Download Therapeutic options for nocturnal problems in Parkinson`s disease

Therapeutic options for nocturnal problems
in Parkinson’s disease and atypical
parkinsonian disorders
Lisa Klingelhoefer, Elisaveta Sokolov &
K. Ray Chaudhuri
Journal of Neural Transmission
Translational Neuroscience, Neurology
and Preclinical Neurological Studies,
Psychiatry and Preclinical Psychiatric
Studies
ISSN 0300-9564
J Neural Transm
DOI 10.1007/s00702-014-1202-6
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Author's personal copy
J Neural Transm
DOI 10.1007/s00702-014-1202-6
NEUROLOGY AND PRECLINICAL NEUROLOGICAL STUDIES - REVIEW ARTICLE
Therapeutic options for nocturnal problems in Parkinson’s
disease and atypical parkinsonian disorders
Lisa Klingelhoefer • Elisaveta Sokolov
K. Ray Chaudhuri
•
Received: 3 December 2013 / Accepted: 18 March 2014
Springer-Verlag Wien 2014
Abstract Sleep disturbances in Parkinson’s disease and
parkinsonism (such as atypical parkinsonian disorders like
multiple system atrophy, progressive supranuclear palsy,
dementia with Lewy bodies and corticobasal degeneration)
are multifactorial and as such treatment needs to be tailored
to the specific patient case and sleep dysfunction. One also
has to consider drug-related effects on sleep architecture.
This article provides an overview of the therapeutic options
for nocturnal problems in Parkinson‘s disease and atypical
parkinsonian disorders.
Keywords Sleep disturbance Nocturnal problems Parkinson’s disease Atypical parkinsonian disorders,
MSA, PSP
Introduction
Sleep disturbances in Parkinson’s disease (PD) and parkinsonism (atypical parkinsonian disorders (APD) such as
multiple system atrophy (MSA), progressive supranuclear
palsy (PSP), dementia with Lewy bodies (LBD) and
L. Klingelhoefer (&) E. Sokolov K. R. Chaudhuri
Department of Neurology, National Parkinson Foundation
International Centre of Excellence, King’s College Hospital and
King’s College, 9th floor Ruskin Wing, Denmark Hill,
London SE5 9RS, UK
e-mail: [email protected]
K. R. Chaudhuri
e-mail: [email protected]
L. Klingelhoefer
Department of Neurology, Technical University Dresden,
Fetscherstraße 74, Dresden, Germany
corticobasal degeneration (CBD)) are complex and multifactorial and therefore treatment needs to be tailored to the
specific patient case and sleep dysfunction. The evidence
base in most cases is not yet substantial and mostly lacks
level 1 evidence for treatment. The American Academy of
Neurology (AAN) and the Movement Disorders Society
(MDS) have issued recent guidance on the evidence-based
management of non-motor symptoms (NMS) in PD
including sleep disorders (Zesiewicz et al. 2010; Seppi
et al. 2011). Recommended treatments from these guidelines are shown in Table 1.
Pharmacologic and non-pharmacologic strategies can be
used to target varying sleep disturbances. Sleep hygiene is
a commonly proposed non-pharmacologic strategy
although unproven specific to PD-related sleep issues.
Strategies summarising sleep hygiene are shown in
Table 2.
Methods
This paper is based on a broad literature review in PubMed
under the following search terms: nocturnal problems AND
Parkinson’s disease/atypical Parkinson’s disease; Nocturnal symptoms AND Parkinson’s disease/atypical Parkinson’s disease; Therapies AND nocturnal symptoms AND
Parkinson’s disease/atypical Parkinson’s disease; Sleep
disorders AND Parkinson’s disease/atypical Parkinson’s
disease; Therapies AND sleep disorders AND Parkinson’s
disease/atypical Parkinson’s disease; Nocturnal problems
AND MSA/PSP/LBD/CBD; Therapies AND sleep disorders AND MSA/PSP/LBD/CBD.
Articles presenting primary research results, review
articles and case reports have been considered and if suitable referenced in this article.
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Table 1 Suggested treatment strategies for sleep disturbances in Parkinson‘s disease
Nocturnal disturbances related to sleep disorders:
Insomnia
Pharmacologic
strategies
Short-acting benzodiazepines
Non-benzodiazepine hypnotics: Zopiclone
Tricyclic antidepressants: Amitriptyline
Tetracyclic antidepressants: Mianserin
Selective serotonin reuptake inhibitors (SSRIs): Paroxetine
NonAvoid alcohol at night, caffeine, tobacco
pharmacologic
Sleep hygiene (Table 2)
strategies
Relaxation and cognitive therapies
REM sleep behaviour disorder (RBD)
Pharmacologic
Clonazepam
strategies
Melatonin
Pramipexole ? clonazepam (Fantini et al. 2003; Sasai et al. 2013)
Levodopa
NonSafe sleeping environment for both the patient and the bed partner to avoid sleeppharmacologic
related injury by placing a mattress on the floor, padding corners of furniture,
strategies
window protection, removing potentially dangerous objects from the bedroom
Excessive daytime sleepiness (EDS)
Pharmacologic
Modafinil
strategies
Sodium oxybate
Methylphenidate
Caffeine tablets may be tried
Dexamfetamine
Restless legs syndrome (RLS)/Periodic Pharmacologic
Dopamine agonists
limb movements (PLM)
strategies
Gabapentin
Opiates
Nocturnal disturbances related to autonomic/vegetative dysfunction:
Sleep apnoea
NonContinuous positive airway pressure (CPAP), oral appliances (mandibular
pharmacologic
repositioning appliance, tongue retaining device)
strategies
Urinary symptoms: Nocturia
Pharmacologic
Low-dose amitriptyline
strategies
Consider transdermal rotigotine patch
If detrusor instability: Oxybutynin, tolterodine
Avoid evening dosing with diuretics, antihypertensives or vasodilators
NonDecrease evening fluid intake
pharmacologic
Empty bladder prior to bed
strategies
Catheters/bedside commode
Nocturnal disturbances related to motor dysfunction:
Fidgeting, cramps, posturing, tremor,
Pharmacologic
Trial of continuous drug delivery (CDD) over night as can be obtained by
akinesia
strategies
nighttime dosing of:
Dopamine agonists: rotigotine transdermal patch [therapy level 1 evidence to
support nighttime use, RECOVER study (Trenkwalder et al. 2011)]
Pramipexole extended release [therapy level 1 evidence, CLEOPATRA-PD
(Poewe et al. 2007; Poewe et al. 2011; Schapira et al. 2011)]
Ropinirole extended release [therapy level 1 evidence, EASE-PD (Pahwa et al.
2007) and EASE-PD Adjunct (Ray Chaudhuri et al. 2012)]
Other nighttime infusions using CDD may also help (apomorphine infusion,
intrajejunal duodopa infusion)
Use of satin bed sheets and bed straps to help moving in bed
Nonpharmacologic
strategies
Nocturnal disturbances related to psychiatric comorbidity:
Psychiatric symptoms: hallucinations,
Pharmacologic
Antipsychotics: quetiapine, clozapine
psychosis, delusion
strategies
Chaudhuri (2002); Chaudhuri and Schapira (2009); Iranzo et al. (2009); Zesiewicz et al. (2010); Seppi et al. (2011); Bhidayasiri and Truong (2012);
Gaig and Iranzo (2012)
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Therapeutic options for nocturnal problems in Parkinson’s disease
Table 2 Strategies for sleep hygiene
Good bedtime routine (similar hours and avoiding daytime naps)
Avoid stimulants at bedtime (caffeine, nicotine, chocolate and
alcohol, approximately 6 h before bedtime) and large meals
close to bedtime
Regular exercise during day (but avoid exercise 4 h before
bedtime)
Associate bed with sleep (avoid watching TV for instance from
bed)
Quiet relaxing bedroom with good ambient temperature
Nocturnal disturbances related to sleep disorders
in Parkinson’s disease and atypical parkinsonian
disorders
Insomnia is common in PD, and economic implications
relate to decreased productivity and more hospital attendance. Chronic insomnia of sleep onset can be also managed by a range of non-pharmacological strategies such as
(Wilson et al. 2010):
•
•
•
•
Cognitive behavioural therapy.
Stimulus control therapy.
Sleep restriction.
Progressive muscle relaxation.
Nocturnal motor symptoms cause sleep maintenance
insomnia and sleep disruption because of nocturnal akinesia and nighttime off symptoms as well as early morning
off periods. Strategies utilising continuous dopamine
delivery overnight such as rotigotine transdermal patch
(RECOVER study), pramipexole extended release (CLEOPATRA-PD) and ropinirole extended release (EASE-PD
and EASE-PD Adjunct) may help in these cases (Pahwa
et al. 2007; Poewe et al. 2007; Trenkwalder et al. 2011;
Ray Chaudhuri et al. 2012). The beneficial effects of rotigotine on sleep disturbances were maintained for up to
1 year measured by Parkinson’s disease Sleep Scale
(Trenkwalder et al. 2012). However, pramipexole use may
be associated with insomnia in some patients.
There are no trials addressing these agents in atypical
parkinsonism. Most PSP patients complain of insomnia,
and early polysomnographic studies reported reduced total
sleep time and increased sleep fragmentation. Furthermore
with disease progression, REM sleep is dramatically
reduced (Montplaisir et al. 1997).
In PD and atypical parkinsonian disorders such as MSA
and DLB, there are disorders of both REM and non-REM
sleep. REM sleep behaviour disorders seem to have a
strong association to synucleinopathies such as PD, MSA
and LBD (Boeve et al. 2001; Gagnon et al. 2006; Iranzo
et al. 2006; Hauw et al. 2011).
While in non-REM sleep, one may experience sleep
terror (night terror, disruption of sleep beginning with a
fearful scream or crying with or without signs of arousal
such as sitting with eyes open while the person remains in
deep sleep) and sleep walking. For both, non-pharmacological measures aimed at reducing stress are important.
RBD can be managed pharmacologically with medications such as clonazepam (0.5–2 mg) at nighttime or
melatonin (3–12 mg). Recently, one study has reported a
beneficial effect of combining the dopamine agonist
pramipexole with clonazepam (Sasai et al. 2013).
RBD can be worsened by (Boeve et al. 2007; Aurora
et al. 2010):
•
•
•
•
•
•
Paroxetine
Fluoxetine
Imipramine
Venlafaxine
Mirtazapine
Beta-blockers (Iranzo and Santamaria 1999; Morrison
et al. 2011)
Excessive daytime sleepiness (EDS) is one of the
commonest and a troublesome problem in PD and APD. As
EDS is multifactorial, it may occur due to (Knie et al.
2011):
•
•
•
•
The underlying disease process (EDS has been shown
to be a pre motor NMS of PD).
Drug induced (dopamine agonists, antidepressants,
anxiolytics, hypnotics, sedatives).
Sleep apnoea and sleep-disordered breathing.
Secondary narcolepsy without cataplexy phenotype.
Some patients show subjective improvement with
Modafinil or otherwise with high-dose caffeine tablets.
Evidence for Modafinil is, however, not robust with some
groups finding it did not improve EDS in PD at all (Ondo
et al. 2005). The SLEEMSA study and others revealed that
more than 25 % of patients with MSA experience EDS, a
frequency similar to that in PD and clearly more than in
healthy controls (2 %) (Moreno-Lopez et al. 2011; Shimohata et al. 2012). EDS seems to be associated with different causes but in contrast to PD, in MSA the amount of
dopaminergic treatment was not correlated with EDS.
Sleep-disordered breathing and sleep efficiency predicted
EDS in MSA (Moreno-Lopez et al. 2011). Ghorayeb et al.
(2002) showed in 57 MSA patients that 56 % complained
of sleep fragmentation and half of them complained of
somnolence, compared with 30 % of age-matched patients
with PD. The somnolence was correlated with the severity
of the disease. Arnulf et al. (2005) performed nighttime
polysomnography in 15 PSP patients and showed EDS was
present in one-third of the patients.
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Table 3 Classification and therapeutic options of sleep problems in atypical parkinsonian disorders (APD)
Category
The type of APD
Therapeutic options
Nocturnal disturbances related to sleep disorders:
Insomnia
PSP ??? (Arnulf et al. 2005;
Gama et al. 2010)
Recommendations are based on clinical practice and extrapolation from data in
Parkinson’s disease-based studies
MSA ? (Gama et al. 2010)
Pharmacologic strategies:
LBD ?? (Pao et al. 2013)
Short-acting benzodiazepines
Non-benzodiazepine hypnotics: Zopiclone
Tricyclic antidepressants: Amitriptyline
Tetracyclic antidepressants: Mianserin
Selective serotonin reuptake inhibitors (SSRIs): Paroxetine
Non-pharmacologic strategies:
Avoid alcohol at night, caffeine, tobacco
Exercise and sunshine
Relaxation and cognitive therapies
REM sleep behaviour
disorder (RBD)
MSA ???? (Iranzo et al. 2006)
Pharmacologic strategies:
PSP ?? (Olson et al. 2000; Arnulf
et al. 2005)
Clonazepam
LBD ???? (Boeve et al. 2001;
Iranzo et al. 2006; Pao et al. 2013)
Alternatives: Carbamazepine, donepezil, levodopa, clozapine, quetiapine
(Yamauchi et al. 2003; Boeve et al. 2007)
Melatonin
RSWA in one patient with CBD
(Kimura et al. 1997)
Excessive daytime sleepiness
(EDS)
MSA ? (Arnulf 2005; Gama et al.
2010)
If patient is treated with a dopamine agonist: decrease dose or change to another
dopamine agonist
PSP ?? (Arnulf 2005; Gama et al.
2010)
Methylphenidate (Hattori et al. 2003)
LBD ?? (Arnulf 2005)
Bupropion (Arnulf 2005).
MSA
Recommendations are based on clinical practice and extrapolation from data in
Parkinson’s disease and RLS based studies (Garcia-Borreguero et al. 2012)
Modafinil (Arnulf 2005)
Caffeine tablets may be useful
Restless legs syndrome
(RLS)
PSP
Pharmacologic strategies:
Dopaminergic agents
Antiepileptic drugs (e.g. gabapentin, carbamazepine, pregabalin)
Benzodiazepines
Hypnotics (e.g. clonazepam, zopiclone)
Analgesics (e.g. codeine, tramadol, oxycodone combined with naloxone)
Non-pharmacologic strategies:
Sleep hygiene (quiet, comfortable, cool environment; appropriate bed clothes)
Avoid alcohol at night, caffeine, tobacco
During an attack:
Using a hot or cold massage
Bathing in hot or cold water
Walking, stretching and exercise
Relaxation exercises (biofeedback or yoga)
Distracting mind by mental exercises
Periodic limb movements
(PLM)
MSA
LBD (Pao et al. 2013)
Pharmacologic strategies:
Levodopa
Gabapentin
Opiates
The evidence base is very poor and these therapies need to be used with
clinician’s discretion
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Table 3 continued
Category
The type of APD
Therapeutic options
Nocturnal disturbances related to autonomic/vegetative dysfunction:
Sleep-disordered breathing
(SDB)
PSP (Gama et al. 2010)
Ventilation with continuous positive airway pressure, indicated in patients with
MSA suffering from nocturnal stridor (Iranzo et al. 2000)
LBD (Gama et al. 2010; Pao et al.
2013)
Tracheostomy, indicated in patients with MSA if stridor appears during sleep
and wakefulness on diurnal base (Iranzo 2005)
MSA ??? (Iranzo 2005)
Other treatment options for stridor in MSA patients: botulinum toxin injections,
laryngeal surgery (e.g. unilateral cordectomy) (Iranzo 2005; Gaig and Iranzo
2012)
Nocturnal disturbances related to motor dysfunction:
Fidgeting, cramps, posturing,
tremor, akinesia
MSA
Pharmacologic strategies:
PSP
Sustained dopaminergic stimulation (nighttime dosing of): levodopa, COMT
inhibitor
LBD
Magnesium
Nocturnal disturbances related to psychiatric comorbidity:
Psychiatric symptoms:
hallucinations, psychosis,
delusion
MSA ??
Pharmacologic strategies:
PSP ????
Antipsychotics: quetiapine, clozapine
LBD ????
Quetiapine may aggravate parkinsonism and has a poor evidence base, however
clinically often used. Clozapine needs regular monitoring for agranulocytosis
Larsen and Tandberg (2001), Zesiewicz et al. (2010)
Appearance of nocturnal disturbances in the different types of APD ranging from: ? rarely, ?? often, ??? frequent, ???? very frequent
APD atypical parkinsonian disorder, MSA multiple system atrophy, PSP progressive supranuclear palsy, LBD dementia with Lewy bodies, CBD
corticobasal degeneration, REM rapid eye movement RSWA REM sleep without atonia
Drugs shown to be effective for daytime sleepiness
(however not specific to PD and APD) are (Hogl et al.
2002; Ondo et al. 2008; Knie et al. 2011):
•
•
•
•
Modafinil (licensed for use in narcolepsy and PD).
Sodium oxybate (licensed for use in narcolepsy).
Methylphenidate.
Dexamfetamine.
Sodium oxybate, Methylphenidate and Dexamfetamine
have potential for abuse, and thus Modafinil is generally
recommended as first line (Chaudhuri and Schapira 2009;
Zesiewicz et al. 2010).
Nocturnal disturbances related to autonomic/vegetative
dysfunction in Parkinson’s disease and atypical
parkinsonian disorders
Sleep-disordered breathing (SDB) maybe a specific issue in
MSA, but also occurs in PD patients in particular sleep
apnoea. This leads to troublesome EDS. As with the
treatment of obstructive sleep apnoea in non-PD patients,
first-line treatment methods such as continuous positive
airway pressure (CPAP) and oral appliances (mandibular
repositioning appliance, tongue retaining device) have
shown a clear benefit in maintaining a patent airway at
night and also in decreasing risks associated with EDS
secondary to sleep apnoea (Findley et al. 2000; Epstein
et al. 2009; Shimohata et al. 2012).
SDB is an important nocturnal problem in patients with
APD, especially MSA as it is associated with decreased
survival and higher rates of sudden death during sleep
(Silber and Levine 2000; Shimohata et al. 2008). There are
different underlying causes of SDB (Iranzo et al. 2004;
Shimohata et al. 2007; Suzuki et al. 2010; Gaig and Iranzo
2012):
•
•
•
•
Upper airway obstruction at the pharyngeal level (e.g.
obstructive sleep apnoea).
Upper airway obstruction at the level of the glottic
aperture in the larynx (e.g. stridor).
Central owing to the degeneration of the pontomedullary respiratory centers.
Dysfunction of bulbar and diaphragmatic muscles.
CPAP and tracheostomy, but not oral appliances have
been shown to eliminate nocturnal stridor and increase
survival in MSA patients (Iranzo et al. 2000; Yamaguchi
et al. 2003; Iranzo et al. 2004). CPAP treats nocturnal
stridor by increasing the glottic aperture separating the
vocal cords and reducing the downward displacement of
the larynx (Kuzniar et al. 2009). If CPAP is not tolerated by
the patient tracheostomy, an invasive surgical procedure
should be considered. Tracheostomy eliminates stridor
during sleep and wakefulness by bypassing the vocal cord
obstruction and is indicated if diurnal stridor also during
wakefulness is presented (Iranzo 2005). Other treatment
options for stridor in MSA patients are botulinum toxin
injections and laryngeal surgery (e.g. unilateral
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Table 4 Some possible future developments as therapeutic options
of sleep problems focussed on Parkinson‘s disease (PD)
Agent
Condition
Tozadenant (adenosine A2a receptor
antagonists)
Excessive daytime sleepiness
(EDS) in PD
Pitolisant (histamine H3 receptor
inverse agonist)
Narcolepsy, cataplexy, EDS
ADX-N05
Narcolepsy, EDS
Tasimelteon (melatonin MT1/MT2
receptor agonist)
Sleep wake cycle disorder
Armodafinil
Narcolepsy
Long acting melatonin
REM sleep behaviour
disorder
cordectomy), however both procedures can increase the
risk of aspiration which is one of the most frequent causes
of death in MSA patients (Iranzo 2005; Gaig and Iranzo
2012).
Nocturia is and remains one of the most bothersome
NMS for PD patients (Stocchi et al. 2001; Politis et al.
2010). There are a number of treatment options, but once
again relies on good sleep hygiene and measures such as
reducing evening oral fluid intake, avoiding prior to bed
and consideration of whether a urinary catheter or bedside
commode may be of benefit. Pharmacologic options
include low-dose amitriptyline or even a trial of dopamine
agonists, which may have D1 receptor activity such as
transdermal rotigotine patch. Oxybutynin or tolterodine can
be useful for detrusor instability.
In APD, treatment lines of nocturnal problems are
similar to one adopted and discussed above for PD. These
are shown in Table 3.
For future developments, there are a few trials
addressing aspects of sleep problems in general and not
specifically PD or APD. These are shown in Table 4.
Conclusions
A proposed scheme for examination of parkinsonian
patients with sleep-related problems would be first to
examine and assess the patient and evaluate with the Parkinson’s disease sleep scale (PDSS) (Chaudhuri et al.
2002) and the Epworth sleepiness scale (Johns 1991), both
recommended by the MDS task force on sleep scales.
Treatment can then be specifically aligned to the observed
problems. In some cases, further examination such as
polysomnography and multiple sleep latency test may be
required.
Acknowledgments This review presents independent research
funded by the National Institute for Health Research (NIHR) Mental
123
Health Biomedical Research Centre and Dementia Unit at South
London and Maudsley NHS Foundation Trust and King’s College
London. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health.
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