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Published in: Journal of Neurology 1/2021

Open Access 01-01-2021 | Parkinson's Disease | Original Communication

Sex and freezing of gait in Parkinson’s disease: a systematic review and meta-analysis

Authors: Anouk Tosserams, Masood Mazaheri, Priya Vart, Bastiaan R. Bloem, Jorik Nonnekes

Published in: Journal of Neurology | Issue 1/2021

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Abstract

Objective

It is unknown how sex affects the prevalence of freezing of gait (FOG). We conducted a systematic review and meta-analysis to establish the sex-specific prevalence of FOG in persons with Parkinson’s disease (PD). In addition, we investigated whether men and women were represented accurately in intervention trials targeting FOG.

Methods

We queried the EMBASE and PubMed databases and identified 2637 articles. Of these, 16 epidemiological studies were included in the meta-analysis, and 51 intervention studies were included in the comparative analysis.

Results

In total, 5702 persons were included in the final meta-analysis of epidemiological studies. The pooled estimate of overall FOG prevalence was 43% [95% CI 33–53%]. We found no difference in FOG prevalence between men [44% (34–54%)] and women [42% (31–52%)] with PD. However, women were markedly underrepresented in intervention trials targeting FOG, with an average proportion of only 29.6% of women in trial populations. The percentage of women included in trials was similar across intervention types but differed greatly across geographical regions.

Conclusion

Sex is not a predictor of FOG. This could aid clinicians in counseling persons with PD about FOG. Importantly, a global effort is needed to include more women into clinical trials. Given the skewed distribution of men and women included in intervention trials targeting FOG, caution might be warranted when extrapolating results from FOG trials to women.
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Literature
1.
go back to reference Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10(8):734–744CrossRef Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10(8):734–744CrossRef
2.
go back to reference Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn PA (2010) Predictors of future falls in Parkinson disease. Neurology 75(2):116–124CrossRef Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn PA (2010) Predictors of future falls in Parkinson disease. Neurology 75(2):116–124CrossRef
3.
go back to reference Rahman S, Griffin HJ, Quinn NP, Jahanshahi M (2008) Quality of life in Parkinson’s disease: the relative importance of the symptoms. Mov Disord 23(10):1428–1434CrossRef Rahman S, Griffin HJ, Quinn NP, Jahanshahi M (2008) Quality of life in Parkinson’s disease: the relative importance of the symptoms. Mov Disord 23(10):1428–1434CrossRef
4.
go back to reference Giladi N, Treves TA, Simon ES et al (2001) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm (Vienna) 108(1):53–61CrossRef Giladi N, Treves TA, Simon ES et al (2001) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm (Vienna) 108(1):53–61CrossRef
5.
go back to reference Naismith SL, Shine JM, Lewis SJ (2010) The specific contributions of set-shifting to freezing of gait in Parkinson’s disease. Mov Disord 25(8):1000–1004CrossRef Naismith SL, Shine JM, Lewis SJ (2010) The specific contributions of set-shifting to freezing of gait in Parkinson’s disease. Mov Disord 25(8):1000–1004CrossRef
6.
go back to reference Giladi N, McDermott MP, Fahn S et al (2001) Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology 56(12):1712–1721CrossRef Giladi N, McDermott MP, Fahn S et al (2001) Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology 56(12):1712–1721CrossRef
7.
go back to reference Lieberman A (2006) Are Freezing of Gait (FOG) and panic related? J Neurol Sci 248(1–2):219–222CrossRef Lieberman A (2006) Are Freezing of Gait (FOG) and panic related? J Neurol Sci 248(1–2):219–222CrossRef
8.
go back to reference Nonnekes J, Ruzicka E, Nieuwboer A, Hallett M, Fasano A, Bloem BR (2019) Compensation strategies for gait impairments in Parkinson disease: a review. JAMA Neurol 76(6):718–725CrossRef Nonnekes J, Ruzicka E, Nieuwboer A, Hallett M, Fasano A, Bloem BR (2019) Compensation strategies for gait impairments in Parkinson disease: a review. JAMA Neurol 76(6):718–725CrossRef
9.
go back to reference Snijders AH, Bloem BR (2010) Cycling for freezing of gait. N Eng J Med 362(13):e46CrossRef Snijders AH, Bloem BR (2010) Cycling for freezing of gait. N Eng J Med 362(13):e46CrossRef
10.
go back to reference Nonnekes J, Janssen S, Bloem BR (2017) Superficial brain stimulation to overcome freezing of gait in Parkinson disease. Neurology 88(17):1681–1682CrossRef Nonnekes J, Janssen S, Bloem BR (2017) Superficial brain stimulation to overcome freezing of gait in Parkinson disease. Neurology 88(17):1681–1682CrossRef
11.
go back to reference Snijders AH, Jeene P, Nijkrake MJ, Abdo WF, Bloem BR (2012) Cueing for freezing of gait: a need for 3-dimensional cues? Neurologist 18(6):404–405CrossRef Snijders AH, Jeene P, Nijkrake MJ, Abdo WF, Bloem BR (2012) Cueing for freezing of gait: a need for 3-dimensional cues? Neurologist 18(6):404–405CrossRef
12.
go back to reference Janssen S, Soneji M, Nonnekes J, Bloem BR (2016) A painted staircase illusion to alleviate freezing of gait in Parkinson’s disease. J Neurol 263(8):1661–1662CrossRef Janssen S, Soneji M, Nonnekes J, Bloem BR (2016) A painted staircase illusion to alleviate freezing of gait in Parkinson’s disease. J Neurol 263(8):1661–1662CrossRef
13.
go back to reference Macht M, Kaussner Y, Moller JC et al (2007) Predictors of freezing in Parkinson’s disease: a survey of 6,620 patients. Mov Disord 22(7):953–956CrossRef Macht M, Kaussner Y, Moller JC et al (2007) Predictors of freezing in Parkinson’s disease: a survey of 6,620 patients. Mov Disord 22(7):953–956CrossRef
14.
go back to reference Lamberti P, Armenise S, Castaldo V et al (1997) Freezing gait in Parkinson’s disease. Eur Neurol 38(4):297–301CrossRef Lamberti P, Armenise S, Castaldo V et al (1997) Freezing gait in Parkinson’s disease. Eur Neurol 38(4):297–301CrossRef
15.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG, The Prisma Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLOS Med 6(7):e1000097CrossRef Moher D, Liberati A, Tetzlaff J, Altman DG, The Prisma Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLOS Med 6(7):e1000097CrossRef
16.
go back to reference Nyaga VN, Arbyn M, Aerts M (2014) Metaprop: a Stata command to perform meta-analysis of binomial data. Arch Public Health 72:39CrossRef Nyaga VN, Arbyn M, Aerts M (2014) Metaprop: a Stata command to perform meta-analysis of binomial data. Arch Public Health 72:39CrossRef
17.
go back to reference Giladi N, Tal J, Azulay T et al (2009) Validation of the freezing of gait questionnaire in patients with Parkinson’s disease. Mov Disord 24(5):655–661CrossRef Giladi N, Tal J, Azulay T et al (2009) Validation of the freezing of gait questionnaire in patients with Parkinson’s disease. Mov Disord 24(5):655–661CrossRef
18.
go back to reference Fahn S, E.R., Members of the UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M (eds) Recent developments in Parkinson’s disease, vol 2. Macmillan Health Care Information, Florham Park, pp 153–163 Fahn S, E.R., Members of the UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M (eds) Recent developments in Parkinson’s disease, vol 2. Macmillan Health Care Information, Florham Park, pp 153–163
19.
go back to reference Nieuwboer A, Rochester L, Herman T et al (2009) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture 30(4):459–463CrossRef Nieuwboer A, Rochester L, Herman T et al (2009) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture 30(4):459–463CrossRef
20.
go back to reference Kim YE, Jeon B, Yun JY, Yang HJ, Kim HJ (2019) Chronological view of peak and diphasic dyskinesia, wearing off and freezing of gait in parkinson’s disease. J Parkinsons Dis 9(4):741–747CrossRef Kim YE, Jeon B, Yun JY, Yang HJ, Kim HJ (2019) Chronological view of peak and diphasic dyskinesia, wearing off and freezing of gait in parkinson’s disease. J Parkinsons Dis 9(4):741–747CrossRef
21.
go back to reference G.B.D. Parkinson’s Disease Collaborators (2018) Global, regional, and national burden of Parkinson’s disease, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 17(11):939–953CrossRef G.B.D. Parkinson’s Disease Collaborators (2018) Global, regional, and national burden of Parkinson’s disease, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 17(11):939–953CrossRef
22.
go back to reference Elbaz A, Bower JH, Maraganore DM et al (2002) Risk tables for parkinsonism and Parkinson’s disease. J Clin Epidemiol 55(1):25–31CrossRef Elbaz A, Bower JH, Maraganore DM et al (2002) Risk tables for parkinsonism and Parkinson’s disease. J Clin Epidemiol 55(1):25–31CrossRef
23.
go back to reference Goldman SM, Tanner CM, Olanow CW, Watts RL, Field RD, Langston JW (2005) Occupation and parkinsonism in three movement disorders clinics. Neurology 65(9):1430–1435CrossRef Goldman SM, Tanner CM, Olanow CW, Watts RL, Field RD, Langston JW (2005) Occupation and parkinsonism in three movement disorders clinics. Neurology 65(9):1430–1435CrossRef
24.
go back to reference Willis AW, Schootman M, Evanoff BA, Perlmutter JS, Racette BA (2011) Neurologist care in Parkinson disease: a utilization, outcomes, and survival study. Neurology 77(9):851–857CrossRef Willis AW, Schootman M, Evanoff BA, Perlmutter JS, Racette BA (2011) Neurologist care in Parkinson disease: a utilization, outcomes, and survival study. Neurology 77(9):851–857CrossRef
25.
go back to reference Abraham DS, Gruber-Baldini AL, Magder LS et al (2019) Sex differences in Parkinson’s disease presentation and progression. Parkinsonism Relat Disord 69:48–54CrossRef Abraham DS, Gruber-Baldini AL, Magder LS et al (2019) Sex differences in Parkinson’s disease presentation and progression. Parkinsonism Relat Disord 69:48–54CrossRef
26.
go back to reference Scott B, Borgman A, Engler H, Johnels B, Aquilonius SM (2000) Gender differences in Parkinson’s disease symptom profile. Acta Neurol Scand 102(1):37–43CrossRef Scott B, Borgman A, Engler H, Johnels B, Aquilonius SM (2000) Gender differences in Parkinson’s disease symptom profile. Acta Neurol Scand 102(1):37–43CrossRef
27.
go back to reference Tosserams A, Araujo R, Pringsheim T et al (2018) Underrepresentation of women in Parkinson’s disease trials. Mov Disord 33(11):1825–1826CrossRef Tosserams A, Araujo R, Pringsheim T et al (2018) Underrepresentation of women in Parkinson’s disease trials. Mov Disord 33(11):1825–1826CrossRef
28.
go back to reference Duma N, Vera Aguilera J, Paludo J et al (2018) Representation of minorities and women in oncology clinical trials: review of the past 14 Years. J Oncol Pract 14(1):e1–e10CrossRef Duma N, Vera Aguilera J, Paludo J et al (2018) Representation of minorities and women in oncology clinical trials: review of the past 14 Years. J Oncol Pract 14(1):e1–e10CrossRef
29.
go back to reference Nguyen QD, Peters E, Wassef A, Desmarais P, Remillard-Labrosse D, Tremblay-Gravel M (2018) Evolution of age and female representation in the most-cited randomized controlled trials of cardiology of the last 20 years. Circ Cardiovasc Qual Outcomes 11(6):e004713CrossRef Nguyen QD, Peters E, Wassef A, Desmarais P, Remillard-Labrosse D, Tremblay-Gravel M (2018) Evolution of age and female representation in the most-cited randomized controlled trials of cardiology of the last 20 years. Circ Cardiovasc Qual Outcomes 11(6):e004713CrossRef
30.
go back to reference Geller SE, Koch A, Pellettieri B, Carnes M (2011) Inclusion, analysis, and reporting of sex and race/ethnicity in clinical trials: have we made progress? J Womens Health (Larchmt) 20(3):315–320CrossRef Geller SE, Koch A, Pellettieri B, Carnes M (2011) Inclusion, analysis, and reporting of sex and race/ethnicity in clinical trials: have we made progress? J Womens Health (Larchmt) 20(3):315–320CrossRef
Metadata
Title
Sex and freezing of gait in Parkinson’s disease: a systematic review and meta-analysis
Authors
Anouk Tosserams
Masood Mazaheri
Priya Vart
Bastiaan R. Bloem
Jorik Nonnekes
Publication date
01-01-2021
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 1/2021
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-020-10117-w

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