Top

Published in:

Open Access 28-08-2022 | Parkinson's Disease | Research Article

Burden of caregiving for cardiovascular dysautonomia in Parkinson’s disease

Authors: Claudia Ledda, Elisa Montanaro, Gabriele Imbalzano, Aristide Merola, Ilaria Bruno, Carlo Alberto Artusi, Maurizio Zibetti, Mario Giorgio Rizzone, Marco Bozzali, Gabriele Sobrero, Fabrizio Vallelonga, Simona Maule, Leonardo Lopiano, Alberto Romagnolo

Published in: Clinical Autonomic Research | Issue 6/2022

Abstract

Purpose

We sought to estimate the impact of cardiovascular autonomic neuropathy (cAN) on informal caregivers of patients with Parkinson’s disease (PD), defined as individuals providing regular care to a friend, partner, or family member with PD, and to evaluate the mutual relationship between caregiver burden and patient health-related quality of life (HRQoL).

Methods

We enrolled 36 consecutive patients with PD and their informal caregivers. Patients underwent a detailed motor, autonomic, cognitive, and functional assessment. Caregivers were assessed using the Zarit Burden Interview (ZBI). Differences in caregiver burden, expressed by the ZBI score, and strength of association between caregiver burden, cAN, and HRQoL were assessed using analysis of covariance (ANCOVA), logistic regression, and linear regression analyses. Analyses were adjusted for patients’ age, PD duration, and motor and cognitive disability, as well as caregivers’ age.

Results

Moderate-severe caregiver burden was reported in 41.7% of PDcAN⁺ versus 8.7% of PDcAN⁻ (p < 0.001). The ZBI score was increased in PDcAN⁺ versus PDcAN⁻ (31.5 ± 3.4 versus 15.2 ± 2.3; p < 0.001), with tenfold higher odds (p = 0.012) of moderate-severe caregiver burden in PDcAN⁺, even after adjusting for potential confounders. The ZBI score correlated with cAN severity (p = 0.005), global autonomic impairment (p = 0.012), and HRQoL impairment (p < 0.001).

Conclusion

These results highlight the significant impact of cAN on PD caregivers and the need for targeted interventions addressing this frequently overlooked and insufficiently treated source of nonmotor disability in PD.

Jain S, Goldstein DS (2012) Cardiovascular dysautonomia in Parkinson disease: from pathophysiology to pathogenesis. Neurobiol Dis 46(3):572–580. https://doi.org/10.1016/j.nbd.2011.10.025CrossRefPubMed

Merola A, Romagnolo A, Rosso M, Suri R, Berndt Z, Maule S, Lopiano L, Espay AJ (2018) Autonomic dysfunction in Parkinson’s disease: a prospective cohort study. Mov Disord 33(3):391–397. https://doi.org/10.1002/mds.27268CrossRefPubMed

Merola A, Romagnolo A, Comi C, Rosso M, Artusi CA, Zibetti M, Lanotte M, Duker AP, Maule S, Lopiano L, Espay AJ (2017) Prevalence and burden of dysautonomia in advanced Parkinson’s disease. Mov Disord 32:796–797. https://doi.org/10.1002/mds.26970CrossRefPubMed

Romagnolo A, Zibetti M, Merola A, Canova D, Sarchioto M, Montanaro E, Artusi CA, Vallelonga F, Maule S, Lopiano L (2019) Cardiovascular autonomic neuropathy and falls in Parkinson disease: a prospective cohort study. J Neurol 266(1):85–91. https://doi.org/10.1007/s00415-018-9104-4CrossRefPubMed

Kotagal V, Lineback C, Bohnen NI, Albin RL, CALM-PD Parkinson Study Group Investigators (2016) Orthostatic hypotension predicts motor decline in early Parkinson disease. Parkinsonism Relat Disord 32:127–129. https://doi.org/10.1016/j.parkreldis.2016.09.011CrossRefPubMedPubMedCentral

Longardner K, Bayram E, Litvan I (2020) Orthostatic hypotension is associated with cognitive decline in Parkinson disease. Front Neurol 11:897. https://doi.org/10.3389/fneur.2020.00897CrossRefPubMedPubMedCentral

Goldstein DS, Holmes C, Sharabi Y, Wu T (2015) Survival in synucleinopathies: a prospective cohort study. Neurology 85(18):1554–61. https://doi.org/10.1212/WNL.0000000000002086CrossRefPubMedPubMedCentral

Pilotto A, Romagnolo A, Tuazon JA, Vizcarra JA, Marsili L, Zibetti M, Rosso M, Rodriguez-Porcel F, Borroni B, Rizzetti MC, Rossi C, Vizcarra-Escobar D, Molano JR, Lopiano L, Ceravolo R, Masellis M, Espay AJ, Padovani A, Merola A (2019) Orthostatic hypotension and REM sleep behaviour disorder: impact on clinical outcomes in α-synucleinopathies. J Neurol Neurosurg Psychiatry 90(11):1257–1263. https://doi.org/10.1136/jnnp-2019-320846CrossRefPubMed

Merola A, Sawyer RP, Artusi CA, Suri R, Berndt Z, Lopez-Castellanos JR, Vaughan J, Vizcarra JA, Romagnolo A, Espay AJ (2018) Orthostatic hypotension in Parkinson disease: impact on health care utilization. Parkinsonism Relat Disord 47:45–49. https://doi.org/10.1016/j.parkreldis.2017.11.344CrossRefPubMed

10.

Pilotto A, Romagnolo A, Scalvini A, Masellis M, Shimo Y, Bonanni L, Camicioli R, Wang LL, Dwivedi AK, Longardner K, Rodriguez-Porcel F, DiFrancesco M, Vizcarra JA, Montanaro E, Maule S, Lupini A, Ojeda-López C, Black SE, Delli Pizzi S, Gee M, Tanaka R, Yamashiro K, Hatano T, Borroni B, Gasparotti R, Rizzetti MC, Hattori N, Lopiano L, Litvan I, Espay AJ, Padovani A, Merola A (2021) Association of orthostatic hypotension with cerebral atrophy in patients with Lewy body disorders. Neurology 97(8):e814–e824. https://doi.org/10.1212/WNL.0000000000012342CrossRefPubMedPubMedCentral

11.

Claassen DO, Adler CH, Hewitt LA, Gibbons C (2018) Characterization of the symptoms of neurogenic orthostatic hypotension and their impact from a survey of patients and caregivers. BMC Neurol 18(1):125. https://doi.org/10.1186/s12883-018-1129-xCrossRefPubMedPubMedCentral

12.

Grün D, Pieri V, Vaillant M, Diederich NJ (2016) Contributory factors to caregiver burden in Parkinson disease. J Am Med Dir Assoc 17(7):626–32. https://doi.org/10.1016/j.jamda.2016.03.004CrossRefPubMed

13.

Martínez-Martín P, Forjaz MJ, Frades-Payo B, Rusiñol AB, Fernández-García JM, Benito-León J, Arillo VC, Barberá MA, Sordo MP, Catalán MJ (2007) Caregiver burden in Parkinson’s disease. Mov Disord 22(7):924–31. https://doi.org/10.1002/mds.21355CrossRefPubMed

14.

Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, Obeso J, Marek K, Litvan I, Lang AE, Halliday G, Goetz CG, Gasser T, Dubois B, Chan P, Bloem BR, Adler CH, Deuschl G (2015) MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 30(12):1591–601. https://doi.org/10.1002/mds.26424CrossRefPubMed

15.

Freeman R (2005) Autonomic peripheral neuropathy. Lancet 365(9466):1259–1270. https://doi.org/10.1016/S0140-6736(05)74815-7CrossRefPubMed

16.

Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N, Movement Disorder Society UPDRS Revision Task Force (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23(15):2129–70. https://doi.org/10.1002/mds.22340CrossRefPubMed

17.

Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4):695–9. https://doi.org/10.1111/j.1532-5415.2005.53221.xCrossRefPubMed

18.

Dalrymple-Alford JC, MacAskill MR, Nakas CT, Livingston L, Graham C, Crucian GP, Melzer TR, Kirwan J, Keenan R, Wells S, Porter RJ, Watts R, Anderson TJ (2010) The MoCA: well-suited screen for cognitive impairment in Parkinson disease. Neurology 75(19):1717–25. https://doi.org/10.1212/WNL.0b013e3181fc29c9CrossRefPubMed

19.

Peto V, Jenkinson C, Fitzpatrick R (1998) PDQ-39: a review of the development, validation and application of a Parkinson’s disease quality of life questionnaire and its associated measures. J Neurol 245(Suppl 1):S10-4. https://doi.org/10.1007/pl00007730CrossRefPubMed

20.

Visser M, Marinus J, Stiggelbout AM, Van Hilten JJ (2004) Assessment of autonomic dysfunction in Parkinson’s disease: the SCOPA-AUT. Mov Disord 19(11):1306–12. https://doi.org/10.1002/mds.20153CrossRefPubMed

21.

Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–53. https://doi.org/10.1002/mds.23429CrossRefPubMed

22.

Low PA, Tomalia VA, Park KJ (2013) Autonomic function tests: some clinical applications. J Clin Neurol 9(1):1–8. https://doi.org/10.3988/jcn.2013.9.1.1CrossRefPubMedPubMedCentral

23.

Lahrmann H, Cortelli P, Hilz M, Mathias CJ, Struhal W, Tassinari M (2006) EFNS guidelines on the diagnosis and management of orthostatic hypotension. Eur J Neurol 13(9):930–6. https://doi.org/10.1111/j.1468-1331.2006.01512.xCrossRefPubMed

24.

Zarit SH, Reever KE, Bach-Peterson J (1980) Relatives of the impaired elderly: correlates of feelings of burden. Gerontologist 20(6):649–55. https://doi.org/10.1093/geront/20.6.649CrossRefPubMed

25.

Arnao V, Cinturino A, Valentino F, Perini V, Mastrilli S, Bellavia G, Savettieri G, Realmuto S, D’Amelio M (2015) In patient’s with Parkinson disease, autonomic symptoms are frequent and associated with other non-motor symptoms. Clin Auton Res 25(5):30–17. https://doi.org/10.1007/s10286-015-0306-xCrossRef

26.

Bhimani R (2014) Understanding the burden on caregivers of people with Parkinson’s: a scoping review of the literature. Rehabil Res Pract. https://doi.org/10.1155/2014/718527CrossRefPubMedPubMedCentral

27.

D’Amelio M, Terruso V, Palmeri B, Di Benedetto N, Famoso G, Cottone P, Aridon P, Ragonese P, Savettieri G (2009) Predictors of caregiver burden in partners of patients with Parkinson’s disease. Neurol Sci 30(2):171–4. https://doi.org/10.1007/s10072-009-0024-zCrossRefPubMed

28.

Carter JH, Stewart BJ, Lyons KS, Archbold PG (2008) Do motor and nonmotor symptoms in PD patients predict caregiver strain and depression? Mov Disord 23(9):1211–6. https://doi.org/10.1002/mds.21686CrossRefPubMed

29.

Adelman RD, Tmanova LL, Delgado D, Dion S, Lachs MS (2014) Caregiver burden: a clinical review. JAMA 311(10):1052–1060. https://doi.org/10.1001/jama.2014.304CrossRefPubMed

30.

Ransmayr G (2021) Challenges of caregiving to neurological patients. Herausforderungen in der Betreuung und Pflege neurologischer Patientinnen und Patienten. Wien Med Wochenschr 171(11–12):282–288. https://doi.org/10.1007/s10354-021-00844-8CrossRefPubMedPubMedCentral

31.

Hagedoorn M, Sanderman R, Buunk BP, Wobbes T (2002) Failing in spousal caregiving: the “identity-relevant stress” hypothesis to explain sex differences in caregiver distress. Br J Health Psychol 7:481–494. https://doi.org/10.1348/135910702320645435CrossRefPubMed

32.

Dowding CH, Shenton CL, Salek SS (2006) A review of the health-related quality of life and economic impact of Parkinson’s disease. Drugs Aging 23(9):693–721. https://doi.org/10.2165/00002512-200623090-00001CrossRefPubMed

33.

Kelly DH, McGinley JL, Huxham FE, Menz HB, Watts JJ, Iansek R, Murphy AT, Danoudis M, Adair B, Morris ME (2012) Health-related quality of life and strain in caregivers of Australians with Parkinson’s disease: an observational study. BMC Neurol 12:57. https://doi.org/10.1186/1471-2377-12-57CrossRefPubMedPubMedCentral

Title: Burden of caregiving for cardiovascular dysautonomia in Parkinson’s disease
Authors: Claudia Ledda
Elisa Montanaro
Gabriele Imbalzano
Aristide Merola
Ilaria Bruno
Carlo Alberto Artusi
Maurizio Zibetti
Mario Giorgio Rizzone
Marco Bozzali
Gabriele Sobrero
Fabrizio Vallelonga
Simona Maule
Leonardo Lopiano
Alberto Romagnolo
Publication date: 28-08-2022
Publisher: Springer Berlin Heidelberg
Keyword: Parkinson's Disease
Published in: Clinical Autonomic Research / Issue 6/2022
Print ISSN: 0959-9851
Electronic ISSN: 1619-1560
DOI: https://doi.org/10.1007/s10286-022-00888-9

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Burden of caregiving for cardiovascular dysautonomia in Parkinson’s disease

Abstract

Purpose

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 6/2022

Utricular dysfunction in patients with orthostatic hypotension

Imaging in autonomic failure: a window into real-time physiological mechanisms and other updates on recent autonomic research

Comment to the article titled: “Autonomic nervous system function in women with anorexia nervosa” by Jenkins and coll

Self-recorded heart rate variability profiles are associated with health and lifestyle markers in young adults

Does exercise training still augment the heart rate variability of contemporary treated heart failure patients?

Correction to: Faintly tired: a systematic review of fatigue in patients with orthostatic syncope