Comparison Between Angiographic and Arterial Duplex Ultrasound Assessment of Tibial Arteries in Patients With Peripheral Arterial Disease: On Behalf of the Joint Endovascular and Non-Invasive Assessment of LImb Perfusion (JENALI) Group

Abstract: Background. Endovascular treatment of peripheral arterial disease (PAD) involving the tibial arteries is becoming an increasingly important part of revascularization. The current anatomical description of vessel patency in tibial arteries does not contribute effectively to therapeutic strategies. The Joint Endovascular and Non-Invasive Assessment of Limb Perfusion (JENALI) score, is a novel scoring system developed to further assess patency of tibial arteries, via both angiography and arterial duplex ultrasonography. A comparison was made between the JENALI score obtained by ultrasound and by angiography. Angiography is currently considered the gold standard of tibial artery imaging. Methods. This prospective single-center study involved 49 patients undergoing peripheral angiography for evaluation of PAD between November 2011 and November 2012. All patients underwent a detailed ultrasound assessment of the tibial arteries ± 7 days from diagnostic angiography. Eligible patients had a Rutherford score ≥III or abnormal ankle-brachial index values. Angiography and ultrasound were evaluated in a blinded fashion. Results. Average age of patients was 69.8 years. A total of 846 segments were assessed by both angiography and ultrasound. We found that 648 segments (76.6%) were deemed to be patent by angiography compared to 723 (85.5%) by ultrasound. Critical limb ischemia (CLI; Rutherford score ≥4) was described in 26 patients (53%). Average JENALI score for the right lower extremity was 7.0 by angiogram vs 7.7 by ultrasound. The average JENALI score of the left leg was 6.7 by angiogram vs 7.7 by ultrasound. A total of 94 lower extremities were assigned a JENALI score. Ultrasound was accurate in detecting tibial artery patency or occlusion in 80% of segments. The overall sensitivity/specificity of ultrasound detecting tibial artery patency was calculated at 93% and 40% (P<.05), respectively. Detection of patency via ultrasound was highest for the anterior tibial artery and the lowest for the peroneal artery. The angiographic and ultrasound JENALI scores better correlated with vessel patency (higher scores) than the lower angiographic and ultrasound JENALI scores. Conclusion. Using the novel JENALI scoring system allowed for direct comparison between two imaging modalities. In theory, the comparison can be extended to other imaging modalities. Ultrasound imaging had a high sensitivity in detecting patent vessels confirmed by angiography. Detecting occluded segments via ultrasound was less accurate. The highest accuracy was in the more superficial arteries (ie, anterior tibial, posterior tibial), compared to the deeper peroneal arteries. Risk stratification, treatment, and patient outcomes may be future applications of the JENALI scoring system.

J INVASIVE CARDIOL 2013;25(11):606-611

Key words: risk stratification, peripheral vascular disease

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Peripheral arterial disease (PAD) is an epidemic that impacts a large number of patients worldwide. Unfortunately, this number is expected to rise. Risk factors including age, gender, hyperlipidemia, hypertension, tobacco abuse, diabetes, and coronary artery disease were associated with an increased risk of developing PAD. Worldwide prevalence of PAD has increased between 13%-27% depending on the continent.¹ Symptoms of PAD may vary; 10%-20% of patients may have typical claudication symptoms.^2,3 Almost 50% of patients may suffer from silent PAD or have atypical symptoms.³

The impact of PAD on patient morbidity and mortality is well established. Patients with PAD have a three-fold increased risk of mortality compared to patients with no PAD.^4-6 With the rate of increase of PAD, critical limb ischemia (CLI) rates will rise. The prevalence of CLI is estimated to be 0.1%-0.2%.⁷ Within 1 year of clinical diagnosis, an estimated 30% of patients will undergo a major amputation, and 25%-30% will die.⁸

CLI represents the gravest stage of PAD. Adjusting for concomitant risk factors, amputation is an independent predictor of mortality. Fifty percent of non-diabetics and 61% of diabetic patients who underwent a below-the-knee amputation were deceased within 5 years.⁴ Despite advances in medical therapies, the number of patients with CLI continues to increase, presumably secondary to the aging population, increasing rates of obesity and diabetes, and the failure to substantially reduce tobacco consumption. The continuation of tobacco consumption triples the risk of CLI, and diabetes mellitus (DM) exacerbates it four-fold.⁵ Not surprisingly, CLI patients with infrapopliteal disease represent a sizable and ever-growing portion of our daily practice. The Trans-Atlantic Inter-Society Consensus for the management of peripheral arterial disease (TASC II) document does not describe the myriad of scenarios involving disease of the tibial and pedal vessels that are common in CLI patients.⁹ Currently, these are all grouped under a “TASC D” classification for which the recommended treatment is surgery, although the document acknowledges that there is an increasing body of evidence for the use of endovascular modalities in the treatment of tibial lesions.⁶

Historically, the evaluation of tibial disease has been performed by non-selective angiography with injection of a contrast bolus in the abdominal aorta and imaging the run-off to the feet. Using this method, contrast dissipates while traveling to the lower extremities and, as a result, good visualization of the extent of tibial PAD cannot be properly obtained. 

Selective angiography performed by injection of contrast directly into the superficial femoral, popliteal, or infrapopliteal arteries is considered to be the gold standard for the examination of tibial disease. However, this method still relies on the individual operator’s ability to identify and describe the tibial vascular tree, introducing a significant interoperator variability error. The Joint Endovascular and Non-Invasive Assessment of LImb Perfusion (JENALI) scoring system is a novel tool designed to standardize the description of tibial vessel anatomy and patency. To our knowledge, this is the first descriptive scoring method to comment on the patency of the entire tibial arterial tree. This simple scoring modality will allow clinicians across different specialties to communicate efficiently and clearly, as it can be applied to multiple imaging modalities.

Methods

This is a prospective, single-center study involving patients undergoing peripheral angiography for evaluation of PAD. After Internal Review Board approval was obtained, a total of 49 patients were enrolled in the trial between November 2011 and November 2012. All patients, as part of the study, underwent a detailed ultrasound assessment of the tibial arteries within 7 days of angiography (always prior to peripheral vascular intervention). Within the study group, three angiograms were deemed inadequate for interpretation due to poor visualization of the tibial vessels, and therefore excluded from the analysis. 

All eligible patients were diagnosed with PAD, and had a Rutherford score ≥III or abnormal ABI values (<0.9). Four endovascular specialists interpreted each angiogram independently and were blinded to both the ultrasound results as well as to each other’s scores. A non-invasive cardiovascular specialist, blinded to the angiographic assessments, interpreted the ultrasound images. Each lower extremity was scored separately. Each tibial vessel was divided into three segments: proximal, mid, and distal. Patent segments were given a score of 1 and occluded segments a score of 0. A total score of 9 signifies that the three tibial arteries (anterior, posterior, and peroneal) in the studied limb are patent in all segments. The lower the score, the more segments occluded, correlating with increased disease burden. The same scoring system was applied to the tibial vessels imaged via arterial duplex ultrasound. A comparison was made between the JENALI score obtained by ultrasound and by angiography. Assuming angiography as the gold standard, sensitivity and specificity were calculated for patency and occlusion of individual segments. Also, selective angiography was performed in 94 limbs (49 patients). Selective angiography was defined as placement of a diagnostic catheter as distal as safely possible into the vascular tree of the studied limb.

In an attempt to categorize the patients based on their tibial disease burden, we divided the cohort into three groups depending on their JENALI score (ultrasound and angiographic score): group I (JENALI 0-3), group II (JENALI 4-6) and group III (JENALI 7-9). 

Angiographic JENALI scoring system. The JENALI scoring system is the first to describe tibial vessel patency as it applies to the whole tibial vascular tree. It divides each tibial vessel into 3 segments. The anterior tibial artery starts from its take-off in the popliteal artery and it ends at the ankle level with the take-off of the dorsalis pedis artery. The posterior tibial artery starts at the end of the tibio-peroneal trunk (TPT) and it ends usually at the ankle level, where the vessel divides into the medial and lateral plantar arteries. The peroneal artery starts from the TPT and usually ends after the anterior and posterior communicating arteries, where it provides the lateral calcaneal branch. Each tibial vessel is divided into proximal, mid, and distal segments. The angiographer determines vessel patency. The segment is considered patent and is assigned a score of 1 if contrast is visualized within the segment. If the segment is occluded, it is assigned a score of 0. The segment will be considered patent, so long as there is a constant contrast line filling it, regardless if it fills through direct antegrade flow or indirect retrograde flow via collaterals. If there is evidence of high-grade stenosis, the segment is still considered patent. For example, if the proximal portion of the anterior tibial artery is occluded and the mid-to-distal segments reconstitute via collaterals, the mid and distal segments are considered patent. The JENALI scoring system tries to describe the actual segment status in terms of patency. Segment opacification with contrast from antegrade or retrograde filling via collaterals has no relevance in terms of scoring. A maximum score of 9 signifies that all tibial vessels are patent. A minimum score of 0 signifies that none of the segments is angiographically patent. The operators decided to divide the vessels subjectively without using any additional anatomical cut-offs beyond the take-off and the distal end of the vessel before it bifurcates into the next anatomical vessel. This is mainly to take into account the complexity of tibial anatomy and its variations. 

Ultrasound JENALI scoring system. The ultrasound scoring system applies the same angiographic principles. All images were digitally stored in a picture archiving and communication system (PACS) for review. Patients, as part of the study, underwent a detailed ultrasound assessment of all lower-extremity arteries. Standard duplex ultrasound images were obtained of the lower-extremity vessels from iliac to tibial arteries. Color-flow Doppler and pulse-wave Doppler interrogation of each artery was also obtained. If imaging of a segment was deemed technically difficult by standard techniques, then power Doppler was utilized. Philips iE33 or iU22 ultrasound machines with L9-3 broad-band linear array (9-3 MHz) were used to obtain ultrasound images. Technologists involved in imaging were registered vascular technologists. A certified non-invasive cardiovascular specialist, blinded to the angiographic assessments, ABI, and clinical background of the patient, interpreted the ultrasound images. Using ultrasound, a vessel was deemed patent if there was flow by color-flow Doppler, pulse-wave Doppler, or power Doppler in at least two-thirds of the segment being evaluated. Each tibial vessel was evaluated at the proximal, mid, and distal segments. Due to vessel depth, patient body habitus, and the presence of lower-extremity wounds, we could not image some tibial segments. Depending on the status of the adjacent segment, a JENALI score was assigned. If the adjacent segment was occluded, then the non-imaged segment was also considered occluded. The reader assumes that there is a continuity of flow. Figures 1-3 show an example of the JENALI scoring system by ultrasound and angiography. In Figure 1A, all segments in all tibial vessels were patent angiographically, giving the limb a JENALI score of 9. Figure 1B shows an angiographic example of an occluded distal posterior tibial segment. Figure 2 shows an ultrasound image of a patent distal anterior tibial segment. Figure 3 shows an ultrasound image of an occluded distal posterior tibial segment. The ultrasound images are visualized with color Doppler.

Statistical analysis. Continuous data were summarized as mean ± standard deviation. Categorical data are summarized as frequency and percentages. A total of 49 patients were enrolled in the trial. Three patients were excluded, because their angiograms were deemed inadequate for visualization. A student Chi-square test was used to compare the angiograms with the ultrasound. A P-value <.05 was considered statistically significant.

Overall sensitivity and specificity of ultrasound detecting patent tibial vessels in comparison to angiography were calculated. Sensitivity and specificity were also calculated for each tibial vessel separately. Additionally, the authors wanted to examine the sensitivity and specificity for selective and non-selective angiography in comparison to ultrasound. Correlation between angiography and ultrasound for the JENALI groups (I, II, III) was also tested. This comparison with ultrasound was carried out in selective and non-selective angiography (Figures 4 and 5). 

Results 

The average age of patients was 69.8 years. A total of 846 segments were assessed by both angiography and ultrasound; 648 segments (76.6%) were deemed patent by angiography compared to 723 (85.5%) deemed patent by ultrasound. 

Table 1 highlights the most prevalent components of patient’s demographics and clinical presentation. CLI (Rutherford ≥4) was described in 26 patients (53%). Average JENALI score for the right lower-extremity by angiogram was 7.0 compared to 7.7 by ultrasound. The average JENALI score of the left leg was 6.7, compared to 7.7 by ultrasound. Figure 6 shows the distribution of the JENALI score via angiography and ultrasound. Out of 94 lower extremities evaluated, 54 limbs (57.4%) had a high JENALI score.^7-9 The angiographic and ultrasound JENALI scores better correlated with vessel patency (higher scores) than the lower angiographic and ultrasound JENALI scores. Overall, ultrasound was accurate in detecting tibial artery patency or occlusion in 80% of segments. The overall sensitivity/specificity of ultrasound detecting tibial artery patency was calculated at 93% and 40%, respectively (P<.05) (Figure 7). Detection of patency remained the highest for the anterior tibial artery and the lowest for the peroneal artery (Figure 8). The operators also compared sensitivity and specificity of ultrasound in detecting vessel patency in selective and non-selective angiography (Figure 9). Ultrasound correlation with overall selective angiography had no statistical advantage, compared to overall non-selective angiography (P=.81). We also performed an ultrasound comparison to selective angiography and non-selective angiography according to the JENALI groups (I, II, III). There was a trend for ultrasound to correlate better with selective angiography, especially with low JENALI score (Figure 4). The correlation is not as significant with non-selective angiography (Figure 5). This suggests that the higher the burden of tibial disease, the better visualization the operator will achieve with selective angiography. 

Overall agreement for vessel patency and occlusion between angiography and ultrasound was calculated at 81.7%. Agreement on vessel patency was calculated at 79%. Agreement on vessel occlusion was estimated at 33.6%. This is a reflection of the low specificity calculated for ultrasound imaging.

On average, three interventional cardiologists read each vascular study. Disagreement in determining vessel patency ranged from 2.3% to 7.7% depending on selective vs non-selective angiography. 

Discussion

The purpose of this prospective, single-center study was to develop a system assessing tibial vessel patency in patients with advanced PAD and CLI. As a result, the JENALI score was created to evaluate the infrapopliteal circulation with angiography and ultrasound. This is, to our knowledge, the first study to grade tibial vessel patency. The authors went a step further and applied the JENALI scoring system to ultrasound mapping of the tibial vessels. This allowed for direct comparison between angiography and ultrasound mapping. This direct comparison was made feasible by the simple scoring system. Direct comparison between tibial angiography and tibial ultrasound using this scoring system has never been attempted before.

Tibial anatomy can be complex and confusing. Lower-extremity angiosome concept relies on tibial vessel supply to a certain anatomical distribution of the lower extremity. The anterior tibial artery supplies the front of the leg to the dorsum of the foot. The peroneal artery supplies the lateral aspect of the heel through its calcaneal branches. Finally, the posterior tibial artery supplies the medial aspect of the heel with the plantar surface of the foot through its plantar branches.^10,11 Revascularization based on the angiosome concept has been challenged. Some operators have argued that improving flow to any of the tibial vessels can be beneficial.¹² This assumes that collaterals between all tibial vessels are healthy and pedal arches are preserved. With the increasing rate of diabetes and chronic kidney disease, these assumptions can’t be accurate. Direct tibial vessel revascularization has been shown to speed wound healing and decrease the rate of major amputation.^13,14 Employing angiosome-directed therapy will allow the operator to target the vessel required, thus decreasing the amount of radiation and contrast.

Peripheral angiography has been performed by non-selective injection of a contrast bolus in the abdominal aorta and then following the run-off to both lower extremities. When using this method, contrast dissipates while traveling to the lower extremities and, as a result, good visualization of the extent of PAD in the tibial vessels cannot be properly obtained. Based on this outdated technique, many patients may have undergone unnecessary amputations due to an inaccurate assessment of tibiopedal circulation, and overestimation of disease severity. It is safe to assume that regardless of the modality of invasive imaging (requiring contrast), the contrast will require opacification of the vascular segment. However, if there is an arterial occlusion and the contrast has to rely on collaterals to reach distal segments, issues such as imaging delay and systemic pressure to allow complete opacification of these vascular beds comes into play. In a systematic review evaluating more than 28 trials examining the accuracy of ultrasound in detecting PAD, there was evidence of variation in accuracy between above- and below-the-knee vessels.¹⁵ With ultrasound, the median sensitivity and specificity were 88% and 95% for above-the-knee and 84% and 93% for below-the-knee, respectively. The inclusion criteria for these trials included more than 50% stenoses. There are limited data evaluating tibial vessel patency by non-invasive studies compared to angiography. In a limited analysis by Hoffmann et al, the use of ultrasound had a lower sensitivity and specificity of 64% and 80%, respectively.¹⁶ An interesting similar finding to our study was the higher frequency of patent vessels by ultrasound compared to selective angiography.

In our study, duplex ultrasound was accurate in detecting tibial artery patency or occlusion in 80% of segments. Overall, the ability of ultrasound to document if a tibial segment is truly patent (specificity) seems to be lower. 

The increasing prevalence of PAD and CLI is prompting a great interest in revascularization of our patients. Tibial disease remains very common in our PAD and CLI population. Unfortunately, amputation without arterial angiography occurs frequently in patients with CLI. There appears to be a significant variation in the evaluation and treatment of patient with PAD and CLI. Almost 50% of patients undergoing a major amputation did not receive a vascular procedure in the year prior to amputation.¹⁷ Furthermore, patient management varied even by geographic region where the patients reside.¹⁷ Also, patients of ethnic minorities or lower socio-economic status are less likely to be evaluated or undergo revascularization for CLI.^17,18 There are multiple and complex reasons to explain the variation in patient evaluation and management. The complexity of tibial anatomy in patients with PAD and CLI compounds the issue. With the advent of new invasive and non-invasive technologies, coupled with the skills of experienced endovascular specialists, treatment outcome of PAD patients should improve. The JENALI scoring system may have multiple future applications, such as risk stratification, prognosis, therapeutic planning, clinical follow-up, and outcome measures.

Study limitations. The JENALI scoring system has multiple limitations. The simplicity of the concept is in part responsible for its shortcomings. There are no clear anatomical cut-offs to define the segments. Anatomical variation is common among patients. The system also cannot inform the operators of which tibial vessel is patent, or which segment is patent. Modifications are certainly feasible; however, it will compromise the simplicity of the process. The study itself did not enroll only patients with tibial disease. Both angiographic and ultrasound assessment have limitations that may interfere in documenting vessel patency. We did not comment on the location of the catheter with selective angiography. Whether the catheter utilized to perform selective angiography was placed in the contralateral superficial femoral artery or popliteal artery, versus being placed in the external iliac artery secondary to infrainguinal occlusions (which might make a difference), was not addressed in this paper. Other factors, such as the amount of contrast utilized for each selective angiogram, were not standardized. Overall, our operators utilize the same techniques. The fact that we were not able to show a difference between selective and unselective angiography as it compares to ultrasound imaging might be related to the relatively higher tibial vessel JENALI scores. 

Conclusion

This is, to our knowledge, the first anatomical scoring system that describes tibial vessel patency in both invasive and non-invasive imaging modalities. The JENALI scoring system allowed for direct comparison between two different imaging modalities. The strength of the scoring system lies in its simplicity. Future application of the system will ultimately impact patient selection for revascularization. Another possible use is in risk stratification, ultimately impacting patient’s short- and long-term outcomes.

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From the Department of Internal Medicine, Metro Health Hospital, Michigan State University College of Osteopathic Medicine, Wyoming, Michigan.

Funding: The Metro Health Hospital Foundation awarded a private grant to fund duplex ultrasounds.

Disclosure: The authors have completed and returned the ICMJE Form for Disclosure of Potential Conflicts of Interest. The authors report no conflicts of interest regarding the
content herein.

Manuscript submitted September 24, 2013, provisional acceptance given September 27, 2013, final version accepted October 2, 2013.

Address for correspondence: J.A. Mustapha, Director of Cardiovascular Catheterization Laboratories, Metro Health Hospital, 5900 Byron Center Ave, SW, Wyoming, MI 49519.
Email: Jihad.Mustapha@metrogr.org