International Journal of Cardiology 187 (2015) 430–433
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International Journal of Cardiology journal homepage: www.elsevier.com/locate/ijcard
Letter to the Editor
In-stent restenosis after vertebral artery stenting☆ Yongjun Jiang, Xiaomeng Xu, Zhuoyu Wen, Xiaohui Xu, Lian Yang, Xinfeng Liu ⁎ Department of Neurology, Jinling Hospital, Medical School of Nanjing University, 305 Zhongshan East road, Nanjing, Jiangsu, China
a r t i c l e
i n f o
Article history: Received 23 March 2015 Accepted 24 March 2015 Available online 27 March 2015
More than 1/4 of strokes occur in the vertebral artery (VA) or basilar artery (BA) [1]. The major cause of stroke is atherosclerotic stenosis [2] and revascularization was introduced to treat VA stenosis. Researchers have demonstrated the feasibility, safety and efficiency of VA stenting (VAS) [3]. The major concern for current VAS is in-stent restenosis (ISR), which induces recurrent stroke during follow-up [4]. However, the incidence of ISR varies among different studies from 0 [5] to more than 50% [6] due to the heterogeneity in study design, type of stent, follow-up time and evaluation method. In the present study, we aimed to investigate the incidence of ISR and its underlying risks in published reports through April 2014. We searched the PubMed and EMBASE databases with the terms “vertebral artery” in combination with “stenting OR stent OR stent*”. Reference lists of the retrieved publications were scanned manually for all relevant additional studies and review articles. No attempts were made to locate any unpublished data. Studies were included in this analysis if they met the following criteria: (1) The individuals were asymptomatic or symptomatic in the VA territory; (2) stents were used to target atherosclerotic plaques; (3) there was follow-up post-stenting; (4) the incidence of ISR was verified by digital subtraction angiography (DSA). Due to artifact, the ISR detected by magnetic resonance angiography (MRA) was excluded from analysis. Though computed tomography angiography (CTA) could partly detect ISR, its sensitivity and specificity were lower than DSA; therefore, the ISR detected by CTA was also excluded. Studies were excluded if (1) the study was a case report; (2) the incidence of ISR in the VA was not clearly illustrated in the paper; (3) the outcome was only risk of stroke without ISR; (4) only angioplasty was performed.
☆ This study was financially supported by the National Science Foundation of China (31200817, 81471181 and 31171016) and the Jiangsu Provincial Special Program of Medical Science (BL2013025). There was no relationship with any industry. ⁎ Corresponding author. E-mail address: xfl[email protected] (X. Liu).
http://dx.doi.org/10.1016/j.ijcard.2015.03.377 0167-5273/© 2015 Elsevier Ireland Ltd. All rights reserved.
A pooled risk estimate was obtained by the Mantel–Haenszel method. The validity of pooling the risk estimates (test of homogeneity) was assessed with the Q-test and I2 statistics. In the presence of significant heterogeneity, the random-effects model based on the method described by DerSimonian and Laird was adopted. A flow diagram for the literature search is shown in Fig. 1A. A total of 53 studies met the criteria. The characteristics of included studies are summarized in Table 1. All of the studies comprised of 2200 patients with 279 asymptomatic and 1893 symptomatic patients in the VA territory with 2389 lesions successfully receiving 2292 stents (628 drug eluting stents (DES) and 1664 bare metal stents (BMS)). A total of 1942 stents were visualized by DSA at a mean of 16.7 months after stent placement. ISR was defined as ≥ 50% stenosis within the stents. A total of 341 ISR cases (17.6%) were identified and the incidence of recurrent vascular events was higher compared to patients without ISR (17.5% vs. 2.2%). The ISR risk for DES (28/214) was lower than for BMS (73/287), but there was no significant difference (Fig. 1B). The pool risk was 0.74 (95% CI, 0.44–1.24). The intracranial ISR rate (15.4%, 47/306) was lower than the extracranial ISR rate (17.8%, 269/1,513). In a subgroup analysis of the 8 case–control studies that compared intracranial and extracranial VAS in a single study (Fig. 1C), the pooled risk for ISR in intracranial stents was 1.17 (95% CI, 0.67–2.03). For the extracranial VAS, there was 16.7% (9/48) ISR for stent placed in the non-ostium of VA, which was slightly lower compared to the VA ostium (18.5%, 253/1,368). Over time, the total ISR rate for VA stents decreased (Fig. 1D). Before 2008, the ISR risk of VA stents was almost 28.8% but decreased to 15.1% based on data from 2009 to 2014. Our study demonstrated that 17.6% of patients receiving VAS had ISR, which increased the risk of recurrent stroke. This result was inconsistent with previous studies, which showed that ISR was a major concern for VAS [7]. The ISR was influenced by lesion location and stent type. Intracranial VAS ISR was lower than for extracranial VAS based on all of the studies. However, when a meta-analysis was performed based on case–control studies to decrease possible bias, the ISR rate was comparable between intracranial and extracranial VAS. The result was partially supported by previous studies [8]. The reason for different ISR rates between the VA and carotid artery is not clear. As for extracranial VAS, non-ostial ISR was slightly lower than ostial ISR (16.7% vs. 18.5%). Since 2006, Gupta et al. used DES to treat VA atherosclerotic stenosis to avoid ISR [9]. A previous systematic review summarized that DES were associated with a lower restenosis rate (11%) compared to BMS (30%) at a mean of 24 months of follow-up [10]. Our data were consistent with these findings. A slight difference was that the ISR rate for
Y. Jiang et al. / International Journal of Cardiology 187 (2015) 430–433
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Fig. 1. ISR of VAS. (A) Flow diagram for the literature search. (B) The pooled risk for in-stent restenosis of DES and BMS. The data were extracted from case–control studies. (C) The pooled risk of in-stent restenosis in intra- and extracranial VA stents. The data were extracted from case–control studies. (D) The annual incidence of in-stent restenosis. Over time, the rate of in-stent restenosis decreased.
Table 1 Study characteristics. Author
Year
Region
Patients Asymptom (n)
Langwieser [11] Lin [12] He [13] Li [14] Lee [15] Uygunoglu [16] Mohammadian [17] Tang [18] He [19] Lu [20] Song [8] Vajda [21]
2014 2014 2013 2014 2013 2013 2013 2013 2013 2013 2012 2012
Germany China China China Korea Turkey Iran China China China China Germany
4 0 0 18 57 0 0 0 0 0 0 NR
Lesions Symptom TIA (n)
Stroke (n)
Total (n)
19 30 0 3 0 0 206 21 21 14 134 NR
12 60 27 11 0 9 0 5 0 10 72 NR
31 90 27 14 0 9 206 26 21 24 206 NR
Stent placement
Intra (n)
Extra (n)
DES (n)
BMS (n)
0 14 26 0 0 0 21 0 9 24 29 15
35 76 0 32 57 9 218 26 12 0 199 0
12 42 0 0 9 0 0 0 0 24 121 15
23 48 26 32 48 9 223 26 20 0 98 0
Follow up (months)
5 12 8.6 18.3 8.2 50.2 13.2 12.0 15.5 35 43 6.9
Restenosis Case (n)
Total (n)
7 15 2 1 13 0 38 0 4 2 23 0
30 90 9 32 57 9 223 16 10 20 226 15
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Y. Jiang et al. / International Journal of Cardiology 187 (2015) 430–433
Table 1 (continued) Author
Year
Region
Patients Asymptom (n)
Edgell [22] Raghuram [23] Al-Ali [24] Fields [25] Vajda [26] Hatano [27] Chen [28] Zhou [29] Park [30] Wener [31] Chung [32] Jenkins [33] Karameshev [34] Vajda [35] Parkhutik [36] Vajda [37] Taylor [6] Yu [38] Kakino [39] Seifert [40] Edgell [41] Ralea [42] Du [43] Abruzzo [44] Tsutsumi [45] Qureshi [46] Dabus [47] Fessler [48] Gupta [49] Lin [50] Weber [51] Weber [52] Kim [53] SSYLYIA [54] Jiang [55] Albuquerque [56] Cloud [57] Kogure [58] Mukherjee [59] Michel [60] Chastain [61]
2013 2012 2011 2011 2012 2011 2011 2011 2010 2010 2010 2010 2010 2009 2010 2010 2008 2009 2009 2009 2010 2008 2007 2007 2007 2006 2006 1998 2006 2006 2005 2005 2005 2004 2003 2003 2003 2001 2001 2000 1999
USA USA USA USA USA Japan China China Korea Germany Korea USA Switzerland USA Spain USA USA Hongkong Japan Austria USA France China USA Japan USA USA USA USA Taiwan Germany Germany Korea USA China USA UK Japan Japan USA USA
0 0 0 0 0 90 0 0 0 19 0 96 0 38 13 NR 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 9 0 5 0 0 11
Lesions Symptom TIA (n)
Stroke (n)
Total (n)
55 NR NR 16 NR 64 NR 18 0 0 9 9 5 0 1 NR 0 0 0 15 2 5 37 0 3 0 19 0 0 17 2 15 0 0 0 9 6 0 12 0 21
82 NR NR 10 NR 44 NR 43 20 9 11 0 5 10 15 NR 44 10 36 31 3 7 4 10 9 8 6 6 59 63 19 23 17 41 11 12 8 14 0 7 18
137 24 113 26 118 108 47 61 20 9 20 9 10 10 16 NR 44 10 36 46 5 12 41 10 12 8 25 6 59 80 21 38 17 41 11 21 14 14 12 7 39
BMS in the present study was 19.4% and when we analyzed data from the 7 case–control studies that compared the ISR rates for DES and BMS in the same study, though the risk of ISR was low in the DES group, there was no significant difference. There were several limitations in this systematic review. First, the quality of the data in the present analysis was relatively low. Second, there was a limited number of subjects in each study, which may produce false positive or negative results. Hence, more trials with a larger number of subjects are needed. In conclusion, our data demonstrated that 17.6% of VA stents were associated with ISR, which was influenced by lesion location and stent type. Conflict of interest No conflict of interest. References [1] B. Kocak, B. Korkmazer, C. Islak, N. Kocer, O. Kizilkilic, Endovascular treatment of extracranial vertebral artery stenosis, World J. Radiol. 4 (2012) 391–400. [2] T.A. Glass, P.M. Hennessey, L. Pazdera, H.M. Chang, R.J. Wityk, L.D. Dewitt, M.S. Pessin, L.R. Caplan, Outcome at 30 days in the New England Medical Center Posterior Circulation Registry, Arch. Neurol. 59 (2002) 369–376.
Stent placement
Intra (n)
Extra (n)
0 0 0 13 50 0 0 0 0 0 0 11 0 0 0 13 0 0 0 17 0 12 0 10 0 8 0 1 18 0 0 5 17 23 11 0 0 0 0 0 0
148 24 113 14 58 116 47 63 20 28 20 106 11 52 29 0 45 10 36 29 5 0 48 0 12 0 23 5 31 80 22 34 0 18 0 30 14 20 12 7 55
DES (n)
BMS (n)
84 13 45 27 0 0 47 0 19 28 0 3 0 52 0 13 4 10 0 0 0 0 3 0 0 8 0 0 49 0 0 0 0 0 0 0 0 0 0 0 0
64 15 81 0 118 0 0 63 0 0 20 130 11 0 29 0 41 0 36 46 5 14 45 10 12 0 23 6 0 80 22 38 17 41 11 30 10 20 12 7 54
Follow up (months)
8.5 12 12 10 6.9 6 28.3 12.5 14.7 16 14.8 29.1 48 6 34 15.2 7.7 12 54 12 15.6 15 6.7 31 24 6 24 8.4 4 11.7 9 11 17 6 8 16.2 33.6 11.3 7 15 6
Restenosis Case (n)
Total (n)
9 5 21 6 19 10 2 17 4 6 0 14 1 6 1 1 23 0 0 16 0 0 9 1 1 1 5 0 2 11 2 11 0 6 0 13 1 6 1 0 5
58 24 85 22 107 104 38 63 19 21 20 107 11 50 7 13 45 10 17 38 5 12 21 9 12 8 19 4 41 40 9 26 11 14 11 30 10 14 12 7 49
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Letter to the Editor
In-stent restenosis after vertebral artery stenting☆ Yongjun Jiang, Xiaomeng Xu, Zhuoyu Wen, Xiaohui Xu, Lian Yang, Xinfeng Liu ⁎ Department of Neurology, Jinling Hospital, Medical School of Nanjing University, 305 Zhongshan East road, Nanjing, Jiangsu, China
a r t i c l e
i n f o
Article history: Received 23 March 2015 Accepted 24 March 2015 Available online 27 March 2015
More than 1/4 of strokes occur in the vertebral artery (VA) or basilar artery (BA) [1]. The major cause of stroke is atherosclerotic stenosis [2] and revascularization was introduced to treat VA stenosis. Researchers have demonstrated the feasibility, safety and efficiency of VA stenting (VAS) [3]. The major concern for current VAS is in-stent restenosis (ISR), which induces recurrent stroke during follow-up [4]. However, the incidence of ISR varies among different studies from 0 [5] to more than 50% [6] due to the heterogeneity in study design, type of stent, follow-up time and evaluation method. In the present study, we aimed to investigate the incidence of ISR and its underlying risks in published reports through April 2014. We searched the PubMed and EMBASE databases with the terms “vertebral artery” in combination with “stenting OR stent OR stent*”. Reference lists of the retrieved publications were scanned manually for all relevant additional studies and review articles. No attempts were made to locate any unpublished data. Studies were included in this analysis if they met the following criteria: (1) The individuals were asymptomatic or symptomatic in the VA territory; (2) stents were used to target atherosclerotic plaques; (3) there was follow-up post-stenting; (4) the incidence of ISR was verified by digital subtraction angiography (DSA). Due to artifact, the ISR detected by magnetic resonance angiography (MRA) was excluded from analysis. Though computed tomography angiography (CTA) could partly detect ISR, its sensitivity and specificity were lower than DSA; therefore, the ISR detected by CTA was also excluded. Studies were excluded if (1) the study was a case report; (2) the incidence of ISR in the VA was not clearly illustrated in the paper; (3) the outcome was only risk of stroke without ISR; (4) only angioplasty was performed.
☆ This study was financially supported by the National Science Foundation of China (31200817, 81471181 and 31171016) and the Jiangsu Provincial Special Program of Medical Science (BL2013025). There was no relationship with any industry. ⁎ Corresponding author. E-mail address: xfl[email protected] (X. Liu).
http://dx.doi.org/10.1016/j.ijcard.2015.03.377 0167-5273/© 2015 Elsevier Ireland Ltd. All rights reserved.
A pooled risk estimate was obtained by the Mantel–Haenszel method. The validity of pooling the risk estimates (test of homogeneity) was assessed with the Q-test and I2 statistics. In the presence of significant heterogeneity, the random-effects model based on the method described by DerSimonian and Laird was adopted. A flow diagram for the literature search is shown in Fig. 1A. A total of 53 studies met the criteria. The characteristics of included studies are summarized in Table 1. All of the studies comprised of 2200 patients with 279 asymptomatic and 1893 symptomatic patients in the VA territory with 2389 lesions successfully receiving 2292 stents (628 drug eluting stents (DES) and 1664 bare metal stents (BMS)). A total of 1942 stents were visualized by DSA at a mean of 16.7 months after stent placement. ISR was defined as ≥ 50% stenosis within the stents. A total of 341 ISR cases (17.6%) were identified and the incidence of recurrent vascular events was higher compared to patients without ISR (17.5% vs. 2.2%). The ISR risk for DES (28/214) was lower than for BMS (73/287), but there was no significant difference (Fig. 1B). The pool risk was 0.74 (95% CI, 0.44–1.24). The intracranial ISR rate (15.4%, 47/306) was lower than the extracranial ISR rate (17.8%, 269/1,513). In a subgroup analysis of the 8 case–control studies that compared intracranial and extracranial VAS in a single study (Fig. 1C), the pooled risk for ISR in intracranial stents was 1.17 (95% CI, 0.67–2.03). For the extracranial VAS, there was 16.7% (9/48) ISR for stent placed in the non-ostium of VA, which was slightly lower compared to the VA ostium (18.5%, 253/1,368). Over time, the total ISR rate for VA stents decreased (Fig. 1D). Before 2008, the ISR risk of VA stents was almost 28.8% but decreased to 15.1% based on data from 2009 to 2014. Our study demonstrated that 17.6% of patients receiving VAS had ISR, which increased the risk of recurrent stroke. This result was inconsistent with previous studies, which showed that ISR was a major concern for VAS [7]. The ISR was influenced by lesion location and stent type. Intracranial VAS ISR was lower than for extracranial VAS based on all of the studies. However, when a meta-analysis was performed based on case–control studies to decrease possible bias, the ISR rate was comparable between intracranial and extracranial VAS. The result was partially supported by previous studies [8]. The reason for different ISR rates between the VA and carotid artery is not clear. As for extracranial VAS, non-ostial ISR was slightly lower than ostial ISR (16.7% vs. 18.5%). Since 2006, Gupta et al. used DES to treat VA atherosclerotic stenosis to avoid ISR [9]. A previous systematic review summarized that DES were associated with a lower restenosis rate (11%) compared to BMS (30%) at a mean of 24 months of follow-up [10]. Our data were consistent with these findings. A slight difference was that the ISR rate for
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Fig. 1. ISR of VAS. (A) Flow diagram for the literature search. (B) The pooled risk for in-stent restenosis of DES and BMS. The data were extracted from case–control studies. (C) The pooled risk of in-stent restenosis in intra- and extracranial VA stents. The data were extracted from case–control studies. (D) The annual incidence of in-stent restenosis. Over time, the rate of in-stent restenosis decreased.
Table 1 Study characteristics. Author
Year
Region
Patients Asymptom (n)
Langwieser [11] Lin [12] He [13] Li [14] Lee [15] Uygunoglu [16] Mohammadian [17] Tang [18] He [19] Lu [20] Song [8] Vajda [21]
2014 2014 2013 2014 2013 2013 2013 2013 2013 2013 2012 2012
Germany China China China Korea Turkey Iran China China China China Germany
4 0 0 18 57 0 0 0 0 0 0 NR
Lesions Symptom TIA (n)
Stroke (n)
Total (n)
19 30 0 3 0 0 206 21 21 14 134 NR
12 60 27 11 0 9 0 5 0 10 72 NR
31 90 27 14 0 9 206 26 21 24 206 NR
Stent placement
Intra (n)
Extra (n)
DES (n)
BMS (n)
0 14 26 0 0 0 21 0 9 24 29 15
35 76 0 32 57 9 218 26 12 0 199 0
12 42 0 0 9 0 0 0 0 24 121 15
23 48 26 32 48 9 223 26 20 0 98 0
Follow up (months)
5 12 8.6 18.3 8.2 50.2 13.2 12.0 15.5 35 43 6.9
Restenosis Case (n)
Total (n)
7 15 2 1 13 0 38 0 4 2 23 0
30 90 9 32 57 9 223 16 10 20 226 15
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Table 1 (continued) Author
Year
Region
Patients Asymptom (n)
Edgell [22] Raghuram [23] Al-Ali [24] Fields [25] Vajda [26] Hatano [27] Chen [28] Zhou [29] Park [30] Wener [31] Chung [32] Jenkins [33] Karameshev [34] Vajda [35] Parkhutik [36] Vajda [37] Taylor [6] Yu [38] Kakino [39] Seifert [40] Edgell [41] Ralea [42] Du [43] Abruzzo [44] Tsutsumi [45] Qureshi [46] Dabus [47] Fessler [48] Gupta [49] Lin [50] Weber [51] Weber [52] Kim [53] SSYLYIA [54] Jiang [55] Albuquerque [56] Cloud [57] Kogure [58] Mukherjee [59] Michel [60] Chastain [61]
2013 2012 2011 2011 2012 2011 2011 2011 2010 2010 2010 2010 2010 2009 2010 2010 2008 2009 2009 2009 2010 2008 2007 2007 2007 2006 2006 1998 2006 2006 2005 2005 2005 2004 2003 2003 2003 2001 2001 2000 1999
USA USA USA USA USA Japan China China Korea Germany Korea USA Switzerland USA Spain USA USA Hongkong Japan Austria USA France China USA Japan USA USA USA USA Taiwan Germany Germany Korea USA China USA UK Japan Japan USA USA
0 0 0 0 0 90 0 0 0 19 0 96 0 38 13 NR 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 9 0 5 0 0 11
Lesions Symptom TIA (n)
Stroke (n)
Total (n)
55 NR NR 16 NR 64 NR 18 0 0 9 9 5 0 1 NR 0 0 0 15 2 5 37 0 3 0 19 0 0 17 2 15 0 0 0 9 6 0 12 0 21
82 NR NR 10 NR 44 NR 43 20 9 11 0 5 10 15 NR 44 10 36 31 3 7 4 10 9 8 6 6 59 63 19 23 17 41 11 12 8 14 0 7 18
137 24 113 26 118 108 47 61 20 9 20 9 10 10 16 NR 44 10 36 46 5 12 41 10 12 8 25 6 59 80 21 38 17 41 11 21 14 14 12 7 39
BMS in the present study was 19.4% and when we analyzed data from the 7 case–control studies that compared the ISR rates for DES and BMS in the same study, though the risk of ISR was low in the DES group, there was no significant difference. There were several limitations in this systematic review. First, the quality of the data in the present analysis was relatively low. Second, there was a limited number of subjects in each study, which may produce false positive or negative results. Hence, more trials with a larger number of subjects are needed. In conclusion, our data demonstrated that 17.6% of VA stents were associated with ISR, which was influenced by lesion location and stent type. Conflict of interest No conflict of interest. References [1] B. Kocak, B. Korkmazer, C. Islak, N. Kocer, O. Kizilkilic, Endovascular treatment of extracranial vertebral artery stenosis, World J. Radiol. 4 (2012) 391–400. [2] T.A. Glass, P.M. Hennessey, L. Pazdera, H.M. Chang, R.J. Wityk, L.D. Dewitt, M.S. Pessin, L.R. Caplan, Outcome at 30 days in the New England Medical Center Posterior Circulation Registry, Arch. Neurol. 59 (2002) 369–376.
Stent placement
Intra (n)
Extra (n)
0 0 0 13 50 0 0 0 0 0 0 11 0 0 0 13 0 0 0 17 0 12 0 10 0 8 0 1 18 0 0 5 17 23 11 0 0 0 0 0 0
148 24 113 14 58 116 47 63 20 28 20 106 11 52 29 0 45 10 36 29 5 0 48 0 12 0 23 5 31 80 22 34 0 18 0 30 14 20 12 7 55
DES (n)
BMS (n)
84 13 45 27 0 0 47 0 19 28 0 3 0 52 0 13 4 10 0 0 0 0 3 0 0 8 0 0 49 0 0 0 0 0 0 0 0 0 0 0 0
64 15 81 0 118 0 0 63 0 0 20 130 11 0 29 0 41 0 36 46 5 14 45 10 12 0 23 6 0 80 22 38 17 41 11 30 10 20 12 7 54
Follow up (months)
8.5 12 12 10 6.9 6 28.3 12.5 14.7 16 14.8 29.1 48 6 34 15.2 7.7 12 54 12 15.6 15 6.7 31 24 6 24 8.4 4 11.7 9 11 17 6 8 16.2 33.6 11.3 7 15 6
Restenosis Case (n)
Total (n)
9 5 21 6 19 10 2 17 4 6 0 14 1 6 1 1 23 0 0 16 0 0 9 1 1 1 5 0 2 11 2 11 0 6 0 13 1 6 1 0 5
58 24 85 22 107 104 38 63 19 21 20 107 11 50 7 13 45 10 17 38 5 12 21 9 12 8 19 4 41 40 9 26 11 14 11 30 10 14 12 7 49
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