Abstract
Laser interstitial thermal therapy (LITT) has emerged as a potential tool in the armamentarium of neurosurgeons managing patients with deep-seated and difficult-to-access brain tumors. Advances in stereotactic neurosurgery coupled with neuroimaging tools have led to the resurgence of interest in laser therapy for a variety of neurosurgical indications. Stereotactic placement of laser probe using minimally invasive techniques and the ability to monitor the tissue ablation in real time using MR thermometry are two distinct advantages of LITT. Patients with recurrent gliobastoma multiforme (GBM) or newly diagnosed gliomas with significant medical comorbidities, radiation necrosis, radiosurgery-resistant brain metastasis and cancer-related pain pose significant challenges in the field of neuro-oncology. LITT offers an opportunity to obtain stereotactic biopsy and cytoreduction in a minimally invasive nature. In this chapter, we have described the current applications of LITT in neuro-oncology, including malignant gliomas, brain metastatic disease, radiation necrosis and other indications such as cancer-related pain and epilepsy. We have also described the principles, technical nuances and LITT systems currently available in the clinical practice. With growing interest and acceptance of LITT in neuro-oncology, we are likely to obtain high-quality evidence supporting the utility of this modality in patients with a variety of neuro-oncological conditions in the near future.
Keywords
- laser therapy
- thermal therapy
- gliomas
- radiation necrosis
- brain metastasis
- epilepsy
- cancer pain
1. Introduction
Laser interstitial thermal therapy (LITT) has established itself as a new treatment modality in neurosurgery due to its minimally invasiveness nature, safety and efficacy. Nowadays, LITT has become a reality in the world of neuro-oncology [1–4], epilepsy surgery [5–7], and is also emerging as an attractive option in the fields of spine surgery [8–10] and chronic pain syndromes[10–12]. In neuro-oncology, LITT has emerged as an option for malignant gliomas, refractory brain metastatic disease and radiation necrosis. LITT is best suited, but not limited, for patients with tumors located in deep-seated, difficult-to-access areas that could develop significant postoperative neurological deficits and poor performance status with traditional microsurgical resection. It is a FDA-approved treatment option for intracranial lesions including recurrent glioblastomas [4]. Concerning brain metastatic disease, although stereotactic radiosurgery (SRS) has become the standard of care for most patients, the failure rate associated with SRS is up to 23% [13–15]. Additionally, the potential risk of developing radiation necrosis following SRS can vary from 1.4 to 24% [16–18], and this complication can be refractory to standard therapeutic options like steroids and Bevacizumab. LITT has been effective in managing both radiosurgery-resistant brain metastasis [2, 3, 19–22] and radiation necrosis [3, 21–24].
The surgical applications of lasers are represented by three distinct functionalities of this technology: photocoagulation, photovaporization and photosensitization [25]. LITT is referred to the first one, photocoagulation, which implies tissue damage by thermal energy provided by a source of constant and continuous laser delivery to a planned target volume. It was first introduced in 1983 by Bown and colleagues [26], who used a neodymium-doped yttrium aluminum garnet (Nd:YAG) laser and achieved focal tissue coagulation in an experimental brain tumor model without tissue vaporization. Research using experimental animal models demonstrated the brain tissue changes in response to hyperthermia and confirmed that coagulation necrosis could result from the application of thermal energy to brain tissue [27–30]. However, the inability to monitor and control the laser-induced thermal effects limited the widespread application of this technology. Recent advances in magnetic resonance (MR) thermography [31] allowed real-time image feedback of laser thermal energy delivery, making it possible to predict the thermal damage of a planned target in the brain.
In the present chapter, the authors describe the current applications of LITT in neuro-oncology, including malignant gliomas, brain metastatic disease and radiation necrosis together with the basic principles and technical nuances related to the surgical procedure and the current LITT systems available in clinical practice. We also touched upon other applications of LITT such as cancer-related refractory pain and epilepsy. Future directions are also discussed in this chapter.
2. Laser interstitial thermal therapy: principles and rationale
Treating cancers with heat energy dates back to 1960s when Rosomoff et al. [32] first reported the application of ruby pulsed laser beam in two patients with GBM and in experimental animals. They reported that in normal brains of experimental animals, laser application was associated with total cellular destruction with vacuolization secondary to vaporization and hemorrhage. The sensitivity to laser can be increased by Cardio-green and Evans blue injections. Whereas on brain tumors in patients with GBM, laser therapy induced cellular necrosis without hemorrhage and inflammation. Laser bursts were given at 2 min interval at estimated 3 cm depth from the cortical surface, followed by progressive 1 cm depth till approximately 9 cm depth from the surface was reached. Differential susceptibility of normal and tumor to laser application was noted in this study. However, given that the precise application and delivery of laser energy were not feasible at that time, this therapy has fallen out of favor and did not get acceptance in routine clinical practice. In 1985, Winter et al. [33] used microwave hyperthermia for treating brain tumors. Later, brain tumors were treated with focused ultrasound by Britt and coworkers [34]. Following these reports, another study [35] investigated the use of interstitial hyperthermia and iridium brachytherapy in malignant gliomas.
Without the availability of technology to safely monitor the extent of hyperthermia, these techniques remained largely experimental and were unable to be integrated in mainstream clinical practice. When the technological advancements overcome these limitations, thermal ablation using LITT was considered as a more viable, practical and cost-effective approach in treating brain tumors in selected patients. Using LITT, otherwise surgically inaccessible tumors were made amenable to surgical ablation with good outcomes [36, 37]. Though earlier generation probes like Nd-YAG lasers had limitations such as charring of adjacent tissue, thus limiting energy penetration and uncertainties in the extent of tissue ablation [37, 38], new-generation probes have protective mechanisms to prevent charring and also use real-time MR imaging (MR thermometry) to monitor the extent of ablation for minimizing thermal damage to normal surrounding brain parenchyma.
3. Histopathological and biological effects of LITT
Delivering thermal injury with LITT causes some major biological changes in the tissues [39]. Laser photons in the near-infrared range, when directed to the target tissue, get absorbed and converted to heat energy. Aided by abundant blood flow, conduction, convection and refraction all play a significant role in distributing the heat energy around the target tissue [39]. The inherent biology of the surrounding structures and the physical properties of the laser determine the uniformity in the distribution of the heat applied. Ablation of the entire target lesion is the primary aim of using LITT [40].
Cellular homeostasis is usually not disturbed with mild elevation in temperature to approximately 40°C. However, when the temperature is increased in the range of 42 to 45°C (hyperthermia), there is a substantial increase in susceptibility to cellular damage [40, 41]. When the temperature is increased from 46 to 60°C, marked cytotoxicity and cell death ensue with considerably decreased time needed to kill the cells [42, 43]. Above 60°C, there is substantial damage to the mitochondrial enzymes, cytosol and the nucleic acid proteins that culminate to coagulation necrosis [44]. Super boiling temperatures like 105°C results in charring, tissue boiling, vaporization, and carbonization which if not released immediately might culminate in increased intracranial pressure. Apart from the true values of the temperature used, the time of exposure to such temperatures is also important. For example, 43°C for 2 min causes reversible damage to the tissue, while the same temperature for 10 min causes permanent tissue damage and for 60 min causes coagulative necrosis [22, 45]. Based upon the Arrhenius equation, only shorter intervals are needed when using high temperatures to get the same results [46].
The target lesion usually undergoes central coagulation necrosis following LITT therapy, surrounded by a zone of edema next to the undamaged tissue [36]. By the end of 1st week, granulation tissue gradually replaces the zone of necrosis. The targeted lesion then develops into a cystic lesion with remnant necrotic debris surrounded by reactive gliosis with mesenchymal deposits [47, 48].
Three distinct zones can be identified on MRI following LITT. The first central zone represents the zone of coagulation necrosis and if the temperature inadvertently exceeds 100°C, then there is a chance of charring and vaporization followed by a pseudo cavity formation. Just outside the core area lays a non-viable part with increased interstitial fluid called the intermediate zone. The outermost marginal zone is viable consisting of edematous viable surrounding brain parenchyma following thermal exposure and sharply delineates itself from the inner two zones. The ultra-structure of the inner two zones of thermal injury show disrupted organelles and evidence of apoptosis, whereas the outer zone shows only axonal swelling, neuronal shrinkage and hypertrophied endothelial cells with no evidence of vessel thrombosis [4, 49–51]. Following LITT therapy, the target lesions might exhibit an increase in size due to necrosis and perilesional edema, but eventually will shrink and form a rim of granulation tissue.
4. Technical aspects and commercially available components of LITT
4.1. MR thermometry
After numerous attempts of measuring the thermal energy delivery to the target tissue during LITT, including the use of skin thermometers, subcutaneous and interstitial probes, infrared detectors and thermographic cameras [28, 29, 52–56], it was the addition of MR thermometer that played the most significant role in allowing real-time monitoring and quantification of thermal energy delivery leading to thermal ablation [27]. MR thermography based on the temperature-dependent water proton resonance frequency (PRF) is capable of providing visual imaging together with a quantification model of thermal deposition with accurate temporal and spatial resolution. The theory behind PRF is based on the fact that as temperature increases during LITT, the number of free H2O molecules also increases due to breakage of hydrogen bonds between H2O molecules. The hydrogen nuclei (proton) are mobilized more efficiently within the gradient field when in the free H2O molecule state, producing real-time imaging that can be interpreted and visualized using the proper computer software in the treatment workstation [57, 58].
4.2. Lasers and probes used for LITT
The two most common types of lasers used for LITT are the continuous-wave neodymium-doped yttrium aluminum garnet (Nd:YAG), with a wavelength of 1064 nm, and diode lasers with wavelengths between 800–980 nm, which operate at a wide range of powers [1, 59, 60]. Nd:YAG lasers are capable to achieve deeper tissue penetration compared to diode lasers, especially in soft tissues with high blood perfusion at wavelengths between 1000–1100 nm [59, 61]. Diode lasers have the advantage of producing lesions faster, but typically with less penetration [2].
LITT probes have three main components: an optical fiber with a 600 μm diameter, a heat-resistant terminal tip made of sapphire or quartz, measuring around 10 mm [59] and a cooling system, which is required to avoid overheating, tissue carbonization and optical fiber damage [61]. The current cooling mechanisms use either a cooled gas system (CO2) or a constant stream of fluid (water or saline) delivered to the tip of the probe through a sheath associated to the optic fiber [60, 62]. The thermal energy delivery at the probe tip has been classically described as a symmetrical ellipsoid shape centered along the axis of the probe. Recent advances in probe design, most specifically by the NeuroBlate® System (Monteris Medical Corporation, Plymouth, MN, USA), also led to the development of side firing laser probes, which allows the surgeon to control the laser ablation of complex shaped tumors in a real-time fashion.
4.3. Commercially available LITT systems used in neurosurgery
Currently, there are two commercially available FDA-cleared LITT systems for neurosurgery in the United States: the NeuroBlate® System (Monteris Medical Corporation, Plymouth, MN, USA) and the Visualase Thermal Therapy System (Medtronic Inc., Minneapolis, MN, USA).
5. Animal models and preclinical studies
Various canine [32, 64, 65] and murine [48, 66–68] animal models of brain tumors have been used to investigate the efficacy of laser thermal therapy on tumors and surrounding brain tissue, as well as to evaluate the thermal dose models. First, animal experiments evaluating the impact of laser energy on normal murine brains can be dated back to 1960s. Fine et al. [68] used ruby pulsed laser delivering 100 J of energy to the forehead of mice, which resulted in a mortality rate of 75% within a day of exposure. Later, Earle et al. [67] showed that 20–40 J of energy delivered using ruby laser was not lethal and resulted in sub-arachnoid and intracerebral hemorrhage with minimal neurological effects. Later, Rosomoff et al. [32] reported similar findings using 8 J ruby laser in a rat and dog experiment models. They also reported that the sensitivity to laser could be increased by Cardio-green and Evans blue injections. Kangasniemi et al. [64] reported the feasibility and utility of MR-guided laser (980 nm diode) ablation of tumors (transmissible venereal tumors) in seven canines. Utility of LITT was studied in Lewis mice implanted with glioma cells [48] and neoplastic lesion was monitored using MRI. In addition, proliferation of implanted tumor cells, gliosis and apoptosis was monitored using immunohistological techniques. LITT caused necrosis of neoplastic cells; however, apoptosis of residual tumor cells at the margin (more vascularized compared to pre-treatment) was noted following LITT [48]. Canine models have also been used to establish various thermal dose models, so as to reliably predict post-LITT tissue damage as well as to monitor tissue ablation in real time [65]. Localized interstitial thermal therapy using magnetic nanoparticles (dextran- or aminosilane-coated iron-oxide nanoparticles) have been described in a rat model of GBM [69]. Interestingly, rats treated with aminosilane-coated nanoparticles showed improvement in survival (4.5 times prolongation), whereas those treated with dextran-coated particles did not show any difference in survival compared to controls. These animal experiments paved a way to the development of LITT and future therapeutic options for gliomas.
6. Use of LITT in gliomas
High-grade glioma or glioblastoma multiforme (GBM, WHO grade IV), in particular, is a significant clinical challenge in the field of neuro-oncology with a high rate of morbidity and mortality. GBM constitutes approximately 45% of all malignant primary glial neoplasms [70]. Gross total surgical resection with concurrent chemo-radiotherapy is the mainstay treatment modality for this aggressive tumor [71]. However, even with the best available treatment options, 5-year overall survival (OS), progression-free survival (PFS) and median survival have been reported to be 9.9%, 6.9 months and 14.6 months, respectively [59, 71, 72]. The median survival decreases to 12.1 months with post-resection radiotherapy alone instead of concurrent chemo-radiotherapy and to 6.2 months in patients with progressive disease following standard treatment regimen [71, 72]. There is controversial data regarding optimal management (surgical vs. medical) in patients with recurrent GBM. Extent of resection greater than 80% has been shown to have improved overall survival in carefully selected patients with recurrent GBM [73–75]. Young patients with good performance status have been shown to have improved overall survival following surgical resection for recurrent GBM [76, 77]; however, after adjusting for age, no significant benefit was achieved following repeat surgery [77]. In addition, redo craniotomy for progressive GBM is associated with increased risk of per-operative complications including neurological deficits (18–22%) [78, 79]. Also, there is a cumulative risk of these complications following each craniotomy with maximum risk between first and second procedures [80]. There is insufficient evidence supporting the role of radiosurgery, stereotactic fractionated radiation therapy or interstitial brachytherapy in patients with recurrent GBM [81, 82]. Of note, radiosurgery has also been shown to be associated with increased toxicity in patients with recurrent disease [81]. Survival benefit of 9.3 months have been reported in patients (good performance status) receiving interstitial brachytherapy for recurrent GBM [82]. Given a high incidence of this primary brain tumor with lack of effective therapies and dismal outcome, significant research is directed toward developing effective medical and surgical treatment modalities to improve overall and progression free survival. Laser interstitial thermal therapy (LITT) is one of the advancements in the surgical management of these tumors. LITT is a minimally invasive procedure, which involves stereotactic-guided placement of laser probe and utilizes thermal energy to cause protein coagulation and cell death [83, 84]. Advances in neuroimaging coupled with stereotactic techniques have led to the resurgence of interest in the utility of laser thermacoagulation in patients with brain tumors. In addition, integration of MR thermography to LITT made it possible to deliver thermal energy under real-time monitoring, thus avoiding injury to surrounding normal brain tissue [85]. Given these advantages of LITT, this technique has been utilized for a variety of neurosurgical indications such as deep-seated gliomas [1, 4, 86, 87], epilepsy [20, 88], brain metastasis with radiation necrosis [19, 23, 24, 49] and cingulotomy for intractable pain [12, 89].
First report of utilization of Nd-YAG laser thermal therapy in five patients with deep-seated brain tumors was published in 1990 [90]. Later, several studies with a smaller (
Although there is no Class 1 evidence supporting the efficacy of LITT in patients with high-grade gliomas, there is also paucity of high-quality data supporting the role of craniotomy and surgical resection in such patients [99]. Given the minimally invasive nature of LITT coupled with advances in neuroimaging stereotactic techniques and thermography, LITT can be a useful treatment modality in patients with poor performance status or medical comorbidities and high-grade glioma. The advantages of LITT have led to the exploration of this technique for a variety of intracranial tumors. LITT has been investigated in various prospective case-controlled studies and there is a likelihood to have Class 2 evidence data in the next couple of years.
7. Use of LITT in brain metastasis and radiation necrosis
Brain metastasis is a common and challenging clinical scenario affecting up to 40% of patients with systemic malignancies [100–102]. Lung carcinoma (16–19%) is the leading systemic cause of brain metastasis followed by renal (6–9%), melanoma (7–7.4%), breast (5%) and colorectal cancers (1.2–1.8%) [103, 104]. Prognosis in patients with brain metastasis is often dismal, due to limited therapeutic options. Majority of chemotherapeutic agents and targeted immunotherapies do not cross the blood brain barrier, hence limited applicability of these agents in management of patients with brain metastasis. Stereotactic radiosurgery (SRS) has emerged as a primary therapeutic modality in patients with single or multiple brain metastases with an improvement in overall survival and quality of life [13, 14, 105, 106]. However, there is a subset of patients (up to 23%) who fail SRS with progression of metastatic disease and subsequent mortality [13, 15]. Brain metastasis from radio-resistant systemic tumors such as renal cell carcinoma, sarcoma, melanoma and triple negative breast carcinoma carries a worse prognosis, despite better control rates with SRS as compared to conventional radiotherapy [107]. Stereotactic radiosurgery is also associated with adverse radiation effects (AREs) with a 1-year cumulative incidence of 13–14%, which increases with size and volume of the tumor [108–111]. Of these adverse radiation effects, radiation necrosis (RN) is the most challenging in terms of diagnosis and management with a reported incidence ranging between 1.4% and 25% [16–18, 112]. Imaging modalities such as MR perfusion, MR spectroscopy, 6-[(18)F]-fluoro-L-3,4-dihydroxyphenylalanine (F-DOPA)/FDG PET, l-methyl-(11)C-methionine ((11)C-MET) and SPECT scan have been shown to be useful in differentiating radiation necrosis from recurrent metastasis or tumor [113–116]. The sensitivity, specificity, accuracy of perfusion MRI and F-DOPA PET have been reported to be 86.7, 68.2, 75.6 and 90, 92.3, 91.3%, respectively [114]. SPECT scan has been shown to have the highest specificity of 97.8% (sensitivity 87.6%) for differentiating tumor progression and radiation necrosis and may be preferred over other imaging modalities [116]. Medical therapeutic options for RN include corticosteroids, Bevacizumab, hyperbaric oxygen therapy, anticoagulation (heparin or warfarin) or vitamin E [117–125]. Surgical resection of RN can be considered in symptomatic patients with mass effect in accessible areas [125]. Therefore, there is always a scope for newer treatment strategies in the management of patients with brain metastasis to improve the clinical outcomes. LITT is a minimally invasive technique that offers an alternative therapeutic option in patients with either SRS-failed or radio-resistant brain metastasis. LITT also offers an opportunity to have a histological diagnosis before laser ablation in cases of suspicion between recurrence of metastasis and radiation-related changes. The minimally invasive nature of this technology permits its utility in patients with multiple medical comorbidities with poor Karnofsky performance status (KPS) and tumors in difficult-to-access locations.
First use of laser therapy for brain metastasis was reported in 1986, with successful-laser assisted ablation of a midbrain metastasis from primary lung adenocarcinoma [126]. In 1990, Sugiyama et al. [90] reported the utility of laser in patients with deep-seated tumors including metastasis. Later, Schulze et al. [36] studied the histological effects of laser thermotherapy in seven patients with brain metastasis and eight patients with glial tumors. In this study, authors reported that laser therapy created a unique pattern of architectural changes at the histological level with central zone of necrosis surrounded by edematous tissue. This surrounding edematous tissue tends to undergo cystic changes following regenerative and resorptive changes [36]. In addition to thermal coagulation, laser-induced tumor damage is caused by disruption of cellular membranes and organelles. Authors advocated this technique in older patients with significant medical comorbidities and brain tumors. First pilot clinical trial investigating the safety and feasibility of LITT in patients with resistant focal metastatic brain tumors was reported in 2008 [2]. Four patients with six metastatic brain tumors (temporal lobe,
Another study reported progression-free and overall median survival of 5.8 months each following LITT in five patients with metastasis (non-small cell lung carcinoma,
Torres-Reveron et al. [3] reported the utility of LITT in six patients with progressive brain metastatic tumors (non-small cell lung cancer,
A recent study reported delayed failure in two patients who underwent LITT following tumor progression and refractory cerebral edema after SRS [23, 49]. LITT was performed 7 months (breast adenocarcinoma) and 14 weeks (lung adenocarcinoma) after stereotactic radiosurgery. Patient with lung adenocarcinoma metastasis to the external capsule had significant perilesional edema following radiosurgery and also experienced severe side effects secondary to steroid therapy (refractory hyperglycemia, weight gain and bilateral proximal muscle weakness), therefore LITT was considered 14 weeks after SRS [23]. This patient had significant clinical improvement and steroid was weaned off in 2 weeks following ablation therapy. However, first patient with parietal metastasis and second patient with external capsule metastasis demonstrated tumor recurrence at 6 and 11 months, respectively, which was histologically confirmed following surgical resection [49]. A recent review based on pooled 25 patients with brain metastasis who were treated with LITT reported a median overall survival (OS) of 12.6 months (range 9.0–19.8 months) and progression-free survival (PFS) to vary between 3.8–8.5 months [127]. Severe complication rate was reported to be 8% and included events such as perioperative hemorrhage (non-surgical) and blood suffusion. Intracranial progression of disease (excluding local progression, 8%) and extra cranial progression as the etiology of mortality was reported in 36 and 55% of patients respectively following LITT for brain metastasis. Median survival time (9.0–19.8 months) and severe complication rate of 8% following LITT are similar to 1.4–16.1 months and 6–19%, respectively, following surgical management of brain metastasis [128]. Given these comparable outcomes, LITT is an effective therapeutic option for patients with resistant brain metastasis in difficult-to-access areas. There is a paucity of literature on the utility of LITT in patients with radiation necrosis (RN). It is often difficult to distinguish patients with radiation necrosis and those with tumor recurrence following stereotactic radiosurgery. Therefore, the majority of reported cases could represent a mixture of these clinical conditions, even following stereotactic biopsy. In an anecdotal report, LITT was used for diagnosed RN following stereotactic biopsy (may represent a mixed lesion), as patient was refractory and not able to tolerate standard medical management (steroids and bevacizumab) for suspected RN [24]. Patient developed several steroid-related complications along with several medical comorbidities. In light of these facts and the presence of a lesion in a difficult-to-access area (left centrum semiovale), LITT was considered in this patient with RN following SRS for brain metastasis (non-small cell lung carcinoma). As demonstrated in earlier reports, there was a significant improvement in clinical symptoms following LITT and patient was weaned off the steroid in 2 weeks after the procedure. However, there was a mild increase in size of lesion with no significant FLAIR signal changes at 7 weeks postoperative MRI, which was consistent with the literature.
Patel et al. [98] reported the utility of LITT in patients with a variety of intracranial pathologies including patients with recurrent metastasis or radiation necrosis (
LITT has shown initial promising results in patients with recurrent brain metastasis and RN (to some extent) following SRS. However, long-term prospective randomized controlled studies are warranted and required to validate the efficacy of LITT for these clinical indications.
8. Use of LITT in other intracranial tumors
Jethwa et al. [63] reported the application of Visualase laser system in 20 patients (33 procedures) with a variety of intracranial tumors over a period of 1 year. GBM was the most common pathology treated (
9. Use of LITT in cancer-related pain
Cancer-related pain is a significant clinical problem affecting up to 60–90% of patients with cancer in terminal stages [130]. The first line of management in such patients is pharmacological including opioids; however, 10–20% of such patients are refractory to medical line of management and thus requires intervention for pain management [131–133]. Various neuromodulation and ablative procedures such as intrathecal morphine, myelotomy, cordotomy, DREZotomy, sympathetic blocks, paravertebral blocks and cingulotomy have been described for pharmacological-resistant, cancer-related and various refractory pain syndromes [131–137]. Ablative cingulotomy using radiofrequency [136] and neuromodulation using DBS [138] has been described in patients with various refractory pain syndromes. With the advances in neuroimaging and stereotactic techniques and introduction of LITT, this technique has been explored in patients with pharmacoresistant cancer-related pain [12, 98]. Patel et al. [12] describe the feasibility of MRgLITT in three patients (four procedures) with cancer-related pain. Ablation coordinates used in patients who underwent first-time ablation includes
Another recent study reported the utility of LITT in five patients with chronic pain syndrome [98]. Total operative time and ablation time were 2.9±0.3 h and 4.3±0.6 mins, respectively. No postoperative complications were noted following LITT in patients with chronic pain [98]. Outcomes in terms of pain control was not reported in this study [98].
10. Use of LITT in epilepsy
Pharmacoresistant or drug-resistant epilepsy (DRE) is a significant clinical challenge with prevalence of approximately 28 to 40% in patients with epilepsy [139, 140]. In addition, approximately 10% of pediatric patients with epilepsy meet the criterion of DRE within 18 months of diagnosis [140]. Epilepsy surgery has been shown to have beneficial long-term effects in terms of seizure control (seizure free outcome rate of 67 and 26% at 5 and 15 years follow-up, respectively) and psychosocial outcomes in patients with DRE [141–143]. Based on a recent meta-analysis, the incidence of neurological deficits, permanent neurological deficits, wound infection/meningitis following temporal lobectomy with/without amygdalohippocampectomy and extratemporal lobar/multilobar resections have been reported to be 5.2, 0.8, 1.1 and 19.5, 3.2, 1.9%, respectively [144]. The complication rates have been shown to increase from 10% during first resective surgery in pediatric patients with complex refractory epilepsy to 50% during second respective surgery [145]. Given this success of epilepsy surgery in controlling seizures with associated morbidity in patients with DRE, there is always a need to improvise on surgical techniques so as to reduce the morbidity while improving the outcomes. Introduction of MRI-guided LITT in neurosurgery over the past decades have paved a way to exploration of this technique in patients with DRE. MRgLITT is a minimally invasive stereotactic technique that can be used to ablate the epileptogenic zone and associate fibers so as to simulate the resection and disconnection procedures, respectively. FDA approved Auto LITT in 2009, following a successful Phase 1 multicenter trial investigating the safety of this system in patients with recurrent GBM. In 2012, Curry et al. [146] first reported the use of MRI-guided (1.5T) LITT (Visualase thermal system) in five patents with DRE. In this study, they ablated six epileptic zones (cingulate tuber
11. Future trends
FDA approved AutoLITT in 2009, following a multicenter trial investigating the efficacy of this modality in patients with recurrent GBM. Laser ablation has currently been investigated as a potential treatment modality in patients with failed stereotactic radiosurgery for brain metastasis (NCT01651078, Laser Ablation after Stereotactic Radiosurgery, LAASR study). Following these results, LITT is likely to be explored in other areas of neuro-oncology.
12. Our experience
At Cleveland clinic we have an experience of about 150 patients, who underwent LITT for a variety of indications since 2011. At our center, we use NeuroBlate® System (Monteris Medical Corporation, Plymouth, MN, USA) with a side firing probes (Figure 1). Regarding intra-axial tumors, we have used LITT in 30 patients with de novo GBM, 24 patients with recurrent GBM (following standard treatment), 22 patients with recurrent anaplastic tumors, upfront in 10 patients with anaplastic tumors, 24 patients with low-grade gliomas (7 upfront and 17 recurrent). We have also used this modality in 17 patients with radiation necrosis and 15 patients with metastasis. We are also participating in a multi-institutional study investigating the role of this modality in patients with failed SRS (LAASR study). We have also utilized this therapy in patients with recurrent meningioma (
13. Conclusion
LITT is a stereotactic minimally invasive technique that involves ablation of pathological tissue using laser energy. This technique has shown promising results in a variety of neuro-oncological conditions such as recurrent GBM, upfront deep-seated GBM, recurrent metastasis following SRS, radiation necrosis and cancer-related pain. LITT was approved by FDA in 2009 for unlimited intracranial usage. Minimally invasive nature of the therapy coupled with real-time monitoring of thermal ablation are distinct advantages of LITT over traditional surgical approaches, especially for deep-seated tumors in patients with significant co-morbidities. Currently, there is Level III /Level IV evidence in the literature supporting the role of LITT in patients with recurrent GBM/high-grade gliomas, metastasis and radiation necrosis. There is a paucity of data regarding other indications of LITT. However, trials are underway and are likely to provide significant level of evidence supporting the efficacy of LITT in a variety of the above-mentioned indications in coming years.
References
- 1.
Schwarzmaier HJ, Eickmeyer F, von Tempelhoff W, Fiedler VU, Niehoff H, Ulrich SD, Yang Q, Ulrich F. MR-guided laser-induced interstitial thermotherapy of recurrent glioblastoma multiforme: preliminary results in 16 patients. European journal of radiology 2006;59(2):208–15. - 2.
Carpentier A, McNichols RJ, Stafford RJ, Itzcovitz J, Guichard JP, Reizine D, Delaloge S, Vicaut E, Payen D, Gowda A, George B. Real-time magnetic resonance-guided laser thermal therapy for focal metastatic brain tumors. Neurosurgery 2008;63(1 Suppl 1):ONS21-8; discussion ONS8-9. - 3.
Torres-Reveron J, Tomasiewicz HC, Shetty A, Amankulor NM, Chiang VL. Stereotactic laser induced thermotherapy (LITT): a novel treatment for brain lesions regrowing after radiosurgery. Journal of neuro-oncology 2013;113(3):495–503. - 4.
Sloan AE, Ahluwalia MS, Valerio-Pascua J, Manjila S, Torchia MG, Jones SE, Sunshine JL, Phillips M, Griswold MA, Clampitt M, Brewer C, Jochum J, McGraw MV, Diorio D, Ditz G, Barnett GH. Results of the neuroblate system first-in-humans phase i clinical trial for recurrent glioblastoma: clinical article. Journal of neurosurgery 2013;118(6):1202–19. - 5.
Kang JY, Wu C, Tracy J, Lorenzo M, Evans J, Nei M, Skidmore C, Mintzer S, Sharan AD, Sperling MR. Laser interstitial thermal therapy for medically intractable mesial temporal lobe epilepsy. Epilepsia 2016;57(2):325–34. - 6.
Buckley R, Estronza-Ojeda S, Ojemann JG. Laser ablation in pediatric epilepsy. Neurosurgery clinics of North America 2016;27(1):69–78. - 7.
Gross RE, Willie JT, Drane DL. The role of stereotactic laser amygdalohippocampotomy in mesial temporal lobe epilepsy. Neurosurgery clinics of North America 2016;27(1):37–50. - 8.
Tatsui CE, Stafford RJ, Li J, Sellin JN, Amini B, Rao G, Suki D, Ghia AJ, Brown P, Lee SH, Cowles CE, Weinberg JS, Rhines LD. Utilization of laser interstitial thermotherapy guided by real-time thermal MRI as an alternative to separation surgery in the management of spinal metastasis. Journal of neurosurgery. Spine 2015;23(4):400–11. - 9.
Brouwer PA, Brand R, van den Akker-van Marle ME, Jacobs WC, Schenk B, van den Berg-Huijsmans AA, Koes BW, van Buchem MA, Arts MP, Peul WC. Percutaneous laser disc decompression versus conventional microdiscectomy in sciatica: a randomized controlled trial. The spine journal: official journal of the North American Spine Society 2015;15(5):857–65. - 10.
Lee GW, Jang SJ, Kim JD. The efficacy of epiduroscopic neural decompression with Ho:YAG laser ablation in lumbar spinal stenosis. European journal of orthopaedic surgery & traumatology: orthopedie traumatologie 2014;24(Suppl 1):S231–7. - 11.
Ammar TA. Monochromatic infrared photo energy versus low level laser therapy in chronic low back pain. Journal of lasers in medical sciences 2015;6(4):157–61. - 12.
Patel NV, Agarwal N, Mammis A, Danish SF. Frameless stereotactic magnetic resonance imaging-guided laser interstitial thermal therapy to perform bilateral anterior cingulotomy for intractable pain: feasibility, technical aspects, and initial experience in 3 patients. Neurosurgery 2015;11(Suppl 2):17–25; discussion. - 13.
Flickinger JC, Kondziolka D, Lunsford LD, Coffey RJ, Goodman ML, Shaw EG, Hudgins WR, Weiner R, Harsh GRt, Sneed PK, et al. A multi-institutional experience with stereotactic radiosurgery for solitary brain metastasis. International journal of radiation oncology, biology, physics 1994;28(4):797–802. - 14.
Kondziolka D, Patel A, Lunsford LD, Kassam A, Flickinger JC. Stereotactic radiosurgery plus whole brain radiotherapy versus radiotherapy alone for patients with multiple brain metastases. International journal of radiation oncology, biology, physics 1999;45(2):427–34. - 15.
Petrovich Z, Yu C, Giannotta SL, O’Day S, Apuzzo ML. Survival and pattern of failure in brain metastasis treated with stereotactic gamma knife radiosurgery. Journal of neurosurgery 2002;97(5 Suppl):499–506. - 16.
Minniti G, Clarke E, Lanzetta G, Osti MF, Trasimeni G, Bozzao A, Romano A, Enrici RM. Stereotactic radiosurgery for brain metastases: analysis of outcome and risk of brain radionecrosis. Radiation oncology (London, England) 2011;6:48. - 17.
Jagannathan J, Petit JH, Balsara K, Hudes R, Chin LS. Long-term survival after gamma knife radiosurgery for primary and metastatic brain tumors. American journal of clinical oncology 2004;27(5):441–4. - 18.
Kano H, Shuto T, Iwai Y, Sheehan J, Yamamoto M, McBride HL, Sato M, Serizawa T, Yomo S, Moriki A, Kohda Y, Young B, Suzuki S, Kenai H, Duma C, Kikuchi Y, Mathieu D, Akabane A, Nagano O, Kondziolka D, Lunsford LD. Stereotactic radiosurgery for intracranial hemangioblastomas: a retrospective international outcome study. Journal of neurosurgery 2015;122(6):1469–78. - 19.
Carpentier A, McNichols RJ, Stafford RJ, Guichard JP, Reizine D, Delaloge S, Vicaut E, Payen D, Gowda A, George B. Laser thermal therapy: real-time MRI-guided and computer-controlled procedures for metastatic brain tumors. Lasers in surgery and medicine 2011;43(10):943–50. - 20.
Hawasli AH, Bagade S, Shimony JS, Miller-Thomas M, Leuthardt EC. Magnetic resonance imaging-guided focused laser interstitial thermal therapy for intracranial lesions: single-institution series. Neurosurgery 2013;73(6):1007–17. - 21.
Rao MS, Hargreaves EL, Khan AJ, Haffty BG, Danish SF. Magnetic resonance-guided laser ablation improves local control for postradiosurgery recurrence and/or radiation necrosis. Neurosurgery 2014;74(6):658–67; discussion 67. - 22.
Sharma M, Balasubramanian S, Silva D, Barnett GH, Mohammadi AM. Laser interstitial thermal therapy in the management of brain metastasis and radiation necrosis after radiosurgery: An overview. Expert review of neurotherapeutics . 2016;16(2):223–232. - 23.
Fabiano AJ, Alberico RA. Laser-interstitial thermal therapy for refractory cerebral edema from post-radiosurgery metastasis. World neurosurgery 2014;81(3–4):652.e1–4. - 24.
Rahmathulla G, Recinos PF, Valerio JE, Chao S, Barnett GH. Laser interstitial thermal therapy for focal cerebral radiation necrosis: a case report and literature review. Stereotactic and functional neurosurgery 2012;90(3):192–200. - 25.
Ryan RW, Spetzler RF, Preul MC. Aura of technology and the cutting edge: a history of lasers in neurosurgery. Neurosurgical focus 2009;27(3):E6. - 26.
Bown SG. Phototherapy in tumors. World journal of surgery 1983;7(6):700–9. - 27.
Chen L, Wansapura JP, Heit G, Butts K. Study of laser ablation in the in vivo rabbit brain with MR thermometry. Journal of magnetic resonance imaging: JMRI 2002;16(2):147–52. - 28.
Cheng MK, McKean J, Boisvert D, Tulip J, Mielke BW. Effects of photoradiation therapy on normal rat brain. Neurosurgery 1984;15(6):804–10. - 29.
Elias Z, Powers SK, Atstupenas E, Brown JT. Hyperthermia from interstitial laser irradiation in normal rat brain. Lasers in surgery and medicine 1987;7(4):370–5. - 30.
Tracz RA, Wyman DR, Little PB, Towner RA, Stewart WA, Schatz SW, Wilson BC, Pennock PW, Janzen EG. Comparison of magnetic resonance images and the histopathological findings of lesions induced by interstitial laser photocoagulation in the brain. Lasers in surgery and medicine 1993;13(1):45–54. - 31.
De Poorter J. Noninvasive MRI thermometry with the proton resonance frequency method: study of susceptibility effects. Magnetic resonance in medicine 1995;34(3):359–67. - 32.
Rosomoff HL, Carroll F. Reaction of neoplasm and brain to laser. Archives of neurology 1966;14(2):143–8. - 33.
Winter A, Laing J, Paglione R, Sterzer F. Microwave hyperthermia for brain tumors. Neurosurgery 1985;17(3):387–99. - 34.
Britt RH, Pounds DW, Lyons BE. Feasibility of treating malignant brain tumors with focused ultrasound. Progress in experimental tumor research 1984;28:232–45. - 35.
Roberts DW, Coughlin CT, Wong TZ, Fratkin JD, Douple EB, Strohbehn JW. Interstitial hyperthermia and iridium brachytherapy in treatment of malignant glioma. A phase I clinical trial. Journal of neurosurgery 1986;64(4):581–7. - 36.
Schulze PC, Vitzthum HE, Goldammer A, Schneider JP, Schober R. Laser-induced thermotherapy of neoplastic lesions in the brain—underlying tissue alterations, MRI-monitoring and clinical applicability. Acta neurochirurgica 2004;146(8):803–12. - 37.
Svaasand LO, Ellingsen R. Optical properties of human brain. Photochemistry and photobiology 1983;38(3):293–9. - 38.
Takizawa T. The carbon dioxide laser surgical unit as an instrument for surgery of brain tumours—its advantages and disadvantages. Neurosurgical review 1984;7(2–3):135–44. - 39.
Jaunich M, Raje S, Kim K, Mitra K, Guo Z. Bio-heat transfer analysis during short pulse laser irradiation of tissues. International Journal of Heat and Mass Transfer 2008;51(23–24):5511–21. - 40.
Goldberg SN, Gazelle GS, Mueller PR. Thermal ablation therapy for focal malignancy: a unified approach to underlying principles, techniques, and diagnostic imaging guidance. AJR. American journal of roentgenology 2000;174(2):323–31. - 41.
Seegenschmiedt MH, Brady LW, Sauer R. Interstitial thermoradiotherapy: review on technical and clinical aspects. American journal of clinical oncology 1990;13(4):352–63. - 42.
Goldberg SN, Gazelle GS, Halpern EF, Rittman WJ, Mueller PR, Rosenthal DI. Radiofrequency tissue ablation: importance of local temperature along the electrode tip exposure in determining lesion shape and size. Academic radiology 1996;3(3):212–8. - 43.
Larson TR, Bostwick DG, Corica A. Temperature-correlated histopathologic changes following microwave thermoablation of obstructive tissue in patients with benign prostatic hyperplasia. Urology 1996;47(4):463–9. - 44.
Thomsen S. Pathologic analysis of photothermal and photomechanical effects of laser-tissue interactions. Photochemistry and photobiology 1991;53(6):825–35. - 45.
Mohammadi AM, Schroeder JL. Laser interstitial thermal therapy in treatment of brain tumors—the NeuroBlate System. Expert review of medical devices 2014;11(2):109–19. - 46.
Laidler KJ. The development of the Arrhenius equation. Journal of chemical education 1984;61(6):494. - 47.
Schober R, Bettag M, Sabel M, Ulrich F, Hessel S. Fine structure of zonal changes in experimental Nd:YAG laser-induced interstitial hyperthermia. Lasers in surgery and medicine 1993;13(2):234–41. - 48.
Schulze PC, Adams V, Busert C, Bettag M, Kahn T, Schober R. Effects of laser-induced thermotherapy (LITT) on proliferation and apoptosis of glioma cells in rat brain transplantation tumors. Lasers in surgery and medicine 2002;30(3):227–32. - 49.
Fabiano AJ, Qiu J. Delayed failure of laser-induced interstitial thermotherapy for postradiosurgery brain metastases. World neurosurgery 2014;82(3–4):e559–63. - 50.
Hawasli AH, Ray WZ, Murphy RK, Dacey RG, Jr., Leuthardt EC. Magnetic resonance imaging-guided focused laser interstitial thermal therapy for subinsular metastatic adenocarcinoma: technical case report. Neurosurgery 2012;70(2 Suppl Operative):332–7; discussion 8. - 51.
Murovic JA, Chang SD. The pathophysiology of cerebral radiation necrosis and the role of laser interstitial thermal therapy. World neurosurgery 2015;83(1):23–6. - 52.
Berns MW, Coffey J, Wile AG. Laser photoradiation therapy of cancer: possible role of hyperthermia. Lasers in surgery and medicine 1984;4(1):87–92. - 53.
Dougherty TJ, Grindey GB, Fiel R, Weishaupt KR, Boyle DG. Photoradiation therapy. II. Cure of animal tumors with hematoporphyrin and light. Journal of the national cancer institute 1975;55(1):115–21. - 54.
Henderson BW, Waldow SM, Mang TS, Potter WR, Malone PB, Dougherty TJ. Tumor destruction and kinetics of tumor cell death in two experimental mouse tumors following photodynamic therapy. Cancer research 1985;45(2):572–6. - 55.
Gomer CJ, Rucker N, Razum NJ, Murphree AL. In vitro and in vivo light dose rate effects related to hematoporphyrin derivative photodynamic therapy. Cancer research 1985;45(5):1973–7. - 56.
Marchesini R, Andreola S, Emanuelli H, Melloni E, Schiroli A, Spinelli P, Fava G. Temperature rise in biological tissue during Nd:YAG laser irradiation. Lasers in surgery and medicine 1985;5(2):75–82. - 57.
Rieke V, Butts Pauly K. MR thermometry. Journal of magnetic resonance imaging. JMRI 2008;27(2):376–90. - 58.
McNichols RJ, Gowda A, Kangasniemi M, Bankson JA, Price RE, Hazle JD. MR thermometry-based feedback control of laser interstitial thermal therapy at 980 nm. Lasers in surgery and medicine 2004;34(1):48–55. - 59.
Norred SE, Johnson JA. Magnetic resonance-guided laser induced thermal therapy for glioblastoma multiforme: a review. BioMed research international 2014;2014:761312. - 60.
Rahmathulla G, Recinos PF, Kamian K, Mohammadi AM, Ahluwalia MS, Barnett GH. MRI-guided laser interstitial thermal therapy in neuro-oncology: a review of its current clinical applications. Oncology 2014;87(2):67–82. - 61.
Stafford RJ, Fuentes D, Elliott AA, Weinberg JS, Ahrar K. Laser-induced thermal therapy for tumor ablation. Critical reviews in biomedical engineering 2010;38(1):79–100. - 62.
Anvari B, Tanenbaum BS, Hoffman W, Said S, Milner TE, Liaw LH, Nelson JS. Nd:YAG laser irradiation in conjunction with cryogen spray cooling induces deep and spatially selective photocoagulation in animal models. Physics in medicine and biology 1997;42(2):265–82. - 63.
Jethwa PR, Barrese JC, Gowda A, Shetty A, Danish SF. Magnetic resonance thermometry-guided laser-induced thermal therapy for intracranial neoplasms: initial experience. Neurosurgery 2012;71(1 Suppl Operative):133–44; 44–5. - 64.
Kangasniemi M, McNichols RJ, Bankson JA, Gowda A, Price RE, Hazle JD. Thermal therapy of canine cerebral tumors using a 980 nm diode laser with MR temperature-sensitive imaging feedback. Lasers in surgery and medicine 2004;35(1):41–50. - 65.
Yung JP, Shetty A, Elliott A, Weinberg JS, McNichols RJ, Gowda A, Hazle JD, Stafford RJ. Quantitative comparison of thermal dose models in normal canine brain. Medical physics 2010;37(10):5313–21. - 66.
Day ES, Thompson PA, Zhang L, Lewinski NA, Ahmed N, Drezek RA, Blaney SM, West JL. Nanoshell-mediated photothermal therapy improves survival in a murine glioma model. Journal of neuro-oncology 2011;104(1):55–63. - 67.
Earle KM, Carpenter S, Roessmann U, Ross MA, Hayes JR, Zeitler E. Central nervous system effects of laser radiation. Federation proceedings 1965;24(Suppl 14):129. - 68.
Fine S, Klein E, Nowak W, Scott RE, Laor Y, Simpson L, Crissey J, Donoghue J, Derr VE. Interaction of laser radiation with biologic systems. I. Studies on interaction with tissues. Federation proceedings 1965;24(Suppl 14):35–47. - 69.
Jordan A, Scholz R, Maier-Hauff K, van Landeghem FK, Waldoefner N, Teichgraeber U, Pinkernelle J, Bruhn H, Neumann F, Thiesen B, von Deimling A, Felix R. The effect of thermotherapy using magnetic nanoparticles on rat malignant glioma. Journal of neuro-oncology 2006;78(1):7–14. - 70.
Ostrom QT, Bauchet L, Davis FG, Deltour I, Fisher JL, Langer CE, Pekmezci M, Schwartzbaum JA, Turner MC, Walsh KM, Wrensch MR, Barnholtz-Sloan JS. The epidemiology of glioma in adults: a “state of the science” review. Neuro-oncology 2014;16(7):896–913. - 71.
Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RO. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. The Lancet. Oncology 2009;10(5):459–66. - 72.
Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. The New England journal of medicine 2005;352(10):987–96. - 73.
Oppenlander ME, Wolf AB, Snyder LA, Bina R, Wilson JR, Coons SW, Ashby LS, Brachman D, Nakaji P, Porter RW, Smith KA, Spetzler RF, Sanai N. An extent of resection threshold for recurrent glioblastoma and its risk for neurological morbidity. Journal of neurosurgery 2014;120(4):846–53. - 74.
Hervey-Jumper SL, Berger MS. Reoperation for recurrent high-grade glioma: a current perspective of the literature. Neurosurgery 2014;75(5):491–9; discussion 8–9. - 75.
Chaichana KL, Zadnik P, Weingart JD, Olivi A, Gallia GL, Blakeley J, Lim M, Brem H, Quinones-Hinojosa A. Multiple resections for patients with glioblastoma: prolonging survival. Journal of neurosurgery 2013;118(4):812–20. - 76.
Barbagallo GM, Jenkinson MD, Brodbelt AR. ‘Recurrent’ glioblastoma multiforme, when should we reoperate? British journal of neurosurgery 2008;22(3):452–5. - 77.
Ortega A, Sarmiento JM, Ly D, Nuno M, Mukherjee D, Black KL, Patil CG. Multiple resections and survival of recurrent glioblastoma patients in the temozolomide era. Journal of clinical neuroscience: official journal of the Neurosurgical Society of Australasia 2016;24:105–11. - 78.
Chang SM, Parney IF, McDermott M, Barker FG, 2nd, Schmidt MH, Huang W, Laws ER, Jr., Lillehei KO, Bernstein M, Brem H, Sloan AE, Berger M. Perioperative complications and neurological outcomes of first and second craniotomies among patients enrolled in the Glioma Outcome Project. Journal of neurosurgery 2003;98(6):1175–81. - 79.
Moiyadi AV, Shetty PM. Surgery for recurrent malignant gliomas: feasibility and perioperative outcomes. Neurology India 2012;60(2):185–90. - 80.
Hoover JM, Nwojo M, Puffer R, Mandrekar J, Meyer FB, Parney IF. Surgical outcomes in recurrent glioma: clinical article. Journal of neurosurgery 2013;118(6):1224–31. - 81.
Tsao MN, Mehta MP, Whelan TJ, Morris DE, Hayman JA, Flickinger JC, Mills M, Rogers CL, Souhami L. The American Society for Therapeutic Radiology and Oncology (ASTRO) evidence-based review of the role of radiosurgery for malignant glioma. International journal of radiation oncology, biology, physics 2005;63(1):47–55. - 82.
Chan TA, Weingart JD, Parisi M, Hughes MA, Olivi A, Borzillary S, Alahakone D, Detorie NA, Wharam MD, Kleinberg L. Treatment of recurrent glioblastoma multiforme with GliaSite brachytherapy. International journal of radiation oncology, biology, physics 2005;62(4):1133–9. - 83.
Anzai Y, Lufkin R, DeSalles A, Hamilton DR, Farahani K, Black KL. Preliminary experience with MR-guided thermal ablation of brain tumors. AJNR. American journal of neuroradiology 1995;16(1):39–48; discussion 9–52. - 84.
Sakai T, Fujishima I, Sugiyama K, Ryu H, Uemura K. Interstitial laserthermia in neurosurgery. Journal of clinical laser medicine & surgery 1992;10(1):37–40. - 85.
McDannold N. Quantitative MRI-based temperature mapping based on the proton resonant frequency shift: review of validation studies. International journal of hyperthermia: the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group 2005;21(6):533–46. - 86.
Leonardi MA, Lumenta CB. Stereotactic guided laser-induced interstitial thermotherapy (SLITT) in gliomas with intraoperative morphologic monitoring in an open MR: clinical expierence. Minimally invasive neurosurgery: MIN 2002;45(4):201–7. - 87.
Kahn T, Bettag M, Ulrich F, Schwarzmaier HJ, Schober R, Furst G, Modder U. MRI-guided laser-induced interstitial thermotherapy of cerebral neoplasms. Journal of computer assisted tomography 1994;18(4):519–32. - 88.
Tovar-Spinoza Z, Carter D, Ferrone D, Eksioglu Y, Huckins S. The use of MRI-guided laser-induced thermal ablation for epilepsy. Child’s nervous system: ChNS: official journal of the International Society for Pediatric Neurosurgery 2013;29(11):2089–94. - 89.
Sundararajan SH, Belani P, Danish S, Keller I. Early MRI characteristics after MRI-guided laser-assisted cingulotomy for intractable pain control. AJNR. American journal of neuroradiology 2015;36(7):1283–7. - 90.
Sugiyama K, Sakai T, Fujishima I, Ryu H, Uemura K, Yokoyama T. Stereotactic interstitial laser-hyperthermia using Nd-YAG laser. Stereotactic and functional neurosurgery 1990;54–55:501–5. - 91.
Roux FX, Merienne L, Fallet-Bianco C, Beuvon F, Devaux B, Leriche B, Cioloca C. Stereotaxic laser interstitial thermotherapy. A new alternative in the therapeutic management of some brain tumors. Neuro-Chirurgie 1992;38(4):238–44. - 92.
Ascher PW, Justich E, Schrottner O. A new surgical but less invasive treatment of central brain tumours Preliminary report. Acta neurochirurgica. Supplementum 1991;52:78–80. - 93.
Bettag M, Ulrich F, Schober R, Furst G, Langen KJ, Sabel M, Kiwit JC. Stereotactic laser therapy in cerebral gliomas. Acta neurochirurgica. Supplementum 1991;52:81–3. - 94.
Leonardi MA, Lumenta CB, Gumprecht HK, von Einsiedel GH, Wilhelm T. Stereotactic guided laser-induced interstitial thermotherapy (SLITT) in gliomas with intraoperative morphologic monitoring in an open MR-unit. Minimally invasive neurosurgery: MIN 2001;44(1):37–42. - 95.
Schwarzmaier HJ, Eickmeyer F, von Tempelhoff W, Fiedler VU, Niehoff H, Ulrich SD, Ulrich F. MR-guided laser irradiation of recurrent glioblastomas. Journal of magnetic resonance imaging: JMRI 2005;22(6):799–803. - 96.
Carpentier A, Chauvet D, Reina V, Beccaria K, Leclerq D, McNichols RJ, Gowda A, Cornu P, Delattre JY. MR-guided laser-induced thermal therapy (LITT) for recurrent glioblastomas. Lasers in surgery and medicine 2012;44(5):361–8. - 97.
Mohammadi AM, Hawasli AH, Rodriguez A, Schroeder JL, Laxton AW, Elson P, Tatter SB, Barnett GH, Leuthardt EC. The role of laser interstitial thermal therapy in enhancing progression-free survival of difficult-to-access high-grade gliomas: a multicenter study. Cancer medicine 2014;3(4):971–9. - 98.
Patel P, Patel NV, Danish SF. Intracranial MR-guided laser-induced thermal therapy: single-center experience with the Visualase thermal therapy system. Journal of neurosurgery 2016:1–8. - 99.
Metcalfe SE, Grant R. Biopsy versus resection for malignant glioma. The Cochrane database of systematic reviews 2001(3):Cd002034. - 100.
Mintz A, Perry J, Spithoff K, Chambers A, Laperriere N. Management of single brain metastasis: a practice guideline. Current oncology (Toronto, Ont.) 2007;14(4):131–43. - 101.
Colaco R, Martin P, Chiang V. Evolution of multidisciplinary brain metastasis management: case study and literature review. The Yale journal of biology and medicine 2015;88(2):157–65. - 102.
Nayak L, Lee EQ, Wen PY. Epidemiology of brain metastases. Current oncology reports 2012;14(1):48–54. - 103.
Barnholtz-Sloan JS, Sloan AE, Davis FG, Vigneau FD, Lai P, Sawaya RE. Incidence proportions of brain metastases in patients diagnosed (1973 to 2001) in the Metropolitan Detroit Cancer Surveillance System. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 2004;22(14):2865–72. - 104.
Schouten LJ, Rutten J, Huveneers HA, Twijnstra A. Incidence of brain metastases in a cohort of patients with carcinoma of the breast, colon, kidney, and lung and melanoma. Cancer 2002;94(10):2698–705. - 105.
Soon YY, Tham IW, Lim KH, Koh WY, Lu JJ. Surgery or radiosurgery plus whole brain radiotherapy versus surgery or radiosurgery alone for brain metastases. The Cochrane database of systematic reviews 2014;3:Cd009454. - 106.
Greto D, Scoccianti S, Compagnucci A, Arilli C, Casati M, Francolini G, Cecchini S, Loi M, Desideri I, Bordi L, Bono P, Bonomo P, Meattini I, Detti B, Livi L. Gamma Knife radiosurgery in the management of single and multiple brain metastases. Clinical neurology and neurosurgery 2015;141:43–7. - 107.
Powell JW, Chung CT, Shah HR, Canute GW, Hodge CJ, Bassano DA, Liu L, Mitchell L, Hahn SS. Gamma Knife surgery in the management of radioresistant brain metastases in high-risk patients with melanoma, renal cell carcinoma, and sarcoma. Journal of neurosurgery 2008;109(Suppl):122–8. - 108.
Yamamoto M, Hara M, Ide M, Ono Y, Jimbo M, Saito I. Radiation-related adverse effects observed on neuro-imaging several years after radiosurgery for cerebral arteriovenous malformations. Surgical neurology 1998;49(4):385–97; discussion 97–8. - 109.
Chin LS, Ma L, DiBiase S. Radiation necrosis following gamma knife surgery: a case-controlled comparison of treatment parameters and long-term clinical follow up. Journal of neurosurgery 2001;94(6):899–904. - 110.
Ganz JC, Reda WA, Abdelkarim K. Adverse radiation effects after Gamma Knife Surgery in relation to dose and volume. Acta neurochirurgica 2009;151(1):9–19. - 111.
Sneed PK, Mendez J, Vemer-van den Hoek JG, Seymour ZA, Ma L, Molinaro AM, Fogh SE, Nakamura JL, McDermott MW. Adverse radiation effect after stereotactic radiosurgery for brain metastases: incidence, time course, and risk factors. Journal of neurosurgery 2015;123(2):373–86. - 112.
Kohutek ZA, Yamada Y, Chan TA, Brennan CW, Tabar V, Gutin PH, Yang TJ, Rosenblum MK, Ballangrud A, Young RJ, Zhang Z, Beal K. Long-term risk of radionecrosis and imaging changes after stereotactic radiosurgery for brain metastases. Journal of neuro-oncology 2015;125(1):149–56. - 113.
Chuang MT, Liu YS, Tsai YS, Chen YC, Wang CK. Differentiating radiation-induced necrosis from recurrent brain tumor using MR perfusion and spectroscopy: a meta-analysis. PloS one 2016;11(1):e0141438. - 114.
Cicone F, Minniti G, Romano A, Papa A, Scaringi C, Tavanti F, Bozzao A, Maurizi Enrici R, Scopinaro F. Accuracy of F-DOPA PET and perfusion-MRI for differentiating radionecrotic from progressive brain metastases after radiosurgery. European journal of nuclear medicine and molecular imaging 2015;42(1):103–11. - 115.
Terakawa Y, Tsuyuguchi N, Iwai Y, Yamanaka K, Higashiyama S, Takami T, Ohata K. Diagnostic accuracy of 11C-methionine PET for differentiation of recurrent brain tumors from radiation necrosis after radiotherapy. Journal of nuclear medicine: official publication, Society of Nuclear Medicine 2008;49(5):694–9. - 116.
Shah AH, Snelling B, Bregy A, Patel PR, Tememe D, Bhatia R, Sklar E, Komotar RJ. Discriminating radiation necrosis from tumor progression in gliomas: a systematic review what is the best imaging modality? Journal of neuro-oncology 2013;112(2):141–52. - 117.
Shaw PJ, Bates D. Conservative treatment of delayed cerebral radiation necrosis. Journal of neurology, neurosurgery, and psychiatry 1984;47(12):1338–41. - 118.
Kohshi K, Imada H, Nomoto S, Yamaguchi R, Abe H, Yamamoto H. Successful treatment of radiation-induced brain necrosis by hyperbaric oxygen therapy. Journal of the neurological sciences 2003;209(1–2):115–7. - 119.
Levin VA, Bidaut L, Hou P, Kumar AJ, Wefel JS, Bekele BN, Grewal J, Prabhu S, Loghin M, Gilbert MR, Jackson EF. Randomized double-blind placebo-controlled trial of bevacizumab therapy for radiation necrosis of the central nervous system. International journal of radiation oncology, biology, physics 2011;79(5):1487–95. - 120.
Wong ET, Huberman M, Lu XQ, Mahadevan A. Bevacizumab reverses cerebral radiation necrosis. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 2008;26(34):5649–50. - 121.
Gonzalez J, Kumar AJ, Conrad CA, Levin VA. Effect of bevacizumab on radiation necrosis of the brain. International journal of radiation oncology, biology, physics 2007;67(2):323–6. - 122.
Liu AK, Macy ME, Foreman NK. Bevacizumab as therapy for radiation necrosis in four children with pontine gliomas. International journal of radiation oncology, biology, physics 2009;75(4):1148–54. - 123.
Matuschek C, Bolke E, Nawatny J, Hoffmann TK, Peiper M, Orth K, Gerber PA, Rusnak E, Lammering G, Budach W. Bevacizumab as a treatment option for radiation-induced cerebral necrosis. Strahlentherapie und Onkologie: Organ der Deutschen Rontgengesellschaft … [et al] 2011;187(2):135–9. - 124.
Glantz MJ, Burger PC, Friedman AH, Radtke RA, Massey EW, Schold SC, Jr. Treatment of radiation-induced nervous system injury with heparin and warfarin. Neurology 1994;44(11):2020–7. - 125.
Parvez K, Parvez A, Zadeh G. The diagnosis and treatment of pseudoprogression, radiation necrosis and brain tumor recurrence. International journal of molecular sciences 2014;15(7):11832–46. - 126.
Tobler WD, Sawaya R, Tew JM, Jr. Successful laser-assisted excision of a metastatic midbrain tumor. Neurosurgery 1986;18(6):795–7. - 127.
Banerjee C, Snelling B, Berger MH, Shah A, Ivan ME, Komotar RJ. The role of magnetic resonance-guided laser ablation in neurooncology. British journal of neurosurgery 2015;29(2):192–6. - 128.
Paek SH, Audu PB, Sperling MR, Cho J, Andrews DW. Reevaluation of surgery for the treatment of brain metastases: review of 208 patients with single or multiple brain metastases treated at one institution with modern neurosurgical techniques. Neurosurgery 2005;56(5):1021–34; discussion 34. - 129.
Vadivelu S, Schulder M. MRI-guided interstitial laser therapy of brain tumours. In: Jolesz FA, ed. Intraoperative imaging and image-guided therapy. New York, NY, 2014. - 130.
Daut RL, Cleeland CS. The prevalence and severity of pain in cancer. Cancer 1982;50(9):1913–8. - 131.
Bentley JN, Viswanathan A, Rosenberg WS, Patil PG. Treatment of medically refractory cancer pain with a combination of intrathecal neuromodulation and neurosurgical ablation: case series and literature review. Pain medicine (Malden, Mass.) 2014;15(9):1488–95. - 132.
Naja Z, Al-Tannir M, Ziade F, Daher M. Management of cancer pain: different intervention techniques. Le Journal medical libanais. The Lebanese medical journal 2008;56(2):100–4. - 133.
Harsh V, Viswanathan A. Surgical/radiological interventions for cancer pain. Current pain and headache reports 2013;17(5):331. - 134.
Christo PJ, Mazloomdoost D. Interventional pain treatments for cancer pain. Annals of the New York Academy of Sciences 2008;1138:299–328. - 135.
Sloan PA. Neuraxial pain relief for intractable cancer pain. Current pain and headache reports 2007;11(4):283–9. - 136.
Viswanathan A, Harsh V, Pereira EA, Aziz TZ. Cingulotomy for medically refractory cancer pain. Neurosurgical focus 2013;35(3):E1. - 137.
Sharma M, Shaw A, Deogaonkar M. Surgical options for complex craniofacial pain. Neurosurgery clinics of North America 2014;25(4):763–75. - 138.
Rasche D, Rinaldi PC, Young RF, Tronnier VM. Deep brain stimulation for the treatment of various chronic pain syndromes. Neurosurgical focus 2006;21(6):E8. - 139.
Jobst BC. Consensus over individualism: validation of the ILAE definition for drug resistant epilepsy. Epilepsy currents/American Epilepsy Society 2015;15(4):172–3. - 140.
Berg AT, Shinnar S, Levy SR, Testa FM, Smith-Rapaport S, Beckerman B. Early development of intractable epilepsy in children: a prospective study. Neurology 2001;56(11):1445–52. - 141.
Wasade VS, Elisevich K, Tahir R, Smith B, Schultz L, Schwalb J, Spanaki-Varelas M. Long-term seizure and psychosocial outcomes after resective surgery for intractable epilepsy. Epilepsy & behavior E&B 2015;43:122–7. - 142.
Tellez-Zenteno JF, Dhar R, Wiebe S. Long-term seizure outcomes following epilepsy surgery: a systematic review and meta-analysis. Brain: a journal of neurology 2005;128(Pt 5):1188–98. - 143.
Spencer S, Huh L. Outcomes of epilepsy surgery in adults and children. The Lancet. Neurology 2008;7(6):525–37. - 144.
Tebo CC, Evins AI, Christos PJ, Kwon J, Schwartz TH. Evolution of cranial epilepsy surgery complication rates: a 32-year systematic review and meta-analysis. Journal of neurosurgery 2014;120(6):1415–27. - 145.
Bower RS, Wirrell EC, Eckel LJ, Wong-Kisiel LC, Nickels KC, Wetjen NM. Repeat resective surgery in complex pediatric refractory epilepsy: lessons learned. Journal of neurosurgery. Pediatrics 2015;16(1):94–100. - 146.
Curry DJ, Gowda A, McNichols RJ, Wilfong AA. MR-guided stereotactic laser ablation of epileptogenic foci in children. Epilepsy & behavior: E&B 2012;24(4):408–14. - 147.
Wellmer J, Kopitzki K, Voges J. Lesion focused stereotactic thermo-coagulation of focal cortical dysplasia IIB: a new approach to epilepsy surgery? Seizure 2014;23(6):475–8. - 148.
Gonzalez-Martinez J, Vadera S, Mullin J, Enatsu R, Alexopoulos AV, Patwardhan R, Bingaman W, Najm I. Robot-assisted stereotactic laser ablation in medically intractable epilepsy: operative technique. Neurosurgery 2014;10(Suppl 2):167–72; discussion 72–3. - 149.
Esquenazi Y, Kalamangalam GP, Slater JD, Knowlton RC, Friedman E, Morris SA, Shetty A, Gowda A, Tandon N. Stereotactic laser ablation of epileptogenic periventricular nodular heterotopia. Epilepsy research 2014;108(3):547–54. - 150.
Lewis EC, Weil AG, Duchowny M, Bhatia S, Ragheb J, Miller I. MR-guided laser interstitial thermal therapy for pediatric drug-resistant lesional epilepsy. Epilepsia 2015;56(10):1590–8.