Refractory Chronic Subdural Hematoma Associated with Dural Metastasis of Lung Adenocarcinoma Treated with Endovascular Embolization for the Middle Meningeal Artery: A Case Report and Review of the Literature

Journal Pre-proof Refractory chronic subdural hematoma associated with dural metastasis of lung adenocarcinoma treated with endovascular embolization for the middle meningeal artery: a case report Takuya Kosaka, Naokado Ikeda, Motomasa Furuse, Naosuke Nonoguchi, Ryo Hiramatsu, Ryokichi Yagi, Shinji Kawabata, Shigeru Miyachi, Toshihiko Kuroiwa, Masahiko Wanibuchi PII:

S1878-8750(19)32650-6

DOI:

https://doi.org/10.1016/j.wneu.2019.10.035

Reference:

WNEU 13506

To appear in:

World Neurosurgery

Received Date: 26 September 2019 Revised Date:

5 October 2019

Accepted Date: 8 October 2019

Please cite this article as: Kosaka T, Ikeda N, Furuse M, Nonoguchi N, Hiramatsu R, Yagi R, Kawabata S, Miyachi S, Kuroiwa T, Wanibuchi M, Refractory chronic subdural hematoma associated with dural metastasis of lung adenocarcinoma treated with endovascular embolization for the middle meningeal artery: a case report, World Neurosurgery (2019), doi: https://doi.org/10.1016/j.wneu.2019.10.035. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Elsevier Inc. All rights reserved.

Refractory chronic subdural hematoma associated with dural metastasis of lung adenocarcinoma treated with endovascular embolization for the middle meningeal artery: a case report

Takuya Kosaka1, Naokado Ikeda1, Motomasa Furuse1, Naosuke Nonoguchi1, Ryo Hiramatsu1, Ryokichi Yagi1, Shinji Kawabata1, Shigeru Miyachi2, Toshihiko Kuroiwa1,3 and Masahiko Wanibuchi1

Department of Neurosurgery and Neuroendovascular Surgery, Osaka Medical College1 Department of Neurosurgery and Neuroendovascular Center, Aichi Medical University2 Department of Neurosurgery, Tesseikai Neurosurgical Hospital3

Corresponding Author; Naokado Ikeda Department of Neurosurgery and Neuroendovascular Surgery, Osaka Medical College 2-7 Daigaku-machi, Takatsuki, Osaka, Japan 569-8686 E-mail; [email protected] Tel; +81-72-683-1221 Fax; +81-72-683-1221

Keywords: chronic subdural hematoma, dural metastasis, middle meningeal artery, embolization

Short title: Embolization for dural metastasis with CSDH

1

Abstract

2

Background

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Endovascular embolization of the middle meningeal artery (MMA) is effective for recurrent

4

chronic subdural hematoma (CSDH). CSDH associated with dural metastasis is generally

5

refractory to burr hole surgery and has poor prognosis even if any interventions are applied. To

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the best of our knowledge, this study is the first to report a case of refractory CSDH associated

7

with dural metastasis that was successfully treated with embolization of the MMA.

8

Case Description

9

A 66-year-old man with a 1-year history of lung adenocarcinoma had also undergone

10

whole-brain irradiation for multiple brain metastases 5 months prior to presentation, surgical

11

removal of relapse of brain metastases 3 months prior, and stereotactic radiotherapy for the

12

relapses 1 month prior. He was admitted to our institution with speech disturbance, severe

13

headache, and right-sided motor weakness. Head computed tomography on admission revealed

14

left-sided CSDH, and emergency burr hole irrigation surgery was performed. However, CSDH

15

recurred twice in a short period after hospitalization. Histological examination revealed

16

adenocarcinoma cells in the dura mater and in hematoma samples during the first surgery;

17

therefore, the patient was diagnosed with refractory CSDH associated with dural metastasis of

18

lung adenocarcinoma. Therefore, we performed endovascular embolization of the MMA,

1

19

followed by systemic chemotherapy at 1 month after embolization, and no recurrence of the

20

CSDH was observed.

21

Conclusions

22

Embolization of the MMA has few surgical risks and could be a treatment option for refractory

23

CSDH associated with dural metastasis as it might prolong the therapeutic time window until

24

radical therapies are administered.

25

26

2

27

Introduction

28

The efficacy of endovascular embolization of the middle meningeal artery (MMA) has been

29

reported for recurrent chronic subdural hematoma (CSDH).1 CSDH associated with dural

30

metastasis is generally refractory to burr hole surgery and has a poor prognosis even if any

31

interventions are applied.2 The present study reports the case of CSDH associated with dural

32

metastasis successfully treated with endovascular embolization of the MMA and presents a

33

literature review.

34

35

Clinical Presentation

36

A 66-year-old man with a 1-year history of lung adenocarcinoma was admitted to our institution

37

with speech disturbance, severe headache, and right-sided motor weakness. He had undergone

38

whole-brain irradiation for multiple brain metastases 5 months prior to presentation, and relapse

39

of the metastases had been treated with surgical removal 3 months prior and stereotactic

40

radiotherapy 1 month prior. He had no history of a prior head injury and had not received

41

antithrombotic agents.

42

On admission, neurological examination revealed disorientation, motor aphasia, and

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right-sided hemiparesis. Blood testing, including congealing fibrinogenolysis assay, indicated no

44

abnormalities. Head computed tomography (CT) on admission revealed left-sided CSDH and

3

45

midline shift (Fig. 1A). Magnetic resonance imaging (MRI) revealed neither recurrent nor new

46

metastatic lesions in the brain parenchyma; however, the dura mater on the CSDH was partially

47

enhanced with gadolinium (Fig. 1B). The patient underwent emergency burr hole irrigation, and

48

biopsy samples were obtained from the affected dura mater. Immediately postoperatively, his

49

symptoms improved, and postoperative head CT confirmed that the hematoma had been

50

evacuated (Fig. 1C). The subdural fluid was drained with a closed subdural drainage system for

51

approximately 20 hours postoperatively.

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On postoperative day 3, the patient’s right hand demonstrated motor weakness, and

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head CT revealed recurrence of the left-sided CSDH (Fig. 1D). A second burr hole procedure

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was performed 7 days after the first procedure, and the CSDH was completely evacuated (Fig.

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1E). However, approximately 200 mL/day of pinkish subdural serous fluid was drained into the

56

subdural drainage tube. Clamping of the subdural drainage tube caused motor aphasia;

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neuroradiological images indicated relapse of the CSDH, which caused his clinical symptoms

58

(Fig. 1F). The total protein level in the drained fluid was elevated to 436.5 mg/dL. In addition,

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because histological examination revealed adenocarcinoma cells in the dura mater and in the

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hematoma sample collected during the first surgery (Fig. 2), the patient was diagnosed with

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refractory CSDH associated with dural metastasis of lung adenocarcinoma.

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We decided to perform endovascular embolization of the MMA with local anesthesia

4

63

to treat the relapsed CSDH and discontinued the subdural drainage. Using a transfemoral

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approach, a 5-Fr guiding catheter was placed in the left proximal external carotid artery, and a

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flow-directed microcatheter (Marathon; Medtronic Japan, Tokyo) was inserted into the left

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MMA. Superselective angiography of the left MMA showed dura mater staining (Fig. 3A). We

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injected 13% N-butyl-2-cyanoacrylate into the parietal branch of the MMA via a microcatheter

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(Fig. 3B). After endovascular embolization, the volume of the subdural drainage continued to

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decrease and the neurological symptoms improved. Even after the subdural drainage tube was

70

removed 4 days after embolization, head CT revealed no recurrence of CSDH (Fig. 1G).

71

The patient was discharged 10 days after the embolization with a Karnofsky

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Performance Status score of 90. One month after embolization, chemotherapy (pemetrexed) was

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administered for lung adenocarcinoma. MRI with gadolinium administration before the

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chemotherapy revealed few collections of subdural fluid, but the patient had no symptoms (Fig.

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1H). Currently, CSDH has not recurred at 30 months postoperatively (Fig. 1I).

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Discussion

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In cases of refractory recurrent CSDH, embolization of the MMA at the affected site has been

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proven to be effective for CSDH.3 However, to the best our knowledge, this is the first report of

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endovascular embolization for refractory CSDH associated with dural metastasis of cancer.

5

81

The possible causes of CSDH associated with dural metastasis include

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neovascularization of dura mater accompanying cancer metastasis and the disruption of this

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neovascularization2,4,5; accumulation of plasma components as a result of the osmolality gap

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caused by the migration of proteins such as mucin from tumor cells to the subdural space6,7; and

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a mechanism related to tumor embolization of disseminated intravascular coagulation and

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meningeal vein drainage associated with the aggravated general state.8

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In addition to embolization of the MMA, available treatments for dural

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metastasis-associated CSDH that recurs after burr hole irrigation include (1) removal of

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hematoma, resection of the dura mater, and replacement with artificial dura mater through

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craniotomy; (2) subdural-peritoneal shunting or placement of an Ommaya reservoir9; and (3)

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irradiation of the affected dura mater and subdural cavity.10 However, these therapeutic

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strategies are associated with some problems. Surgery with a large craniotomy is invasive and

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especially risky in patients whose general condition is poor, and it might be difficult to

94

determine the range of dura mater to be resected. Placement of a shunt system has the potential

95

to cause both dissemination of tumor cells from the hematoma to the peritoneal cavity and

96

obstruction by subdural effusions or hematomas comprising high amounts of protein. Irradiation

97

of the dura mater may be effective for long-term control of CSDH but requires subdural

98

drainage for a long time, as observed in our patient. Conversely, endovascular embolization is

6

99

less invasive, and complications are less likely to occur as long as proper caution is exercised in

100

cases involving dangerous anastomoses.3 Therefore, embolization of the MMA appears to be the

101

best treatment option for recurrent CSDH associated with dural metastasis.

102

Although we did not expect the tumor cells of the dura mater to disappear only after

103

embolization of the MMA, we hypothesized that blood feeding to the tumor cells would be

104

decreased at least. We speculate that the decrease in blood flow helped in preventing the

105

recurrence of CSDH as a result of the two aforementioned mechanisms of CSDH formation

106

with dural metastasis: reduction of dural neovascularization accompanying cancer metastasis

107

and reduction in the migration of proteins from tumor cells to the subdural space. Conversely,

108

Ikeda et al. reported a case of metastasis-related refractory CSDH wherein endovascular

109

embolization of the MMA was not effective for CSDH11. However, in their case, CSDH was

110

associated with metastasis to the hematoma capsule and not to the dura mater as in our case.

111

This difference might be one reason for the differences in therapeutic responses to the

112

endovascular embolization in these two cases.

113

In our patient, chemotherapy was administered to the primary cancer 1 month after

114

embolization.

Contrast

material-enhanced

MRI

115

improvement in the thickening and enhancement of the dura mater, which suggests that the

116

metastasized tumor cells had been inactive or decreased in number. However, this possibility is

7

before

chemotherapy

demonstrated

117

difficult to prove because additional surgery would be necessary to sample the affected dura.

118

Therefore, we believe that it is better to follow embolization with chemotherapy or radiotherapy

119

as radical therapy after endovascular embolization assuming that tumor cells remain in the dura

120

mater.

121

We speculated that immediately after embolization of the MMA, delivery of the

122

anticancer agent to the dura mater could be reduced during chemotherapy for dural tumors.

123

However, the long-term therapeutic effects of the anticancer drug were not adversely affected

124

because new blood vessels to the dura mater would be formed as bypass routes. Indeed, relapses

125

have been reported even after embolization11 presumably because a new bypass to the dura

126

mater was created. In our patient, chemotherapy with pemetrexed seemed to contribute to

127

long-term control of CSDH, but embolization of the MMA was effective as an acute treatment

128

until radical therapy was administered for dural metastasis.

129

130

Conclusions

131

For the first time, we report a case of refractory CSDH associated with dural metastasis of

132

cancer treated successfully with endovascular embolization. Embolization of the MMA has few

133

surgical risks, and we believe that it is a good alternative to invasive craniotomy in the treatment

134

of refractory CSDH associated with dural metastasis. In addition, it prolongs the therapeutic

8

135

time window until radical therapies are administered, as observed in our study.

136

137

Conflict of Interest

138

The authors declare that they have no conflict of interest.

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140

9

141

Figure legends

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Figure 1

143

Neuroradiological images of the patient.

144

Head computed tomography (CT) on admission (A) revealed left-sided chronic subdural

145

hematoma (CSDH) and midline shift. Magnetic resonance imaging (MRI) with gadolinium (B)

146

revealed partial dural enhancement on CSDH. CSDH was immediately evacuated after the first

147

burr hole irrigation (C), but CSDH recurred 4 days after the first surgery (D). CT after the

148

second surgery demonstrated disappearance of the CSDH (E). CSDH recurred again 4 days after

149

the second surgery (F). Seven days after endovascular embolization, no recurrence of CSDH

150

was observed (G), and enhanced MRI 1 month after embolization revealed only few subdural

151

fluid collections (H). Currently, CSDH has not recurred as of 30 months after embolization (I).

152

153

Figure 2

154

Histopathological microphotographs of the dura mater sampled during the first surgery.

155

Adenocarcinoma cells were detected in the dura mater. (Hematoxylin and eosin staining;

156

magnification, 400×)

157

158

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159

Figure 3

160

Superselective angiography for the parietal branch of the middle meningeal artery (MMA)

161

demonstrated dural staining (A). After embolization with 3% of N-butyl-2-cyanoacrylate in the

162

parietal branch of the MMA, casts of N-butyl-2-cyanoacrylate (arrows) were formed and dural

163

staining disappeared (B).

164 165

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Abbreviations list: CSDH: chronic subdural hematoma CT: computed tomography MMA: middle meningeal artery MRI: magnetic resonance image NBCA:N-butyl-2-cyanoacrylate