Introduction

The Tullio phenomenon is a symptom or physical exam finding, whereas nystagmus or vertigo are induced in response to sound. Professor Pietro Tullio in Bologna, Italy, described this in animals nearly 90 years ago. In humans, the phenomenon was first observed in patients suffering from advanced syphilis. Since then, numerous reports and studies have shown that the Tullio phenomenon can be seen in various pathologies, including patients with no pathology.[1] Today, however, the Tullio phenomenon is most commonly associated with superior semicircular canal dehiscence.[2]

Function

Professor Tullio was the director of the Laboratory of Experimental Physiology in Bologna during the early twentieth century. He was inspired by the work of Frenchman Jean Flourens, who had discovered that pigeons would make sudden and impetuous movements in the same plane as an injured semicircular canal.[1] Tullio performed a majority of his experiments on live pigeons. Pigeons were well known in testing labyrinthine physiology because of their favorable anatomy and prominent head nystagmus, allowing for easy observations of responses.[3]

Tullio’s first experiments were made observing the movements of water on tuning forks, followed by particle currents in vibrating water. He then began introducing particles into the endolymph and perilymph of pigeons and observed the current movement in response to sounds. These currents were seen to wave rhythmically against the ampulla, generating a movement in the pigeon's head in the plane of the canal. As Tullio increased the sound's intensity, the current would begin to oscillate, and the head of the animal would demonstrate nystagmus at a frequency corresponding to the oscillation of the current. Sounds stimulating the ear affected all 3 canals simultaneously; however, the difference in the intensity of the currents distributed through these canals generated head movement. When opening a semicircular canal, its current dominates the other 2 canals, leading to observable movement of the open canal.

Tullio later analyzed pigeons' head movements after opening each canal by attaching a lever to the beak to create a graphic of the reflexes in response to the sound stimuli. He found that the pigeons would move their heads in the same plane as the opened canal. Tullio would then apply cocaine to the osseous openings, which would paralyze the nerve endings, and the pigeon would not move to further stimulation. After opening all 3 canals, the heads would remain motionless from the fenestrations neutralizing each other. Tullio could produce head rotation around an anterior-posterior axis, with the head-turning toward the unaffected ear. This is due to utricle excitation, which persisted after the ampullae of all 3 canals had been paralyzed. In later experiments, Tullio recreated the lesions induced by Flourens and concluded that irritative stretching of ampullae nerves causes labyrinth ataxia. This is now known as Flourens syndrome.[1]

After 20 years of research, Tullio presented his findings in the work Some Experiments and Considerations on Experimental Otology and Phonetics in 1929. His work was nominated for the Nobel Prize in Physiology or Medicine in 1932.[1]

Several investigators have reported the phenomenon occurring in other conditions after Tullio’s work and its implications with labyrinthine fistula. Initially, the presence of the Tullio phenomenon in humans was considered to be an indication of congenital syphilis where patients developed osteomyelitis of the labyrinth, with miliary gumma in the endosteum capable of creating labyrinthine fistulas, and was considered to be an indication of congenital syphilis.[1] The presence of this fistula was thought to cause the Tullio phenomenon. Cawthorne suggested that the Tullio phenomenon only occurred in humans when more than 1 mobile window opened into the internal ear on the vestibular side of the vestibular membrane.[4] However, several studies over the past 60 years have indicated the presence of the Tullio phenomenon in a wide range of situations.

Kacker and Hinchcliffe reported a positive Tullio sign in 2 patients with Meniere syndrome with negative fistula tests and 1 patient with a history of trauma where the stapes were found to have subsumed into the vestibule. In all 3 cases, serologic testing for syphilis was negative.[5] Kwee investigated the incidence of the Tullio phenomenon in a group of 150 deaf children and found that 50 demonstrated a positive Tullio phenomenon in 1 or both ears, representing 76 of the 300 ears. He reported that, in all cases, the direction of the nystagmus was toward the stimulated ear. In some cases, there were accompanying side effects such as deviation of the head away from the source of the tone and subjective sensations of dizziness. As would be expected, it was also noted that there was no incidence of a Tullio phenomenon in the absence of a calorically excitable labyrinth.[6] Nadol was found in a patient with bilateral deafness after an upper respiratory infection in childhood and a positive Hennebert sign, fibrous adhesions to parts of the membranous labyrinth named vestibulofibrosis, and suggested a pathological basis for a positive fistula sign with intact tympanic membrane.[7] Later studies also found this histologic finding in several post-inflammatory or progressive inner ear disorders, including congenital syphilis, viral labyrinthitis, and Meniere disease. These findings are of note because they may be the pathophysiology behind sound-induced vestibular symptoms in patients with endolymphatic hydrops. The membranous labyrinth becomes distended enough to contact the medial aspect of the stapes footplate. All patients with Meniere disease had a positive Tullio in the Erlich study.[8]

The high incidence of the Tullio phenomenon in healthy subjects and patients with various cochleovestibular disorders suggests that sound-induced vestibular stimulation can be observed when properly monitored. Parker examined the physiologic response in the vestibular system to acoustic stimulation and found that either pressure changes or high-intensity sound caused a measurable displacement of the stapes paralleling changes in the perilymph pressure, as well as measurable changes in the rates of vestibular neuron firings. It demonstrated that ontologically normal patients exhibited nystagmus and other vestibular symptoms in response to intense pressure or audio-frequency stimulation. Treatment of the Tullio phenomenon is unique to each particular cause.[9]

Issues of Concern

While the Tullio phenomenon cannot be considered a diagnostic tool for a particular disease, which Tullio had hoped for, it can point towards a cochleovestibular or other otologic pathology that warrants further investigation. A detailed history and thorough physical exam can narrow the differential, but additional testing may be required, including an audiogram, tympanogram, stapedial reflexes, fistula test, videonystagmography, electrocochleography, and CT imaging.

Clinical Significance

The Tullio phenomenon is most commonly associated with superior semicircular canal dehiscence (SSCD). Table 1 lists several conditions linked with the phenomenon. Superior semicircular canal dehiscence was first described in 1998 and is a disease characterized by sound-induced vertigo and eye movements, chronic dysequilibrium, conductive hearing loss (CHL), and decreased hearing thresholds for bone-conducted sounds. Conductive hyperacusis may lead to autophony (hearing one’s voice), pulsatile tinnitus, or hearing one’s eye movements.[10] The disorder is caused by absent bone over the superior semicircular canal. When patients suffering from SSCD exhibit the Tullio phenomenon, they experience mixed vertical-torsional nystagmus in which the slow phase of nystagmus rotates up and away from the affected ear. This type of nystagmus aligns in the same plane as the superior semicircular canal affected and is pathognomonic for SSCD.[2][11] Depending on the type of stimulus, either excitation or inhibition of the superior canal may occur. Excitation is caused by ampullofugal displacement of the cupola through positive external auditory canal (EAC) pressure in tragal compression, sound, or nasal Valsalva. Inhibition is caused by ampullopetal deflection of the cupola through negative EAC pressure via jugulovenous compression or glottis Valsalva. Patients may also experience the Hennebert sign, which is eye movement induced by pressure in the external auditory canal.[12] Diagnosis of SSCD is made with CT imaging, which shows thin or dehiscence bone over the superior semicircular canal. Treatment is surgical, where the superior canal is plugged with bone chips and fascia and covered with bone cement via a middle fossa approach. The transmastoid, endoscopic, and transcranial or endaural approaches have been used recently.[13]

Table 1: Conditions linked to the Tullio phenomenon include:

• Superior semicircular canal dehiscence
• Otosclerosis
• Congenital syphilis
• Ménière’s disease
• Perilymph fistula
• Cholesteatoma with semicircular canal erosion & fenestration
• Head trauma
• Normal individuals
• Post stapedectomy
• Post tympanomastoidectomy
• Collapsed canal syndrome
• Congenital deafness
• Seronegative Lyme Borreliosis
• Middle ear osteoma [14][15][8][16][17][18]

Enhancing Healthcare Team Outcomes

While not frequently encountered in clinical practice, healthcare professionals in disciplines more apt to encounter the Tullio phenomenon should at least be familiar with the sign and report it to the treating clinician when necessary. Obviously, clinicians who perform examinations in visual, auditory, and neurological disciplines should be very familiar with this sign.