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01-03-2022 | Deep Brain Stimulation | Original Article

Short- and long-term motor outcome of STN-DBS in Parkinson’s Disease: focus on sex differences

Authors: Nico Golfrè Andreasi, Luigi Michele Romito, Roberta Telese, Roberto Cilia, Antonio Emanuele Elia, Alessio Novelli, Giovanni Tringali, Giuseppe Messina, Vincenzo Levi, Grazia Devigili, Sara Rinaldo, Angelo Amato Franzini, Roberto Eleopra

Published in: Neurological Sciences | Issue 3/2022

Abstract

Introduction

Subthalamic nucleus deep brain stimulation (STN-DBS) is an established treatment for patients with Parkinson’s disease (PD) with motor complications; the contribution of sex in determining the outcome is still not understood.

Methods

We included 107 patients (71 males) with PD consecutively implanted with STN-DBS at our center. We reviewed patient charts from our database and retrospectively collected demographical and clinical data at baseline and at three follow-up visits (1, 5 and 10 years).

Results

We found a long-lasting effect of DBS on motor complications, despite a progressive worsening of motor performances in the ON medication condition. Bradykinesia and non-dopaminergic features seem to be the major determinant of this progression. Conversely to males, females showed a trend towards worsening in bradykinesia already at 1-year follow-up and poorer scores in non-dopaminergic features at 10-year follow-up. Levodopa Equivalent Daily Dose (LEDD) was significantly reduced after surgery compared to baseline values; however, while in males LEDD remained significantly lower than baseline even 10 years after surgery, in females LEDD returned at baseline values. Males showed a sustained effect on dyskinesias, but this benefit was less clear in females; the total electrical energy delivered was consistently lower in females compared to males. The profile of adverse events did not appear to be influenced by sex.

Conclusion

Our data suggest that there are no major differences on the motor effect of STN-DBS between males and females. However, there may be some slight differences that should be specifically investigated in the future and that may influence therapeutic decisions in the chronic follow-up.

Deuschl G, Schade-Brittinger C, Krack P et al (2006) A randomized trial of deep-brain stimulation for Parkinson’s disease. New Engl J Medicine 355:896–908. https://doi.org/10.1056/nejmoa060281CrossRef

Limousin P, Foltynie T (2019) Long-term outcomes of deep brain stimulation in Parkinson disease. Nat Rev Neurol 15:234–242. https://doi.org/10.1038/s41582-019-0145-9CrossRefPubMed

Picillo M, Nicoletti A, Fetoni V et al (2017) The relevance of gender in Parkinson’s disease: a review. J Neurol 264:1583–1607. https://doi.org/10.1007/s00415-016-8384-9CrossRefPubMed

Meoni S, Macerollo A, Moro E (2020) Sex differences in movement disorders. Nat Rev Neurol 16:84–96. https://doi.org/10.1038/s41582-019-0294-xCrossRefPubMed

Lubomski M, Rushworth RL, Lee W et al (2014) Sex differences in Parkinson’s disease. J Clin Neurosci 21:1503–1506. https://doi.org/10.1016/j.jocn.2013.12.016CrossRefPubMed

Shpiner DS, Luca DGD, Cajigas I et al (2019) Gender disparities in deep brain stimulation for Parkinson’s disease. Neuromodulation Technology Neural Interface 22:484–488. https://doi.org/10.1111/ner.12973CrossRef

Accolla E, Caputo E, Cogiamanian F et al (2007) Gender differences in patients with Parkinson’s disease treated with subthalamic deep brain stimulation. Movement Disord 22:1150–1156. https://doi.org/10.1002/mds.21520CrossRefPubMed

Romito LM, Contarino FM, Albanese A (2010) Transient gender-related effects in Parkinson’s disease patients with subthalamic stimulation. J Neurol 257:603–608. https://doi.org/10.1007/s00415-009-5381-2CrossRefPubMed

Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. Journal of Neurology, Neurosurgery & Psychiatry 55. https://doi.org/10.1136/jnnp.55.3.181

10.

Defer G-L, Widner H, Marié R-M et al (1999) Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Movement Disord 14:572–584. https://doi.org/10.1002/1531-8257(199907)14:4%3c572::aid-mds1005%3e3.0.co;2-cCrossRefPubMed

11.

Fahn S, Elton R, Members of the UPDRS Development Committee. In: Fahn S, Marsden CD, Calne DB, Goldstein M, eds. Recent developments in Parkinson’s disease, Vol 2. Florham Park, NJ. Macmillan Health Care Information 1987, pp 15 3–163, 293–304

12.

Levy G, Tang MX, Cote LJ et al (2000) Motor impairment in PD: relationship to incident dementia and age. Neurology 4:539–544. https://doi.org/10.1212/wnl.55.4.539CrossRef

13.

Hoehn MM, Yahr MD (1967) Parkinsonism onset, progression, and mortality. Neurology 17:427–427. https://doi.org/10.1212/wnl.17.5.427CrossRefPubMed

14.

Tomlinson CL, Stowe R, Patel S et al (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Movement Disord 25:2649–2653. https://doi.org/10.1002/mds.23429CrossRefPubMed

15.

Schade S, Mollenhauer B, Trenkwalder C (2020) Levodopa equivalent dose conversion factors: an updated proposal including opicapone and safinamide. Mov Disord Clin Pract 7:343–345. https://doi.org/10.1002/mdc3.12921CrossRefPubMedPubMedCentral

16.

Voon V, Sohr M, Lang AE et al (2011) Impulse control disorders in Parkinson disease: a multicenter case–control study. Ann Neurol 69:986–996. https://doi.org/10.1002/ana.22356CrossRefPubMed

17.

Koss AM, Alterman RL, Tagliati M, Shils JL (2005) Calculating total electrical energy delivered by deep brain stimulation systems. Ann Neurol 58:168–168. https://doi.org/10.1002/ana.20525CrossRefPubMed

18.

Hamberg K, Hariz G-M (2014) The decision-making process leading to deep brain stimulation in men and women with Parkinson’s disease—an interview study. Bmc Neurol 14:89. https://doi.org/10.1186/1471-2377-14-89CrossRefPubMedPubMedCentral

19.

Hariz G, Lindberg M, Hariz MI, Bergenheim AT (2003) Gender differences in disability and health-related quality of life in patients with Parkinson’s disease treated with stereotactic surgery. Acta Neurol Scand 108:28–37. https://doi.org/10.1034/j.1600-0404.2003.00092.xCrossRefPubMed

20.

Bjornestad A, Forsaa EB, Pedersen KF et al (2016) Risk and course of motor complications in a population-based incident Parkinson’s disease cohort. Parkinsonism Relat D 22:48–53. https://doi.org/10.1016/j.parkreldis.2015.11.007CrossRef

21.

Martinez-Ramirez D, Giugni J, Vedam-Mai V et al (2014) The “brittle response” to Parkinson’s disease medications: characterization and response to deep brain stimulation. PLoS ONE 9(4):e94856. https://doi.org/10.1371/journal.pone.0094856CrossRefPubMedPubMedCentral

22.

Olanow CW, Kieburtz K, Rascol O et al (2013) Factors predictive of the development of Levodopa-induced dyskinesia and wearing-off in Parkinson’s disease. Movement Disord 28:1064–1071. https://doi.org/10.1002/mds.25364CrossRef

23.

Georgiev D, Hamberg K, Hariz M et al (2017) Gender differences in Parkinson’s disease: a clinical perspective. Acta Neurol Scand 136(6):570–584. https://doi.org/10.1111/ane.12796CrossRefPubMed

24.

Chandran S, Krishnan S, Rao RM et al (2014) Gender influence on selection and outcome of deep brain stimulation for Parkinson’s disease. Ann Indian Acad Neur 17:66–70. https://doi.org/10.4103/0972-2327.128557CrossRef

25.

Lezcano E, Gómez-Esteban JC, Tijero B, et al (2016) Long-term impact on quality of life of subthalamic nucleus stimulation in Parkinson’s disease. Journal of Neurology 263. https://doi.org/10.1007/s00415-016-8077-4

26.

Aviles-Olmos I, Kefalopoulou Z, Tripoliti E, et al (2014) Long-term outcome of subthalamic nucleus deep brain stimulation for Parkinson’s disease using an MRI-guided and MRI-verified approach. Journal of Neurology, Neurosurgery & Psychiatry 85. https://doi.org/10.1136/jnnp-2013-306907

27.

Castrioto A, Lozano AM, Poon Y-Y et al (2011) Ten-year outcome of subthalamic stimulation in Parkinson disease: a blinded evaluation. Arch Neurol 68:1550–1556. https://doi.org/10.1001/archneurol.2011.182CrossRefPubMed

28.

Schüpbach WMM, Chastan N, Welter ML et al (2005) Stimulation of the subthalamic nucleus in Parkinson’s disease: a 5 year follow up. J Neurol Neurosurg Psychiatry 76:1640–1644. https://doi.org/10.1136/jnnp.2005.063206CrossRefPubMedPubMedCentral

29.

Hartmann CJ, Wojtecki L, Vesper J, et al (2015) Long-term evaluation of impedance levels and clinical development in subthalamic deep brain stimulation for Parkinson’s disease. Parkinsonism & Related Disorders 21. https://doi.org/10.1016/j.parkreldis.2015.07.019

30.

Gervais-Bernard H, Xie-Brustolin J, Mertens P, et al (2009) Bilateral subthalamic nucleus stimulation in advanced Parkinson’s disease: five year follow-up. Journal of Neurology 256. https://doi.org/10.1007/s00415-009-0076-2

31.

Zibetti M, Merola A, Rizzi L, et al (2011) Beyond nine years of continuous subthalamic nucleus deep brain stimulation in Parkinson’s disease. Movement Disorders 26. https://doi.org/10.1002/mds.23903

32.

Li J, Zhang Y, Li Y (2015) Long-term follow-up of bilateral subthalamic nucleus stimulation in Chinese Parkinson’s disease patients. British Journal of Neurosurgery 29. https://doi.org/10.3109/02688697.2014.997665

33.

Haaxma CA, Bloem BR, Borm GF et al (2007) Gender differences in Parkinson’s disease. J Neurology Neurosurg Psychiatry 78:819. https://doi.org/10.1136/jnnp.2006.103788CrossRef

34.

Marceglia S, Mrakic-Sposta S, Foffani G et al (2006) Gender-related differences in the human subthalamic area: a local field potential study. Eur J Neurosci 24:3213–3222. https://doi.org/10.1111/j.1460-9568.2006.05208.xCrossRefPubMed

35.

Sato K, Hatano T, Yamashiro K et al (2006) Prognosis of Parkinson’s disease: time to stage III, IV, V, and to motor fluctuations. Movement Disord 21:1384–1395. https://doi.org/10.1002/mds.20993CrossRefPubMed

36.

Williams NR, Foote KD, Okun MS (2014) Subthalamic nucleus versus globus pallidus internus deep brain stimulation: translating the rematch into clinical practice. Mov Disord Clin Pract 1:24–35. https://doi.org/10.1002/mdc3.12004CrossRefPubMedPubMedCentral

37.

Picillo M, Phokaewvarangkul O, Poon YY (2021) Levodopa versus dopamine agonist after subthalamic stimulation in Parkinson’s disease. Mov Disord 36(3):672–680. https://doi.org/10.1002/mds.28382CrossRefPubMed

38.

Fasano A, Romito LM, Daniele A et al (2010) Motor and cognitive outcome in patients with Parkinson’s disease 8 years after subthalamic implants. Brain 133:2664–2676. https://doi.org/10.1093/brain/awq221CrossRefPubMed

39.

Picillo M, Lozano AM, Kou N (2016) Programming deep brain stimulation for Parkinson’s disease: the Toronto Western Hospital Algorithms. Brain Stimul 9(3):425–437. https://doi.org/10.1016/j.brs.2016.02.004CrossRefPubMed

40.

Schrag A, Jahanshahi M, Quinn N (2000) What contributes to quality of life in patients with Parkinson’s disease? J Neurology Neurosurg Psychiatry 69:308. https://doi.org/10.1136/jnnp.69.3.308CrossRef

41.

Debû B, Godeiro CDO, Lino JC, Moro E (2018) Managing gait, balance, and posture in Parkinson’s disease. Curr Neurol Neurosci 18:23. https://doi.org/10.1007/s11910-018-0828-4CrossRef

42.

Almeida L, Rawal PV, Ditty B et al (2016) Deep brain stimulation battery longevity: comparison of monopolar versus bipolar stimulation mode. Mov Disord Clin Pract 3(4):359–366. https://doi.org/10.1002/mdc3.12285CrossRefPubMedPubMedCentral

43.

Zangaglia R, Pacchetti C, Pasotti C et al (2009) Deep brain stimulation and cognitive functions in Parkinson’s disease: a three-year controlled study. Mov Disord 24(11):1621–1628. https://doi.org/10.1002/mds.22603CrossRefPubMed

44.

Bove F, Fraix V, Cavallieri F et al (2020) Dementia and subthalamic deep brain stimulation in Parkinson disease: a long-term overview 95(4):e384–e392. https://doi.org/10.1212/WNL.0000000000009822CrossRef

Title: Short- and long-term motor outcome of STN-DBS in Parkinson’s Disease: focus on sex differences
Authors: Nico Golfrè Andreasi
Luigi Michele Romito
Roberta Telese
Roberto Cilia
Antonio Emanuele Elia
Alessio Novelli
Giovanni Tringali
Giuseppe Messina
Vincenzo Levi
Grazia Devigili
Sara Rinaldo
Angelo Amato Franzini
Roberto Eleopra
Publication date: 01-03-2022
Publisher: Springer International Publishing
Keywords: Deep Brain Stimulation
Parkinson's Disease
Levodopa
Published in: Neurological Sciences / Issue 3/2022
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-021-05564-w

At a glance: The STEP trials

Springer Medicine

Short- and long-term motor outcome of STN-DBS in Parkinson’s Disease: focus on sex differences

Abstract

Introduction

Methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Introduction

Methods

Results

Conclusion

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