Clinical Usefulness of Retropulsion Tests in Persons with Mild to Moderate Parkinson’s Disease
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Study Design
2.3. Participants
2.4. Assessments and Procedure
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Allen, N.E.; Schwarzel, A.K.; Canning, C.G. Recurrent Falls in Parkinson’s Disease: A Systematic Review. Parkinsons Dis. 2013, 2013, 906274. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Almeida, L.R.; Sherrington, C.; Allen, N.E.; Paul, S.S.; Valenca, G.T.; Oliveira-Filho, J.; Canning, C.G. Disability is an Independent Predictor of Falls and Recurrent Falls in People with Parkinson’s Disease Without a History of Falls: A One-Year Prospective Study. J. Parkinson’s Dis. 2015, 5, 855–864. [Google Scholar] [CrossRef] [PubMed]
- Gazibara, T.; Tepavcevic, D.K.; Svetel, M.; Tomic, A.; Stankovic, I.; Kostic, V.S.; Pekmezovic, T. Recurrent falls in Parkinson’s disease after one year of follow-up: A nested case-control study. Arch. Gerontol. Geriatr. 2016, 65, 17–24. [Google Scholar] [CrossRef] [PubMed]
- Gazibara, T.; Tepavcevic, D.K.; Svetel, M.; Tomic, A.; Stankovic, I.; Kostic, V.S.; Pekmezovic, T. Near-falls in people with Parkinson’s disease: Circumstances, contributing factors and association with falling. Clin. Neurol. Neurosurg. 2017, 161, 51–55. [Google Scholar] [CrossRef] [PubMed]
- Lindholm, B.; Hagell, P.; Hansson, O.; Nilsson, M.H. Prediction of Falls and/or Near Falls in People with Mild Parkinson’s Disease. PLoS ONE 2015, 10, e0117018. [Google Scholar] [CrossRef] [PubMed]
- Jonasson, S.B.; Nilsson, M.H.; Lexell, J. Psychometric properties of four fear of falling rating scales in people with Parkinson’s disease. BMC Geriatr. 2014, 14, 66. [Google Scholar] [CrossRef] [Green Version]
- Stack, E.; Ashburn, A. Fall events described by people with Parkinson’s disease: Implications for clinical interviewing and the research agenda. Physiother. Res. Int. 1999, 4, 190–200. [Google Scholar] [CrossRef] [PubMed]
- Huxham, F.E.; Goldie, P.A.; Patla, A.E. Theoretical considerations in balance assessment. Aust. J. Physiother. 2001, 47, 89–100. [Google Scholar] [CrossRef] [Green Version]
- Błaszczyk, J.W.; Orawiec, R.; Duda-Kłodowska, D.; Opala, G. Assessment of postural instability in patients with Parkinson’s disease. Exp. Brain Res. 2007, 183, 107–114. [Google Scholar] [CrossRef]
- Ashburn, A.; Stack, E.; Ballinger, C.; Fazakarley, L.; Fitton, C. The circumstances of falls among people with Parkinson’s disease and the use of Falls Diaries to facilitate reporting. Disabil. Rehabil. 2008, 30, 1205–1212. [Google Scholar] [CrossRef]
- Gazibara, T.; Pekmezovic, T.; Tepavcevic, D.K.; Tomic, A.; Stankovic, I.; Kostic, V.S.; Svetel, M. Circumstances of falls and fall-related injuries among patients with Parkinson’s disease in an outpatient setting. Geriatr. Nurs. 2014, 35, 364–369. [Google Scholar] [CrossRef] [PubMed]
- Winter, D.A. Human balance and posture control during standing and walking. Gait Posture 1995, 3, 193–214. [Google Scholar] [CrossRef]
- Nutt, J.; Hammerstad, J.; Gancher, S. Diagnosis: Is it Parkinsonism? Major Symptoms and Signs of the Disorder. In Parkinson’s Disease: 100 Maxims; Edward Arnold: London, UK, 1992; pp. 3–9. [Google Scholar]
- Visser, M.; Marinus, J.; Bloem, B.R.; Kisjes, H.; Berg, B.M.V.D.; van Hilten, J.J. Clinical tests for the evaluation of postural instability in patients with parkinson’s disease. Arch. Phys. Med. Rehabil. 2003, 84, 1669–1674. [Google Scholar] [CrossRef]
- Jacobs, J.V.; Earhart, G.M.; McNeely, M.E. Can postural instability tests improve the prediction of future falls in people with Parkinson’s disease beyond knowing existing fall history? J. Neurol. 2015, 263, 133–139. [Google Scholar] [CrossRef]
- Horak, F.B.; Dimitrova, D.; Nutt, J.G. Direction-specific postural instability in subjects with Parkinson’s disease. Exp. Neurol. 2005, 193, 504–521. [Google Scholar] [CrossRef] [PubMed]
- Fahn, S.; Elton, R.; UPDRS Development Committee. Unified Parkinson’s Disease Rating Scale. In Recent Developments in Parkinson’s Disease; McMillan Healthcare Information: Florham Park, NJ, USA, 1987; pp. 153–163, 293–304. [Google Scholar]
- Valkovič, P.; Brožová, H.; Bötzel, K.; Růžička, E.; Benetin, J. Push and release test predicts better Parkinson fallers and nonfallers than the pull test: Comparison in OFF and ON medication states. Mov. Disord. Off. J. Mov. Disord. Soc. 2008, 23, 1453–1457. [Google Scholar] [CrossRef] [PubMed]
- Bewick, V.; Cheek, L.; Ball, J. Statistics review 13: Receiver operating characteristic curves. Crit. Care 2004, 8, 508–512. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Loong, T.-W. Understanding sensitivity and specificity with the right side of the brain. BMJ 2003, 327, 716–719. [Google Scholar] [CrossRef] [PubMed]
- Akobeng, A.K. Understanding diagnostic tests 1: Sensitivity, specificity and predictive values. Acta Paediatr. 2007, 96, 338–341. [Google Scholar] [CrossRef]
- Akobeng, A.K. Understanding diagnostic tests 2: Likelihood ratios, pre- and post-test probabilities and their use in clinical practice. Acta Paediatr. 2007, 96, 487–491. [Google Scholar] [CrossRef]
- Hughes, A.J.; Daniel, S.E.; Kilford, L.; Lees, A.J. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: A clinico-pathological study of 100 cases. J. Neurol. Neurosurg. Psychiatry 1992, 55, 181–184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoehn, M.M.; Yahr, M.D. Parkinsonism: Onset, progression, and mortality. Neurology 2001, 57, 11–26. [Google Scholar]
- Folstein, M.F.; Folstein, S.E.; McHugh, P.R. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975, 12, 189–198. [Google Scholar] [CrossRef]
- Goetz, C.G.; Stebbins, G.T.; Chmura, T.A.; Fahn, S.; Klawans, H.L.; Marsden, C.D. Teaching tape for the motor section of the unified Parkinson’s disease rating scale. Mov. Disord. Off. J. Mov. Disord. Soc. 1995, 10, 263–266. [Google Scholar] [CrossRef] [PubMed]
- Lamb, S.E.; Jã¸rstad-Stein, E.C.; Hauer, K.; Becker, C.; Prevention of Falls Network Europe and Outcomes Consensus Group. Development of a Common Outcome Data Set for Fall Injury Prevention Trials: The Prevention of Falls Network Europe Consensus. J. Am. Geriatr. Soc. 2005, 53, 1618–1622. [Google Scholar] [CrossRef] [PubMed]
- Gray, P.; Hildebrand, K. Fall risk factors in Parkinson’s disease. J. Neurosci. Nurs. 2000, 32, 222–228. [Google Scholar] [CrossRef] [PubMed]
- Tomlinson, C.L.; Stowe, R.; Patel, S.; Rick, C.; Gray, R.; Clarke, C.E. Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov. Disord. 2010, 25, 2649–2653. [Google Scholar] [CrossRef]
- Abramson, J.H. WINPEPI updated: Computer programs for epidemiologists, and their teaching potential. Epidemiol. Perspect. Innov. 2011, 8, 1. [Google Scholar] [CrossRef] [Green Version]
- Jacobs, J.V.; Horak, F.B.; Tran, V.K.; Nutt, J.G. Multiple balance tests improve the assessment of postural stability in subjects with Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 2006, 77, 322–326. [Google Scholar] [CrossRef] [Green Version]
- Nonnekes, J.; Goselink, R.; Weerdesteyn, V.; Bloem, B.R. The retropulsion test: A good evaluation of postural instability in Parkinson’s disease? J. Parkinson’s Dis. 2015, 5, 43–47. [Google Scholar] [CrossRef] [PubMed]
- van der Marck, M.A.; Klok, M.P.C.; Okun, M.S.; Giladi, N.; Munneke, M.; Bloem, B.R.; Force, N.F.T. Consensus-based clinical practice recommendations for the examination and management of falls in patients with Parkinson’s disease. Parkinsonism Relat. Disord. 2014, 20, 360–369. [Google Scholar] [CrossRef]
- Segev-Jacubovski, O.; Herman, T.; Yogev-Seligmann, G.; Mirelman, A.; Giladi, N.; Hausdorff, J.M. The interplay between gait, falls and cognition: Can cognitive therapy reduce fall risk? Expert Rev. Neurother. 2011, 11, 1057–1075. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paul, S.S.; Canning, C.G.; Sherrington, C.; Lord, S.R.; Close, J.C.; Fung, V.S. Three simple clinical tests to accurately predict falls in people with Parkinson’s disease. Mov. Disord. 2013, 28, 655–662. [Google Scholar] [CrossRef] [PubMed]
- Duncan, R.P.; Cavanaugh, J.T.; Earhart, G.M.; Ellis, T.D.; Ford, M.P.; Foreman, K.B.; Leddy, A.L.; Paul, S.S.; Canning, C.G.; Thackeray, A.; et al. External validation of a simple clinical tool used to predict falls in people with Parkinson disease. Parkinsonism Relat. Disord. 2015, 21, 960–963. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lindholm, B.; Nilsson, M.H.; Hansson, O.; Hagell, P. External validation of a 3-step falls prediction model in mild Parkinson’s disease. J. Neurol. 2016, 263, 2462–2469. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lindholm, B.; Brogårdh, C.; Odin, P.; Hagell, P. Longitudinal prediction of falls and near falls frequencies in Parkinson’s disease: A prospective cohort study. J. Neurol. 2021, 268, 997–1005. [Google Scholar] [CrossRef]
- Bloem, B.R.; Grimbergen, Y.A.; Cramer, M.; Willemsen, M.; Zwinderman, A.H. Prospective assessment of falls in Parkinson’s disease. J. Neurol. 2001, 248, 950–958. [Google Scholar] [CrossRef]
- Sipp, A.R.; Rowley, B.A. Detection of baseline and near-fall postural stability. In Proceedings of the 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Vancouver, BC, Canada, 20–25 October 2008; pp. 1262–1265. [Google Scholar]
- Srygley, J.M.; Herman, T.; Giladi, N.; Hausdorff, J.M. Self-Report of Missteps in Older Adults: A Valid Proxy of Fall Risk? Arch. Phys. Med. Rehabil. 2009, 90, 786–792. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Teno, J.; Kiel, D.; Mor, V. Multiple Stumbles: A Risk Factor for Falls in Community-Dwelling Elderly; A Prospective Study. J. Am. Geriatr. Soc. 1990, 38, 1321–1325. [Google Scholar] [CrossRef]
- Lee, J.K.; Robinovitch, S.; Park, E.J. Inertial Sensing-Based Pre-Impact Detection of Falls Involving Near-Fall Scenarios. IEEE Trans. Neural Syst. Rehabil. Eng. 2015, 23, 258–266. [Google Scholar] [CrossRef]
- Stack, E.; King, R.; Janko, B.; Burnett, M.; Hammersley, N.; Agarwal, V.; Hannuna, S.; Burrows, A.; Ashburn, A. Could In-Home Sensors Surpass Human Observation of People with Parkinson’s at High Risk of Falling? An Ethnographic Study. BioMed Res. Int. 2016, 2016, 3703745. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hansson, E.E.; Tornberg, Å. Coherence and reliability of a wearable inertial measurement unit for measuring postural sway. BMC Res. Notes 2019, 12, 201. [Google Scholar]
- Kerr, G.K.; Worringham, C.J.; Cole, M.H.; Lacherez, P.F.; Wood, J.M.; Silburn, P.A. Predictors of future falls in Parkinson disease. Neurology 2010, 75, 116–124. [Google Scholar] [CrossRef] [PubMed]
- Pickering, R.M.; Grimbergen, Y.A.; Rigney, U.; Ashburn, A.; Mazibrada, G.; Wood, B.; Gray, P.; Kerr, G.; Bloem, B.R. A meta-analysis of six prospective studies of falling in Parkinson’s disease. Mov. Disord. 2007, 22, 1892–1900. [Google Scholar] [CrossRef] [PubMed]
Time 1 (n = 146) | Time 2 (n = 58) | |
---|---|---|
Age (years), mean (SD; min–max) | 68 (9.6; 35–80) | 69 (8.9; 46–84) |
Female gender, n (%) | 67 (46) | 32 (55) |
PD duration (years), mean (SD; min–max) | 4.0 (3.9; 0.1–17.0) | 7.0 (3.7; 3.6–20) |
PD severity (HY), median (q1–q3; min–max) | 2 (2–3; 1–4) | 2 (2–3; 1–4) |
Daily total levodopa equivalent (LDE) dose (mg), median (q1–q3; min–max) | 400 (300−600; 0–1477) | 500 (400–675; 150–1580) |
Self-rated motor status at the time of clinical examination “on” or “on with dyskinesias,” n (%) “off,” n (%) | 128 (88) 18 (12) | 48 (83) 10 (17) |
Motor symptoms (UPDRS part III), median (q1–q3; min–max) | 12 (8–18; 1–46) | 13.5 (9–20; 1–40) |
Cognition (MMSE), median (q1–q3; min–max) | 28 (26–29; 19–30) | 28 (27–29; 20–30) |
Retropulsion (NRT), median (q1–q3; min–max) | 0 (0–1; 0–2) | 0 (0–1; 0–3) |
Retropulsion (UPDRS30), median (q1–q3; min–max) | 0 (0–1; 0–2) | 0 (0–1; 0–3) |
p-Value for ROC Analysis | Cut-Off Score | Sens (95% CI) | Spec (95% CI) | YI (95% CI) | PPV (95% CI) | NPV (95% CI) | LR+ (95% CI) | LR− (95% CI) | |
---|---|---|---|---|---|---|---|---|---|
Golden standard: falls (prevalence, 32%) | |||||||||
NRT (0–3) 1 | <0.001 | 1 | 0.47 (0.33–0.61) | 0.85 (0.77–0.10) | 0.32 (0.16–0.48) | 0.60 (0.46–0.72) | 0.77 (0.72–0.82) | 3.09 (1.77–5.39) | 0.63 (0.47–0.83) |
2 | 0.34 (0.22–0.48) | 0.96 (0.90–0.98) | 0.30 (0.16–0.44) | 0.80 (0.60–0.91) | 0.75 (0.71–0.91) | 8.43 (2.98–23.82) | 0.69 (0.56–0.82) | ||
UPDRS i 30 (0–4) 2 | 0.010 | 1 | 0.51 (0.37–0.65) | 0.70 (0.60–0.78) | 0.21 (0.04–0.38) | 0.44 (0.35–0.55) | 0.75 (0.69–0.83) | 1.69 (1.12–2.54) | 0.70 (0.51–0.97) |
2 | 0.19 (0.10–0.34) | 0.95 (0.89–0.98) | 0.14 (0.02–0.26) | 0.64 (0.40–0.83) | 0.71 (0.68–0.74) | 3.79 (1.34–10.69) | 0.85 (0.74–0.99) | ||
Golden standard: falls and/or near falls (prevalence, 46%) | |||||||||
NRT (0–3) 1 | 0.001 | 1 | 0.40 (0.29–0.52) | 0.87 (0.78–0.93) | 0.28 (0.14–0.41) | 0.73 (0.59–0.84) | 0.63 (0.58–0.68) | 3.18 (1.66–5.49) | 0.68 (0.55–0.85) |
2 | 0.25 (0.17–0.37) | 0.93 (0.89–0.99) | 0.22 (0.10–0.33) | 0.85 (0.65–0.95) | 0.60 (0.57–0.64) | 6.68 (2.05–21.82) | 0.78 (0.67–0.90) | ||
UPDRS30 (0–4) 2 | 0.005 | 1 | 0.49 (0.38–0.61) | 0.73 (0.63–0.82) | 0.23 (0.07–0.38) | 0.61 (0.50–0.71) | 0.63 (0.57–0.69) | 1.85 (1.19–2.88) | 0.69 (0.53–0.91) |
2 | 0.15 (0.08–0.25) | 0.95(0.88–0.98) | 0.10 (0.00–0.20) | 0.71 (0.46–0.88) | 0.57 (0.54–0.60) | 2.95 (0.97–8.97) | 0.90 (0.80–1.00) |
p-Value for ROC Analysis | Cut–Off Score | Sens (95% CI) | Spec (95% CI) | YI (95% CI) | PPV (95% CI) | NPV (95% CI) | LR+ (95% CI) | LR− (95% CI) | |
---|---|---|---|---|---|---|---|---|---|
Golden standard: falls (prevalence, 45%) | |||||||||
NRT (0–3) | 0.034 | 1 | 0.48 (0.30–0.67) | 0.78 (0.61–0.89) | 0.26 (0.02–0.50) | 0.63 (0.46–0.79) | 0.66 (0.56–0.75) | 2.19 (1.01–4.75) | 0.67 (0.44–1.01) |
2 | 0.23 (0.11–0.42) | 0.91 (0.77–0.98) | 0.14 (−0.05–0.33) | 0.68 (0.28–0.95) | 0.59 (0.53–0.65) | 2.46 (0.68–8.90) | 0.85 (0.67–1.08) | ||
3 | 0.08 (0.02–0.24) | 1.00 (0.89–1.00) | 0.08 (−0.03–0.18) | 1.00 (0.13–1.00) | 0.57 (0.52–0.62) | NA (0.18–NA) | 0.92 (0.83–1.03) | ||
UPDRS30 (0–4) | 0.079 | NA | |||||||
Golden standard: falls and/or near falls (prevalence, 52%) | |||||||||
NRT (0–3) | 0.043 | 1 | 0.45 (0.28–0.63) | 0.79 (0.61–0.90) | 0.23 (0.00–0.47) | 0.68 (0.50–0.83) | 0.58 (0.48–0.67) | 2.09 (0.92–4.73) | 0.70 (0.48–4.73) |
2 | 0.20 (0.10–0.37) | 0.89 (0.73–0.96) | 0.09 (−0.09–0.28) | 0.66 (0.27–0.91) | 0.51 (0.45–0.57) | 1.87 (0.52–6.76) | 0.90 (0.72–1.12) | ||
3 | 0.07 (0.02–0.21) | 1.00 (0.88–1.00) | 0.07 (−0.02–0.16) | 1.00 (0.15–1.00) | 0.50 (0.45–0.56) | NA (0.16–NA) | 0.93 (0.85–1.03) | ||
UPDRS30 (0–4) | 0.231 | NA |
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Lindholm, B.; Franzén, E.; Duzynski, W.; Odin, P.; Hagell, P. Clinical Usefulness of Retropulsion Tests in Persons with Mild to Moderate Parkinson’s Disease. Int. J. Environ. Res. Public Health 2021, 18, 12325. https://doi.org/10.3390/ijerph182312325
Lindholm B, Franzén E, Duzynski W, Odin P, Hagell P. Clinical Usefulness of Retropulsion Tests in Persons with Mild to Moderate Parkinson’s Disease. International Journal of Environmental Research and Public Health. 2021; 18(23):12325. https://doi.org/10.3390/ijerph182312325
Chicago/Turabian StyleLindholm, Beata, Erika Franzén, Wojciech Duzynski, Per Odin, and Peter Hagell. 2021. "Clinical Usefulness of Retropulsion Tests in Persons with Mild to Moderate Parkinson’s Disease" International Journal of Environmental Research and Public Health 18, no. 23: 12325. https://doi.org/10.3390/ijerph182312325
APA StyleLindholm, B., Franzén, E., Duzynski, W., Odin, P., & Hagell, P. (2021). Clinical Usefulness of Retropulsion Tests in Persons with Mild to Moderate Parkinson’s Disease. International Journal of Environmental Research and Public Health, 18(23), 12325. https://doi.org/10.3390/ijerph182312325