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Acta Neurologica Belgica

, Volume 118, Issue 2, pp 201–210 | Cite as

Parkinson’s disease and risk of hip fracture: systematic review and meta-analysis

  • Ali Hosseinzadeh
  • Malahat Khalili
  • Behnaz Sedighi
  • Sohrab Iranpour
  • Ali Akbar Haghdoost
Review
  • 71 Downloads

Abstract

The relationship between Parkinson’s disease (PD) and risk of hip fracture yielded inconsistent results. Therefore, we conducted the present systematic review and meta-analysis of published observational studies to assess the association between PD and risk of hip fracture. PubMed, ISI, EMBASE, and Cochrane databases were searched systematically to identify studies assessing the relationship between PD and the risk of hip fracture up to July 01, 2017. In addition, to find related articles, the reference section of retrieved articles was checked. Random-effects model was used for calculation of pooled hazard ratio (HR) and 95% confidence intervals (CI). Thirteen independent studies containing 564,947 participants were included in the meta-analysis. The overall results of included studies showed PD to be associated with the risk of hip fracture (HRoverall = 3.13, 95% CI 2.53–3.87) in women 3.11 (2.51–3.86) and men 2.60 (2.19–3.09). Our meta-analysis showed the direct association between PD and the risk of hip fracture in both men and women. However, due to the limitations of this study, further well-designed studies are required to confirm our findings.

Keywords

Parkinson’s disease Hip fracture Meta-analysis Risk factor 

Notes

Compliance with ethical standards

Conflict of interest

Ali Hosseinzadeh, Malahat Khalili, Behnaz Sedighi, Sohrab Iranpour, and Ali Akbar Haghdoost declare that they have no conflict of interest. The authors alone are responsible for the content and writing of this paper.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

For this type of study formal consent is not required.

References

  1. 1.
    Launer L, Berger K, Breteler M, Dartigues J, Baldereschi M, Fratiglioni L, Lobo A, Martinez-Lage J, Trenkwalder C, Hofman A (2000) Prevalence of Parkinson’s disease in Europe: a collaborative study of population-based cohorts. Neurologic Diseases in the Elderly Research Group. Neurology 54(11 Suppl 5):S21-23Google Scholar
  2. 2.
    Pringsheim T, Jette N, Frolkis A, Steeves TDL (2014) The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 29(13):1583–1590CrossRefPubMedGoogle Scholar
  3. 3.
    Burch D, Sheerin F (2005) Parkinson’s disease. Lancet 365(9459):622–627CrossRefPubMedGoogle Scholar
  4. 4.
    Johnell O, Melton Iii LJ, Atkinson EJ, O’Fallon WM, Kurland LT (1992) Fracture risk in patients with parkinsonism: a population-based study in Olmsted County, Minnesota. Age Ageing 21(1):32–38CrossRefPubMedGoogle Scholar
  5. 5.
    Johnell O, Sernbo I (1986) Health and social status in patients with hip fractures and controls. Age Ageing 15(5):285–291CrossRefPubMedGoogle Scholar
  6. 6.
    Grisso JA, Kelsey JL, Strom BL, Ghiu GY, Maislin G, O’Brien LA et al (1991) Risk factors for falls as a cause of hip fracture in women. N Engl J Med 324(19):1326–1331CrossRefPubMedGoogle Scholar
  7. 7.
    Fink HA, Kuskowski MA, Orwoll ES, Cauley JA, Ensrud KE (2005) Association between Parkinson’s disease and low bone density and falls in older men: the osteoporotic fractures in men study. J Am Geriatr Soc 53(9):1559–1564CrossRefPubMedGoogle Scholar
  8. 8.
    Sato Y, Kikuyama M, Oizumi K (1997) High prevalence of vitamin D deficiency and reduced bone mass in Parkinson’s disease. Neurology 49(5):1273–1278CrossRefPubMedGoogle Scholar
  9. 9.
    Kao CH, Chen CC, Wang SJ, Chia LG, Yeh SH (1994) Bone mineral density in patients with Parkinson’s disease measured by dual photon absorptiometry. Nucl Med Commun 15(3):173–177CrossRefPubMedGoogle Scholar
  10. 10.
    Lees AJ, Hardy J, Revesz T (2009) Parkinson’s disease. Lancet 373(9680):2055–2066CrossRefPubMedGoogle Scholar
  11. 11.
    Vaserman N (2005) Parkinson’s disease and osteoporosis. Joint Bone Spine 72:484–488CrossRefPubMedGoogle Scholar
  12. 12.
    Williams DR, Watt HC, Lees AJ (2006) Predictors of falls and fractures in bradykinetic rigid syndromes: a retrospective study. J Neurol Neurosurg Psychiatry 77(4):468–473CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Schneider JL, Fink HA, Ewing SK, Ensrud KE, Cummings SR, Study of Osteoporotic Fractures Research G (2008) The association of Parkinson’s disease with bone mineral density and fracture in older women. Osteoporos Int 19(7):1093–1097CrossRefPubMedGoogle Scholar
  14. 14.
    Taylor BC, Schreiner PJ, Stone KL, Fink HA, Cummings SR, Nevitt MC et al (2004) Long-term prediction of incident hip fracture risk in elderly white women: study of osteoporotic fractures. J Am Geriatr Soc 52(9):1479–1486CrossRefPubMedGoogle Scholar
  15. 15.
    Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 283(15):2008–2012CrossRefPubMedGoogle Scholar
  16. 16.
    Mayor S (2016) Parkinson’s disease diagnosis is preceded by increased risk of falls, study finds. BMJ 352:i695CrossRefPubMedGoogle Scholar
  17. 17.
    Kauppi M, Stenholm S, Impivaara O, Mäki J, Heliövaara M, Jula A (2014) Fall-related risk factors and heel quantitative ultrasound in the assessment of hip fracture risk: a 10-year follow-up of a nationally representative adult population sample. Osteoporos Int 25(6):1685–1695CrossRefPubMedGoogle Scholar
  18. 18.
    Pouwels S, Bazelier MT, De Boer A, Weber WEJ, Neef C, Cooper C et al (2013) Risk of fracture in patients with Parkinson’s disease. Osteoporos Int 24(8):2283–2290CrossRefPubMedGoogle Scholar
  19. 19.
    Huang Y-F, Cherng Y-G, Hsu SPC, Yeh C-C, Chou Y-C, Wu C-H et al (2015) Risk and adverse outcomes of fractures in patients with Parkinson’s disease: two nationwide studies. Osteoporos Int 26(6):1723–1732CrossRefPubMedGoogle Scholar
  20. 20.
    Melton LJ, Leibson CL, Achenbach SJ, Bower JH, Maraganore DM, Oberg AL et al (2006) Fracture risk after the diagnosis of Parkinson’s disease: influence of concomitant dementia. Mov Disord 21(9):1361–1367CrossRefPubMedGoogle Scholar
  21. 21.
    Cauley JA, Cawthon PM, Peters KE, Cummings SR, Ensrud KE, Bauer DC et al (2016) Risk factors for hip fracture in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res 31(10):1810–1819CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Chen Y-Y, Cheng P-Y, Wu S-L, Lai C-H (2012) Parkinson’s disease and risk of hip fracture: an 8-year follow-up study in Taiwan. Parkinsonism Relat Disord 18(5):506–509CrossRefPubMedGoogle Scholar
  23. 23.
    Walker RW, Chaplin A, Hancock RL, Rutherford R, Gray WK (2013) Hip fractures in people with idiopathic Parkinson’s disease: incidence and outcomes. Mov Disord 28(3):334–340CrossRefPubMedGoogle Scholar
  24. 24.
    Yamanashi A, Yamazaki K, Kanamori M, Mochizuki K, Okamoto S, Koide Y et al (2005) Assessment of risk factors for second hip fractures in Japanese elderly. Osteoporos Int 16(10):1239–1246CrossRefPubMedGoogle Scholar
  25. 25.
    Schousboe JT, Paudel ML, Taylor BC, Virnig BA, Cauley JA, Curtis JR et al (2013) Magnitude and consequences of misclassification of incident hip fractures in large cohort studies: the study of osteoporotic fractures and medicare claims data. Osteoporos Int 24(3):801–810CrossRefPubMedGoogle Scholar
  26. 26.
    Wiklund R, Toots A, Conradsson M, Olofsson B, Holmberg H, Rosendahl E et al (2016) Risk factors for hip fracture in very old people: a population-based study. Osteoporos Int 27(3):923–931CrossRefPubMedGoogle Scholar
  27. 27.
    Cauley JA, Lui L, Genant HK, Salamone L, Browner W, Fink HA et al (2009) Risk factors for severity and type of the hip fracture. J Bone Miner Res 24(5):943–955CrossRefPubMedGoogle Scholar
  28. 28.
    Abstracts of the eighteenth international congress of Parkinson’s disease and movement disorders, June 8–12, 2014, Stockholm, Sweden (2014). Mov Disord 29(Suppl 1):S1–S687Google Scholar
  29. 29.
    Olsen J, Nøhr EA, Thomsen RW, Støvring H (2013) Non-communicable disease epidemic: epidemiology in action (EuroEpi 2013 and NordicEpi 2013) Aarhus, Denmark from 11 August to 14 August 2013. Eur J Epidemiol 28:S1-270Google Scholar
  30. 30.
    Nyström H, Nordström A, Nordström P (2016) Risk of injurious fall and hip fracture up to 26 y before the diagnosis of Parkinson disease: Nested case-control studies in a nationwide cohort. PLoS Med 13(2):e1001954CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Cummings SR, Nevitt MC, Browner WS, Stone K, Fox KM, Ensrud KE et al (1995) Risk factors for hip fracture in white women. N Engl J Med 332(12):767–774CrossRefPubMedGoogle Scholar
  32. 32.
    Paul SS, Harvey L, Canning CG, Boufous S, Lord SR, Close JCT et al (2017) Fall-related hospitalization in people with Parkinson’s disease. Eur J Neurol 24(3):523–529CrossRefPubMedGoogle Scholar
  33. 33.
    Kalilani L, Asgharnejad M, Palokangas T, Durgin T (2016) Comparing the incidence of falls/fractures in Parkinson’s disease patients in the US population. PLoS One 11(9):e0161689CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Chen YY, Cheng PY, Wu SL, Lai CH (2012) Parkinson’s disease and risk of hip fracture: an 8-year follow-up study in Taiwan. Parkinsonism Relat Disord 18(5):506–509CrossRefPubMedGoogle Scholar
  35. 35.
    Stang A (2010) Critical evaluation of the Newcastle–Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605CrossRefPubMedGoogle Scholar
  36. 36.
    DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188CrossRefPubMedGoogle Scholar
  37. 37.
    Higgins J, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Higgins JPT, Green S (eds) (2011) Cochrane handbook for systematic reviews of interventions. Wiley, HobokenGoogle Scholar
  39. 39.
    Rosenthal L, Schisterman E (2010) Meta-analysis: drawing conclusions when study results vary. Methods Mol Biol 594:427–434CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101CrossRefPubMedGoogle Scholar
  42. 42.
    Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Johnson AL, Smith JJ, Smith JM, Sanzone AG (2013) Vitamin D insufficiency in patients with acute hip fractures of all ages and both sexes in a sunny climate. J Orthop Trauma 27(12):e275–e280CrossRefPubMedGoogle Scholar
  44. 44.
    Chalmers J, Conacher W, Gardner D, Scott P (1967) Osteomalacia—a common disease in elderly women. J Bone Joint Surg Br 49(3):403–423CrossRefPubMedGoogle Scholar
  45. 45.
    Feskanich D, Willett WC, Colditz GA (2003) Calcium, vitamin D, milk consumption, and hip fractures: a prospective study among postmenopausal women. Am J Clin Nutr 77(2):504–511CrossRefPubMedGoogle Scholar
  46. 46.
    Brown IRF, Bakowska A, Millard PH (1976) Vitamin D status of patients with femoral neck fractures. Age Ageing 5(3):127–131CrossRefPubMedGoogle Scholar
  47. 47.
    Wootton R, Brereton PJ, Clark MB, Hesp R, Hodkinson HM, Klenerman L et al (1979) Fractured neck of femur in the elderly: an attempt to identify patients at risk. Clin Sci 57(1):93–101CrossRefPubMedGoogle Scholar
  48. 48.
    Van Den Bos F, Speelman AD, Samson M, Munneke M, Bloem BR, Verhaar HJJ (2012) Parkinson’s disease and osteoporosis. Age Ageing 42(2):156–162PubMedGoogle Scholar
  49. 49.
    Holick MF (2007) Vitamin D deficiency. N Engl J Med 357(3):266–281CrossRefPubMedGoogle Scholar
  50. 50.
    Sato Y, Honda Y, Iwamoto J, Kanoko T, Satoh K (2005) Abnormal bone and calcium metabolism in immobilized Parkinson’s disease patients. Mov Disord 20(12):1598–1603CrossRefPubMedGoogle Scholar
  51. 51.
    Evatt ML, DeLong MR, Khazai N, Rosen A, Triche S, Tangpricha V (2008) Prevalence of vitamin D insufficiency in patients with Parkinson disease and Alzheimer disease. Arch Neurol 65(10):1348–1352CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Snow-Harter C, Bouxsein M, Lewis B, Charette S, Weinstein P, Marcus R (1990) Muscle strength as a predictor of bone mineral density in young women. J Bone Miner Res 5(6):589–595CrossRefPubMedGoogle Scholar
  53. 53.
    Blain H, Vuillemin A, Teissier A, Hanesse B, Guillemin F, Jeandel C (2001) Influence of muscle strength and body weight and composition on regional bone mineral density in healthy women aged 60 years and over. Gerontology 47(4):207–212CrossRefPubMedGoogle Scholar
  54. 54.
    Pang MYC, Eng JJ, McKay HA, Dawson AS (2005) Reduced hip bone mineral density is related to physical fitness and leg lean mass in ambulatory individuals with chronic stroke. Osteoporos Int 16(12):1769–1779CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Cano-de-la-Cuerda R, Pérez-de-Heredia M, Miangolarra-Page JC, Munoz-Hellín E, Fernández-de-las-Penas C (2010) Is there muscular weakness in Parkinson’s disease? Am J Phys Med Rehabil 89(1):70–76CrossRefPubMedGoogle Scholar
  56. 56.
    Lorefält B, Toss G, Granérus A (2007) Bone mass in elderly patients with Parkinson’s disease. Acta Neurol Scand 116(4):248–254CrossRefPubMedGoogle Scholar
  57. 57.
    Johnell O, Gullberg BO, Kanis JA, Allander E, Elffors L, Dequeker J et al (1995) Risk factors for hip fracture in European women: the MEDOS study. J Bone Miner Res 10(11):1802–1815CrossRefPubMedGoogle Scholar
  58. 58.
    van Nimwegen M, Speelman AD, Smulders K, Overeem S, Borm GF, Backx FJG et al (2010) Design and baseline characteristics of the ParkFit study, a randomized controlled trial evaluating the effectiveness of a multifaceted behavioral program to increase physical activity in Parkinson patients. BMC Neurol 10(1):70CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Sato Y, Kaji M, Tsuru T, Oizumi K (2001) Risk factors for hip fracture among elderly patients with Parkinson’s disease. J Neurol Sci 182(2):89–93CrossRefPubMedGoogle Scholar
  60. 60.
    Bikle DD (2008) Integrins, insulin like growth factors, and the skeletal response to load. Osteoporos Int 19(9):1237–1246CrossRefPubMedGoogle Scholar
  61. 61.
    Santos A, Bakker AD, Klein-Nulend J (2009) The role of osteocytes in bone mechanotransduction. Osteoporos Int 20(6):1027–1031CrossRefPubMedGoogle Scholar
  62. 62.
    Minaire P (1989) Immobilization osteoporosis: a review. Clin Rheumatol 8(2):95–103CrossRefPubMedGoogle Scholar
  63. 63.
    Wyshak G (1981) Hip fracture in elderly women and reproductive history. J Gerontol 36(4):424–427CrossRefPubMedGoogle Scholar
  64. 64.
    Smith JR (1980) Dietary and hormonal factors in bone loss. Henry Ford Hosp Med J 28(2–3):171–181PubMedGoogle Scholar
  65. 65.
    Vestergaard P, Rejnmark L, Mosekilde L (2007) Fracture risk associated with parkinsonism and anti-Parkinson drugs. Calcif Tissue Int 81(3):153–161CrossRefPubMedGoogle Scholar
  66. 66.
    Rogers JD, Sanchez-Saffon A, Frol AB, Diaz-Arrastia R (2003) Elevated plasma homocysteine levels in patients treated with levodopa: association with vascular disease. Arch Neurol 60(1):59–64CrossRefPubMedGoogle Scholar
  67. 67.
    Melton LJ (2000) Who has osteoporosis? A conflict between clinical and public health perspectives. J Bone Miner Res 15(12):2309–2314CrossRefPubMedGoogle Scholar
  68. 68.
    Garriguet D (2011) Bone health: osteoporosis, calcium and vitamin D. Health Rep 22(3):7PubMedGoogle Scholar
  69. 69.
    Dhanwal DK, Dennison EM, Harvey NC, Cooper C (2011) Epidemiology of hip fracture: worldwide geographic variation. Indian J Orthop 45(1):15CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Dhanwal D, Cooper C, Dennison E (2010)Geographic variation in osteoporotic hip fracture incidence: the growing importance of Asian influences in coming decades.J Osteoporos 2010:757102PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Belgian Neurological Society 2018

Authors and Affiliations

  • Ali Hosseinzadeh
    • 1
  • Malahat Khalili
    • 1
  • Behnaz Sedighi
    • 2
  • Sohrab Iranpour
    • 3
  • Ali Akbar Haghdoost
    • 1
  1. 1.Research Center for Modeling in Health, Institute for Future Studies in HealthKerman University of Medical SciencesKermanIran
  2. 2.Department of Neurology, Shafa HospitalKerman University of Medical ScienceKermanIran
  3. 3.Department of EpidemiologyShahid Beheshti University of Medical SciencesTehranIran

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