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26 avril 2015
Mult Scler Relat Disord
2014;3(4):527-32
Pathologic yawning
in neuromyelitis optica spectrum disorders
 
Lana-Peixoto MA, Callegaro D, Talim N,
Talim LE, Pereira SA, Campos GB
 
Brazilian Committee for Treatment and Research in Multiple Sclerosis

Chat-logomini

Introduction
 
Neuromyelitis optica (NMO) is an immune-mediated inflammatory disease of the central nervous System (CNS), which predominantly affects the optic nerve and spinal cord. Since the discovery of NMO-lgG as a highly specific marker of the disease (Lennon et al., 2004), a wide variety of brainstem, hypothalamic, cortical and subcortical symptoms have been added to the classical association of optic neuritis (ON) and transverse myelitis (TM) (Jarius et al., 2012; Poppe et al., 2005; Magana et al., 2009). In over 60% of NMO patients, brain MRI may detect lesions, which are often localized at sites of high AQP4 expression (Pittock et al., 2006a, 2006b).
 
The term neuromyelitis optica spectrum disorders (NMOSD) (Wingerchuk et al., 2007) includes definite NMO (Wingerchuk et al., 2006) and limited forms of the disease such as recurrent ON, bilateral and simultaneous ON, and longitudinally extensive transverse myelitis (LETM) in AQP4-lgG-seropositive patients.
 
Patients with NMOSD who complained of excessive yawning spells initially drew our attention to this symptom. The spells were distressing and embarrassing, and even drew attention from the patients' family and caregivers. Most frequently, the yawns occurred in association with nausea and vomiting, hiccups and other brainstem or hypothalamic symptoms.
 
Some patients also reported recurring spells of excessive yawning preceding TM or ON for months or years. Because yawning is a primitive complex involuntary paroxysmal phenomenon involved in brainstem and hypothalamic mechanisms of brain thermorégulation and homeostasis (Walusinski, 2006; Gallup and Gallup, 2008), we postulated that excessive yawning in NMOSD may reflect sleep and thermoregulatory dysfunction due to brainstem or hypothalamic involvement. Pathologie yawning has also been reported in multiple sclerosis (Postert et al., 1996) and a variety of conditions as well as an adverse effect of drugs (Walusinski., 2009). However, it had not been previously described in NMOSD patients.
 
Clinical findings
 
Nine AQP4-lgG-seropositive patients expen'enced excessive yawning that were not related to periods of fatigue or sleep debt (Table 1). AU patients were women aged 19-57 years (médian: 39 years) at disease onset. Seven patients had ON and TM, whereas two patients demonstrated LETM as a limited fomn of NMO. Excessive yawning occurred at disease présentation in five patients, preceded ON or TM in three patients, and followed the présentation in four patients. In one patent (Case 6) abnormal yawning occurred 15 years after the first attack of optic neuritis and transverse myelitis which followed a severe and unexplained épisode of vertigo and nystagmus for four years. Eight patients exhibited incoercible nausea and vomiting, and seven patients had hiccups in association with abnormal yawning. Although pathological yawning appeared during the acute phase of disease in six patients it persisted during remission in three patients. Yawning occurred in clusters of three to 10 yawns, which tended to repeat at a frequency of five to over 20 times a day, continuously lasting for two to 16 weeks. Two patients were still experiencing intermittent abnormal yawning at their last visit, which was four and 12 years after their onset, respectively. Brainstem symptoms other than nausea, vomiting and hiccups, were observed in six patients whereas hypothalamic symptoms were observed in five. Five out of six patients who received high-dosage IV methylprednisolone for ON/TM attacks observed a relief of the accompanied pathologie yawning.
 
MRI findings
Eight patients had brain MRI within 1 month whereas one patient had it at 32 months following the onset of excessive yawning. In ail patients, the brain MRI was abnormal and atypical forMS. An abnormal hyperintense signal was found in the optic nerve in eight patients, in the brainstem in eight patients and in the hypothalamus in five patients. Figure 1 shows représentative MRI lésions in two NMO patients with excessive yawning. Three patients had lésions in the periven-tricular région; two patients demonstrated lésions in the corpus callosum, and one patient had a large anterior hemi-spheric lésion. Unspecific small patches or dots in the deep white matter or subcortical régions were found in four patients. In ail patients spinal MRI showed hyperintense signal in the central part of the cord contiguously involving three or more vertébral segments (Table 2).
 
Discussion
The présent observation suggests that pathological yawning should be added to the wide variety of clinical manifestations of NMOSD. Yawning is a phylogenetically old reflexive phenomenon involving the activity of motor nuclei of the cranial nerves V, VII, IX, X, XI and XII, brainstem reticular formation, hypothalamic paraventricular nucleus (PVN) and connections to the frontal lobe and cervical spinal cord (Walusinski, 2009). The PVN also plays a rôle in the control of osmolarity, blood pressure, heart rate and sexuality (Walusinski, 2009).
 
Although the ultimate function of yawning is still a matter of dispute, a number of results suggest that it may serve multiple purposes. Yawning may hâve a social and commu-nicative function and may be related to complex psychological mechanisms involved in imitation and boredom (Guggisberg et al., 2011). In addition, it may also be involved in intero-ceptiveness via its capacity to increase arousal and self-awareness. The hypothalamus, thalamus, locus coeruleus, brainstem reticular formation, and insula are CNS structures that are predominantly involved in yawning, which are also related to the représentation and régulation of homeostasis (Walusinski, 2007). Moreover, a better understanding of the physiological sympathetic hypothalamic activity that accom-panies yawning, such as sharp increases in lung volume, blood pressure and heart rate as well as an increase in facial température and decrease in respiratory rate, suggests that yawning may play a rôle in brain cooling mechanisms. An represent key factors in determining the température of the brain (Corey et al., 2012).
Symptoms of hypothalamic dysfunction such as sleep disturbance, anorexia, disordered thermorégulation, hypotension and behavioral disorders may be found in NMO patients (Poppe et al., 2005). Similarly, 26% of NMO patients hâve clinical or radiological évidence of brainstem involvement (Jarius et al., 2012). Interestingly, MRI may show abnormal signais in the hypothalamus and brainstem even in patients with no symptoms related to damage of thèse structures. Large lésions involving the anterior subcortical and deep white matter, as observed in Case 3, have been attributed to excessive yawning in patients with an anterior circulation stroke (Singer et al., 2007).
 
As pathologie yawning may also occur in MS (Postent et al., 1996) spinal and brain MRI may help to differentiate between thèse conditions. A LETM centrally-located lésion is the most spécifie imaging feature of NMOSD and is very rare in MS (Wingerchuk et al., 1999). "NMO-typical" brain MRI lésions that are considered exceptional for MS, such as those in dorsal medulla oblongata (area postrema), periaqueductal and perie-pendymal régions of the third or fourth ventricles, as well as diencephalic and large tumefactive hemispheric lésions are found in 7% of NMO patients (Pittock et al., 2006a). On the other hand, 16% of NMOSD patients fulfill Barkof MS MRI criteria (Huh et al., 2013). Brain MRI lésions in temporal lobe and periventricular région, similar to those found in Case 3, are frequently observed in MS. However, Case 3 presented MRI abnormalities that are highly suggestive of NMOSD such as LETM lésion on spinal MRI, and brain lésions in the dorsal aspect of the medulla oblongata (area postrema) and periaqueductal région (Wingerchuk et al., 1999; Pittock et al., 2006a, 2006b; Huh et al., 2013). Thèse findings in association with AQP4-seropositive status fulfill NMO diagnostic criteria (Wingerchuk et al., 2006).
 
Four of our patients reported hypersomnia which occurred in association with pathological yawning at disease présentation in three of them. In thèse patients excessive yawning could be attributed to hypersomnia. However, abnormal yawning spells were observed on subséquent occasions not related to periods of hypersomnia.
 
Some of our patients with associated nausea and vomiting could hâve used anti-emetic drugs. It is unlikely, however, that pathological yawning in our séries could be related to increased sleepiness as a side effect of thèse médications as nausea and vomiting lasted only for a few days whereas pathological yawning most frequently lasted for two to three months.
 
Conclusion
The present series supports the hypothesis that pathological yawning may not be a rare symptom in NMOSD. However, because yawning is a physiological phenomenon, patients may not associate its increased frequency to illness and, consequently, do not report thèse symptoms to their doctors unless they are markedly disturbed and distressed. However, our case séries is too small to provide a définitive answer of defining the frequency and significance of excessive yawning in NMOSD. We hâve not performed an active search of pathologie yawning in our entire population of NMOSD patients to assess its frequency and meaning. This present séries just comprise patients in whom pathologic yawning was psontaneously reported by themselves or their relatives. an active survey of tthe symptom in a lager cohort of NMOSD patients may clarify the issue.