Dysphagia, dysphonia and a deviated tongue: diagnosing Collet-Sicard syndrome

Abstract

A healthy middle-aged man presents with symptoms of dysphagia and dysphonia following an upper respiratory infection, and is diagnosed and treated for complications of pharyngitis. He presents for evaluation at a tertiary care hospital after symptoms fail to resolve, with the final diagnosis being a carotid artery dissection with compressing pseudoaneurysm. This patient’s constellation of symptoms and physical examination findings are consistent with Collet-Sicard syndrome, a rare disorder caused by cranial nerve compression at the skull base. Understanding the morbidity of missing, or delaying, a diagnosis of carotid artery pathology, such as Collet-Sicard syndrome, underscores the importance of an accurate diagnosis. A review of cranial nerve anatomy, surrounding structures and potential mechanism of injury to the carotid artery are emphasised as key learning points.

Background

Spontaneous carotid artery dissection leading to formation of pseudoaneurysm is estimated to occur in less than 3 of 100 000 cases.¹ There is evidence to suggest a temporal association with neck position and trauma to the cervical region, as well as upper respiratory illnesses with prolonged coughing. Due to the potential for vague or generic descriptor of symptoms in patients with this specific pathology, such as changes in voice quality, headache or even migraine-like visual aura, Collet-Sicard syndrome is often missed at the time of initial presentation. Delays in diagnosis could result in subsequent stroke or other morbidity associated with prolonged cranial nerve compression. Knowledge of the anatomy and function of the associated cranial nerves is paramount to the diagnosis of this clinical entity, as the symptoms a patient displays with this condition may be seen in a variety of competing diagnoses, most with more benign courses. Attention to detail in order to correctly interpret the neurological examination is pivotal in guiding the diagnostic workup and subsequent management.

Case presentation

A 42-year-old healthy right-handed man presented to his primary care physician with 1 week of dysphagia and change in voice quality. He noted difficulty swallowing and choking on foods during a recent winter holiday meal and described his voice as weak, coarse and strained. He also described recent symptoms of sore throat, sinus congestion and heavy non-productive coughing, but these symptoms had since resolved. He denied visual changes, such as double vision or blurry vision, paresthesias or sensory loss on the face, headache, tinnitus, dizziness, limb weakness, fevers, rashes or weight loss. His medical history was significant only for allergic rhinitis, mucocutaneous herpes simplex virus infection, and a focal cutaneous basal cell carcinoma of the back removed years prior. He was a non-smoker, never incarcerated, worked in sales at a car dealership and did not endorse any exposure to toxins or other chemicals. There was no history of trauma to the head or neck.

Initial examination by his primary care physician was concerning for right tongue swelling and bifacial weakness of the cheeks. He was sent to the hospital for further evaluation. He was found to be dehydrated secondary to poor oral intake as swallowing would result in coughing. He was mildly tachycardic, which resolved with administration of fluids, but was not febrile, hypertensive or hypoxic. He was subsequently discharged with an oral steroid course and azithromycin for a presumptive diagnosis of pharyngitis.

When his symptoms failed to resolve, he represented to his primary care physician, additionally reporting that his neck felt swollen and a ‘heaviness’ sensation on the back of his head. A referral to otolaryngology with laryngoscopy revealed right-sided vocal cord paralysis, palate deviation to the left, and tongue deviation to the right on protrusion.

On arrival to our tertiary care hospital for an expedited workup, examination was significant for lingual dysarthria, uvula deviation to the left and tongue deviation to the right with concern for left-sided tongue atrophy and fasciculations. He had mild atrophy of the right sternocleidomastoid muscle but retained full strength on head turn and shoulder shrug. The remainder of his neurological examination was normal, including facial strength, eye movements, pupil examination, reflexes, strength testing, coordination and gait. (figure 1)

Figure 1.

Neurological examination showing uvular deviation to left and right hemitongue swelling.

Investigations

Clinical investigation centred around evaluating for disease processes that would produce his physical examination findings, as well as his symptoms (see differential diagnosis). Repeat laryngoscopy by otolaryngology confirmed immobility of the right vocal cord, an adynamic right pharynx with pooling of secretions, palate deviation to the left and tongue deviation to the right. To evaluate for a focal lesion in the brain parenchyma, the patient had an MRI study with contrast which was normal, without mass, stroke or contrast enhancement. A lumbar puncture was also normal (white cell count, red cell count, protein and glucose levels). Serum studies were negative for infection, including negative Lyme serology. While considered, workup for HIV was not performed given the patient’s normal serum white blood cell count, low overall suspicion (no history of high-risk exposures or activities), as well as alternate diagnosis obtained by localisation and imaging. Testing for the novel COVID-19 was not performed as this case occurred over a year prior to the onset of the entity of severe acute respiratory syndrome associated with COVID-19.

In consideration of a possible compressive lesion leading to the patient’s symptoms, a CT scan of the soft-tissues of the neck was performed, followed by an MRI scan of the skull base. The CT scan supported the initial exam with evidence of right tongue haemiatrophy, right vocal cord paralysis, slight atrophy of the right sternocleidomastoid muscle and suggested the presence of a mass in the carotid sheath on the right side distal to the jugular foramen. The MRI clarified that the carotid sheath mass represented a right internal carotid artery dissection with pseudoaneurysm formation at the skull base. Digital subtraction angiography confirmed a saccular, irregular outpouching of the distal cervical internal carotid artery on the right with dissection and pseudoaneurysm projecting medially (figure 2).

Figure 2.

Angiogram image of right carotid artery with visualised pseudoaneurysm measuring 9×4.4 mm, projecting medially.

Differential diagnosis

The combination of a proper understanding of cranial nerve anatomy, a careful physical examination and a stepwise approach to the different disease processes that could result in this patient’s symptoms of dysphagia and dysphonia resulted in establishing the final diagnosis. Challenges to localisation involved conflicting documentation of the neurologic exam, as well as fluctuations in the examination findings during different stages of nerve compression. Most notable was the patient’s tongue (swelling of the right side noted by the primary care physician, deviation to the right noted by the otolaryngologist and atrophy with fasciculations on the left side on the initial examination in the tertiary care hospital emergency room) as well as concern for bifacial weakness of the cheeks initially, but never found on our examinations. Discerning the objective neurological examination correctly is paramount to accurate neurological localisation.

Considerations of where these findings would localise include a lesion of the medial medulla, such as from ischaemic stroke or demyelination, affecting dorsal vagal and hypoglossal nuclei and the nucleus of tractus solitarius (the latter being a bundle of sensory nerve cell bodies of the lower cranial nerves that relay to various brain regions including in autonomic functions). This could result in contralateral tongue deviation, tachycardia and voice change. Additionally, a meningeal process, from either infection or inflammation, such as neurosarcoidosis, could selectively affect multiple cranial nerves unilaterally or bilaterally. The normal MRI study of the brain and normal cerebrospinal fluid profile makes these diagnostic considerations less likely. Lyme disease can affect individual cranial nerves, with the facial nerve being the most common, however, this was less likely given his negative lyme serology. Tuberculosis can also affect isolated cranial nerves, though more typically involves ocular cranial nerves, and with lack of any risk factors or exposure, this was also lower on the differential.

Left tongue atrophy and fasciculations would localise to the left hypoglossal nerve. When taken in tandem with left uvular deviation, which localises to a right vagal nerve palsy, and concern for facial weakness, this suggests a lower motor neuron process. Differential would then include a post-viral inflammatory process or demyelination. Examples could include a bulbar acute inflammatory demyelinating polyneuropathy, where a normal cerebrospinal fluid profile can be seen initially, or a myasthenic syndrome, which is less likely for this patient given the acute onset, lack of any extraocular muscle abnormalities, intermittent diplopia or shortness of breath.

Our examination revealed right tongue deviation, which when paired with a right adynamic vocal cord, left uvular deviation and atrophy of the right sternocleidomastoid, suggests a unilateral right-sided lower cranial neuropathy process. Therefore, the correct interpretation of the affected cranial nerves would be the right hypoglossal nerve, right accessory nerve, right glossopharyngeal nerve, as well as right vagus nerve given the right vocal cord paralysis and the patient’s voice changes. A right-sided unilateral compressive lesion to the lower cranial nerves, such as from a mass, including an extracranial vascular lesion, as was discovered in this case, would result in these findings.

Treatment

The patient was started on dual antiplatelet therapy with acetylsalicylic acid and clopidogrel. After review of the angiogram by a multidisciplinary team, the decision to pursue treatment of the carotid artery was made and the pseudoaneurysm was coiled. This decision included weighing of risks and benefits to mitigate risk of stroke as well as worsening cranial nerve dysfunction due to the presence of persistent mass effect by the pseudoaneurysm of the carotid artery (figure 3).

Figure 3.

Angiogram images showing coiling of the pseudoaneurysm.

He was also treated with injection augmentation of the right true vocal cord for symptomatic improvement in voice quality and learnt head-turn technique to direct a food bolus appropriately and with low aspiration risk due to his asymmetric pharyngeal weakness.

Outcome and follow-up

One month later, the patient reported an improved ability to swallow and full facial strength.

Two months after discharge, his examination was notable for a stronger voice quality, with normal tongue protrusion and midline palate. Three months postprocedure, he was no longer using the compensatory swallowing approach as his dysphagia had completely resolved.

Discussion

The constellation of unilateral cranial nerve palsies of the glossopharyngeal nerve, vagus nerve, spinal accessory nerve and hypoglossal nerve is consistent with a diagnosis of Collet-Sicard syndrome.

Collet-Sicard syndrome is rare, with less than 100 cases reported since first described in 1915 by otolaryngologist and pathologist Frederic Collet after assessing injuries sustained by a soldier in World War I.¹ This was later further characterised by neurologist and radiologist Jean Sicard, hence the name of the syndrome.² It can be caused by a range of conditions including vascular lesions such as of the carotid artery or the jugular vein, inflammatory, malignant, and traumatic, with the three most frequently cited causes being invasive metastatic disease, basilar skull fracture, and carotid artery dissection.^{2 3} A summary of the known cases with etiologies of Collet-Sicard syndrome reported in the literature since 1915 has been included for reference, adapted from an excellent overview by Gutiérrez Ríos et al and updated to reflect cases since 2013² (table 1).

Table 1.

Summary table of cases and suggested aetiologies of Collet-Sicard syndrome

Aetiology	No of case reports 1915–2012	Details	Updated no of case reports including 2013–2020
Tumour/oncologic	20		30
Metastatic	12	Prostate (6), breast (2), colon, cervix, other	15
Primary intracranial	3	Glomus jugulare tumour (2) hypoglossal nerve schwannoma (1)	6
Extracranial	5	Plasmacytoma (2), fibrosarcoma, other	9
Vascular: thrombosis/dissection	13		19
Jugular vein	4		5
Carotid artery pathology	9	Dissection (6), aneurysm (2), dysplasia	14 (not including present case)
Trauma	10		17
Basilar skull fracture	7		9
C1 fracture (Jefferson fracture)	2		3
Other/trauma	1		5
Iatrogenic	6	Angiography (4), cardiovascular surgery oral/maxilla-facial surgery	6
Inflammatory or Infectious	2	Polyarteritis nodosa, granulomatosis polyangiitis, osteomyelitis, otitis media/externa, viral	6
Other/congenital	0		2
Total	51		80

The incidence of spontaneous carotid artery dissection is estimated to be between 2.5 and 3 per 100 000, although it is the cause of stroke in up to 20% of patients younger than age 45.¹ Precipitating events causally related to carotid artery trauma such as hyperextension of the neck (documented to have occurred while doing yoga, painting ceilings, chiropractic manoeuvres or hairdressing), or temporally related to periods of moderate to severe coughing or vomiting.¹ The mechanism of pseudoaneurysm formation is thought to be due to mechanical injury from stretch of the vessel wall, as well as Valsalva.

Associated morbidity of spontaneous carotid artery dissection is difficult to fully characterise given that many cases may be asymptomatic. Some studies estimate that up to 70% of carotid artery dissections lead to stroke, through suspected thromboembolic mechanism, with stroke risk peaking in the first 2 weeks after dissection.¹

Mechanistically, the artery dissection can lead to cranial nerve dysfunction from mass effect exerted by either the artery itself, or from a pseudoaneurysm, in this case projecting medially from the vessel and affecting the lower cranial nerves running medially to the carotid artery.

Other literature supports spontaneous carotid artery dissection occurring after prolonged periods of coughing, interestingly the majority being in healthy, middle-aged men, as was the case in our patient.^4–6 Symptoms included headache and migraine-like scintillating scotomas, neck and facial pain, Horner’s syndrome, as well as possible tongue pathology, reported as hemitongue swelling on the affected side.⁷ This transient oedema was mechanistically thought to be due to fluid shifts that occur initially in denervation of the hypoglossal nerve.⁵ This was the likely phenomenon attributing to the fluctuations in the patient’s physical examination over his course of presentation, with right-sided tongue swelling being initially noted by his primary care physician and his last exam prior to diagnosis notable for right tongue deviation, and interpretation of left tongue atrophy with fasciculations when compared with the right hemitongue swelling.

Given the rarity of cases of Collet-Sicard syndrome producing cranial nerve dysfunction from carotid artery dissection with pseudoaneurysm formation, no clear treatment guidelines have been established for this specific clinical circumstance. Treatment was decided based on multidisciplinary discussion within the context of preserving the patient’s cranial nerve function and preventing worse outcomes, including stroke and worsening dysphagia potentially requiring enteral support. Given these risks, it was decided to pursue endovascular coiling of the pseudoaneurysm to prevent increasing size and worsening mass effect. This patient continued to remain stable after treatment and improved symptomatically to full recovery in the following 3 months.

Patient’s perspective.

‘The whole thing was a great process, after I was diagnosed so quickly in the hospital ED after going to all the clinic visits and the other hospital, and no one really knowing what was going on. It was very informative learning about the aneurysm in the blood vessel and how it was causing my symptoms, as well as the treatment they offered me. My wife and I are very appreciative we were able to find this out through the expertise of the teams, the doctors in the ED, and the in-patient experience.’

Learning points.

• Accurate interpretation of the neurological examination is pivotal to discerning lesion localisation and the subsequent diagnostic approach, which can decrease delays in diagnosis and treatment.

• Anatomic courses of cranial nerves and their associated functions must be considered in the context of a patient’s symptoms and can aid in forming a differential diagnosis.

• Compression through mass effect by adjacent vascular pathology can be a rare source of acute disruption of multiple lower cranial nerves, such as in Collet-Sicard syndrome.