The Open Neurology Journal




ISSN: 1874-205X ― Volume 14, 2020

The Impact of Deep Brain Stimulation on Sleep and Olfactory Function in Parkinson’s Disease



David P Breen*, Hu Liang Low , Anjum Misbahuddin
Essex Centre for Neurological Sciences, Queen’s Hospital, Romford, UK

Abstract

Objective:

Relatively little is known about the effects of deep brain stimulation on non-motor symptoms. The aim of this pilot study was to assess the impact of deep brain stimulation on sleep and olfactory function in Parkinson’s disease.

Methods:

Subjective sleep quality and olfactory testing were performed on 11 consecutive Parkinson’s disease patients (eight men and three women) undergoing bilateral subthalamic nucleus stimulation. All patients consented to undergo clinical assessments prior to the procedure, and at regular intervals afterwards.

Results:

Subjective sleep quality improved at six months following deep brain stimulation and this benefit was sustained in the majority of patients at later follow-up assessments. There was no significant change in olfactory function following deep brain stimulation.

Conclusions:

In addition to having beneficial effects on motor function and quality of life, bilateral subthalamic nucleus stimulation improves subjective sleep quality in Parkinson’s disease.

Keywords: Deep brain stimulation, sleep, olfaction, smell, Parkinson s disease.


Article Information


Identifiers and Pagination:

Year: 2015
Volume: 9
First Page: 70
Last Page: 72
Publisher Id: TONEUJ-9-70
DOI: 10.2174/1874205X01509010070

Article History:

Received Date: 29/9/2014
Revision Received Date: 1/12/2014
Acceptance Date: 11/12/2014
Electronic publication date: 30/9/2015
Collection year: 2015

© Breen et al.; Licensee Bentham Open.

open-access license: This is an open access article licensed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted, non-commercial use, distribution and reproduction in any medium, provided the work is properly cited.


* Address correspondence to this author at the Essex Centre for Neurological Sciences, Queen’s Hospital, Rom Valley Way, Romford, RM7 0AG, UK; Tel: 01708 435000; Fax: 01708 435538; Email: dpbreen1@gmail.com





INTRODUCTION

The pathology of Parkinson’s disease (PD) extends far beyond the nigrostriatal system, resulting in a variety of non-motor symptoms which cause significant morbidity. Whilst deep brain stimulation (DBS) has been shown to be more effective than best medical therapy in improving motor fluctuations in selected PD patients [1Deuschl G, Schade-Brittinger C, Krack P, et al. A randomized trial of deep-brain stimulation for Parkinson’s disease N Engl J Med 2006; 355(9): 896-908.
[http://dx.doi.org/10.1056/NEJMoa060281] [PMID: 16943402]
], relatively little is known about its effects on non-motor symptoms. The aim of this pilot study was to assess the impact of bilateral subthalamic nucleus (STN) DBS on sleep and olfactory function in PD.

MATERIAL AND METHODS

We recruited 11 consecutive PD patients (eight men and three women) undergoing bilateral STN DBS at the Essex Centre for Neurological Sciences. All patients consented to undergo clinical assessments prior to the procedure, and at regular intervals afterwards. Local institutional approval was granted for the study and the study was conducted according to the Declaration of Helsinki principles.

Subjective sleep quality was evaluated using the Parkinson’s Disease Sleep Scale (PDSS) [2Chaudhuri KR, Pal S, DiMarco A, et al. The Parkinson’s disease sleep scale: a new instrument for assessing sleep and nocturnal disability in Parkinson’s disease J Neurol Neurosurg Psychiatry 2002; 73(6): 629-35.
[http://dx.doi.org/10.1136/jnnp.73.6.629] [PMID: 12438461]
]. This scale – which is validated for use in PD – asks patients to rate 15 aspects of nocturnal and daytime sleep on a linear scale from 0 (bad) to 10 (good). In addition to the overall score (maximum 150), PDSS questions were combined to assess eight specific sleep sub-domains: sleep quality, sleep onset and maintenance, nocturnal restlessness, nocturnal psychosis, nocturia, nocturnal motor disturbance, sleep refreshment and daytime dozing.

Olfactory testing was performed using the University of Pennsylvania Smell Identification Test (UPSIT), a 40-question multiple choice scratch-and-sniff test [3Doty RL, Shaman P, Kimmelman CP, Dann MS. University of Pennsylvania Smell Identification Test: a rapid quantitative olfactory function test for the clinic Laryngoscope 1984; 94(2 Pt 1): 176-8.
[http://dx.doi.org/10.1288/00005537-198402000-00004] [PMID: 6694486]
]. Patients were classified into three groups according to gender-specific cut-off scores: anosmia=<20; hyposmia=20-33 (men) and 20-34 (women); normosmia=>33 (men) and >34 (women). Other assessments included Unified Parkinson’s Disease Rating Scale (UPDRS) part III (motor impairment), Beck Depression Inventory (BDI) (depression) and Parkinson’s Disease Questionnaire (PDQ-39) (quality of life).

RESULTS

Mean age at diagnosis was 43 years and mean disease duration at DBS surgery was 134 months. 9 out of 11 (82%) patients had a higher PDSS score at six months compared to pre-DBS assessment, indicating a subjective improvement in sleep quality. PDSS score was significantly higher at six months compared to pre-DBS assessment (mean 113.2 versus 95.9; paired t-test, p=0.050). Apart from nocturnal psychosis, there was a trend towards improvement in all sleep sub-domains following DBS (Table 1).

Table 1

Effect of DBS on subjective sleep quality.




Compared to pre-DBS assessment, the vast majority of patients also had higher PDSS score at later follow-up assessments: 7 out of 8 (88%) at one year, 6 out of 6 (100%) at two years, and 5 out of 7 (71%) at three years. No significant difference was observed over the entire follow-up period due to large inter-individual variation (1 way ANOVA, p=0.159).

Three patients were excluded from the olfactory analysis due to missing data. All PD patients had an impaired sense of smell prior to DBS (five were anosmic, three were hyposmic). One patient was re-classified from anosmia to hyposmia at six months, but the rest remained the same. There was no significant difference in UPSIT score at six months compared to pre-DBS assessment (mean 20.1 versus 19.6; paired t-test, p=0.761).

There was no significant correlation between change in PDSS/UPSIT and change in clinical parameters (UPDRS part III score, BDI score or levodopa equivalent daily dose).

DISCUSSION

Our preliminary results indicate that DBS leads to sustained improvement in subjective sleep quality across a variety of different domains. Previous polysomnography studies have shown that bilateral STN DBS patients have improved total sleep time and sleep efficiency, but no changes in sleep architecture, suggesting that the observed sleep benefit may be due to improved nocturnal motor activity rather than being the direct result of altered sleep physiology [4Amara AW, Watts RL, Walker HC. The effects of deep brain stimulation on sleep in Parkinson’s disease Ther Adv Neurol Disorder 2011; 4(1): 15-24.
[http://dx.doi.org/10.1177/1756285610392446] [PMID: 21339905]
]. Our results on olfactory testing are in line with Fabbri and colleagues who found no effect of STN DBS on olfactory function [5Fabbri M, Guedes LC, Coelho M, et al. Subthalamic deep brain stimulation effects on odor identification in Parkinson’s disease Eur J Neurol 2015; 22(1): 207-10.
[http://dx.doi.org/10.1111/ene.12396] [PMID: 24602222]
]. However, three previous studies found significant improvements in odour identification following bilateral STN stimulation [6Guo X, Gao G, Wang X, et al. Effects of bilateral deep brain stimulation of the subthalamic nucleus on olfactory function in Parkinson’s disease patients Stereotact Funct Neurosurg 2008; 86(4): 237-44.
[http://dx.doi.org/10.1159/000131662] [PMID: 18477840]
-8Peters ML, Ravin P, Novak P, et al. DBS-implanted Parkinson’s disease patients show better olfaction than those treated medically Neurol Bull 2010; 2: 1-6.
[http://dx.doi.org/10.7191/neurol_bull.2010.1016]
]. It has been suggested that STN DBS may increase neuronal activity in the orbitofrontal and primary olfactory cortices, thereby having a positive effect on the cognitive processing of olfactory information. The differences in study outcomes may reflect small sample sizes, different cohort characteristics and/or different olfactory testing protocols used.

CONCLUSION

Bilateral STN DBS improves subjective sleep quality but we did not observe any significant change in olfactory function. Future studies should consider non-motor symptoms when assessing the effectiveness of DBS on PD patients.

ABBREVIATIONS

BDI  =  Beck Depression Inventory;
DBS  =  Deep Brain Stimulation;
PD  =  Parkinson’s disease;
PDQ-39  =  Parkinson’s Disease Questionnaire;
PDSS  =  Parkinson’s Disease Sleep Scale;
STN  =  Subthalamic nucleus;
UPDRS  =  Unified Parkinson’s Disease Rating Scale;
UPSIT  =  University of Pennsylvania Smell Identification Test

CONFLICT OF INTEREST

The authors confirm that this article content has no conflict of interest.

ACKNOWLEDGEMENTS

Declared none.

REFERENCES

[1] Deuschl G, Schade-Brittinger C, Krack P, et al. A randomized trial of deep-brain stimulation for Parkinson’s disease N Engl J Med 2006; 355(9): 896-908.
[http://dx.doi.org/10.1056/NEJMoa060281] [PMID: 16943402]
[2] Chaudhuri KR, Pal S, DiMarco A, et al. The Parkinson’s disease sleep scale: a new instrument for assessing sleep and nocturnal disability in Parkinson’s disease J Neurol Neurosurg Psychiatry 2002; 73(6): 629-35.
[http://dx.doi.org/10.1136/jnnp.73.6.629] [PMID: 12438461]
[3] Doty RL, Shaman P, Kimmelman CP, Dann MS. University of Pennsylvania Smell Identification Test: a rapid quantitative olfactory function test for the clinic Laryngoscope 1984; 94(2 Pt 1): 176-8.
[http://dx.doi.org/10.1288/00005537-198402000-00004] [PMID: 6694486]
[4] Amara AW, Watts RL, Walker HC. The effects of deep brain stimulation on sleep in Parkinson’s disease Ther Adv Neurol Disorder 2011; 4(1): 15-24.
[http://dx.doi.org/10.1177/1756285610392446] [PMID: 21339905]
[5] Fabbri M, Guedes LC, Coelho M, et al. Subthalamic deep brain stimulation effects on odor identification in Parkinson’s disease Eur J Neurol 2015; 22(1): 207-10.
[http://dx.doi.org/10.1111/ene.12396] [PMID: 24602222]
[6] Guo X, Gao G, Wang X, et al. Effects of bilateral deep brain stimulation of the subthalamic nucleus on olfactory function in Parkinson’s disease patients Stereotact Funct Neurosurg 2008; 86(4): 237-44.
[http://dx.doi.org/10.1159/000131662] [PMID: 18477840]
[7] Hummel T, Jahnke U, Sommer U, Reichmann H, Müller A. Olfactory function in patients with idiopathic Parkinson’s disease: effects of deep brain stimulation in the subthalamic nucleus J Neural Transm 2005; 112(5): 669-76.
[http://dx.doi.org/10.1007/s00702-004-0207-y] [PMID: 15517435]
[8] Peters ML, Ravin P, Novak P, et al. DBS-implanted Parkinson’s disease patients show better olfaction than those treated medically Neurol Bull 2010; 2: 1-6.
[http://dx.doi.org/10.7191/neurol_bull.2010.1016]

Endorsements



"Open access will revolutionize 21st century knowledge work and accelerate the diffusion of ideas and evidence that support just in time learning and the evolution of thinking in a number of disciplines."


Daniel Pesut
(Indiana University School of Nursing, USA)

"It is important that students and researchers from all over the world can have easy access to relevant, high-standard and timely scientific information. This is exactly what Open Access Journals provide and this is the reason why I support this endeavor."


Jacques Descotes
(Centre Antipoison-Centre de Pharmacovigilance, France)

"Publishing research articles is the key for future scientific progress. Open Access publishing is therefore of utmost importance for wider dissemination of information, and will help serving the best interest of the scientific community."


Patrice Talaga
(UCB S.A., Belgium)

"Open access journals are a novel concept in the medical literature. They offer accessible information to a wide variety of individuals, including physicians, medical students, clinical investigators, and the general public. They are an outstanding source of medical and scientific information."


Jeffrey M. Weinberg
(St. Luke's-Roosevelt Hospital Center, USA)

"Open access journals are extremely useful for graduate students, investigators and all other interested persons to read important scientific articles and subscribe scientific journals. Indeed, the research articles span a wide range of area and of high quality. This is specially a must for researchers belonging to institutions with limited library facility and funding to subscribe scientific journals."


Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


Browse Contents




Webmaster Contact: info@benthamopen.net
Copyright © 2020 Bentham Open