Effect of deep brain stimulation on depression of Parkinson’s disease: a network meta-analysis_West China Medical Journal

Authors：

KONG Xiangwei ^1,2 , KANG Simin ^1,3 , SHANG Huifang ¹ ,  SONG Wei ¹

1. Department of Neurology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
2. Department of Neurology, Jiujiang No.1 People’s Hospital, Jiujiang, Jiangxi 330200, P. R. China;
3. Department of Neurology, Medical Center Hospital of Qionglai City, Qionglai, Sichuan 611500, P. R. China;

Corresponding author：

SONG Wei, Email: 36255368@qq.com

Keywords：

Parkinson’s disease; deep brain stimulation; depression; network meta-analysis

DOI：

10.7507/1002-0179.202007282

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Objective To assess the changes in depression symptoms in patients with Parkinson’s disease (PD) receiving combined treatment of deep brain stimulation (DBS) and antiparkinsonian drug therapy (DT) compared with under DT alone. Methods Related literature was retrieved from electronic databases, including PubMed, Cochrane Library, Embase, China National Knowledge Infrastructure, Wanfang Data, and VIP databases. Stata 14.0 software was used for statistical analysis. Network meta-analysis was performed using frequentist model to compare different interventions with each other. Results Five cohort studies and seven randomized controlled trials (RCTs) were included. The total number of participants was 1241. Assessed by the Beck Depression Inventory (BDI) score as the primary outcome, patients who received DT alone showed worse outcome in depression as compared to those who received subthalamic nucleus (STN)-DBS plus DT [standardized mean difference (SMD)=0.30, 95% confidence interval (CI) (0.01, 0.59), P<0.05], and there was no significant difference between the patients receiving globus pallidus interna (GPi)-DBS plus DT and those receiving STN-DBS plus DT [SMD=–0.12, 95%CI (–0.41, 0.16), P>0.05] or those receiving DT alone [SMD=–0.42, 95%CI (–0.84, 0.00), P>0.05]. Assessed by BDI-Ⅱ as the primary outcome, patients who received DT alone showed worse outcome in depression than those who received STN-DBS plus DT [SMD=0.29, 95%CI (0.05, 0.54), P<0.05]; compared with STN-DBS plus DT and DT alone, GPi-DBS plus DT was associated with better improvement in depression [SMD=–0.26, 95%CI (–0.46, –0.06), P<0.05; SMD=–0.55, 95%CI (–0.88, –0.23), P<0.05]. The ranking results of surface under the cumulative ranking curves showed that DBS plus DT had a better superiority in depression symptoms, and GPi-DBS was better than STN-DBS. Conclusion Compared with DT, STN-DBS plus DT is more likely to improve the depressive symptoms of PD patients, and GPi-DBS may be better than STN-DBS.

Citation： KONG Xiangwei, KANG Simin, SHANG Huifang, SONG Wei. Effect of deep brain stimulation on depression of Parkinson’s disease: a network meta-analysis. West China Medical Journal, 2023, 38(3): 416-423. doi: 10.7507/1002-0179.202007282 Copy

1.	GBD 2016 Parkinson’s Disease Collaborators. Global, regional, and national burden of Parkinson’s disease, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol, 2018, 17(11): 939-953.
2.	Hommel ALAJ, Meinders MJ, Lorenzl S, et al. The prevalence and determinants of neuropsychiatric symptoms in late-stage parkinsonism. Mov Disord Clin Pract, 2020, 7(5): 531-542.
3.	Jakobs M, Fomenko A, Lozano AM, et al. Cellular, molecular, and clinical mechanisms of action of deep brain stimulation: a systematic review on established indications and outlook on future developments. EMBO Mol Med, 2019, 11(4): e9575.
4.	Weaver FM, Follett KA, Stern M, et al. Randomized trial of deep brain stimulation for Parkinson disease: thirty-six-month outcomes. Neurology, 2012, 79(1): 55-65.
5.	Accolla EA, Pollo C. Mood effects after deep brain stimulation for Parkinson’s disease: an update. Front Neurol, 2019, 10: 617.
6.	Beck AT, Ward CH, Mendelson M, et al. An inventory for measuring depression. Arch Gen Psychiatry, 1961, 4: 561-571.
7.	Beck AT, Steer RA, Brown GK. Manual for the Beck Depression Inventory–II. San Antonio, TX: Psychological Corporation, 1996: 13-80.
8.	Williams JR, Hirsch ES, Anderson K, et al. A comparison of nine scales to detect depression in Parkinson disease: which scale to use?. Neurology, 2012, 78(13): 998-1006.
9.	Higgins JPT, Thomas J, Chandler J, et al. Cochrane handbook for systematic reviews of interventions version 6.3 (updated February 2022). Cochrane, 2022.
10.	Higgins JP, Altman DG, Gøtzsche PC, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ, 2011, 343: d5928.
11.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
12.	Chaimani A, Higgins JP, Mavridis D, et al. Graphical tools for network meta-analysis in STATA. PLoS One, 2013, 8(10): e76654.
13.	White IR. Network meta-analysis. Stata J, 2015, 15(4): 951-985.
14.	York MK, Dulay M, Macias A, et al. Cognitive declines following bilateral subthalamic nucleus deep brain stimulation for the treatment of Parkinson’s disease. J Neurol Neurosurg Psychiatry, 2008, 79(7): 789-795.
15.	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.
16.	Capecci M, Ricciuti RA, Burini D, et al. Functional improvement after subthalamic stimulation in Parkinson’s disease: a non-equivalent controlled study with 12-24 month follow up. J Neurol Neurosurg Psychiatry, 2005, 76(6): 769-774.
17.	Burdick AP, Foote KD, Wu S, et al. Do patient’s get angrier following STN, GPi, and thalamic deep brain stimulation. Neuroimage, 2011, 54(Suppl 1): S227-S232.
18.	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.
19.	Rothlind JC, Cockshott RW, Starr PA, et al. 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.
20.	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.
21.	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.
22.	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.
23.	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.
24.	Okun MS, Wu SS, Fayad S, et al. Acute and chronic mood and apathy outcomes from a randomized study of unilateral STN and GPi DBS. PLoS One, 2014, 9(12): e114140.
25.	Lhommée E, Wojtecki L, Czernecki V, et al. Behavioural outcomes of subthalamic stimulation and medical therapy versus medical therapy alone for Parkinson’s disease with early motor complications (EARLYSTIM trial): secondary analysis of an open-label randomised trial. Lancet Neurol, 2018, 17(3): 223-231.
26.	Couto MI, Monteiro A, Oliveira A, et al. Depression and anxiety following deep brain stimulation in Parkinson’s disease: systematic review and meta-analysis. Acta Med Port, 2014, 27(3): 372-382.
27.	Greenhouse I, Gould S, Houser M, et al. Stimulation at dorsal and ventral electrode contacts targeted at the subthalamic nucleus has different effects on motor and emotion functions in Parkinson’s disease. Neuropsychologia, 2011, 49(3): 528-534.
28.	Patriat R, Cooper SE, Duchin Y, et al. Individualized tractography-based parcellation of the globus pallidus pars interna using 7T MRI in movement disorder patients prior to DBS surgery. Neuroimage, 2018, 178: 198-209.
29.	Karachi C, Yelnik J, Tandé D, et al. The pallidosubthalamic projection: an anatomical substrate for nonmotor functions of the subthalamic nucleus in primates. Mov Disord, 2005, 20(2): 172-180.
30.	Parent A, Hazrati LN. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev, 1995, 20(1): 91-127.
31.	Groenewegen HJ, Berendse HW. Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol, 1990, 294(4): 607-622.
32.	Stefani A, Trendafilov V, Liguori C, et al. Subthalamic nucleus deep brain stimulation on motor-symptoms of Parkinson’s disease: focus on neurochemistry. Prog Neurobiol, 2017, 151: 157-174.
33.	Faggiani E, Delaville C, Benazzouz A. The combined depletion of monoamines alters the effectiveness of subthalamic deep brain stimulation. Neurobiol Dis, 2015, 82: 342-348.
34.	Wang XH, Zhang L, Sperry L, et al. Target selection recommendations based on impact of deep brain stimulation surgeries on nonmotor symptoms of Parkinson’s disease. Chin Med J (Engl), 2015, 128(24): 3371-3380.
35.	Irmen F, Horn A, Mosley P, et al. Left prefrontal connectivity links subthalamic stimulation with depressive symptoms. Ann Neurol, 2020, 87(6): 962-975.
36.	Thobois S, Ardouin C, Lhommée E, et al. Non-motor dopamine withdrawal syndrome after surgery for Parkinson’s disease: predictors and underlying mesolimbic denervation. Brain, 2010, 133(Pt 4): 1111-1127.
37.	Storch A, Schneider CB, Wolz M, et al. Nonmotor fluctuations in Parkinson disease: severity and correlation with motor complications. Neurology, 2013, 80(9): 800-809.

1. GBD 2016 Parkinson’s Disease Collaborators. Global, regional, and national burden of Parkinson’s disease, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol, 2018, 17(11): 939-953.
2. Hommel ALAJ, Meinders MJ, Lorenzl S, et al. The prevalence and determinants of neuropsychiatric symptoms in late-stage parkinsonism. Mov Disord Clin Pract, 2020, 7(5): 531-542.
3. Jakobs M, Fomenko A, Lozano AM, et al. Cellular, molecular, and clinical mechanisms of action of deep brain stimulation: a systematic review on established indications and outlook on future developments. EMBO Mol Med, 2019, 11(4): e9575.
4. Weaver FM, Follett KA, Stern M, et al. Randomized trial of deep brain stimulation for Parkinson disease: thirty-six-month outcomes. Neurology, 2012, 79(1): 55-65.
5. Accolla EA, Pollo C. Mood effects after deep brain stimulation for Parkinson’s disease: an update. Front Neurol, 2019, 10: 617.
6. Beck AT, Ward CH, Mendelson M, et al. An inventory for measuring depression. Arch Gen Psychiatry, 1961, 4: 561-571.
7. Beck AT, Steer RA, Brown GK. Manual for the Beck Depression Inventory–II. San Antonio, TX: Psychological Corporation, 1996: 13-80.
8. Williams JR, Hirsch ES, Anderson K, et al. A comparison of nine scales to detect depression in Parkinson disease: which scale to use?. Neurology, 2012, 78(13): 998-1006.
9. Higgins JPT, Thomas J, Chandler J, et al. Cochrane handbook for systematic reviews of interventions version 6.3 (updated February 2022). Cochrane, 2022.
10. Higgins JP, Altman DG, Gøtzsche PC, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ, 2011, 343: d5928.
11. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
12. Chaimani A, Higgins JP, Mavridis D, et al. Graphical tools for network meta-analysis in STATA. PLoS One, 2013, 8(10): e76654.
13. White IR. Network meta-analysis. Stata J, 2015, 15(4): 951-985.
14. York MK, Dulay M, Macias A, et al. Cognitive declines following bilateral subthalamic nucleus deep brain stimulation for the treatment of Parkinson’s disease. J Neurol Neurosurg Psychiatry, 2008, 79(7): 789-795.
15. 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.
16. Capecci M, Ricciuti RA, Burini D, et al. Functional improvement after subthalamic stimulation in Parkinson’s disease: a non-equivalent controlled study with 12-24 month follow up. J Neurol Neurosurg Psychiatry, 2005, 76(6): 769-774.
17. Burdick AP, Foote KD, Wu S, et al. Do patient’s get angrier following STN, GPi, and thalamic deep brain stimulation. Neuroimage, 2011, 54(Suppl 1): S227-S232.
18. 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.
19. Rothlind JC, Cockshott RW, Starr PA, et al. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. Okun MS, Wu SS, Fayad S, et al. Acute and chronic mood and apathy outcomes from a randomized study of unilateral STN and GPi DBS. PLoS One, 2014, 9(12): e114140.
25. Lhommée E, Wojtecki L, Czernecki V, et al. Behavioural outcomes of subthalamic stimulation and medical therapy versus medical therapy alone for Parkinson’s disease with early motor complications (EARLYSTIM trial): secondary analysis of an open-label randomised trial. Lancet Neurol, 2018, 17(3): 223-231.
26. Couto MI, Monteiro A, Oliveira A, et al. Depression and anxiety following deep brain stimulation in Parkinson’s disease: systematic review and meta-analysis. Acta Med Port, 2014, 27(3): 372-382.
27. Greenhouse I, Gould S, Houser M, et al. Stimulation at dorsal and ventral electrode contacts targeted at the subthalamic nucleus has different effects on motor and emotion functions in Parkinson’s disease. Neuropsychologia, 2011, 49(3): 528-534.
28. Patriat R, Cooper SE, Duchin Y, et al. Individualized tractography-based parcellation of the globus pallidus pars interna using 7T MRI in movement disorder patients prior to DBS surgery. Neuroimage, 2018, 178: 198-209.
29. Karachi C, Yelnik J, Tandé D, et al. The pallidosubthalamic projection: an anatomical substrate for nonmotor functions of the subthalamic nucleus in primates. Mov Disord, 2005, 20(2): 172-180.
30. Parent A, Hazrati LN. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev, 1995, 20(1): 91-127.
31. Groenewegen HJ, Berendse HW. Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol, 1990, 294(4): 607-622.
32. Stefani A, Trendafilov V, Liguori C, et al. Subthalamic nucleus deep brain stimulation on motor-symptoms of Parkinson’s disease: focus on neurochemistry. Prog Neurobiol, 2017, 151: 157-174.
33. Faggiani E, Delaville C, Benazzouz A. The combined depletion of monoamines alters the effectiveness of subthalamic deep brain stimulation. Neurobiol Dis, 2015, 82: 342-348.
34. Wang XH, Zhang L, Sperry L, et al. Target selection recommendations based on impact of deep brain stimulation surgeries on nonmotor symptoms of Parkinson’s disease. Chin Med J (Engl), 2015, 128(24): 3371-3380.
35. Irmen F, Horn A, Mosley P, et al. Left prefrontal connectivity links subthalamic stimulation with depressive symptoms. Ann Neurol, 2020, 87(6): 962-975.
36. Thobois S, Ardouin C, Lhommée E, et al. Non-motor dopamine withdrawal syndrome after surgery for Parkinson’s disease: predictors and underlying mesolimbic denervation. Brain, 2010, 133(Pt 4): 1111-1127.
37. Storch A, Schneider CB, Wolz M, et al. Nonmotor fluctuations in Parkinson disease: severity and correlation with motor complications. Neurology, 2013, 80(9): 800-809.

West China Medical Journal

Effect of deep brain stimulation on depression of Parkinson’s disease: a network meta-analysis

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