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An Extension of the Bollinger Scoring System to Analyse the Distribution of Macrovascular Disease of the Lower Limb in Diabetes

Open ArchivePublished:December 09, 2020DOI:https://doi.org/10.1016/j.ejvs.2020.11.017

      Objective

      While it is generally considered that patients with diabetes mellitus (DM) have more distal peripheral arterial disease (PAD), there is little information on how individual vessels are affected. The aim of this study was to adapt Bollinger's scoring system for lower limb angiograms (DSAs) to include the distal and planter vessels. The reliability of this extension was tested and was used to compare the distribution of disease in two cohorts of patients with and without DM.

      Methods

      Patients who had undergone DSA ± angioplasty for PAD at a single centre between September 2010 and April 2014 were identified. Twenty-five patients' images were reviewed by four clinicians and scored using an extended version of the Bollinger score. A total of 153 patients with DM were matched, for age, sex, ethnicity, smoking, and hypertension, with 153 patients without DM. The infrainguinal vessels were divided into 16 arterial segments, including plantar vessels, and scored using the Bollinger score. The score ranges from 0 to 15. Fifteen represents an arterial segment with more than 50% of its length occluded. Interobserver reliability was tested using interclass correlation (ICC) and Cohen's kappa coefficient.

      Results

      The ICC demonstrated good agreement between observers (0.76 [0.72–0.79]) with good internal consistency (Cronbach's alpha 0.93). When the Bollinger scores were categorised, the results were weaker, Cohen's kappa ranged from 0.39 (standard error 0.033) to 0.54 (0.030). Patients with DM had a higher burden of disease in the anterior tibial and posterior tibial arteries with relative sparing of the peroneal artery and no difference in the plantar vessels.

      Conclusion

      It has been demonstrated that the Bollinger score can be extended to include the distal vessels. This amended scoring system can be used to compare the burden of distal disease in patients with PAD. How the score relates to clinical presentation and outcomes needs further investigation.

      Keywords

      This study extends the original description of Bollinger's semi-quantitative scoring system for arterial disease on digital subtraction angiograms, to include the full length of the crural vessels and the major plantar vessels; the validity of this extension is tested.

      Introduction

      The number of people with diabetes mellitus (DM) is increasing worldwide.
      NCD Risk factor Collaboration (NCD-RisC)
      Worldwide trends in diabetes since 1980: a pooled analysis of 751 population-based studies with 4.4 million participants.
      In the United Kingdom, there are almost 3.9 million people currently living with DM, with an estimated million people who are as yet undiagnosed. The global odds ratio for peripheral arterial disease (PAD) in the presence of DM is 1.68 (95% CI 1.53–1.84, p = .009).
      • Fowkes F.G.R.
      • Rudan D.
      • Rudan I.
      • Aboyans V.
      • Denenberg J.O.
      • McDermott M.M.
      • et al.
      Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis.
      Patients with DM are generally thought to have a higher burden of disease in the tibial arteries.
      • Lowry D.
      • Saeed M.
      • Narendran P.
      • Tiwari A.
      A review of distribution of atherosclerosis in the lower limb arteries of patients with diabetes mellitus and peripheral vascular disease.
      However, there is little information on how the individual vessels are affected. In 1981 Bollinger described a scoring system for segments of the lower limb arterial tree that has commonly been used in the literature.
      • Bollinger A.
      • Breddin K.
      • Hess H.
      • Heystraten F.M.J.
      • Kollath J.
      • Kontilla A.
      • et al.
      Semiquantitative assessment of lower limb atherosclerosis from routine angiographic images.
      • Jude E.B.
      • Oyibo S.O.
      • Chalmers N.
      • Boulton A.J.M.
      Peripheral arterial disease in diabetic and nondiabetic patients.
      • Bradbury A.W.
      • Adam D.J.
      • Bell J.
      • Forbes J.F.
      • Fowkes F.
      • Gerry R.
      • et al.
      Bypass versus Angioplasty in Severe Ischaemia of the Leg (BASIL) trial: a description of the severity and extent of disease using the Bollinger angiogram scoring method and the TransAtlantic Inter-Society Consensus II classification.
      The system semi-quantitatively assesses 10 arterial segments (per leg) from the infrarenal aorta to the proximal 3 cm of the anterior tibial artery (ATA) and proximal 5 cm of the posterior tibial artery (PTA) and peroneal artery (PEA) (Fig. 1). Each segment is scored individually using the scoring matrix shown in Fig. 1. One of the limitations of the original description of the scoring system is that it does not extend beyond the proximal tibial arteries, which means the arterial runoff is not adequately assessed. The aim of this study was to extend the Bollinger score to include the distal vessels and to compare the distribution of atherosclerotic disease in the lower limb angiograms of a matched group of patients with and without DM.
      Figure 1
      Figure 1Arterial segments as described by Bollinger et al., 1981
      • Bollinger A.
      • Breddin K.
      • Hess H.
      • Heystraten F.M.J.
      • Kollath J.
      • Kontilla A.
      • et al.
      Semiquantitative assessment of lower limb atherosclerosis from routine angiographic images.
      and extended segments used in study. Each arterial segment will have an additive score based on the above scoring matrix. To avoid inadequate scoring the following rules should be obeyed: (1) In the presence of occlusion, plaques or stenosis are not considered. (2) When both categories of stenosis (> 50% and ≤ 50%) are present plaques are not scored. (3) For each type of occlusive lesion only one length category is indicated. A = infrarenal aorta; CIA = common iliac artery; IIA = internal iliac artery; EIA = external iliac artery; PFA = profunda femoris artery; SFA = superficial femoral artery; PA = popliteal artery; ATA = proximal 3 cm of anterior tibial artery; PEA = proximal 5 cm of peroneal artery; PTA = proximal 5 cm of posterior tibial artery; TPT = tibial-peroneal trunk; ATA1 = proximal 3rd of anterior tibial artery; ATA2 = middle 3rd of anterior tibial artery; ATA3 = distal 3rd of anterior tibial artery; DPA = dorsalis pedis artery; PEA1 = proximal 3rd of peroneal artery; PEA2 = middle 3rd of peroneal artery; PEA3 = distal 3rd of peroneal artery; PTA1 = proximal 3rd of posterior tibial artery; PTA2 = middle 3rd of posterior tibial artery; PTA3 = distal 3rd of posterior tibial artery; MPA = medial plantar artery; LPA = lateral plantar artery.

      Patients and Methods

      All patients who had a lower limb angiogram between September 2010 and April 2014 at the centre were identified from the prospective radiology database. From this cohort, all the patients with DM were identified. Each of these patients was matched for age ±5 years, sex, ethnicity, smoking, and hypertension with a patient without DM (NDM) who underwent an angiogram in the same period. Matching was performed using Microsoft Excel (Excel for Mac version 16.4), a formula was created that identified patients that matched on the above criteria. In the event a patient needed to be replaced an alternative that fitted the same criteria and was not already included was identified manually. Details of when this occurred are included in the Results section. The first angiogram performed within the study period with images saved on the hospitals imaging system (IMPAX) was assessed. If the patient had bilateral disease and complete imaging of both legs, only the left leg was scored.
      The Bollinger score was used in the following way. Based on the results of a pilot study, the infra-inguinal segments only were assessed with the tibioperoneal trunk (TPT) and assessed separately from the popliteal artery. The ATA, PTA and PEA were assessed divided into thirds and also as the segments that Bollinger originally described for a comparison. The dorsalis pedis (DPA), lateral (LPA), and medial (MPA) plantar arteries were also assessed (Fig. 1).
      The primary aim was to assess the interrater reliability of the extension of the arterial segments. Secondary outcome was a difference between median Bollinger score in each arterial segment in patients with DM compared with patients without DM.

      Statistical analysis

      Advice on matching/cohort selection and subsequent analysis was taken from a statistician. Four clinicians, with experience of reading lower limb angiograms and who had been trained in using the Bollinger system, independently scored 25 randomly selected angiograms from the dataset. ICC, with Cronbach's alpha and Cohen's kappa coefficient were calculated to assess the level of agreement. A two way random effects model with measures of absolute agreement was used.

      Comparison of cohorts

      All angiograms were assessed by one observer (D.L.), who also carried out the statistical analysis using IBM SPSS (IBM Corp. Released 2016. IBM SPSS Statistics for Macintosh, Version 24.0.). During assessment of the angiograms, the observer was unaware which study group the patient belonged too. As the cohorts were matched, paired statistical analysis was used where possible. Normality of continuous data (age, length of follow up) was tested using Shapiro–Wilk test and Q–Q plots.
      • Shapiro S.S.
      • Wilk M.B.
      An analysis of variance test for normality (complete samples).
      Parametric data were reported as mean (± standard deviation (SD)) and compared using paired t tests. Non-parametric data were reported as median (IQR) and compared using Wilcoxon signed rank test. Categorical data were compared using Fisher's exact test or chi squared test.
      The Bollinger score ranges from 0 to 15. It is only possible to score integers, and it is not possible to score 11 or 12, as such scores are non-parametric data and were reported using median (IQR) and appropriate non-parametric tests. Each arterial segment was analysed separately and also summed to form a proximal segment (SFA, PFA, and PA), distal segment (TPT, ATA 1/2/3, PEA 1/2/3, and PTA 1/2/3), pedal segment (DPA, MPA, LPA) and infrainguinal segment (all segments).

      Results

      A total of 986 unique patients were identified in the original database. Ninety per cent of patients were of a white ethnic origin, 4.2% were of a black ethnic origin, and 4.5% were of an Asian ethnic origin. In total, 310 patients were identified as being matched by the criteria set out above, 155 per cohort. The demographics in the matched cohorts were compared with those of the raw dataset. There was no significant difference in age in the DM group (matched 70.31 ± 9.17 years vs. raw dataset 69.74 ± 11.12, p = .55) or in the NDM group (70.33 ± 9.4 vs. 69.26 ± 13.7, p = .26). During the process of collecting the data for the Bollinger score in the DM cohort, two duplicate entries were identified. This necessitated the removal of the matching pairs from the NDM group and reduced the cohort sizes to 153 patients. Eight other patients were manually replaced with the next nearest match for the following reasons. Five patients only had iliac images saved, two patients underwent their angiogram to plan for plastic surgery rather than for peripheral arterial disease (PAD), and one patient's angiogram failed with no images stored (Fig. 2). The demographics for the patients are summarised in Table 1. Patients with DM were more likely to have presented with critical ischaemia (32% vs. 54.9%) and more likely to have had an emergency procedure (10.5% vs. 29.4%). All the patients with claudication had short distance claudication (Fontaine IIb) and the critical ischaemia group included those with rest pain and or tissue loss (Fontaine III – IV). The asymptomatic patients were all patients who had had a previous bypass and surveillance had revealed a flow limiting stenosis. In these patients the Bollinger score was only applied to their native vessels.
      Figure 2
      Figure 2Flow chart demonstrating the selection process for the matched cohorts consisting of patients with peripheral arterial disease with and without diabetes mellitus (DM) to adapt Bollinger's scoring system.
      Table 1Demographics of angiography patients with and without diabetes studied for adapting Bollinger's scoring system
      No diabetes (n = 153)Diabetes (n = 153)p value
      Age – y
      Paired t test.
      70.3 ± 9.470.3 ± 9.2.94
      Median LoF (IQR) – y
      Wilcoxon signed rank test.
      2.3 (2.1)2.4 (2.4).29
      Male sex
      Chi squared test.
      111 (72.5)110 (71.9)1.0
      Ethnic group
      Chi squared test.
      1.0
       White149 (97.4)149 (97.4)
       Asian2 (1.3)2 (1.3)
       Black2 (1.3)2 (1.3)
      Smoking
      Chi squared test.
      1.0
       Never smoked17 (11.1)17 (11.1)
       Ex-smoker103 (67.3)104 (68.0)
       Still smoking33 (21.6)32 (20.9)
      Hypertension
      Chi squared test.
      25 (16.3)25 (16.3)1.0
      Hypercholesterolaemia
      Chi squared test.
      59 (38.6)60 (39.2)1.0
      Renal function
      Chi squared test.
      1.0
       Normal148 (96.7)148 (96.7)
       Renal failure5 (3.3)5 (3.3)
      Indication
      Chi squared test.
      <.001
       Asymptomatic12 (7.8)11 (7.2)
       Claudication92 (60.1)58 (37.9)
       Critical ischaemia49 (32.0)84 (54.9)
      Timing of procedure
      Chi squared test.
      <.001
       Elective137 (89.5)108 (70.6)
       Emergency16 (10.5)45 (29.4)
      Data are provided as n (%) or mean ± standard deviation unless stated otherwise. LoF = length of follow up; IQR = interquartile range.
      Paired t test.
      Wilcoxon signed rank test.
      Chi squared test.

      Inter-class correlation

      For all the scorers, the ICC coefficient was 0.76 (0.72–0.79). This result suggests there was good agreement. There was good internal consistency with Cronbach's alpha .93.

      Cohen's kappa coefficient

      The Bollinger scores were categorised as 1 = < 3, 2 = 3–5, 3 = 6–8, 4 = ≥ 9.
      • Bradbury A.W.
      • Adam D.J.
      • Bell J.
      • Forbes J.F.
      • Fowkes F.
      • Gillespie I.
      • et al.
      Bypass versus Angioplasty in Severe Ischaemia of the Leg (BASIL) trial: a survival prediction model to facilitate clinical decision making.
      The kappa values ranged from 0.39 (standard error 0.033) to 0.54 (0.030) demonstrating a fair to moderate correlation.

      Bollinger score results

      The Bollinger scores are summarised in Table 2. The only individual arterial segment that showed significant difference between groups was the proximal third of PTA with the DM group having a higher burden of disease. The trend was similar, but non-significant, in the distal third of the ATA but also showed that the PEA was similar in both groups with relatively little burden of disease. However, when the segments of the distal vessels were added there was a significant higher burden of disease in the ATA and PTA but, again, not in the PEA.
      Table 2Bollinger scores, by arterial segment, for angiography patients with and without diabetes
      Arterial segmentMedian Bollinger score (IQR)p value
      Related samples Wilcoxon signed rank test.
      No diabetes (n = 153)Diabetes (n = 153)
      Superficial femoral9 (9)8 (8).28
      Profunda femoris0 (1)0 (2).055
      Popliteal3 (11)4 (5).73
      TP trunk0 (3)2 (4).45
      Anterior tibial, proximal 3rd2 (13)4 (13).078
      Anterior tibial, middle 3rd0 (15)3 (15).17
      Anterior tibial, distal 3rd3 (15)13 (15).12
      Dorsalis pedis4 (15)13 (15).31
      Peroneal, proximal 3rd0 (4)1 (6).40
      Peroneal, middle 3rd0 (7)0 (13).29
      Peroneal, distal 3rd0 (13)0 (15).55
      Posterior tibial, proximal 3rd0 (13)3 (15).038
      Posterior tibial, middle 3rd2 (15)3 (15).17
      Posterior tibial, distal 3rd2 (15)4 (15).11
      Medial plantar15 (15)10 (15).98
      Lateral plantar15 (15)14 (15).60
      Sum anterior tibial scores8 (33.5)15 (40).027
      Sum peroneal scores3 (20)5 (28).29
      Sum posterior tibial scores4 (34)13 (45).035
      IQR = interquartile range; TP = tibioperoneal.
      Related samples Wilcoxon signed rank test.
      The sum of all the infrainguinal segments showed no significant difference between groups (Table 3). However, there was a significant difference overall in the distal vessels with a higher atherosclerotic load in the DM group. In Bollinger's original description of his scoring system, only the first 3 cm of the ATA and 5 cm of the PEA and PTA were included. The results from these segments were significantly lower than the median score for the whole vessel in both the PEA and the PTA (Table 4).
      Table 3Median sum of Bollinger scores by arterial region in angiography patients with and without diabetes
      Arterial regionMedian sum of Bollinger scores (IQR)p value
      Related Samples Wilcoxon signed rank test.
      No diabetes (n = 153)Diabetes (n = 153)
      Proximal15 (12)15 (9).90
      Distal44 (62)51 (59).009
      Pedal15 (30)15 (30).66
      Infrainguinal77 (80)88 (71).061
      IQR = interquartile range. Proximal = superficial femoral artery, profunda femoris artery, popliteal artery; Distal = tibioperoneal trunk, anterior tibial artery 1/2/3, peroneal artery 1/2/3, posterior tibial artery 1/2/3; Pedal = dorsalis pedis artery, medial plantar artery, lateral plantar artery; Infrainguinal = all segments.
      Related Samples Wilcoxon signed rank test.
      Table 4Comparison of Bollinger score for the originally described tibial segment to the median score for the whole vessel in 306 patients
      Tibial segmentOriginal segmentMedian score for whole vesselp value
      Related samples Wilcoxon signed rank test.
      nMedian (IQR)nMedian (IQR)
      Anterior tibial3040 (4)3052 (15).20
      Peroneal3040 (3)3040 (13).001
      Posterior tibial3051 (15)3041.75 (15).004
      IQR = interquartile range.
      Related samples Wilcoxon signed rank test.

      Discussion

      This study has demonstrated that extending the segments assessed by the Bollinger score is valid with good correlation between assessors with good internal consistency. In Bollinger's original description of the scoring system, the agreement between five scorers on six angiograms was examined using Kendall's coefficient of concordance (KCC).
      • Bollinger A.
      • Breddin K.
      • Hess H.
      • Heystraten F.M.J.
      • Kollath J.
      • Kontilla A.
      • et al.
      Semiquantitative assessment of lower limb atherosclerosis from routine angiographic images.
      They stated that the agreement appeared to be excellent with p < .001 but unfortunately did not quote the actual value of KCC. Since then a few other studies have addressed this question using a variety of methods. Bradbury et al.
      • Bradbury A.W.
      • Adam D.J.
      • Bell J.
      • Forbes J.F.
      • Fowkes F.
      • Gerry R.
      • et al.
      Bypass versus Angioplasty in Severe Ischaemia of the Leg (BASIL) trial: a description of the severity and extent of disease using the Bollinger angiogram scoring method and the TransAtlantic Inter-Society Consensus II classification.
      compared the mean score for the whole leg, above the knee and below the knee, for two observers. These scores were further divided into four groups (<3, 3–5, 6–8, ≥9) to allow comparison with the TASC II classification. They found that in approximately 75% of cases the two observers placed the patient in the same Bollinger score group. Morris et al. compared two observers' scores of 20 patients using weighted kappa values.
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      They found poor intra- and interobserver agreement for the profunda femoris segment (−0.07 [standard error 0.14] and 0.26 (0.16) respectively), but the rest of the values were moderate to very good and particularly strong on the tibial vessels. Owing to the variation in methods used it is difficult to compare the results with these, but it would seem that the agreement between observers was comparable with other studies; however, the results were weaker when the scores were treated categorically.
      The extension of the segments appears to provide additional information on the burden of disease (Table 4). It may not be particularly surprising that when a longer segment of vessel is looked at more disease is seen. However, this finding does demonstrate that Bollinger's original description is inadequate to detect the full burden of disease. This study demonstrated that in a well matched group, patients with DM had more disease than those without DM in below the knee vessels, but not in the above knee segments or the pedal vessels. In the tibial vessels there appeared to be relative sparing of the PEA, particularly in the DM group. This is a finding that has been observed before,
      • Jude E.B.
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      Historically there has been concern that patients with PEA only run off are likely to have worse outcomes due to outflow to the foot being reliant on collaterals. However, there are studies that demonstrate comparable outcomes to those with single tibial vessel run off for both bypass and endovascular intervention.
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      The results demonstrated that patients in both groups had a similar degree of disease in the pedal vessels. In the literature, this has been an inconsistent finding
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      and the influence of chronic kidney disease may be partly responsible for this.
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      It has been suggested that patients with tibial disease related to DM will have relative sparing of the pedal vessels. In 2007, Graziani et al., in a cohort all with DM and tissue loss secondary to ischaemia, found that of the 118 patients whose tibial vessels were all occluded, 88% had at least one patent pedal vessel.
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      The presence, or not, of pedal disease is important as when there is significant tibial disease the pedal vessels can be a potential target for bypass and, as endovascular techniques are improving, are a potential target or retrograde conduit for endovascular therapy.
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      In addition to that patients with pedal disease have been found to have higher rates of amputation and mortality and it is an independent predictor of failure of revascularisation.
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      The difficulty with classification systems that consider the burden of arterial disease is relating the severity of visualised disease to the clinical picture and treatment outcomes. The global vascular guidelines on the management of chronic limb threatening ischaemia published in 2019 have tried to address this.
      • Conte M.S.
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      • Kolh P.
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      • Dick F.
      • Fitridge R.
      • et al.
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      They have proposed the Global Limb Anatomic Staging System (GLASS) that aims to improve on previously described classification systems like Bollinger and TASC II. High quality angiographic imaging is used to identify a target artery path based on achieving in line flow to the foot. Following this the degree of femoropopliteal and infrapopliteal disease is graded separately and combined into three stages of severity. A consensus process, with review of available evidence, was used to estimate the expected technical failure rate and one year limb based patency for each GLASS stage.
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      • et al.
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      GLASS differs from the Bollinger score in that the grading is based on an anatomical pattern of disease rather than a purely segmental description. The description of patterns, that give an overall picture of the degree of disease, are more likely to be relevant to the revascularisation strategy choice than the burden of disease in individual segments.
      • Conte M.S.
      • Bradbury A.W.
      • Kolh P.
      • White J.V.
      • Dick F.
      • Fitridge R.
      • et al.
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      So far, GLASS, and its relationship to clinical outcomes, has only been tested on the cohorts from the Bypass versus Angioplasty in Severe Ischaemia of the Leg (BASIL)-1 trial.
      • Kodama A.
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      • Conte M.S.
      • Bradbury A.W.
      Relationship between global anatomic staging system (GLASS) and clinical outcomes following revascularisation for chronic limb threatening ischaemia in the bypass versus angioplasty in Severe ischaemia of the leg (BASIL)-1 trial.
      They found that GLASS was associated with outcomes, including immediate technical failure, amputation free survival, and freedom from major adverse limb events, for the endovascular cohort but not the open surgery cohort.
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      • Bate G.
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      Relationship between global anatomic staging system (GLASS) and clinical outcomes following revascularisation for chronic limb threatening ischaemia in the bypass versus angioplasty in Severe ischaemia of the leg (BASIL)-1 trial.

      Limitations

      Limitations of this study include the lack of information in the dataset on co-morbidities and patient characteristics including body mass index, alcohol intake, and cardiovascular disease. Information on pressures indices was also not consistently available. The decision was made to match the control and study groups for risk factors for peripheral arterial disease. A potential problem with closely matching cohorts is that they may no longer represent the general population. This has a potential impact on how generalisable the results are.

      Future directions

      The extension of the Bollinger score needs to be assessed in a prospective manner with a focus on how the score relates to both clinical presentation and outcomes. Whether the extension of the score correlates better with clinical severity than the original is not known. This future work can be related to the Global vascular guidelines on the management of chronic limb threatening ischaemia stated research priorities. It would fall into the category of below knee run off scores and how they relate to procedural or clinical outcomes.
      • Conte M.S.
      • Bradbury A.W.
      • Kolh P.
      • White J.V.
      • Dick F.
      • Fitridge R.
      • et al.
      Global vascular guidelines on the management of chronic limb-threatening ischemia.

      Conclusions

      It has been demonstrated that it is possible to extend Bollinger's original segments to include the entirety of the tibial vessels and the pedal vessels with good interobserver reliability. In well matched cohorts, those with DM were found to have a higher burden of disease in the tibial vessels. Overall, there was no significant difference in burden of infra-inguinal disease. Further work is required to assess how the radiological findings relate to clinical presentation and outcomes.

      Conflicts of interest

      None.

      Funding

      None.

      Acknowledgements

      James Hodson for advice on data analysis and patient matching.

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