In situ hemodynamics of perforating veins in chronic venous insufficiency

In situ hemodynamics of perforating veins in chronic venous insufficiency Konstantinos T. Delis, MSc, MD, PhD, Marc Husmann, MD, Evi Kalodiki MD, PhD, John H. Wolfe, MS, FRCS, and Andrew N. Nicolaides MS, FRCS, London, United Kingdom Purpose: The prevalence of incompetent perforators increases linearly with the clinical severity of chronic venous insufficiency (CVI) and the presence of deep vein incompetence. Putative transmission of deep vein pressure to skin may cause dermal hypoxia and ulceration. Despite extensive prospective interest in the contribution of perforators toward CVI, their hemodynamic role remains controversial. The aim of this prospective study was to determine the in situ hemodynamic performance of incompetent perforating veins across the clinical spectrum of CVI, by means of duplex ultrasonography. Methods: A total of 265 perforating veins of 90 legs that had clinical signs and symptoms consistent with CVI in 67 patients referred consecutively to the blood flow laboratory were studied. The clinical distribution of the examined limbs was CEAP0, 10 limbs; CEAP1-2, 39 limbs; CEAP3-4, 21 limbs; and CEAP5-6, 20 limbs. With the use of gatedDoppler ultrasonography on real-time B-mode imaging, the flow velocity waveforms were obtained from the lumen of perforators on release of manual distal leg compression in the sitting position and analyzed for peak and mean velocities, time to peak velocity, volume flow, venous volume displaced outward, and flow pulsatility. The diameter and duration of outward flow (abnormal reflux > 0.5 seconds) were also measured. Results: Incompetent perforators had bigger diameters, higher peak and mean velocities and volume flow, longer time to peak velocity, and bigger venous volume displaced outward (VVoutward) than competent perforators (all, P < .0001). The diameter of incompetent perforators did not change significantly with CEAP class (all, P > .1). Incompetent thigh and lower-third calf perforators had a significantly bigger diameter than perforators in the upper and middle calf combined (both, P < .05), in incompetent perforators: reflux duration was unaffected by CEAP class or site (P > .3); peak velocity was higher in those in CEAP3-4 than those in CEAP1-2 (P = .024); mean velocity in those in CEAP3-6 during the first second of reflux was twice that of those in CEAP1-2 (P < .0001); both higher volume flow and VVoutward were found in the thigh perforators than those in the upper and middle calf thirds (P < .03); CEAP3-6 volume flow and VVoutward, both in the first second, were twice that in those in CEAP1-2 (P < .002); flow pulsatility in those in CEAP5-6 was lower than in those in CEAP1-2 (P = .014); in deep vein incompetence, higher peak velocity, volume flow, VVoutward, and diameter occurred than in its absence (P < .01). CEAP designation correlated significantly with mean velocity and flow pulsatility, both in the first second (r = 0.3, P < .01). The flow direction pattern in perforator incompetence was uniform across the CVI spectrum: inward on distal manual limb compression, and outward on its release; competent perforators had a smaller percentage of outward flow on limb compression (P < .01). Conclusion: In addition to an increase in diameter, perforator incompetence is characterized by significantly higher mean and peak flow velocities, volume flow, and venous volume displaced outward, and a lower flow pulsatility. Differences in early reflux enable a better hemodynamic stratification of incompetent perforators in CVI classes. In the presence of deep reflux, incompetent perforators sustain further hemodynamic impairment. In situ hemodynamics enable quantification of the function of perforators and can be used in the identification of the clinically relevant perforators and the impact of surgery. (J Vasc Surg 2001;33:773-82.)

Despite extensive interest in the contribution of perforating veins toward chronic venous insufficiency (CVI), spanning just less than two centuries since they were first From the Irvine Laboratory for Cardiovascular Investigation and Research, Academic Vascular Surgery, St Mary’s Hospital, Imperial College School of Medicine. Competition of interest: nil. Presented at the Twelfth Annual Meeting of the American Venous Forum, Phoenix, Ariz, Feb 3-6, 2000. Reprint requests: Konstantinos T. Delis MSc, MD, PhD, Irvine Laboratory, 10th Floor QEQM Wing, St Mary’s Hospital, Imperial College School of Medicine, Praed Street, Paddington, London, W2 1NY, UK (e-mail: [email protected]). Copyright © 2001 by The Society for Vascular Surgery and The American Association for Vascular Surgery. 0741-5214/2001/$35.00 + 0 24/6/112707 doi:10.1067/mva.2001.112707

mentioned by the Russian anatomist von Loder (1803),1 their hemodynamic role remains controversial.2,3 Incompetent perforators occur mainly in the middle and distal thirds of the medial calf,1,4-8 and then most often in the middle thirds of the medial thigh and posterior calf.7 Their prevalence increases linearly with the clinical severity of CVI, stratified according to CEAP (clinical, etiological, anatomical, and pathological)7,9 classification; it also increases significantly with the prevalence of deep vein incompetence.7,10 This, in the invariable presence of superficial reflux in CEAP classes 2 to 6,7,11 emphasizes the possible etiopathogenic role of the deep system in perforator incompetence, which, however, may occur in the absence of deep vein reflux.12-14 It has been suggested that incompetent perforators transmit the deep vein pressure to the skin, causing dermal hypoxia15 and explaining 773

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Table I. Distribution of the investigated perforators in thigh and calf Anterolateral Competent thigh perforators (n = 7) Upper Middle Lower Competent calf perforators (n = 112) Upper Middle Lower Incompetent thigh perforators (n = 21) Upper Middle Lower Incompetent calf perforators (n = 125) Upper Middle Lower

Table II. Reproducibility of the hemodynamic parameters of perforator flow (coefficient of variation range) in 10 limbs (≥ 1 perforator/limb)* Hemodynamic parameters of perforator flow Peak velocity Mean velocity Time to peak velocity Duration

Coefficient of variation (range) 4.5%-24% 2.6%-22% 3.3%-20% 6.5%-23%

*No. = 10 subjects.

the reported clinical16-18 and hemodynamic19 improvement after their ablation. However, the recently reported midterm results of the North American subfascial endoscopic perforator surgery (SEPS) trial have shown a gross skin ulcer recurrence of 30% within 1 year of subfascial ablation of incompetent perforators, which increases to 40% in post-thrombotic limbs.3 This highlights claims of previous investigators that the contribution of perforators to venous hypertension,20 calf muscle pump function,21 and venous hemodynamics22 is overemphasized. In view of the increasing resources invested in national and international trials on the clinical significance of perforator surgery, the modest outcome so far, and today’s environment of cost containment, more emphasis needs to be placed on understanding the hemodynamic behavior of perforators, which may also depend on the specific pattern and severity of CVI.23 However, with the exception of the direction of flow at different time points5,24 and the duration of outward flow on the release of manual compression distal to their anatomic location, the actual hemodynamic performance of perforators at a local level is poorly understood. The current prospective study determined the in situ hemodynamic performance of perforators across the clinical spectrum of CVI using duplex ultrasonography.

Posterior

Medial

0 0 0

0 0 1

0 5 1

0 8 4

3 19 3

9 34 32

2 0 2

0 1 2

0 11 3

0 12 4

1 22 1

5 46 34

MATERIALS AND METHODS Two hundred sixty-five perforating veins of 90 legs with clinical signs and symptoms consistent with CVI were studied. The 67 patients involved (34 women, 33 men; median age, 63.5 years; age range, 18-92 years) were referred consecutively by general practitioners, physicians, and surgeons of the northwest London region to the blood flow laboratory for duplex scanning. The clinical severity of the examined limbs, stratified according to the update by Porter et al9 was CEAP0, 10 limbs; CEAP1-2, 39 limbs; CEAP3-4, 21 limbs; and CEAP5-6, 20 limbs. The examination protocol entailed a medical history and physical examination, measurement of the resting ankle-brachial pressure indices, and color flow duplex scanning of the lower-limb venous system. Excluded were legs with peripheral vascular disease (resting pressure index < 0.95), venous malformations, a history of varicose vein surgery, orthopedic procedures for fractures, injection compression therapy, infection, deep vein thrombosis, and clinically suspected venous outflow obstruction confirmed by means of occlusive air plethysmography. Duplex scanning was performed with the Hewlett Packard Sonos 2500 (Palo Alto, Calif) fitted with a 7.5/5.5-MHz–linear array scanhead. Color flow duplex imaging was used as a means of enabling only a crude hemodynamic evaluation of the venous system, particularly when more than one venous structure were imaged simultaneously, and as a means of steering investigation to the sites of flow abnormality. However, all crucial data were based on real-time gated Doppler ultrasound flow velocity waveform analysis superimposed on realtime B-mode ultrasound imaging of the insonated venous structures. Scanning was performed with the patients sitting on a high examining couch, with their feet resting on a low stool and their knees partially flexed. Reflux times were measured on the release of manual compression of the foot, calf, or thigh, always distal to the evaluated venous segment, on a thoroughly

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primed venous system. Reflux exceeding 0.5 seconds was considered abnormal.25 Perforators were identified on cross-sectional scanning of all aspects of the calf and thigh, and their gross hemodynamic performance was assessed with duplex ultrasonography. The flow velocities were obtained on optimal longitudinal imaging of the perforator lumen. A perforator was considered to be incompetent when outward flow exceeding 0.5 seconds in duration was documented immediately after the release of manual compression on three consecutive evaluations. Doppler velocity waveforms generated during and immediately after the release of manual limb compression applied distal to the investigated structures were obtained by insonating the lumen of perforators at the fascial level. The waveforms were stored in the computer and analyzed with software offering automated calculation of the mean venous velocity (MV) and peak venous velocity (PV). The diameter in centimeters (at a fascial level), total duration and venous volume flow (Q = MV × diameter) of reflux, the time to peak velocity (TTPV), and the total venous volume displaced outward (VVoutward) on release of distal limb compression were also measured in all identified perforating veins. Hemodynamic differences of perforators in the early reflux, immediately after the release of compression, were assessed by measuring the MV, Q, flow pulsatility (FP = PV differential/MV; equivalent to pulsatility index used in arterial flow), and VVoutward in the first postcompression second. The average of at least three measurements was used. Perforators were classified anatomically as medial, posterior, and anterolateral. Their location in the thigh and calf was further subdivided into upper, middle, and lower thirds, resulting in a total of nine anatomical sites in both the calf and thigh. The distribution of investigated perforators is depicted in Table I. Throughout the duplex investigation, which was performed by the same operator (K.T.D.), the settings of gain, compression, and rejection on gated Doppler ultrasound scanning and the insonation angle (60°) were scrupulously maintained. Suboptimal Doppler signals and those containing noise from adjacent arterial flow or aliasing were discarded, and the measurements were repeated. The scanning protocol in limbs with CVI has been presented.7 Reproducibility of PV, MV, TTPV, and duration of perforator flow, obtained by repeating flow measurements 5 times per perforator in 10 limbs (n = 10 subjects) is depicted in Table II. Statistical analysis of the data was performed with the Mann-Whitney U test for intergroup comparisons, with 95% CI, and the Bonferroni Correction when required. Correlational analysis of bivariate quantitative data was performed with the Spearman rank test. Differences in proportions were evaluated with the χ2 test. RESULTS Assessment of the distribution of abnormal venous reflux in the 90 limbs examined revealed no reflux in 4 limbs (4.4%); superficial reflux in 17 limbs (19%); superfi-

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cial and perforator reflux in 33 limbs (37%); superficial and deep reflux in 4 limbs (4.4%); and reflux involving all systems in 32 limbs (36%). The overall incidence of abnormal reflux in the superficial, deep and perforating systems was 95.5%, 40%, and 72.2%, respectively. The PV, MV, Q, TTPV, and VVoutward in perforators on release of manual distal leg compression, the diameter of perforating veins, and the duration of perforator flow across the CEAP classes and at different anatomic locations are depicted in Figs 1 through 4. Incompetent perforators had a bigger diameter, five times longer reflux times, higher PV, MV, and Q, longer TTPV, and larger VVoutward than competent perforators (all, P < .0001). The diameter of incompetent perforators did not change with CEAP class (P > .1). The median diameter of incompetent thigh perforators was 18% larger than that of the calf perforators, the difference missing significance in our sample (P = .114; 95% CI: 0.12, – 0.013 cm). Incompetent thigh perforators had a larger diameter than incompetent perforators in the upper and middle calf combined (P < .04; 95% CI: 0.03, 0.13 cm). The median diameter of incompetent lower calf perforators (median, 0.32 cm) was 25.5% larger than that of the middle and upper calf perforators (P = .04; 95% CI: 0.015, 0.11). The duration of outward flow of incompetent perforators was unaffected by the severity of CVI and the anatomic location (both, P > .3). The PV of the outward flow of incompetent perforators was significantly higher in those in CEAP3-4 than in those in CEAP1-2 (P = .024); the difference between CEAP1-2 and CEAP5-6 groups was not significant in our sample (P > .1). Differences in the PVs between incompetent thigh and calf perforators and also between PVs in the lower calf and PVs in the upper or middle calf were all nonsignificant (P > .3). The TTPV in incompetent perforators on the release of leg compression was unaffected by their anatomic location or the severity of CVI (CEAP1-6; P > .7). The median MV of incompetent perforators was 21% higher in those in CEAP3-4 than those in CEAP1-2; however, the difference, as well as that between CEAP3-4 and CEAP5-6, was not significant (P > .15) in our sample. MV differences caused by anatomic location were not significant (P > .34). MV in the first second after the release of limb compression (1-second-MV) was more than four times higher in incompetent perforators than in competent ones (P < .0001; point-estimate, 9.9 cm/s; 95% CI: 7.8, 13.2 cm/s) (Fig 5). The median 1-second-MV of incompetent perforators was more than twice as high in those in CEAP3-6 as in those in CEAP1-2 (P < .0001; point-estimate, 6 cm/s; 95% CI: 3, 9.1 cm/s). The Q of incompetent perforators was unaffected by CVI class (P > .42); incompetent perforators in the thigh had a higher Q than the upper and middle calf perforators (P < .03; 95% CI: 0.33, 40.4 mL/min). Differences based on calf location were not significant (P = .35). The Q in the first second after the release of limb compression (Fig 6) (1-second-Q) was more than 12 times higher in incompe-

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Fig 1. A, Perforator diameter measured at the fascial level and B, duration of perforator flow on release of manual distal leg compression (median and interquartile range) in 265 perforators across the spectrum of chronic venous insufficiency. Incompetent (Inc) perforators are stratified according to CEAP classes and anatomic level (thigh and calf; upper, middle, and lower calf). A, Incompetent versus competent (Comp) perforators, P < .0001; thigh or lower calf versus upper-middle calf, P ≤ .04. B, Incompetent versus competent perforators, P < .0001.

Fig 2. A, Peak velocity and B, time to peak velocity (median and interquartile range) of (outward) perforator flow on release of manual distal leg compression in 265 perforators, across the spectrum of chronic venous insufficiency. Incompetent (Inc) perforators are stratified according to CEAP classes and anatomic level (thigh and calf; upper, middle and lower calf). A, Incompetent versus competent (Comp) perforators, P < .0001; CEAP3-4 versus CEAP1-2, P = .024. B, Incompetent versus competent perforators, P < .0001.


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Fig 3. A, Mean velocity and B, volume flow (median and interquartile range) of perforator reflux (265 perforators) on release of distal leg compression, across the spectrum of chronic venous insufficiency. Incompetent (Inc) perforators are stratified according to CEAP classes and anatomic level (thigh and calf; upper, middle, and lower calf). A, Incompetent versus competent (Comp) perforators, P < .0001; CEAP or anatomic differences all nonsignificant, P > .34. B, Incompetent versus competent perforators, P < .0001; CEAP differences all nonsignificant, P > .42; thigh versus upper-middle calf, P < .03.

Table III. The direction of perforator flow during and immediately after manual distal limb compression During distal compression Type of perforators Competent Incompetent CEAP1-2 Incompetent CEAP3-4 Incompetent CEAP5-6

Inward 78.3% 70% 86.1% 85.4%

Outward 21.7% 30% 13.9% 14.6%

On release of compression

Overall

Inward

Outward

Bidirectional

Unidirectional

29.9% 2.4% 0% 2%

70%* 97.6% 100% 98%

77% 68.3% 81.6% 82.4%

23% 31.7% 18.4% 17.6%

*P < .001 (competent vs incompetent CEAP1-2 or CEAP3-4 or CEAP5-6 or CEAP1-6).

tent perforators than in competent ones (P < .0001; pointestimate, 38.30 mL/min; 95% CI: 30.6, 49.5 mL/min). Incompetent perforators in CEAP3-6 had a 1-second-Q that was more than twice that of those in CEAP1-2 (P = .002; point-estimate, 20.2 mL/min; 95% CI: 37.7, 7.4 mL/min). The VVoutward of incompetent perforators was higher in those in CEAP3-6 than those in CEAP1-2, just missing significance in our sample (P = .12; point-estimate, 0.32 mL; 95% CI: 0.85, –0.07 mL). Incompetent thigh perforators had a larger VVoutward than the upper and middle calf incompetent perforators (P = .03; 95% CI: 0.06, 1.8 mL). The median VVoutward in the first second of reflux (1-secondVVoutward) was 13 times larger in incompetent perforators than in competent ones (P < .0001; point-estimate, 0.64 mL; 95% CI: 0.51, 0.82 mL). The median 1-second-

VVoutward was more than twice larger in incompetent perforators in CEAP3-6 than in those in CEAP1-2 (P = .001; point-estimate, 0.35 mL; 95% CI: 0.64, 0.14 mL). The FP was higher in perforator competence than in incompetence (P < .0001; point-estimate, 3.7; 95% CI: 3.17, 4.1). The FP of incompetent perforators was significantly higher in those in CEAP1-2 than in those in CEAP5-6 (P = .015; point-estimate, 0.41; 95% CI: 0.05, 1.1). In the presence of deep reflux, incompetent perforators had higher PV, Q, VVoutward, and diameter than they did in its absence (all, P < .01). The perforator flow direction during and immediately after application of limb compression, across the CVI spectrum, is depicted in Table III. Bivariate correlation analysis conducted between the

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Fig 4. Venous volume displaced outward (median and interquartile range) in 265 perforators on release of manual distal leg-compression, across the spectrum of chronic venous insufficiency. Incompetent (Inc) perforators are stratified according to CEAP classes and anatomic level (thigh and calf; upper, middle, and lower calf). Incompetent versus competent (Comp) perforators, P < .0001; thigh versus upper-middle calf, P = .03.

investigated hemodynamic parameters of perforators (irrespective of competence) and between these and the perforator diameter and CVI severity showed that the PV correlated well with the MV (r = 0.76; P < .001), VVoutward (r = 0.46; P < .001), and Q (r = 0.484; P < .001); the MV correlated significantly with the VVoutward (r = 0.666; P < .001) and Q (r = 0.61; P < .001); the duration of perforator flow correlated well with the VVoutward (r = 0.47; P < .01) and Q (r = 0.61; P < .001); and the Q correlated significantly with the perforator diameter (r = 0.68; P < .001). The CVI class correlated significantly with the 1-second-MV (r = 0.31; P < .01) and FP (r = 0.3; P < .01). DISCUSSION The duration of venous reflux and direction of flow during and on the release of leg compression are the only hemodynamic parameters investigated so far in perforators. No hemodynamic criteria specific to perforating veins are currently available, so incompetence is assumed when outward flow exceeds 0.5 seconds,7,8,10,24 the cutoff point accepted for axial vein incompetence.25 Inward flow on leg compression, with or without outward flow on its release, in CVI and in health, respectively, is the most frequent flow pattern demonstrated in perforating veins.5,8,10,24 Flow

from the superficial to the deep system (inward) is demonstrated in 85% of perforators on distal compression of legs with or without reflux.5 Outward flow on release of distal leg compression, representing deep-to-superficial vein leak, has been reported to increase with CVI severity (57% in limbs with primary varicose veins, and 67% and 66% in limbs with lipodermatosclerosis or past ulceration, respectively).10 The presence of deep reflux increases the frequency of outward flow26 from 22% to 54% in limbs with uncomplicated varicose veins and from 34% to 66% in limbs with skin changes.27 Outward flow on release of distal leg compression has recently been shown to be present in 17% of competent perforators,24 although it was previously thought to be absent20 or nonrecordable.5 Incompetent perforators have a bigger diameter than competent ones,8,24 with the diameter being predictive of pathologic reflux in 90% of veins if their diameter is 3.5 mm or larger, according to Sandri et al,8 and in 86% of veins if their diameter is 3.9 mm or larger, according to Labropoulos et al.24 Perforating veins, like any other vessel, have anatomic features corresponding to their specific hemodynamic function; however, this still remains undefined.2,3 The evaluation of perforator hemodynamics in the current study includes all the aforementioned parameters,


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Fig 5. A, Mean velocity and B, venous volume (median and interquartile range) during the first second of outward perforator flow on release of manual distal leg compression in 265 perforators, across the spectrum of chronic venous insufficiency. Incompetent perforators are stratified according to CEAP classes. A, Incompetent versus competent perforators, P < .0001; mean velocity CEAP3-6 or CEAP3-4 versus CEAP1-2, P < .001. B, Incompetent versus competent perforators, P < .0001; venous volume CEAP3-6 or CEAP3-4 or CEAP5-6 versus CEAP1-2, P < .009.

but mainly depends on the perforator flow velocities generated on the release of manual compression distal to the perforator site, which are obtained by insonating their lumen with duplex scanning. We found that perforator incompetence is characterized not only by longer reflux times and larger lumens, supporting recent reports, but also by higher peak (by 117%) and mean (by 50%) flow velocities, and subsequently a bigger mean volume flow. The median Q and VVoutward of incompetent perforators exceeds those of competent ones by 158.3% and 1796.2%, respectively; these numbers are explicable by consideration of the 27% bigger median diameter and 525% longer reflux times of incompetent perforators. The perforator MVs attained on the release of leg compression are equivalent to or higher than those generated within the common femoral artery,28,29 whereas the Q during the first second of reflux is comparable with or higher than that in the popliteal artery of healthy sitting individuals.30,31 These flow velocities, combined with a flow pulsatility that is equivalent to or higher than that in the peripheral arteries of patients with claudication,30,31 indicate that the rheologic conditions generated within the lumens of incompetent perforating veins simulate those in the peripheral arterial conduits. We found no significant differences in the Q, MV, and

duration of reflux of incompetent perforators between those in limbs stratified as CEAP1-2 and those in CEAP3-4 or CEAP5-6. However, incompetent perforators in CEAP3-4 had higher PVs (P = .024) than those in CEAP12 and much higher VVoutward (by 154%), indicating some change in their function with increasing CVI severity, which is probably mediated by higher early shear-stress and venous volumes expelled into the extrafascial circulation. To examine the hemodynamic function of perforators during the early reflux, we compared their performance during the first second after the release of manual distal leg compression. The differences between competent and incompetent perforators were very significant during the first second of reflux (P < .0001), with an incremental change in all main hemodynamic parameters from CEAP1-2 to CEAP3-4 through CEAP5-6. The mean velocity and volume flow during the first second increased by 92% and 130% from CEAP1-2 to CEAP3-4 (both P < .007), and increased further from CEAP3-4 to CEAP5-6, respectively. This was reflected similarly in the 1-secondVVoutward, which increased by 130% from CEAP1-2 to CEAP3-4 (P = .003) and further from CEAP3-4 to CEAP5-6. These findings suggest that the hemodynamic function of incompetent perforators is graded according to CVI severity, reflecting the overall venous hemodynamic deteriora-

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Fig 6. A, Volume flow and B, flow pulsatility (median and interquartile range) during the first second of (outward) perforator flow on release of manual distal leg compression in 265 perforators, across the spectrum of chronic venous insufficiency. Incompetent perforators are stratified according to CEAP classes. A, Incompetent versus competent perforators, P < .0001; CEAP3-6 or CEAP3-4 or CEAP5-6 versus CEAP1-2, P < .009. B, Incompetent versus competent perforators, P < .0001; CEAP5-6 versus CEAP1-2, P = .015.

tion that is known to occur with CEAP class.7,11,32,33 The enhanced hemodynamic differences between competent and incompetent perforators across the disease spectrum at the early phase of reflux indicate that it is probably their early hemodynamic function that determines their clinical impact on the leg, rather than their hemodynamic function in the entire reflux time. Our data confirmed that overall incompetent perforators have a significantly larger diameter than the competent ones.8,24 When stratified according to CEAP classification, incompetent perforators in classes 1 to 2 had diameters that were not significantly different than those in classes 3 to 4 or 5 to 6. On the contrary, incompetent thigh perforators (classes 1-6) demonstrated much larger diameters than those in the calf overall, particularly the upper and middle thirds (both significantly different P < .04), confirming recent accounts.8 Also, incompetent perforators in the lower third of the calf had larger diameters than those in either the middle or upper calf thirds. These differences in the diameter of incompetent perforating veins were not associated with discrepancies in either the duration or the mean and peak velocities of outward flow, nor in the time to peak velocity. However, significantly higher levels of Q and VVoutward were documented in incompetent thigh perforators on the release of manual distal leg compression. Higher Q and VVoutward were also documented during the first second of outward flow in

incompetent distal third calf perforators, compared with those at the middle and upper calf thirds. If the amounts of outward flow and venous volume displaced from the subfascial to the extrafascial space are a measure of the hemodynamic significance of an incompetent perforator and the diameter is a reflection of the shear-stress on the perforating vessel wall, the aforementioned findings indicate that the thigh and distal calf perforators may be of the most significance hemodynamically. This is in accord with published data, which considered thigh perforators to be a significant source of gross hemodynamic failure after superficial vein surgery,34 and in support of the clinical observation that venous ulcers most likely develop at the distal third of the calf (ankle) medially.35 Perforator flow pulsatility, the equivalent of arterial pulsatility index and a measure of downstream flow resistance, was significantly higher (3 times) in perforator competence than in incompetence (CEAP1-6). FP in competent perforators was similar to that in the popliteal artery of healthy subjects lying horizontal,30 indicating that the shear-stress generated in perforators on the release of distal manual leg compression is equivalent to that in the arterial system. This, in view of the compliant vein walls and the high flow velocities, suggests that the specific mechanism regulating outward flow, either valvular or functional, must be structurally stiff enough to enable perforators to operate in conditions similar to those of the


arterial circulation. Based on MV, reflux times, diameter, and VVoutward, the dynamic and kinetic energy absorbed by extrafascial tissues in perforator incompetence is on average 20 times that in competence. Competent perforators demonstrate rapid attenuation in outward flow velocity occurring within a 0.1 seconds, the median time to peak velocity, with complete control of flow being achieved within a median reflux time of 0.32 seconds. Attenuation of outward flow through incompetent perforators within a median time of 0.2 seconds, irrespective of anatomic site and CVI class, indicates that their early function is maintained despite their failure to control venous outflow in 0.5 seconds, the standard point of competence. Accepting that unimpeded outward flow would be characterized by a much longer time to peak velocity, the early attenuation of flow in perforator incompetence may indicate the presence of some residual valvular function or may be attributable to the elastic recoiling of the vascular bed to which the refluxing venous volume is directed. This study has shown that incompetent perforators in the presence of deep venous reflux have a significantly higher PV (by 25%) and Q (by 85%), bigger VVoutward (151%), and a larger diameter (by 35%) than incompetent perforators in limbs without deep venous reflux, suggesting that whatever their actual hemodynamic role in CVI may be, it is significantly enhanced in the presence of deep vein insufficiency. We demonstrated bidirectional flow in 77% of competent perforators on manual distal leg compression/sudden release, which is not different from that in incompetent perforators (68.3% to 82.4% for CEAP1-6). Unidirectional flow, representing the remaining cases, was evenly distributed in the CVI spectrum (CEAP0-6). The pattern of inward flow on manual distal leg compression and outward flow on its release was also distributed evenly in classes 1 to 6 in perforator incompetence. Differences in the flow direction during manual distal limb compression between competent and incompetent perforators were not found. On release of distal leg compression, 70% of competent perforators and almost all incompetent ones demonstrated flow from the deep to superficial veins. Therefore, across the CVI spectrum, incompetent perforators have predominantly bidirectional flow (> 68.3%), inward on distal leg compression and outward on its release, and are different from the competent perforators only in the higher percentage of deep-to-superficial flow on release of compression (P < .001). Our findings are different from earlier reports, which indicated either increase of unidirectional flow with CEAP class24 or small percentages of outward flow in competent perforators.8,10,24 Velocity spectra in the current study were retrieved with real-time gated-Doppler, placed within and parallel to the longitudinal axis of perforators, and imaged in real time. The clinical importance of investigated velocity parameters was assessed by means of their correlation with CEAP classes, diameter, and reflux times. MV, Q, VVoutward, and PV correlated significantly with each other, and Q correlated with the perforator diameter. The 1-second-MV and FP

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correlated well with CVI severity; however, neither the perforator diameter nor reflux times and remaining investigated hemodynamic parameters correlated with the CEAP classes, indicating that CVI severity does not depend primarily on the function of isolated perforators, but is the overall product of a multitude of hemodynamic impairments occurring simultaneously in the venous system. In addition to an increase in diameter, incompetent perforators are characterized by significantly higher mean and peak flow velocities, volume flow, and venous volumes displaced outward, and a lower flow pulsatility; their hemodynamic function deteriorates significantly in the presence of deep reflux. Discrepancies in early reflux enable a better hemodynamic stratification of incompetent perforators in CVI classes. In situ hemodynamics enabling quantification of perforator function can be used in identifying the clinically relevant perforators and in determining the impact of surgery. REFERENCES 1. Linton RR. The communicating veins of the lower leg and the operative technique for their ligation. Ann Surg 1938;107:582-93. 2. Ruckley CV, Makhdoomi KR. The venous perforator. Br J Surg 1996;83:1492-3. 3. Gloviczki P, Bergan JJ, Rhodes JM, Canton LG, Harmsen S, Ilstrup DM. Mid-term results of endoscopic perforator vein interruption for chronic venous insufficiency: lessons learned from the North American subfascial endoscopic perforator surgery registry. The North American Study Group. J Vasc Surg 1999;29:489-502. 4. Townsend J, Jones H, Williams JE. Detection of incompetent perforating veins by venography at operation. BMJ 1967;3:583-5. 5. Sarin S, Scurr JH, Smith PD. Medial calf perforators in venous disease: the significance of outward flow. J Vasc Surg 1992;16:40-6. 6. Mozes G, Gloviczki P, Menawat SS, Fisher DR, Carmichael SW, Kadar A. Surgical anatomy for endoscopic subfascial division of perforating veins. J Vasc Surg 1996;24:800-8. 7. Delis KT, Ibegbuna V, Nicolaides AN, Lauro A, Hafez H. Prevalence and distribution of incompetent perforating veins in chronic venous insufficiency. J Vasc Surg 1998;28:815-25. 8. Sandri JL, Barros FS, Pontes SP, Jacques C, Salles-Cunha SX. Diameter-reflux relationship in perforating veins of patients with varicose veins. J Vasc Surg 1999;30:867-74. 9. Porter JM, Moneta GL, An International Consensus Committee on Chronic Venous Disease. Reporting standards in venous disease: an update. J Vasc Surg 1995;21:635-45. 10. Myers KA, Ziegenbein RW, Zeng GH, Matthews PG. Duplex ultrasonography scanning for chronic venous disease: patterns of venous reflux. J Vasc Surg 1995;21:605-12. 11. Labropoulos N, Delis K, Nicolaides AN, Leon M, Ramaswami G. The role of the distribution and anatomic extent of reflux in the development of signs and symptoms in chronic venous insufficiency. J Vasc Surg 1996;23:504-10. 12. Weingarten MS, Czeredarczuk M, Scovell S, Branas CC, Mignogna GM, Wolferth CC. A correlation of air-plethysmography and color flow assisted duplex scanning in the quantification of chronic venous insufficiency. J Vasc Surg 1996;24:750-4. 13. Van Rij AM, Solomon C, Christie R. Anatomic and physiologic characteristics of venous ulceration. J Vasc Surg 1994;20:759-64. 14. Welch HJ, Young CM, Semegran AB, Iafrati MD, Mackey WC, O’Donnell TF Jr. Duplex assessment of venous reflux and chronic venous insufficiency: the significance of deep venous reflux. J Vasc Surg 1996;24:755-62. 15. Browse NL, Burnand KG. The cause of venous ulceration. Lancet 1982;2:243-5. 16. Wilkinson GE, Maclaren IF. Long term review of procedures for venous perforator insufficiency. Surg Gynecol Obstet 1986;163:117-20.


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17. Cikrit DF, Nichols WK, Silver D. Surgical management of refractory venous stasis ulceration. J Vasc Surg 1988;7:473-8. 18. Jugenheimer M, Junginger T. Endoscopic subfascial sectioning of incompetent perforating veins in treatment of primary varicosis. World J Surg 1992;16:971-5. 19. Akesson H, Brudin L, Cwikiel W, Ohlin P, Plate G. Does the correction of insufficient superficial and perforation veins improve function on patients with deep vein insufficiency? Phlebology 1990;5:113-23. 20. Bjordal RI. Circulation patterns in incompetent perforating veins in the calf and in the saphenous system in primary varicose veins. Acta Chir Scand 1972;138:251-61. 21. Stacey MC, Burnand KG, Layer GT, Pattison M. Calf pump function in patients with healed venous ulcers is not improved by surgery to the communicating veins or by elastic stockings. Br J Surg 1988; 75:436-9. 22. Burnand KG, O’Donnell TF, Thomas ML, Browse NL. The relative importance of incompetent communicating veins in the production of varicose veins and venous ulcers. Surgery 1977;82:9-14. 23. Zukowski AJ, Nicolaides AN, Szendro G, Irvine A, Lewis R, Malouf GM, et al. Haemodynamic significance of incompetent calf perforating veins. Br J Surg 1991;78:625-9. 24. Labropoulos N, Mansour MA, Kang SS, Gloviczki P, Baker WH. New insights into perforator vein incompetence. Eur J Vasc Endovasc Surg 1999;18:228-34. 25. van Bemmelen PS, Bedford G, Beach K, Strandness DE. Quantitative segmental evaluation of venous valvular reflux with duplex ultrasound scanning. J Vasc Surg 1989;10:425-31. 26. Hanrahan LM, Araki CT, Fisher JB, Rodriguez AA, Walker TG, Woodson J, et al. Evaluation of the perforating veins of the lower extremity using high resolution duplex imaging. J Cardiovasc Surg (Torino) 1991;32:87-97.

27. Lees TA, Lambert D. Patterns of venous reflux in limbs with skin changes associated with chronic venous insufficiency. Br J Surg 1993;80:725-8. 28. Fronek A, Coel M, Bernstein EF. Quantitative ultrasonographic studies of lower extremity flow velocities in health and disease. Circulation 1976;6:957-60. 29. Lewis P, Psaila JV, Morgan RH, Davies WT, Woodcock JP. Common femoral artery volume flow in peripheral vascular disease. Br J Surg 1990;77:183-7. 30. Delis KT, Nicolaides AN, Stansby G. Effect of posture on popliteal artery hemodynamics. Arch Surg 2000;135:265-71. 31. Delis KT, Labropoulos N, Nicolaides AN, Glenville B, Stansby G. The effect of intermittent pneumatic foot compression on popliteal artery haemodynamics. Eur J Vasc Endovasc Surg 2000;19:270-8. 32. Welkie JF, Comerota AJ, Katz ML, Aldridge SC, Kerr RP, White JV. Hemodynamic deterioration in chronic venous disease. J Vasc Surg 1992;16:733-40. 33. Ibegbuna V, Delis KT, Nicolaides AN. Distribution of venous reflux and haemodynamic changes associated with CEAP classes (1–6). Objective: to determine in limbs with chronic venous disease, reflux patterns and haemodynamic changes associated with CEAP classes (1–6). Presentation at the 11th American Venous Forum Annual Meeting; 1999 Feb 18–21; Dana Point, Calif. 34. Papadakis K, Christodoulou C, Christopoulos D, Hobbs J, Malouf GM, Grigg M, et al. Number and anatomical distribution of incompetent thigh perforating veins. Br J Surg 1989;76:581-4. 35. Stansby G, Delis K. The case for endoscopic perforator surgery. In: Earnshow JJ, Murie JA, editors. The evidence for vascular surgery. Shropshire (UK): TFM Publishing, JVRG; 1999. p. 145-9. Submitted Feb 17, 2000; accepted Oct 30, 2000.

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