Introduction

A previously health 33-year-old man without a family history of epilepsy or sleep disorder was admitted to our epilepsy monitoring unit (EMU) for the characterization and management of his nocturnal groaning spells. At the age of 21 years, he had had two brief (i.e., < 1 min each) episodes of nocturnal whole-body tonic-clonic movements without auras or postictal features occurring in the context of extreme emotional stress and sleep deprivation. He was treated with phenytoin until age 23 years, at which point it was discontinued because he had no further recurrences. At age 24 years, he developed exclusively nocturnal episodes consisting of moaning and groaning sounds that would occasionally wake him up and be followed by a sensation of cold "chills" in the right shoulder which would then migrate across his chest. He frequently turned to the right side during these spells. These spells recurred up to 15 times per night and each lasted approximately 2-3 seconds. He had no known daytime events and the spells were not associated with loss of awareness. He tried multiple antiseizure medications (ASMs) to abate these events (phenytoin, valproic acid, levetiracetam, and lacosamide) but had to discontinue them due to undesirable adverse effects. He was finally successfully treated with carbamazepine. He had no further spells on low-dose carbamazepine monotherapy until age 30 years, when the same spells recurred nearly every night basis and became resistant to therapy despite taking lamotrigine, phenobarbital, and clobazam. At age 33 years, he was admitted to the EMU. At first, there were no abnormal electrographic activities or clinical events in his continuous video-electroencephalograms (VEEGs) for several days, and given the semiology of his spells, the diagnosis of catathrenia was raised by the consultant sleep medicine specialist (GFPG).

Results of investigations

His brain magnetic resonance imaging (MRI) was normal. Sleep study revealed mild to moderately severe sleep-disordered breathing but it did not capture the spells (Fig. 1).

Figure 1 Sample polysomnogram from patient. Patient did not produce catathrenia during this recording although he did demonstrate obstructive sleep patterns. 

Continuous VEEGs using scalp electrodes showed normal background activity in wakefulness and normal sleep potentials. Eventually, frequent interictal epileptic discharges (IEDs, a.k.a. epileptic spikes) from the right temporal-central-frontal region were captured on EEG during sleep (Fig. 2).

Figure 2 EEG recording shows the right temporal-central-frontal spikes. 1A bipolar montage; 1B ipsilateral ear montage. Settings: LFF = 1 Hz, HFF = 75 Hz, Notch Filter Off, Sensitivity = 10 µv/mm. 

Several typical nocturnal spells were captured that were consistent with right hemispheric seizures with predominant involvement of the right frontotemporal regions. Significant muscle and movement artifacts during them distorted the EEG signals that prevented so a very precise localization. On a subsequent admission, intracranial EEG electrodes using stereoencephalography (SEEG) revealed the seizure onset zone within the right frontal opercular region with rapid spread to the right insular region during his typical nocturnal spells (Fig. 3).

Figure 3 Intracranial electrode recording (left) shows a seizure focus within the right frontal opercular area (see MRI correlate on the right). Note seizure onset at electrodes 163, 164, and 165. Settings: LFF = 1 Hz, HFF = 75 Hz, Notch Filter Off, Sensitivity = 10 µv/mm. 

His neuropsychological assessment revealed frontal dysfunction. He is currently waiting for resective surgery of the seizure onset zone in the right frontal opercular region.

Discussion

Catathrenia was first described De Roek et al. in 1983 as the production of nocturnal groaning during episodes of prolonged expiration¹. Catathrenia is classified as a "sleep-related breathing disorder" by the international classification of sleep disorders diagnostic and coding manual and consists of repeated groaning during exhalation, mainly in rapid eye movement (REM) sleep². The groaning quality of catathrenia is described as "morose" or containing "sexual connotations" which can cause social problems for many patients³,⁴. Typically, the patients do not have any subjective complaints of sleep disturbances or excessive daytime sleepiness (Fig. 4). The referral to a sleep clinic is generally made by family or bed partners. Some case series have described frequent epochs during non-REM sleep³,⁵,⁶ but most describe a predominance during REM sleep, especially during awakening from REM sleep⁴,⁷-¹⁴. Groaning is not typically associated with significant oxygen desaturation, although concurrent obstructive sleep apnea has been reported⁶,⁸-¹⁰ (Table 1)³-⁶,⁸-¹⁸.

Figure 4 A: illustrative sequence of the anatomical structures involved in Catathrenia (top) and its treatment (bottom). B: nocturnal seizures of the frontal opercular origin with spread to the insula (top) and its treatment (bottom). 

The differential diagnosis for catathrenia includes sleep talking (somniloquy), stridor, laryngospasm, snoring, and, notably, nocturnal epilepsy-related vocalization²,⁵,¹¹. It is crucial to distinguish the latter from catathrenia as their treatments differ markedly. There is indeed some evidence supporting the use of continuous positive airway pressure (CPAP) in patients with catathrenia⁵-⁸,¹⁰,¹²-¹⁴,¹⁹. There is a paucity of the literature that focuses on the topic of distinguishing between these two disorders (Table 2).¹¹ Zinke et al.¹¹ described a 22-year-old male who developed catathrenia 10 years after being diagnosed and successfully treated with ASMs for daytime seizures secondary to generalized epilepsy. He had no improvements in his nocturnal spells from catathrenia despite multiple adjustments to his ASMs until he was treated effectively for his coexisting presumed catathrenia. Neutel et al.¹³ describe the case of a 32-year-old man with somatosensory seizures due to perisylvian polymicrogyria successfully controlled with valproic acid who later developed catathrenia. His nocturnal groaning spells responded to treatment with CPAP. Neither of the above-mentioned reported epilepsy cases had intracranial EEG recording. To the best of our knowledge, this is the first case report of frontal opercular epilepsy masquerading as catathrenia as confirmed by SEEG recordings.

Ictal screaming or crying is more commonly associated with generalized seizures²⁰. The seizure semiology of our case closely mimicked the breathing patterns seen in catathrenia. The opercular onset is in keeping with early vocalization while the subsequent somatosensory semiology across the chest is compatible with spread to the insula seen in his SEEG²¹-²³. This patient could have been misdiagnosed as catathrenia due to his presenting nocturnal grunting and given the inherent challenges of capturing frontal opercular and insular seizures on scalp EEG. However, our continuous VEEG in the EMU did eventually demonstrate that these events were epileptic in origin and SEEG confirmed the localization so that he could be treated accordingly. This case highlights the importance of longer VEEG monitoring and possible SEEG in patients in whom there is a higher clinical suspicion of epileptic seizures as the cause of their nocturnal vocalizations.

Conclusion

Catathrenia and frontal opercular epilepsy may share overlapping symptoms such as nocturnal screaming, grunting, or moaning during deep expirations. Catathrenia is a respiratory disorder that does not respond to ASMs. Seizures of the frontal opercular origin can be difficult to detect with scalp EEGs. Intracranial EEGs (especially SEEGs) are required to identify frontal opercular seizures and their patterns of spread to the adjacent brain areas including insula. VEEG telemetry to exclude epileptic seizures is necessary before diagnosing a patient with catathrenia because treatments of the two conditions are vastly different. Close collaborations between sleep medicine specialists and epileptologists are needed to work up such potentially overlapping cases.