Accepted Manuscript Title: A case of ipsilateral chin-eyelid synkinesis after brain trauma without peripheral facial nerve lesion Author: Davide Ferrazzoli Pietro Balbi Luca Caremani Luca Sebastianelli Alessio Zarucchi Marina Capobianco Lorenza Bettiga Leopold Saltuari Giuseppe Frazzitta PII: DOI: Reference:
S0303-8467(14)00168-1 http://dx.doi.org/doi:10.1016/j.clineuro.2014.05.002 CLINEU 3711
To appear in:
Clinical Neurology and Neurosurgery
Received date: Revised date: Accepted date:
13-3-2014 30-4-2014 3-5-2014
Please cite this article as: Ferrazzoli Davide, Balbi Pietro, Caremani Luca, Sebastianelli Luca, Zarucchi Alessio, Capobianco Marina, Bettiga Lorenza, Saltuari Leopold, Frazzitta Giuseppe.A case of ipsilateral chin-eyelid synkinesis after brain trauma without peripheral facial nerve lesion.Clinical Neurology and Neurosurgery http://dx.doi.org/10.1016/j.clineuro.2014.05.002 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Case Report A case of ipsilateral chin-eyelid synkinesis after brain trauma without peripheral facial nerve lesion. Davide Ferrazzoli1, Pietro Balbi2, Luca Caremani1, Luca Sebastianelli1, Alessio Zarucchi1, Marina
ip t
Capobianco1, Lorenza Bettiga1, Leopold Saltuari3, Giuseppe Frazzitta1,4.
Department of Neurorehabilitation, “Moriggia-Pelascini” Hospital, Gravedona ed Uniti, Italy.
2
Department of Neurorehabilitation, Scientific Institute of Pavia via Boezio, IRCCS, 'Salvatore
cr
1
Maugeri' Foundation, Pavia, Italy. Department of Neurology, Hospital Hochzirl, Austria.
4
Fondazione Europea Ricerca Biomedica FERB, “S.Isidoro” Hospital, Trescore Balneario, Italy.
an
us
3
Keywords: brain trauma, facial nerve lesion, chin-eyelid synkinesis, central nervous plasticity.
M
Corresponding author: Davide Ferrazzoli, MD
d
Department of Neurorehabilitation, “Moriggia-Pelascini” Hospital, Gravedona ed Uniti, Italy.
Ac ce pt e
Via Pelascini, 3 22015 – Gravedona ed Uniti, Como, Italy. email: [email protected]
Phone: +393318643163 +39034492111 1. Introduction
The involuntary co-contraction of ipsilateral muscles of the face is a common consequence of facial nerve lesion. A chin-eyelid synkinesis is a common consequence of facial nerve pathologies generally due to a peripheral facial paresis, although other pathological processes might be involved [1]. The most frequently observed phenomenon is a contraction of perioral muscles synchronous with the rhythmic eyelid closures. It is generally accepted that a pathologic rearrangement of facial nerve fibers leads to an ectopic diffusion of the contraction signals [2-3]. To our knowledge, there are no reports of patients showing chin-eyelid synkinesis in absence of a facial nerve injury. Here we report the clinical case of a young male who developed an orbicularis oculi - mentalis muscle synkinesis after a brain trauma. Interestingly, neither clinical nor instrumental evidences of facial nerve lesion were demonstrated. We therefore hypothesize that the abnormal coactivation was due to central nervous plasticity. 2. Clinical case
Page 1 of 7
A 20 years old male had a traumatic brain injury during a car accident in September 2011, determining a two months prolonged loss of consciousness. He was admitted to an intensive care unit, mechanically ventilated and underwent an endovascular procedure in order to treat a right cavernous sinus-carotid fistula. After six months of rehabilitation, he was admitted to a long term care facility, in a stable condition of minimally conscious state and bilateral hemiparesis, more severe to the left side. Eighteen months after the trauma, he was admitted to our neurorehabilitation
ip t
unit, with three main purposes: titration of intrathecal baclofen and treatment of postural deformities, evaluation/treatment of a post-hemorrhagic hydrocephalus to possibly ameliorate the
cr
level of consciousness. At the hospitalization, he showed a left chin and perioral contraction for every spontaneous closure of the eyelids (video).
us
Furthermore, when the left palmomental reflex was elicited, the ipsilateral eyelid closure was consistently induced. The smiling was completely symmetric, and all the facial muscles of the left
an
side had a normal strength, including the orbicularis oculi. The patient had not a previous history of facial palsy and no signs of facial hemiatrophy were detected at the physical examination. MRI scan
3. Electrophysiologic evaluation
Ac ce pt e
3.1 ENG-EMG-Blink Reflex
d
poles (Fig.2).
M
showed sequelae of diffuse axonal injury, and contusive lesions in both frontal lobes and temporal
ENG-EMG data were collected using a data acquisition system (Micromed Myoquick Device, Mogliano Veneto, Italy). The signals were amplified with an overall gain of 1000 (common mode rejection ratio:>100 dB at 60 Hz and input impedance:>100 MΩ). The analog signals were converted to digital ones at a sampling rate of 32768 Hz for EMG and at a sampling rate of 16384 Hz for ENG and Blink reflex, by using a 16-bit converter (System plus evolution software, Micromed, Mogliano Veneto, Italy). Two pole filter IIR (infinite impulse response) was chosen and the Bandpass (5–5000 Hz) and bandstop (50 Hz) filters have been set to process the signal.
3.1.1 ENG Disposable bipolar rectangular surface electrodes (Neuroline 70010-K/C/12, Ambu ®, Ballerup, Denmark) with a diameter of 11.4 mm (3 M) were positioned at an interelectrode distance of 3 cm. Prior to applying the electrodes, skin impedance was reduced by shaving excess body hair, gently abrading the skin with fine-grade sandpaper, and wiping the skin with alcohol swabs. Motor latency and cMAP amplitude of VII cranial nerves were assessed by electrical stimulation 1 cm before the tragus recording from the inferior orbicularis oculi muscle, with the reference electrode placed on
Page 2 of 7
the lateral canthus of the eye, using the standard belly tendon montage. Facial nerve motor latency was 2 ms on the affected side and 2.1 ms on the contralateral side; cMAP amplitude was 2.5 mV on the affected side and 2.3 mV on the contralateral orbicularis oculi muscle. These values were considered normal, according to the normative data of our laboratory (amplitude (mV) ≥ 1.0; distal latency (ms) ≤ 3.1).
ip t
3.1.2 EMG
An EMG coaxial needle examination (Neuroline concentric needle, 38x0,45 mm – 1,5''x26G, Ambu
cr
®, Ballerup, Denmark) was performed on the orbicularis oculi muscle at 0,5 cm lateral to the bony margin of orbit and on the orbicularis oris muscle at approximately 0,5 cm below the lower border
us
of the lower lip, in order to search for signs of denervation. Voluntary contraction for the muscles investigated was performed too. Needle examination did not show spontaneous activity, nor
an
reduced voluntary EMG activity, nor increased size of motor units.
3.1.3 Blink-Reflex
M
The blink reflex was evoked by stimulation of the left and right supraorbital nerves. Stimuli of 0.1 ms duration and 3–20 mA intensity were applied percutaneously at a frequency of 0,3 Hz. The
d
orbicularis oculi muscle responses were recorded by surface electrodes with the active electrode
Ac ce pt e
over the lower lid halfway between the inner and outer edges of the orbit and reference electrode over the ipsilateral temple.
Following the stimulation of each supraorbital nerve, we performed a bilateral blink-reflex corecording with surface electrodes from the orbicularis oculi and mentalis muscles. After stimulation on the affected left side, the ipsilateral R1 and R2 components were present with normal latency (9.8 ms and 38.6 ms respectively) on the orbicularis oculi. In addition, both R1 and R2 responses were also recorded from the ipsilateral mentalis muscle (latency of 10.5 ms and 37.5 ms, respectively). The contralateral R2 component was present only on the right orbicularis oculi with normal latency (41.9 ms) (Fig.1).
After stimulation on the right side, the R1 and R2 components were present on the ipsilateral orbicularis oculi with normal latency (10.8 ms and 38 ms respectively), while the contralateral R2 component was simultaneously recorded from the left orbicularis oculi and mentalis muscles with a latency of 41.8 ms.
4. Discussion and conclusions
Page 3 of 7
Synkinesis of facial muscles mainly occurs as an effect of aberrant reinnervation following axonal damage of the facial nerve [3]. In these cases, the fibers that originally innervated a facial muscle may supply other muscle by misdirection. In addition, facial synkinesis are also featured in hemifacial spasm, both in the idiopathic form and in that sustained by vascular compression of the facial nerve [4]. An ephaptic transmission (cross-talk) of the nervous impulses at the site of the compression, or the hyperexcitability of the facial nucleus have been proposed as the most likely
ip t
pathophysiologies of the disease.
In this paper we report on a patient who exhibited unilateral synkinesis of facial muscles following
cr
a major traumatic brain injury, in absence of clinical, radiologic and electrophysiological signs of peripheral facial nerve involvement. To the best of our knowledge, this case report is the first
us
description of periocular-mentalis abnormal co-contraction following uniquely hemispheric posttraumatic lesions.
an
Moreover, our electrophysiological findings, apart from ruling out peripheral facial nerve abnormalities, show that the left mentalis muscle identically performs to the left orbicularis oculi. It can be indeed activated a) through a reflex oligosynaptic pathway following the ipsilateral
M
supraorbital nerve stimulation, b) through a reflex polysynaptic pathway after contralateral supraorbital nerve stimulation, c) during spontaneous eyeblink. The consistency and the latencies of
d
the reflex responses from the mentalis muscle support the view that an identical brainstem pathway
muscle.
Ac ce pt e
is responsible for the synchronous reflex activation of the left orbicularis oculi and mentalis
The most likely explanation, in our opinion, of the behavior of the left mentalis muscle could be found in a partial lesion of contralateral cortico-nuclear inhibitory connections to the facial nucleus, responsible to free from a tonic supranuclear inhibition some parts of the left facial nucleus. This hypothesis is reminiscent of the abnormal post-stroke coactivation in paretic limb muscles following lesions of cortico-spinal pathways, where the muscle synergies rely on the decreased selective control of each individual muscle [5]. Finally, as an alternative explanation of the clinical and electrophysiological behavior of the left mentalis muscle, a reorganization of brainstem circuits could be also hypothesized. According to this, a post-traumatic damage at the pons or medulla has to be postulated, although neither clinical nor imaging data were indicative of brainstem lesions.
References [1] Moran CJ, Neely JC. Patterns of Facial Nerve Synkinesis. The Laryngoscope 1996;106:1491–6.
Page 4 of 7
[2] Tan NC, Chan LL, Tan EK. Hemifacial spasm and involuntary facial movements. QJM 2002;95:493-500. [3] Kimura J, Rodnitzky RL, Okawara S. Electrophysiological analysis of aberrant regeneration after facial nerve paralysis. Neurology 1975;25:989-93. [4] Auger RG. Hemifacial spasm: clinical and electrophysiological observations. Neurology 1979;29:1261-72.
ip t
[5] Ohn SH, Yoo W-K, Kim DY, Ahn S, Jung B, Choi I et al. Measurement of synergy and spasticity during functional movement of the post-stroke hemiplegic upper limb. J
cr
Electromyogr Kinesiol 2013 Apr;23:501-7.
us
Fig. 1.
Blink reflex evoked by stimulation of the supraorbital nerve on the left side
an
Trace n.1: recording of the left orbicolaris oculi, showing a normal R1 and R2 response; Trace n.2: recording of the right orbicolaris oculi, showing a normal R2 response; Trace n. 3: recording of the
oculi;
M
left mentalis muscle, showing a R1 and R2 components with the same latency of the left orbicularis
Ac ce pt e
d
Trace n.4: recording of the right mentalis muscle, showing no response.
Page 5 of 7
ip t cr us an M d Ac ce pt e
Fig. 2.
MRI images
MRI scan shows sequelae of diffuse axonal injury, and contusive lesions in frontal lobes and temporal poles. A: T1W/SE Sag; B: FLAIR Ax; C: FLAIR Ax.
Page 6 of 7
Page 7 of 7
d
Ac ce pt e us
an
M
cr
ip t
S0303-8467(14)00168-1 http://dx.doi.org/doi:10.1016/j.clineuro.2014.05.002 CLINEU 3711
To appear in:
Clinical Neurology and Neurosurgery
Received date: Revised date: Accepted date:
13-3-2014 30-4-2014 3-5-2014
Please cite this article as: Ferrazzoli Davide, Balbi Pietro, Caremani Luca, Sebastianelli Luca, Zarucchi Alessio, Capobianco Marina, Bettiga Lorenza, Saltuari Leopold, Frazzitta Giuseppe.A case of ipsilateral chin-eyelid synkinesis after brain trauma without peripheral facial nerve lesion.Clinical Neurology and Neurosurgery http://dx.doi.org/10.1016/j.clineuro.2014.05.002 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Case Report A case of ipsilateral chin-eyelid synkinesis after brain trauma without peripheral facial nerve lesion. Davide Ferrazzoli1, Pietro Balbi2, Luca Caremani1, Luca Sebastianelli1, Alessio Zarucchi1, Marina
ip t
Capobianco1, Lorenza Bettiga1, Leopold Saltuari3, Giuseppe Frazzitta1,4.
Department of Neurorehabilitation, “Moriggia-Pelascini” Hospital, Gravedona ed Uniti, Italy.
2
Department of Neurorehabilitation, Scientific Institute of Pavia via Boezio, IRCCS, 'Salvatore
cr
1
Maugeri' Foundation, Pavia, Italy. Department of Neurology, Hospital Hochzirl, Austria.
4
Fondazione Europea Ricerca Biomedica FERB, “S.Isidoro” Hospital, Trescore Balneario, Italy.
an
us
3
Keywords: brain trauma, facial nerve lesion, chin-eyelid synkinesis, central nervous plasticity.
M
Corresponding author: Davide Ferrazzoli, MD
d
Department of Neurorehabilitation, “Moriggia-Pelascini” Hospital, Gravedona ed Uniti, Italy.
Ac ce pt e
Via Pelascini, 3 22015 – Gravedona ed Uniti, Como, Italy. email: [email protected]
Phone: +393318643163 +39034492111 1. Introduction
The involuntary co-contraction of ipsilateral muscles of the face is a common consequence of facial nerve lesion. A chin-eyelid synkinesis is a common consequence of facial nerve pathologies generally due to a peripheral facial paresis, although other pathological processes might be involved [1]. The most frequently observed phenomenon is a contraction of perioral muscles synchronous with the rhythmic eyelid closures. It is generally accepted that a pathologic rearrangement of facial nerve fibers leads to an ectopic diffusion of the contraction signals [2-3]. To our knowledge, there are no reports of patients showing chin-eyelid synkinesis in absence of a facial nerve injury. Here we report the clinical case of a young male who developed an orbicularis oculi - mentalis muscle synkinesis after a brain trauma. Interestingly, neither clinical nor instrumental evidences of facial nerve lesion were demonstrated. We therefore hypothesize that the abnormal coactivation was due to central nervous plasticity. 2. Clinical case
Page 1 of 7
A 20 years old male had a traumatic brain injury during a car accident in September 2011, determining a two months prolonged loss of consciousness. He was admitted to an intensive care unit, mechanically ventilated and underwent an endovascular procedure in order to treat a right cavernous sinus-carotid fistula. After six months of rehabilitation, he was admitted to a long term care facility, in a stable condition of minimally conscious state and bilateral hemiparesis, more severe to the left side. Eighteen months after the trauma, he was admitted to our neurorehabilitation
ip t
unit, with three main purposes: titration of intrathecal baclofen and treatment of postural deformities, evaluation/treatment of a post-hemorrhagic hydrocephalus to possibly ameliorate the
cr
level of consciousness. At the hospitalization, he showed a left chin and perioral contraction for every spontaneous closure of the eyelids (video).
us
Furthermore, when the left palmomental reflex was elicited, the ipsilateral eyelid closure was consistently induced. The smiling was completely symmetric, and all the facial muscles of the left
an
side had a normal strength, including the orbicularis oculi. The patient had not a previous history of facial palsy and no signs of facial hemiatrophy were detected at the physical examination. MRI scan
3. Electrophysiologic evaluation
Ac ce pt e
3.1 ENG-EMG-Blink Reflex
d
poles (Fig.2).
M
showed sequelae of diffuse axonal injury, and contusive lesions in both frontal lobes and temporal
ENG-EMG data were collected using a data acquisition system (Micromed Myoquick Device, Mogliano Veneto, Italy). The signals were amplified with an overall gain of 1000 (common mode rejection ratio:>100 dB at 60 Hz and input impedance:>100 MΩ). The analog signals were converted to digital ones at a sampling rate of 32768 Hz for EMG and at a sampling rate of 16384 Hz for ENG and Blink reflex, by using a 16-bit converter (System plus evolution software, Micromed, Mogliano Veneto, Italy). Two pole filter IIR (infinite impulse response) was chosen and the Bandpass (5–5000 Hz) and bandstop (50 Hz) filters have been set to process the signal.
3.1.1 ENG Disposable bipolar rectangular surface electrodes (Neuroline 70010-K/C/12, Ambu ®, Ballerup, Denmark) with a diameter of 11.4 mm (3 M) were positioned at an interelectrode distance of 3 cm. Prior to applying the electrodes, skin impedance was reduced by shaving excess body hair, gently abrading the skin with fine-grade sandpaper, and wiping the skin with alcohol swabs. Motor latency and cMAP amplitude of VII cranial nerves were assessed by electrical stimulation 1 cm before the tragus recording from the inferior orbicularis oculi muscle, with the reference electrode placed on
Page 2 of 7
the lateral canthus of the eye, using the standard belly tendon montage. Facial nerve motor latency was 2 ms on the affected side and 2.1 ms on the contralateral side; cMAP amplitude was 2.5 mV on the affected side and 2.3 mV on the contralateral orbicularis oculi muscle. These values were considered normal, according to the normative data of our laboratory (amplitude (mV) ≥ 1.0; distal latency (ms) ≤ 3.1).
ip t
3.1.2 EMG
An EMG coaxial needle examination (Neuroline concentric needle, 38x0,45 mm – 1,5''x26G, Ambu
cr
®, Ballerup, Denmark) was performed on the orbicularis oculi muscle at 0,5 cm lateral to the bony margin of orbit and on the orbicularis oris muscle at approximately 0,5 cm below the lower border
us
of the lower lip, in order to search for signs of denervation. Voluntary contraction for the muscles investigated was performed too. Needle examination did not show spontaneous activity, nor
an
reduced voluntary EMG activity, nor increased size of motor units.
3.1.3 Blink-Reflex
M
The blink reflex was evoked by stimulation of the left and right supraorbital nerves. Stimuli of 0.1 ms duration and 3–20 mA intensity were applied percutaneously at a frequency of 0,3 Hz. The
d
orbicularis oculi muscle responses were recorded by surface electrodes with the active electrode
Ac ce pt e
over the lower lid halfway between the inner and outer edges of the orbit and reference electrode over the ipsilateral temple.
Following the stimulation of each supraorbital nerve, we performed a bilateral blink-reflex corecording with surface electrodes from the orbicularis oculi and mentalis muscles. After stimulation on the affected left side, the ipsilateral R1 and R2 components were present with normal latency (9.8 ms and 38.6 ms respectively) on the orbicularis oculi. In addition, both R1 and R2 responses were also recorded from the ipsilateral mentalis muscle (latency of 10.5 ms and 37.5 ms, respectively). The contralateral R2 component was present only on the right orbicularis oculi with normal latency (41.9 ms) (Fig.1).
After stimulation on the right side, the R1 and R2 components were present on the ipsilateral orbicularis oculi with normal latency (10.8 ms and 38 ms respectively), while the contralateral R2 component was simultaneously recorded from the left orbicularis oculi and mentalis muscles with a latency of 41.8 ms.
4. Discussion and conclusions
Page 3 of 7
Synkinesis of facial muscles mainly occurs as an effect of aberrant reinnervation following axonal damage of the facial nerve [3]. In these cases, the fibers that originally innervated a facial muscle may supply other muscle by misdirection. In addition, facial synkinesis are also featured in hemifacial spasm, both in the idiopathic form and in that sustained by vascular compression of the facial nerve [4]. An ephaptic transmission (cross-talk) of the nervous impulses at the site of the compression, or the hyperexcitability of the facial nucleus have been proposed as the most likely
ip t
pathophysiologies of the disease.
In this paper we report on a patient who exhibited unilateral synkinesis of facial muscles following
cr
a major traumatic brain injury, in absence of clinical, radiologic and electrophysiological signs of peripheral facial nerve involvement. To the best of our knowledge, this case report is the first
us
description of periocular-mentalis abnormal co-contraction following uniquely hemispheric posttraumatic lesions.
an
Moreover, our electrophysiological findings, apart from ruling out peripheral facial nerve abnormalities, show that the left mentalis muscle identically performs to the left orbicularis oculi. It can be indeed activated a) through a reflex oligosynaptic pathway following the ipsilateral
M
supraorbital nerve stimulation, b) through a reflex polysynaptic pathway after contralateral supraorbital nerve stimulation, c) during spontaneous eyeblink. The consistency and the latencies of
d
the reflex responses from the mentalis muscle support the view that an identical brainstem pathway
muscle.
Ac ce pt e
is responsible for the synchronous reflex activation of the left orbicularis oculi and mentalis
The most likely explanation, in our opinion, of the behavior of the left mentalis muscle could be found in a partial lesion of contralateral cortico-nuclear inhibitory connections to the facial nucleus, responsible to free from a tonic supranuclear inhibition some parts of the left facial nucleus. This hypothesis is reminiscent of the abnormal post-stroke coactivation in paretic limb muscles following lesions of cortico-spinal pathways, where the muscle synergies rely on the decreased selective control of each individual muscle [5]. Finally, as an alternative explanation of the clinical and electrophysiological behavior of the left mentalis muscle, a reorganization of brainstem circuits could be also hypothesized. According to this, a post-traumatic damage at the pons or medulla has to be postulated, although neither clinical nor imaging data were indicative of brainstem lesions.
References [1] Moran CJ, Neely JC. Patterns of Facial Nerve Synkinesis. The Laryngoscope 1996;106:1491–6.
Page 4 of 7
[2] Tan NC, Chan LL, Tan EK. Hemifacial spasm and involuntary facial movements. QJM 2002;95:493-500. [3] Kimura J, Rodnitzky RL, Okawara S. Electrophysiological analysis of aberrant regeneration after facial nerve paralysis. Neurology 1975;25:989-93. [4] Auger RG. Hemifacial spasm: clinical and electrophysiological observations. Neurology 1979;29:1261-72.
ip t
[5] Ohn SH, Yoo W-K, Kim DY, Ahn S, Jung B, Choi I et al. Measurement of synergy and spasticity during functional movement of the post-stroke hemiplegic upper limb. J
cr
Electromyogr Kinesiol 2013 Apr;23:501-7.
us
Fig. 1.
Blink reflex evoked by stimulation of the supraorbital nerve on the left side
an
Trace n.1: recording of the left orbicolaris oculi, showing a normal R1 and R2 response; Trace n.2: recording of the right orbicolaris oculi, showing a normal R2 response; Trace n. 3: recording of the
oculi;
M
left mentalis muscle, showing a R1 and R2 components with the same latency of the left orbicularis
Ac ce pt e
d
Trace n.4: recording of the right mentalis muscle, showing no response.
Page 5 of 7
ip t cr us an M d Ac ce pt e
Fig. 2.
MRI images
MRI scan shows sequelae of diffuse axonal injury, and contusive lesions in frontal lobes and temporal poles. A: T1W/SE Sag; B: FLAIR Ax; C: FLAIR Ax.
Page 6 of 7
Page 7 of 7
d
Ac ce pt e us
an
M
cr
ip t
