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

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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.

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Availability of data and material

Original data are available upon reasonable request.

Code availability

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References

  1. 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/nejmoa060281

    Article  CAS  Google Scholar 

  2. 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/s41582-019-0145-9

    Article  PubMed  Google Scholar 

  3. 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/s00415-016-8384-9

    Article  PubMed  Google Scholar 

  4. 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-x

    Article  CAS  PubMed  Google Scholar 

  5. 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.2013.12.016

    Article  PubMed  Google Scholar 

  6. 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.12973

    Article  Google Scholar 

  7. 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.21520

    Article  PubMed  Google Scholar 

  8. 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/s00415-009-5381-2

    Article  PubMed  Google Scholar 

  9. 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-c

    Article  CAS  PubMed  Google Scholar 

  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.55.4.539

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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.23429

    Article  PubMed  Google Scholar 

  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/mdc3.12921

    Article  PubMed  PubMed Central  Google Scholar 

  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.22356

    Article  PubMed  Google Scholar 

  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.20525

    Article  PubMed  Google Scholar 

  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/10.1186/1471-2377-14-89

    Article  PubMed  PubMed Central  Google Scholar 

  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.x

    Article  PubMed  Google Scholar 

  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.2015.11.007

    Article  Google Scholar 

  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.0094856

    Article  PubMed  PubMed Central  Google Scholar 

  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.25364

    Article  CAS  Google Scholar 

  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.12796

    Article  CAS  PubMed  Google Scholar 

  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/10.4103/0972-2327.128557

    Article  Google Scholar 

  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.2011.182

    Article  PubMed  Google Scholar 

  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.2005.063206

    Article  PubMed  PubMed Central  Google Scholar 

  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.2006.103788

    Article  Google Scholar 

  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.x

    Article  CAS  PubMed  Google Scholar 

  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.20993

    Article  PubMed  Google Scholar 

  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/mdc3.12004

    Article  PubMed  PubMed Central  Google Scholar 

  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.28382

    Article  CAS  PubMed  Google Scholar 

  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/awq221

    Article  PubMed  Google Scholar 

  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.2016.02.004

    Article  PubMed  Google Scholar 

  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.69.3.308

    Article  CAS  Google Scholar 

  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/s11910-018-0828-4

    Article  CAS  Google Scholar 

  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/mdc3.12285

    Article  PubMed  PubMed Central  Google Scholar 

  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.22603

    Article  PubMed  Google Scholar 

  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.0000000000009822

    Article  Google Scholar 

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Correspondence to Nico Golfrè Andreasi.

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This work is based on retrospective clinical data and does not require specific approval from our Ethical Committee.

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All the authors have read and approved the current version of the manuscript and agreed for its publication.

Conflict of interest

NGA, LR, RT, RC, AEE, AN, GT, GM, GD, SR, AAF, RE have no financial disclosures to report. VL has been medical advisor at Newronika SRL (Neuromodulation system manufacturer) from December 2018 to December 2019.

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Golfrè Andreasi, N., Romito, L.M., Telese, R. et al. Short- and long-term motor outcome of STN-DBS in Parkinson’s Disease: focus on sex differences. Neurol Sci 43, 1769–1781 (2022). https://doi.org/10.1007/s10072-021-05564-w

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