DOI: 10.5137/1019-5149.JTN.8552-13.0

Case Report

Simultaneous Bilateral Hypertensive Putaminal or
Thalamic Hemorrhage: Case Report and Systematic
Review of the Literature
Eşzamanlı Bilateral Hipertansif Putaminal veya Talamik Kanama:
Olgu Sunumu ve Literatürün Sistematik Gözden Geçirilmesi
Kenichi KONO, Tomoaki TERADA
Wakayama Rosai Hospital, Department of Neurosurgery, Wakayama, Japan
Corresponding Author: Kenichi Kono / E-mail: [email-masked]

ABSTRACT
Simultaneous multiple hypertensive intracranial hemorrhage is rare, and its mechanism is unclear. We report a case of simultaneous
hypertensive bilateral thalamic hemorrhage. A 58-year-old man presented with sudden mild right hemiparesis. Computed tomography 1 hour
after the onset showed bilateral thalamic hemorrhage. Gradient-echo T2*-weighted magnetic resonance imaging showed 17 microbleeds. The
patient was treated with medication, discharged home, and achieved a modified Rankin scale of 1 at 3 months from the onset. Additionally, by
systematically searching in PubMed, we found 41 cases of simultaneous bilateral hypertensive putaminal or thalamic hemorrhage, including our
case: 18 bilateral putaminal, 12 bilateral thalamic, and 11 unilateral putaminal and contralateral thalamic hemorrhage. Symmetric hemorrhage
occurred more frequently than expected ratios of hemorrhage occurring randomly in terms of location (p=0.013; Fisher’s exact test). These
new findings raise the hypothesis that patients may have symmetrically vulnerable vessels. Such conditions would result in coincidence or
subsequent rupture of perforating arteries or micro-aneurysms by increased blood pressure and cause symmetric hemorrhages. Studies on
the distribution of microbleeds may address these issues.
Keywords: Simultaneous multiple intracranial hemorrhages, Hypertension, Microbleeds, Putaminal hemorrhage, Thalamic hemorrhage

ÖZ
Eş zamanlı çoklu hipertansif intrakraniyal kanama nadirdir ve mekanizması açık değildir. Bir eş zamanlı hipertansif bilateral talamik kanama
olgusu bildiriyoruz. 58 yaşında bir erkek ani hafif sağ hemiparezi ile geldi. Başlangıçtan 1 saat sonra bilgisayarlı tomografi bilateral talamik
kanama gösterdi. Gradiyent eko T2*-ağırlıklı manyetik rezonans görüntüleme 17 mikrokanama gösterdi. Hasta ilaçla tedavi edildi, eve
gönderildi ve başlangıçtan 3 ay sonra modifiye Rankin ölçeği değeri 1 bulundu. Ek olarak PubMed’de sistematik bir arama yaptığımızda
kendi olgumuz dahil 41 eş zamanlı bilateral hipertansif putaminal veya talamik kanama olgusu bulduk: 18 bilateral putaminal, 12 bilateral
talamik ve 11 unilateral putaminal ve kontralateral talamik kanama. Simetrik kanama, konum açısından rastgele beklenecek, beklenen kanama
oranlarından daha sık bulundu (p=0,013; Fisher kesin testi). Bu yeni bulgular hastalarda simetrik narin damarlar bulunabileceği hipotezini
düşündürmektedir. Bu gibi durumlar artmış kan basıncı nedeniyle perforan arterler veya mikroanevrizmaların aynı anda veya arka arkaya
rüptürüne yol açıp simetrik kanamalara neden olacaktır. Mikrokanamaların dağılımı konusunda çalışmalar bu konuları açıklığa kavuşturabilir.
ANAHTAR SÖZCÜKLER: Eş zamanlı çoklu intrakraniyal kanamalar, Hipertansiyon, Mikrokanamalar, Putaminal kanama, Talamik kanama

Introduction
Hypertensive intracranial hemorrhage (ICH) is generally
solitary. Simultaneous multiple ICHs are rare and associated
with hypertension, amyloid angiopathy, hemorrhagic infarction, coagulation defects, and sinus thrombosis (4, 11). The
incidence of multiple hypertensive ICHs is reported as 0.9%
to 4.7% (1, 11, 18, 20, 24, 28), and its mechanism is unclear. We
report a case of simultaneous hypertensive bilateral thalamic
hemorrhage, and review the literature and analyze data regarding the location of hemorrhage.
Case presentation
A 58-year-old man presented with sudden mild right

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hemiparesis. Computed tomography 1 hour after the
onset showed bilateral thalamic hemorrhage (Figure 1A).
Gradient-echo T2*-weighted magnetic resonance imaging
(MRI) showed 17 microbleeds (Figure 1B). There were
three microbleeds on each side of the putamen and two
microbleeds on each side of the thalamus. MRI and magnetic
resonance angiography showed no vessel abnormalities and
no other lesions, such as tumors. As the patient had a history
of hypertension and had stopped anti-hypertensive drugs by
his own decision, ICH was considered to be associated with
hypertension. The patient was treated with medication and
discharged home, and achieved a modified Rankin scale of 1
at 3 months from the onset.
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Kono K and Terada T: Simultaneous Bilateral Intracranial Hemorrhages

A

b

Figure 2: Distribution of locations of hemorrhage are shown.
Forty-one cases of simultaneous bilateral hypertensive
putaminal or thalamic hemorrhage were classified into three
categories: bilateral putaminal (Put-Put), unilateral putaminal
and contralateral thalamic (Put-Tha), and bilateral thalamic
hemorrhage (Tha-Tha). Actual and expected numbers of cases
are shown in the graph. The expected numbers were calculated
based on the assumption that hemorrhage occurs at random
in locations regardless of other hemorrhagic locations. Bilateral
symmetric hemorrhage (Put-Put and Tha-Tha) occurred more
frequently in the actual cases than in the expected cases.
Put = putamen; Tha = thalamus.

Review of the Literature and Statistical Analysis
We systematically searched the literature by PubMed using
several keywords, including “simultaneous”, “multiple”, “bilateral”, “hypertensive”, “hemorrhage/hematoma”, “intracranial/
Turk Neurosurg 2014, Vol: 24, No: 3, 434-437

Figure 1: A) Computed
tomography shows bilateral
thalamic hemorrhage.
B) Gradient-echo T2*weighted magnetic
resonance imaging shows
the hemorrhage and multiple
microbleeds.

intracerebral”, “thalamic/thalamus”, and “putaminal/putamen”.
We narrowed down articles by conditions that “simultaneous” and “hemorrhage/hematoma” appear in the titles. After
checking titles and abstracts, 23 articles on simultaneous
multiple hypertensive ICHs were found. There were 105 cases
of simultaneous multiple ICHs in the 23 articles and our case
report (1, 3, 5, 7-9, 11-15, 17-20, 22-29). In references in the
literature (5, 26), we found nine additional cases of simultaneous hypertensive ICH, which were all written in Japanese
and not cited by PubMed. We did not include these nine cases
because this could cause difficulty for other researchers to
trace our search and examine the statistical analysis. Among
the 105 cases, there were 10 non-hypertensive ICH and nine
hypertensive ICH without a description of the hemorrhagic
sites. Therefore, there remained 86 cases of simultaneous
multiple hypertensive ICHs with a description of the location
of hemorrhage. The locations of hemorrhage were the putamen (n=73), thalamus (n=49), subcortex (n=18), cerebellum
(n=16), pons (n=14), and caudate nucleus (n=2). We selected
cases of bilateral putaminal or thalamic hemorrhage because
the putamen and thalamus are the two most frequent locations of hypertensive ICH (29). One case of unilateral thalamic
and putaminal hemorrhage was excluded from this study.
Finally, we analyzed 41 cases of simultaneous bilateral hypertensive putaminal or thalamic hemorrhage, including our
case. The mean age ± standard deviation was 60.6±12.0 years
(range, 35–89 years). There were 24 males and 17 females.
There were 18 bilateral putaminal, 12 bilateral thalamic, and
11 unilateral putaminal and contralateral thalamic hemorrhage cases. There were 47 hemorrhagic sites in the putamen
(57%; a=0.57) and 35 in the thalamus (43%; b=0.43). If hemorrhage randomly occurred in terms of location, regardless of
the location of other hemorrhages, the expected ratios of
hemorrhagic locations were 33% (a2), 18% (b2), and 49% (2ab)

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Kono K and Terada T: Simultaneous Bilateral Intracranial Hemorrhages

at the bilateral putamen, bilateral thalamus, and unilateral
putamen and contralateral thalamus, respectively. We performed statistical analysis using SPSS version 20 (IBM Corp.,
Armonk, NY, USA). p<0.05 was considered as significant. Symmetric hemorrhage occurred significantly more frequently in
41 cases compared with the expected ratios (p=0.013; Fisher’s
exact test). Namely, bilateral putaminal or bilateral thalamic
hemorrhage occurred more frequently than unilateral putaminal and contralateral thalamic hemorrhage based on the
expected numbers when each hemorrhage occurs at random
in terms of location, regardless of the location of other hemorrhages (Figure 2).
Discussion
The majority of spontaneous ICHs are associated with
hypertension (3, 28). Hypertensive ICH commonly occurs at
the putamen, thalamus, pons, and cerebellum. The putamen
and thalamus are the most common sites of hypertensive
ICH (29). Our review of 86 cases of simultaneous multiple
hypertensive ICHs shows a similar trend on the distribution
of location. Lenticulostriate arteries are responsible for
putaminal hemorrhage and originate from the middle
cerebral artery (M1) or proximal anterior cerebral artery (A1)
in the anterior circulation. Thalamoperforating arteries are
responsible for thalamic hemorrhage and originate from the
posterior cerebral arteries in the posterior circulation. Chronic
hypertension produces hyaline degeneration of perforating
arteries. Rupture of micro-aneurysms or perforating arteries
is considered a cause of hypertensive ICH. Although the
mechanism of bilateral simultaneous hypertensive ICH is
unclear, two possible mechanisms have been proposed (3,
11, 13, 18, 24). First, coincidental rupture of bilateral microaneurysms or perforating arteries can cause bilateral ICHs.
Second, subsequent rupture of bilateral micro-aneurysms
or perforating arteries can cause multiple ICHs. An initial
hemorrhage increases blood pressure, which may result in
subsequent contralateral hemorrhage. Both mechanisms
are probable. Which mechanism causes bilateral ICH in each
case is difficult to determine unless subsequent neurological
symptoms of each side are observed. Although not proven,
rupture of bilateral micro-aneurysms or perforating arteries
occurring at exactly the same time may be rare. Therefore,
we consider that subsequent rupture is more probable than
coincidental rupture. The time lag of subsequent rupture
can be from a few seconds to a few hours. The initial rupture
increases systemic blood pressure, which may result in
rupture of most vulnerable vessels at other sites.
Our analysis showed that symmetrical bilateral hemorrhage
occurs more frequently than asymmetric bilateral hemorrhage.
This finding raises the hypothesis that perforation of arteries
or micro-aneurysms are prone to occurring at symmetrical
locations. Namely, the distribution of hyaline degeneration
of lenticulostriate or thalamoperforating arteries is likely
to be symmetric. Symmetrical distribution of vulnerable
vessels could explain the deviation to a high frequency of

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occurrence of symmetrical bilateral hemorrhage. Microbleeds
are associated with ICH (2), and there is a close positional
association between recurrent ICH and prior microbleeds
(21). Sorimachi et al. reported that the number of microbleeds
is significantly higher in simultaneous multiple ICHs (mode;
15-19) than in single ICH (mode; 1-4) (20). The number of
microbleeds in our case (n=17) is consistent with their results.
In their study, the distribution of location of microbleeds
was not examined. Although studies have examined the
distribution of location of microbleeds (10, 16), there are no
studies on laterality of distribution of microbleeds. Jia et al.
demonstrated that systolic blood pressure had a significant
association with microbleeds in the territory of the posterior
cerebral artery (6). Their study may be supportive evidence
of our hypothesis that microbleeds tend to be distributed
symmetrically because perforating arteries originating
from the anterior or posterior circulation are responsible for
putaminal or thalamic hemorrhage, respectively. Trends of
distribution of microbleeds were unable to be determined
from our single case. A large-scale study focusing on
laterality of distribution of microbleeds by T2*-weighted
MRI may address our hypothesis that distribution of hyaline
degeneration of lenticulostriate or thalamoperforating
arteries is prone to be symmetric.
In our systematic review, there may be selection bias because
some of the literature included case reports without complete
surveys. Symmetric bilateral ICH is likely to be reported rather
than asymmetric bilateral ICH. When only complete surveys
of consecutive ICHs were selected, there were 27 cases of
simultaneous bilateral hypertensive putaminal or thalamic
hemorrhage among 5334 cases of ICH in total (9, 20, 24,
26, 29). The same statistical analysis of hemorrhagic sites as
described above showed p=0.050 (details not shown), and
there was still a strong trend of deviation to symmetrical
hemorrhage. Therefore, we consider that our analysis and
discussion are still valid.
Conclusion
We report a rare case of simultaneous hypertensive bilateral
ICH. A systematic review found 41 cases of simultaneous
hypertensive putaminal or thalamic hemorrhage. In these
cases, symmetrical hemorrhage frequently occurs. These
new findings suggest that patients may have symmetrically
vulnerable vessels. Further examinations of the distribution
of vulnerable vessels by T2*-weighted MRI may address these
issues.
References
1. Balasubramaniam S, Nadkarni TD, Goel A: Simultaneous
thalamic and cerebellar hypertensive haemorrhages. Neurol
India 55:183-184, 2007
2. Bokura H, Saika R, Yamaguchi T, Nagai A, Oguro H, Kobayashi
S, Yamaguchi S: Microbleeds are associated with subsequent
hemorrhagic and ischemic stroke in healthy elderly
individuals. Stroke 42:1867-1871, 2011

Turk Neurosurg 2014, Vol: 24, No: 3, 434-437

Kono K and Terada T: Simultaneous Bilateral Intracranial Hemorrhages

3. Hickey WF, King RB, Wang AM, Samuels MA: Multiple
simultaneous intracerebral hematomas. Clinical, radiologic,
and pathologic findings in two patients. Arch Neurol 40:
519-522, 1983

17. Sato M, Tanaka S, Kohama A, Sone T, Fukunaga M, Morita R:
Spontaneous bilateral intracerebral hemorrhage occurring
simultaneously--case report. Neurol Med Chir (Tokyo) 26:
545-547, 1986

4. Ikram MA, Wieberdink RG, Koudstaal PJ: International
epidemiology of intracerebral hemorrhage. Curr Atheroscler
Rep 14:300-306, 2012

18. Shiomi N, Miyagi T, Koga S, Karukaya T, Tokutomi T, Shigemori
M: Simultaneous multiple hypertensive intracerebral hematoma. No Shinkei Geka 32:237-244, 2004

5. Imai K: Bilateral simultaneous thalamic hemorrhages--case
report. Neurol Med Chir (Tokyo) 40:369-371, 2000

19. Silliman S, McGill J, Booth R: Simultaneous bilateral hypertensive putaminal hemorrhages. J Stroke Cerebrovasc Dis 12:
44-46, 2003

6. Jia Z, Mohammed W, Qiu Y, Hong X, Shi H: Hypertension
increases the risk of cerebral microbleed in the territory
of posterior cerebral artery: A Study of the Association of
Microbleeds Categorized on a Basis of Vascular Territories
and Cardiovascular Risk Factors. J Stroke Cerebrovasc Dis
23(1):e5-11, 2014
7. Kabuto M, Kubota T, Kobayashi H, Nakagawa T, Arai Y,
Kitai R: Simultaneous bilateral hypertensive intracerebral
hemorrhages--two case reports. Neurol Med Chir (Tokyo)
35:584-586, 1995
8. Kohshi K, Abe H, Tsuru E: Simultaneous hypertensive
intracerebral hematomas: Two case reports. J Neurol Sci
181:137-139, 2000
9. Lin CN, Howng SL, Kwan AL: Bilateral simultaneous
hypertensive intracerebral hemorrhages. Gaoxiong Yi Xue Ke
Xue Za Zhi 9:266-275, 1993
10. Liu PF, Cui YZ, Na J, Gao PY: Cerebral microbleeds - prevalence,
distribution and risk factors in northeast population without
preceding large-area stroke. Chin Med J (Engl) 123:286-290,
2010

20. Sorimachi T, Ito Y, Morita K, Fujii Y: Microbleeds on gradientecho T2(*)-weighted MR images from patients with multiple
simultaneous intracerebral haemorrhages. Acta Neurochir
(Wien) 149:171-176, 2007
21. Sueda Y, Naka H, Ohtsuki T, Kono T, Aoki S, Ohshita T, Nomura
E, Wakabayashi S, Kohriyama T, Matsumoto M: Positional
relationship between recurrent intracerebral hemorrhage/
lacunar infarction and previously detected microbleeds.
AJNR Am J Neuroradiol 31:1498-1503, 2010
22. Sugiura M, Himuro H, Tanikawa T, Beppu T: A case of bilateral
hypertensive intracerebral hemorrhage which occurred
simultaneously (author’s transl). No Shinkei Geka 10:193-198,
1982
23. Sunada I, Nakabayashi H, Matsusaka Y, Nishimura K,
Yamamoto S: Simultaneous bilateral thalamic hemorrhage:
Case report. Radiat Med 17:359-361, 1999
24. Takeuchi S, Takasato Y, Masaoka H, Hayakawa T, Yatsushige H,
Sugawara T: Simultaneous multiple hypertensive intracranial
hemorrhages. J Clin Neurosci 18:1215-1218, 2011

11. Mauriño J, Saposnik G, Lepera S, Rey RC, Sica RE: Multiple
simultaneous intracerebral hemorrhages: Clinical features
and outcome. Arch Neurol 58:629-632, 2001

25. Tanikake T, Kawaguchi S, Tada T, Kyoi K, Utsumi S, Nakasone K:
Simultaneous, bilateral hypertensive intracranial hematomas.
No Shinkei Geka 11:1085-1090, 1983

12. Miyasaka Y, Nakayama K, Matsumori K, Beppu T, Kurata
A, Satoh K, Kitahara T, Morii S, Owada T, Yada K: Bilateral
hypertensive intracerebral hemorrhage diagnosed by CT
scan: report of five cases and review of literature. Neurol Med
Chir (Tokyo) 22:661-667, 1982

26. Tanno H, Ono J, Suda S, Karasudani H, Yamakami I, Isobe
K, Watanabe Y: Simultaneous, multiple hypertensive
intracerebral hematomas: report of 5 cases and review of
literature. No Shinkei Geka 17:223-228, 1989

13. Nakamura T, Kadoya S, Umemori T, Suzuki T, Kwaku R: A case
report of simultaneous multiple intracerebral hematomas.
No Shinkei Geka 16:435-439, 1988
14. Ozdemir O, Calisaneller T, Yildirim E, Altinors N: Simultaneous
supra and infratentorial hypertensive intracerebral haemorrhage. J Clin Neurosci 14:775-777, 2007
15. Raabe A, Krug U: Migraine associated bilateral intracerebral
haemorrhages. Clin Neurol Neurosurg 101:193-195, 1999

27. Uno M, Hondo H, Matsumoto K: Simultaneous supra- and
infratentorial hypertensive intracerebral hemorrhage. No
Shinkei Geka 19:933-938, 1991
28. Weisberg L: Multiple spontaneous intracerebral hematomas:
Clinical and computed tomographic correlations. Neurology
31:897-900, 1981
29. Yen CP, Lin CL, Kwan AL, Lieu AS, Hwang SL, Lin CN, Howng
SL: Simultaneous multiple hypertensive intracerebral haemorrhages. Acta Neurochir (Wien) 147:393-399, 2005

16. Roob G, Lechner A, Schmidt R, Flooh E, Hartung HP, Fazekas
F: Frequency and location of microbleeds in patients with
primary intracerebral hemorrhage. Stroke 31:2665-2669,
2000

Turk Neurosurg 2014, Vol: 24, No: 3, 434-437

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