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Neuropsychological performance changes following subthalamic versus pallidal deep brain stimulation in Parkinson’s disease: a systematic review and metaanalysis

Published online by Cambridge University Press:  27 February 2017

Ahmed Elgebaly ,
Mohamed Elfil ,
Attia Attia ,
Mayar Magdy  and
Ahmed Negida
Ahmed Elgebaly*
Affiliation:
Medical Research Group of Egypt, Cairo, Egypt Faculty of Medicine, Al Azhar University, Cairo, Egypt
Mohamed Elfil
Affiliation:
Medical Research Group of Egypt, Cairo, Egypt Faculty of Medicine, Alexandria University, Alexandria, Egypt
Attia Attia
Affiliation:
Medical Research Group of Egypt, Cairo, Egypt Faculty of Medicine, Al Azhar University, Cairo, Egypt
Mayar Magdy
Affiliation:
Medical Research Group of Egypt, Cairo, Egypt Faculty of Medicine, Beni Suef University, Bani Sweif, Beni Suef Governorate, Egypt
Ahmed Negida
Affiliation:
Medical Research Group of Egypt, Cairo, Egypt Faculty of Medicine, Zagazig University, Zagazig, Sharkia, Egypt Student Research Unit, Zagazig University, Zagazig, Sharkia, Egypt
*
*Address correspondence to: Ahmed Saber Elgebaly, Faculty of Medicine, Al-Azhar University, Nasr City, Cairo, Egypt 11651. (Email1: ahmedelgebaly94@azhar.edu.eg) (Email2: ahmedelgebaly94@gmail.com)
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Abstract

Background

Studies comparing subthalamus (STN) and globus pallidus internus (GPi) deep brain stimulation (DBS) for the management of Parkinson’s disease in terms of neuropsychological performance are scarce and heterogeneous. Therefore, we performed a systematic review and metaanalysis to compare neuropsychological outcomes following STN DBS versus GPi DBS.

Methods

A computer literature search of PubMed, the Web of Science, and Cochrane Central was conducted. Records were screened for eligible studies, and data were extracted and synthesized using Review Manager (v. 5.3 for Windows).

Results

Seven studies were included in the qualitative synthesis. Of them, four randomized controlled trials (n=345 patients) were pooled in the metaanalysis models. The standardized mean difference (SMD) of change in the Stroop color-naming test favored the GPi DBS group (SMD=–0.31, p=0.009). However, other neuropsychological outcomes did not favor either of the two groups (Stroop word-reading: SMD=–0.21, p=0.08; the Wechsler Adult Intelligence Scale (WAIS) digits forward: SMD=0.08, p=0.47; Trail Making Test Part A: SMD=–0.05, p=0.65; WAIS–R digit symbol: SMD=–0.16, p=0.29; Trail Making Test Part B: SMD=–0.14, p=0.23; Stroop color–word interference: SMD=–0.16, p=0.18; phonemic verbal fluency: bilateral DBS SMD=–0.04, p=0.73, and unilateral DBS SMD=–0.05, p=0.83; semantic verbal fluency: bilateral DBS SMD=–0.09, p=0.37, and unilateral DBS SMD=–0.29, p=0.22; Boston Naming Test: SMD=–0.11, p=0.33; Beck Depression Inventory: bilateral DBS SMD=0.15, p=0.31, and unilateral DBS SMD=0.36, p=0.11).

Conclusions

There was no statistically significant difference in most of the neuropsychological outcomes. The present evidence does not favor any of the targets in terms of neuropsychological performance.

Keywords

Parkinson’s diseasedeep brain stimulationsubthalamusglobus pallidusneuropsychological performance

Information

Type
Review Articles
Information
CNS Spectrums , Volume 23 , Issue 1 , February 2018 , pp. 10 - 23
Copyright
© Cambridge University Press 2017 

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References

1. Gelb, DJ, Oliver, E, Gilman, S. Diagnostic criteria for Parkinson disease. Arch Neurol. 1999; 56(1): 33–39.CrossRefGoogle ScholarPubMed
2. Limousin, P, Krack, P, Pollak, P, et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 1998; 339(16): 1105–1111. http://www.nejm.org/doi/full/10.1056/NEJM199810153391603#t=articleResults. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
3. Iacono, RP, Lonser, RR, Maeda, G, et al. Chronic anterior pallidal stimulation for Parkinson’s disease. Acta Neurochir (Wien). 1995; 137(1–2): 106–112.CrossRefGoogle ScholarPubMed
4. Baunez, C, Robbins, TW. Bilateral lesions of the subthalamic nucleus induce multiple deficits in an attentional task in rats. Eur J Neurosci. 1997; 9(10): 2086–2099.CrossRefGoogle Scholar
5. Temel, Y, Blokland, A, Steinbusch, HWM, Visser-Vandewalle, V. The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog Neurobiol. 2005; 76(6): 393–413. Epub ahead of print Oct 24.CrossRefGoogle ScholarPubMed
6. Pillon, B, Ardouin, C, Damier, P, et al. Neuropsychological changes between “off” and “on” STN or GPi stimulation in Parkinson’s disease. Neurology. 2000; 55(3): 411–418.CrossRefGoogle ScholarPubMed
7. Funkiewiez, A, Ardouin, C, Caputo, E, et al. Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2004; 75(6): 834–839. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1739075/pdf/v075p00834.pdf. Accessed February 1, 2017.Google ScholarPubMed
8. Rothlind, JC, Cockshott, RW, Starr, PA, Marks, WJ. Neuropsychological performance following staged bilateral pallidal or subthalamic nucleus deep brain stimulation for Parkinson’s disease. J Int Neuropsychol Soc. 2007; 13(1): 68–79.CrossRefGoogle ScholarPubMed
9. Lang, AE, Obeso, JA. Challenges in Parkinson’s disease: restoration of the nigrostriatal dopamine system is not enough. Lancet Neurol. 2004; 3(5): 309–316.CrossRefGoogle ScholarPubMed
10. Lang, AE, Obeso, JA. Time to move beyond nigrostriatal dopamine deficiency in Parkinson’s disease. Ann Neurol. 2004; 55(6): 761–765.CrossRefGoogle ScholarPubMed
11. Troster, AI, Fields, JA, Wilkinson, SB, et al. Unilateral pallidal stimulation for Parkinson’s disease: neurobehavioral functioning before and 3 months after electrode implantation. Neurology. 1997; 49(4): 1078–1083.CrossRefGoogle ScholarPubMed
12. Smeding, HMM, Speelman, JD, Huizenga, HM, Schuurman, PR, Schmand, B. Predictors of cognitive and psychosocial outcome after STN DBS in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2011; 82(7): 754–760; Epub ahead of print May 21, 2009.Google ScholarPubMed
13. Ardouin, C, Pillon, B, Peiffer, E, et al. Bilateral subthalamic or pallidal stimulation for Parkinson’s disease affects neither memory nor executive functions: a consecutive series of 62 patients. Ann Neurol. 1999; 46(2): 217–223.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
14. Odekerken, VJJ, van Laar, T, Staal, MJ, et al. Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson’s disease (NSTAPS Study): a randomised controlled trial. Lancet Neurol. 2013; 12(1): 37–44. Epub ahead of print Nov 16, 2012.CrossRefGoogle ScholarPubMed
15. Altman, DG, Bland, JM. Standard deviations and standard errors. BMJ. 2005; 331(7521): 903. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1255808/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
16. Egger, M, Davey Smith, G, Schneider, M, Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997; 315(7109): 629–634. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2127453/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
17. Terrin, N, Schmid, CH, Lau, J, Olkin, I. Adjusting for publication bias in the presence of heterogeneity. Stat Med. 2003; 22(13): 2113–2126; Erratum in Stat Med. 2005; 24(5): 825–826.CrossRefGoogle ScholarPubMed
18. Trépanier, LL, Kumar, R, Lozano, AM, Lang, AE, Saint-Cyr, JA. Neuropsychological outcome of GPi pallidotomy and GPi or STN deep brain stimulation in Parkinson’s disease. Brain Cogn. 2000; 42(3): 324–347.CrossRefGoogle ScholarPubMed
19. Rothlind, JC, York, MK, Carlson, K, et al. Neuropsychological changes following deep brain stimulation surgery for Parkinson’s disease: comparisons of treatment at pallidal and subthalamic targets versus best medical therapy. J Neurol Neurosurg Psychiatry. 2015; 86(6): 622–629; Epub ahead of print Sep 2, 2014.CrossRefGoogle ScholarPubMed
20. Odekerken, VJ, Boel, JA, Geurtsen, GJ, Schmand, BA, de Haan, RJ, Schuurman, PR. Neuropsychological outcome after deep brain stimulation for Parkinson disease. Neurology. 2015; 84: 1355–1361.CrossRefGoogle ScholarPubMed
21. Okun, MS, Fernandez, HH, Wu, SS, et al. Cognition and mood in Parkinson’s disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: the COMPARE Trial. Ann Neurol. 2009; 65(5): 586–595. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2692580/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
22. Perozzo, P, Rizzone, M, Bergamasco, B, et al. Deep brain stimulation of subthalamic nucleus: behavioural modifications and familiar relations. Neurol Sci. 2001; 22(1): 81–82.CrossRefGoogle ScholarPubMed
23. Lopiano, L, Rizzone, M, Bergamasco, B, et al. Deep brain stimulation of the subthalamic nucleus: clinical effectiveness and safety. Neurology. 2001; 56(4): 552–554.CrossRefGoogle ScholarPubMed
24. Kim, HJ, Jeon, BS, Paek, SH, et al. Long-term cognitive outcome of bilateral subthalamic deep brain stimulation in Parkinson’s disease. 2014; 261(6): 1090–1096; Epub ahead of print Apr 1.CrossRefGoogle Scholar
25. Aono, M, Iga, J, Ueno, S, Agawa, M, Tsuda, T, Ohmori, T. Neuropsychological and psychiatric assessments following bilateral deep brain stimulation of the subthalamic nucleus in Japanese patients with Parkinson’s disease. J Clin Neurosci. 2014; 21(9): 1595–1598; Epub ahead of print May 1.CrossRefGoogle ScholarPubMed
26. Kleiner-Fisman, G, Lin Liang, GS, Moberg, PJ, et al. Subthalamic nucleus deep brain stimulation for severe idiopathic dystonia: impact on severity, neuropsychological status, and quality of life. J Neurosurg. 2007; 107(1): 29–36.CrossRefGoogle ScholarPubMed
27. Alberts, JL, Voelcker-Rehage, C, Hallahan, K, Vitek, M, Bamzai, R, Vitek, JL. Bilateral subthalamic stimulation impairs cognitive–motor performance in Parkinson’s disease patients. Brain. 2008; 131(Pt 12): 3348–3360. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2639204/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
28. Saint-Cyr, JA, Trépanier, LL, Kumar, R, Lozano, AM, Lang, AE. Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson’s disease. Brain. 2000; 123(Pt 10): 2091–2108.CrossRefGoogle ScholarPubMed
29. Auclair-Ouellet, N, Chantal, S, Cantin, L, Prud’homme, M, Langlois, M, Macoir, J. Transient executive dysfunction following STN DBS in Parkinson’s disease. Can J Neurol Sci. 2011; 38(2): 360–363.CrossRefGoogle Scholar
30. Fields, JA, Troster, AI, Wilkinson, SB, Pahwa, R, Koller, WC. Cognitive outcome following staged bilateral pallidal stimulation for the treatment of Parkinson’s disease. Clin Neurol Neurosurg. 1999; 101(3): 182–188.CrossRefGoogle ScholarPubMed
31. Vingerhoets, G, van der Linden, C, Lannoo, E, et al. Cognitive outcome after unilateral pallidal stimulation in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1999; 66(3): 297–304. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1736258/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
32. Smeding, HM, Esselink, RA. J, Schmand, B, et al. Unilateral pallidotomy versus bilateral subthalamic nucleus stimulation in PD: a comparison of neuropsychological effects. J Neurol. 2005; 252(2): 176–182.CrossRefGoogle ScholarPubMed
33. Daniels, C, Krack, P, Volkmann, J, et al. Risk factors for executive dysfunction after subthalamic nucleus stimulation in Parkinson’s disease. Mov Disord. 2010; 25(11): 1583–1589.CrossRefGoogle ScholarPubMed
34. Yamanaka, T, Ishii, F, Umemura, A, et al. Temporary deterioration of executive function after subthalamic deep brain stimulation in Parkinson’s disease. Clin Neurol Neurosurg. 2012; 114(4): 347–351; Epub ahead of print Dec 15, 2011.CrossRefGoogle ScholarPubMed
35. Moretti, R, Torre, P, Antonello, RM, et al. Neuropsychological changes after subthalamic nucleus stimulation: a 12-month follow-up in nine patients with Parkinson’s disease. Parkinsonism Relat Disord. 2003; 10(2): 73–79.Google Scholar
36. Gironell, A, Kulisevsky, J, Rami, L, Fortuny, N, Garcia-Sanchez, C, Pascual-Sedano, B. Effects of pallidotomy and bilateral subthalamic stimulation on cognitive function in Parkinson disease: a controlled comparative study. J Neurol. 2003; 250(8): 917–923.CrossRefGoogle ScholarPubMed
37. Marshall, DF, Strutt, AM, Williams, AE, Simpson, RK, Jankovic, J, York, MK. Alternating verbal fluency performance following bilateral subthalamic nucleus deep brain stimulation for Parkinson’s disease. Eur J Neurol. 2012; 19(12): 1525–1531. Epub ahead of print May 26.CrossRefGoogle ScholarPubMed
38. De Gaspari, D, Siri, C, Di Gioia, M, et al. Clinical correlates and cognitive underpinnings of verbal fluency impairment after chronic subthalamic stimulation in Parkinson’s disease. Parkinsonism Relat Disord. 2006; 12(5): 289–295. Epub ahead of print Mar 22.CrossRefGoogle ScholarPubMed
39. Smith, KM, O’Connor, M, Papavassiliou, E, Tarsy, D, Shih, LC. Phonemic verbal fluency decline after subthalamic nucleus deep brain stimulation does not depend on number of microelectrode recordings or lead tip placement. Parkinsonism Relat Disord. 2014; 20(4): 400–404. Epub ahead of print Jan 20.CrossRefGoogle ScholarPubMed
40. Harati, A, Müller, T. Neuropsychological effects of deep brain stimulation for Parkinson′s disease. Surg Neurol Int. 2013; 4(Suppl 6): S443–S447. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3858804/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
41. Zangaglia, R, Pacchetti, C, Pasotti, C, et al. Deep brain stimulation and cognitive functions in Parkinson’s disease: a three-year controlled study. Mov Disord. 2009; 24(11): 1621–1628.Google ScholarPubMed
42. Zahodne, LB, Okun, MS, Foote, KD, et al. Cognitive declines one year after unilateral deep brain stimulation surgery in Parkinson’s disease: a controlled study using reliable change. Clin Neuropsychol. 2009; 23(3): 385–405; Epub ahead of print Sep 23, 2008. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3045862/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
43. Miyawaki, E, Perlmutter, JS, Troster, AI, Videen, TO, Koller, WC. The behavioral complications of pallidal stimulation: a case report. Brain Cogn. 2000; 42(3): 417–434.CrossRefGoogle ScholarPubMed
44. Zahodne, LB, Okun, MS, Foote, KD, et al. Greater improvement in quality of life following unilateral deep brain stimulation surgery in the globus pallidus as compared to the subthalamic nucleus. J Neurol. 2009; 256(8): 1321–1329; Epub ahead of print Apr 12, 2009. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3045861/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
45. Woods, SP, Fields, JA, Troster, AI. Neuropsychological sequelae of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a critical review. Neuropsychol Rev. 2002; 12(2): 111–126.CrossRefGoogle ScholarPubMed
46. Witt, K, Daniels, C, Reiff, J, et al. Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson’s disease: a randomised, multicentre study. Lancet Neurol.. 2008; 7(7): 605–614. Epub ahead of print Jun 4.CrossRefGoogle ScholarPubMed
47. Lhommée, E, Klinger, H, Thobois, S, et al. Subthalamic stimulation in Parkinson’s disease: restoring the balance of motivated behaviours. Brain. 2012; 135(5): 1463–1477. Epub ahead of print Apr 15. https://academic.oup.com/brain/article-lookup/doi/10.1093/brain/aws078. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
48. Heo, JH, Lee, KM, Paek, SH, et al. The effects of bilateral subthalamic nucleus deep brain stimulation (STN DBS) on cognition in Parkinson disease. J Neurol Sci. 2008; 273(1–2): 19–24.CrossRefGoogle ScholarPubMed
49. Rizzone, MG, Fasano, A, Daniele, A, et al. Long-term outcome of subthalamic nucleus DBS in Parkinson’s disease: from the advanced phase towards the late stage of the disease? Parkinsonism Relat Disord. 2014; 20(4): 376–381; Epub ahead of print Jan 23.CrossRefGoogle ScholarPubMed
50. Krack, P, Batir, A, Van Blercom, N, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 2003; 349(20): 1925–1934. http://www.nejm.org/doi/full/10.1056/NEJMoa035275#t=articleTop. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
51. Fasano, A, Romito, LM, Daniele, A, et al. Motor and cognitive outcome in patients with Parkinson’s disease 8 years after subthalamic implants. Brain. 2010; 133(9): 2664–2676. https://academic.oup.com/brain/article-lookup/doi/10.1093/brain/awq221. Accessed February 1, 2017.Google ScholarPubMed
52. Kaiser, I, Kryspin-Exner, I, Brucke, T, Volc, D, Alesch, F. Long-term effects of STN DBS on mood: psychosocial profiles remain stable in a 3-year follow-up. BMC Neurol. 2008; 8: 43. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2596774/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
53. York, MK, Wilde, EA., Simpson, R, Jankovic, J. Relationship between neuropsychological outcome and DBS surgical trajectory and electrode location. J Neurol Sci. 2009; 287(1–2): 159–171. Epub ahead of print Sep 19. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2783787/. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
54. Combs, HL, Folley, BS, Berry, DTR, et al. Cognition and depression following deep brain stimulation of the subthalamic nucleus and globus pallidus pars internus in Parkinson’s disease: a meta-analysis. Neuropsychol Rev. 2015; 25(4): 439–454. Epub ahead of print Oct 12.CrossRefGoogle ScholarPubMed
55. Higgins, JP, Green, S. eds. Cochrane Handbook for Systematic Reviews of Interventions: Cochrane Book Series. New York: John Wiley & Sons; 2008. http://onlinelibrary.wiley.com/book/10.1002/9780470712184. Accessed February 1, 2017.Google Scholar
56. Glenny, AM, Altman, DG, Song, F, et al. Indirect comparisons of competing interventions. Health Technol Assess. 2005; 9(26): 1–134; iii–iv. https://www.journalslibrary.nihr.ac.uk/hta/hta9260#/abstract. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
57. Follett, KA, Weaver, FM, Stern, M, et al. Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease. N Engl J Med. 2010; 362(22): 2077–2091. http://www.nejm.org/doi/full/10.1056/NEJMoa0907083#t=articleTop. Accessed February 1, 2017.CrossRefGoogle ScholarPubMed
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