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Adult Chiari malformation and sleep apnoea

Article · Literature Review · August 2005with173 Reads
DOI: 10.1007/s10143-005-0400-y · Source: PubMed
Abstract
Chiari malformation (CM) is primarily characterised by herniation of the cerebellar tonsils through the foramen magnum. Clinically, two main types of CM represent the vast majority of cases: type I (in adults) and type II (in infants). CM may result in neuronal impairment of the brainstem, upper spinal cord and cranial nerves. Part of the afferent and efferet systems and the central respiratory controlling system are located in the cranium-cervical transition and may be damaged in these pathologies, leading to respiratory disorders, such as respiratory failure and death. The ventilatory responses to exogenous and endogenous stimuli, such as responses to hypoxia and hypercapnia, are usually diminished, and apnea may be manifested and detected during sleep, allowing for the diagnosis. This study is a review of the relationship between sleep apnoea and adult CM.
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Neurosurg Rev (2005) 28: 169?176
DOI 10.1007/s10143-005-0400-y
REVIEW
Ricardo Vieira Botelho
.
Lia Rita Azeredo Bittencourt
.
Jos? Marcus Rotta
.
S?rgio Tufik
Adult Chiari malformation and sleep apnoea
Received: 9 July 2004 / Revised: 1 September 2004 / Accepted: 25 October 2004 / Published online: 21 May 2005
# Springer-Verlag 2005
Abstract Chiari malformation (CM) is primarily charac-
terised by herniation of the cerebellar tonsils through the
foramen magnum. Clinically, two main types of CM rep-
resent the vast majority of cases: type I (in adults) and type
II (in infants). CM may result in neuronal impairment of
the brainstem, upper spinal cord and cranial nerves. Part of
the afferent and efferet systems and the central respiratory
controlling system are located in the cranium-cervical tran-
sition and may be damaged in these pathologies, leading to
respiratory disorders, such as respiratory failure and death.
The ventilatory responses to exogenous and endogenous
stimuli, such as responses to hypoxia and hypercapnia, are
usually diminished, and apnea may be manifested and de-
tected during sleep, allowing for the diagnosis. This study
is a review of the relationship between sleep apnoea and
adult CM.
Keywords Chiari malformation
.
Basilar invagination
.
Syringomyelia
.
Sleep apnoea
Introduction
Chiari malformation (CM) was first described by Hans
Chiari in 1891, and is primarily characterised by herniation
of the cerebellar tonsils into the foramen magnum [10].
Clinically, two main types of CM represent the vast
majority of the cases: type I (adult type) (Fig. 1) and type II
(infant type) (Fig. 2). Both are distinct clinical and anatomo-
pathological entities. More often, the infant malformation
is associated with spinal dysraphysm and hydrocephalus.
Type I is not associated with severe neural malformation
[52].
With the advent of magnetic resonance imaging (MRI),
the identification of adult CM has become more frequent
and may occur during investigation of other pathologies
[8]. Birns [11] states that although CM had been described
early in 1891, it was not generally recognized because of the
lack of pap ers until the work of Russell and Donald in 1935.
This review is focused on adult CM.
This study is based on an electronic review (MedLine-
PubMed) of the relationship between sleep apnoea and
CM, using the terms ?adult and Chiari malformation and
sleep apnoea? , published in the English language.
Not all existing papers are described, only those neces-
sary for text comprehension.
Terminology of the Chiari malformation
There has been considerable debate regarding terminology,
since Chiari malformation and Arnold-Chiari malformation
are used as synonyms. Recently, Beijani [10] published a
historical review on the subject. In 1894, 3 years after
Chiari?s original publication, Arnold described the case of a
child with a dysraphic spine and hydrocephalus, similar to
type II cases described by Chiari. In 1907, Schwalbe and
Greding described four cases of myelomeningocele and
added the term Arnold to type II, originating the term
Arnold-Chiari malformation. Arnold described a case re-
port of a child with spina bifida, hydrocephaly and cere-
bellar alterations, whereas Chiari described and classified
the pathology in full [10].
Blumental and Riggs [14] suggest that Arnold-Chiari
malformation should be restricted to type II CM. With the
increasing identification of adult CM, even in asymptomatic
patients, it is necessary to make diagnostic criteria clearer.
A commentary on this paper is available at http://dx.doi.org/10.1007/
s10143-005-0401-x
R. V. Botelho
.
L. R. A. Bittencourt
.
S. Tufik
Departamento de Psicobiologia, Universidade Federal de S?o Paulo,
Sao Paulo, Brazil
R. V. Botelho
.
J. M. Rotta
Servi?o de Neurocirurgia do Hospital do Servidor Publico do Estado
de S?o Paulo,
Sao Paulo, Brazil
R. V. Botelho (*)
R Haberbeck Brand?o 68-122,
Indian?polis-Sao Paulo-Capital, Cep 04027040, Brazil
e-mail: bitbot@uol.com.br
Fax: +55-115-5725092
Development of radiological diagnostic criteria for adult
Chiari malformation
MRI represented such a revolution in the identification of
CM that the description of the disease is divided into pre-
and post-MRI eras [9, 10].
Pre-MRI era
Beijani suggests that Baker was the first to try to establish
criteria for the diagnosis of CM based on the descent of the
cerebellar tonsils [10]. This author studied 28 CM cases
and considered individuals to be normal when the tonsils
did not descend below the foramen magnum (FM) .
In 1937, O?Connor and co-workers [60] studied 100
myelographs obtained in several clinical situations, without
CM, to determine the positioning of cerebellar tonsils.
They were always above the basion-opistion line and con-
sidered strong evidence of CM when tonsil was located at
or bellow the foramen magnum.
In 1974, Bloch and colleagues [13] measured the ex-
tension of tonsillar herniation below the foramen magnum
in 60 healthy volunteers and 19 CM patients. The tonsils
were positioned 7 mm above to 8 mm below the foramen
magnum in normal cases, and 3 mm above to 25 mm below
the foramen magnum in CM patients. The authors con-
cluded that there could be a large herniation in symptom-
atic patients. Radiological magnification inherent to the
examination was not taken into consideration.
No criteria of computerized tomography have been de-
veloped for CM diagnosis [10].
Post-MRI era
In 1985, Aboulezz and colleagues [1] used MRI to study
the positioning of cerebellar tonsils in a healthy population
(82 subjects) and in 13 CM patients. Positioning of the
tonsils in the healthy population varied from 2.8 mm below
to 2.0 mm above the foramen magnum, whereas in CM
patients the tonsils were placed 5.2?17.7 mm below the
foramen magnum. In conclusion, normal tonsils may ex-
tend up to 3 mm below the foramen magnum, but in CM
patients they extend 5 mm or more. Barkovich and co-
workers [8] compared the MRI of 200 no-CM patients with
distinct symptoms to those of 25 type I CM patients. The
tonsils of the control group were located between 8 mm
above and 5 mm below the foramen magnum, whereas
those of CM patients were placed between 3 and 29 mm
below the foramen magnum. The authors concluded that
herniation of 2 mm below the foramen magnum should be
the limit of diagnosis because no symptomatic patient
showed less than 3 mm and only one asymptomatic patient
exhibited a 3 mm herniation.
In 1988, Ishikawa and colleagues [39] studied 50 healthy
volunteers and found that the tonsils were always above the
foramen magnum. In 1992, Elster and Chen [27] assessed
all patients who underwent cranial MRI in a tertiary center
and concluded that a 5 mm herniation of one tonsil and 3?
5 mm for both tonsils should be the limit, above which CM
should be diagnosed. However, the authors concluded that
clinical data, and not the net measurement of tonsillar
herniation, are the basis of an adequate diagnosis.
In the same year, Mikulis and colleagues [51] studied
220 patients to determine the variability of the cerebellar
tonsils positioning in relation to age (between 5 months to
Fig. 2 Type II (infant type) Chiari malformation. The black line is in
the foramen magnum (white arrow). Note the extent of tonsillar
herniation
Fig. 1 Chiari I malformation. Note the tonsillar herniation (white
arrow ). The brainstem respiratory centers are represented according
to Nogues et al. [58]
170
89 years of age). They concluded that the tonsils rise with
age and suggested the following measurements of tonsil
herniation below the foramen magnum for diagnosis:
1. First decade, 6 mm below the foramen magnum;
2. Second to 3rd decade, 5 mm;
3. Fourth to 8th decade, 4 mm;
4. Ninth decade, 3 mm below the foramen magnum.
These criteria were based on a distance higher than 2 SD
from the normal variation for each decade. In 1999,
Milhorat and colleagues [52] studied Chiari malformation
type I symptomatic patients. The authors found that 9% of
the patients presented cerebellar ectopia smaller than 5 mm,
though with compression of the posterior fossa. In 2000,
Meadows and co-workers [50] reviewed 22,591 MRI
findings in an attempt to estimate the incidence of CM.
Herniation of the tonsils greater than 5 mm below the
foramen magnum was present in 0.77% of the examina-
tions. Of these patients, 14% were asymptomatic (herni-
ation of 7?25 mm) and 25% presented variations of the
cerebellar tonsil shape, pear-shaped tonsils, which is often
found in CM. The authors concluded that isolated herni-
ation of the cerebellar tonsils is of limited usefulness for
diagnosis and should be considered within a context of
clinical and radiological data. Based on the review of these
studies, the following recommendations were made [10]:
there may be evident herniation in the imaging examination
without clinical significance. There are patients with
herniation smaller than 5 mm and with features similar to
those with CM, including syringohydromyelia. The radio-
logical criteria for tonsillar herniation must always be
related to a clinical context for diagnosis [50].
Introduction to the term ?Chiari zero?
In 1988, Iskandar and co-workers [40] reported five chil-
dren with syringomyelia without tonsillar herniation, who
underwent decompression of the posterior fossa and pre-
sented good clinical and radiological outcomes. Clinical
features were similar to those of MC patients. Patients in
whose cerebrospinal fluid (CSF) flow was assessed by
MRI presented a reduced flow. All five cases showed the
tonsils at the foramen magnum level, i.e. did not present
herniation, though there was syringomyelia. Three years
later, Tubbs and colleagues [71] added a sixth case and
analyzed several radiological measurements, proving that
even in the absence of tonsillar herniation there were
alterations of several measurements of the posterior fossa.
Such measurements were more than 2 SD lower than
normal. The term ?Chiari malformation zero? was chosen
for this pathology.
Syringomyelia
CM is often associated with hydric dilatation of the spinal
cord, known as syringomyelia, which contributes to its
clinical worsening [63].
Syringomyelia is defined as a cavity inside the spinal
cord filled with a liquid similar or identical to the CSF [9].
Pillay and colleagues [63] report a 57% incidence of syrin-
gomyelia in their sample of CM patients.
The cavity made by syringomyelia often produces
clinical features that are predominant in the clinical context
of the CM, over the originating cranium-vertebral malfor-
mation defect, which deteriorates the illness prognosis
[33].
In healthy individuals, during cardiac systoles, the cere-
bellar tonsills and the spinal cord are dislocated downwards
together with the CSF [6, 20] and return at diastole. In the
malformation of the cranium-cervical transition, CSF flow
is altered. The volumetric capacity of CSF space is reduced
as well as the amount and speed of CSF flow. This is due to
mechanical blockade conditioned by the low volumetric
capacity of the posterior fossa and the herniation of cere-
bellar tonsils toward the caudal direction, to the vertebral
canal. These disorders of the CSF circulation lead to accu-
mulation of CSF inside the spinal cord and its cavitation.
The evolvement of syringomyelia is caused by the cere-
bellar tonsils, which partially close the subarachnoid space,
at the level of the foramen magnum, and act like a piston in
a relatively inexpandable space. This leads to an increase in
the subarachnoid pressure, which compresses the spinal cord
inwards propagating the syringe liquid downwards at each
systole, leading to the progression of the syringe [6, 20].
Basilar invagination (BI)
Ackerman (cited in 25) was the first to describe basilar
invagination and to call attention to the small size of the
posterior fossa. BI is characterized by the same mesoder-
mic malformations that originate the defects of the growth
of the occipital bone in CM. Nonetheless, in CM the three
parts of occipital bone (basioccipital, exooccipital and su-
praoccipital) are malformed [48, 49, 56, 69]. The basio-
condrocanium is the more impaired, and consequently,
causes hypoplasia of the clivus. The upper cervical verte-
brae, C1 and the C2 odontoid process project toward the
cranium and compress the neuro-axis of the cranium-cer-
vical transition [49]. The volumetric capacity of the pos-
terior fossa has been demonstrated to be smaller in CM and
BI patients than in healthy subjects [49, 56].
There are two groups of BI : one without CM (group I)
and one with CM [32]. Chiari malformation and syringo-
myelia are present in 35% of BI patients [52].
Malformations of the cranium-cervical transition (MCCT)
and respiratory sleep disorders
MCCT may result in neuronal impairment of the brainstem,
upper spinal cord and cranial nerves. Part of the afferent
and efferent systems and the central respiratory controlling
system are located in the cranium-cervical transition and
may be harmed in these pathologies, leading to respiratory
disorders, especially during sleep.
171
Components of the central respiratory control system
Ventilation is constantly monitored and adjusted to main-
tain the blood pH, and adequate arterial oxygen (PaO
2
) and
carbon dioxide (PaCO
2
) partial pressure [22]. To this end,
the respiratory center uses sensors and afferent pathways of
the central control system and effector systems and
pathways. Changes in gas and acid-basic concentrations
in the blood, changes in ventilation mechanics, in meta-
bolic rate and respiratory neural receptors influence the
respiratory center to perform adaptations to physiological
conditions such as sleep, exercise, high altitude or to path-
ological conditions [22].
Sensory afferents to the central nervous system are
provided by peripheral arterial chemoceptors (present in
the aorta and carotid bodies), by central chemoceptors
(located in or near the ventral surface of the medulla) and
by the pulmonary receptors (present in the airways and
lungs). The central respiratory controllers are distributed in
two groups: one in the brainstem (involuntary) (Fig. 1) and
the other, in the cerebral cortex (voluntary). The first is
subdivided in pneumotaxic, apneustic and bulbar. Nogues
and cols.[58] subdivided the brainstem group into pontine
respiratory group and ventral and dorsal group (medulla)
(Fig. 1). The cerebral cortex plays a role in the ventilatory
control and may influence or overcome the respiratory
control to adequate to the behavioural respiratory activity,
as in coughing, speaking, singing, voluntarily maintained
inspiration, among others.
The effector system consists of efferent nervous path-
ways to the muscles involved in the inspiration and ex-
piration performances, such as thoracic, diaphragm and
other accessory respiratory muscles.
Respiratory control during sleep
At sleep onset behavioural and cognitive influences of the
ventilatory control are strongly inhibited. Ventilation and
respiratory responses to exogenous and endogenous stim-
uli, such as responses to hypoxia and hypercapnia are
usually diminished. Moreover, increased airflow resistance
takes place at sleep onset due to a relative hypotonia of the
dilator airway muscles. Ventilatory compensation to both
inspiratory resistances, in addition to the intrinsic one, is
highly reduced during REM sleep. Hypoventilation during
slow wave sleep is a consequence of both decreased current
volume and respiratory rate, resulting in a 2?7 mm increase
in the PaCO
2
and a concomitant drop in PaO
2
[26].
A pattern of periodic breathing after sleep onset often
takes place during sleep stages 1 and 2. The ventilatory
pattern is considerably more regular during stages 3 and 4.
Another change is the reduction of skeletal muscle tone
during REM sleep, except for the diaphragm and ocular
muscles. This reduction in muscle tone results from the
supra-spinal inhibition of the alpha-motor action associated
to REM sleep and to a specific depression of the neuro-
muscular spindles, inhibiting the polysynaptic spindle
reflexes. The diaphragm is somehow set aside for pre-
senting few spindles. However, during REM sleep dia-
phragm contraction becomes uncoordinated (diaphragmat-
ic fragmentation). Breathing during phasic REM sleep is
very irregular and consists of sudden changes in respiratory
amplitude and frequency, associated to rapid eye move-
ments. SaO
2
is also slightly reduced during this phase. The
diaphragm maintains ventilation during REM sleep. Any
alteration of the diaphragmatic function during this sleep
phase results in profound nocturnal hypoventilation.
Respiratory sleep disorders: definitions
In the last 30 years, numerous types of respiratory disorders
have been reported to occur during sleep. The 1999 AASM
task force [4] classified the respiratory syndromes as:
1. Obstructive sleep apnoea-hypopnoea syndrome (OSAHS).
2. Central sleep apnoea syndrome.
3. Sleep hypoventilation syndrome, previously known as
the Pickwick syndrome.
4. Cheyne?Stokes periodic respiration syndrome.
Obstructive sleep apnoea-hypopnoea syndrome (OSAHS)
OSAHS is characterized by recurrent episodes of partial or
complete obstruction of the upper airways during sleep.
This is manifested by reduction (hypopnoea) or suppression
(apnoea) of the airflow despite the presence of respiratory
effort. Lack of adequate alveolar ventilation often results in
oxyhemoglobin desaturation and in prolonged cases, in
increased PaCO
2
. The events are usually halted by arousals.
Daytime symptoms, such as excessive somnolence, are due
to arousals and possibly to recurrent hypoxaemia.
Central sleep apnoea syndrome The idiopathic central
sleep apnoea-hypopnoea syndrome is characterised by
recurrent episodes of apnoea without obstruction of the
upper airways during sleep, which typically leads to oxygen
desaturation, frequent arousals and daytime symptoms.
In general, central apnoeas during sleep must be dis-
tinguished in those patients who are hypercapnic and those
who are normocapnic or hypocapnic. Central sleep hyper-
capnic apnoea overlays to hypoventilation syndromes and
is considered as part of the sleep hypoventilation syndrome.
These may result from metabolic and neurological diseases.
This is the most frequent type of apnoea described in the
reports of respiratory failure in CM.
Central sleep hypocapnic or normocapnic apnoea may
arise from numerous forms of physiological conditions,
such as high altitude sleep apnoea, being part of the
Cheyne-Stokes Syndrome (described below) or diseases in
which there are impairments of the primary respiratory
center (idiopathic central sleep apnoea).
Sleep hypoventilation syndrome The central feature of this
syndrome is the abnormal rise in PaCO
2
during sleep that
results in severe hypoxemia. Hypoxemia leads to clinical
outcomes that include erythocytosis, pulmonary hyperten-
sion, cor pulmonale and respiratory failure.
172
Sleep hypoxaemia is commonly present during the whole
sleep recording period, with episodes of oxygen desatura-
tion that occur in addition to, but not associated with,
apnoeas and hypopnoeas. Desaturation episodes may be
long (>1 min) and are more intense (level and duration)
during REM sleep.
Cheyne-Stokes periodic respiration syndrome This syn-
drome is characterised by a clinical fluctuation of respira-
tion with periods of central apnoeas and hypopnoeas. It
occurs in patients with cardiac dysfunction or cerebrovas-
cular neurological diseases. The Cheyne-Stokes respiration
may be observed during sleep and, in most severe cases,
during wakefulness.
Abnormalities of the ventilatory response to hypoxia
and to CO
2
Abnormalities of respiratory control have been reported in
children with type II CM (associated with myelomeningo-
cele) and has not been thoroughly studied in type I CM
(adult).
Rodman and colleagues, in 1962 [65], described a series
of four cases in which there was alveolar hypoventilation
due to diseases of the central nervous system. The case four
was a 27-year-old man with cervical and thoracic syringo-
myelia, presenting episodes of apnoea. His response to
stimulation with carbon dioxide was abnormal, indicating
respiratory center abnormality.
Choi, Tran and Zalzal [24] retrospectively studied
ventilatory abnormalities in 24 patients presenting type I
and type II CM. The authors also found that patients had
paralysis of the vocal folds and central sleep apnoea,
indicating a disorder of the generation of the respiratory
stimulus only in type II, but not in type I CM patients.
Fanfulla and colleagues [29] studied the ventilatory
response of a young adult patient with type I CM and
syringomyelia, who exhibited central ventilatory failure.
The patient did not respond to hypoxia or hypercapnia. A
major reduction of the X cranial nerve function was
observed, which persisted after neurosurgery. Houzi and
co-workers [36] studied the response of a 25-year-old
patient who did not show increased, exercise-induced ven-
tilatory response, but could voluntarily augment the ven-
tilatory response, demonstrating alteration of automatic
respiratory control. No associated corticomotor dysfunc-
tion was observed.
Chiari malformation and sleep respiratory disorders
In 1941, List [47] published a series of cases of malfor-
mations of the cranial-cervical transition (MCCT) anoma-
lies, analyzing its clinical manifestations, and described
that respiratory alterations took place in later phases of the
clinical features and that the high sites of compression
caused supranuclear paralysis of the components of the
ventilatory control. There was no reference to sleep re-
spiratory disorders as we know them today.
Severe sleep respiratory disorders, such as respiratory
failure and death, have been described to be associated to
these malformations [2, 3, 15, 19, 28?31, 35, 41, 44, 56,
61, 62, 70?72, 74].
Respiratory dysfunction as the first manifestation of CM
clinical features, including nocturnal hypoventilation, was
described by Campbell in 1965 [21]. The most frequently
described respiratory dysfunction is sleep apnoea [ 7, 45,
64], despite its variable nature. Most cases were of central
apnoeas that improved with surgical decompression [45,
54, 55, 74, 75]. Nonetheless, there are descriptions of
obstructive [26] and mixed apnoeas [12, 16?18, 42?44].
Paralysis of the vocal folds (adductor and abductor mus-
cles) and the diaphragm has been diagnosed in association
to apnoea [28, 54, 66]. Montserrat and colleagues [54]
reported a case of diaphragm paralysis and raised the
hypothesis of spinal or nerve roots lesion as the cause of
alteration.
Paralysis of the vocal folds is well known in the infant
Chiari malformation with myelomeningocele [11, 38, 42,
46]. Explanations include direct lesion of the brainstem and
of the lower cranial nerves, especially the vagus nerve [11].
In the adult CM patient, vocal fold paralysis has also been
identified [11, 24, 28, 58, 68, 75].
Milhorat and colleagues [52] described a paper related to
clinical and radiographic findings for 364 symptomatic
patients with Chiari I malformation. Among these they
found 191 patients (52%) with lower cranial nerve, brain-
stem and cerebellar disturbances. The diagnose of sleep
apnea was made in 30 patients and the diagnosis confirmed
through 24-h sleep monitoring. The authors did not
describe in detail their method of 24-h sleep monitoring,
nor did they give any description of results.
There are several descriptions of improvement of re-
spiratory events after surgical decompression of the poste-
rior fossa [2, 3, 5, 16, 30, 43, 45, 56, 62, 73, 75].
Nevertheless, there are reports of onset of apnoeas after
decompressive surgery [15, 28]. One of the most feared
complications of surgery for MCCT is respiratory depres-
sion following decompressive surgery of the posterior
fossa. Paul and co-workers [62] reported that in 71 cases of
operated type I CM, collected between 1943 and 1981,
14% exhibited nocturnal respiratory depression within the
first 5 post-operative days and one patient died from sleep
apnoea. The cause of post-operative deaths following
decompression of the posterior fossa has been attributed to
apnoea, which may be due to re-herniation of the cerebellar
tonsils, in which case further decompression is recom-
mended [75].
In adults, the papers related to surgery in the treatment of
sleep apnoea in an MCCT population are case reports. We
are not aware of any controlled study dealing with the
results of surgery.
With the increasing identification of sleep apnoea and
CM, there have been many reports of patients without other
signs and symptoms or other neurological abnormalities
[19, 23, 31, 35?38, 59, 63, 65, 68, 69]. Because of that, the
173
real prevalence of these disorders, especially, sleep apnoea,
has not been systematically evaluated [75]. Our group
recently carried out two studies aiming at clearing up the
sleep respiratory dysfunction in MCCT patients.The first
one [17] was a prospective study with 11 MCCT patients,
where we found sleep respiratory dysfunction in 72% of
the cases. Most of the patients presented central sleep
apnoea. In the second study [18], 32 patients were com-
pared to a sample of healthy volunteers. MCCT patients
were distributed in three groups: type I Chiari malforma-
tion without syringomyelia, with syringomyelia and with
basilar invagination. Sleep respiratory dysfunction was
observed in 59% of the group with malformation. Sleep
apnoea syndrome was identified in 60% of the CM group,
in 44% of the CM with syringomyelia and in 88% of the
subgroup with basilar invagination. Differently from the
first study, the second verified there was a prevalence of
obstructive events in the malformation and control groups.
Patients with basilar invagination presented more severe
sleep respiratory impairments than the other subgroups, for
their apnoea-hypopnoea index (AHI) was higher, and oxy-
haemoglobin saturation concentrations were lower. Central
apnoea events were more frequent in the basilar invagina-
tion and MC syringomyelia subgroups.
Mechanism of respiratory dysfunction
The mechanism of induction of respiratory dysfunction
remains obscure. Central apnoeas involve direct compres-
sion of the central respiratory components, compression of
the IX and X pairs of cranial nerves and alterations of
afferent nerves through the syringomyelic cavities [33, 57].
Hypothetically, lesions of the motor efferents of cranial
nerves might lead to the tendency towards pharyngeal
collapse due to muscle atrophy, resulting in obstructive
apnoeas [17]. However, some biotype-related factors (ret-
rognathia and increased neck circumference, mcroglossia
in relation to small oral cavity) that are also present in these
patients [ 48, 49] may contribute to the pathophysiological
aspects of sleep apnoea and must not be forgotten.
The role of studies of sleep respiratory dysfunctions in
the MCCT with the numbness of voluntary respiration
control centers, and the sole predominance of the automatic
control, respiratory disorders in these pathologies may be
manifested and detected during sleep, allowing adequate
treatment [53].
Future research fields
With the acknowledgement of respiratory disorders in
this population, studies of the relationship between cra-
niometric factors and sleep apnoea can be expected and
encouraged and the role of the several new kinds of de-
compressive surgeries of the posterior fossa [67] on the
natural history of sleep apnoea will surely be established.
A question that remains without answer is related to the
natural history of sleep apnoea in MCCT: there is a linear
progression from frequent episodes of sleep apnea to re-
spiratory failure [34]?
References
1. Aboulezz AO, Sartor K, Geyer CA, Gado MH (1985) Position of
cerebellar tonsils in the normal population and in patients with
Chiari malformation: a quantitative approach with MR imaging.
J Comput Assist Tomogr 9:1033?1036
2. Ali MM, Russell N, Awada A, McLean D (1996) A cranio-
cervical malformation presenting as acute respiratory failure. J
Emerg Med 14:569?572
3. Alvarez D, Pequena I, Arias M, Valdez L, Pereiro I, De la Torre R
(1995) Acute respiratory failure as the first sign of Arniold-
Chiari malformation associated with Syringomyelia. Eur Respir
J 8:661?663
4. American Academy of Sleep Medicine (1999) Sleep related
breathing disorders in adults: recommendations for syndrome
definitions and measurements techniques in clinical research.
Sleep 22:667?689
5. Arcaya J, Cacho J, Del Campo F, Grande J, Maillo A (1993)
Arnold Chiari malformation associated with sleep apnea and
central dysregulation of arterial pressure. Acta Neurol Scand
88:224?261
6. Armonda RA, Citrin CM, Foley KT, Ellenbogen RG (1994)
Quantitative cinemode magnetic resonance imaging of Chiari I
malformations: an analysis of cerebral fluid dynamics. Neuro-
surgery 35:214?224
7. Balk R, Hiller C, Lucas EA, Scrima L, Wilson FJ, Wooten V
(1985) Sleep apnea and the Arnold-Chiari malformation. Am
Rev Respir Dis 132:929?930
8. Barkowich AJ, Wippold FJ, Sherman JL, Citrin MC (1986)
Significance of cerebellar tonsillar position on MRI. Am J
Neuroradiol 7:759?799
9. Batzdorf U (1984) Chiari I malformation with syringomyelia.
Evaluation of surgical terapy by magnetic resonance imaging. J
Neurosurg 68:726?730
10. Beijani GK. Adult Chiari malformation. Neurosuurgical focus.
Available in URL: http://www.org/education/journal/neurosur gical/
july01/1 1-1-nsf-toc.asp
11. Birns JW (1988) An anusual form of laryngeal paralysis
associated with Arnold-Chiari malformation. Ann Otol Rhinol
Laryngol 93:447?451
12. Bittencourt LRA, Moura SMT, Palombini LO, Botelho RV, Nery
LE (1996) S?ndrome da apn?ia do sono e dor cervical. J Pneumol
22(2):93?94
13. Bloch S, Van Rensburg MJ, Danziger J (1974) The Arnold-
Chiari malformation. Clin Radiol 25:335?341
14. Blumental DT, Riggs JE (1997) Please don?t call me Arnold-
Chiari unless you mean it. Arch Neurol 54(1):16
15. Bokinsky GE, Hudson LD, Weil JV (1973) Impaired peripheral
chemosensitivity and acute respiratory failure in Arnold-Chiari
malformation and syringomyelia. N Engl J Med 288:947?948
16. Botelho RV, Bittencourt LRA, Rotta JM, Nery LE, Tuffik S
(1998) Apneia do sono central em paciente com malforma??o de
Chiari tipo I e siringomielia: tratamento com cirurgia descom-
pressiva. Relato de caso. J Bras Neurocir 9(3):111?114
17. Botelho RV, Bittencourt LRA, Rotta JM, Tufik S (2000)
Polysomnographic respiratory findings in patients with Arnold-
Chiari type I malformation and Basilar Invagination, with or
without syringomyelia: preliminary report of a series of cases.
Neurosurg Rev 23(3):151?155
18. Botelho RV, Bittencourt LRA, Rotta JMR, Tuffik S (2003) A
prospective controlled study of sleep respiratory events in
patients with craniovertebral junction malformation. J Neuro-
surg 99:1004?1009
19. Bullock R, Todd NV, Easton J, Hadley D (1988) Isolated central
respiratory failure due3 to syringomyelia and Arnold-Chiari
malformation. BMJ 5:1451?1460
174
20. Cahan LD, Bentson JR (1982) Considerations in the diagnosis
and treatement of syringomyelia and the Chiari malformation. J
Neurosurg 57:24?31
21. Campbell EJM (1965) Respiratory failure. BMJ 1451?1460
22. Caruana-Montaldo C, Glesson K, Zwillich CW (2000) The
control of breathing in clinical practice. Chest 117:205?225
23. Chartier A, Martinot A, Dhellemmes P, Vallee L, Lamblin MD,
Goran C, Leclerc F (2002) Chiari type I malformation in
children: presentation in 34 cases. Arch Pediatr 9(8):789?796
24. Choi SS, Tran LP, Zalal LP (1999) Airway abnormalities in
patients with Arnold-Chiari malformations. Otolaryngol Head
Neck Surg 121(6):720?724
25. da Silva JAG, Holanda MMA (2003) Basilar impression, Chiari
malformation and syringomyelia. A retrospective study of 53
surgically treated patients. Arch Neuropsiquiatr 61:368?375
26. Doerty MJ, Spence DP, Young C, Calverley PM (1995) Ob-
structive sleep apnea with Arnold-Chiari malformation. Thorax
50(6):607?696
27. Elster AD, Chen MY (1992) Chiari malformations: clinical and
radiological reappraisal. Radiology 183:347?353
28. Ely EW, McCall WV, Haponik EF (1994) Multifatorial
obstructive sleep apnea in a patient with Chiari malformation.
J Neurol Sci 126(2):232?236
29. Fanfulla F, Eleotherion D, Patruno V, Bruschi C, Rampulla C
(1998) Chronic respiratory failure in a patient with type I Arnold-
Chiari malformation (ACM1) and syringomyelia. Monaldi Arch
Chest Dis 53(2):138?141
30. Fish DR, Howard RS, Wiles CM, Simon L (1988) Respiratory
arrest: a complication of cerebellar ectopia in adults. J Neurol
Neurosurg Psychiatry 51:714?716
31. Gentry JB, Gonzalez JM, Blacklook JB (2001) Respiratory
failure caused by Chiari I malformation with associated syrin-
gomyelia. Clin Neurol Neurosurg 103(1):43?45
32. Goel A, Batjiwale A, Desai K (1998) Basilar invagination: a
study of 190 treated patients. J Neurosurg 88:962?968
33. Guilleminault C, Robinson A (1999) Central sleep apnea. Neurol
Clin 14:611?628
34. Gupta R, Oh U, Spessot AL, Anderson RCE, Kaiser MG,
Fitzsimmons BFM (2003) Resolution of Ondine?s curse after
subocciptal decompression in a 72-year-old woman. Neurology
61(2):275?276
35. Halpin DM, Trend P, Symon L, Harding AE (1990) Type 1
Arnold-Chiari malformation in a 77 year old woman. J Neurol
Neurosurg Psychiatry 53(1):88?89
36. Haouzi P, Marchal J, Allioui EM, Hannahart B, Chalon B, Braun
M (2000) Corticospinal pathway and exercise hyperpnea.
Lessons from a patient with Arnold-Chiari malformation. Respir
Physiol 123(1?2):13?22
37. Hershberger ML, Chidekel A (2003) Arnold-Chiari malforma-
tion type I and sleep-disordered breathing: an uncommon
manifestation of an important pediatric problem. J Pediatr
Health Care 17(4):190?197
38. Hollinger PC, Holinger LD, Reichart TJ, Holliger PH (1978)
Respiratory obstruction and apnea in infants with bilateral
abductor vocal cord paralysis, meningocele, hydrocephalus and
Arnold-Chiari malformation. J Pediatr 92:368?373
39. Ishikawa M, Kikuchi H, Fujisawa I, Yonekawa Y (1988)
Tonsillar herniation on magnetic resonance imaging. Neurosur-
gery 22:77
?81
40. Iskandar BJ, Hedlund GL, Grabb PA, Oakes WJ (1998) The
resolution of syringohydromyelia without hindbrain herniation
after posterior fossa decompression. J Neurosurg 89:212?216
41. Juan G, Ramon M, Ciscar MA, Garcia B, Lioret T, Cervello MA,
Marin J (1999) Acute respiratory insufficiency as initial
manifestation of brain stem lesions. Arch Bronchopneumol 35
(11):560?563
42. Kirsch WM, Duncan BR, Black FO, Stears JC (1968) Laryngeal
palsy in association with myelomeningocele, hydrocephalus and
the Arnold-Chiari malformation. J Neurosurg 28(3):207?214
43. Lam B, Ryan CF (2000) Arnold-Chiari malformation presenting
as sleep apnea syndrome. Sleep Med 1(2):139?144
44. Lee JH, Chung CK, Kim HJ (2001) Cerebral dissection from
syringomyelia demonstrated using cine magnetic resonance
imaging. Case report. J Neurosurg 94(2):318?321
45. Levitt P, Cohn MA (1988) Sleep apnea and the Arnold-Chiari
malformation: case report. Neurosurgery 23(4):508?510
46. Linder A, Lindholm CE (1997) Laryngologic management of
infants with the Chiari II syndrome. Int J Pediatr Otorhinolar-
yngol 39(3):187?197
47. List CF (1941) Neurologic syndromes accompanying develop-
mental anomalies of occiptal bone, atlas and axis. Arch Neurol
45:577?616
48. Marin-Padilla M, Marin-Padilla TM (1981) Morphogenesis of
experimentally induced Arnold-Chiari malformation. J Neurol
Sci 50(1):29?55
49. Marin-Padilla M (1991) Cephalic axial skeletal-neural dysraphic
disorders: embryology and pathology. Can J Neurol Sci 18:153?
169
50. Meadows J, Kraut M, Guarnieri M, Haroun RI, Carson BS
(2000) Asymptomatic Chiari type I malformation identified on
magnetic resonance imaging. J Neurosurg 92:920?926
51. Mikulis DJ, Diaz O, Egglin TK, Sanchez R (1992) Variance of
the position of the cerebellar tonsils with age: preliminary report.
Radiology 183:725?728
52. Milhorat TH, Chow MW, Trinidad E, Kula RW, Mandell M,
Wolpert C, Speer MC (1999) Chiari I malformation redefined:
clinical and radiographic findings for 364 symptomatic patients.
Neurosurgery 44(5):1005?1017
53. Miyamoto M, Miyamoto T, Hirata K, Katayama S (1998) A case
of Arnold-Chiari type I malformation presenting with dysrhyth-
mic breathing during sleep. Psychiatr Clin Neurosci 52:212?216
54. Montserrat JM, Picado C, Agusti-Vidal A (1988) Arnold-Chiari
malformation and paralysis of the diaphragm. Respiration
53:128?131
55. Moro ERP, Teive HAG, de Souza SMP, Lambrecht F, Werneck
LC (1999) Malforma??o de Chiari tipo I. Relato de dois casos
com apresenta??es cl?nicas pouco usuais. Arq Neuro-psiquiatr
57(3-A):666?671
56. Nishikawa M, Sakamoto H, Hakuba A, Nakanishi N, Inoue Y
(1997) Pathogenesis of Chiari malformation: a morphometric
study of the posterior cranial fossa. J Neurosurg 86(1):40?47
57. Nogu?s MA, Gen? R, Encabo H (1992) Risk of sudden death
during sleep in syringomyelia and syringobulbia. J Neurol
Neurosurg Psychiatry 55:585?589
58. Nogues MA, Roncoroni AJ, Benarroch E (2002) Breathing
control in neurological diseases. Clin Auton Res 12:440?449
59. Noseda A, Devriendt J, Hoffmann G, Schmerber J (1996)
Insuffisance respiratoire isolee sur malformatio d?Arnold-Chiari.
Ver Mal Respir 13:440
?442
60. O?Connor S, du Boulay G, Logue V (1973) The normal position
of the cerebellar tonsils as demonstrated by myelography. J
Neurosurg 39(3):387?389
61. Omer S, al-Kawi MZ, Bohlega SS, Bouchama A, Mclean D
(1996) Respiratory arrest: a complication of Arnold-Chiari
malformation in adults. Eur Neurol 36:36?38
62. Paul KS, Lye RH, Strang FA, Dutton J (1983) Arnold-Chiari
malformation. Review of 71 cases. J Neurosurg 58:183?187
63. Pillay PK, Awad IA, Little JR, Hahn JF (1991) Symptomatic
Chiari malformation in adults: a new classification based on
magnetic resonance imaging with clinical and prognostic
significance. Neurosurgery 28(5):639?645
64. Reybet-Degat O (2001) Pathology of craniocervical junction and
sleep disorders. Rev Neurol 157:S156?S160
65. Rodman T, Resnik ME, Berkowitx RD, Fenelly JF, Olivia J
(1962) Alveolar hypoventilation due to involvement of the
respiratory center by obscure disease of the central nervous
system. Am J Med 32:208?217
66. Ruff ME, Oakes WJ, Fisher S, Spock A (1987) Sleep apnea and
vocal cord paralysis secondary to type I Chiari malformation.
Pediatrics 80(2):231?234
175
67. Sahuquillo J, Rubio E, Po?a M, Rovira A, Rodriguez-Baeza A,
Cervera C (1994) Posterior fossa reconstruction: a surgical
technique for the treatment of Chiari I-Syringomyelia complex.
Preliminary results and magnetic resonance imaging quantitative
assessment. Neurosurgery 35(5):874?884
68. Shiihara T, Shimizu Y, Mitsui T, Saitoh E, Sato S (1995) Isolated
sleep apnea due to Chiari type I malformation and syringomy-
elia. Pediatr Neurol 13(3):266?267
69. Smoker WRK (1994) Craniovertebral junction. Normal anato-
my, craniometry and congenital anomalies. Radiographics
14:255?277
70. Tsao TC, Juang YC, Chiang YC, Tsay YH, Lan RS, Lee CH
(1991) Pneumonia preceding respiratory failure. A rare mis-
leading clinical manifestation in adult Arnold-Chiari malforma-
tion. Chest 99(5):1294?1295
71. Tubbs RS, Elton S, Grabb P, Dockery SE, Bartolucci AA, Oakes
WJ (2001) Analysis of the posterior fossa in children with the
Chiari 0 malformation. Neurosurgery 48:1050?1055
72. Wolf DA, Veasey SP III, Wilson SK, Adame J, Korndorffer WE
(1998) Death following minor head trauma in two adult in-
dividuals with the Chiari I deformity. J Forens Sci 43(6):1241?
1243
73. Yoshimi A, Nomura K, Furune S (2002) Sleep apnea syndrome
associated with a type I Chiari malformation. Brain Dev 24
(1):49?51
74. Zager EL, Ojemann RG, Poletti CE (1990) Acute presentations
of syringomyelia. Report of three cases. J Neurosurg 72:133?
138
75. Zolty P, Sanders MH, Pollack IF (2000) Chiari Malformation
and sleep-disordered breathing: a review of diagnostic and
management issues. Sleep 23(5):637?643
176
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