Abstract
Laser interstitial thermal therapy (LITT) is a minimally invasive and cytoreductive neurosurgical technique that has gained significant momentum in the last decade. Several technological enhancements such as MRI thermometry and improved laser probe design have enabled feasibility and improved the safety of LITT procedures. Numerous reports have been published describing the treatment of lesions ranging from tumors to epileptogenic foci, but the indications for LITT continue to evolve. We describe the general physical and biological concepts underlying LITT, clinical workflow, and established and emerging indications.
Introduction
Stereotactic laser interstitial thermal therapy (LITT) is an emerging, minimally invasive and cytoreductive neurosurgical technique for a variety of central nervous system (CNS) lesions ranging from tumors to epilepsy foci. Although the technique was first described in 1983, enthusiasm for its use was limited in large part due to the inability to monitor tissue temperature during laser treatment and thus control the extent of ablation.1,2
In the past decade, renewed interest in LITT has been sparked by advances in intraoperative magnetic resonance imaging (MRI) techniques that now enable real-time thermometry using T1-weighted 2D images obtained during the ablation procedure.2–4 Use of stereotactic LITT with MR thermometry has since been described for treatment of primary and metastatic brain tumors, radiation necrosis, and epilepsy foci.5 Investigation of new uses and the limitations of LITT is currently a highly active area of research. In this review, we describe the surgical procedure, technological advances, treatment indications, and emerging uses of LITT (Table 1).
Table 1.
Laser Interstitial Thermal Therapy
The first experiments using laser ablation in brain tumor models were described in 1983 by Bown, who used a neodymium:yttrium-aluminum-garnet (Nd:YAG) laser.1,2,4,5 Subsequently, animal studies and clinical trials were performed, establishing LITT as a potential treatment for intracranial neoplasms. Numerous technical advancements in laser probe design and MRI have led to the development of the modern stereotactic LITT neurosurgical procedure.
Typical LITT Surgical Workflow
Surgical technique and workflow vary by institution and LITT system in use but in general are as follows: Prior to surgery, a thin section CT scan or MRI suitable for use in stereotactic surgery is performed. An optimal trajectory for ablation is then planned using a computer-based stereotactic neuro-navigation system, following the first-order principle of treating the lesion down the center of its long axis. In some cases, multiple trajectories may be required to optimally ablate the lesion. Once in the operating room, the patient is positioned to facilitate placement of the laser probe, keeping in mind the space restrictions of the MRI. This may require positioning the patient’s head such that the entry point and the direction of the laser probe is more in line with the barrel of the MRI bore and not at the top of the field as in traditional open cases. The laser probe may be placed using either frameless or frame-based stereotactic techniques or using a robotic arm, such as the ROSA® system, depending on surgeon preference and resources available.
A stab incision no more than 5 mm is then made at the planned probe entry site and a drill used to generate a bur hole in the skull. A rigid guide is then affixed to the skull and the fiberoptic laser probe inserted through the bur hole, following the preplanned trajectory. Once the probe is secured in place, the patient must be placed in an MRI scanner. This can be achieved either by transporting the patient with the probe in place to a suitable MRI scanner or by utilizing an intra-operative MRI scanner. After initial MRI images are captured to verify probe position, the ablation process is initiated. During this time, firing of the laser probe is interleaved with periodic acquisition of 2D T1 MRI images. These images are generally overlaid with a graphical representation of the temperature of the brain surrounding the probe. Once the ablation is completed, the patient is removed from the MRI scanner. If no additional trajectories are planned, the laser probe is then removed, and the surgical incision irrigated and closed. All patients undergo post-procedure monitoring for at least 24 hours before being discharged from the hospital.
LITT Technology
Significant technological advances continue to be made in the tools and techniques used to perform stereotactic LITT surgeries. In the United States, there are currently two LITT systems available: the NeuroBlate® System (Monteris Medical, Winnipeg, Manitoba, Canada), which received FDA clearance in 2009 and the Visualase® Thermal Therapy System (Visualase Inc., Houston, Texas, USA), which received FDA clearance in 2007. Detailed descriptions of both systems have previously been reported, and the underlying biological mechanism of action between the two systems is similar.6–9
During a LITT ablation, light energy emitted by the laser is converted into thermal energy by the surrounding tissue. This process occurs when photons emitted by the laser optical fiber are absorbed by tumor cell chromophores, resulting in chromophore excitation followed by release of thermal energy.5,10 Once a sufficiently elevated temperature is achieved and maintained, protein denaturation, cellular necrosis, and tissue coagulation occur. Numerous factors influence the speed, pattern, and degree of tissue heating, including intrinsic properties of the target tissue and its surrounding environment, properties of the laser used, and the temperature and duration of ablation. For example, diode and Nd:YAG lasers are the two types of lasers used for neurosurgical LITT procedures. The NeuroBlate® system uses a 12 watt 1064 nm Nd:YAG laser that is cooled with carbon dioxide while the Visualase® system uses a 15 watt 980 nm diode laser that is saline cooled. The differing wavelengths and other properties of these laser probe designs may result in different degrees of tissue penetration and ablation.5,10
Several innovations in laser probe design have significantly enhanced the LITT procedure. For example, laser probes were initially designed with diffusion tips that emitted laser photons in all directions from the probe tip. Subsequently, a side-fire probe was designed to emit photons in one direction, orthogonal to the laser probe. When this probe is paired with an MRI-compatible driver capable of rotating, advancing, and withdrawing the probe, a more conformal pattern of ablation can be achieved, although at the expense of increased ablation time.2 Significant advances in probe cooling also made LITT a tractable solution for lesion ablation. Initial probe designs lacked enough cooling and insulation to protect tissue traversed by the laser probe, limiting lasers to a power of 1–5 watts. Furthermore, if temperatures at the probe tip exceed 100°C, a pseudocapsule can form around the tip with charring and carbonization of the surrounding tissue, limiting further laser penetration and reducing the treatment volume.5 The introduction of carbon dioxide and saline cooled probe sheaths allowed for use of increased laser power, improved protection of traversed tissue, reduced treatment times, and increased treatment volume.2,5 Temperature changes from heat conduction fall off exponentially with distance from the laser probe. Currently available probes have an effective treatment radius between 1 and 2 cm from the tip. The tip can be moved along the implanted axis of the probe to create a treatment “cylinder” approximately 3 cm in diameter for a single pass of a laser probe.2 Depending on the shape and size of the target lesion, multiple trajectories may be used, at the expense of additional operative time.5,8
Both commercially available LITT systems depend on intraoperative MRI scanning. During a LITT procedure, a computer is connected directly to the MRI scanner and runs software used to integrate images acquired from the MRI scanner in real time. This integration allows for verification of the initial probe position and of any new probe position that results from advancing or withdrawing the probe, and measurement of tissue temperature using MR thermometry. The development of MR thermometry was a critical step in making LITT feasible for neurosurgical applications. MR thermometry is a noninvasive means of measuring tissue temperature to within 1°C with a spatial resolution of 1–2 mm that is based on changes in MR characteristics (primarily proton resonance frequency) of living tissue that occur with change in temperature.3,5 Critically, MR thermometry can be used to measure temperatures distant from the laser probe, allowing surgeons to maximize ablation of the target lesion while avoiding damage to surrounding normal tissue. Several MR sequences, including T1-weighted, diffusion coefficient and water proton resonant frequency sequences can be used for MR thermometry.5 Once firing of the laser probe begins, newly acquired MR images are compared to baseline images by the computer. The Arrhenius equation predicts cell death as a function of tissue temperature and ablation time and is used to display zones of tissue damage.5,8,11 For example, in the NeuroBlate® system, the white line encircles the target volume that has received the thermal dose equivalent of 43°C for at least 60 minutes, the blue line surrounds the target volume that has been exposed to 43°C for at least 10 minutes, and the yellow line surrounds tissue exposed to 43°C for 2 minutes. These lines are also referred to as thermal damage thresholds (TDT). Tissue within the white line is considered to have undergone coagulation necrosis, while tissue within the blue line is considered to be severely damaged and tissue outside the yellow line is considered to have no permanent damage.8
Tumor
An increasing number of neuro-oncological applications for LITT have been reported in the literature, with a growing body of evidence gradually clarifying its role. Studies have described its use in brain metastases, low- and high-grade gliomas, meningiomas, and radiation necrosis.2,4,6,7,12–15 In general, the minimally invasive nature of LITT is particularly well suited for treating deep-seated or otherwise difficult to access lesions, lesions resistant to alternative therapies such as stereotactic radiation, or lesions in patients who could otherwise not tolerate a larger, open surgical resection.
The median overall survival of GBM is 15 months in the setting of maximal surgical resection, radiation and chemotherapy with temozolamide.16 Several retrospective and prospective studies have established that maximal cytoreduction with gross total resection of glioblastoma is associated with improved survival compared to biopsy alone.2,17,18 While patients are generally able to tolerate radiation and chemotherapy, surgery may not be feasible for all patients, either because the patient is too ill to tolerate a craniotomy or because the lesion is located in or adjacent to eloquent structures, making resection impossible without significant neurological deficit. Recently, a multicenter matched cohort study compared outcomes of patients undergoing LITT versus biopsy followed by standard chemo- and radiation therapy for treatment of newly diagnosed GBM. The authors reported that patients undergoing LITT with near total blue TDT-line coverage had improved survival compared to matched patients undergoing biopsy alone. Thus, as a cytoreductive, minimally invasive procedure, LITT may represent a favorable alternative to biopsy alone in patients with difficult to access tumors or who cannot tolerate a craniotomy.15
Recurrent GBMs have limited options available for additional therapy, and there is currently no widely recognized standard of care. At the time of recurrence, patients may have already undergone multiple prior craniotomies, fractionated radiation, radiosurgery, and/or chemotherapy, all of which increase the risk of subsequent surgeries. Prior studies have reported a significantly increased risk of systemic infection, worsening neurological status, and increased wound-related surgical complications in patients undergoing a second surgery for glioblastoma.5 Several studies have described the safe utilization of LITT as a cytoreductive therapy in patients with recurrent glioblastoma.19,20 In a recently published study of LITT treatment of 41 recurrent GBM lesions, the post-LITT median overall survival was found to be 11.6 months, with a 16% rate of 30-day procedure-related morbidity.20 As a comparison, patients with recurrent GBM treated with lomustine and bevacizumab have a median overall survival of 9.1 months with a 40–60% incidence of serious adverse events.21 No head-to-head comparison has been performed comparing LITT to chemotherapy for recurrent GBM, but these data suggest that LITT may present a favorable, alternative strategy for treatment of recurrent GBM.
LITT has also been used for treatment of brain metastases, particularly for lung, breast, and colon adenocarcinoma.6,14,19 At present, standard treatment modalities for cerebral metastases include surgery, radiotherapy, and/or stereotactic radiosurgery. A recently published multicenter prospective study of 20 patients with recurrent metastatic brain lesions treated with LITT suggests that LITT may stabilize Karnofsky performance score (KPS), preserve quality of life and reduce steroid use in patients with few alternative options for salvage therapy.13 The authors reported a 12% rate of immediate LITT-related complication, including 4 cases of worsening neurological deficit due to damage to adjacent eloquent tissue and 1 case of intracerebral hemorrhage that did not require additional surgery and did not result in neurological deficit. Other complications related to LITT included seizures, transient neurological symptoms, and asymptomatic increase in radiographic cerebral edema.13 Given the limited data available, how LITT will fit into the treatment paradigm for brain metastases remains to be determined, but there is increasing enthusiasm for its use in treatment-refractory brain metastases.
Lastly, LITT has been used to treat patients with radiation necrosis. Radiation necrosis occurs in approximately 5–10% of patients treated with radiation therapy and 10–20% of patients treated with stereotactic radiosurgery.5 Treatment for radiation necrosis is generally conservative, with observation and, when symptomatic, dexamethasone. However, in cases of medically refractory, symptomatic radiation necrosis, surgical resection may be necessary. As with recurrent glioblastoma, patients requiring a second surgery for resection of radiation necrosis are at elevated risk of surgical complications, with many patients unable to tolerate a craniotomy due to their general health and medical comorbidities. In their study of 19 patients with biopsy confirmed radiation necrosis treated with LITT, Ahluwalia and colleagues reported that LITT stabilized KPS, preserved quality of life, and reduced steroid. Furthermore, nearly 100% lesion control was achieved with LITT in patients with radiation necrosis.13 It is of interest to note also that the thermal dose threshold (yellow TDT line) for effective treatment of radiation necrosis is thought to be lower than that for tumor.5,13
Epilepsy
Epilepsy has a lifetime prevalence of 3%, with significant medical, social, psychological, and economic implications for patients. The first line of treatment for epilepsy generally relies on anticonvulsant drugs, but approximately one third of patients treated with anticonvulsants continue to have seizures that are medically refractory. Drug-resistant epilepsy, defined as lack of seizure freedom despite a two anti-epileptic drug regimen, is frequently associated with mesial temporal sclerosis. In these patients, and in many patients with seizures localizable to a defined epileptogenic focus, surgery has been proven to be highly effective in controlling or abolishing seizures.22 Given the potential morbidity associated with many epilepsy surgeries such as selective amygdalohippocampectomy, hemispherotomy, corpus callosotomy, and resection of deep-seated hamartomas, significant efforts have been devoted to improving the safety profile of these surgeries.9 Multiple authors have described the successful use of LITT to treat epilepsy, harnessing its minimally invasive nature to improve the safety of epilepsy surgery.23–25
In 2014, Willie and colleagues reported their success in performing LITT amygdalohippocampectomy. In 13 patients, 60% of the volume of the amygdalohippocampal complex was ablated, with a median hospitalization of 1 day, and 77% of patients achieved meaningful seizure reduction, with 54% being free of disabling seizures.23 More recently, Lehner et al. described their success in treating 5 patients with medically refractory epilepsy with LITT ablation of the corpus callosum. Four of the 5 patients achieved greater than 80% seizure control after the procedure.25 Selective amygdalohippocampectomy involves creation of a temporal scalp incision and craniotomy, and places structures such as the temporal lobe and optic radiations at risk. Open corpus callosotomy involves creation of a large scalp incision and craniotomy, and risks injury to neurovascular structures such as the sagittal sinus and cingulum. The minimally invasive nature of LITT significantly reduces risk to these structures and makes it a more attractive surgical option for intractable epilepsy patients who are often hesitant to undergo invasive brain procedures.25 Furthermore, Drane and colleagues reported improved object recognition and naming outcomes after LITT amygdalohippocampectomy compared to matched patients undergoing open temporal lobe epilepsy surgery, suggesting that by sparing adjacent eloquent structures, LITT may have fewer neurocognitive side effects compared to open surgery.24
Emerging Uses of LITT
New case reports and series describing the use of LITT in intracranial lesions continue to be published, leading to the discovery of additional indications for the procedure. LITT is particularly well suited for treatment of difficult to access lesions, lesions in or adjacent to eloquent cortex, and/or scenarios in which standard therapies are not feasible. Although LITT has previously most often been used as an alternative to traditional treatments such as open craniotomy, in the future, it may be used as an adjunct to such procedures. For example, tumors near eloquent cortex greater than 3 cm in size that are not suitable for LITT may first be debulked with open surgical techniques, and the residual tumor then treated with LITT to achieve maximal treatment of the tumor.
Importantly, much of the underlying biological mechanism and effects of LITT in the brain remain poorly understood and is therefore an important area of ongoing investigation. In 2016, Leuthardt and colleagues analyzed post-LITT MRI scans and serum brain specific enolase levels in 20 patients with recurrent GBM. Interestingly, they found that peak brain permeability after LITT occurs 1–2 weeks after ablation and resulves by 4–6 weeks.26 These findings suggest that LITT may create a window of time during which drugs may penetrate the blood-brain barrier, opening an interesting new area of investigation on combination therapies of LITT plus adjuvant chemotherapy. Other properties of the area of increased blood brain barrier permeability, such as the spatial distribution of permeability in relation to the area of ablation, have yet to be characterized. The finding of elevated brain specific enolase in the blood after LITT also implies that proteins normally confined to the immune-privileged central nervous system are being released into the systemic circulation. Thus, disruption of the blood-brain barrier after LITT may also have immune implications that are yet to be explored.
Conclusion
LITT is a minimally invasive, cytoreductive surgical technique that can be used to make targeted and conformal lesions in the brain. Several critical advances in probe design and the development of MR thermometry have made LITT a more practical surgical technique. This recent interest in LITT has spurred numerous reports describing efforts to treat neurosurgical pathologies, including neoplasms and epileptogenic foci. The value of LITT for the treatment of certain pathologies such as recurrent GBM and epileptogenic foci has now become well established. Data on emerging uses of LITT are very promising, with the indications of the procedure continuing to grow.
Acknowledgments
Missouri Medicine would like to thank Rhonda Quint, administrative assistant to Keith M. Rich, MD, for her assistance in production of Washington University neurosurgical papers.
Footnotes
Albert H. Kim, MD, PhD, (above), MSMA member since 2011, is Director, Brain Tumor Program, Associate Professor of Neurological Surgery, Genetics, Neurology, and Developmental Biology, and Bhuvic Patel, MD, Neurosurgery Resident PGY5, Department of Neurosurgery, Washington University School of Medicine, St. Louis, Missouri.
Contact: alberthkim@wustl.edu
Disclosure
Funding from Neurosurgery Research and Education Foundation (NREF) Research Fellowship Grant. AHK received a research grant from Monteris Medical and Stryker.
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