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Research ArticleNeurointervention

Predictors of Cerebral Aneurysm Rupture after Coil Embolization: Single-Center Experience with Recanalized Aneurysms

Y. Funakoshi, H. Imamura, S. Tani, H. Adachi, R. Fukumitsu, T. Sunohara, Y. Omura, Y. Matsui, N. Sasaki, T. Fukuda, R. Akiyama, K. Horiuchi, S. Kajiura, M. Shigeyasu, K. Iihara and N. Sakai
American Journal of Neuroradiology May 2020, 41 (5) 828-835; DOI: https://doi.org/10.3174/ajnr.A6558
Y. Funakoshi
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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H. Imamura
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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S. Tani
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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H. Adachi
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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R. Fukumitsu
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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T. Sunohara
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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Y. Omura
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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Y. Matsui
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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N. Sasaki
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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T. Fukuda
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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R. Akiyama
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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K. Horiuchi
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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S. Kajiura
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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M. Shigeyasu
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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K. Iihara
bDepartment of Neurosurgery (K.I.), Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.
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N. Sakai
aFrom the Department of Neurosurgery (Y.F., H.I., S.T., H.A., R.F., T.S., Y.O., Y.M., N.Sasaki, T.F., R.A., K.H., S.K., M.S., N.Sakai), Kobe City Medical Center General Hospital, Kobe, Japan
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    Fig 1.

    Illustration of the Modified Raymond-Roy classification and additional definitions of the type of recanalization used in the present study. Class I: complete obliteration; class II: residual neck; class IIIa: residual aneurysm with contrast within the coil interstices; class IIIb: residual aneurysm with contrast along the aneurysm wall. The appearance of new blebs was distinguished from an increase in the diameter of the coiled aneurysm. Except for the appearance of new blebs, an increase in the diameter of the coiled aneurysm was termed “aneurysm growth.”

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    Fig 2.

    DSA findings for ruptured recanalized aneurysms in the unruptured group. Case 1-pre: preprocedural basilar artery–bifurcation aneurysm; case 1-post: class II aneurysm occlusion immediately after the procedure; case 1–6m: class IIIb recanalization at 6 months after the procedure; case 1–8m: ruptured recanalized aneurysm at 8 months after the procedure; case 2-pre: preprocedural ICA–posterior communicating artery aneurysm; case 2-post: class IIIb aneurysm occlusion immediately after the procedure; case 2–6m: progression of the class IIIb recanalization at 6 months after the procedure; case 2–76m: ruptured recanalized aneurysm with a new bleb at 76 months after the procedure; case 3-pre: preprocedural paraclinoid-ICA aneurysm; case 3-post: class IIIb aneurysm occlusion immediately after the procedure; case 3–2m: ruptured recanalized aneurysm with a new bleb at 2 months after the procedure; case 4-pre: preprocedural basilar artery–bifurcation aneurysm; case 4-post: class IIIb aneurysm occlusion immediately after the procedure; case 4–6m: no change at 6 months after the procedure; case 4–24m: MRA shows the ruptured recanalized aneurysm with a new bleb at 24 months after the procedure.

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    Fig 3.

    DSA findings for ruptured recanalized aneurysms in the ruptured group. Case 1-pre: preprocedural anterior communicating artery aneurysm; case 1-post: class II aneurysm occlusion immediately after the procedure; case 1–1w: class IIIb recanalization at 1 week after the procedure; case 1–1m: ruptured recanalized aneurysm with a new bleb at 1 month after the procedure; case 2-pre: preprocedural anterior communicating artery aneurysm; case 2-post: class II aneurysm occlusion immediately after the procedure; case 2–1w: class IIIb recanalization at 1 week after the procedure; case 2–1m: ruptured recanalized aneurysm with a new bleb at 1 month after the procedure; case 3-pre: preprocedural ICA–posterior communicating artery aneurysm; case 3-post: class IIIb aneurysm occlusion immediately after the procedure; case 3–6m: progression of the class IIIb recanalization at 6 months after the procedure; case 3–29m: ruptured recanalized aneurysm at 29 months after the procedure; case 4-pre: preprocedural ICA–posterior communicating artery aneurysm; case 4-post: class IIIb aneurysm occlusion immediately after the procedure; case 4–6m: progression of the class IIIb recanalization at 6 months after the procedure; case 4–7m: ruptured recanalized aneurysm at 7 months after the procedure.

Tables

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    Table 1:

    Patient and aneurysm characteristics, volume embolization ratio, use of stents, and follow-up terma

    Unruptured GroupRuptured Group
    All Aneurysms (n = 426)Recanalized Aneurysms (n = 38)All Aneurysms (n = 169)Recanalized Aneurysms (n = 37)
    Patient characteristic
     Age (yr)63.0 (52.0–70.0)65.0 (49.8–71.3)66.0 (52.0–77.5)59.0 (44.5–76.5)
     Male sex105 (24.6%)6 (15.8%)56 (33.1%)10 (27.0%)
    Aneurysm location
     ICA-cavernous12 (2.8%)2 (5.3%)0 (0.0%)0 (0.0%)
     ICA-paraclinoid188 (44.1%)9 (23.7%)5 (3.0%)2 (5.4%)
     ICA-PcomA49 (11.5%)9 (23.7%)55 (32.5%)16 (43.2%)
     ICA-AchoA10 (2.3%)0 (0.0%)13 (7.7%)4 (10.8%)
     ICA-bifurcation11 (2.6%)2 (5.3%)3 (1.8%)0 (0.0%)
     MCA6 (1.4%)0 (0.0%)4 (2.4%)0 (0.0%)
     AcomA66 (15.5%)1 (2.6%)57 (33.7%)11 (29.7%)
     VA15 (3.5%)4 (10.5%)8 (4.7%)1 (2.7%)
     BA-SCA16 (3.8%)2 (5.3%)2 (1.2%)1 (2.7%)
     BA-bifurcation41 (9.6%)9 (23.7%)12 (7.1%)2 (5.4%)
     Others12 (2.8%)0 (0.0%)10 (5.9%)0 (0.0%)
    Aneurysm size
     Dome6.2 (4.9–8.4)10.1 (7.0–14.1)6.5 (5.0–9.3)7.7 (5.4–13.0)
     Neck3.8 (2.9–5.1)5.9 (4.7–7.7)3.2 (2.4–4.2)4.0 (2.7–5.9)
    Endovascular procedures
     VER26.9 (21.9–32.8)23.0 (18.0–29.2)25.8 (19.8–33.2)23.7 (18.9–29.5)
     Without stent240 (56.3%)19 (50.0%)169 (100.0%)37 (100.0%)
     With stent186 (43.7%)19 (50.0%)0 (0.0%)0 (0.0%)
    Follow-up
     Duration (mo)58.5 (24.0–86.0)74.0 (30.5–96.3)18.0 (3.0–48.0)28.0 (10.0–56.0)
    • Note:—AchoA indicates anterior choroidal artery; VA, vertebral artery; BA, basilar artery; SCA, superior cerebellar artery; VER, volume embolization ratio.

    • ↵a Unruptured group indicates unruptured aneurysms that underwent coil embolization; ruptured group, ruptured aneurysms that underwent coil embolization. Data are Unruptured Group (n = 426): Recanalization after coil embolization occurred in 38 of 426 unruptured aneurysms. Ruptured Group (n = 169): Recanalization after coil embolization occurred in 37 of 169 ruptured aneurysms.

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    Table 2:

    Outcomes of aneurysms and patients

    Unruptured GroupaRuptured Groupa
    Type of recanalization on final DSA
     Class II3 (7.9%)7 (18.9%)
     Class IIIa12 (31.6%)7 (18.9%)
     Class IIIb23 (60.5%)23 (62.2%)
    Aneurysm growth12 (31.6%)3 (8.1%)
    Appearance of bleb2 (5.3%)1 (2.7%)
    Retreatment18 (47.4%)16 (43.2%)
    Rupture4 (10.5%)4 (10.8%)
    Rupture risk (/aneurysm)0.94%2.37%
    Rupture risk (/yr)0.20%0.97%
    Final mRS score without ruptured recanalized aneurysmb
     0–231 (91.2%)21/33 (63.6%)
     3–41 (2.9%)6/33 (18.2%)
     5–62 (5.9%)6/33 (18.2%)
    Final mRS score with ruptured recanalized aneurysmc
     0–22 (50.0%)1 (25.0%)
     3–40 (0.0%)2 (50.0%)
     5–62 (50.0%)1 (25.0%)
    • ↵a Unruptured Group (n = 38); Ruptured Group (n = 37).

    • ↵b Unruptured Group (n = 34); Ruptured Group (n = 33).

    • ↵c Unruptured Group (n = 4); Ruptured Group (n = 4).

    • View popup
    Table 3:

    Type of aneurysm occlusion and recanalization on follow-up DSA, the timing of retreatment and rupture, and the type of recanalization immediately before retreatment and rupture in the unruptured groupa

    Initial (n = 38) (n = 38)6 Months (n = 36) (n = 38)1 Year (n = 16) (n = 37)2 Years (n = 3) (n = 35)3 Years (n = 0) (n = 26)4 Years (n = 0) (n = 26)5 Years (n = 1) (n = 23)6 Years (n = 1) (n = 22)7 Years (n = 0) (n = 16)8 Years (n = 1) (n = 13)
    Type of aneurysm occlusion and recanalization
     I5200000000
     II10410000000
     IIIa121391000100
     IIIb111762001001
    Type of recanalization of retreated recanalized aneurysms
     IIIa0130000100
     IIIb0821001001
    Type of recanalization of ruptured recanalized aneurysms
     IIIa0000000000
     IIIb1110000100
    • ↵a The first row of numbers in parentheses indicates the number of cases that underwent follow-up DSA at that time; the second row of numbers in parentheses, the number of cases that underwent follow-up MRA at that time.

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    Table 4:

    Type of aneurysm occlusion and recanalization on follow-up DSA, the timing of retreatment and rupture, and the type of recanalization immediately before retreatment and rupture in the ruptured groupa

    Initial (n = 37) (n = 37)1 Week (n = 37) (n = 37)1 Month (n = 34) (n = 37)6 Months (n = 19) (n = 29)1 Year (n = 12) (n = 28)2 Years (n = 0) (n = 22)3 Years (n = 0) (n = 18)4 Years (n = 0) (n = 13)5 Years (n = 0) (n = 9)6 Years (n = 0) (n = 6)
    Type of aneurysm occlusion and recanalization
     I14930000000
     II1719135200000
     IIIa2235300000
     IIIb47159700000
    Type of recanalization of retreated recanalized aneurysms
     IIIa0002100000
     IIIb00111100000
    Type of recanalization of ruptured recanalized aneurysms
     IIIa––00000000
     IIIb––21010000
    • Note:— – indicates not available.

    • ↵a Aneurysms that reruptured in the acute phase (<1 month after the initial rupture) were excluded. The first-row of number in parentheses indicates the number of cases that underwent follow-up DSA at that time. The second-row of number in parentheses indicates the number of cases that underwent follow-up MRA at that time.

    • View popup
    Table 5:

    Factors associated with rupture after coil embolization in untreated recanalized aneurysms in the unruptured groupa

    Untreated Recanalized Aneurysms (n = 20)
    Unruptured (n = 16)Ruptured (n = 4)P Value
    Age (yr)67.0 (60.3–72.8)63.0 (55.8–70.3).570
    Sex
     Male1 (6.3%)1 (25.0%).264
     Female15 (93.7%)3 (75.0%)
    Location
     ICA5 (31.2%)1 (25.0%).937
     ICA-PcomA4 (25.0%)1 (25.0%)
     AcomA1 (6.3%)0 (0.0%)
     Posterior6 (37.5%)2 (50.0%)
    Dome9.2 (7.6–13.4)9.9 (6.6–11.1).813
    Neck5.5 (4.4–7.0)4.5 (3.2–8.8).741
    VER22.1 (13.9–26.1)25.1 (18.5–37.3).321
    Use of stent
     No9 (56.3%)2 (50.0%).822
     Yes7 (43.7%)2 (50.0%)
    Type of recanalization on final DSA
     II + IIIa10 (62.5%)0 (0.0%).025b
     IIIb6 (37.5%)4 (100.0%)
    Aneurysm growth
     No13 (81.3%)3 (75.0%).780
     Yes3 (18.7%)1 (25.0%)
    • Note:—ICA indicates ICA other than ICA-PcomA; VA, vertebral artery; BA, basilar artery; SCA, superior cerebellar artery; VER, volume embolization ratio; Posterior, posterior circulation including the VA, BA-SCA, and BA-bifurcation.

    • ↵a Data are recanalized aneurysms in the unruptured group (n = 38): Twenty of 38 recanalized aneurysms were untreated. Among 20 untreated recanalized aneurysms, 16 aneurysms unruptured and 4 aneurysms ruptured.

    • ↵b Statistical significance.

    • View popup
    Table 6:

    Factors associated with rupture after coil embolization in untreated recanalized aneurysms in the ruptured groupa

    Untreated Recanalized Aneurysms (n = 21)
    Unruptured (n = 17)Ruptured (n = 4)P Value
    Age (yr)62.0 (44.5–78.0)55.5 (47.5–75.5).929
    Sex
     Male6 (35.3%)1 (25.0%).694
     Female11 (64.7%)3 (75.0%)
    Location
     ICA3 (17.7%)0 (0.0%).628
     ICA-PcomA9 (52.9%)2 (50.0%)
     AcomA4 (23.5%)2 (50.0%)
     Posterior1 (5.9%)0 (0.0%)
    Dome6.2 (5.2–8.7)9.4 (5.3–14.4).347
    Neck3.2 (2.5–4.6)5.2 (3.6–9.1).066
    VER24.9 (21.3–29.5)25.5 (16.7–28.5).741
    Use of stent
     No17 (100.0%)4 (100.0%)–
     Yes0 (0.0%)0 (0.0%)
    Type of recanalization on final DSA
     II+IIIa11 (64.7%)0 (0.0%).020b
     IIIb6 (35.3%)4 (100.0%)
    Aneurysm growth
     No16 (94.1%)4 (100.0%).619
     Yes1 (5.9%)0 (0.0%)
    • Note:— – indicates not available.

    • ↵a Data are recanalized aneurysms in the ruptured group (n = 37): Twenty-one of 37 recanalized aneurysms were untreated. Among 21 untreated recanalized aneurysms, 17 aneurysms unruptured and 4 aneurysms ruptured.

    • ↵b Statistical significance.

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American Journal of Neuroradiology: 41 (5)
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Y. Funakoshi, H. Imamura, S. Tani, H. Adachi, R. Fukumitsu, T. Sunohara, Y. Omura, Y. Matsui, N. Sasaki, T. Fukuda, R. Akiyama, K. Horiuchi, S. Kajiura, M. Shigeyasu, K. Iihara, N. Sakai
Predictors of Cerebral Aneurysm Rupture after Coil Embolization: Single-Center Experience with Recanalized Aneurysms
American Journal of Neuroradiology May 2020, 41 (5) 828-835; DOI: 10.3174/ajnr.A6558

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Predictors of Cerebral Aneurysm Rupture after Coil Embolization: Single-Center Experience with Recanalized Aneurysms
Y. Funakoshi, H. Imamura, S. Tani, H. Adachi, R. Fukumitsu, T. Sunohara, Y. Omura, Y. Matsui, N. Sasaki, T. Fukuda, R. Akiyama, K. Horiuchi, S. Kajiura, M. Shigeyasu, K. Iihara, N. Sakai
American Journal of Neuroradiology May 2020, 41 (5) 828-835; DOI: 10.3174/ajnr.A6558
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