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Evaluation of autonomic functions of patients with multiple system atrophy and Parkinson’s disease by head-up tilt test

  • Neurology and Preclinical Neurological Studies - Original Article
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Abstract

The aim of this study was to evaluate the autonomic neural function in Parkinson’s disease (PD) and multiple system atrophy (MSA) with head-up tilt test and spectral analysis of cardiovascular parameters. This study included 15 patients with MSA, 15 patients with PD, and 29 healthy control (HC) subjects. High frequency power of the RR interval (RR-HF), the ratio of low frequency power of RR interval to RR-HF (RR-LF/HF) and LF power of systolic BP were used to evaluate parasympathetic, cardiac sympathetic and vasomotor sympathetic functions, respectively. Both patients with PD and MSA showed orthostatic hypotension and lower parasympathetic function (RR-HF) at tilt position as compared to HC subjects. Cardiac sympathetic function (RR-LF/HF) was significantly high in patients with PD than MSA at supine position. RR-LF/HF tended to increase in MSA and HC, but decreased in PD by tilting. Consequently, the change of the ratio due to tilting (ΔRR-LF/HF) was significantly lower in patients with PD than in HC subjects. Further analysis showed that compared to mild stage of PD, RR-LF/HF at the supine position was significantly higher in advanced stage. By tilting, it was increased in mild stage and decreased in the advanced stage of PD, causing ΔRR-LF/HF to decrease significantly in the advanced stage. Thus, we demonstrated that spectral analysis of cardiovascular parameters is useful to identify sympathetic and parasympathetic disorders in MSA and PD. High cardiac sympathetic function at the supine position, and its reduction by tilting might be a characteristic feature of PD, especially in the advanced stage.

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References

  • Akselrod S, Gordon D, Madwed JB, Snidman NC, Shannon DC, Cohen RJ (1985) Hemodynamic regulation: investigation by spectral analysis. Am J Physiol 249(4 Pt 2):H867–H875

    CAS  PubMed  Google Scholar 

  • Baschieri F, Calandra-Buonaura G, Doria A, Mastrolilli F, Palareti A, Barletta G, Solieri L, Guaraldi P, Martinelli P, Cortelli P (2015) Cardiovascular autonomic testing performed with a new integrated instrumental approach is useful in differentiating MSA-P from PD at an early stage. Parkinsonism Relat Disord 21(5):477–482. https://doi.org/10.1016/j.parkreldis.2015.02.011

    Article  PubMed  Google Scholar 

  • Brisinda D, Sorbo AR, Di Giacopo R, Venuti A, Bentivoglio AR, Fenici R (2014) Cardiovascular autonomic nervous system evaluation in Parkinson disease and multiple system atrophy. J Neurol Sci 336(1–2):197–202. https://doi.org/10.1016/j.jns.2013.10.039

    Article  PubMed  Google Scholar 

  • Chiaravalloti A, Stefani A, Tavolozza M, Pierantozzi M, Di Biagio D, Olivola E, Di Pietro B, Stampanoni M, Danieli R, Simonetti G, Stanzione P, Schillaci O (2012) Different patterns of cardiac sympathetic denervation in tremor-type compared to akinetic-rigid-type Parkinson’s disease: molecular imaging with 123I-MIBG. Mol Med Rep 6(6):1337–1342. https://doi.org/10.3892/mmr.2012.1104

    Article  CAS  PubMed  Google Scholar 

  • Chiaravalloti A, Stefani A, Pierantozzi M, Stanzione P, Schillaci O (2013) Does 123I-MIBG scintigraphy really assist the diagnosis of Parkinson’s disease? Parkinsonism Relat Disord 19(8):772–773. https://doi.org/10.1016/j.parkreldis.2013.04.015

    Article  PubMed  Google Scholar 

  • Chung EJ, Lee WY, Yoon WT, Kim BJ, Lee GH (2009) MIBG scintigraphy for differentiating Parkinson’s disease with autonomic dysfunction from Parkinsonism-predominant multiple system atrophy. Mov Disord 24(11):1650–1655. https://doi.org/10.1002/mds.22649

    Article  PubMed  Google Scholar 

  • Cohen J, Low P, Fealey R, Sheps S, Jiang NS (1987) Somatic and autonomic function in progressive autonomic failure and multiple system atrophy. Ann Neurol 22(6):692–699. https://doi.org/10.1002/ana.410220604

    Article  CAS  PubMed  Google Scholar 

  • Ewen S, Dorr O, Ukena C, Linz D, Cremers B, Laufs U, Hamm C, Nef H, Bauer A, Mancia G, Bohm M, Mahfoud F (2015) Blood pressure variability after catheter-based renal sympathetic denervation in patients with resistant hypertension. J Hypertens 33(12):2512–2518. https://doi.org/10.1097/HJH.0000000000000751

    Article  CAS  PubMed  Google Scholar 

  • Ewing DJ, Campbell IW, Murray A, Neilson JM, Clarke BF (1978) Immediate heart-rate response to standing: simple test for autonomic neuropathy in diabetes. Br Med J 1(6106):145–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fluckiger L, Boivin JM, Quilliot D, Jeandel C, Zannad F (1999) Differential effects of aging on heart rate variability and blood pressure variability. J Gerontol A Biol Sci Med Sci 54(5):B219–B224

    Article  CAS  PubMed  Google Scholar 

  • Friedrich C, Rudiger H, Schmidt C, Herting B, Prieur S, Junghanns S, Schweitzer K, Globas C, Schols L, Berg D, Reichmann H, Ziemssen T (2008) Baroreflex sensitivity and power spectral analysis in different extrapyramidal syndromes. J Neural Transm (Vienna) 115(11):1527–1536. https://doi.org/10.1007/s00702-008-0127-3

    Article  CAS  Google Scholar 

  • Friedrich C, Rudiger H, Schmidt C, Herting B, Prieur S, Junghanns S, Schweitzer K, Globas C, Schols L, Berg D, Reichmann H, Ziemssen T (2010) Baroreflex sensitivity and power spectral analysis during autonomic testing in different extrapyramidal syndromes. Mov Disord 25(3):315–324. https://doi.org/10.1002/mds.22844

    Article  PubMed  Google Scholar 

  • Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56(1):33–39

    Article  CAS  PubMed  Google Scholar 

  • Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71(9):670–676. https://doi.org/10.1212/01.wnl.0000324625.00404.15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Pechnik S, Holmes C, Eldadah B, Sharabi Y (2003) Association between supine hypertension and orthostatic hypotension in autonomic failure. Hypertension 42(2):136–142. https://doi.org/10.1161/01.HYP.0000081216.11623.C3

    Article  CAS  PubMed  Google Scholar 

  • Haga R, Sugimoto K, Nishijima H, Miki Y, Suzuki C, Wakabayashi K, Baba M, Yagihashi S, Tomiyama M (2015) Clinical utility of skin biopsy in differentiating between Parkinson’s disease and multiple system atrophy. Parkinsons Dis 2015:167038. https://doi.org/10.1155/2015/167038

    PubMed  PubMed Central  Google Scholar 

  • Hakusui S, Yasuda T, Yanagi T, Tohyama J, Hasegawa Y, Koike Y, Hirayama M, Takahashi A (1994) A radiological analysis of heart sympathetic functions with meta-[123I]iodobenzylguanidine in neurological patients with autonomic failure. J Auton Nerv Syst 49(1):81–84

    Article  CAS  PubMed  Google Scholar 

  • Hirayama M, Hakusui S, Koike Y, Ito K, Kato T, Ikeda M, Hasegawa Y, Takahashi A (1995) A scintigraphical qualitative analysis of peripheral vascular sympathetic function with meta-[123I]iodobenzylguanidine in neurological patients with autonomic failure. J Auton Nerv Syst 53(2–3):230–234

    Article  CAS  PubMed  Google Scholar 

  • Holmberg B, Kallio M, Johnels B, Elam M (2001) Cardiovascular reflex testing contributes to clinical evaluation and differential diagnosis of Parkinsonian syndromes. Mov Disord 16(2):217–225

    Article  CAS  PubMed  Google Scholar 

  • Hughes AJ, Daniel SE, Ben-Shlomo Y, Lees AJ (2002) The accuracy of diagnosis of parkinsonian syndromes in a specialist movement disorder service. Brain 125(Pt 4):861–870

    Article  PubMed  Google Scholar 

  • Iodice V, Lipp A, Ahlskog JE, Sandroni P, Fealey RD, Parisi JE, Matsumoto JY, Benarroch EE, Kimpinski K, Singer W, Gehrking TL, Gehrking JA, Sletten DM, Schmeichel AM, Bower JH, Gilman S, Figueroa J, Low PA (2012) Autopsy confirmed multiple system atrophy cases: Mayo experience and role of autonomic function tests. J Neurol Neurosurg Psychiatry 83(4):453–459. https://doi.org/10.1136/jnnp-2011-301068

    Article  PubMed  PubMed Central  Google Scholar 

  • Kautzner J, Camm AJ (1997) Clinical relevance of heart rate variability. Clin Cardiol 20(2):162–168

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Lipp A, Sandroni P, Ahlskog JE, Fealey RD, Kimpinski K, Iodice V, Gehrking TL, Weigand SD, Sletten DM, Gehrking JA, Nickander KK, Singer W, Maraganore DM, Gilman S, Wenning GK, Shults CW, Low PA (2009) Prospective differentiation of multiple system atrophy from Parkinson disease, with and without autonomic failure. Arch Neurol 66(6):742–750. https://doi.org/10.1001/archneurol.2009.71

    Article  PubMed  PubMed Central  Google Scholar 

  • Malliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84(2):482–492

    Article  CAS  PubMed  Google Scholar 

  • Malliani A, Lombardi F, Pagani M (1994) Power spectrum analysis of heart rate variability: a tool to explore neural regulatory mechanisms. Br Heart J 71(1):1–2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mancia G (2012) Short- and long-term blood pressure variability: present and future. Hypertension 60(2):512–517. https://doi.org/10.1161/HYPERTENSIONAHA.112.194340

    Article  CAS  PubMed  Google Scholar 

  • Mancia G, Parati G, Pomidossi G, Casadei R, Di Rienzo M, Zanchetti A (1986) Arterial baroreflexes and blood pressure and heart rate variabilities in humans. Hypertension 8(2):147–153

    Article  CAS  PubMed  Google Scholar 

  • Mehlsen J, Kaijer MN, Mehlsen AB (2008) Autonomic and electrocardiographic changes in cardioinhibitory syncope. Europace 10(1):91–95. https://doi.org/10.1093/europace/eum237

    Article  PubMed  Google Scholar 

  • Miwa C, Sugiyama Y, Mano T, Matsukawa T, Iwase S, Watanabe T, Kobayashi F (2000) Effects of aging on cardiovascular responses to gravity-related fluid shift in humans. J Gerontol A Biol Sci Med Sci 55(6):M329–M335

    Article  CAS  PubMed  Google Scholar 

  • Montano N, Ruscone TG, Porta A, Lombardi F, Pagani M, Malliani A (1994) Power spectrum analysis of heart rate variability to assess the changes in sympathovagal balance during graded orthostatic tilt. Circulation 90(4):1826–1831

    Article  CAS  PubMed  Google Scholar 

  • Novak V, Novak P, de Champlain J, Le Blanc AR, Martin R, Nadeau R (1993) Influence of respiration on heart rate and blood pressure fluctuations. J Appl Physiol 74(2):617–626

    Article  CAS  PubMed  Google Scholar 

  • Nutt JG, Woodward WR, Beckner RM, Stone CK, Berggren K, Carter JH, Gancher ST, Hammerstad JP, Gordin A (1994) Effect of peripheral catechol-O-methyltransferase inhibition on the pharmacokinetics and pharmacodynamics of levodopa in parkinsonian patients. Neurology 44(5):913–919

    Article  CAS  PubMed  Google Scholar 

  • Orimo S, Kanazawa T, Nakamura A, Uchihara T, Mori F, Kakita A, Wakabayashi K, Takahashi H (2007) Degeneration of cardiac sympathetic nerve can occur in multiple system atrophy. Acta Neuropathol 113(1):81–86. https://doi.org/10.1007/s00401-006-0160-y

    Article  PubMed  Google Scholar 

  • Pagani M, Lombardi F, Guzzetti S, Rimoldi O, Furlan R, Pizzinelli P, Sandrone G, Malfatto G, Dell’Orto S, Piccaluga E et al (1986) Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog. Circ Res 59(2):178–193

    Article  CAS  PubMed  Google Scholar 

  • Pagani M, Montano N, Porta A, Malliani A, Abboud FM, Birkett C, Somers VK (1997) Relationship between spectral components of cardiovascular variabilities and direct measures of muscle sympathetic nerve activity in humans. Circulation 95(6):1441–1448

    Article  CAS  PubMed  Google Scholar 

  • Parikh SM, Diedrich A, Biaggioni I, Robertson D (2002) The nature of the autonomic dysfunction in multiple system atrophy. J Neurol Sci 200(1–2):1–10

    Article  PubMed  Google Scholar 

  • Phillips AA, Bredin SS, Cote AT, Drury CT, Warburton DE (2013) Aortic distensibility is reduced during intense lower body negative pressure and is related to low frequency power of systolic blood pressure. Eur J Appl Physiol 113(3):785–792. https://doi.org/10.1007/s00421-012-2489-3

    Article  PubMed  Google Scholar 

  • Piccirillo G, Naso C, Moise A, Lionetti M, Nocco M, Di Carlo S, De Laurentis T, Magri D, Cacciafesta M, Marigliano V (2004) Heart rate and blood pressure variability in subjects with vasovagal syncope. Clin Sci (Lond) 107(1):55–61. https://doi.org/10.1042/CS20030327

    Article  Google Scholar 

  • Pomeranz B, Macaulay RJ, Caudill MA, Kutz I, Adam D, Gordon D, Kilborn KM, Barger AC, Shannon DC, Cohen RJ et al (1985) Assessment of autonomic function in humans by heart rate spectral analysis. Am J Physiol 248(1 Pt 2):H151–H153

    CAS  PubMed  Google Scholar 

  • Purves D, Augustin GJ, Fitzpatrick D, Hall WC, LaMantia A, McNamara JO, Williams SM (eds) (2004) Neuroscience, 3rd edn. Sunderland, MA

    Google Scholar 

  • Rajendra Acharya U, Paul Joseph K, Kannathal N, Lim CM, Suri JS (2006) Heart rate variability: a review. Med Biol Eng Comput 44(12):1031–1051. https://doi.org/10.1007/s11517-006-0119-0

    Article  CAS  PubMed  Google Scholar 

  • Rajput AH, Rozdilsky B (1976) Dysautonomia in Parkinsonism: a clinicopathological study. J Neurol Neurosurg Psychiatry 39(11):1092–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rascol O, Schelosky L (2009) 123I-metaiodobenzylguanidine scintigraphy in Parkinson’s disease and related disorders. Mov Disord 24(Suppl 2):S732–S741. https://doi.org/10.1002/mds.22499

    Article  PubMed  Google Scholar 

  • Reichmann H, Herting B, Miller A, Sommer U (2003) Switching and combining dopamine agonists. J Neural Transm (Vienna) 110(12):1393–1400. https://doi.org/10.1007/s00702-003-0081-z

    Article  CAS  Google Scholar 

  • Reimann M, Schmidt C, Herting B, Prieur S, Junghanns S, Schweitzer K, Globas C, Schoels L, Reichmann H, Berg D, Ziemssen T (2010) Comprehensive autonomic assessment does not differentiate between Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy. J Neural Transm (Vienna) 117(1):69–76. https://doi.org/10.1007/s00702-009-0313-y

    Article  Google Scholar 

  • Riley DE, Chelimsky TC (2003) Autonomic nervous system testing may not distinguish multiple system atrophy from Parkinson’s disease. J Neurol Neurosurg Psychiatry 74(1):56–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocchi C, Pierantozzi M, Galati S, Chiaravalloti A, Pisani V, Prosperetti C, Lauretti B, Stampanoni Bassi M, Olivola E, Schillaci O, Stefani A (2015) Autonomic function tests and MIBG in Parkinson’s disease: correlation to disease duration and motor symptoms. CNS Neurosci Ther 21(9):727–732. https://doi.org/10.1111/cns.12437

    Article  CAS  PubMed  Google Scholar 

  • Sako W, Abe T, Murakami N, Miyazaki Y, Izumi Y, Harada M, Kaji R (2016) Imaging-based differential diagnosis between multiple system atrophy and Parkinson’s disease. J Neurol Sci 368:104–108. https://doi.org/10.1016/j.jns.2016.06.061

    Article  PubMed  Google Scholar 

  • Sawada H, Oeda T, Yamamoto K, Kitagawa N, Mizuta E, Hosokawa R, Ohba M, Nishio R, Yamakawa K, Takeuchi H, Shimohama S, Takahashi R, Kawamura T (2009) Diagnostic accuracy of cardiac metaiodobenzylguanidine scintigraphy in Parkinson disease. Eur J Neurol 16(2):174–182. https://doi.org/10.1111/j.1468-1331.2008.02372.x

    Article  CAS  PubMed  Google Scholar 

  • Schmidt C, Herting B, Prieur S, Junghanns S, Schweitzer K, Globas C, Schols L, Reichmann H, Berg D, Ziemssen T (2009) Valsalva manoeuvre in patients with different Parkinsonian disorders. J Neural Transm (Vienna) 116(7):875–880. https://doi.org/10.1007/s00702-009-0239-4

    Article  CAS  Google Scholar 

  • Stys A, Stys T (1998) Current clinical applications of heart rate variability. Clin Cardiol 21(10):719–724

    Article  CAS  PubMed  Google Scholar 

  • Takahashi A (1991) Autonomic nervous system disorders in Parkinson’s disease. Eur Neurol 31(Suppl 1):41–47

    Article  PubMed  Google Scholar 

  • Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93(5):1043–1065

    Article  Google Scholar 

  • Thobois S (2006) Proposed dose equivalence for rapid switch between dopamine receptor agonists in Parkinson’s disease: a review of the literature. Clin Ther 28(1):1–12. https://doi.org/10.1016/j.clinthera.2005.12.003

    Article  CAS  PubMed  Google Scholar 

  • Tsuji H, Larson MG, Venditti FJ Jr, Manders ES, Evans JC, Feldman CL, Levy D (1996) Impact of reduced heart rate variability on risk for cardiac events. The Framingham Heart Study. Circulation 94(11):2850–2855

    Article  CAS  PubMed  Google Scholar 

  • Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1988) Parkinson’s disease: the presence of Lewy bodies in Auerbach’s and Meissner’s plexuses. Acta Neuropathol 76(3):217–221

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Takeda T, Nakamagoe K, Tamaoka A (2011) Sequential imaging analysis using MIBG scintigraphy revealed progressive degeneration of cardiac sympathetic nerve in Parkinson’s disease. Eur J Neurol 18(7):1010–1013. https://doi.org/10.1111/j.1468-1331.2010.03211.x

    Article  CAS  PubMed  Google Scholar 

  • Weise F, Heydenreich F, Runge U (1987) Contributions of sympathetic and vagal mechanisms to the genesis of heart rate fluctuations during orthostatic load: a spectral analysis. J Auton Nerv Syst 21(2–3):127–134

    Article  CAS  PubMed  Google Scholar 

  • Wenning GK, Stefanova N (2009) Recent developments in multiple system atrophy. J Neurol 256(11):1791–1808. https://doi.org/10.1007/s00415-009-5173-8

    Article  PubMed  Google Scholar 

  • Wenning GK, Ben-Shlomo Y, Hughes A, Daniel SE, Lees A, Quinn NP (2000) What clinical features are most useful to distinguish definite multiple system atrophy from Parkinson’s disease? J Neurol Neurosurg Psychiatry 68(4):434–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang R, Iwasaki K, Zuckerman JH, Behbehani K, Crandall CG, Levine BD (2002) Mechanism of blood pressure and R–R variability: insights from ganglion blockade in humans. J Physiol 543(Pt 1):337–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziemssen T, Fuchs G, Greulich W, Reichmann H, Schwarz M, Herting B (2011) Treatment of dysautonomia in extrapyramidal disorders. J Neurol 258(Suppl 2):S339–S345. https://doi.org/10.1007/s00415-011-5946-8

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Clinical Laboratory Division, Shimane University Hospital, Izumo, Japan

    Chikako Watano, Yuri Shiota, Seiji Mishima, Eri Nitta & Atsushi Nagai

  2. Department of Laboratory Medicine, Shimane University School of Medicine, 89-1 Enya Cho, Izumo, 693-8501, Japan

    Abdullah Md Sheikh, Shozo Yano & Atsushi Nagai

  3. Department of Internal Medicine III, Shimane University Faculty of Medicine, Izumo, Japan

    Keiichi Onoda & Shuhei Yamaguchi

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  1. Chikako Watano
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  2. Yuri Shiota
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Correspondence to Atsushi Nagai.

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Watano, C., Shiota, Y., Onoda, K. et al. Evaluation of autonomic functions of patients with multiple system atrophy and Parkinson’s disease by head-up tilt test. J Neural Transm 125, 153–162 (2018). https://doi.org/10.1007/s00702-017-1816-6

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