Primary conservative treatment for peritonitis-absent symptomatic isolated dissection of the superior mesenteric artery with severely compressed true lumen

Abstract

Objectives

The purpose of this study was to evaluate the safety and efficacy of primary conservative treatment (PCT) for peritonitis-absent symptomatic spontaneous isolated dissection of the superior mesenteric artery (S-SIDSMA) with severely compressed true lumen.

Methods

From January 2013 to December 2018, PCT was used in 26 cases of peritonitis-absent S-SIDSMA with severely compressed true lumen in our center based on our previous proposed treatment algorithm for S-SIDSMA. The demographics, duration from the onset to the admission, duration from the start of the conservative treatment to the alleviation of the symptoms, and in-hospital and follow-up clinical and angiographic outcomes were prospectively recorded and then analyzed.

Results

Among the 26 included patients, 84.6% were male. The mean age of the patients was 54.7 years. The mean duration from the onset to the admission was 3.1 days (range, 1–14 days). Symptoms in 22 patients were markedly or completely relieved during the first five-day medical treatment. Endovascular stent placement was attempted in the remaining four patients, which was successfully performed in three (75%) of them. The technical failure occurred in a patient whose compressed true lumen failed to be cannulated. Medical treatment was then continued in this patient, and his symptoms were relieved after a two-day medical treatment. During the mean follow-up period of 14.3 months, endovascular stent placement was performed in three patients due to the recurrence of the abdominal pain and the chronic intestinal ischemia. No patient showed dissection progression during the follow-up. The complete remodeling rate of the stent group was significantly higher than that of the medical group (83.3% vs. 25%, P = 0.021).

Conclusions

Keywords

Symptomatic isolated dissection superior mesenteric artery primary conservative treatment endovascular conversion vascular remodeling

Introduction

Spontaneous isolated dissection of the superior mesenteric artery (SIDSMA) is a rare entity with unclear clinical and angiographic courses. Patients with SIDSMA could be generally divided into three groups according to the presence and severity of the onset symptoms: group I, asymptomatic SIDSMA (A-SIDSMA); group II, symptomatic SIDSMA (S-SIDSMA) with peritonitis; and group III, peritonitis-absent S-SIDSMA with (IIIa) or without (IIIb) true lumen severely compressed (>70%). Although there is still no consensus on the optimal treatment for SIDSMA, with the increasing number of case reports showing that conservative treatment for this uncommon lesion is associated with a good prognosis, both clinically and morphologically, a number of treatment algorithms have been proposed in recent years, mostly based on the retrospective single-center experience.^1–7

With respect to the timing of the invasive interventions, for patients in groups I, II, and IIIb, a consensus has been reached among the majority of previous reported treatment strategies and algorithms, which recommended invasive procedures as a remedy of the failure of primary conservative treatment (PCT) with or without the antithrombotic therapy in groups I and IIIb^8–13 and invasive treatment should be emergently performed in group II, including laparoscopic exploration, endovascular stent placement, and surgical repair with or without bowel resection.^12,14–17 However, for patients in group IIIa, distinct controversies still exist about whether the invasive revascularization procedure should be emergently performed in these lesions. Some algorithms suggested endovascular repair as the first-line therapy in this group in order to avoid possible progression of symptoms into peritonitis during the medical treatment,^15,16,18 whereas a few others proposed that primary invasive procedures are not mandatory and conservative treatment should be initially chosen regardless of the unfavorable morphologic findings.^12,19–22 This discrepancy can be partly attributed to our limited understanding of the clinical and angiographic course of this subgroup of patients after initial medical treatment. Therefore, a dedicated study on this issue is urgently needed to provide more evidence for clinical practice. However, this type of study remains scarce.

We previously reported our management experience in a cohort of patients with S-SIDSMA and proposed a symptom-based treatment algorithm. According to this algorithm, PCT was prospectively used in peritonitis-absent S-SIDSMA patients even with true lumen severe compression since 2013.¹² In this article, we reported the clinical and angiographic outcomes of patients in this subgroup. The aim of this study was to evaluate the safety and efficacy of PCT in peritonitis-absent S-SIDSMA with true lumen severe compression.

Methods

Definition

As described by Kim et al.,²⁰ the diameter of the normal SMA was defined as the diameter of the main trunk of the SMA proximal to the dissection on initial computed tomography angiography (CTA). The percent compression of the true lumen was assessed based on the diameter of the region of the SMA with maximal stenosis occurring between the origin of the ileocolic artery and the diameter of the normal SMA. If the percent compression of the true lumen was more than 70%, the true lumen was regarded as being severely compressed in this study. Complete remodeling was defined as no false lumen and residual stenosis on CTA. Incomplete remodeling was defined as improved SIDSMA lesion with residual stenosis or thrombus in the false lumen. Incomplete remodeling at one-year follow-up was regarded as poor remodeling.

Study population

Between January 2013 and December 2018, 76 patients were diagnosed with S-SIDSMA in our center. Among them, 29 lesions with a severely compressed true lumen of the SMA were found. After exclusion of three cases that included peritonitis with the primary invasive treatment, 26 consecutive patients with peritonitis-absent S-SIDSMA with severely compressed true lumen were included in this study. The diagnosis was made according to CTA findings. The patients’ demographics, duration from the onset to the admission, treatment modalities, duration from the start of the conservative treatment to the alleviation of the symptoms, and in-hospital and follow-up clinical and angiographic outcomes were prospectively recorded. This study was approved by the Committee for the Protection of Human Subjects at Zhongshan Hospital, Fudan University. All patients participating in the study signed an informed consent document.

Treatment algorithm

All these patients went to general surgeons at the onset, and CTA was performed in them after admission. The general surgeons had excluded that the patients’ symptoms were induced by other disease before they referred these patients to vascular surgeons on the basis of CTA findings of SIDSMA. Once the diagnosis of S-SIDSMA was established by vascular surgeons, the primary in-hospital treatment algorithm (Figure 1) was strictly implemented in each of 76 patients. The algorithm remained unchanged from our previous reports.¹² Briefly, the presence of peritonitis is the only determinant of performing emergent invasive treatment. PCT was performed in patients without peritonitis regardless of initial angiographic findings. Conservative treatment was composed of (1) antiplatelet (daily oral administration of 75-mg clopidogrel) during the hospitalization and for six months after charge, (2) anticoagulation (subcutaneous injection of low-molecular-weight heparin) every 12 h throughout the hospitalization, (3) daily intravenous administration of 20-ug prostaglandin E1 during the hospitalization, (4) bowel rest till abdominal pain was alleviated, and (5) antihypertension in cases with hypertension, including β-blockers, angiotensin-converting enzyme inhibitors, angiotensin receptor blockers, or calcium antagonists administrated either alone or in combination to maintain the systolic blood pressure below 140 mm Hg.

After discharge, if the PCT patients presented with recurrence of symptoms or clinical manifestations indicating chronic intestinal ischemia such as postprandial abdominal pain and weight loss, they would be recommended for readmission and treated following the algorithm from the red arrow in Figure 1.

Morphologic evaluation of the lesions

The morphologic characteristics of the S-SIDSMA lesions were documented according to the angiographic findings on CTA at every observation point. The morphologic evaluation was performed in the following steps. First, the diameter of the normal SMA was measured on initial CTA. Second, lesions were divided into three types on initial CTA according to the presence of the re-entry and the condition of distal flow: type I, with both entry and re-entry; type II, without re-entry and with compromised distal flow; type III, without re-entry but with adequate distal flow (Figure 2). Third, the degree of thrombosis formation in the false lumen, percent compression of the true lumen, the maximum diameter of the SMA, and the maximum diameter of the false lumen were measured on initial and follow-up CTA.

Follow-up protocol

The patients were followed up by CTA at 3, 6, and 12 months and yearly thereafter. The recurrence of symptoms, presentations indicating chronic intestinal ischemia, morphologic characteristics, and patency of the stents were recorded.

Statistical analysis

The continuous variables were expressed as median and range values and compared using t tests. Categorical variables were presented as numbers and percentages and compared between groups using cross-table methods with the Fisher’s exact test. Statistical significance was defined as a P value of < 0.05. Statistical analysis was performed with SPSS 23 software (IBM Corp., Armonk, NY).

Results

Demographic and clinical characteristics

This study included 22 men and 4 women, with a mean age of 54.7 years (range, 46–68 years). The comorbidities and clinical manifestations of the 26 patients are shown in Table 1. Hypertension was the most common comorbidity. All patients presented with varying degrees of abdominal pain and were free from peritoneal signs. The mean duration from the onset to the admission was 3.1 days (range, 1–14 days). The initial CTA showed the primary entry site in the SMA and severely compressed true lumen of the dissection in all patients.

Table 1.

Demographic and clinical characteristics.

Characteristic	N (%)
Age, median year (range)	54.7 (46–68)
Men gender	22 (85)
Comorbidities
Hypertension	15 (57)
Diabetes	8 (31)
Dyslipidemia	6 (23)
Smoking	12 (46)
Decreased renal function	6 (23)
Cardiac disease	3 (12)
Chronic Obstructive Pulmonary Disease	1 (4)
Clinical manifestations
Abdominal pain	26 (100)
Vomiting	4 (15)
Diarrhea	2 (8)

Clinical course

Following the treatment algorithm in our center, we initially gave medical treatment to all patients after admission. The symptoms in 22 patients were markedly or completely alleviated during the first five days after the medical treatment. The mean duration from the start of medical treatment to the alleviation of symptoms was 2.4 days (range, 1–5 days) in these 22 patients. The abdominal pain in the remaining four patients did not subside, even though signs of peritonitis were not found among them. Thus, endovascular stent placement was attempted in these four patients, which was successfully performed in three (75%) of them. Alleviation of symptoms was immediately achieved in two patients after the stent placement. Aggravation of abdominal pain was found in the remaining one patient postoperatively; however, his symptoms subsided after an additional three-day medical treatment. The technical failure occurred in a patient whose compressed true lumen could not be cannulated. Medical treatment was then continued in this patient, and his symptoms were relieved after a two-day medical treatment.

The mean follow-up time was 14.3 months (range, 3–48 months). No death, intestinal infarction, or rupture of the dissection developed during the follow-up period. During follow-up, one patient presented with recurrence of abdominal pain at one month. Postprandial pain, irritable bowel syndrome, and weight loss more than 5 kg developed in two patients at one and three months, respectively. These three patients were among the 22 patients whose symptoms subsided within five days after the primary medical treatment. Endovascular stent placement was successfully performed in these three patients, and their symptoms were significantly relieved after the intervention.

Thus, 29.6% (7/26) of cases were converted to endovascular procedures in the current study, and a total of six patients had stent placement into the SMA during the primary in-hospital and the follow-up course (Supplemental Table I). Therefore, the study patients were divided into two groups retrospectively: stent group (n = 6), patients who had stent placement into the SMA; medical group (n = 20), patients without stent placement including one patient in whom the endovascular procedure was attempted but failed. The mean follow-up period of SMA stenting was 14.5 months (range, 3–48 months). During the follow-up, CTA demonstrated that the stents were patent without migration, fracture, or restenosis.

Morphologic changes

The mean diameter of the SMA in 26 patients was 7.4 mm (range, 5.0–9.4 mm). The mean percent compression of the true lumen was 84.4% (range, 70.1%–100%), and occlusion of the true lumen was found in eight (30.8%) patients on initial CTA. Eighteen (69.2%) lesions presented with aneurysmal changes at diagnosis. The morphologic details of the study patients are shown in Table 2. On initial CTA, no significant difference was found between the stent group and medical group in morphologic parameters including diameter of the normal SMA, percent compression of the true lumen, and maximum diameter of the SMA and the false lumen. After a mean follow-up period of 14.5 months, the last follow-up CTA results of the percent compression of the true lumen, maximum diameter of the SMA, and maximum diameter of the false lumen all significantly improved compared with the values on initial CTA. The mean improvement of percent compression of the true lumen in the stent group was three times more than that in the medical group (77.9% vs. 24.7%, P < 0.01). A significant difference was also found in decrease of the maximum diameter of the false lumen between the two groups. Although the mean decrease of the maximum dimeter of the SMA in the stent group was more than that in the medical group (3.5 mm vs. 2.3 mm), the difference was not significant.

Table 2.

Morphologic characteristics.

Initial CTA							CTA at last follow-up
No.	Type	Diameter of normal SMA, mm	FL thrombosis	Percent compression of TL	Maximum diameter of SMA, mm	Maximum diameter of FL, mm	Last follow-up months	Remodeling	Percent compression of TL	Maximum diameter of SMA, mm	Maximum diameter of FL, mm	Improvement of percent compression of TL
SG
1	III	8.6	P	76.7%	9.8	7.4	24.0	C	0	8.6	0	76.7%
2	III	9.0	P	82.2%	9.6	8.0	19.0	C	0	9.0	0	82.2%
3	III	6.2	P	83.9%	10.0	8.0	10.0	I	0	10.0	3.8	83.9%
4	III	6.7	P	70.1%	14.0	11.0	37.0	C	0	6.7	0	70.1%
5	III	7.0	P	82.9%	12.2	10.0	48.0	C	0	7.0	0	82.9%
6	III	8.7	P	71.3%	15.0	12.0	6.0	C	0	8.7	0	71.3%
Mean		7.7		77.9%	11.8	9.4	24.0		0	8.3	0.6	77.9%
MG
1	I	6.9	P	71.0%	15.0	11.0	9.0	I	71.0%	13.4	10.0	0
2	I	9.4	P	100.0%	14.6	10.0	24.0	I	100.0%	13.9	10.0	0
3	I	6.2	P	75.8%	10.2	7.2	14.0	I	59.7%	9.8	5.4	16.1%
4	I	7.3	P	100.0%	11.7	8.1	6.0	I	100.0%	10.9	6.3	0
5	I	8.1	P	100.0%	10.0	6.5	24.0	I	75.3%	9.6	6.0	24.7%
6	II	7.5	P	100.0%	13.7	11.6	36.0	I	48.0%	10.1	4.7	52.0%
7	II	8.0	P	100.0%	12.5	10.3	3.0	I	100.0%	12.3	9.0	0
8	II	6.7	P	100.0%	8.8	8.8	12.0	I	23.9%	8.3	3.2	76.1%
9	III	7.3	P	71.2%	12.4	10.3	12.0	C	0	7.3	0	71.2%
10	III	5.6	P	82.1%	10.4	8.2	12.0	C	0	5.6	0	82.1%
11	III	6.5	C	100.0%	16.0	16.0	24.0	C	0	6.5	0	100%
12	III	7.0	P	78.6%	9.8	7.0	48.0	C	0	7.0	0	78.6%
13	III	6.5	P	81.5%	13.2	8.2	18.0	C	0	6.5	0	81.5%
14	III	8.9	P	83.1%	16.5	15.0	6.0	I	56.2%	13.0	7.4	26.9%
15	III	6.5	P	92.3%	14.0	13.0	6.0	I	30.8%	9.7	5.2	61.5%
16	III	7.5	P	72.0%	13.8	9.5	8.0	I	56.0%	13.4	9.0	16.0%
17	III	5.0	P	100.0%	10.0	10.0	3.0	I	80.0%	10.0	9.0	20.0%
18	III	8.9	P	71.9%	11.0	8.0	6.0	I	57.3%	11.0	7.0	14.6%
19	III	7.6	P	71.1%	9.0	6.8	9.0	I	34.2%	7.6	1.0	36.9%
20	III	9.1	P	81.3%	12.5	9.3	48.0	I	46.2%	13.0	7.4	35.1%
Mean		7.3		86.3%	12.2	9.7	16.8		61.6%	10.0	5.0	24.7%

P: partial; C: complete; I: incomplete; CTA: computed tomography angiography; SMA: superior mesenteric artery; FL: false lumen; TL: true lumen; SG: stent group; MG: medical group.

The lesions in the stent group were all classified as type III. Complete remodeling of the SMA was found in five patients (83.3%) on CTA at three months after the stent placement. Incomplete thrombosis in the false lumen still presented in patient 3 at four months despite that the true lumen of the dissection had a significant improvement immediately after the stent placement. In the medical group, the SIDSMA lesions were categorized into the following groups based on their morphologic findings on initial CTA: 25% type I, 15% type II, and 60% type III. After a mean follow-up time of 14.2 months in this subgroup, complete remodeling was achieved in five patients (25%) of type III. In two of five patients, complete remodeling was found on CTA at six months, whereas it was found in the other three at one year. The complete remodeling rates in the stent group were significantly higher than that in the medical group (83.3% vs. 25%, P = 0.021). Considering that the type of lesions in the stent group were all categorized into type III, the complete remodeling rates in the stent group and that of the type III patients in the medical group (83.3% vs 41.7%) were then compared, and no significant difference was found between the two groups (P = 0.153). Five lesions (25%) had poor remodeling in the medical group (type I, 2; type II, 2; type III, 1).

Discussion

No prospectively randomized controlled trials on the SIDSMA have been reported thus far. The majority of the studies were limited to retrospective case series. Although some treatment algorithms have been proposed based on these cohort studies, the efficacy and safety of them were seldom tested. To the best of our knowledge, only Ahn et al.²³ reported the results of 13 patients prospectively treated according to their published treatment guidelines.¹⁷ Eleven of them had acute onset abdominal pain, and other 2 patients were asymptomatic. PCT was performed in all 14 patients, and only one of them underwent coil embolization due to a slight aneurysmal dilatation with persistent abdominal pain during the follow-up. We reported a treatment algorithm of S-SIDSMA in 2013, on which the management of subsequent S-SIDSMA cases in our center was strictly based. The clinical and radiological data in the current study were prospectively collected, which could provide evidence with a higher level than previous retrospective studies for resolution of this controversial issue. In addition, by means of analyzing the outcomes of this group of patients, the validity of our algorithm could also be effectively tested. Generally speaking, both the clinical and morphological outcomes of the cases of peritonitis-absent S-SIDSMA with true lumen severe compression after PCT are satisfactory.

In the current study, conservative treatment was initially used in all patients with a 76.9% success rate and a 26.9% rate of conversion to endovascular treatment. A recent systematic review and meta-analysis conducted by Zhu et al.²⁴ analyzed the published treatment experience with S-SIDSMA, in which 514 cases were enrolled. Using pooled analyses for calculation, the investigators reported an 85.2% rate of initial conservative treatment, an 84.7% PCT success rate, and a 14.3% rate of invasive treatment conversion. The rate of conversion in our study was almost twice more than the reported one. Except for the discrepancy of case inclusion in different studies, such a higher proportion might also be associated with the following two factors. First, the observation periods before the invasive intervention mostly ranged from 5 to 10 days in previous reports.^7,20,25 The observation duration in the current study was five days, which was relatively shorter than that in other centers. Because of the failed endovascular intervention, the duration from the start of the medical treatment to the alleviation of symptoms in one patient was up to eight days. Similarly, in our previous study,¹² five cases were reported to have failed endovascular intervention after the first five-day medical treatment. Medical treatment was then reinstituted with success within the following one week in all five patients, which might suggest that our results of conservative treatment would have been more satisfactory had it been prolonged, as Ahn et al.²³ and Luan et al.²⁶ mentioned in their studies. Still, further evidence, especially results of the randomized controlled trial, is needed to evaluate the optimal duration of the conservative treatment. Second, in the current study, chronic intestinal ischemia was found as the main cause of conversion to invasive treatment during the follow-up period. Endovascular stenting, rather than observation with medical treatment, was recommended as the first-choice treatment for patients with chronic intestinal ischemia in our center. However, in previous studies, chronic intestinal ischemia was seldom reported as the indication for the endovascular conversion.²⁴ Thus, the discrepancy in this aspect might also contribute to the significantly higher invasive treatment conversion in the current study.

No intestinal necrosis occurred after conservative treatment in the current series. No progression of abdominal signs into peritoneal irritation was found in patients at the time of conversion to endovascular treatment. Meanwhile, no surgical conversion was needed in all patients. These results suggest that PCT could effectively improve symptoms without increasing the risk of bowel necrosis or surgical conversion, even in S-SIDSMA with unfavorable morphologic characteristics. Of course, realization of this required a scientific treatment algorithm that contains a proper duration of observation periods. Although several patients presented with symptoms of chronic intestinal ischemia during the short-term follow-up, the ischemic state could be promptly reversed by endovascular stenting, which was acceptable considering that these patients represented a rather small proportion.

Nearly 70% of cases met the general diagnostic criteria (a 50% increase in diameter compared with an adjacent normal segment) of the dissection aneurysm of SMA. Invasive procedures were recommended for aneurysms with a larger diameter in some previously proposed management algorithms of SIDSMA.^3,16,21,25 However, there are also opinions that the intervention should be considered for the persistent progression of an aneurysm rather than the presence of a larger aneurysm on initial CTA.^1,10,27,28 Park et al.²⁹ reported mild dilatation of SMA in 10 of 46 SIDSMA cases after conservative treatment. Considering the lesions were not aneurysmal, invasive interventions were not performed. Progression of the aneurysmal change was extremely rare in the current series. Dilatation of the lesions decreased significantly or remained stable at every follow-up point in most cases, apart from patient 20, who had a slight increase in the maximum diameter of the SMA, which was almost negligible considering the measurement errors. Based on our experience, the prognosis of the aneurysm in S-SIDSMA might be distinct from that in thoracic aorta dissection, which is the most common vascular dissection in humans, and conservative treatment could be justified in these lesions. The threshold diameter of the aneurysm for invasive interventions is pending further evidence.

Since satisfactory outcomes have been obtained following the treatment algorithm that was completely based on clinical symptoms, morphologic classifications of the S-SIDSMA in our center were proposed to predict the vascular remodeling after conservative treatment rather than guiding the treatment. Therefore, unlike some complex and sophisticated classifications in previous studies,²¹ a more concise classification with three types based on the presence of the re-entry and the distal perfusion was designed, facilitating a quick type definition and remodeling prediction. Our results showed that type III lesions were the most common and tended to achieve complete remodeling within one year after conservative treatment, which is the main reason why we defined incomplete remodeling after one-year follow-up as poor remodeling. Although complete remodeling has not been discovered in type II lesions and nearly all type II lesions had poor remodeling at the last follow-up, the angiographic characteristics gradually improved, and we consider that complete remodeling could occur in type II lesions with a longer follow-up period. Despite that previous studies reported that complete remodeling could be achieved in type I lesions after conservative treatment,^2,29 a very limited improvement in angiographic characteristics was found in type I lesions and no complete remodeling. As there was an opinion that false lumen thrombosis is an important step in the remodeling of the SIDSMA,²³ and considering the presence of the re-entry causing persistent flow in the false lumen that impeded false lumen thrombosis, we believe the complete remodeling in type I lesions was rather difficult to achieve. Unsuccessful false lumen thrombosis was also regarded as the main reason for poor remodeling of the lesion in patient 20 in the medical group (Figure 3). Compared with easier and earlier false lumen thrombosis in other type I lesions, false lumen thrombosis in this patient was still not achieved at 48 months, with the persistent collateral circulation perfusing into the false lumen. Generally, based on our experience, we concluded that in type I lesions, it is difficult to achieve complete remodeling after conservative treatment, and type II lesions might require longer than one year to achieve complete remodeling, whereas type III lesions tend to achieve complete remodeling within one year.

As to the vascular remodeling after endovascular interventions, its greatest advantage is that the true lumen flow could be restored and the false lumen could be compressed after the stent placement. In the current study, all lesions could achieve quick complete remodeling immediately after endovascular stenting, with the exception of patient 3 in the stent group (Figure 4), showing an acceptable result for bare stent use. However, because of the undefined long-term results of endovascular treatment for SIDSMA, this subgroup of patients, especially patient 3 who had false lumen dilatation, were still monitored with regular follow-up. Therefore, we do not recommend that the stent placement in SIDSMA aims for rapid morphologic improvement if the patient symptoms still allow continued conservative treatment.

Our study has several limitations. First, the study had a small sample size. Second, the follow-up period was relatively short. Third, there was selection bias in this study. Even though the results of PCT for peritonitis-absent S-SIDSMA with true lumen severe compression are encouraging, multicenter prospective validation of their algorithms is required to further address this problem.

Conclusion

Based on our previous proposed treatment algorithm for S-SIDSMA, PCT could achieve satisfactory results both clinically and morphologically in peritonitis-absent S-SIDSMA with severely compressed true lumen. Even in cases of aggravation or no relief of symptoms after PCT, there is still a great opportunity for an endovascular conversion to prevent intestinal necrosis. Severity of the symptoms rather than the degree of the true lumen stenosis should be the indications for invasive treatment in S-SIDSMA.

Supplemental Material

VAS892751 Supplemental Material - Supplemental material for Primary conservative treatment for peritonitis-absent symptomatic isolated dissection of the superior mesenteric artery with severely compressed true lumen

Supplemental material, VAS892751 Supplemental Material for Primary conservative treatment for peritonitis-absent symptomatic isolated dissection of the superior mesenteric artery with severely compressed true lumen by Gang Fang, Genying Xu, Yuan Fang, Jue Yang, Tianyue Pan, Xiaolang Jiang, Zhihui Dong and Weiguo Fu in Vascular

Footnotes

Consent for publication

All patients signed a consent form for their data to be used for research or publication.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Ethical approval and consent to participate

This study design was approved by the Ethics Committee of Zhongshan Hospital, Fudan University, Shanghai, China. All included patients were informed about the nature of the study and gave their written informed consent.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was supported by training program for outstanding academic leaders of Shanghai health and family planning system (Hundred Talent Program, Grant No. 2018BR40), China National Natural Science Funds (Grant No. 30801122), and Shanghai Rising-Star Program (Grant No. 19XD1401200).

ORCID iD

Dong Zhihui

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