Outcomes following surgical interventions for hypothalamic hamartomas: protocol for a systematic review and individual patient data meta-analysis

Background

Hypothalamic hamartomas (HHs) are rare, deep-seated congenital lesions arising from the ventral hypothalamus and the tuber cinereum.1 2 HHs are commonly attached to the mammillary bodies, a location which is densely connected to the mammillothalamic tract and fornix of the Papez circuit, which are thought to be responsible for seizure propagation.1 3 4 A subset of patients harbour a pedunculated HH in the anterior portion of the third ventricle, which can be associated with endocrinopathies such as central precocious puberty.5 6

The classic presentation of posterior-located HH is the onset of epilepsy in infancy or early childhood in the form of gelastic seizures with the majority (>80%) progressing to pharmacoresistant epilepsy.7–9 Some authors attribute long-standing epilepsy to secondary epileptogenesis of extra-HH structures and the onset of a more complex and extensive epileptogenic network with additional seizure types, such as focal motor, focal with impaired awareness, tonic, atonic and bilateral tonic–clonic seizures.7 10–14 Without prompt surgical therapy, half of the patients develop a catastrophic progressive encephalopathic syndrome characterised by cognitive impairment involving multiple domains,9 15 a severe behavioural disorder and a major decline in quality of life.16–20

Invasive stereo-electroencephalography (SEEG) recordings21 and non-invasive studies22 over the last 30 years have confirmed intrinsic epileptogenicity of HHs,22 23 which are thought to arise from pacemaker-like activity of small gamma-aminobutyric acidergic (GABAergic) interneuron-like cells within the HH.24 The assorted epileptic semiologies have been shown to originate within the HH itself.1 11 21 Gelastic seizures are thought to arise from synchronised ictal discharges among coordinated regions of the limbic system, including both the hypothalamus and functionally connected extrahypothalamic limbic (e.g., cingulate, parahippocampal gyrus) and orbitofrontal cortices.24 Other semiologies, such as focal impaired awareness seizures (FIAS), typically represent the involvement of mesial temporal lobe structures.24 Surgically targeting the HH has been the mainstay of treatment of HH-related pharmacoresistant epilepsy since the primarily intrinsic epileptogenicity of the hamartoma was documented in the 1990s. In 2003, the first surgical series directly targeting the HH through open microsurgical resection and disconnection showed that good rates of seizure freedom could be obtained, although at the expense of a trade-off of significant surgical and neurological morbidity.23 Specifically, although >90% seizure improvement occurred in 84.6% of patients, only 15% were seizure free and surgery came at the expense of morbidity in 54% of patients, including thalamo-capsular strokes among other neurological and endocrine deficits.23 Over the last 20 years, many groups have published single centre experiences with open microsurgical resection and/or disconnection of HHs associated with pharmacoresistant epilepsy through lateral (pterional) or vertical (transcallosal interforniceal) surgical corridors tailored to the morphology of the HH as defined by the Delalande classification.25–31 While open approaches could result in seizure freedom in about 50% of patients and translate into heterogeneous improvements of psychiatric outcome and cognitive performance at the group level,32–34 there remains significant morbidity, including memory impairments, hypothalamic (hyperphagia, obesity) dysfunction and neurological deficits, and a risk of ischaemic diencephalic/capsular strokes in up to a third of patients.23 27 35

Over the last 20 years, several surgical approaches have been added to the armamentarium with the goal of offering surgical targeting of the HH with less morbidity than open surgery. These techniques include the ‘less invasive’ endoscopic transventricular disconnection, non-invasive stereotactic radiosurgery (SRS) and minimally invasive stereotactic ablation strategies in the form of radiofrequency thermocoagulation (RFTC) and MR-guided interstitial thermal therapy (MRgLITT).36–40 The endoscopic approach, first reported and used by several groups in the early 2000s,28 41 42 has been shown to significantly reduce operative blood loss and shorten the length of stay (LOS) compared with open approaches;28 32 36 37 41 43–49 however, it is only feasible for HH with favourable configuration, such as Delalande Type II and III, and is associated with a non-negligible rate of memory and hypothalamic deficits.36 37 50 SRS was first applied to treat HH in the early 2000s as a non-invasive alternative suited for small- and medium-sized HHs, providing good seizure outcomes without long-term neurological sequelae.32 41 51–53 From a technical standpoint, SRS allows for conformational treatment adapted to the shape of the HH. However, due to the need to limit radiation exposure to <10 Gy at the optic apparatus, indications for SRS are limited in size (<15 mm) and disconnections of larger HHs are largely ineffective.54–56 This technique is hindered by an increase in seizure frequency increase in 16% of patients and a delayed therapeutic effect that can take up to 2–3 years.51 52 56 57 In the largest and only prospective trial in 48 patients with principally intrahypothalamic HHs (Delalande Type II and III), SRS demonstrated very good seizure freedom rates (40%), very low temporary deficits (6% poikilothermia) and no permanent neurological, neuropsychological, hypothalamic or endocrine morbidity.56 Because of its delayed nature, it is ideal for patients with high presurgical cognitive function, who will benefit from the lower risk of memory impairment, and an indolent clinical course (e.g., no progressive neuropsychological decline) who will not be disadvantaged by the delayed efficacy.

Both RFTC and MRgLITT have clear ‘minimally invasive’ benefits, including avoidance of ICU stay, and reduced LOS, blood loss and postoperative pain. These minimally invasive approaches have also been shown to reduce collateral damage to critical structures encountered in the approach (e.g., the corpus callosum and fornices) or at the target (e.g., hypothalamus, mammillary bodies/MTT). As a result, although long-term data are currently unavailable for MRgLITT, these techniques have a favourable risk–benefit profile, with a greater (70%) seizure freedom and reduced morbidity compared with open surgery.58–60 Over the last decade, MRgLITT and RFTC have emerged as the first-line treatment for HH in many centres across North America and Asia, respectively.61–63 In the largest study to date, in 58 cases of HH treated by MRgLITT, 81% were free from gelastic seizures, often requiring staged interventions.60 A variant of the standard SEEG-guided RFTC technique, in which one-stage high density RFTC is performed, may further increase the efficacy of this approach at the expense of requiring multiple probe trajectories in a given patient.47 64 While both stereotactic approaches are safe, there is a non-negligeable rate of transient and permanent morbidity, including memory impairment in 20% and hypothalamic injury in 27% in some studies.56 65–68 Very recently, MR-guided focused ultrasound (MRgFUS) has been discussed in the literature for central lesions in the brain.69 MRgFUS is completely non-invasive procedure that consists of directing multiple acoustic beams at a focal intracranial site, creating a coagulation lesion within the targeted tissue while monitoring the ablation process using real-team MR thermography.70 So far, only a total of five cases (four with epilepsy) have been reported in the literature with favourable outcomes and no major complications.69 71

Despite over 20 years of published reports of these techniques for the treatment of HH-related pharmacoresistant epilepsy, there is a paucity of well-conducted studies that directly compare efficacy and safety, and identify the optimal technique for the entire population or specific subgroups of HHs.32 51 72 The literature is almost exclusively limited to small case series and case reports describing novel techniques and is methodologically hampered by sample size and cohorts with a single treatment arm and limited follow-up. There are also several meta-analyses investigating developmental, endocrine, neuropsychological and seizure outcomes in surgically managed HH; however, to our knowledge, no study investigates the full landscape of surgical approaches to treat HH-related pharmacoresistant epilepsy.32 51 The current study fills an important knowledge gap and can help inform surgical management and decision making for both clinicians and patients with HH undergoing surgical interventions.

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