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STROKEAHA.117.018974

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Original Contribution
Prevalence and Natural History of Superficial Siderosis
A Population-Based Study
Michael Pichler, MD; Prashanthi Vemuri, PhD; Alejandro A. Rabinstein, MD;
Jeremiah Aakre, MPH; Kelly D. Flemming, MD; Robert D. Brown, Jr, MD; Neeraj Kumar, MD;
Kejal Kantarci, MD; Walter Kremers, PhD; Michelle M. Mielke, PhD;
David S. Knopman, MD; Clifford R. Jack, Jr, MD; Ronald C. Petersen, MD; Val Lowe, MD,
Jonathan Graff-Radford, MD
Downloaded from http://stroke.ahajournals.org/ by guest on October 25, 2017
Background and Purpose—Superficial siderosis (SS) is characterized by hemosiderin deposition in the superficial layers
of the central nervous system and can be seen during postmortem examination or with iron-sensitive magnetic resonance
imaging techniques. The distribution of SS may predict the probable underlying cause. This study aimed to report the
prevalence and natural history of SS in a population-based study.
Methods—Brain magnetic resonance imaging scans from the MCSA (Mayo Clinic Study of Aging), a population-based
study of residents 50 to 89 years of age in Olmsted County, Minnesota, were reviewed. Participants with imaging
consistent with SS were identified from 2011 through 2016. An inverse probability weighting approach was used to
convert our observed frequencies to population prevalence of SS. Additional data abstracted included amyloid positron
emission tomography, Apolipoprotein E genotype, coexisting cerebral microbleeds, and extent of SS.
Results—A total of 1412 participants had eligible magnetic resonance imaging scans. Two participants had infratentorial
SS, restricted to the posterior fossa. Thirteen participants had cortical SS involving the cerebral convexities (7 focal
and 6 disseminated). Only 3 of the participants with cortical SS (23%) also had cerebral microbleeds. The population
prevalence of SS was 0.21% (95% confidence interval, 0–0.45) in those 50 to 69 years old and 1.43% (confidence
interval, 0.53–2.34) in those over 69 years old. Apolipoprotein E ε2 allele was more common in those with SS (57.1%
versus 15.0%; P<0.001). Compared with participants without SS, those with SS were also more likely to have a positive
amyloid positron emission tomographic scan (76.9% versus 29.8%; P<0.001).
Conclusions—SS may be encountered in the general elderly population. The association with increased amyloid burden
and Apolipoprotein E ε2 genotype supports cerebral amyloid angiopathy as the most common mechanism. Longitudinal
follow-up is needed to evaluate the risk of subsequent hemorrhage in cases of incidentally discovered SS. (Stroke.
2017;48:00-00. DOI: 10.1161/STROKEAHA.117.018974.)
Key Words: cerebral hemorrhage ◼ hemosiderin ◼ magnetic resonance imaging ◼ prevalence
S
uperficial siderosis (SS) is characterized by hemosiderin
deposition in the superficial layers of the central nervous
system and can be seen during postmortem examination
or with iron-sensitive magnetic resonance imaging (MRI)
techniques.1,2
The distribution of SS may predict the probable underlying
cause. In classical or infratentorial SS, hemosiderin deposition occurs in the posterior fossa, brain stem, and spinal cord
with chronic intermittent bleeding into the subarachnoid space
identified as a potential cause.3 Bleeding is often caused by
dural or nerve root pathologies, prior surgeries, or tumors.
These patients typically present with slowly progressive cerebellar ataxia and sensorineural hearing loss.4
In contrast, cortical SS (cSS) refers to hemosiderin deposition restricted to the cerebral convexities and is associated
with cerebral amyloid angiopathy (CAA), an age-related disease of cerebral vasculature caused by β-amyloid deposition
within the walls of small cortical and leptomeningeal arteries.2,5 cSS has been suggested as a useful radiological finding
to establish a diagnosis of CAA.6,7
The prevalence and clinical significance of SS in the general elderly population remains unclear. The aim of this study
was to report the prevalence of SS in a population-based study
and to determine the clinical outcome of SS.
Materials and Methods
The MCSA (Mayo Clinic Study of Aging) is a population-based
study in Olmsted County, Minnesota. Details of the MCSA have
been published previously.8 In brief, Olmsted County residents 50
to 89 years of age were enumerated using Rochester Epidemiology
Received August 2, 2017; final revision received August 30, 2017; accepted September 21, 2017.
From the Department of Neurology (M.P., A.A.R., K.D.F., R.D.B., N.K., M.M.M., D.S.K., R.C.P., J.G.-R.), Department of Radiology (P.V., K.K., C.R.J.,
V.L.), and Department of Health Sciences Research (J.A., W.K., M.M.M.), Mayo Clinic, Rochester, MN.
Correspondence to Jonathan Graff-Radford, MD, Mayo Clinic College of Medicine, 200 1st St SW, Rochester, MN 55905. E-mail Graff-Radford.
Jonathan@mayo.edu
© 2017 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org
DOI: 10.1161/STROKEAHA.117.018974
1
2 Stroke December 2017
Downloaded from http://stroke.ahajournals.org/ by guest on October 25, 2017
Project resources.9 Eligible subjects were sampled from the population and invited to participate. Recruitment started in 2004, with a
subset undergoing a research MRI and Pittsburgh compound B (PiB)
positron emission tomographic (PET) scans. MRI was performed on
one of three 3T scanners from the same vendor (General Electric,
Waukesha, WI). MRI sequences sensitive to hemosiderin, a T2* gradient echo (repetition time/echo time=200/20 ms; flip angle=12°;
field of view=20 cm; in-plane matrix=256×224; phase field of
view=1.00; slice thickness=3.3 mm), were introduced in October
2011. The Figure demonstrates patient ascertainment.
The study protocols were approved by the Mayo Clinic and
Olmsted Medical Center Institutional Review Boards. All subjects
provided signed informed consent to participate in the study and in
the imaging protocols.
Brain MRI scans were reviewed and documented by a boardcertified neuroradiologist for abnormalities. The radiological report
was searched for the terms SS or hemosiderin deposition. All MRI
scans were also systemically reviewed by a trained image analyst,
and areas of hemosiderin deposition including SS were identified.
Findings from the radiology report and analyst review were confirmed by a vascular neurologist. Participants with SS were identified with the following inclusion criteria: (1) initial head MRI from
October 2011 through June 2016 showing linear pattern of hypointensity on gradient echo imaging consistent with SS. Participants
with an alternative explanation for MRI findings, such as aneurysmal subarachnoid hemorrhage, intracranial surgery, or significant
head trauma, were not counted as SS. Additional data abstracted
included age at the time of MRI, cognitive status, medications,
PiB-PET imaging, Apolipoprotein E (APOE) genotype, number
and location of coexisting cerebral microbleeds (CMBs), and extent
of cSS. Cognitive status was categorized as normal, mild cognitive impairment, or dementia based on consensus diagnosis from
clinician, neuropsychologist, and study coordinator. The details of
the cognitive evaluation have previously been published.8 PiB-PET
findings were classified as PiB positive if the standardized uptake
value ratio was >1.42.10 CMBs were defined according to consensus criteria11 as homogenous hypointense lesions in the gray matter
or white matter distinct from iron or calcium deposits and vessel
flow voids on T2* gradient echo. Location of CMBs was classified
as lobar, deep, or combination. Similar to prior publications,6 the
extent of cSS was defined as focal if restricted to 3 or fewer sulci
or disseminated if affecting >3 sulci. Cases of SS were further categorized as either infratentorial SS or cSS based on distribution of
hemosiderin deposition. Cases involving only the posterior fossa
(cerebellum and brain stem) were considered infratentorial SS,
whereas those with hemosiderin deposition restricted to supratentorial locations (superficial layers of cerebral cortex) were defined as
cSS.2 In participants with a diagnosis of SS, serial MRI scans were
reviewed when available to evaluate for progression of SS, CMBs,
or hemorrhage. However, only the initial MRI scan obtained during
the study period was used when calculating prevalence. The electronic medical record was reviewed to evaluate for interval events
such as symptomatic hemorrhage or stroke.
Statistical Analysis
Descriptive statistics including the median and interquartile range
for continuous variables and the frequency and percent for categorical variables were used to summarize participant characteristics by
the presence of SS. When comparing those with SS to those without
SS, Kruskal–Wallis tests were performed for continuous measures,
whereas χ2 tests (or Fisher exact test where appropriate) were performed for categorical measures.
Logistic regression models were used to determine whether age at
imaging, mild cognitive impairment or dementia status at imaging,
presence of an APOE ε2 allele, or abnormal PiB-PET scan was associated with SS. Each covariate was considered individually with age
to explore confounding as well as in multivariable models. Our final
multivariate model included adjustment for age, abnormal PiB-PET,
and presence of an APOE ε2 allele.
Frequencies of SS were calculated following the original sampling scheme by dividing the number of observed SS by the number
of imaged participants per age/sex strata. A 2-stage inverse probability weighting approach was used to adjust observed frequencies
for 2 possible causes for bias: study nonparticipation and imaging
nonparticipation.12,13 We derived weights from a logistic regression
model adjusting for age, sex, and education for whether an individual
recruited ultimately had an in-person MCSA study visit during the
time period studied. Further covariates abstracted from the medical
record were also considered for inclusion into the logistic models with
very little effect so the weights derived using age, sex, and education
were used. Similarly, weights were derived among those who had an
in-person MCSA study visit on whether or not they had a usable MRI
scan for SS ascertainment adjusting for age, sex, education, and mild
cognitive impairment/dementia prevalence at recruitment for imaging. These 2 sets of weights were then multiplied to give each imaged
participant a single weight to adjust their observation. The frequency
of SS was then standardized to the Olmsted County population (2010
Census) directly by age and sex according to our population-based
sampling to give population prevalence estimates.14,15 All statistical
testing presented was performed at the conventional 2-tailed α level
of 0.05. All analyses were performed using SAS, version 9.4 (SAS
Institute, Cary, NC).
Results
Figure. Algorithm of patient ascertainment. cSS indicates cortical
superficial siderosis; MCSA, Mayo Clinic Study of Aging; MRI,
magnetic resonance imaging; and SS, superficial siderosis.
Among a total of 1412 participants who had eligible MRI
scans, 1381 (98%) had APOE data, and 1239 (88%) had PiB/
PET. Eleven participants were identified through the radiology report with an additional 4 identified through the trained
analysts. Two participants had infratentorial SS (0.14%), and
13 had cSS (0.92%). When stratified by age, the observed
Pichler et al Prevalence of Superficial Siderosis 3
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frequency of SS was 0.39% in those 50 to 69 years old, with
estimated population prevalence 0.21% (95% confidence
interval [CI], 0–0.45). The observed frequency was 1.89% in
those over 69 years old, with estimated prevalence 1.43% (CI,
0.53–2.34). The overall estimated population prevalence in
those 50 to 89 years old was 0.56% (CI, 0.25–0.86).
Demographics of participants with and without SS are
shown in Table 1. The presence of an APOE ε4 allele did
not differ between those with and without SS (28.6% versus
28.5%; P=0.99). Presence of an APOE ε2 allele was more
common in those with SS (57.1% versus 15.0%; P<0.001).
Participants with SS were also more likely to be PiB positive
(76.9% versus 29.8%; P<0.001). In logistic regression models (Table 2), SS was associated with an elevated (positive)
PiB standardized uptake value ratio (odds ratio, 5.68; 95%
CI, 1.33–24.22; P=0.019) and the APOE ε2 allele (odds ratio,
10.67; 95% CI, 3.23–35.28; P<0.001) after adjusting for age
at imaging.
APOE and PiB-PET results were reviewed further based on
location of SS. Seven of 12 participants with cSS and APOE
data available (58.3%) were APOE ε2 positive; neither of the
participants with infratentorial SS had an APOE ε2 allele. Of
those with PiB-PET results available, 9 participants with cSS
(75%) and 1 participant (50%) with infratentorial SS were PiB
positive. Table 3 describes the clinical, genetic, and imaging
features for participants with SS. Of the 13 participants with
cSS, 9 (69%) were on aspirin at the time of diagnosis and none
were on anticoagulation. Seven participants had focal cSS,
and 6 had disseminated involvement. None of the participants
with focal cSS had associated CMBs, but 3 of the 6 (50%)
with disseminated cSS had associated CMBs (range 1–90).
Three participants with cSS (1 focal, 2 disseminated) had
follow-up MRI scans a mean of 31.3 months after the initial scan. There was no further hemorrhage in the participant
with focal cSS. However, both of the participants with disseminated cSS and follow-up MRI experienced additional
hemorrhage: one with multiple new asymptomatic CMBs and
one with multiple new CMBs and symptomatic lobar intracerebral hemorrhage distant to the site of cSS.
Discussion
Our findings indicate that cSS can be seen in ≈1% of people
over age 70 in the general population. The subset of individuals with disseminated cSS and associated microbleeds may be
at risk of developing additional hemorrhage, including lobar
hematomas, but future studies will be necessary to confirm this
increased risk. The association of cSS with APOE ε2 allele,
which is a risk factor lobar hemorrhage, further supports an
increased risk of hemorrhage among these individuals.
The overall prevalence of SS in our study was similar to
another epidemiological study, the Rotterdam study, which
focused only on those with cSS. That study found cSS in
0.7% of nondemented elderly individuals, all with coexisting lobar CMBs suggestive of CAA.16 Unlike the Rotterdam
study, the majority (10 of 13) of our cSS cases occurred in
the absence of CMBs. Our study extends the findings of the
Rotterdam study by including (1) PiB-PET and APOE profiles and (2) participants with infratentorial SS. The association of cSS with increased brain β-amyloid burden and
the APOE ε2 genotype in our study provides supportive evidence of CAA as a possible cause of cSS in older patients,
but none of the participants with cSS had pathological confirmation.17 APOE ε2 has previously been associated with
both focal and disseminated cSS in patients with pathologically proven CAA.18,19
The finding that cSS occurs in the absence of CMBs is not
surprising. Among patients with CAA, the presence of cSS
has been associated with a lower CMB burden.19 Increased
CMB count has been associated with APOE ε4.19 The variations in clinical and imaging characteristics among patients
with CAA suggest that although APOE ε2 and ε4 are both
risk factors for CAA, they present with different phenotypes
Table 1. Characteristics of Participants With and Without Superficial Siderosis
Characteristic*
Negative SS (n=1397)
Positive SS (n=15)
Total (n=1412)
P Value
Age, y
68 (62, 77)
79 (74, 85)
68 (62, 78)
0.002†
Male
736 (52.7)
10 (66.7)
746 (52.8)
0.28‡
Education, years
15 (12, 16)
15 (13, 17)
15 (12, 16)
0.60†
MCI/dementia at MRI
134 (9.6)
4 (26.7)
138 (9.8)
0.027‡
Presence of APOE ε4 allele§
389 (28.5)
4 (28.6)
393 (28.5)
0.99‡
Presence of APOE ε2 allele§
205 (15.0)
8 (57.1)
213 (15.4)
<0.001‡
Global PiB ratio‖
1.35 (1.28, 1.47)
1.96 (1.54, 2.19)
1.35 (1.28, 1.48)
0.002†
Abnormal PiB¶
365 (29.8)
10 (76.9)
375 (30.3)
<0.001‡
APOE indicates apolipoprotein E; MCI, mild cognitive impairment; MRI, magnetic resonance imaging; PiB, Pittsburgh compound
B; and SS = superficial siderosis.
*Data are presented as n (%), except for age, education, and global PiB ratio, which are presented as median (Q1, Q3).
†Kruskal–Wallis.
‡χ2.
§APOE status unavailable in 30 participants with negative SS and 1 with positive SS.
‖Standardized uptake value ratio (SUVR) determined by voxel size–weighted average, gray matter+white matter sharpening, no
partial volume correction, and cerebellar crus reference.
¶Abnormal PiB defined as PiB ratio >1.42; information unavailable in 171 participants with negative SS and 2 with positive SS.
4 Stroke December 2017
Table 2. Multivariate Logistic Model for Superficial Siderosis
Odds Ratio
95% CI
P Value
1.06
0.98–1.14
0.13
Abnormal PiB ratio*
5.68
1.33–24.22
0.019
Any APOE ε2 allele†
10.67
3.23–35.28
<0.001
Age at MRI
Estimates reported from a single multivariate logistic model for SS adjusting
for age at MRI, abnormal PiB ratio and APOE ε2 presence. APOE, apolipoprotein
E; CI, confidence interval; MIR, magnetic resonance imaging; and; PiB,
Pittsburgh compound B.
*PiB data unavailable in 171 participants with negative SS and 2 with positive SS.
†APOE status unavailable in 30 participants with negative SS and 1 with
positive SS.
Downloaded from http://stroke.ahajournals.org/ by guest on October 25, 2017
and may contribute to CAA-related hemorrhage through
distinct mechanisms.19,20 The APOE ε2 allele is associated
with a reduced risk of Alzheimer dementia but a higher risk
of clinical intracerebral hemorrhage, whereas the APOE
ε4 allele is a risk factor for both Alzheimer dementia and
CAA.20
cSS is a risk factor for CAA-related hemorrhage, independent of CMB burden.21,22 The ability to determine which
patients are at increased risk of hemorrhage may influence
decisions on antithrombotic medications. CAA is an important cause of warfarin-associated lobar intracerebral hemorrhage in the elderly, and APOE ε2 status is overrepresented
among these patients.23 The 2 participants with interval hemorrhage during follow-up had disseminated cSS and CMBs at
the time of the initial MRI. This finding supports prior studies
demonstrating extent of cSS and number of CMBs as important risk factors for future hemorrhage.21,24
The prevalence of SS is low, and associations of SS with
APOE status and PiB-PET results must be interpreted cautiously in the setting of such small numbers which limits the
generalizability. In addition, some participants were missing
information such as APOE status, PiB-PET results, and cognitive profile. Lack of follow-up data in a majority of eligible
participants with SS is another limitation and limits our ability
to estimate the risk of subsequent hemorrhage. Although most
participants with siderosis had multiple MRI scans, a minority had subsequent scans after diagnosis of SS because gradient echo imaging was introduced in October 2011. Although
a strength of this study is that we were able to account for 2
potentially large sources of bias, study nonparticipation and
imaging nonparticipation bias, through inverse probability
weighting, unmeasured bias not accounted for by this technique remains a possibility.
Summary
CAA exists on a continuum with additional factors such as
APOE status influencing disease progression. Asymptomatic
cases of focal cSS may represent an early manifestation of
CAA, and more extensive longitudinal follow-up is needed
to determine whether these participants develop CMBs,
disseminated cSS, or intracerebral hemorrhage. Detecting
imaging changes while still asymptomatic is an important
way to track the disease course and to identify risk factors
for progression.
Sources of Funding
Research reported in this publication was supported by the National
Institute on Aging of the National Institutes of Health (NIH) under
Table 3. Characteristics of Participants With SS
Focal cSS*
Disseminated cSS*
Infratentorial SS
Age, Years
Sex
Antithrombotic Use
No. of Cerebral
Microbleeds on Initial
Scan (Location)
86
M
Aspirin 81 mg
0
82
F
None
0
No
No
79
F
Aspirin 81 mg
0
Yes
Yes
78
M
Aspirin 81 mg
0
No
Yes
74
M
Aspirin 81 mg
0
Yes
Yes
71
F
Aspirin 81 mg
0
No
No
62
M
None
0
Yes
No
88
M
None
0
No
Unavailable
87
F
Aspirin 81 mg
0
Yes
Yes
82
M
Aspirin 325 mg
0
Yes
Yes
80
M
Aspirin 325 mg
1 (lobar)
Yes
Yes
79
F
Aspirin 81 mg
16 (lobar)
Yes
Yes
Any APOE ε2
Allele
Abnormal
PiB-PET
No
Yes
76
M
None
90 (lobar)
Unavailable
Yes
61
F
None
0
No
No
85
M
None
0
No
Yes
APOE indicates apolipoprotein E; cSS, cortical superficial siderosis; PiB-PET, Pittsburgh compound B positron emission tomography;
and SS, superficial siderosis.
*Extent of cSS involvement was defined as focal (restricted to ≤3 sulci) or disseminated (>3 sulci).
Pichler et al Prevalence of Superficial Siderosis 5
Award Number K76AG057015 (PI: Dr Graff-Radford) and NIH
grants R01 NS097495 (PI: Dr Vemuri), U01 AG06786 (PI: Dr
Petersen), P50 AG16574 (PI: Dr Petersen), R01 AG034676 (PI:
Dr Rocca), R01 AG11378 (PI: Dr Jack), R01 AG041851 (PIs:
Drs Jack and Knopman); the Gerald and Henrietta Rauenhorst
Foundation grant, the Alexander Family Alzheimer’s Disease
Research Professorship of the Mayo Foundation, and the Elsie and
Marvin Dekelboum Family Foundation. The funding sources were
not involved in the article review or approval. MCSA (Mayo Clinic
Study of Aging) data were as follows: U01 AG006786: (Dr Petersen)
Mayo Clinic Study of Aging (MCSA); P50 AG016574: (Dr Petersen)
Alzheimer’s Disease Research Center (ADRC); R01 AG034676: (Dr
Rocca) Rochester Epidemiology Project (REP); R01 AG011378:
(Dr Jack) Evaluating and Extending Our Hypothetical Model of
Alzheimer’s Biomarkers; R01 AG041851: (Drs Jack/Knopman)
Validating the New Criteria for Preclinical Alzheimer’s disease;
and R01 NS097495: (Dr Vemuri) Development, Validation, and
Application of an Imaging-based CVD Scale.
Disclosures
Downloaded from http://stroke.ahajournals.org/ by guest on October 25, 2017
Dr Vemuri receives research support from the National Institues
of Health (NIH)/National Institute of Aging (NIA). Dr Kremers
receives research funding from NIH, Department of Defense, Agency
for Healthcare Research and Quality, AstraZeneca, and Roche. Dr
Mielke is a consultant for Eli Lilly and Lysosomal Therapeutics,
Inc. She receives research grants from the NIH/NIA, Department of
Defense, Biogen, Roche, and Lundbeck. Dr Knopman serves on a
Data Safety Monitoring Board for Lundbeck Pharmaceuticals and
for the DIAN study (Dominantly Inherited Alzheimer Network);
is an investigator in clinical trials sponsored by Biogen, TauRX
Pharmaceuticals, Lilly Pharmaceuticals, and the Alzheimer’s Disease
Cooperative Study; and receives research support from the NIH. Dr
Jack receives research support from the NIH/NIA, and the Alexander
Family Alzheimer’s Disease Research Professorship of the Mayo
Foundation. Dr Petersen serves on data monitoring committees for
Pfizer, Inc, Janssen Alzheimer Immunotherapy; is a consultant for
Biogen, Roche, Inc, Merck, Inc, and Genentech, Inc; receives publishing royalties from Mild Cognitive Impairment (Oxford University
Press, 2003); and receives research support from the National
Institute of Health. Dr Graff-Radford is supported by NIH/NIA, the
Mayo Clinic Myron and Jane Hanley Career Development Award in
Stroke Research. The other authors report no conflicts.
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Prevalence and Natural History of Superficial Siderosis: A Population-Based Study
Michael Pichler, Prashanthi Vemuri, Alejandro A. Rabinstein, Jeremiah Aakre, Kelly D.
Flemming, Robert D. Brown Jr, Neeraj Kumar, Kejal Kantarci, Walter Kremers, Michelle M.
Mielke, David S. Knopman, Clifford R. Jack Jr, Ronald C. Petersen, Val Lowe and Jonathan
Graff-Radford
Stroke. published online October 25, 2017;
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