Incidence and risk factors for inferior vena cava filter thrombosis detected at time of filter retrieval in patients with lower extremity deep vein thrombosis: a multicenter retrospective cohort study

Introduction

Inferior vena cava filters (IVCFs) are common intravascular devices that are widely applied to prevent fatal pulmonary embolism (PE) from occurring in high-risk patients with lower extremity deep vein thrombosis (LEDVT). Despite IVCFs being first introduced in 1967, many controversies regarding their utilization and net benefit remain (1-3). IVCF can reduce the incidence of PE in the short term, but it does not come without its own risks (2,3). Insertion-site thrombosis is one of the uncommon adverse events of IVCF placement, with other complications being filter migration, fractures, and inferior vena cava (IVC) wall or adjacent organ perforation (3-5). Moreover, the indwelling IVCF may predispose patients to secondary thrombosis below or above the IVCFs or progressive LEDVT, which may result in venous stasis or leg swelling (6) or may even trigger recurrent PE, which is closely related to the dysfunction of IVCFs resulting from extended clotting above the IVCFs (7,8). In addition, the occurrence of IVCFs thrombosis may prolong the length of hospital stay, which imposes increasing financial burdens and demands on time (9).

Despite these challenges, there is currently an overall paucity of specific guidelines to aid with screening, and alternative predictive programs for IVCF thrombosis remain ambiguous (1). The clinical signs and symptoms of IVCF thrombosis are insidious, nonspecific, and frequently concealed and confused in patients with LEDVT (1,6). A previous study reported a follow-up of 1,718 patients with IVCF placement by computer tomography venography (CTV) and found that about 18% of these patients underwent IVCF thrombosis, but only 2% of had clinical manifestations of complete obstruction of the IVC (3,8). Therefore, the detection of IVCF thrombosis according to clinical features alone is problematic. CTV has been widely used in the diagnosis of IVCF thrombosis. The venography of IVC is typically used at the time of filter retrieval to assess the filter position, tilt, penetration of the IVC, clots within or cephalad to the IVCF, and IVC thrombosis (4,8). However, the incidence of IVCF thrombosis in relation to IVCF dwell time has only been reported in a few randomized trials (2,4,9). Hence, evaluating the incidence at the time of filter removal and identifying relevant risk factors may be of considerable clinical benefit.

The objectives of this study were to investigate the incidence and risk factors for acute IVCF thrombosis following filters placement in patients with LEDVT based on the data of a multicenter randomized controlled trial (RCT). This may assist in developing individualized plans and better identifying higher risk patients in whom IVCFs have been implanted and providing preventive intervention for high-risk patients with potential thrombosis after IVCF placement. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-23-724/rc).

Methods

Patients and study design

This retrospective cohort study was conducted using data from a multicenter RCT (9). The study was prospectively carried out in 188 patients with LEDVT, and the efficacy and safety of PE prevention were compared between the Octoparms filter {Kossel MedTech [Suzhou] Co., Ltd., Suzhou, China} and the Celect filter (Cook Medical, Bloomington, IN, USA) in 10 clinical centers from 6 provinces in mainland China from October 2017 to March 2019 (10). The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the institutional review board of Nanjing First Hospital (No. QX20170714-02). The requirement for written informed consent was waived due to the retrospective nature of the study.

A total of 188 patients with identified acute LEDVT were enrolled in this multicenter RCT. The inclusion and exclusion criteria are provided in the Table S1. In this multicenter, retrospective cohort study, 10 patients were subsequently excluded due to the lack of complete records regarding the venography of IVC because the IVCFs were left in situ as permanent filters (the flowchart of this study is shown in Figure 1). Of the remaining 178 eligible patients, 58 patients with IVCF thrombosis were classified into an IVCF thrombosis group, and 120 patients without IVCF thrombosis were placed into an IVCF nonthrombosis group. The data concerning these eligible patients were obtained from medical database systems and/or study records. The following information was analyzed: baseline demographics [comprising age, gender, nation, marital status, and body mass index (BMI)]; the presentation of LEDVT [including symptoms and signs, time from symptom onset to admission (if ≤7 days)]; the relevant abnormal laboratory results prior to IVCF placement [including red blood cell counts, white blood cell counts, hematocrit, platelet counts, urine leukocytes, urine erythrocyte, urine proteins, electrocardiography (ECG), and D-dimer value] within the first 48 h; the thrombus characteristics, including the thrombus segment [proximal LEDVT coupled with/without IVC, isolated distal deep vein thrombosis (IDDVT), saphenous vein thrombosis], numbers of involved vessels in the IDDVT, and thrombus limbs (left side, right side, bilateral side, or isolated IVC thrombosis); concurrent PE; comorbidities, including hypertension, diabetes mellitus, cardiologic artery disease (CAD), history of cerebral vascular disease, hyperlipemia, cancer, bronchitis, penicillin anaphylaxis; the risk factors for LEDVT, including trauma, major surgery history, immobilization, rheumatic diseases of immune system (e.g., antiphospholipid antibody syndrome, systemic lupus erythematosus, and rheumatoid arthritis), previous venous thromboembolism (VTE), cancer, and smoking; IVCF-relevant information (the Octoparms and Celect filters are shown in Figure 2), including IVCF place access (right or left femoral, right internal jugular vein), filter location (infrarenal vein or suprarenal vein), IVC diameter, IVC:filter radial ratio (whether ratio >0.587), filter oblique angle (>15°), and the dwell time (i.e., duration of time between filter placement and initial retrieval attempt); and the conjunctive endovascular treatments, including catheter-directed thrombolysis (CDT), percutaneous mechanical thrombectomy (PMT), percutaneous angioplasty (PTA), and percutaneous stents (PTS).

Figure 1 The study flowchart of the inclusion and exclusion criteria of patients with LEDVT. LEDVT, lower extremity deep vein thrombosis; IVCF, inferior vena cava filter; IVC, inferior vena cava.

Figure 2 A schematic representation of the Octoparms filter and the Celect filter. (A) The Octoparms filter. (B) The Celect filter. The permission to reuse these images are obtained.

Definition, diagnosis, and details of IVCF thrombosis

The decision and timing for retrieval were individualized in each case by the referring clinician and the interventional radiologist. The diagnosis of IVCF thrombosis was determined with venography or CTV before IVCF retrieval. Interpretation of the diagnosis was based on the initial radiologist’s reading and subsequently verified by the operators. IVCF thrombosis was defined as the existing filling defect in the IVCF at the venous phase of CTV or venography. The strategic selections of retrieval were left to the discretion of the endovascular operator team, with the size of thrombus usually being the principal consideration (3). If necessary, thrombolysis or percutaneous aspiration was performed prior to retrieval. IVC diameter was measured on venography under a single inspiratory breath-hold and a nonshock status. The proximal LEDVT and IDDVT were defined according to the clinical practice guidelines (11).

Statistical analysis

Statistical analyses were performed using SPSS version 23.0 (IBM Corp., Armonk, NY, USA) and R statistical language software (version 3.6.3; The R Foundation for Statistical Computing, Vienna, Austria). The continuous data are presented as the mean ± standard deviation (SD), and categorical data are expressed as count and percentage. The independent samples t-test was used to assess the correlation between the 2 groups and to compare continuous data, including age, BMI, IVC diameter, IVC:filter radial ratio, and time to IVCF retrieval. The significance of categorical data was tested with a chi-squared test or Fisher exact test. The risk factors for IVCF thrombosis were assessed with using logistic regression, and the univariate approach was followed by multivariate analysis. The predictive cutoff value of IVC:filter radial ratio value for a suspected diagnosis was evaluated with receiver operating characteristic (ROC) curve using R software, and the area under the curve (AUC) was calculated. Findings with a P value <0.05 (2-tailed) were deemed statistically significant.

Results

Patients and the incidence of IVCF thrombosis

Among the 178 eligible patients in the present study, 32.58% (58/178) of patients (mean age: 58±17 years; 43.10% male; 94.83% Han nationality; 91.38% married) with IVCF thrombosis were placed into an IVCF thrombosis group, and 67.42% (120/178) of patients (mean age: 57±14 years; 56.67% male; 98.33% Han nationality; 96.67% married) were placed into an IVCF nonthrombosis group. As for the symptoms and signs of LEDVT, more than half of the patients (58.62% vs. 59.17%; P=0.95) experienced limb swelling, the majority of the time from symptom onset to admission in both groups was ≤7 days (86.21% vs. 72.50%; P=0.04), and the D-dimer value was ≤10 µg/mL (81.03% vs. 70.83%; P=0.15). In addition, patients from the 2 groups underwent comparable abnormal laboratory tests (all P values >0.05), the majority of whom underwent proximal LEDVT (91.38% vs. 78.33%; P=0.03); however, the subgroup (including those with IVC, IDDVT, and saphenous vein thrombosis) as well the numbers of IDDVT involved vessels were not statistically significant (all P values >0.05). The distribution of thrombus favored the left limbs (65.52% vs. 66.67%; P=0.88). Of note, 56.90% of those patients with IVCF thrombosis and 40.00% of those with IVCF nonthrombosis experienced concurrent PE as identified with computed tomography (CT) angiography imaging (P=0.03). The comorbidities and risk factors for patients in the 2 groups were similar and included hypertension (31.03% vs. 27.50%; P=0.63) and recent major surgery history (37.93% vs. 30.00%; P=0.29). Regarding the IVCF-relevant information, the filters used were “umbrella” IVCFs, including the Octoparms and Celect (P=0.16), which were placed mainly in the infrarenal vein (96.55% vs. 98.33%; P=0.83) via the right femoral vein (70.69% vs. 58.33%; P=0.36). In both groups, conjunctive endovascular treatments (including PMT, PTA, PTS, and CDT) were performed, and the patients with IVCF thrombosis had a higher rate of PTA (32.76% vs. 15.83%; P=0.01).

Data on baseline demographics, LEDVT presentation, laboratory examination, thrombus characteristics, concurrent PE, comorbidities and risk factors for LEDVT, and IVCF-relevant information for patients with LEDVT with IVCFs are summarized in Table 1. The anticoagulant treatment was initiated immediately when LEDVT was identified using subcutaneous low-molecular weight heparin at a bolus dose of 100 units/kg, administered twice daily. Following heparin treatment, a combination of oral warfarin therapy was deployed for 3 to 5 days, with the dosage adjusted thereafter to maintain an international normalized ratio within the range of 2.0 to 3.0. Alternatively, rivaroxaban was initiated directly at a dosage of 20 mg once daily. The overall incidence of IVCF thrombosis in patients with LEDVT who received IVCFs was 32.58% (58/178), with a mean filter dwell time of 22.07±27.91 days (range, 4–190 days). The incidence of IVCF thrombosis was 35.25% (49/139) in the first 30 days after IVCF placement and decreased to 22.73% (5/22) between 30 and 60 days dwell time and to 18.18% (2/11) between 60 and 90 days dwell time, implying a decreasing trend within 90 days (Figure 3). An IVCF dwell time interval of longer than 90 days encompassed an extensive period (range, 90–190 days) in 6 patients, 2 of whom were found to have experienced IVCF thrombus (representing 33.33% of those cases with IVCF thrombosis). These patients were not included in this analysis.

Figure 3 Distributions of patients with IVCF thrombosis and IVCF nonthrombosis in relation to dwell time. IVCF, inferior vena cava filter.

IVC diameter and predictive value of IVC:filter radial ratio

The mean IVC diameter of the included patients with IVCF thrombosis was 19.34±2.47 mm, which was shorter than the 20.92±3.52 mm of patients with IVCF nonthrombosis (P<0.001). Based on the diameter of IVCFs examined in vitro, the IVC:filter radial ratios were 0.52±0.08 and 0.56±0.10 (P=0.02) in the IVCF thrombosis and IVCF nonthrombosis groups, respectively. After univariable analysis, predictive the value of the IVC:filter radial ratio was analyzed with ROC curves to identify the optimal cutoff value. A radial ratio >0.587 was discriminant [AUC =0.59; 95% confidence interval (CI): 0.51–0.68; P<0.05] for predicting IVCF thrombosis (ROC curves are shown in Figure 4). The corresponding Youden index was 0.26, and this indicator had a sensitivity of 38.33% and a specificity of 87.93%. Positive predictive value for the IVC:filter radial ratio >0.587 was 86.79%, and the negative predictive value was 40.80%.

Figure 4 The ROC curve was used to identify the optimal cutoff value of the IVC:filter radial ratio for IVC filter thrombosis in patients with lower extremity deep vein thrombosis who received a filter. The cutoff value was 0.587, and the AUC was 0.59 (95% CI: 0.51–0.68). FPR, false positive rate; TPR, true positive rate; AUC, area under the curve; ROC, receiver operating characteristic; IVC, inferior vena cava; CI, confidence interval.

Risk factors for IVCF thrombosis

The univariable analysis of baseline demographics, presentation of LEDVT, laboratory examination results, thrombus characteristics, PE occurrence, comorbidities and risk factors, and IVCF-relevant information for patients with IVCFs and LEDVT showed that the factors that predicted the probability of IVCF thrombosis were as follows: time from symptom onset to admission (P=0.04), thrombus segment (P=0.03), concurrent PE (P=0.03), rheumatic diseases of the immune system (P=0.02), PTA (P=0.01), and IVC:filter radial ratio (P<0.001). Moreover, IVCF thrombosis seemed slightly more likely to develop in female (P=0.10) and unmarried patients (P=0.07) in the IVCF thrombosis group compared with those in the IVCF the nonthrombosis group. The remaining baseline demographics, abnormal relevant laboratory tests within the first 48 h, symptoms and signs, numbers of involved vessels in IDDVT, thrombus limbs, the comorbidities and risk factors for LEDVT, filter types, IVCF placement access, conjunctive treatments, filter oblique angle, and dwell time were not significantly different (all P values >0.05). Multivariate logistic regression analysis showed that concurrent PE [odds ratio (OR) =2.59; 95% CI: 1.27–5.28; P=0.01], rheumatic diseases of the immune system (OR =14.42; 95% CI: 1.52–136.41; P=0.02), and PTA (OR =2.50; 95% CI: 1.09–5.70; P=0.03) were risk factors for the occurrence of IVCF thrombosis, while an IVC:filter radial ratio >0.587 was a protective factor (Table 2).

Discussion

IVCFs are used to decrease the risk of thrombus migration from LEDVT to pulmonary artery, but may also act as a nidus for the development of IVCF thrombosis (1,2), which can have clinical manifestations varying from symptom-free to phlegmasia or leukophlegmasia. Although its occurrence has been shown to be similarly associated with LEDVT in terms of pathology and clinical spectrum, the predisposing risk factors have not been extensively investigated (11). Therefore, increasing the understanding of IVCF thrombosis and seeking related risk factors may yield important clinical benefit. Previous studies have reported that the types of IVCFs, regular anticoagulants after IVCF placement, oblique angle of IVCFs, and other factors that may cause mechanical changes in venous blood flow are related to the occurrence of IVCF thrombosis (2). However, the majority of these assessments have been performed in retrospective studies (1,11). In the present study, baseline demographics, the presentation of LEDVT, laboratory examination results, thrombus characteristics, concurrent PE, comorbidities and risk factors for LEDVT, and IVCF-relevant information from a multicenter, randomized trial were analyzed. We found that concurrent PE (OR =2.59; 95% CI: 1.27–5.28; P=0.01), rheumatic diseases of the immune system (OR =14.42; 95% CI: 1.52–136.41; P=0.02), and PTA (OR =2.50; 95% CI: 1.09–5.70; P=0.03) were risk factors for the occurrence of IVCF thrombosis, while an IVC:filter radial ratio >0.587 was a protective factor against IVCF thrombosis development. Moreover, the abovementioned risk factors are likely to have complex interactions in fostering the occurrence of IVCF thrombosis.

The incidence of IVC thrombosis has been reported to be 4–15%, but depending on the number of IVC filters, the incidence of IVCF thrombosis can range from 1.6% to 33% in the literature (1,2,12). A higher incidence reaching 40% was also reported and was considered to be associated with a relatively short IVCF dwell time (13). Our study similarly showed that 35.25% of patients experienced IVCF thrombosis within 30 days of placement time, with a decreasing trend thereafter, which is in accordance with other studies (3,13). However, this finding needs to be further validated in a well-designed study since the present study lacked a close follow-up at specific time points and since intrafilter thrombosis tends to resolve over time. Moreover, the temporary IVCFs tend to be thrombosed more often, simply because these are discovered at the time of intended retrieval (2,4). Therefore, the true incidence of IVCF thrombosis may be underestimated because IVCF thrombosis sometimes emerges in relative obscurity and is not consistently detected or reported (6). Of note, the shape of IVCFs has also been considered to be associated with the probability of IVCF thrombosis (14), and prevalence of “umbrella” IVCF-related thrombosis has been reported to be as high as 60% (1,4,13). In the present study, the overall incidence of IVCF thrombosis in the umbrella IVCFs was 32.58%, which is significantly lower than that reported in the prior literature (13), which may be partly attributable to an improvement of rationally designed IVCFs (14). Despite the shortcomings of using this nonspecialized, multicenter, randomized trial for IVCF thrombosis, one clinical advantage was the ability to analyze a relatively large sample of patients who received IVCFs and the consideration of a large number of variables as potential risk factors for the development of IVCF thrombosis.

A classical hypothesis for the pathogenesis of thrombosis (15), also known as Virchow’s triad, proposes that thrombosis occurs due to hypercoagulability of the blood, alterations in hemodynamics, and endothelial/vessel wall injury. IVCF thrombosis is considered a subset of thrombosis and likely has a similar pathogenesis, and the concept of Virchow’s triad can be applied to these patients. However, the underlying pathogenic mechanisms of IVCF thrombosis have not been well elucidated. The risk factors for IVCF thrombosis tend to be multifaceted according to the Virchow’s triad. Within this theory, 3 phenomena are assumed to be associated with the IVCF thrombosis process. First, thrombosis may arise unnoticed or with severe IVC vessel/endothelial wall injury in the course of IVCF insertion, secondary inflammatory reaction, leukocyte and platelet aggregation, etc., which may subsequently trigger insertion situ IVC thrombosis. Second, IVCF placement, IVC thrombus in situ, or the trapped clots intercepted by IVCFs may collectively or separately alter IVC hemodynamics. Finally, the manifestation of the hypercoagulable state of the patients’ blood may aggravate thrombosis. However, this hypothesis has not been tested, and should be investigated in future research. Moreover, digital subtraction IVC venography remains the gold standard for the diagnosis of IVCF thrombosis. However, it is still difficult to be certain if these manifestations represent insertion situ clots or trapped embolisms produced from LEDVT while filling defects are detected at time of retrieval, and sometimes both entities can overlap. Although intimal hyperplasia can also occur at points of IVCF contact with IVC wall, free-floating filling defects on venography are more likely to be thrombus rather than intimal hyperplasia (2,4). However, the pathologies of clots in these patients have not been confirmed, and further study is required.

Previous research regarding PE demonstrated that the time from symptom onset to admission ≤7 days and proximal LEDVT constitute increased risks for PE (16,17). However, few studies have focused on the relationship between the incidence of IVCF thrombosis and these factors as independent predictors. Clots are likely to dislodge from the primary site and be trapped in IVCFs, increasing the risk of IVCF thrombosis. Therefore, the relationship between IVCF thrombosis and symptom onset time and proximal LEDVT was analyzed in the present study, with the results showing that these factors were associated with a significantly higher risk of IVCF thrombosis (P<0.05); however, these factors did not reach statistical significance after the multivariate analysis, implying that the time from symptom onset to admission ≤7 days and proximal LEDVT may be not independent risk factors for IVCF thrombosis. Interestingly, we found that patients with PE had an approximately 2.59-fold increased risk of IVCF thrombosis compared with patients without PE, which is in line with King et al.’s study (2). Patients demonstrating a propensity to develop a large clot burden in one anatomic region are conceivably at a higher risk for developing clots within IVCFs, which implies that patients with PE are more likely to experience recurrent PE during the subsequent disease courses. Of note, the rheumatic diseases of immune system were associated with an approximately 14.42-fold increased risk of IVCF thrombosis compared, which is consistent with a previous report that considered inheritable diseases as one of the main risk factors for IVC thrombosis (18,19). However, the effects of rheumatic diseases of the immune system have not been extensively examined, and thus a complete screening of patients with IVCF thrombosis may be insightful (20). Moreover, PTA was associated with a 2.50-fold higher risk for IVCF thrombosis. Hence, the decision-making process regarding aggressive treatment should carefully weigh these risks with the potential benefits. In addition to the factors mentioned above, compression of the iliac vein may be another cause of IVCF thrombosis (18). However, this was observed in too few cases to constitute a significant difference in our cohort; nonetheless, these factors may be worth examining in studies with larger samples.

Although it has been shown that male patients have increased risk of IVCF thrombosis (10,18), analysis of the correlation between IVCF thrombosis and gender and marital status in patients with LEDVT showed that female and unmarried patients were associated with slightly higher risks of IVCF thrombosis, but this was not a statistically significant association. Although the many other factors believed to be predictive of VTEs did not have sufficiently numerous cases to warrant statistical comparisons or do not demonstrate overwhelming rates, the frequency of these factors is worth noting (2,4,10). In a retrospective review of 164 patients with retrievable IVCF, the risk factors for thrombosis were filter tilt ≥15°, hook wall apposition, IVC dilation rate ≥50%, and dwell time >2 weeks (2). However, in the present study, 3 cases with filter tilt ≥15° were observed, and the mean filter oblique angle was not statistically significant. The cause of the lower rate may be directly attributable to properties of the IVCFs themselves (12), which have been proven to have good performances in close to the center condition of IVC (21). Hook wall apposition was not found in the included patients, time to IVCF retrieval was comparable in the 2 groups, and patients with IVCF nonthrombosis had a significantly higher IVC:filter radial ratio than did those with thrombosis. An IVC:filter radial ratio value of 0.587 could predict IVCF thrombosis and was a protective factor. A prior study (4) might have been influenced by a few confounding variables due to various IVCFs having different filter dilations. Hence, the larger radial ratio is, the larger the IVC dilations. Using IVC:filter radial ratio can reduce the influence of different IVCF diameters and be a more objective means of evaluation. The finding that IVC:filter radial ratio >0.587 was a protective factor suggests that we can choose filters of different diameters depending on the diameter of IVC to reduce the possibility of IVCF thrombosis. Of note, the AUC for IVCF thrombosis was relatively low (AUC =0.59). Hence, further targeted studies may be needed to identify the optimal ratio.

There are several limitations in the present study that merit discussion. First, as with all large multicenter databases, the present study is subject to reporting bias, errors, and the inability to obtain certain case specifics or details. In addition, this study was not specifically designed to investigate the risk factors for IVCF thrombosis, and it did not give a strict definition of IVCF thrombosis nor did it report on patient symptoms. Hence, it has inherent limitations of reporting bias. Second, the timings of IVCF retrieval were limited to be within 90 days, the groups of venography intervals were empirical, which might have affected the findings. Third, the sample sizes included in this study were relatively small for assessing the risk factors. Fourth, the compression of iliac vein may increase the risk of IVCF thrombosis (18); however, the extent of the compression of iliac vein could not be determined due to CTV of the IVC not being conducted in all included patients. Fifth, the indicator of IVC:filter radial ratio was mainly relevant to clinical experience, and IVC measurement may be affected by other variables, but not hydration status or ventilatory moment. Finally, the population examined in this study was predominantly Asian, and our findings may not have external validity in other ethnicities; moreover, many risk factors described in literature related to IVCF thrombosis had very low event rates and thus could not be statistically compared, which might have influenced the results. In addition, a predictive model was not established in the present study. In the future, a study including more factors and excluding confounding factors to overcome these limitations can be designed, and a predictive model can be established.

Conclusions

The present study shows that with increasing dwell time within 90 days, there is a decreasing trend in the incidence of preretrieval venography. Concurrent PE, rheumatic diseases of the immune system, and PTA were found to be risk factors for the occurrence of IVCF thrombosis events, which suggests that intense monitoring of patients with these signs is essential because of the relatively high incidence of IVCF thrombosis in this population. An IVC:filter radial ratio >0.587 was found to be a protective factor against IVCF thrombosis emergence. The conclusions drawn here should be validated in a future study with a close follow-up.

Acknowledgments

We would like to thank all the investigators from 10 centers in mainland China who prepared and executed the trial: Wanyin Shi, Liang Chen, Wensheng Lou, Guoping Chen, Jinhua Song, Haobo Su, Yumei Xiang, Yan Li, Cheng Qian (Nanjing First Hospital, Nanjing Medical University), Jianlong Liu, Xuan Tian, Wei Jia, Peng Jiang, Zhiyuan Chen, Yunxin Zhang, Chenyang Tian, Jinyong Li, Ying Zhang (Beijing Jishuitan Hospital), Gaojun Teng, Gang Deng, Yonglin Qin, Zhibin Bai, Guofeng Zhao, Qi Zhang, Youhua Xue, Lan Gao, Yahong Huang, Zhiping Shen, Sen Lin, Shuguang Zhao, Yue Yang, Yunfang Wang (Zhongda Hospital, Southeast University), Caifang Ni, Yonghai Jin, Pengfei Duan, Baorui Fan, Chao Yang, Lingfang Sun, Qian Ye (The First Affiliated Hospital of Soochow University), Hao Xu, Qingqiao Zhang, Hongtao Liu, Ning Wei, Zhikang Gao, Wenliang Wang, Bin Shen, Duntao Lv, Jing Yang, Yanan Liu, Buqiang Zhuang, Yan Li, Yanfeng Cui, Jinchang Xiao, Xun Wang (The Affiliated Hospital of Xuzhou Medical University), Zhen Li, Hui Cao, Zhouyang Jiao, Shirui Liu, Peng Xu, Zhaohui Hua, Mingxing Li, Zhiwei Wang (The First Affiliated Hospital of Zhengzhou University), Shuiting Zhai, Kun Li, Mingzhe Cui, Kai Liang, Xiaoming Fu, Weixiao Li, Rutao Xu, Dongbin Zhang (Henan Provincial People’s Hospital), Yanrong Zhang, Xiangdong Liu, Haitao Li, Yunsong Li, Liang Li, Jianing Zhao, Xianchao Zhang, Yujie Zhang, Liyuan Liu (The Third Hospital of Hebei Medical University), Hua Xiang, Lin Sun, Ding Li, Peng Yan, Qing Wang, Zhiyong Fang, Xin Xie, Yan Xiao, Shang Ouyang (Hunan Provincial People’s Hospital), Weizhu Yang, Hang Xie, Leye Yan, Zhen Chi, Kun Ke, Junqing Lin, Ning Huang, Na Jiang, Hui Zheng, and Xin Lin (Fujian Medical University Union Hospital).

Funding: This work was supported by the National Natural Science Foundation of China (No. 81871463), the Jiangsu Medical Association Interventional Medicine Special Funding Project (No. SYH-3201140-0026), and the Jiangsu Medical Association Special Fund Project [No. SYH-3201140-0088 (2023035)].

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-23-724/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-23-724/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are 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. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the institutional review board of the Nanjing First Hospital (No. QX20170714-02), and the requirement for written informed consent was waived due to the retrospective nature of the study.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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