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Ischemic stroke
Original research
Efficacy of combined use of a stent retriever and aspiration catheter in mechanical thrombectomy for acute ischemic stroke
  1. Tomohiro Okuda1,
  2. Koichi Arimura1,
  3. Ryu Matsuo2,
  4. So Tokunaga3,
  5. Kenta Hara3,
  6. Shinya Yamaguchi4,
  7. Hidenori Yoshida5,
  8. Ryota Kurogi5,
  9. Katsuharu Kameda6,
  10. Osamu Ito6,7,
  11. Tomoyuki Tsumoto3,8,
  12. Koji Iihara1,9,
  13. Taichiro Mizokami10,
  14. Takeshi Uwatoko11,
  15. Ataru Nishimura1,
  16. Katsuma Iwaki1,
  17. Masahiro Mizoguchi1
  18. QNET investigators
  1. 1 Department of Neurosurgery, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan
  2. 2 Center for Cohort Studies, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan
  3. 3 Department of Neuroendovascular Therapy, National Hospital Organisation Kyushu Medical Center, Fukuoka, Fukuoka, Japan
  4. 4 Department of Neurosurgery, Steel Memorial Yawata Hospital, Kita-Kyushu, Fukuoka, Japan
  5. 5 Department of Neurosurgery, Fukuoka Tokushukai Medical Center, Kasuga, Fukuoka, Japan
  6. 6 Department of Neurosurgery, Shin Koga Hospital, Kurume, Fukuoka, Japan
  7. 7 Department of Neurosurgery, Kieikai Hospital, Fukuoka, Japan
  8. 8 Department of Neurosurgery, Showa University Fujigaoka Hospital, Kanagawa, Japan
  9. 9 Department of Neurosurgery, National Cerebral and Cardiovascular Center Hospital, Suita, Osaka, Japan
  10. 10 Department of Neurosurgery, Saga -Ken Medical Centre Koseikan, Saga, Saga, Japan
  11. 11 Department of Cerebrovascular Medicine, Saga Prefecture Medical Center Koseikan, Saga, Saga, Japan
  1. Correspondence to Dr Koichi Arimura, Neurosurgery, Kyushu University, Fukuoka 812-8582, Japan; karimura{at}ns.med.kyushu-u.ac.jp

Abstract

Background The efficacy of combined stent retriever (SR) and aspiration catheter (AC; combined technique: CBT) use for acute ischemic stroke (AIS) is unclear. We investigated the safety and efficacy of single-unit CBT (SCBT)—retrieving the thrombus as a single unit with SR and AC into the guide catheter—compared with single use of either SR or contact aspiration (CA).

Methods We analysed 763 consecutive patients who underwent mechanical thrombectomy for AIS between January 2013 and January 2020, at six comprehensive stroke centers. Patients were divided into SCBT and single device (SR/CA) groups. The successful recanalization with first pass (SRFP) and other procedural outcomes were compared between groups.

Results Overall, 240 SCBT and 301 SR/CA (SR 128, CA 173) patients were analyzed. SRFP (modified Thrombolysis In Cerebral Infarction (mTICI) ≥2c, 43.3% vs 27.9%, p<0.001; mTICI 3, 35.8% vs 25.5%, p=0.009) and final mTICI ≥2b recanalization (89.1% vs 82.0%, p=0.020) rates were significantly higher, puncture-to-reperfusion time was shorter (median (IQR) 43 (31.5–69) vs 55 (38–82.2) min, p<0.001), and the number of passes were fewer (mean±SD 1.72±0.92 vs 1.99±1.01, p<0.001) in the SCBT group. Procedural complications were similar between the groups. In subgroup analysis, SCBT was more effective in women, cardioembolic stroke patients, and internal carotid artery and M2 occlusions.

Conclusions SCBT increases the SRFP rate and shortens the puncture-to-reperfusion time without increasing procedural complications.

  • catheter
  • stroke
  • intervention
  • thrombectomy

Data availability statement

Data are available upon reasonable request.

https://doi.org/10.1136/neurintsurg-2021-017837

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    Introduction

    Mechanical thrombectomy (MT) is the standard of therapy for acute ischemic stroke (AIS) due to large vessel occlusion, achieving high rates of successful revascularization, with excellent safety.1 However, previous studies have suggested that multiple device passes are associated with reduced recanalization rates, poor clinical outcomes, and hemorrhagic complications.2 3 The goal of MT is the complete recanalization of the target vessel, with a single device pass, as quickly as possible. Therefore, a new index has been proposed: the ‘first pass effect’ (FPE), which is defined as successful recanalization after a single pass of the device, with no rescue maneuver.4 5 Although refinements in MT with newer and integrated techniques,6 novel stent retrievers,7 8 and better catheter designs9 have been developed, the choice of device and technique to achieve the FPE in AIS remains unclear.

    It has been proven in multiple large randomized clinical trials that endovascular recanalization therapy using a stent retriever (SR) is beneficial for AIS.1 Moreover, contact aspiration (CA) using a large-bore aspiration catheter (AC), including a direct first pass aspiration technique (ADAPT), is also an established thrombectomy technique.10 In addition to these two conventional methods, several case series have demonstrated the efficacy of the combined use of an SR and AC for AIS. It has been reported that the combined technique (CBT) using an SR and AC achieved better angiographic and clinical outcomes than MT with single device use11–18; however, contrasting results have also been reported.19–21 CBT may improve the rate of recanalization due to the secure capture of clots with multiple devices, but its efficacy has not been fully determined.

    This study thus aimed to investigate the safety and efficacy of CBT compared with the single-device use of an SR or AC.

    Methods

    Study design and patients

    This multicenter retrospective study evaluated 763 consecutive patients who underwent MT for AIS due to large vessel occlusion, between January 2013 and January 2020, at six comprehensive stroke centers: Kyushu University Hospital (Fukuoka City, Fukuoka, Japan); Saga-Ken Medical Center Koseikan (Saga City, Saga, Japan); Kyushu Medical Center (Fukuoka City, Fukuoka, Japan); Steel Memorial Yahata Hospital (Kitakyushu City, Fukuoka, Japan); Fukuoka Tokushukai Hospital (Fukuoka City, Fukuoka, Japan); and Shin Koga Hospital (Kurume City, Fukuoka, Japan). Institutional review board approval was obtained from each participating institution. Given the retrospective enrollment of the patients in this study, the need for written informed consent was waived.

    The indication for intervention for AIS was discerned based on the guidelines of the American Heart Association/American Stroke Association and the Japanese Society for Neuroendovascular Therapy (JSNET). AIS was diagnosed by CT or MRI. All eligible patients received intravenous administration of recombinant tissue plasminogen activator (rt-PA; at 0.6 mg per kg body weight). Endovascular therapy was performed by experienced neurointerventionalists at each comprehensive stroke center.

    We included patients who underwent MT with the use of an SR or CA, as well as patients treated with the combined use of these devices for isolated anterior circulation large vessel occlusions. Occlusions were defined as blockages in the internal carotid artery (ICA) from the cervical segment to the bifurcation and the middle cerebral artery (MCA) M1 and M2 segments. We excluded patients with posterior circulation stroke, anterior cerebral artery occlusion, common carotid artery occlusion and tandem occlusion (for example, ICA and M1), and who were younger than 18 years of age. We also excluded patients who were provided with no intervention or those otherwise treated using other recanalization techniques, such as intra-arterial thrombolysis, balloon angioplasty, and aspiration by balloon guide catheter (BGC), before MT. Because CBT had several variations, we excluded patients treated with withdrawal CBT, where the thrombus and SR were withdrawn into the AC. Details of the operative techniques were as described in succeeding passages.

    To exclude potential confounders in the selection of treatment strategies between operators and institutions, the six participating institutions were classified into two groups, academic/national centers, and other hospitals (one academic center, one national center, and four other hospitals). Additionally, the attending doctors were classified based on whether they were specialists or non-specialists of the JSNET. In each of the cases involved, the attending doctor provided disposition on the optimal case-to-case strategy for MT.

    Details of the procedure

    Patients were divided into two groups based on the technique used on first attempt at thrombus removal: the combined use of SR and AC (combined technique: CBT) group, and the single device use (SR or CA: SR/CA) group. The decision regarding the thrombectomy technique for each case was at the discretion of the treating physicians. A BGC was used in almost all cases. The combined technique came into use at our institutions in May 2015. It was selected more frequently in recent cases (online supplemental figure 1). If effective reperfusion was not achieved after the first pass procedure, the same or other techniques were employed for rescue maneuvers.

    Combined technique

    The CBT employed, which involved concomitant use of an SR and AC, was based on previous reports. There have been several reports detailing methods for CBT. The first involves retrieving a singular unit with the thrombus lodged between the SR and AC, along the guide catheter11–13 (single-unit CBT (SCBT)). The second involves retracting the SR with the thrombus into the AC14–16 (withdrawal CBT (WCBT)). The former was performed in 88.7% of cases, and the latter in 11.2%. However, only the SCBT group was included in the analysis to limit the effect of bias arising from the diversity of MT techniques. The guide catheters used in 98.4% of the SCBT group were BGCs. The AC used for the procedures were 5MAX ACE (Penumbra, Alameda, CA) in 58.4%, ACE 68 (Penumbra) in 13.9%, 5MAX (Penumbra) in 6.3%, CATALYST 6 (Stryker Neurovascular, Kalamazoo, MI) in 5.5%, SOFIA 5F (Microvention, Tustin, CA) in 1.2%, and SOFIA 6F in 0.8% of the SCBT group. The 4MAX (Stryker), used in 12.7%, and the 3MAX (Stryker), used in 1.2%, were mainly used in M2 occlusions. As an SR, the Trevo XP ProVue Retriever (Stryker) and the Solitaire (Covidien, Irvine, CA) were used in 66.8% and 29.4%, respectively. Rescue therapies were needed in 45% of the patients in the CBT group. SCBT was used as rescue therapy in 50.6%, WCBT in 4.1%, CA in 32.8%, and other techniques involving balloon angioplasty in 12.3%.

    Single device use techniques

    SR technique

    We deployed an SR at the site of the occlusion using a 0.021–0.027 inch microcatheter and a micro-guidewire when using the SR alone. The SR, which captured the thrombus, was slowly withdrawn with proximal protection using a BGC. In the SR group, BGC was used in all patients except for one case in whom a brachial approach was implemented. The Trevo XP ProVue Retriever and Solitaire were used in 45.3% and 46.9% of patients, respectively.

    CA technique

    A large-bore AC was navigated to the proximal end of the thrombus and slowly withdrawn with proximal protection using the CA technique. The BGC was used in all cases except for one case in the CA group in whom a brachial approach was used. The 5MAX, 5MAX ACE, 4MAX, and ACE68 catheters were used in 40%, 34.1%, 10.5%, and 7.6% of cases, respectively. Rescue therapies were required in 59.1% of the patients in the SR/CA group. As rescue therapy, the combined technique was used in 32.6%, CA in 34%, SR alone in 22.9%, and other techniques in 10.4% of the SR/CA group.

    Outcomes

    The primary outcome was the rate of successful recanalization (defined as modified Thrombolysis In Cerebral Infarction (mTICI) 2c‒3) at the first pass procedure. The secondary outcomes were the rate of successful recanalization at the end of all procedures, time from puncture to successful recanalization, and procedural complications.

    Complications included symptomatic hemorrhagic complications (defined as worsening >4 points on the National Institutes of Health Stroke Scale (NIHSS)), vessel perforations, and ischemic complications due to clot migration to a vessel of the same or new territory. Additionally, we conducted a subgroup analysis of the complete recanalization rate at the first pass to compare the SCBT group with the SR/CA group.

    Data collection and statistical analyses

    Patient characteristics and procedural, angiographic and clinical outcome data were retrieved and analyzed at each participating institution. Statistical analysis was performed using JMP 14 (SAS Institute Inc, Cary, NC). Data of baseline and procedural characteristics and the outcomes of the two groups were compared using the χ2 test for categorical data and Student’s t-test or Wilcoxon signed-rank test for continuous data, respectively. Logistic regression analysis was performed to assess the association between the thrombectomy technique and the recanalization rate, with adjustment for confounding factors. Statistical significance was set at p<0.05.

    Results

    We included 541 of 763 patients for analysis in this study. There were 240 (44.3%) patients in the SCBT group and 301 (55.7%) in the SR/CA group (SR 128 (42.5%), CA 173 (57.5%)). The flow diagram illustrates the reasons for patient exclusion (figure 1). The mean age of the patients was 77.0±11.9 years, with 255 male (47.1%) and 286 female patients (52.8%) included. The baseline and procedural characteristics are depicted in table 1. Atrial fibrillation (p=0.027), pre-stroke modified Rankin scale (mRS) score ≥1 (p=0.006), and attending doctor classifications (p=0.023) were statistically different between the two groups (table 1).

    View this table:
    Table 1

    Baseline and procedural characteristics of the two groups

    Figure 1
    Figure 1

    Participant flow diagram depicting reasons for exclusion. AC, aspiration catheter; AIS, acute ischemic stroke; BGC, balloon guide catheter; CA, contact aspiration; CBT, combined technique using stent retriever and aspiration catheter; IA-UK, intra-arterial urokinase; MT, mechanical thrombectomy; SR, stent retriever.

    In terms of procedural outcomes, the SCBT group achieved a significantly higher rate of successful recanalization on first pass procedure (SRFP) (table 2). In the SCBT group, mTICI 2c–3 and mTICI 3 were achieved in 43.3% and 35.8% of patients, respectively, and in 27.9% and 25.5%, respectively, in the SR/CA group. Moreover, the rate of mTICI 2b–3 at the end of all procedures and that of mTICI 2c–3 were significantly higher in the SCBT group than in the SR/CA group (mTICI 2b–3, 89.1% vs 82.0%, p=0.020; mTICI 2c–3, 62.5% vs 51.8%, p=0.012). Logistic regression analysis revealed that SCBT was an independent factor for improving SRFP (mTICI 2c–3) rates, when adjusted for age, sex, pre-stroke mRS score ≥1, atrial fibrillation, site of occlusion, stroke etiology, intravenous administration of rt-PA, and attending doctor classification (odds ratio (OR) 2.12, 95% confidence interval (CI) 1.45 to 3.09, p<0.001). Additionally, SCBT was also found to be an independent factor for mTICI 2b–3 recanalization at the end of all procedures (OR 1.90, 95% CI 1.13 to 3.11, p=0.015).

    View this table:
    Table 2

    Procedural and clinical outcomes of the two groups

    To exclude bias arising from the treatment of those who underwent either SR or CA as one group, we performed post-hoc analysis for three separate groups: SCBT, SR, and CA (online supplemental tables 1 and 2). There was significant difference in the rate of SRFP (mTICI 2c–3) between three groups (SCBT vs SR vs CA, 43.3% vs 31.2% vs 25.4%, respectively, p<0.001). MT technique was still an independent factor for SRFP on logistic regression analysis (SCBT/SR, OR 1.84, 95% CI 1.13 to 2.99, p=0.013; SCBT/CA, OR 2.34, 95% CI 1.51 to 3.62, p<0.001).

    Since we included cases treated between 2013 and 2020, there could have been other confounders such as innovation in the devices and the user experiences. Comparing patients included in this study based on whether they were treated pre-2017 or post-2018 (online supplemental table 3), CBT was more likely to be chosen as the first-line MT technique for post-2018 patients, and large bore aspiration catheters were also more likely to be used in the post-2018 group. Moreover, the rate of specialized operators certified by the national society, onset to puncture time, and the rate of recanalization were not different between the two groups. These results suggest that changes across eras of treatment did not directly affect the rate of SRFP.

    The details and safety of the procedures and clinical outcomes are summarized in table 2. The number of passing clots in all procedures was significantly lower in the SCBT group than in the SR/CA group (mean±SD 1.72±0.92 vs 1.99±1.01, p<0.001). The rate of rescue maneuvers was significantly lower in the SCBT group than in the SR/CA group (45.0% vs 59.1%, p=0.001). Moreover, puncture-to-reperfusion time was significantly shorter in the SCBT group than in the SR/CA group (median (IQR) 43 (31.5–69) vs 55 (38–82.2) min, p<0.001). Additionally, there were no significant between-group differences in procedural complications. The clinical outcomes at 90 days after MT were available for 482 of the 541 patients (89.0%); however, favorable outcome and mortality at 90 days were not statistically different between the groups.

    Finally, we conducted a detailed analysis to investigate the subgroup in which SCBT was more effective (table 3). Subgroup analysis revealed that SRFP with mTICI 2c‒3 was significantly larger in the SCBT group than in the SR/CA group, regardless of age and pre-stroke mRS score. SCBT was more effective in achieving SRFP in female patients, patients with comorbid atrial fibrillation, and those with cardioembolic stroke. Additionally, according to the site of occlusion, the rate of SRFP was significantly higher in the SCBT group than in the SR/CA group for ICA and M2 occlusions, but not for M1 occlusions (ICA 45.1% vs 22.9%, p=0.001; M2 41.1% vs 16.6%, p=0.004; M1 42.7% vs 35.8%, p=0.285).

    View this table:
    Table 3

    Subgroup analysis of successful recanalization rate (mTICI ≥2c) at the first pass

    Discussion

    The main findings of this study were that the SCBT achieved a higher rate of SRFP, a higher rate of successful recanalization at the end of all procedures, required a lower total number of passes, involved a shorter puncture-to-reperfusion time, and resulted in no increase in procedural complications as compared with the use of a single SR or AC device.

    CBT has been reported to increase the rate of successful recanalization as compared with use of a single device such as an SR or AC,11–18 but contradictory results have also been reported.19–21 The efficacy of CBT had not been conclusively evaluated to date, because of the complexity of the procedure and the different contexts of the reported studies. First, the use of a BGC may be important in preventing distal clot migration. In our study, a BGC was used in 98.4% of patients in the SCBT group, and it may have contributed to the efficacy of SCBT. Second, CBT may be classified in SCBT11–13 and WCBT.14–16 Because of the complexity and variation between procedures making it difficult to analyze the advantages of CBT, this study focused specifically on SCBT. Our results suggested that SCBT with a BGC may increase successful recanalization on first pass and shorten puncture to recanalization time compared with the use of single devices.

    In terms of advantage of SCBT, it may increase the rate of successful recanalization by facilitating reliable capture of the clots. Distal-placed SR and proximal AC may grasp the clot more tightly during clot removal and prevent the clot from migrating distally.11–13 In SCBT with a BGC, residual fragmented clots may migrate distally, but using a BGC could prevent clot migration.15 16 A large-bore AC located near the clots may have contributed to the maximum suction ability. Consequently, the SCBT may aid in increasing the SRFP rate. Moreover, a coaxial system using an AC with a microcatheter provides support for safe and easy navigation to the occlusion site of the distal vessel and reduces the instability of the microcatheter. This enables rapid access to the thrombus and improves distal support for the microcatheter and micro-guidewire passing through the lesion, even in complex and tortuous target vessels, and it may shorten the time of the total procedure.22 23 It is probable that the higher rate of SRFP, lower total number of passes, and use of an AC as an intermediate catheter contributed to the shorter puncture-to-reperfusion time in the SCBT group than in the SR/CA group in our study. Finally, an intermediate catheter located distally reduces the straightening and stretching of the vessels during SR retraction, which may prevent hemorrhagic complications.

    Our results are not consistent with those of several previous reports.19–21 This discrepancy could be due to several reasons. First, we focused on the SRFP in this study. Second, we used a BGC in almost all cases in both the SCBT and SR/CA groups. Third, a large case volume was collected from the multicenter study.

    It has been reported that the FPE contributes to improving clinical outcomes by reducing the procedure time and hemorrhagic complications.4 5 In our study, changes from mTICI 2c‒3 on first pass was significantly increased in the SCBT group, and the number of passes and puncture-to-reperfusion times were significantly reduced in the SCBT group as compared with the SR/CA group. These results suggest that the SCBT may increase the FPE as compared with MT with a single device. The rate of successful and final recanalization was also higher in the SCBT group compared with the SR/CA group (table 2); however, this may still be overestimated in the SR/CA group because CBT was used for rescue therapy in 36.2% of the SR/CA group. Moreover, symptomatic hemorrhagic complications in the SCBT and SR/CA groups were 3.3% and 5.6%, respectively. Consequently, the SCBT may reduce the puncture-to-reperfusion time without an increase in hemorrhagic complications. Nevertheless, the clinical outcomes of the mRS score and mortality at 90 days after onset were not different between the SCBT and SR/CA groups. These results may be attributed to differences in patient backgrounds (table 1). In this study we focused on the technical efficacy of SCBT, based on the rate of SRFP and not on improvement of clinical outcomes. Further randomized controlled trials are required to confirm the long-term efficacy of the SCBT.

    Subgroup analysis revealed that female sex, comorbid atrial fibrillation, cardioembolic etiology, and ICA and M2 occlusion were related to the efficacy of the SCBT (table 3). There was a female predominance among those with SRFP by the SCBT. It has been reported that recent MT trials did not find a difference in successful recanalization, defined by mTICI 2b–3, according to the sex of the patients.1 24 However, female patients tended to require a longer procedure time for recanalization in the DEFUSE 3 cohort.24 Therefore, the SCBT may be more effective in achieving earlier SRFP in female patients. In terms of stroke etiology, the SCBT is more beneficial in cardioembolic stroke due to atrial fibrillation, because the total removal of clots leads to better recanalization in cardioembolic stroke. However, clot removal with an SR is insufficient to achieve successful recanalization in atherosclerotic brain infarction (ATBI), because severe stenosis may remain or re-occlusion may occur, even if successful clot retrieval is achieved in ATBI.25 26 Therefore, adequate recanalization may not be achieved even after the SCBT. In terms of the site of occlusion, in ICA occlusions and M2 occlusions, the SCBT presented a significantly higher rate of SRFP than SR/CA. For ICA occlusions, the lower first pass recanalization rate in SR/CA techniques could be explained by large and hard clots as compared with MCA occlusions.27 We believe that concomitant use of a large-bore catheter and an SR can effectively capture even large and hard clots; therefore, the SCBT is more effective in ICA occlusion than SR/CA. However, SR/CA techniques could be sufficient to engage clots in M1 occlusions. This study also showed a higher first-pass recanalization rate for SCBT in M2 occlusions, which is consistent with previous studies.18 28 It is probable that the smaller diameter of the M2 artery decreasing in the dead space between the AC and the artery wall may increase the suction force and enhance entrapment of the clot by the SR and aid in separating the thrombus from the artery wall.28 Moreover, because non-segmented SRs are stretched by passing tortuous vessels,29 clots may be disengaged from SRs during SR withdrawal from the M1-2 bifurcation or the ICA bifurcation.

    Our study had several limitations. First, the data were retrospective and observational. Differences in patient backgrounds and procedure selection bias between the SCBT and SR/CA groups were not completely excluded because of the retrospective study design. Second, despite considering the treatment era in which the procedures were performed, whether they were performed pre-2017 or post-2018, there was no difference in the rate of SRFP between the two groups (online supplemental table 3). However, potential confounders such as the innovations on the devices and the effects of the learning curve for the treatment of AIS could not be completely excluded in our cohort. Third, the SR/CA group included both those who underwent SR alone and those who underwent CA. In the Contact Aspiration vs Stent Retriever for Successful Revascularization (ASTER) trial, the successful recanalization rate and clinical outcomes were equal between the SR-only technique and ADAPT.10 We aimed to investigate the efficacy of the combined use of SR and AC in this study. Therefore, we included patients who underwent SR alone and CA alone in the same SR/CA group, even though there were differences in the procedures.

    Despite these limitations, we believe that this study demonstrated the efficacy of SCBT in achieving SRFP for large vessel occlusion, without an increase in complications. Further randomized studies are required to validate our findings.

    Conclusions

    SCBT may increase the rate of successful recanalization with the first pass and may shorten the puncture-to-reperfusion time without increasing procedural complications.

    Data availability statement

    Data are available upon reasonable request.

    Ethics statements

    Patient consent for publication

    Ethics approval

    The present study was approved by the Institutional Review Board of Kyushu University, which waived the requirement for informed consent from the participants. Approval ID number was 2019–238.

    Acknowledgments

    We thank the individuals who contributed to the study or manuscript preparation but did not meet all criteria for authorship.

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    Supplementary materials

    Footnotes

    • Collaborators QNET investigators; Kyushu University: Koji Yoshimoto, MD, PhD, Masahiro Mizoguchi, MD, PhD, Koichi Arimura, MD, PhD, Ataru Nishimura, MD, PhD, Katsuma Iwaki, MD, Tomohiro Okuda, MD, Yuya Koyanagi, MD. Kyushu Medical Center: So Tokunaga, MD, Kenta Hara, MD. Saga-ken Medical Center Koseikan: Taichiro Mizokami, MD, PhD, Takeshi Uwatoko, MD, Keisuke Ido, MD.

      Fukuoka Tokushukai Hospital: Hidenori Yoshida, MD, Ryota Kurogi, MD, PhD. Steel Memorial Yawata Hospital: Shinya Yamaguchi, MD. Shin Koga Hospital: Katsuharu Kameda, MD, PhD. Kieikai Hospital: Osamu Ito, MD, PhD. Aso Iizuka Hospital: Masanori Kai, MD, PhD.

    • Contributors All authors meet the ICMJE authorship criteria. TO designed this study and wrote the initial draft of the manuscript. All other authors critically reviewed the manuscript and assisted in the preparation of the manuscript. All authors approved the final version of the manuscript, and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

    • Funding This work was supported by JSPS KAKENHI (Grant number, JP20K09350), Daiwa Securities Health Foundation (Grant number, 20204723), and Bristol Myers Squibb Research grant (Grant number, 60961775).

    • Competing interests None declared.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.