Original Paper

Neuroepidemiology 2021;55:56–61 Received: May 13, 2020

Accepted: October 25, 2020
DOI: 10.1159/000512697 Published online: February 18, 2021

Interrelationships between Survival,

Sex, and Blood Pressure in Patients with
Multiple System Atrophy

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Tanya Gurevich a, b, c Ludmila Merkin b Alina Rozenberg d Ariel Fisher e
Elly Atanasova Mishkova-Serafimova a Dina Klepikov a Nir Giladi a, b, c
Chava Peretz b, d
aMovement Disorders Unit and Neuroautonomic Service, Neurological Institute, Tel-Aviv Medical Center, Tel-Aviv,

Israel; bSackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel; cSagol School of Neuroscience, Tel-Aviv
University, Tel-Aviv, Israel; dSchool of Public Health, Tel-Aviv University, Tel-Aviv, Tel-Aviv, Israel; eDiagnostic
Radiology Department University of Rochester Medical Center, Rochester, NY, USA

Keywords fer between the groups {medians: 12 years (95% confidence

Multiple system atrophy · Survival · Sex · Blood pressure
changes · Orthostatic hypotension
Abstract
Objective: The aim of this study is to estimate survival among
patients with multiple system atrophy-parkinsonian type
(MSA-P) or cerebellar type MSA (MSA-C) in relation to blood
pressure (BP) measurements, by sex. Methods: A cohort of
99 MSA patients was studied retrospectively. Their BP mea-
surements were obtained during prolonged (40 min, vertical
position) drug-free tilt testing. We used K-M survival curves
and Cox regression to calculate adjusted (to age of onset)
hazard ratios (HRs) of BP measurements on time to death by
MSA subtype and sex. Results: Fifty-two MSA patients were
males and 47 were females. Sixty-three of them had MSA-P
and 36 had MSA-C. The mean age at motor symptom onset
was 61.1 ± 10.4 years, and mean disease duration at the time
of BP assessment was 8.0 ± 4.7 years. The 2 study groups
(MSA-P and MSA-C) did not differ significantly in age at MSA
onset, sex ratio, or disease duration. Survival time did not dif-
interval [CI]: 8–28) and 10 years (95% CI: 8–13), respectively}.
The MSA-P group showed a trend towards better survival for
males (log-rank p = 0.0925). The maximal diastolic orthostat-
ic BP decline during tilt testing had a borderline positive as-
sociation with death risk among MSA-C males (adjusted
HR = 1.18, p = 0.0665), and systolic BP after 10 min in a supine
position had a significant positive association with death risk
among MSA-P males (adjusted HR = 1.06, p = 0.0354). Con-
clusions: The findings of a sex-based difference in the effect
of BP on death risk may be important for adjusting the ther-
apeutic approach to MSA patients. © 2021 S. Karger AG, Basel
Introduction
Multiple system atrophy (MSA) is a rapidly progres-
sive, adult-onset neurodegenerative disorder. The surviv-
al prognosis from onset of the first symptom has great
variability from case to case, with a large mean survival
range of 6–10 years [1–5]. MSA patients with prolonged

karger@karger.com © 2021 S. Karger AG, Basel Tanya Gurevich

www.karger.com/ned Tel-Aviv Sourasky Medical Center, Movement Disorders Unit
Neurological Institute
6 Weizmann Street, Tel-Aviv 6423906 (Israel)
tanyag @ tlvmc.gov.il
survival (≥15–20 years) have recently been described in
the literature [6–8]. Different factors were proposed for
determining the survival length, and the data continue to
be controversial, although most of the recent studies link
the reduced survival to the severity and time of onset of
the autonomic failure in the course of the disease [1–3,
9–11]. One of the typical, disabling, and frequent symp-
toms of MSA is highly unstable blood pressure (BP) with
orthostatic hypotension (OH) [12], which is often accom-
panied by supine hypertension [13–15]. The tilt-table test
(tilt test) is an accepted method of cardiovascular auto-
nomic function assessment whose results, together with
those of other tests, may reflect the prognosis of MSA.
Based on the facts that OH has been described as an in-
dependent predictor of all-cause mortality [16, 17] and
that OH is one of the definitive diagnostic criteria of
MSA, we speculated that the severity of an orthostatic BP
drop (OBPD) will affect the survival of MSA patients and
that survival might differ between sexes as seen in other
diseases [18–21]. OH is defined as a sustained reduction
of systolic BP (SBP) of at least 20 mm Hg or of diastolic
BP (DBP) of 10 mm Hg within 3 min of standing or head-
up tilt to at least 60° on a tilt table [12]. Supine hyperten-
sion is defined as a SBP ≥140 mm Hg and/or DBP ≥90
mm Hg, measured after at least 5 min of rest in the supine
position [13]. We were interested in the values of BP
drops after 10–40 min and/or absolute supine BP values
since they might be risk factors for common OH that has
been proven to be associated with falls. Our aim in the
present study was to investigate the effect of BP parame-
ters, as measured by tilt-table testing, on survival in 2 sub-
types MSAs and by sex.
Methods
Study Population
We conducted a retrospective cohort study based on the clin-
ical recordings of MSA patients who were being followed in the
Movement Disorders Unit of the Neurological Institute of Tel-
Aviv Medical Center. All of these patients underwent a prolonged
(40-min), 70° head-up tilt-test in the Neuroautonomic Labora-
tory, which was performed with the aim of supporting the diag-
nosis and adjusting the treatment. A total of 97 patients fulfilled
diagnostic criteria for probable MSA [11], and 2 patients had def-
inite MSA according to pathological diagnosis postmortem. They
were divided into subgroups according to whether they had par-
kinsonian MSA (MSA-P) or cerebellar syndrome MSA (MSA-C).
The follow-up period for each patient was measured from the
date of the first appearance of motor or nonmotor symptoms, as
reported by the patient, to either study closure or death (dates of
demise were derived from records of the Israeli Interior Minis-
try).
Interrelationships between Survival, Sex,
and Blood Pressure in MSA Patients
Tilt-Test Procedure and Blood Pressure Measurements
BP and heart rate were measured manually after 10 min of lying
supine on an examining table (baseline) and then at minutes 1, 2,
3, 5, 10, 15, 20, 25, 30, 35, and 40 in a head-up position at an angle
of 70°. All tests were performed by the same physician who also
recorded the patients’ complaints during the procedure. The pa-
rameters that were included in our analyses were maximal ortho-
static drop of SBP and DBP during the tilt test and 10 min of supine
SBP and DBP measurements. We analyzed the maximal BP deltas
during the prolonged tilt-table test based on the widely accepted
concept of delayed OH and on the recent findings that most MSA
patients develop OH after more than 3 min of standing [21, 22].
Statistics
We stratified the cohort by MSA subtype and sex. Only patients
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for whom there was all relevant information were included in the
analyses.
Baseline characteristics of the 2 subgroups were compared us-
ing t test and χ2 test. Kaplan-Meier curves were used to describe
time from disease onset to death, and log-rank tests to compare
between subgroups. Cox regressions were used to assess the hazard
ratios (HRs) for death in association with 10 min of supine BP
measurements and maximum BP drop on the tilt-test, controlling
for pulse, age at disease onset, and age at tilt testing. Statistical data
were processed using SAS software.
Results
Characteristics of the Study Subjects
There was a total of 99 MSA patients of whom 63 (64%)
had MSA-P and 36 had MSA-C (Table 1). The mean (±stan-
dard deviation) age at onset for the entire cohort was
61.1 ± 10.4 years, the mean disease duration was 8.0 ± 4.7
years, and 52 subjects (53%) were males. The 2 groups did
not differ significantly in age at symptom onset, sex ratio,
or disease duration. A further stratification by sex yielded
nonsignificant differences within each group.
Survival
The median survival of the MSA-P group was 12 years
(95% confidence interval [CI]: 8–28) and the median sur-
vival of the MSA-C patients was 10 years (95% CI: 8–13).
Survival curves did not differ significantly between
groups. A further stratification by sex (Fig. 1) yielded bor-
derline significant sex differences in the MSA-P group
(log-rank p = 0.0925) with a better survival for males.
There was no sex effect on survival in the MSA-C group.
The Association between BP Measures and Death Risk
We estimated the HRs for the potential effect of BP
measurements taken during the tilt test on time to death,
accounting for age at disease onset and age at tilt testing.
When the model included BP and pulse decline mea-
Neuroepidemiology 2021;55:56–61 57
DOI: 10.1159/000512697
Table 1. Characteristics of the MSA study patients by MSA subtype and sex (mean±SD)

MSA-P (n = 63) MSA-C (n = 36)

F (n = 28) M (n = 35) F (n = 19) M (n = 17)

Symptom onset age, years 61.9±9.7 60.7±11.6 60.4±10.0 61.2±10.0

Duration since symptom onset (motor or nonmotor), years 8.0±3.7 8.7±6.0 7.1±4.3 7.7±4.1
Follow-up, years 8.0±3.7 8.7±6.0 7.1±4.3 7.7±4.1
Death rate, % 54 31 37 47
Age at tilt test, years 65.0±10.4 64.9±11.6 63.1±9.7 63.6±11.2
Max SBP_drop 27.8±20.5 27.8±22.6 21.1±17.1 29.7±21.0
Max DBP_drop 15.8±22.0 12.0±12.3 8.4±9.6 14.6±12.1
Max pulse_drop 2.4±28.1 −6.9±12.7 −4.8±12.6 −2.9±7.4
SBP_10 min supine 135.2±20.4 140.0±20.5 137.9±15.9 135.7±20.3
DBP_10 min supine 76.1±15.3 80.6±11.6 74.0±21.5 81.8±8.7

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Pulse_10 min supine 71.7±22.2 70.3±14.5 77.6±12.9 72.8±10.0

MSA-P, parkinsonian MSA; MSA-C, cerebellar syndrome MSA; Max, maximum; BP, blood pressure; DBP, diastolic blood pressure;
SBP, systolic blood pressure; SD, standard deviation. The sex differences were nonsignificant in both MSA types for all variables.

Color version available online

1.0 + + + +
+
+
0.8 + +
+ +
+
Survival probability

0.6 + +
+ + + + +
+
0.4
+
Gender
+ +
0.2 Male
Female
+ + Censored
0
Fig. 1. K-M survival curve of sex difference 0 5 10 15 20 25
in survival (p = 0.0925) of MSA-P patients Duration, years
(n = 63) by sex. MSA-P, parkinsonian
MSA.

sures (Table 2, model 1) among the MSA-C patients, the
maximum DBP decline was found to have a borderline
significant positive association with death risk among
the males (HR = 1.18, p = 0.0665) but not among the
females. When the model included BP and pulse 10-min
supine measurements (Table 2, model 2), there was no
association between those measurements and death risk
among either the males or females. In contrast, there
was a significant positive association between the 10-
min supine SBP measurement and death risk (model 2)
for the male MSA-P patients (HR = 1.06, p = 0.0354),
and a borderline negative association (HR = 0.96, p =
0.0878) for the female MSA-P patients. The results for
model 1 did not differ between the MSA-P males and
females. In most models, age at onset and age at tilt test-
ing were found as either significant or borderline sig-
nificant covariates.
Discussion
The results of this retrospective study yielded that MSA-
P and MSA-C patients have similar age at disease onset and
similar survival time (median 12 years [95% CI: 8–28] and
10 years [95% CI: 8–13], respectively). These survival peri-
ods are longer than those reported in 2 recent studies [1, 2,

58 Neuroepidemiology 2021;55:56–61 Gurevich et al.

DOI: 10.1159/000512697
 Table 2. Association between BP and death risk: adjusted* HRs and p value, by MSA type and sex

MSA-P MSA-C
F M F M
HR, p value HR, p value HR, p value HR, p value

Model 1
Max SBP_drop 0.99, ns 1.05, ns 0.98, ns 0.92, ns
Max DBP_drop 1.00, ns 0.99, ns 1.05, ns 1.18, 0.0665
Max pulse_drop 1.00, ns 1.00, ns 0.98, ns 0.91, ns
Model 2
SBP_10 min supine 0.96, 0.0878 1.06, 0.0354 0.89, ns 0.97, ns
DBP_10 min supine 1.06, ns 0.93, ns 1.05, ns 1.08, ns
Pulse_10 min supine 0.96, ns 1.02, ns 0.97, ns 0.99, ns

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MSA-P, parkinsonian MSA; MSA-C, cerebellar syndrome MSA; F, female; M, male; HR, hazard ratio; Max,
maximum; BP, blood pressure; DBP, diastolic blood pressure; SBP, systolic blood pressure; HR, hazard ratio. * To
age at onset and age at tilt-testing.

11], and slightly longer than those cited in a number of
other reports [3–5, 10, 23]. Our findings of a higher sur-
vival were unexpected: they might have been due to differ-
ent criteria for the time of initial symptom onset or they
might reflect the longer life expectancy in the general pop-
ulation of Israel [24] and the referral of most MSA patients
to be treated and followed in a multidisciplinary special-
ized MSA clinic [25]. Our finding of a similar survival for
MSA-P and MSA-C patients is in line with most of the
other reports [1, 3–5, 10], with one exception [26].
Survival of male patients in our study was somewhat
better than that of female patients in the MSA-P group but
not in the MSA-C group. Conflicting results have been
reported regarding sex differences in the survival of MSA
patients. Longer survival was described in males in some
studies [24, 27], while others showed no difference [1, 3,
4, 5, 10, 27, 28], or longer survival in females [7, 11, 29, 30].
We further tried to associate between BP parameter
changes and death risk. There was no significant associa-
tion between BP parameters and survival in our cohort
taken. However, an analysis stratified by MSA type and
the patients’ sex did yield some different BP effects. Spe-
cifically, 10-min BP values in the supine position were
associated with increased mortality risk in the male MSA-
P patients and decreased mortality in the female MSA-P
patients. The severity of OBPD significantly increased the
mortality risk in the male MSA-C patients but not in the
female MSA-C patients (HR = 1.05, p = ns).
Tilt-testing was performed late in the course of the dis-
ease (the meantime from symptom onset to tilt testing
was 8.0 ± 4.7 years), demonstrating that it may help in
predicting survival in the later stages of the disease. This
may have therapeutic implications as well as importance
for the design and interpretation of future clinical studies.
Important strengths of our study are the consecutive
recruitment of MSA patients from 1 outpatient clinic and
the medium size of the cohort that allowed subgrouping
by MSA type and sex for investigating a possible interac-
tion between sex and BP. Another strength is the validity
of the BP measurements that were obtained during a uni-
fied prolonged (10 min lying and 40 min standing) tilt-
testing setting which enabled the identification of delayed
OBPD [22]. The main limitation of this study is its retro-
spective nature. However, all included patients met con-
sensus criteria for probable or possible MSA [12], and we
excluded those with competing diagnoses therefore the
likelihood of misdiagnosis is probably low [30]. We did
not evaluate other signs of autonomic failure and other
potential risk factors for death (i.e., sleep breathing disor-
ders, syncope and falls, injuries, urinary tract infections,
and urosepsis) other than OBPD and 10 min supine BP
value, and we had no information on the official cause of
death. However, intercurrent diseases had been consid-
ered during the diagnosis process (e.g., patients with a
clinical syndrome like the MSA but with autonomic fail-
ure which could be associated with diabetes were exclud-
ed). Our conclusions are based on the results of measure-
ments obtained during single prolonged tilt testing, and
we did not analyze heart rate fluctuations [31]. We fo-
cused on the amplitude of the BP fall upon standing, with-
out taking into account either the time needed to achieve
such a fall or the absolute lowest BP value reached upon

Interrelationships between Survival, Sex, Neuroepidemiology 2021;55:56–61 59

and Blood Pressure in MSA Patients DOI: 10.1159/000512697
standing or the upright mean BP, all of which were shown Statement of Ethics
to be important for clinical decision-making [32]. Finally,
This retrospective study was approved by the Institutional Re-
the results do not enable an assessment of the relative view Boards of Tel-Aviv Sourasky Medical Center, and patient
contribution of OBPD to survival compared to other au- consent was waived.
tonomic and nonmotor aspects of PD.
In conclusion, we have demonstrated a value of tilt
testing in the later stages of MSA for the prediction of Conflict of Interest Statement
survival. We also showed the effect of sex on the mortal-
ity risk of patients with higher supine BP in a group of The authors have no conflicts of interest to disclose.
patients with MSA-P and the effect of diastolic OBPD in
a group of patients with MSA-C. The findings of a sex dif-
ference in the effect of BP on mortality risk may have Author Contributors
clinical implications in terms of adjusting the therapeutic

Downloaded from http://karger.com/ned/article-pdf/55/1/56/3158088/000512697.pdf by Chulalongkorn University user on 11 May 2024

approach [33]. In addition, these data may be important
for the design and interpretation of future clinical studies.
Acknowledgements
The authors are thankful to Esther Eshkol for superb editorial
assistance and to all the staff of Movement Disorders Unit at the
Tel-Aviv Medical Center for the fruitful cooperation in this project.
T.G. and C.P. contributed to the conception and design of the
study. T.G., L.M., and E.A. collected data. C.P., T.G., and A.R.
worked on the analysis and interpretation of the data. T.G., C.P.,
and A.F. drafted the manuscript and N.G. revised it critically for
intellectual content. D.K. performed the tilt testing. All authors
gave their final approval of the revised version to be published.

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