multi-clinical center randomized trials.

1. Introduction

Around the world, traumatic brain injury (TBI) is a critical public health problem and the leading cause of mortality and morbidity.¹ TBI mortality and morbidity rates are rising annually, placing a huge burden on families and society.²

TBI involves 2 stages of injury. The primary brain injury is caused by an external force that lead to mechanical damage to brain tissue. While the secondary brain injury is a biochemical cascade that includes inflammation, apoptosis, oxidative stress, and other pathophysiological complications.³ The pathologic alterations increase the volume that the lesion occupies, which raises the intracranial pressure (ICP).¹ Cerebral ischemia and edema are made worse by raised ICP, which might ultimately result in brain herniation and death. And intracranial hypertension is associated with increased mortality in TBI studies.⁴ Normal ICP is defined as the pressure inside the lateral ventricles or lumbar subarachnoid space in supine position. It normally ranges from 5 to 15 mmHg in adults. According to the guidelines, raised ICP can be manageed by improving the airway, dehydration, sedation, analgesia, and cooling.⁵

Since Kocher's modern description of decompressive craniectomy (DC) was established in 1901, it has been considered the therapy of choice for the decrease of ICP in patients with intractable intracranial hypertension following severe TBI, and it remains in use today.^6,7 Relevant clinical investigations have shown that DC is one of the best ways to lower ICP and can decrease death rates.⁸ DC, however, may enhance the likelihood of a negative outcome.⁹ To present, 2 clinical trials in DC have demonstrated that DC reduces ICP, mortality, and the neurosurgical intensive care unit (NICU) duration of stay, but may be associated with increased rates of impairment and risk of vegetative state.^10,11 A recent study (RESCUE-ASDH) found that DC was not associated with a better outcome than craniotomy for patients with traumatic acute subdural hematoma (SDH) that required surgical intervention.¹² Is there a way to achieve both outcomes? Can it reduce the mortality rate for severe TBI patients while also leading to a positive prognosis?

In recent years, basal cisternostomy (BC) has attracted worldwide attention and has had successful outcomes as a surgical intervention for persistent intracranial hypertension and cerebral edema.^13,14 The glymphatic system provides an explanation for surgical rationalization. According to the glymphatic system, severe head trauma can cause diffuse traumatic subarachnoid hemorrhage. As a result, the cisternal pressure rises compared to the intracerebral pressure. In this case, cerebrospinal fluid (CSF) shifts into the brain parenchyma through the Virchow-Robin space, causing edema, increased ICP, and loss of compliance.¹⁵ BC could reduce ICP by exposing the basal cistern to atmospheric pressure, allowing CSF to drain out of the enlarged brain through the Virchow-Robin space and backshift into the cistern. Meanwhile, it could reduce cerebral edema, relax the brain, and allow the replacement of bone flap in situations when it would otherwise be irreplaceable.¹⁰ By draining lactic acid, tau protein, free radicals, and harmful metabolites from the CSF, this technique also reduces secondary damage.¹⁵

We conducted a retrospective study comparing the different prognostic outcomes of the DC and BC procedures to better understand how to manage patients with severe TBI.

2. Methods

2.1. Patient selection

We performed a retrospective cohort study in patients who were surgically treated for TBI between January 1, 2019, to March 1, 2023, in Shanxi Bethune Hospital (Taiyuan, Shanxi province, China) and the Second Affiliated Hospital of Nanchang University (Nanchang, Jiangxi province, China). According to the clinical data, senior neurosurgeons carried out the DC treatment, while a specialized research team handled the BC procedure. The same approach was taken in both groups of cases, including preoperative surgical criteria, preoperative preparation, and postoperative management. The inclusion criteria were the age range of 18 – 70 years, and initial disease onset were all consistent diagnostic criteria for severe TBI. After examining the imaging and clinical manifestation, clinicians came to the conclusion that there were strong indications for surgery: clinical manifestations: (1) acute SDH larger than 20 mm or midline shift greater than 5 mm on imaging; (2) patient's impaired consciousness that worsened gradually after admission, dilated pupils, and severe intracranial hypertension that was uncontrollable with conservative treatments.

The exclusion criteria were patients who have one of the following 5 conditions: (1) severe multiple injuries at the time of admission; (2) preoperative ICP > 60 mmHg; (3) cognitive impairment before the onset of the disease; (4) hematologic disorders; or (5) impaired functioning of the heart, liver, kidneys, or other visceral organs, which may have a negative impact on the prognosis.

Patients who met the indications for surgery were operated on as soon as possible after admission, and a consent document was signed in accordance with the required legal obligations. The Glasgow outcome scale extended (GOS-E) was used to assess the patient's clinical outcomes after surgery. Pre-operative and post-operative neurological evaluations were examined using Glasgow coma scale (GCS), and postoperative ICP and GCS were also recorded. Patients who were unable to be contacted by phone were also not included. Patients received care in accordance with a severe TBI management protocol that followed the most recent recommendations. Sedation and mechanical ventilation were given to all patients.

The primary objective was to determine the clinical outcomes of these patients after 6 months of DC surgery and BC surgery treatment.

2.2. Treatment

2.2.1. Surgical procedure

Enrolled patients underwent acute SDH removal in the operating room under general anesthesia. For DC, a classic trauma flap with an inverted question mark incision measuring no less than 12 × 15 cm² or 8 cm in diameter was lifted to open the dura mater and remove the hematoma. Other lesions, such as intracerebral hematomas or contusions, may be removed at the surgeon's discretion.

The BC procedure requires a head immobilization device, a microscope, brain spatulas, etc. The principal steps can be summarized in the following steps: (1) incision of frontotemporal skin; (2) perform a craniotomy (8 × 12 cm² or 8 cm in diameter) and remove the bone flap; (3) dural opening and dural tack-up sutures are applied to avoid epidural bleeding; (4) conventional surgery (aspiration of hematoma or removal of contusive and necrotic brain tissues); (5) cut the arachnoid at the chiasmatic cistern and aspirate hemorrhagic cerebrospinal fluid; (6) expose and cut the Liliequist's membrane at the optical-carotid cistern; (7) CSF was released from the basal cistern and a saline wash ensured the satisfactory removal of subarachnoid blood; (8) the drain tube is inserted under the microscope at the level of the optical-carotid cistern.¹⁶ (Fig. 1)

Fig. 1.

The view shows (A) the optic nerve and the intraoperative drainage of bloody cerebrospinal fluid; (B) the optic nerve and the excision of Liliequist's membrane; (C) the optic nerve (CN II), and internal carotid artery. The cisternal drain is placed into the prepontine cistern.

ICA: internal carotid artery

2.2.2. Postoperative treatment

Both groups were admitted to the NICU for 1 week of continuous ICP monitoring, endotracheal intubation, ventilator-assisted respiration, sedation, analgesia, and symptomatic supportive treatment. In the exposure group, postoperative cerebral cistern drainage lasted for 5 − 7 days (ventricular catheter, Medtronic, U.S.), with a drainage rate of 150 – 200 mL/day. In the non-exposure group, postoperative epidural drainage lasted 1 – 2 days.

2.3. Data collection

Clinical data retrieved from medical records comprised patient demographics, GCS at onset, pupil size, and reactivity. Early clinical outcome measurements investigated were duration of postoperative ventilation, length of stay in NICU, postoperative GCS, ICP, CSF drainage, the Glasgow outcome scale at discharge and length of hospital stay. Specifically, we collected GCS values the 3rd, 5th, and 7th days following surgery, as well as the first 24 h after surgery. We collected ICP values 24 h following the conclusion of the procedure, as well as on the 3rd, 5th, and 7th postoperative days and when the drain was removed. The GOS-E was used to measure long-term clinical results at 6 months after surgery.

Statistical analysis was performed using SPSS software (version 25.0, IBM Corp, Armonk, NY, USA). All variables were analyzed descriptively, and results were expressed as mean ± standard deviation (SD) or median (Q₁, Q₃). For categorical variables, the Chi-square test or Fisher's exact test was used for between-group comparisons; for continuous variables, the Student's t-test or the Mann-Whitney U test was used for between-group comparisons. Statistical significance was defined as a p value less than 0.05.

The study was approved by the Ethics Committee of Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, China (YXLL-2018-05).

3. Results

There were 41 patients who met the inclusion criteria (32 men and 9 women) enrolled in the study (Fig. 2). A total of 16 patients underwent BC, while 25 patients underwent DC. between the 2 groups, the patient's baseline characteristics, GCS, pupillary reactivity, and the mechanism of damage, did not have significant difference (Table 1). The mortality in the BC groups was 0 (no patient) while in the DC groups was 5 (20%). Preoperative ICP in group BC ranged from 13 to 43 mmHg (31.09 ± 11.07) mmHg.

Fig. 2.

Patient screening flowchart.

TBI: traumatic brain injury; DC: decompressive craniectomy; BC: basal cisternostomy

Table 1.

Baseline characteristics.

Variables	DC group (n = 25)	BC group (n = 16)	p value
Age (years), mean ± SD	50.08 ± 12.70	54.25 ± 12.92	0.389
Gender (male), n (%)	17 (68.0%)	15 (93.8%)	0.055
Type of injury, n (%)			0.110
Car accident	14 (56.0%)	5 (31.3%)
Tumble	7 (28.0%)	6 (37.5%)
Hit	2 (8.0%)	2 (12.5%)
Unknown	2 (8.0%)	3 (18.8%)
Mydriasis	16 (64.0%)	12 (75.0%)	0.064

DC: decompressive craniectomy; BC: basal cisternostomy.

Our data showed that compared with DC group, BC group had lower ICP values on the 3rd (DC group is 17.15 ± 14.65 mmHg and BC is 10.07 ± 2.94 mmHg, p = 0.013) and 7th day (DC group is 11.10 ± 1.22 mmHg and BC group is 8.33 ± 2.22 mmHg, p = 0.032). At the time of drain removal, ICP was lower in the BC group (DC group is 15.09 ± 11.93 mmHg and BC group is 7.11 ± 2.03 mmHg, p = 0.001) (Fig. 3) (Table 2)

Fig. 3.

The trend in ICP during the first week following surgery is depicted in this line graph.

DC: decompressive craniectomy; BC: basal cisternostomy; ICP: intracranial pressure.

Table 2.

Comparison of GCS score at 24 h, day 3, and day 5 postoperatively, and ICP (mmHg) at 24 h, day 3, day 5, and day 7 postoperatively, and at the time of drain removal between groups, (mean ± SD).

Variables	DC group (n = 25)	BC group (n = 16)	p value
GCS at 24h postoperative	5.16 ± 2.32	6.38 ± 2.45	0.424
GCS on the 3rd postoperative day	5.96 ± 3.31	6.25 ± 2.38	0.450
GCS on the 5th postoperative day	6.00 ± 3.43	6.44 ± 2.99	0.539
ICP at 24 h postoperatively (mmHg)	12.56 ± 6.08	10.10 ± 3.28	0.230
ICP on the 3rd postoperative day (mmHg)	17.15 ± 14.65	10.07 ± 2.94	0.013
ICP on the 5th postoperative day (mmHg)	17.14 ± 17.94	10.09 ± 3.29	0.112
ICP on the 7th postoperative day (mmHg)	11.10 ± 1.22	8.33 ± 2.22	0.032
ICP at drain removal (mmHg)	15.09 ± 11.93	7.11 ± 2.03	0.001

GCS: Glasgow coma scale; ICP: intracranial pressure; DC: decompressive craniectomy; BC: basal cisternostomy.

After surgical treatment, the median (Q₁, Q₃) of postoperative admission to the NICU duration was significantly longer in the BC group (10 (5.75, 13.25) days) than in the DC group (6.58 (3.00, 10.62) days) (p = 0.007). And the mean ± SD of hospitalization was significantly higher in the BC group (26.88 ± 13.29) days than in the DC group (19.72 ± 13.93) days (p = 0.017) (Table 3).

Table 3.

Comparison of NICU time, duration of mechanical ventilation, and length of hospitalization between groups.

Variables	DC group (n = 25)	BC group (n = 16)	p value
NICU time (day), median (Q1, Q3)	6.58 (3.00, 10.62)	10 (5.75, 13.25)	0.007
Duration of mechanical ventilation (day), mean ± SD	11.58 ± 12.22	13.21 ± 5.86	0.236
Hospitalization (day), mean ± SD	19.72 ± 13.93	26.88 ± 13.29	0.017

NICU: neurosurgical intensive care unit; DC: decompressive craniectomy; BC: basal cisternostomy.

The GCS of patients in the BC group at 1 week postoperatively (BC group is 6.81 ± 3.21, and DC group is 6.64 ± 4.10, p = 0.028) and the GOS-E scores at 6 months were higher than those in the DC group (BC group is 4.73 ± 2.28 and DC group is 3.14 ± 2.15, p = 0.027) (Fig. 4) (Table 4). The amount of bloody CSF drainage was higher in the BC group (129.46 ± 49.75) mL/day than in the DC group (68.05 ± 68.64) mL/day with the drain in place (p = 0.007) (Table 4). In addition, there were no statistically significant differences between the 2 groups as far as ICP values (mmHg) at the end of the operation (BC group is 7.84 ± 4.67 and DC group is 9.48 ± 6.66, p = 0.583), and GOS values at discharge were concerned (BC group is 3.00 ± 1.15 and DC group is 2.32 ± 0.75, p = 0.057) (Table 5).

Fig. 4.

The trend in GCS during the 1st week following surgery is depicted in this line graph.

DC: decompressive craniectomy; BC: basal cisternostomy; GCS: Glasgow coma scale.

Table 4.

Comparison of GCS score at 1 week postoperatively, CSF drainage, and the GOS-E in the 6th month, (mean ± SD).

Variables	DC group (n = 25)	BC group (n = 16)	p value
GCS at 1 week postoperative	6.64 ± 4.10	6.81 ± 3.23	0.028
CSF drainage (mL/day)	68.05 ± 65.64	129.46 ± 49.75	0.007
GOS-E score at 6th month	3.14 ± 2.15	4.73 ± 2.28	0.027

GCS: Glasgow coma scale; CSF: cerebrospinal fluid; GOS-E: Glasgow outcome scale extended; DC: decompressive craniectomy; BC: basal cisternostomy.

Table 5.

Comparison of postoperative ICP and GOS at discharge, (mean ± SD).

Variables	DC group (n = 25)	BC group (n = 16)	p value
Postoperative ICP (mmHg)	9.48 ± 6.66	7.84 ± 4.67	0.583
GOS at discharge	2.32 ± 0.75	3.00 ± 1.15	0.057

ICP: intracranial pressure; GOS: Glasgow outcome outcome scale; DC: decompressive craniectomy; BC: basal cisternostomy.

In the present case, all patients in the BC group replaced the bone flap and avoided cranioplasty and the second hospitalization was avoided.

4. Discussion

A new method for treating TBI is BC, in which the basal cerebral cisterns (the inter-optic, optic-carotid, and lateral carotid cisterns) are opened to atmospheric pressure, causing CSF to backshift from the edema brain tissues through the perivascular spaces into the cerebral cisterns.^17,18 During surgery, incision of the Liliequist's membrane allows for the release of bloody CSF, resulting in better control of ICP.19, 20, 21 However, the BC group protocol required 1 week of postoperative sedation and analgesia, mechanical ventilation, and cardiac monitoring. Therefore, the NICU time as well as the total length of hospitalization was a bit longer for patients in the BC group.

BC is theoretically explained by the glymphatic system. This microscopic structure is characterized by the inflow of CSF into the brain parenchyma along the arterial perivascular space in response to arterial pulsations and osmotic pressure gradients, as well as the exchange of substances through the interstitium and the inflow of metabolites into the interstitial fluid, which drains throughout the body.²²

Following TBI, astrocytes turn into the cytotoxic A1 subtype, altering the location of the aquaporin-4 (depolarization), impairing the glymphatic system, and causing cytotoxic cerebral edema and neuronal necrosis to worsen.²³ Following the development of cerebral edema in TBI, the swollen tissues exert mechanical pressure on the surrounding tissues and capillaries, increasing ICP, causing local ischemia, and increasing edema, all of which have an impact on the patient's prognosis.²⁴ After a TBI, the glymphatic system is impaired and normal CSF drainage is disrupted for about a month as a result of the elevated ICP, deposition of erythrocyte debris and inflammatory cells, and other pathologic responses.²⁵

This hypothesis has led to the development of BC as a potential treatment for high ICP, potential brain herniation, and potential ischemia following TBI.¹⁸ BC was initially employed in aneurysm surgery,²⁶ a treatment that relaxes the brain by opening the cerebral cisterns. Later, Cherian and Munakomi pioneered this technique in surgery for severe TBI. They came to the conclusion that BC improves prognosis and lowers morbidity and death in TBI patients.²⁷

More researchers have been researching BC in recent years. Cherian et al.²⁸ documented certain cases in which BC was carried out for the treatment of TBI, and the outcomes showed that, in comparison to DC, these procedures might reduce intraoperative cerebral edema, lower mortality, and enhance the patient's prognosis. In a recent randomized controlled trial, Chandra et al.²⁹ evaluated the effectiveness of DC for TBI. They found that the BC group had lower mortality. Academics conducted a prospective, longitudinal study of the impact of BC on patient prognosis in a 3-center study, and the results of the trial demonstrated that patients who underwent either DC + BC or BC alone had a favorable clinical outcome at both early and long-term follow-up.³⁰ Additionally, there are case reports that back up the claim that BC is effective in treating severe TBI or persistently high ICP.31, 32, 33

However, it is now thought that patients with severe cerebral edema and those with a high number of hematomas have harder cisterns to expose, which makes BC more challenging. Consequently, there may have been a bias in selection if the death rate in the BC group was lower than that in the DC group.³⁴ Several other researchers have questioned whether CSF drainage could raise the risk of infection and peripheral artery damage.³⁵ The quality of postoperative care, physician skills, and hospital hardware conditions may have contributed to some studies' inability to demonstrate the benefits of BC.³⁶

Adults typically have ICP levels between 5 and 15 mmHg; values above 30 mmHg are regarded as pathologic, 40 mmHg as life-threatening, and 60 mmHg as lethal.³⁷ Our study demonstrated that patients with a preoperative ICP of less than 60 mmHg can release CSF during surgery to improve cerebral perfusion and quickly lower ICP. In this study, all patients in the BC and DC group had a preoperative ICP < 60 mmHg. There was no mortality in the BC group because their patients had superior ICP management due to increased CSF outflow and removal of toxic metabolites. However, no patients with a preoperative ICP of greater than 60 mmHg survived because they had liquefied and necrotic brain tissue, inadequate CSF release during surgery, raised and uncontrollably high postoperative ICP, and no cerebral perfusion.³⁷

The indications for BC are similar to those for DC,³⁸ but the technique necessitates an understanding of cerebral cisterns and vascular anatomy of the anterior skull base and is performed under a surgical microscope, necessitating a more challenging learning curve for neurosurgeons.³⁹ However, it has been demonstrated that the procedure enhances the prognosis of TBI patients.^16,40 The next phase involves testing brain metabolites in TBI patients to demonstrate that BC is effective. According to the trial's findings, BC offers TBI patients a better prognosis. The main limitations of the trial are the small sample size and single-center data, and sample selection bias due to retrospective studies and loss to follow-up may have affected the accuracy of the final results. Large, multicenter, prospective trials are still required to confirm the effectiveness of BC in TBI.

In conclusion, it has been suggested that BC, a new procedure that combines knowledge of the anterior skull base, cerebral cisterns, and blood vessels, will lessen brain swelling, mortality, and morbidity following severe TBI, as well as avoid intraoperative brain expansion. Our study, however, showed that patients treated with BC have better outcomes at long-term follow-up than DC group. The BC procedure allows for a one-stage replacement of the bone flap and also serves as a replacement to DC. At the same time, it can reduce ICP and improve the prognosis of patients with severe TBI, it can also reduce the economic burden of patients and avoid the need of secondary cranioplasty. For the treatment of individuals with severe TBI, the study's findings are highly significant. BC looks to be a promising treatment; however, clinical multicenter trials and basic research are required to demonstrate the effectiveness and scientific validity of BC.

CRediT authorship contribution statement

Tangrui Han: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft. Zhiqiang Jia: Data curation, Formal analysis, Methodology, Software. Xiaokai Zhang: Investigation, Methodology, Resources. Hao Wu: Conceptualization, Data curation, Resources. Qiang Li: Data curation, Methodology, Project administration. Shiqi Cheng: Formal analysis, Resources, Supervision. Yan Zhang: Resources, Supervision. Yonghong Wang: Conceptualization, Data curation, Validation, Writing – original draft, Writing – review & editing.

Ethical statement

Obtain the patient's informed consent when conducting the study, and respect the patient's privacy rights of human subjects.

Funding

This work was supported by Shanxi Provincial Department of Science and Technology [grant number 202203021221241].

Declaration of competing interest

The authors declare no conflict of interest.

Declaration of generative AI and AI-assisted technologies in the writing process

During the preparation of this work the authors used Grammarly in order to check grammar and spelling. After using this tool, the authors reviewed and edited the content as needed and took full responsibility for the content of the publication.