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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 1 23 Your article is protected by copyright and all rights are held exclusively by SpringerVerlag Wien. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 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. 123 Author's personal copy L. Klingelhoefer et al. 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) 123 Author's personal copy 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. 123 Author's personal copy L. Klingelhoefer et al. 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 123 Author's personal copy Therapeutic options for nocturnal problems in Parkinson’s disease 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 123 Author's personal copy L. Klingelhoefer et al. 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. References Arnulf I (2005) Excessive daytime sleepiness in parkinsonism. 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