Abstracts
Cardiovascular variability (CVV) has been evaluated in patients with Parkinson's disease (PD) in other countries and exhibit ethnic differences.
Objective
We investigated heart rate variability (HRV) and blood pressure variability (BPV) in Mexican patients with PD.
Method
We further compared HRV and BPV between this group and young healthy controls (YHC) in order to estimate, for the first time in our country, the magnitude of the difference. Twenty patients were examined. Time- and frequency-domain CVV parameters were studied during supine rest (SR), active standing (AS) and controlled breathing. These measurements were compared to those of 20 YHC.
Results
In the three conditions tested, our study showed a decrease in almost all HRV parameters in PD patients; on the contrary, decreased BPV parameters were found less frequently and only during SR and AS.
Conclusion
Our results indicate that HRV is impaired in PD. Some BPV parameters are also diminished.
Parkinson's disease; autonomic nervous system; heart rate variability; blood pressure variability; dysautonomia
A variabilidade cardiovascular (VCV) tem sido avaliada em doentes parkinsonianos em vários países e apresenta diferenças étnicas.
Objetivo
Investigar a variabilidade da frequência cardíaca (VFC) e a variabilidade da pressão arterial (VPA) em doentes parkinsonianos mexicanos.
Método
Comparamos VFC e VPA entre o grupo de estudo e controles jovens (CJ), a fim de estimar a magnitude da diferença. CVV foi estudada no domínio do tempo e da frequência durante repouso supino (RS), ortostase ativa (OA) e respiração controlada. Estas medições foram comparadas com aquelas de 20 CJ.
Resultados
Nosso estudo mostrou diminuição em quase todos os parâmetros da VFC em doentes parkinsonianos. A diminuição dos parâmetros da VPA foi encontrada com menos frequência.
Conclusão
Nossos resultados indicam que a VFC é prejudicada na doença de Parkinson. Alguns parâmetros do VPA também são reduzidos.
doença de Parkinson; sistema nervoso autônomo; variabilidade da frequência cardíaca; variabilidade da pressão arterial; disreflexia autonômica
The clinical features of Parkinson's disease (PD) are not restricted to the
classical triad of resting tremor, rigidity, and bradykinesia, but also include
autonomic disturbances11 . Kallio M, Haapaniemi T, Turkka J, Suominem K, Tolonen U, Sotaniemi
K et al. Heart rate variability in patients with untreated Parkinson's
disease. Eur J Neurol. 2000;7(6):667-72.
http://dx.doi.org/10.1046/j.1468-1331.2000.00127.x
https://doi.org/10.1046/j.1468-1331.2000...
, which were
first noted by James Parkinson in his original description. Concretely, the prevalence
of clinically relevant dysautonomia in PD exceeds 50%22 . Wolters ECh, Braak H. Parkinson's disease: premotor
clinico-pathological correlations. J Neural Transm Suppl. 2006;70:309-19.
http://dx.doi.org/10.1007/978-3-211-45295-0_47
https://doi.org/10.1007/978-3-211-45295-...
. The period between the onset of neurodegeneration and
appearance of the cardinal motor signs is referred to as premotor or prodromal phase of
PD and its duration has been estimated to be from years to decades33 . Gaenslen A, Swid I, Liepelt-Scarfone I, Godau J, Berg D et al. The
patients' perception of prodromal symptoms before the initial diagnosis of
Parkinson's disease. Mov Disord. 2011;26(4):653-8.
http://dx.doi.org/10.1002/mds.23499
https://doi.org/10.1002/mds.23499 ...
. During this phase patients later diagnosed with PD
have more autonomic symptoms than control subjects33 . Gaenslen A, Swid I, Liepelt-Scarfone I, Godau J, Berg D et al. The
patients' perception of prodromal symptoms before the initial diagnosis of
Parkinson's disease. Mov Disord. 2011;26(4):653-8.
http://dx.doi.org/10.1002/mds.23499
https://doi.org/10.1002/mds.23499 ...
,44 . Gonera EG, Van't Hof M, Berger HJ, Weel C, Horstink MWIM.
Symptoms and duration of the prodromal phase in Parkinson's disease. Mov
Disord. 1997;12(6):871-6.
http://dx.doi.org/10.1002/mds.870120607
https://doi.org/10.1002/mds.870120607...
. Likewise, existing reports indicate that autonomic dysfunction
occurs before any medical intervention and often precedes motor disturbances55 . Brown R, Duma S, Piguet O, Broe GA, Macefield VG. Cardiovascular
variability in Parkinson's disease and extrapyramidal motor slowing. Clin
Auton Res. 2012;22(4):191-6.
http://dx.doi.org/10.1007/s10286-012-0163-9
https://doi.org/10.1007/s10286-012-0163-...
.
All three branches of the autonomic nerve system (ANS) are affected in PD66 . Shibata M, Morita Y, Shimizu T, Takahashi K, Suzuki N. Cardiac
parasympathetic dysfunction concurrent with cardiac sympathetic denervation in
Parkinson's disease. J Neurol Sci. 2009;276(1-2):79-83.
http://dx.doi.org/10.1016/j.jns.2008.09.005
https://doi.org/10.1016/j.jns.2008.09.00...
. Sympathetic cardioneuropathy was first
described about 15 years ago using 6-[18F]fluorodopamine positron-emission
tomography and later confirmed by neuropathological and neuroimaging findings77 . Jain S, Goldstein DS. Cardiovascular dysautonomia in Parkinson
disease: from pathophysiology to pathogenesis. Neurobiol Dis. 2012;46(3):572-80.
http://dx.doi.org/10.1016/j.nbd.2011.10.025
https://doi.org/10.1016/j.nbd.2011.10.02...
. Furthermore, Shibata et al.
demonstrated that in the early stages of PD, cardiovagal dysfunction occurs concurrently
with cardiosympathetic denervation66 . Shibata M, Morita Y, Shimizu T, Takahashi K, Suzuki N. Cardiac
parasympathetic dysfunction concurrent with cardiac sympathetic denervation in
Parkinson's disease. J Neurol Sci. 2009;276(1-2):79-83.
http://dx.doi.org/10.1016/j.jns.2008.09.005
https://doi.org/10.1016/j.jns.2008.09.00...
,
but possibly the latter is incomplete and the remaining fibers are sufficient for the
maintenance of sympathetic control88 . Buob A, Winter H, Kindermann M, Becker G, Möller JC, Oertel
WH et al. Parasympathetic but not sympathetic cardiac dysfunction at early
stages of Parkinson's disease. Clin Res Cardiol. 2010;99(11):701-6.
http://dx.doi.org/10.1007/s00392-010-0170-6
https://doi.org/10.1007/s00392-010-0170-...
.
Neuropathological studies have demonstrated the presence of Lewy bodies (LB) in both
tyrosine hydroxylase-positive and -negative nerve processes of the cardiac plexus, and
also in Auerbach's and Meissner's plexuses55 . Brown R, Duma S, Piguet O, Broe GA, Macefield VG. Cardiovascular
variability in Parkinson's disease and extrapyramidal motor slowing. Clin
Auton Res. 2012;22(4):191-6.
http://dx.doi.org/10.1007/s10286-012-0163-9
https://doi.org/10.1007/s10286-012-0163-...
,66 . Shibata M, Morita Y, Shimizu T, Takahashi K, Suzuki N. Cardiac
parasympathetic dysfunction concurrent with cardiac sympathetic denervation in
Parkinson's disease. J Neurol Sci. 2009;276(1-2):79-83.
http://dx.doi.org/10.1016/j.jns.2008.09.005
https://doi.org/10.1016/j.jns.2008.09.00...
. The occurrence of prodromal symptoms appears to correspond to
the neuropathological staging of PD-associated LB pathology as proposed by Braak et al.
and later modified by Przuntek et al.33 . Gaenslen A, Swid I, Liepelt-Scarfone I, Godau J, Berg D et al. The
patients' perception of prodromal symptoms before the initial diagnosis of
Parkinson's disease. Mov Disord. 2011;26(4):653-8.
http://dx.doi.org/10.1002/mds.23499
https://doi.org/10.1002/mds.23499 ...
.
The cardiovascular autonomic assessment is therefore of chief importance in PD. As
previous studies have shown ethnic differences in cardiovascular variability (CVV)99 . Wang X, Thayer JF, Treiber F, Snieder H. Ethnic differences and
heritability of heart rate variability in African- and European American youth.
Am J Cardiol. 2005;96(8):1166-72.
http://dx.doi.org/10.1016/j.amjcard.2005.06.050
https://doi.org/10.1016/j.amjcard.2005.0...
; the purpose of the current study was
to investigate it, for the first time, in Mexican patients with PD.
Method
Heart rate variability (HRV) analysis is a widely accepted, non-invasive, method for
indirect assessment of the ANS activity1010 . Devos D, Kroumova M, Bordet R, Vodougnon H, Guieu JD, Libersa C.
Heart rate variability and Parkinson's disease severity. J Neural Transm.
2003;110(9):997-1011.
http://dx.doi.org/10.1007/s00702-003-0016-8
https://doi.org/10.1007/s00702-003-0016-...
. This method, which provides information on sympathetic
and parasympathetic modulation of the sinus node, has been utilized in many studies
involving PD. Despite an obvious lack of parasympathetic innervation to the systemic
vasculature (which presumably allows an exclusive evaluation of the sympathetic
system), blood pressure variability (BPV) analysis has received far less attention
than HRV55 . Brown R, Duma S, Piguet O, Broe GA, Macefield VG. Cardiovascular
variability in Parkinson's disease and extrapyramidal motor slowing. Clin
Auton Res. 2012;22(4):191-6.
http://dx.doi.org/10.1007/s10286-012-0163-9
https://doi.org/10.1007/s10286-012-0163-...
. Short-term CVV can be
calculated by means of both time- and frequency-domain techniques1111 . Task Force of the European Society of Cardiology the North
American Society of Pacing Electrophysiology. Heart rate variability: standards
of measurement, physiological interpretation, and clinical use. Circulation.
1996;93(5):1043-65. http://dx.doi.org/10.1161/01.cir.93.5.1043
https://doi.org/10.1161/01.cir.93.5.1043...
,1212 . Elghozi JL. Variabilité à court terme de la pression
artérielle : physiologie et pharmacologie. Ann Pharm Fr. 2008;66(3):158-68.
http://dx.doi.org/10.1016/j.pharma.2008.05.002
https://doi.org/10.1016/j.pharma.2008.05...
. Certain HRV parameters have been shown to act as
independent predictors of mortality in postinfarcted1111 . Task Force of the European Society of Cardiology the North
American Society of Pacing Electrophysiology. Heart rate variability: standards
of measurement, physiological interpretation, and clinical use. Circulation.
1996;93(5):1043-65. http://dx.doi.org/10.1161/01.cir.93.5.1043
https://doi.org/10.1161/01.cir.93.5.1043...
, chronically hemodialyzed1313 . Ranpuria R, Hall M, Chan CT, Unruh M. Heart rate variability (HRV)
in kidney failure: measurement and consequences of reduced HRV. Nephrol Dial
Transplant. 2008;23(2):444-9.
http://dx.doi.org/10.1093/ndt/gfm634
https://doi.org/10.1093/ndt/gfm634...
, heart failure1414 . Ponikowski P, Anker SD, Chua TP, Szelemej R, Piepoli M,
Adamapoulos S et al. Depressed heart rate variability as an independent
predictor of death in chronic congestive heart failure secondary to ischemic or
idiopathic dilated cardiomyopathy. Am J Cardiol. 1997;79(12):1645-50.
http://dx.doi.org/10.1016/s0002-9149(97)00215-4
https://doi.org/10.1016/s0002-9149(97)00...
, diabetic1515 . May O, Arildsen H. Long-term predictive power of heart rate
variability on all-cause mortality in the diabetic population. Acta Diabetol.
2011;48(1):55-9. http://dx.doi.org/10.1007/s00592-010-0222-4
https://doi.org/10.1007/s00592-010-0222-...
and hemodynamically stable trauma patients1616 . Ryan ML, Ogilvie MP, Pereira BM, Gomez-Rodriguez JC, Manning RJ,
Vartas PA et al. Heart rate variability is an independent predictor of morbidity
and mortality in hemodynamically stable trauma patients. J Trauma.
2011;70(6):1371-80.
http://dx.doi.org/10.1097/TA.0b013e31821858e6
https://doi.org/10.1097/TA.0b013e3182185...
. A decrease in BPV has been
reported in patients with mildly impaired renal function1717 . Diaz KM, Feairheller DL, Sturgeon KM, Veerabhadrappa P, Williamson
ST, Crabbe DL et al. Increased nitric oxide and attenuated diastolic blood
pressure variability in African Americans with mildly impaired renal function.
Int J Hypertens. 2011;2010:137206. http://dx.doi.org/10.4061/2010/137206
https://doi.org/10.4061/2010/137206 ...
, renovascular hypertension1818 . Mussalo H, Vanninen E, Ikäheimo R, Laitinen T, Hartikainen J.
Short-term blood pressure variability in renovascular hypertension and in severe
and mild essential hypertension. Clin Sci (Lond). 2003;105(5):609-14.
http://dx.doi.org/10.1042/CS20020268
https://doi.org/10.1042/CS20020268...
and congestive heart failure1919 . Radaelli A, Perlangeli S, Cerutti MC, Mircoli L, Mori I, Boselli L
et al. Altered blood pressure variability in patients with congestive heart
failure. J Hypertens. 1999;17(Suppl 12):1905-10.. However, the effect of this reduction on patient
mortality is unknown.
Study population
We studied autonomic function in 20 patients with mild-to-moderate PD (13 males,
mean age 60.9±6.27 years, mean duration of disease 3.65±2.39 years,
Hoehn and Yahr stage ≤3). All participants with PD fulfilled the UK Brain
Bank Clinical Criteria. None of these patients had evidence of diabetes mellitus
or hypertension. PD group was not divided into subgroups according to their
treatment, since previous studies have found little or no difference as to
whether the patient was or was not taking medication55 . Brown R, Duma S, Piguet O, Broe GA, Macefield VG. Cardiovascular
variability in Parkinson's disease and extrapyramidal motor slowing. Clin
Auton Res. 2012;22(4):191-6.
http://dx.doi.org/10.1007/s10286-012-0163-9
https://doi.org/10.1007/s10286-012-0163-...
,2020 . Friedrich C, Rüdiger H, Schmidt C, Herting B, Prieur S,
Junghanns S et al. Baroreflex sensitivity and power spectral analysis in
different extrapyramidal syndromes. J Neural Transm. 2008;115(11):1527-36.
http://dx.doi.org/10.1007/s00702-008-0127-3
https://doi.org/10.1007/s00702-008-0127-...
. As control group, we included 20 young subjects
(9 males, mean age 37.6±8.84 years) who were in good health status as
determined by physical exam. This study was approved by the Ethical Committee of
the National Institute of Medical Sciences and Nutrition and an informed written
consent was obtained from all patients and controls.
Protocol
Evaluations were performed between 9:00 and 11:00. Participants in both groups
were instructed to avoid alcohol, caffeinated beverages and over-the-counter
medications after 22:00 on the night before the measurements. A
photoplethysmographic finger cuff was wrapped on the mid-phalanx of the left
index finger and placed in the midaxillary line at heart level for continuous
non-invasive beat-to-beat recording of blood pressure (BP) and interbeat
intervals (IBI) using the volume-clamp technique of Peňáz
(Finometer® PRO, Finapres Medical Systems, Amsterdam). Relatively short
recordings (≈ 6 minutes) were obtained in each of the following
conditions: supine rest (SR), active standing (AS) and 0.1 Hz controlled
breathing (CB). The latter frequency was chosen because it profoundly increases
HRV power to an individual maximum in normal subjects2121 . Baevsky RM, Baranov VM, Funtova II, Diedrich A, Pashenko AV,
Chernikova AG et al. Autonomic cardiovascular and respiratory control during
prolonged spaceflights aboard the International Space Station. J Appl Physiol.
2007;103(1):156-61.
http://dx.doi.org/10.1152/japplphysiol.00137.2007
https://doi.org/10.1152/japplphysiol.001...
. Total recording time per subject was
approximately 40 minutes. All participants completed the three conditions.
Hemodynamic parameters were extracted with BeatScope® (Finapres Medical
Systems).
Data analysis and statistics
All data were entered into Microsoft Excel® spreadsheets. Prior to all
analyses, hemodynamic parameters were visually inspected and artifacts were
manually removed and corrected by means of linear interpolation. Only stable
recordings were included for analysis. Kubios HRV® (v.2.0, Biosignal
Analysis and Medical Imaging Group, University of Eastern Finland) was used to
generate the following parameters from the recorded IBI1111 . Task Force of the European Society of Cardiology the North
American Society of Pacing Electrophysiology. Heart rate variability: standards
of measurement, physiological interpretation, and clinical use. Circulation.
1996;93(5):1043-65. http://dx.doi.org/10.1161/01.cir.93.5.1043
https://doi.org/10.1161/01.cir.93.5.1043...
: mean and standard deviation of heart rate
(MHR, SDHR, bpm), standard deviation of all IBI (standard deviation of all
normal-to-normal intervals, SDNN, ms), square root of the mean of the sum of the
squares of differences between adjacent IBI (square root of the mean of the sum
of the squares of differences between adjacent NNI, RMSSD, ms), number of pairs
of adjacent IBI differing by more than 50 ms in the entire recording (NN50),
percentage of adjacent IBI differing by more than 50 ms in the entire recording
(pNN50), total power (TP, ms2), power in low frequency range (LF,
0.04-0.15 Hz, ms2), power in high frequency range (HF, 0.15-0.4 Hz,
ms2), LF in normalized units (LFnu), HF in normalized
units (HFnu) and the ratio between LF/HF (LF/HF). Spectral analysis
was performed by Kubios HRV® through a Fast Fourier Transformation (FFT) of
the IBI time series. In addition, a software written in MATLAB® (v.R2012a,
MathWorks, Massachusetts) was developed to spectrally analyze the BP by applying
FFT. These parameters were generated by the software: TP (mmHg2), LF
(mmHg2) and HF (mmHg2). Time domain parameters of BPV
were calculated with STATISTICA for Windows® (v.5.1). Statistical analysis
was performed with the same software. Prior to group analyses, individual data
were tested for normality (Shapiro-Wilk test). Comparison between the two groups
was performed by either using Student's t-test or Mann-Whitney U test. A
p-value below 0.05 (p<0.05) was considered significant. All results are
expressed as mean ± SD or median (range).
Results
HRV
All the parameters studied for both groups were significantly different during SR, except for maximal heart rate (HRmax). The following time-domain parameters were higher in PD as compared to young healthy controls (YHC): MHR and minimal heart rate (HRmin). On the contrary, the remaining time-domain parameters were comparatively lower (SDHR, SDNN, RMSSD, NN50 and pNN50). With respect to the frequency domain, TP (ms2), LF (ms2), HF (ms2) and HFnu were also comparatively lower in PD; whereas the opposite occurred with LFnu and LF/HF. These results are shown in Table 1. MHR, HRmax, HRmin, LFnu, HFnu and LF/HF were not significantly different between the two groups during AS; while all other parameters were lower in PD as compared to YHC. These results are shown in Table 2. HRmax, LFnu, HFnu and LF/HF were not significantly different between the two groups during CB; whilst SDHR, SDNN, RMSSD, NN50, pNN50, TP (ms2), LF (ms2) and HF (ms2) were comparatively lower in PD. The remaining time-domain parameters were contrarily higher (MHR and HRmin). These results are shown in Table 3.
BPV
Mean systolic blood pressure (MSBP), maximal systolic blood pressure (SBPmax) and minimal systolic blood pressure (SBPmin) were lower in PD as compared to YHC during SR. With respect to the frequency domain, TP (mmHg2) were also comparatively lower in PD. All other parameters were not significantly different between groups. These results are shown in Table 4. Although most parameters were not significantly different between the two groups during AS, LF (mmHg2) y HF (mmHg2) were lower in PD as compared to YHC. These results are shown in Table 5. None of the parameters were significantly different between the groups during CB. These results are shown in Table 6.
Discussion
HRV
Consistent with other studies11 . Kallio M, Haapaniemi T, Turkka J, Suominem K, Tolonen U, Sotaniemi
K et al. Heart rate variability in patients with untreated Parkinson's
disease. Eur J Neurol. 2000;7(6):667-72.
http://dx.doi.org/10.1046/j.1468-1331.2000.00127.x
https://doi.org/10.1046/j.1468-1331.2000...
,1010 . Devos D, Kroumova M, Bordet R, Vodougnon H, Guieu JD, Libersa C.
Heart rate variability and Parkinson's disease severity. J Neural Transm.
2003;110(9):997-1011.
http://dx.doi.org/10.1007/s00702-003-0016-8
https://doi.org/10.1007/s00702-003-0016-...
, our results showed a decrease in overall HRV (i.
e., SDNN, TP) in PD as compared to YHC during the three conditions. More
specifically, cardiovagal indicators (i. e., RMSSD, NN50, pNN50 and HF)11 . Kallio M, Haapaniemi T, Turkka J, Suominem K, Tolonen U, Sotaniemi
K et al. Heart rate variability in patients with untreated Parkinson's
disease. Eur J Neurol. 2000;7(6):667-72.
http://dx.doi.org/10.1046/j.1468-1331.2000.00127.x
https://doi.org/10.1046/j.1468-1331.2000...
,1010 . Devos D, Kroumova M, Bordet R, Vodougnon H, Guieu JD, Libersa C.
Heart rate variability and Parkinson's disease severity. J Neural Transm.
2003;110(9):997-1011.
http://dx.doi.org/10.1007/s00702-003-0016-8
https://doi.org/10.1007/s00702-003-0016-...
,1111 . Task Force of the European Society of Cardiology the North
American Society of Pacing Electrophysiology. Heart rate variability: standards
of measurement, physiological interpretation, and clinical use. Circulation.
1996;93(5):1043-65. http://dx.doi.org/10.1161/01.cir.93.5.1043
https://doi.org/10.1161/01.cir.93.5.1043...
were significantly reduced in
PD. At rest LF variations are greatly mediated by vagal fluctuations1010 . Devos D, Kroumova M, Bordet R, Vodougnon H, Guieu JD, Libersa C.
Heart rate variability and Parkinson's disease severity. J Neural Transm.
2003;110(9):997-1011.
http://dx.doi.org/10.1007/s00702-003-0016-8
https://doi.org/10.1007/s00702-003-0016-...
. Hence, we should be cautious
when interpreting LF/HF elevation in PD during SR as sympathetic dominance.
Conversely, if we consider the traditional paradigms of spectral analysis of HRV
during AS55 . Brown R, Duma S, Piguet O, Broe GA, Macefield VG. Cardiovascular
variability in Parkinson's disease and extrapyramidal motor slowing. Clin
Auton Res. 2012;22(4):191-6.
http://dx.doi.org/10.1007/s10286-012-0163-9
https://doi.org/10.1007/s10286-012-0163-...
,1111 . Task Force of the European Society of Cardiology the North
American Society of Pacing Electrophysiology. Heart rate variability: standards
of measurement, physiological interpretation, and clinical use. Circulation.
1996;93(5):1043-65. http://dx.doi.org/10.1161/01.cir.93.5.1043
https://doi.org/10.1161/01.cir.93.5.1043...
, LF reduction reflects
cardiosympathetic impairment in PD. LFnu and HFnu were not
significantly different between groups during both AS and CB, this lack of
difference indicates a proportional reduction of both LF (ms22 . Wolters ECh, Braak H. Parkinson's disease: premotor
clinico-pathological correlations. J Neural Transm Suppl. 2006;70:309-19.
http://dx.doi.org/10.1007/978-3-211-45295-0_47
https://doi.org/10.1007/978-3-211-45295-...
) y HF (ms22 . Wolters ECh, Braak H. Parkinson's disease: premotor
clinico-pathological correlations. J Neural Transm Suppl. 2006;70:309-19.
http://dx.doi.org/10.1007/978-3-211-45295-0_47
https://doi.org/10.1007/978-3-211-45295-...
). In both groups, LF (ms22 . Wolters ECh, Braak H. Parkinson's disease: premotor
clinico-pathological correlations. J Neural Transm Suppl. 2006;70:309-19.
http://dx.doi.org/10.1007/978-3-211-45295-0_47
https://doi.org/10.1007/978-3-211-45295-...
) values were considerably increased in
magnitude but different from each other during CB, a condition known to augment
cardiovagal control2121 . Baevsky RM, Baranov VM, Funtova II, Diedrich A, Pashenko AV,
Chernikova AG et al. Autonomic cardiovascular and respiratory control during
prolonged spaceflights aboard the International Space Station. J Appl Physiol.
2007;103(1):156-61.
http://dx.doi.org/10.1152/japplphysiol.00137.2007
https://doi.org/10.1152/japplphysiol.001...
.
Nevertheless this finding does not reflect sympathetic dominance but rather an
effect of low respiratory frequency (<0.2 Hz), which causes an overlap of the
LF and HF components of CVV signals2222 . Strano S, Lino S, Calcagnini G, Di Virgilio V, Ciardo R, Crutti S
et al. Respiratory sinus arrhythmia and cardiovascular neural regulation in
athletes. Med Sci Sports Exerc. 1998;30(2):215-9.
http://dx.doi.org/10.1097/00005768-199802000-00007
https://doi.org/10.1097/00005768-1998020...
,2626 . Oka H, Toyoda C, Yogo M, Mochio S. Cardiovascular dysautonomia in
de novo Parkinson's disease without orthostatic hypotension. Eur J Neurol.
2011;18(2):286-92.
http://dx.doi.org/10.1111/j.1468-1331.2010.03135.x
https://doi.org/10.1111/j.1468-1331.2010...
.
BPV
Our results showed a decrease in overall BPV (i. e., TP) in PD as compared to YHC
during SR. Despite this significant difference in TP (mmHg2), LF
(mmHg2) and HF (mmHg2) were similar in both groups.
One likely explanation for this apparently contradictory result is that power in
very low frequency range (≤0.04 Hz, mmHg2), whose nature
remains unclear2424 . Langager AM, Hammerberg BE, Rotella DL, Strauss HM. Very
low-frequency blood pressure variability depends on voltage-gated L-type Ca2+
channels in conscious rats. Am J Physiol Heart Circ Physiol.
2007;292(3):H1321-7.
http://dx.doi.org/10.1152/ajpheart.00874.2006
https://doi.org/10.1152/ajpheart.00874.2...
, is also
part of TP. During AS, the opposite occurred: TP (mmHg2) was similar
in both groups and, notwithstanding this result, LF (mmHg2) and HF
(mmHg2) were significantly different between the two groups. The
above explanation is also quite plausible here. LF (mmHg2) was
comparatively lower in PD during AS, this reduction in the so-called Mayer waves
reflects an impairment in the vasosympathetic outflow55 . Brown R, Duma S, Piguet O, Broe GA, Macefield VG. Cardiovascular
variability in Parkinson's disease and extrapyramidal motor slowing. Clin
Auton Res. 2012;22(4):191-6.
http://dx.doi.org/10.1007/s10286-012-0163-9
https://doi.org/10.1007/s10286-012-0163-...
,2525 . Barbic F, Perego F, Canesi M, Gianni M, Biagiotti S, Constantino G
et al. Early abnormalities of vascular and cardiac autonomic control in
Parkinson's disease without orthostatic hypotension. Hypertension.
2007;49(1):120-6.
http://dx.doi.org/10.1161/01.HYP.0000250939.71343.7c
https://doi.org/10.1161/01.HYP.000025093...
. Meanwhile, during SR, a similar though
statistically not significant trend was noticed as shown in Figure.
Vasosympathetic dysfunction in PD has been already reported2525 . Barbic F, Perego F, Canesi M, Gianni M, Biagiotti S, Constantino G
et al. Early abnormalities of vascular and cardiac autonomic control in
Parkinson's disease without orthostatic hypotension. Hypertension.
2007;49(1):120-6.
http://dx.doi.org/10.1161/01.HYP.0000250939.71343.7c
https://doi.org/10.1161/01.HYP.000025093...
,2626 . Oka H, Toyoda C, Yogo M, Mochio S. Cardiovascular dysautonomia in
de novo Parkinson's disease without orthostatic hypotension. Eur J Neurol.
2011;18(2):286-92.
http://dx.doi.org/10.1111/j.1468-1331.2010.03135.x
https://doi.org/10.1111/j.1468-1331.2010...
. The coincidence of LF (mmHg2)
comparatively decreased in PD and MSBP similar between groups after orthostatic
challenge (i. e., AS) is consistent with a previously proposed hypothesis that
initial alterations of vasosympathetic control may primarily affect BPV and only
subsequently induce changes in MSBP values leading to orthostatic
hypotension2525 . Barbic F, Perego F, Canesi M, Gianni M, Biagiotti S, Constantino G
et al. Early abnormalities of vascular and cardiac autonomic control in
Parkinson's disease without orthostatic hypotension. Hypertension.
2007;49(1):120-6.
http://dx.doi.org/10.1161/01.HYP.0000250939.71343.7c
https://doi.org/10.1161/01.HYP.000025093...
. As noted
above, HF (mmHg2) was lower in PD as compared to YHC. For an accurate
interpretation of this result, it must be taken into account that this
respiratory oscillation depends on fluctuation in cardiac output1212 . Elghozi JL. Variabilité à court terme de la pression
artérielle : physiologie et pharmacologie. Ann Pharm Fr. 2008;66(3):158-68.
http://dx.doi.org/10.1016/j.pharma.2008.05.002
https://doi.org/10.1016/j.pharma.2008.05...
,2424 . Langager AM, Hammerberg BE, Rotella DL, Strauss HM. Very
low-frequency blood pressure variability depends on voltage-gated L-type Ca2+
channels in conscious rats. Am J Physiol Heart Circ Physiol.
2007;292(3):H1321-7.
http://dx.doi.org/10.1152/ajpheart.00874.2006
https://doi.org/10.1152/ajpheart.00874.2...
,2727 . Hughson RL, Maillet A, Dureau G, Yamamoto Y, Gharib C. Spectral
analysis of blood pressure variability in heart transplant patients.
Hypertension. 1995;25(4 Pt 1):643-50. http://dx.doi.org/10.1161/01.hyp.25.4.643
https://doi.org/10.1161/01.hyp.25.4.643 ...
. Finally, it is known that
slow breathing (0.1 Hz) improves baroreflex sensitivity by increasing HRV and
BPV2828 . Rosengård-Bärlund M, Bernardi L, Holmqvist J, Debarbieri
G, Mäntysaari M, Björkesten C-G et al. Deep breathing improves blunted
baroreflex sensitivity even after 30 years of type 1 diabetes. Diabetologia.
2011;54(7):1862-70. http://dx.doi.org/10.1007/s00125-011-2164-y
https://doi.org/10.1007/s00125-011-2164-...
; this may partially
explain the lack of a significant difference between the groups during CB. In
both groups, LF (mmHg2) values were considerably increased in
magnitude during CB. This finding, as in the case of HRV, does not reflect
sympathetic dominance but rather an effect of low respiratory frequency2323 . Pinna GD, Maestri R, La Rovere MT, Gobbi E, Fanfulla F. Effect of
paced breathing on ventilatory and cardiovascular variability parameters during
short-term investigations of autonomic function. Am J Physiol Heart Circ
Physiol. 2006;290(1):H424-33.
http://dx.doi.org/10.1152/ajpheart.00438.2005
https://doi.org/10.1152/ajpheart.00438.2...
.
To our knowledge, these findings are the first to document a blunted CVV in
Mexican patients with PD2929 . Estañol B, Delgado G, Bertado N, Callejas C, Medina Z,
Infante O et al. Loss of heart rate variability in Parkinson's disease
shown by the Poincaré plots during rhytmic breathing. Neurology.
2012;78(Meeting Abstracts 1):P05.196.
http://dx.doi.org/10.1212/wnl.78.1_meetingabstracts.p05.196
https://doi.org/10.1212/wnl.78.1_meeting...
.
Such assessment is particularly relevant because CVV exhibit ethnic
differences99 . Wang X, Thayer JF, Treiber F, Snieder H. Ethnic differences and
heritability of heart rate variability in African- and European American youth.
Am J Cardiol. 2005;96(8):1166-72.
http://dx.doi.org/10.1016/j.amjcard.2005.06.050
https://doi.org/10.1016/j.amjcard.2005.0...
. The mortality
of PD patients is almost doubled compared with age- and sex-matched healthy
controls, and it is worth noting that increased cardiovascular mortality has
been also reported in parkinsonian patients (as for diabetic or postinfarcted
patients). Therefore, the clinical implications of our results are consistent
with a previously proposed hypothesis that cardiovascular autonomic dysfunction
(which can be quantified by HRV analysis) can be at least partially responsible
for the increased mortality in PD patients2020 . Friedrich C, Rüdiger H, Schmidt C, Herting B, Prieur S,
Junghanns S et al. Baroreflex sensitivity and power spectral analysis in
different extrapyramidal syndromes. J Neural Transm. 2008;115(11):1527-36.
http://dx.doi.org/10.1007/s00702-008-0127-3
https://doi.org/10.1007/s00702-008-0127-...
. Lastly, the absence of a second control group of
age-matched healthy subjects was the main limitation of this study, primarily
since HRV decreases with age. Yet it has been reported that aging process has no
influence on systolic BPV3030 . Fluckiger L, Boivin JM, Quilliot D, Jeandel C, Zannad F.
Differential effects of aging on heart rate variability and blood pressure
variability. J Gerontol A Biol Sci Med Sci. 1999;54(5):B219-24.
http://dx.doi.org/10.1093/gerona/54.5.b219
https://doi.org/10.1093/gerona/54.5.b219...
.
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» https://doi.org/10.1152/ajpheart.00438.2005 -
24Langager AM, Hammerberg BE, Rotella DL, Strauss HM. Very low-frequency blood pressure variability depends on voltage-gated L-type Ca2+ channels in conscious rats. Am J Physiol Heart Circ Physiol. 2007;292(3):H1321-7. http://dx.doi.org/10.1152/ajpheart.00874.2006
» https://doi.org/10.1152/ajpheart.00874.2006 -
25Barbic F, Perego F, Canesi M, Gianni M, Biagiotti S, Constantino G et al. Early abnormalities of vascular and cardiac autonomic control in Parkinson's disease without orthostatic hypotension. Hypertension. 2007;49(1):120-6. http://dx.doi.org/10.1161/01.HYP.0000250939.71343.7c
» https://doi.org/10.1161/01.HYP.0000250939.71343.7c -
26Oka H, Toyoda C, Yogo M, Mochio S. Cardiovascular dysautonomia in de novo Parkinson's disease without orthostatic hypotension. Eur J Neurol. 2011;18(2):286-92. http://dx.doi.org/10.1111/j.1468-1331.2010.03135.x
» https://doi.org/10.1111/j.1468-1331.2010.03135.x -
27Hughson RL, Maillet A, Dureau G, Yamamoto Y, Gharib C. Spectral analysis of blood pressure variability in heart transplant patients. Hypertension. 1995;25(4 Pt 1):643-50. http://dx.doi.org/10.1161/01.hyp.25.4.643
» https://doi.org/10.1161/01.hyp.25.4.643 -
28Rosengård-Bärlund M, Bernardi L, Holmqvist J, Debarbieri G, Mäntysaari M, Björkesten C-G et al. Deep breathing improves blunted baroreflex sensitivity even after 30 years of type 1 diabetes. Diabetologia. 2011;54(7):1862-70. http://dx.doi.org/10.1007/s00125-011-2164-y
» https://doi.org/10.1007/s00125-011-2164-y -
29Estañol B, Delgado G, Bertado N, Callejas C, Medina Z, Infante O et al. Loss of heart rate variability in Parkinson's disease shown by the Poincaré plots during rhytmic breathing. Neurology. 2012;78(Meeting Abstracts 1):P05.196. http://dx.doi.org/10.1212/wnl.78.1_meetingabstracts.p05.196
» https://doi.org/10.1212/wnl.78.1_meetingabstracts.p05.196 -
30Fluckiger L, Boivin JM, Quilliot D, Jeandel C, Zannad F. Differential effects of aging on heart rate variability and blood pressure variability. J Gerontol A Biol Sci Med Sci. 1999;54(5):B219-24. http://dx.doi.org/10.1093/gerona/54.5.b219
» https://doi.org/10.1093/gerona/54.5.b219
Publication Dates
-
Publication in this collection
Oct 2014
History
-
Received
28 Feb 2014 -
Reviewed
25 June 2014 -
Accepted
15 July 2014