
==== Front
J Med Ultrasound
J Med Ultrasound
JMU
J Med Ultrasound
Journal of Medical Ultrasound
0929-6441
2212-1552
Wolters Kluwer - Medknow India

JMU-32-221
10.4103/jmu.jmu_82_23
Original Article
Feeding Flow Velocity on Doppler Ultrasound Predicting the Outcome of Type II Endoleak following Endovascular Aneurysm Repair of Abdominal Aortic Aneurysm
Seevaleephan Parames
Treesit Tharintorn
Bua-ngam Chinnarat
Feinggumloon Sasikorn
Sriprachyakul Apichaya
Pichitpichatkul Kaewpitcha
Panpikoon Tanapong *
Department of Radiology, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
Address for correspondence: Dr. Tanapong Panpikoon, Faculty of Medicine, Ramathibodi Hospital, 270, Rama VI Road, Bangkok 10400, Thailand. E-mail: tanapongpanpikoon@gmail.com
Jul-Sep 2024
30 1 2024
32 3 221226
13 7 2023
06 9 2023
Copyright: © 2024 Journal of Medical Ultrasound
2024
https://creativecommons.org/licenses/by-nc-sa/4.0/ This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.
Background:

The objective is to study the relation between the velocity of the arterial feeder and the progression of the postendovascular aneurysm repair aneurysm to find out the cut point velocity, which causes a significant increase in size of the aneurysm sac.

Methods:

Retrospective study of patients with Type II endoleak followed up with the duplex ultrasound between January 2010 and June 2022. The sensitivity, specificity, and accuracy of the velocity, number of feeding artery, and flow pattern were studied. Receiver operating characteristic analysis was performed to evaluate a test performance and the most appropriate cutoff velocity of the arterial feeder.

Results:

The peak systolic velocity (PSV) of >75 cm/s, multiple feeding arteries, and the to-and-fro pattern show a significant distinguish the stable size from the significant increase in the size of the aneurysm with a sensitivity of 100.0%, a specificity of 100.0%, and an accuracy of 100.0% (P = 0.002).

Conclusion:

The patient with a PSV >75 cm/s, multiple feeding arteries, and the to-and-fro pattern are correlated with significant aneurysm expansion and need closer follow-up than the patient with low PSV, single feeding artery, and monophasic pattern.

Abdominal aortic aneurysm
blood flow velocity
Doppler ultrasonography
Doppler ultrasound
endoleak
endovascular aneurysm repair
pulse wave velocity
==== Body
pmcINTRODUCTION

Nowadays, the standard treatment of abdominal aortic aneurysm (AAA) is an endovascular aneurysm repair (EVAR) because it can significantly reduce a 1-year mortality rate than the conventional open repair.[1234]

After the EVAR, an endoleak occurs in 44% of cases. The rates of late complications requiring further interventions are 2.1%–2.8%. The endoleak can cause a recurring AAA, leading to aneurysm rupture. The most common type of endoleak is type II, reporting 6%–30%.[5678] The type II endoleak needs to be detected early, and a proper follow-up with a computed tomographic angiography (CTA) or a duplex ultrasound because it can cause a significant progression of the post-EVAR aneurysm sac, which needs to be treated by embolization.

Every patient needed to follow-up with a CTA or a Doppler ultrasound according to the standard protocol of each institute, recommending study at 1–3 months and 6 months–1 year after EVAR.

The recent data show no significant difference between the duplex ultrasound and the CTA in detecting the endoleak after EVAR. Moreover, the duplex ultrasound is more radiation-safe and gives more information about the velocity of the feeding artery and the flow direction. However, the duplex ultrasound is an operator-dependent study requiring an experienced operator.[9101112]

Many factors from the duplex ultrasound affect the progression of the aneurysm, such as feeding flow velocity, flow direction, and number of feeding arteries.[13]

The high flow velocity of the feeding artery, bidirectional flow (to-and-fro pattern), and multiple feeding arteries are the critical factors causing a significant increase size of the post-EVAR aneurysm sac, which needs further embolization.[1415] However, there is no definite cut point of the high flow velocity of the feeding artery, which may predict the prognosis of Type II endoleak.

This retrospective study reviews the findings from the duplex ultrasound, such as the velocity of the feeding artery, flow direction, and the number of feeding arteries in the follow-up of Type II endoleak after EVAR and focuses on the relationship between the velocity of feeding arteries and the progression of the aneurysm.

We intend to find the most appropriate cut-point velocity of feeding arteries, which can cause a significant increase size of the post-EVAR aneurysm.

MATERIALS AND METHODS

A study included consecutive patients who underwent EVAR and were diagnosed with Type II endoleak from the CTA between January 2010 and June 2022. All data were collected retrospectively from electronic medical records and in-picture archiving and communication systems from February to April 2023. The study conformed to the principles outlined in the Declaration of Helsinki and was approved by the institutional ethics committee (COA. MURA2023/62; Date of approval February 6, 2023), and informed consent was waived because of a retrospective study.

The surveillance ultrasound protocol was applied to every patient with Type II endoleak. Within 1 month after CTA, the duplex ultrasound was done for baseline information, including the size of the aneurysm, location and number of feeder arteries, flow velocity of feeder artery, and flow pattern or character of the spectral waveform. After that, a follow-up ultrasound was done every 6 months to evaluate the progression or resolution of endoleak Type II.

Inclusion criteria

All patients diagnosed with Type II endoleak from CTA

Complete information of the baseline duplex ultrasound within 1 month after CTA

Complete information of the follow-up duplex ultrasound 6 months after the baseline ultrasound.

Exclusion criteria

No official report of the duplex ultrasound

Lack of follow-up.

Five consultant radiologists with a minimum of 5 years of postqualification experience performed the same protocol for the first ultrasound scanning after diagnosis of endoleak type II from the CTA and the follow-up study.

All patients underwent ultrasound examination on a Philip iU22 (Philips Health care, Andover, Mass) with a C5-1 curved linear array transducer and an Aplio™ 500 (Canon Medical Systems Corporation, Japan) with a 3.5 MHz convex transducer PVT-7375BT. The ultrasound protocol begins with a cross-sectional grayscale image for measurement of the maximum anteroposterior (AP) and transverse diameter of the aneurysm.

The endoleak Type II was diagnosed by a retrograde flow in a branch into the aneurysm sac during the color flow image study, confirmed by the arterial spectral waveform. The flow velocity measurement was performed at the entrance of feeding vessels with an angle of <60°. The peak systolic velocity (PSV) was recorded in cm/s. The highest velocity was used in patients with more than one vessel diagnosed as Type II endoleak. The to and flow waveform was noted when the arterial blood went into the aneurysm in a systolic cycle and exited the aneurysm in a diastolic cycle [Figure 1].

Figure 1 The Type II endoleak through right lumbar artery was diagnosed by a retrograde flow (red color) in a right lumbar artery into the aneurysm sac in color flow image (a) and the to and flow waveform on spectral PW Doppler ultrasound (b)

We defined stable size as an increase of AP and transverse diameters <5 mm in 6 months and progression as an increase of AP and transverse diameter of more than 5 mm in 6 months, and the aneurysm needed to be embolized.

This study pays attention to three factors from duplex ultrasound: the PSV of feeding arteries, flow pattern (presence of to-and-fro pattern or not), and the number of feeding arteries (single or multiple feeders) affecting Type II endoleak.

Using Statistical Package for the Social Science for Mac version 25, the PSV of feeding arteries, flow pattern, the number of feeding arteries, the progression of the aneurysm size, and other descriptive information were recorded statistically.

Receiver operating characteristic (ROC) analysis was performed to evaluate a test performance and the most appropriate cut-off velocity of feeding arteries to distinguish low-flow and high-flow feeding arteries, significantly leading to the progression of an aneurysm sac from Type II endoleak.

Chi-square tests were also done to obtain sensitivity, specificity, and accuracy of high-flow feeding arteries, flow pattern, and the number of feeding arteries and combined all three factors in identifying significant Type II endoleak.

RESULTS

From the total of 34 patients, two patients showed a significant increase in the aneurysm size (>5 mm in both AP and transverse diameter) and continued embolization. One patient refers to embolization after the first follow-up ultrasound, and another one undergoes embolization after the 2nd time of follow-up ultrasound due to the persistence of Type II endoleak and the increased size of the aneurysm. Spontaneous complete resolution of Type II endoleak was observed in the rest of the 32 patients at the first follow-up ultrasound.

Feeding arteries’ PSV ranges from 9.6 to 104 cm/s (mean 40.87 ± 23.03). The to-and-fro pattern was found in eight patients. Four patients have more than one feeding artery [Table 1].

Table 1 Characteristics of patients and ultrasound findings

Characteristics	All patients (%)	Stable size of the aneurysm	Increase in size of aneurysm*	
Gender				
 Male	27 (79.41)	26	1	
 Female	7 (20.59)	6	1	
Total	34 (100)	32	2	
Age (years)				
 Mean (±SD)	77.71 (±7.09)	77.91 (±7.24)	74.5 (±3.54)	
 Minimum	58	58	72	
 Maximum	90	90	77	
Concerning factors affecting significant type II endoleak				
Peak systolic velocity of feeding arteries (PSV, cm/s)				
 Mean (±SD)	40.87 (±23.03)	37.81 (±19.66)	89.9 (±19.87)	
 Minimum	9.6	9.6	75.9	
 Maximum	104	81.7	104	
The flow patterns of feeding arteries (number of patients)				
 To-and-fro pattern	8 (23.53)	6	2	
 Monophasic pattern	26 (76.47)	26	0	
Number of feeding arteries (number of patients)				
 Multiple (≥2)	4 (11.76)	2	2	
 Single	30 (88.24)	30	0	
*>5 mm in 6 months and needed to be embolization. SD: Standard deviation, PSV: Peak systolic velocity

In comparison between the stable and aneurysmal progression groups, the PSV of feeding arteries in the aneurysmal progression group (mean PSV = 89.9 cm/s) is higher than the stable group (mean PSV = 37.81 cm/s). Moreover, the to-and-fro pattern and multiple feeding arteries are seen in all patients needing embolization [Table 1].

The ROCs curve was constructed to determine the PSV that maximizes the summation of sensitivity and specificity for the progression of the aneurysm. The ROC area of the PSV of the feeding artery was 0.953 [Figure 2 and Table 2].

Figure 2 ROC curve analysis of the peak systolic velocity. ROC: Receiver operating characteristic

Table 2 Area under the receiver operating characteristic curve of peak systolic velocity

Area	SEa	Asymptotic significantb	Asymptotic 95% CI	
	
Lower bound	Upper bound	
0.953	0.046	0.034	0.863	1.000	
aUnder the nonparametric assumption, bNull hypothesis: True area=0.5. CI: Confidence interval, SE: Standard error

The PSV of more than 75 cm/s can significantly distinguish the stable size of the AAA from the significant increase in the size of the aneurysm with a sensitivity of 100.0%, a specificity of 90.6%, and an accuracy of 91.2% (P = 0.018).

The to-and-fro pattern can significantly distinguish the stable size from the significant increase in the size of the aneurysm with a sensitivity of 100.0%, a specificity of 81.3%, and an accuracy of 82.4% (P = 0.050).

Multiple feeding arteries can also significantly distinguish the stable size of the AAA from the significant increase in the size of the aneurysm with a sensitivity of 100.0%, a specificity of 93.8%, and an accuracy of 94.1% (P = 0.011).

Finally, when combined, all three mentioned factors. The test shows a significant difference in the stable size from the significant increase in the size of the aneurysm with a sensitivity of 100.0%, a specificity of 100.0%, and an accuracy of 100.0% (P = 0.002). The sensitivity and specificity of each factor are shown in Table 3.

Table 3 Sensitivity and specificity

Factors	Significant increased size of aneurysm (S)	Total (a+b)	P	
	
Yes, n (%)	No, n (%)	
	
PSV of feeding arteries	
PSV (A)					
 ≥75 cm/s					
  Number of patients	2	3	5	0.018	
  Percentage in A	40.0	60.0	100.0		
  Percentage in S	100.0	9.4	14.7		
 <75 cm/s					
  Number of patients	0	29	29		
  Percentage in A	0.0	100.0	100.0		
  Percentage in S	0.0	90.6	85.3		
 Total					
  Number of patients	2	32	34		
  Percentage in A	5.9	94.1	100.0		
  Percentage in S	100.0	100.0	100.0		
	
The flow pattern of feeding arteries	
	
To-and-fro (B)					
 Yes					
  Number of patients	2	6	8	0.050	
  Percentage in B	25.0	75.0	100.0		
  Percentage in S	100.0	18.8	23.5		
 No					
  Number of patents	0	26	26		
  Percentage in B	0.0	100.0	100.0		
  Percentage in S	0.0	81.3	76.5		
Total					
 Number of patients	2	32	34		
 Percentage in B	5.9	94.1	100.0		
 Percentage in S	100.0	100.0	100.0		
	
The number of feeding arteries	
	
Number (C)					
 Multiple					
  Number of patients	2	2	4	0.011	
  Percentage in C	50.0	50.0	100.0		
  Percentage in S	100.0	6.3	11.8		
 Single					
 Number of patients	0	30	30		
 Percentage in C	0.0	100.0	100.0		
 Percentage in S	0.0	93.8	88.2		
Total					
 Number of patients	2	32	34		
 Percentage in C	5.9	94.1	100.0		
 Percentage in S	100.0	100.0	100.0		
	
Combined three factors	
	
3 factors (D)					
 Yes					
  Number of patients	2	0	2	0.002	
  Percentage in D	100.0	0.0	100.0		
  Percentage in S	100.0	0.0	5.9		
 No					
 Number of patients	0	32	32		
 Percentage in D	0.0	100.0	100.0		
 Percentage in S	0.0	100.0	94.1		
Total					
 Number of patients	2	32	34		
 Percentage in D	5.9	94.1	100.0		
 Percentage in S	100.0	100.0	100.0		
*Chi-square tests (Fisher’s exact test), **3 factors=high PSV (≥75 cm/s), to-and-fro flow pattern and multiple numbers of feeding arteries. PSV: Peak systolic velocity

DISCUSSION

Currently, the optimal management of Type II endoleak remains controversial, with no definite consensus. Due to the low risk of aneurysm rupture, approximately 1% of ruptured aneurysm associated with Type II endoleak was reported.[16] And the type II endoleak, detected 1 year after EVAR, can be resolved spontaneously in 75% of cases.[17] Therefore, many clinicians support the conservative observation of the Type II endoleak with surveillance follow-up ultrasound. However, the treatment was a concern when the post-EVAR aneurysm showed a significant increase in size. The most recent guideline from the Society of Vascular Surgery[18] recommends the treatment when the aneurysm expansion is more than 5 mm. Other criteria include endoleak persistence longer than 6 months.

It is a reason for this study aims to determine the parameter for predicting the progression of aneurysm size not only for selecting patients for the treatment but also for the appropriate interval of the follow-up duplex ultrasound. The patient with a risk for an aneurysm progression and endoleak persistence should be examined more frequently than the patient without.

From this study, the PSV >75 cm/s and the multiple numbers of feeding arteries can distinguish the stable size of the AAA from the significant increase in the size of the aneurysm with statistically significant (P < 0.05). Our result supports the previous publication from Maximus et al.[14] about the velocity of Type II endoleak might be able to predict spontaneous resolution of Type II endoleak or progression of aneurysm size and report that every patient with growing aneurysm size had a PSV >100 cm/s. Correspond with the publication from Arko et al.,[15] which analyzed the velocity and resolution of Type II endoleak. They found that patient with spontaneous resolution of Type II endoleak has an average velocity of 75.5 cm/s.

It can be concluded that the velocity of Type II endoleak affects the aneurysm size. The aneurysm expansion will depend on the retrograde blood volume into the aneurysm. A large amount of blood volume will affect the aneurysm expansion more than a small blood volume because the blood volume is the summation of the blood flow velocity and cross-sectional area of the feeding artery. The high PSV and multiple feeder arteries significantly correlate with aneurysm expansion.

Furthermore, the to-and-fro pattern, which causes blood flow inward to the aneurysm in the systolic phase and outward in the diastolic phase, also correlates with a significant increase in the size of the aneurysm with statistically significant (P < 0.05). To explain this finding, the to-and-fro pattern represents a pseudoaneurysm-like phenomenon. The blood flow moves into and out of the un-clotted, sac-like area in the partially thrombosed aneurysm through the same channel. Together with the high velocity, these are the resist factors for the spontaneous closure of the feeding artery. Interestingly, our study shows that the to-and-fro pattern is always founded with a high PSV. Moreover, two patients with aneurysm expansion show higher blood flow velocity during the diastolic phase than the mean of PSV in the patient with the monophasic pattern. All patients with PSV lower than 75 cm/s, single artery feeder, and monophasic pattern show spontaneous regression or absence of Type II endoleak at the 6 months’ follow-up ultrasound.

Even if we found the three parameters from the duplex ultrasound included the PSV >75 cm/s, multiple numbers of feeding arteries, and to-and-fro pattern correlate with a significant increase in aneurysm size. However, the indication for the treatment of Type II endoleak also depends on many factors. The essential benefit of our results is knowing about the natural history of Type II endoleak detected on the follow-up duplex ultrasound and setting up the appropriate follow-up ultrasound protocol.

The patient with PSV >75 cm/s, multiple feeding arteries, and to-and-fro pattern need closer follow-up than those with low PSV, single arterial feeder, and monophasic pattern.

There are some limitations due to the small population, low prevalence of aneurysm expansion in the single-center study and the size measurement by the ultrasound alone. However, we achieve our objective, which might affect the current treatment but has validity for the follow-up study.

CONCLUSION

Patients with PSV >75 cm/s, multiple feeding arteries, and to-and-fro pattern correlate with significant aneurysm expansion and need closer follow-up than those with low PSV, single arterial feeder, and monophasic pattern.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Acknowledgment

We would like to thank the following doctors for taking part in treating patients with abdominal aortic aneurysms: Dr. Piyanut Pootrakool, Dr. Gorawee Tepsamrithporn, Dr. Chaowanan Pornwaragorn and Dr. Nutsiri Kitritirapong from the Department of Surgery, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Thailand.
==== Refs
REFERENCES

1 Powell JT Sweeting MJ Ulug P Blankensteijn JD Lederle FA Becquemin JP Meta-analysis of individual-patient data from EVAR-1, DREAM, OVER and ACE trials comparing outcomes of endovascular or open repair for abdominal aortic aneurysm over 5 years Br J Surg 2017 104 166 78 28160528
2 Greenhalgh RM Brown LC Kwong GP Powell JT Thompson SG EVAR Trial Participants Comparison of endovascular aneurysm repair with open repair in patients with abdominal aortic aneurysm (EVAR trial 1), 30-day operative mortality results: Randomised controlled trial Lancet 2004 364 843 8 15351191
3 United Kingdom EVAR Trial Investigators Greenhalgh RM Brown LC Powell JT Thompson SG Epstein D Endovascular versus open repair of abdominal aortic aneurysm N Engl J Med 2010 362 1863 71 20382983
4 Lederle FA Freischlag JA Kyriakides TC Matsumura JS Padberg FT Jr Kohler TR Long-term comparison of endovascular and open repair of abdominal aortic aneurysm N Engl J Med 2012 367 1988 97 23171095
5 Kranokpiraksa P Kaufman JA Follow-up of endovascular aneurysm repair: Plain radiography, ultrasound, CT/CT angiography, MR imaging/MR angiography, or what? J Vasc Interv Radiol 2008 19 S27 36 18502384
6 Gelfand DV White GH Wilson SE Clinical significance of type II endoleak after endovascular repair of abdominal aortic aneurysm Ann Vasc Surg 2006 20 69 74 16378143
7 Timaran CH Ohki T Rhee SJ Veith FJ Gargiulo NJ 3rd Toriumi H Predicting aneurysm enlargement in patients with persistent type II endoleaks J Vasc Surg 2004 39 1157 62 15192552
8 Buth J Harris PL van Marrewijk C Causes and outcomes of open conversion and aneurysm rupture after endovascular abdominal aortic aneurysm repair: Can type II endoleaks be dangerous? J Am Coll Surg 2002 194 S98 102 11800362
9 Beeman BR Doctor LM Doerr K McAfee-Bennett S Dougherty MJ Calligaro KD Duplex ultrasound imaging alone is sufficient for midterm endovascular aneurysm repair surveillance: A cost analysis study and prospective comparison with computed tomography scan J Vasc Surg 2009 50 1019 24 19656651
10 Collins JT Boros MJ Combs K Ultrasound surveillance of endovascular aneurysm repair: A safe modality versus computed tomography Ann Vasc Surg 2007 21 671 5 17980791
11 Wolf YG Johnson BL Hill BB Rubin GD Fogarty TJ Zarins CK Duplex ultrasound scanning versus computed tomographic angiography for postoperative evaluation of endovascular abdominal aortic aneurysm repair J Vasc Surg 2000 32 1142 8 11107086
12 Sternbergh WC 3rd Greenberg RK Chuter TA Tonnessen BH Zenith Investigators Redefining postoperative surveillance after endovascular aneurysm repair: Recommendations based on 5-year follow-up in the US Zenith multicenter trial J Vasc Surg 2008 48 278 84 18572368
13 Beeman BR Murtha K Doerr K McAfee-Bennett S Dougherty MJ Calligaro KD Duplex ultrasound factors predicting persistent type II endoleak and increasing AAA sac diameter after EVAR J Vasc Surg 2010 52 1147 52 20691559
14 Maximus S Skelly C Milner R Velocities of type II endoleaks on Doppler ultrasonography predict outcome J Vasc Surg 2020 71 1719 25 31619352
15 Arko FR Filis KA Siedel SA Johnson BL Drake AR Fogarty TJ Intrasac flow velocities predict sealing of type II endoleaks after endovascular abdominal aortic aneurysm repair J Vasc Surg 2003 37 8 15 12514572
16 Sidloff DA Stather PW Choke E Bown MJ Sayers RD Type II endoleak after endovascular aneurysm repair Br J Surg 2013 100 1262 70 23939840
17 Pineda DM Calligaro KD Tyagi S Troutman DA Dougherty MJ Late type II endoleaks after endovascular aneurysm repair require intervention more frequently than early type II endoleaks J Vasc Surg 2018 67 449 52 29389419
18 Chaikof EL Dalman RL Eskandari MK Jackson BM Lee WA Mansour MA The society for vascular surgery practice guidelines on the care of patients with an abdominal aortic aneurysm J Vasc Surg 2018 67 2 77.e2 29268916
