Neurological Sciences
https://doi.org/10.1007/s10072-018-3444-9

ORIGINAL ARTICLE

Hippocampal deep brain stimulation: persistent seizure control
after bilateral extra-cranial electrode fracture
Massimo Piacentino 1

1

1

& Giacomo Beggio & Lara Zordan & Paolo Bonanni

2

Received: 11 September 2017 / Accepted: 8 May 2018
# Springer-Verlag Italia S.r.l., part of Springer Nature 2018

Abstract
Hippocampal deep brain stimulation (DBS) can provide an effective alternative for intractable temporal lobe epilepsy. In this case
report, we describe a peculiar outcome after a post-traumatic wire-disconnection of a bilateral hippocampal DBS device. The
patient presented a postoperative long-term significant reduction in seizure frequency even with an absent electric stimulation.
This case gives the possibility to consider alternatives in epilepsy surgery, based on stimulation interference (lesional or electrical
disturbing) in the epileptogenic zone.
Keywords Hippocampal DBS . Temporal lobe epilepsy . Traumatic wire-disconnection . Epilepsy surgery . Long-term seizure
control

Introduction

Case description

Epilepsy is a common neurological disorder that affects 0.5 to
1% of the population [4]. Almost 30% of epileptic patients
suffers from an uncontrolled disease or presents drug-related
side effects [6]. Surgery for epilepsy or deep brain stimulation
(DBS) could provide an effective alternative in this medical
refractory subgroup [3].
Hippocampal DBS showed good results for intractable
temporal lobe epilepsy [8] by inducing significant ameliorations in seizure freedom and a borderline significant improvement in quality of life [1, 2, 10, 12].
Here, we present a peculiar outcome after posttraumatic
wire-disconnection of a bilateral hippocampal DBS device
for medical-refractory temporal lobe epilepsy with a longterm significant reduction in seizure frequency even with an
absent electric stimulation.

A 48-year-old male patient with a history of epilepsy with
complex partial seizures came to our institution for a
presurgical evaluation. He reported a posttraumatic generalized seizure at 9 months of age without subsequent episodes
until the age of 25. From that moment on, he complained of
occasional seizures starting with dizziness and generalized discomfort (face sensation of warmth) followed by hypertonic or
tonic-clonic generalized episodes. After the loss of consciousness, the family members reported the presence of staring,
chewing automatisms, vocalizations, and purposeless hands
automatisms with final trunk inconstant (in terms of laterality)
deviations. During the first years, the patient underwent several inconclusive neurological evaluations (electroencephalogram, clinical examination and seizures observation). All the
tests were not able to identify a clear epileptogenic focus or at
least the lateralization in terms of temporal side. All the electroencephalograms (EEGs) showed inter-ictal phases without
a prevalence in terms of electrical pathological signs (spikes,
spike-waves, and constant Delta-Tetha rhythms with no lateralization). The epileptic seizures were characterized by a frequency of 8 episodes per month, presented a mean duration of
2 to 3 min each, and were followed by drowsiness lasting up to
10 min. The patient was unsuccessfully treated by an association of carbamazepine, phenobarbital, and clonazepam (regularly controlled plasma concentrations).

* Massimo Piacentino
massimo.piacentino@ulssvicenza.it
1

Department of Neurosurgery, San Bortolo Hospital, Viale Rodolfi,
37, 36100 Vicenza, Italy

2

IRCS A. Meda, Conegliano, Italy

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Presurgical evaluation
The patient was admitted for presurgical evaluation on
March 2009. The neurological examination was normal
and the neuropsychological tests showed a QIv at 67, a QIp
at 75 and a QIt at 67 with verbal and visuospatial memory
alteration associated to a deficit of attention. Standard and
functional cerebral MRI showed a bi-temporal hippocampal
sclerosis and a left dominant hemispheric localization. The
preoperative antiepileptic therapy was rufinamide 1200 mg/
day (600 mg + 600 mg), valproate 1000 mg/day (500 mg +
500 mg), phenobarbital 200 mg/day (100 mg + 100 mg), and
topiramate 250 mg/day (50 mg + 100 mg + 100 mg). The
inter-critical EEG showed bi-temporal slow wave rhythm
with fronto-temporal left sharp waves and temporooccipital high-voltage slow waves on the right hemisphere.

The video EEG recording documented two different kinds of
seizure: staring with gestural automatism with both hands
and feet followed by chewing and swallowing (Fig. 1a).
During the attack, the patient was not able to respond to
simple questions with evident unawareness and confusion.
The episodes lasted about 1 min and were followed by confusion and aphasia up to 3 min. These seizures were characterized by temporal spikes starting and lasting on the left
temporal hemisphere. The second typology of epileptic attacks was characterized by blinking, face muscle contractions with mouth repetitive movements, trunk bending on
both sides, complex gestural automatisms, vocalization with
confusion, and unawareness (Fig. 1b). These seizures lasted
about 1 min and presented post-ictal dizziness up to 2 or
3 min. The video EEG recording showed spikes starting
from the right temporal hemisphere.

Fig. 1 EEG recording. Left (a) and right (b) temporal seizure. The red star indicates the beginning of the seizure

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Surgery
The presurgical evaluation did not give the possibility to plan
a surgical action that could obtain a complete control of the
symptomatology. The remaining alternative solutions were
vagal nerve stimulation (VNS), anterior thalamic nucleus
DBS (AN-DBS), or bilateral hippocampal stimulation.
Considering the preoperative assessment and the evidence of
bi-temporal independent foci with bilateral hippocampal sclerosis, we decided to perform a bilateral DBS hippocampal
stimulation.
Surgery was performed in two steps. First, the stereotactic
hippocampal electrodes were implanted, followed by electrode externalization and video EEG recording, and second,
the leads were internalized and connected to the pulse
generator.
Under general anesthesia, the patient was fixed to the stereotactic frame (Radionics CRW Burlington Vermont), stereotactic computed tomography (CT) scan was performed,
charged into the neuronavigation system (Stealth Station
Medronic Minneapolis) and merged with gadoliniumenhanced T1-weighted MRI and cerebral Angio-CT scan.
Right and left hippocampal targeting was obtained choosing
the Subiculum as center. The trajectory passed through an
occipital extra-ventricular line parallel to the length of the
hippocampus with contact 0 at the tip of the hippocampal
head. The intraoperative X-ray control showed a
mispositioning of the right electrode although the EEG signal
was compatible with the chosen target (slow wave rhythm
with sharp wave). The electrode was removed and replaced
in the planned position. After surgery, the external cables were
connected to the electrodes for stereo EEG recording. The
inter-critical EEG showed bilateral slow waves rhythm with
bilateral independent spikes and waves. Unfortunately, no seizures were seen in the postoperative week. The external cables
were subsequently removed because of the potential infection
risk. Successively, the wire extensions were tunneled along
the neck and connected to the pulse generator (Medtronic
Kinetra Medtronic Inc. Minneapolis MN) in a sub-clavicular
pouch on the anterior right side of the chest. During the postoperative period, no seizures were recorded and the pulse
generator was activated 2 weeks later starting with 0.5 V,
130 Hz PW 450 Ms. The intensity was progressively increased up to 1.5 V in the following month. No side effect
or surgical complications were observed. Medical therapy was
left unchanged.

had a severe bladder infection with high fever that induced a
generalized tonic-clonic seizure with fall and consequently
fracture of the right electrode and stretching of both extensions. After this episode, the patient experienced only 3 minor
episodes that lasted up to 1 min without loss of consciousness.
In January 2015, a bronchopneumonia induced a second generalized seizure with subsequent fall and fracture of the left
implanted electrode, confirmed by impedance measurement,
cranial and neck X-ray (Figs. 2 and 3). The post-traumatic CT
scan did not show any kind of contusive or hemorrhagic brain
damages (Fig. 4). Secondary to the low frequency of epileptic
symptoms, we decided a wait-and-see solution. After
2 months, the patient presented a new generalized seizure.
We newly decided to wait-and-see and eventually propose a
surgical solution in case of epileptic recurrence. After the
posttraumatic total disconnection of the DBS system, the patient reported no major seizure (Fig. 5). The EEG presented
the absence of great pathological aspects except for few spikes
and some bilateral slow waves. At present, at 5 years from the
surgery, the patient describes only minor dizziness sensation at
the awakening. The most recent neuropsychological evaluation showed a QIv at 74, a QIp at 82 and a QIt at 75.

Follow-up
After an initial stability of the illness, in May 2011, the number of seizures started to decrease progressively reaching a
frequency of 2 episodes per month. In June 2012, the patient

Fig. 2 Coronal X-ray confirming the fracture and the stretching of the
implanted electrodes

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Fig. 3 Sagittal X-ray confirming the fracture and the stretching of the
implanted electrodes

Fig. 5 Graphic representation of seizure episodes during the 8 years of
follow-up. The y-axis indicates the number of episodes per year. The xaxis shows the years of follow-up

Discussion

Fig. 4 Axial reconstruction of post traumatic CT scan, showing the
absence of contusive or hemorrhagic brain damages

Medial temporal lobe epilepsy is characterized by electrical
seizure onset in the amygdala and hippocampus [8] and medial temporal lobe structures stimulation via DBS showed the
possibility to control the symptomatology [11]. As described
by Sprengers et al. [9], a direct stimulation of the epileptogenic
onset region may lead to a focal inhibition of the hyper excitable region and suppression of the epileptic symptoms.
However, the mechanism of action of DBS remains unclear
and some authors explain the efficacy of DBS by the induced
lesion secondary to the insertion of the electrode, the
microthalamotomy effect [5].
This case report shows a very particular outcome in terms
of controlling a refractory epileptic disease without a real current delivery. Discussing the patient’s file two possible explanations is fundable to describe the produced DBS effect. First,
the related iatrogenic lesion secondary to the repositioning of
the right electrode for the reported misplacement could have
produced a disconnection on the right hippocampus.
However, this could not efficiently explain the control of the
bi-temporal epilepsy. Secondly, the presence of a foreign body

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inside the hippocampus may interfere with the electrical activity inside the involved neuronal pathway. Theoretically, a
deep electrical recording represents the only way to show a
possible change in the involved neural structures. However,
this cannot be proposed to the patient with the only goal to
detect a merely speculative aspect.
The amelioration of QI reported by the patient was in contrast with the results reported by the literature. Both TellezZenteno et al. [9] and McLachlan et al. [7] reported the absence
of amelioration or even slight worsening in neuropsychological outcome after hippocampal DBS. However, the effects of
neuromodulation were recorded with a short follow-up and
therefore could not be appropriately compared to our results.
This case focuses also on the fragility of the DBS implant.
Patients that are suspected to be prone to falls need a periodical test concerning the impedence of their neuromodulating
system. This control should be made in all patients implanted
with DBS system without a disease selection subgroup.
Therefore, either patients affected by epilepsy or by other
neurological disorders, like Parkinson’s Disease, should be
continuously monitored.

Patient consent The patient has consented to submission of this case
report to the journal.

References
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Conclusions
This case gives the possibility to explore and consider new
alternatives in epilepsy surgery. Less invasive methodologies,
based on the idea of stimulation interference (lesional or electrical disturbing) in the epileptogenic zone, could represent a
potential surgical solution. Moreover, this does not contraindicate or prevent a traditional and more aggressive surgical
treatment in case of failure.
Although the particular interest that this case could rise, it is
necessary to gather a larger number of patients with similar
conditions in order to draw reliable conclusions.

Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.

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