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J Appl Physiol 102: 1105-1112, 2007. First published November 16, 2006; doi:10.1152/japplphysiol.00912.2006
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Estimation of the functional role of arterial pathways to the buttock circulation during treadmill walking in patients with claudication

Vincent Jaquinandi,1,2 Pierre Abraham,1,2 Jean Picquet,3 Francine Paisant-Thouveny,4 Georges Leftheriotis,1,2 and Jean-Louis Saumet1,2

1Physiologie, Explorations Fonctionnelles Vasculaires et d'Effort; 2Laboratoire de Physiologie, UMR-Centre National de la Recherche Scientifique 6214-Institut National de la Santé et de la Recherche Médicale 771; 3Service de Chirurgie Vasculaire et Thoracique, and 4Radiologie C, Centre Hospitalier Universitaire, Angers Cedex 9, France

Submitted 18 August 2006 ; accepted in final form 7 November 2006


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
The aim of the study was to estimate the functional contribution of the arterial inflow pathways to the pelvic circulation during walking in patients with stage 2 lower extremity arterial disease. Transcutaneous oxygen pressure (PtcO2) changes during exercise can be used to estimate the severity of regional blood flow impairment while walking. Seventy patients with stable lower limb claudication were studied using a multivariate linear regression model. The relationship between exercise-induced buttock PtcO2 changes, the ipsilateral calf PtcO2 changes, and the arterial diameters of the pelvic arteriographic pathways were analyzed. The ipsilateral hypogastric and lumbar pathway, as well as the ipsilateral calf PtcO2 changes, were the only variables significantly related to buttock PtcO2 changes (r = 0.47; P < 0.001). Their normalized respective contribution to the regressive model was 39%, 19%, and 18%. None of the contralateral hypogastric, mesenteric, and sacral pathways or pathways stemming from the external iliac artery showed significant correlation to buttock PtcO2 changes. The ipsilateral hypogastric and ipsilateral lumbar pathways are the major pathways responsible for the functional buttock blood flow supply during walking. The role of contralateral hypogastric, inferior mesenteric, and median sacral pathways and arteries distal to the internal iliac trunk is negligible in the normal or compensatory blood flow supply. Distal PtcO2 decrease at exercise aggravates proximal PtcO2 decrease, possibly through the occurrence of a "steal phenomenon" of distal over proximal circulation during walking.

peripheral arterial disease; hemodynamic; regional blood flow; exercise; pelvis

THE AORTA and the common iliac and internal iliac arteries are the direct pathway by which blood flow is supplied to the pelvic organs and to buttock muscles and skin. However, the pelvic circulation is a very complex functional network with multiple potential collateral pathways. Many arteries could contribute to the blood flow supply to the buttocks and pelvic organs (see Fig. 1), especially in case of lesions impairing the flow through the hypogastric pathway, assumed to be the direct and main pathway for blood supply. These potential collateral routes include the inferior mesenteric and median sacral arteries, the contralateral internal iliac artery, and the ipsilateral lumbar and circumflex arteries. Previous reports have focused on the description of the pelvic vascular anatomy (14) or on the effect of acute surgical occlusion of internal iliac arteries, in limited number of subjects (17, 20). Indeed, the role of collaterals may be different in the acute or chronic settings of blood flow impairment, and functional differences may also exist between blood flow at rest and during exercise. A wide interindividual variability in the collateral vessels involved is also expected and cannot satisfactorily be estimated in small groups.


Figure 1
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  		Fig. 1. Representation of the different segments used for the analysis. For abbreviations, see Arteriography. Note that the distal part of the external iliac artery has been included in the inferior circumflex artery.

 
We have previously shown that recording of transcutaneous oxygen pressure (PtcO2) with surface electrodes on buttocks may provide useful information as to the presence of lesions in the aorta and common and internal iliac arteries leading to the hypogastric claudication (2).The amplitude of the PtcO2 decrease during exercise at the calf level is dependent on the number of consecutive lesions in the arterial tree (1), suggesting that the PtcO2 exercise-induced changes can provide an index of the severity of the blood flow impairment in the area of interest. The aim of the present work was to use a regression model to determine the relationship between different arterial pathways as observed on arteriography and exercise-induced PtcO2 changes, assumed to reflect exercise-induced regional blood flow impairment (RBFI) to the buttocks and calves bilaterally. We hypothesized that this model can be useful in estimating the respective average functional contribution of the different arterial inflow pathways to the buttock blood supply at exercise under normal and chronic compensatory conditions. We hypothesized that 1) the statistical weight of the hypogastric pathway in the model (its relative role in the estimated ipsilateral buttock flow impairment) would not reach 50%, consistent with the relatively good tolerance of unilateral iliac occlusion observed in clinical studies; 2) differences might be observed from previous reported observations of acute arterial clamping, due to the chronic nature of ischemia; specifically, we expected that arteries distal to the internal iliac arterial trunk would not participate in the buttock blood flow supply at exercise; and 3) the presence of a distal (calf) ischemia would limit the duration of exercise, preventing proximal ischemia to occur, resulting in an inverse relationship between buttock and calf PtcO2 changes.

Few studies have analyzed the respective functional hemodynamic contribution of various pathways to the buttock circulation in humans (17, 20). The major goals of the present study are to 1) integrate the different pathways into a single regressive model; 2) study a large number of subjects, thus accounting in part for interindividual variability; 3) analyze the functional response during exercise; and 4) provide estimation of buttock RBFI during exercise. To the best of our knowledge, none of these four approaches has been considered before.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Population.   A retrospective analysis was performed on patients referred to our laboratory for exercise PtcO2 testing between 2000 and 2006. Most patients were referred for claudication of questionable vascular origin or for systematic investigation before vascular surgery as a part of the Evaluation Objective des Ischémies Proximales (EOIP) Study (EOIP National Institutes of Health Database: NCT-00152737). In this population, we selected patients who had a diagnostic arteriography performed according to our standard procedure within 3 mo of the PtcO2 exercise test. Patients with an abdominal aortic aneurysm >40 mm or a history of vascular surgery or angioplasty between the exercise test and arteriography were excluded.

This study was conducted according to the principles outlined in the Declaration of Helsinki and approved by the Institutional Review Board of Angers. Informed written consent was obtained from the patients. Seventy patients (59 men, 11 women) were included in this study. The average (mean and SD) age, height, and weight were 62 yr (SD 11), 169 cm (SD 8), and 71 kg (SD 12). Estimated walking distance was 264 m (SD 266). Maximal walking distance on treadmill was 280 m (SD 284). All patients suffered stable claudication for a minimum of 3 mo and an average of 3 yr. Treatments included antiplatelet agents (n = 44), vasodilator drugs (n = 41), hypocholesterolemic drugs (n = 26), antidiabetic drugs (n = 13), and beta-blockers (n = 6), and all medications were taken at the time of the study.

Exercise procedure and PtcO2 measurements.   Treadmill tests were performed by a trained operator with a standard method extensively described elsewhere (2, 5) using a 10% slope at 3.2 km/h (speed being progressively reached in 4 min). Walking was stopped at patient's request. In the absence of limiting claudication, the test was arbitrarily stopped after 20 min of walking (walking distance ~1,000 m). For PtcO2 measurements, we used five PtcO2 devices (TINA TCM3 Radiometer, Copenhagen, Denmark) with probes heated to 44.5°C to improve transcutaneous oxygen diffusion. Recorded values were automatically temperature corrected to 37°C. A one-point calibration to air was performed before each experiment. The calibration value was set according to the actual barometric pressure. Before fixing the probes, the skin was cleansed by gently rubbing the skin with gauze. Probes were positioned on the chest, on each buttock (4–5 cm behind the bony prominence of the trochanter), and on each calf (2–4 cm above the ankle). A pretest heating period of 15–20 min in the standing position without walking was required to allow stable resting values to be reached. The data were recorded on a computer via an analog-to-digital converter (Biopac System) with a sample rate of 2 Hz and 16 bits. Moving averaging and resampling over 5-s intervals were performed on raw data to reduce the electronic noise of the signal. PtcO2 values were recorded for 2 min in the standing position before the treadmill was started, during the walking period, and for 10 min in the standing position following the end of the exercise test.

Arteriography.   All digitized diagnostic arteriograms were performed by the standard method required for the study: 1) catheterization of the femoral artery via the Seldinger technique and 4-Fr pigtail catheters, and 2) presence of at least three series of images in the arteriogram (frontal view centered on the lower aorta, left oblique anterior view, and right oblique anterior view). Exams were reanalyzed by pairs of investigators who were blinded to the results of the PtcO2 exercise tests. Three sessions of common reading were performed at the beginning of the study to homogenize the methods for readings. Common sessions were also organized during the study to discuss difficult interpretations and maintain homogeneous readings.

For the analysis, the arterial tree was divided into segments as presented in Fig. 1. Analyses and measurements were made using the advantage Workstation 4.1–6 (General Electric, Buc/Yvette, France). On the frontal view, measurements were done on the inferior mesenteric artery, down to its projection on the aorto-iliac bifurcation; the aorta above (aorta 1) and below (aorta 2) the fourth lumbar artery; the largest fourth or fifth lumbar arteries on both sides, until their respective first branch of division; and the median sacral artery, down to the sacrum extremity. Oblique views were used to study the common and external iliac arteries; the internal iliac arteries until their first major branch of division; the iliac circumflex artery; and the inferior circumflex arteries.

For each patient, the external diameter (number of pixels) of the 4-Fr catheter was measured at the center of the image to estimate the radiological enlargement on the frontal and oblique views. Radiological enlargement was assumed to be the same on both oblique views. For each arterial segment, the maximal and minimal arterial diameters of the arteries were measured as the number of pixels and then converted to millimeters according to individual enlargement estimated from catheter measurement on the corresponding view. If an artery was completely occluded, its minimal diameter was noted as 0 mm and its maximal diameter noted "missing value." Variability of diameter measurement within the study between two observers was measured to be lower than 10% from 18 double-blinded analyses.

Analysis of the results.   The PtcO2 values at rest were the mean of PtcO2 values over the 2 min of the resting period (24 intervals of 5 s). At each 5-s interval, the absolute PtcO2 change from rest at the chest level was subtracted from the corresponding absolute value of each limb PtcO2 change. By design, this decrease from rest of oxygen pressure (DROP) is zero at rest, is a negative value during exercise and recovery, and is expressed in millimeters of Hg. The lowest negative value resulting from this calculation during or in the 10 min following exercise was used. Calculation of DROP and determination of its minimal value was automated through a custom-made computerized program, automatically correcting for eventual small probe drift, such as the last DROP value of the recovery period will be zero. As previously reported (5) the transcutaneous gradient is unpredictable but assumed to remain stable over time within each experiment. Then DROP calculation is independent of the transcutaneous muscle-to-surface gradient. It is likely that the DROP value reflects not only blood flow but perfusion relative to the oxygen demand of the tissue. Therefore, DROP should be considered as being an indication of the oxygen supply/demand ratio of the small region of tissue underlying the electrode. Using the same exercise in all patients, the oxygen demand was assumed to be constant in all subjects, and thus a decrease of PtcO2 is assumed to principally rely on oxygen supply in the present study. Furthermore, in case of exercise-induced systemic hypoxemia, a simultaneous chest and limb PtcO2 decrease during exercise will result in DROP remaining unchanged. Then a DROP decrease is expected to result mainly, if only, from RBFI. DROP variability was estimated to be 15% in test-retest experiments (5). In normal subjects or in the absence of vascular lesions in patients with peripheral arterial disease, DROP during exercise remains close to zero, whereas, at least at the level of calves, DROP decreases with the number of successive lesions on the arterial tree. The lowest negative values for DROP reflect more severe RBFI during exercise (1). Each test resulted in four DROP values: two at the buttock level (DROPbuttock) and two at the calf level (DROPcalf).

For the analysis of arteriography, various pathways were defined to represent the anatomic routes to the buttock circulation as described in the literature. Pathways are composed of different combinations of the arteries analyzed. Table 1 summarizes the arteries involved in each pathway. For each buttock, we selected seven pathways that are likely to participate to the pelvic circulation. These pathways are the median sacral pathway, the inferior mesenteric pathway, the ipsilateral hypogastric pathway and contralateral hypogastric pathway, the ipsilateral infrarenal lumbar pathway, the ipsilateral circumflex iliac pathway, and the ipsilateral inferior circumflex pathway.


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  		Table 1. Arteries involved in each pathway for the calculation of lowest minimal diameter

 
The percent stenosis (ratio of minimal to maximal diameter) is generally used to analyze lesions in arteriography. The advantage of this ratio is that it is independent of the radiological enlargement. Conversely, a thin or hypoplasic pathway will have the same statistical weight in the model as a large pathway, whereas it is clear that they do not provide comparable flow to the underlying tissues. For example, the use of absolute diameter and not percent stenosis may account for the increase in size of the collateral pathway (e.g., the mesenteric pathway) in case of occlusion of the ipsilateral hypogastric pathway. Then, in the models, we used the lowest minimal diameter encountered on each pathway (LMD) rather than the percent diameter stenosis of the arteries.

Statistical analyses.   For the whole statistical analysis, DROPbuttock was used as the variable to be explained by the models used. A monovariate analysis of the relationship between DROPbuttock and DROPcalf and between DROPbuttock and each of the seven studied pathways was performed. For this monovariate analysis, we used both the DROPbuttock raw value and a log-transformation of the absolute DROPbuttock value to test whether a nonlinear model should be preferred.

Since a monovariate analysis provides no information about the respective role of the explanatory variables in the DROPbuttock value, and since the seven pathways are not independent variables (one artery may be included in different pathways), a multivariate linear regression with a step-by-step analysis was performed (SPSS 12.0.1; SPSS, Chicago, IL). The multivariate model used tested the LMD of all the seven composite pathways defined in Table 1, as well as ipsilateral DROPcalf value, as "explanatory" variables. Then the mathematical model was of the following type: DROPbuttock = betacalf x DROPcalf + betaMes x LMDMes + betaSac x LMDSac + betaLum x LMDLum +... + betaInf x LMDInf, where the beta coefficient for each explanatory variable is an estimation of the relative participation of explanatory variable to the variable to be explained by the model, as in any multivariate linear regressive model. Beta coefficients were automatically normalized to percent values, providing an estimation of the relative "weight" of the corresponding variable in the model. We assumed that a positive beta for one pathway would suggest that this pathway is providing blood to the buttock in the normal situation and that its alteration (low LMD) result in regional blood flow impairment (low DROPbuttock). On the contrary, a negative beta along a pathway would suggest that the arteries along this pathway act as a collateral pathway (large LMD) in case of exercise-induced blood flow impairment (low DROPbuttock). For DROPcalf, a negative beta would indicate that the presence of a distal blood flow impairment (low DROPcalf) would limit the decrease of proximal DROPbuttock.

The statistical significance of beta (P value) can be regarded as a mean to estimate the reliability of the pathway participation in the model.

For all statistical tests, a two-sided P < 0.05 was used to indicate statistical significance. Results are presented as mean (SD; minimal value/maximal value).

The calculation of the number of subjects to be included was performed to include a minimum of 15 observations per tested explanatory variable included in the regression model. According to the number of variables to be included (7 pathways and ipsilateral DROPcalf), 120 observations (60 patients) or more were required.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
PtcO2 resting values before exercise were 77 mmHg (SD 11; 45/103) and 77 mmHg (SD 12; 44/98) on the right and left buttocks, respectively, and were 78 mmHg (SD 14; 37/108) and 79 mmHg (SD 12; 48/104) on the right and left calves, respectively. Resting value for chest PtcO2 was 73 mmHg (SD 13; 40/104). On the average, following the treadmill test, DROPbuttock values were –23 mmHg (SD 15; –73/–2) and –19 mmHg (SD 11; –56/–3) on the right and left buttocks, respectively, and DROPcalf values were –22 mmHg (SD 15; –70/–1) and –21 mmHg (SD 15; –60/–3) on the right and left calves, respectively. A typical example of exercise test result is presented in Fig. 2A.


Figure 2
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  		Fig. 2. A: transcutaneous oxygen pressure (PtcO2) measurements at exercise for patient PC. Minimal values for decrease from rest of oxygen pressure (DROP) are –8, –25, –32, and –33 on the right calf, left calf, right buttock, and left buttock, respectively. B: frontal view centered on the lower aorta for patient PC. The patient walked 500 m and stopped for left buttock and calf pain. The other views used for measurements are not presented. The linear image at the origin of the right common iliac arteries is resulting from subtraction of bowel interposition, and only the left common iliac artery shows a long severe stenosis (arrows).

 
Maximal diameters of each artery studied are reported in Table 2. As expected, the maximal diameters of the arteries decreased from the aorta to the external iliac artery. Extreme values were observed as a result of arterial aneurysms at the level of the aorta (2 patients) or the right hypogastric artery (1 patient). Although the mean values were within normal, extreme maximal values for mesenteric, lumbar, and circumflex arterial diameters could reach 7 mm or more as a consequence of collateral pathway development in some patients with chronic buttock ischemia resulting from occlusion of the hypogastric pathway. Minimal diameters of each artery studied are reported in Table 3. As shown, no patient had a complete occlusion of the terminal aorta; however, one patient suffered a severe subocclusion. Table 4 summarizes the LMD on the different composite pathways. In brief, patent mesenteric pathway and right and left lumbar pathways were found in 58, 63, and 64 patients, respectively, whereas a patent sacral pathway was observed in only 17 patients. Occlusion of the hypogastric pathway was found on both sides in 3 patients and on one side in 21 patients. Most of the patients (66 of 70) had a patent circumflex iliac pathway on one (n = 28) or both (n = 38) sides, whereas only 54 of the 70 patients had patent femoral circumflex pathway on one (n = 22) or both (n = 32) sides. As shown, the hypogastric pathway average LMD is low, due to the high prevalence of lesions on the common and internal iliac arteries in this population. An example of arteriography is presented in Fig. 2B, corresponding to the exercise test shown in Fig. 2A. (Oblique views are not shown for simplification.) Surprisingly, the right hypogastric pathway showed only a mild stenosis, whereas right DROPbuttock was low. In this patient, one possible assumption would be that it was due, at least in part, to the total absence of lumbar and circumflex arteries on the right side.


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  		Table 2. Maximal diameter of each studied artery

 

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  		Table 3. Values for minimal diameter of each studied artery

 

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  		Table 4. Lowest minimal diameter on each of the studied pathways included in the model

 
Results for the univariate analysis for the raw and log-transformed DROPbuttock with the studied explanatory variables are presented in Table 5. These suggest that the log transformation of DROPbuttock did not improve the correlations observed. Results for the multivariate linear regression model found only three variables for which beta reached significance [the ipsilateral hypogastric pathway (P < 0.0001) and lumbar pathway (P < 0.05) and the ipsilateral DROPcalf (P < 0.05)]. The r coefficient of the model with these three variables was 0.47 (P < 0.001). None of the other variables reached statistical significance for beta. The contralateral hypogastric pathway LMD was positively associated to DROPbuttock (P = 0.09). Both the mesenteric pathway and the sacral pathway showed an inverse but nonsignificant correlation (negative beta) with DROPbuttock (P = 0.57 and P = 0.33, respectively). None of the pathways stemming from the external iliac artery showed significant beta values, with beta being negative in both cases. The histogram of normalized beta values estimated from the model is presented in Fig. 3.


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  		Table 5. Results for the monovariate analysis with Spearman "r" coefficient and P for Spearman using raw DROPbuttock and log-transformed absolute DROPbuttock

 

Figure 3
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  		Fig. 3. Normalized beta values (%) resulting from the model to explain the DROPbuttock result. For the studied pathways (solid bars), a positive beta suggests that a smaller minimal diameter along the pathway is associated to more severe blood flow impairment at the buttock level. A negative beta value suggests that buttock blood flow impairment is associated to larger minimal diameter along the pathway. *P < 0.05.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
The study suggests that during exercise 1) the ipsilateral hypogastric pathway participation in buttock RBFI is <50%; 2) the ipsilateral lumbar pathway has a major role in the buttock blood flow supply, whereas the contralateral hypogastric, inferior mesenteric, and median sacral pathways do not compensate for chronic buttock RBFI; 3) arteries distal to the internal iliac trunk do not participate in arterial pelvic inflow at exercise, although it does not preclude that they may play a role on resting blood flow; 4) the presence of ipsilateral calf RBFI aggravates buttock walking-induced RBFI, likely through reversal of flow in circumflex arteries, and a "steal phenomenon" of distal over proximal circulation during walking.

Beyond the objective mathematical correlations that may exist between arterial minimal diameter and RBFI, it is clear that the causal interpretations of the relationships found are speculative. Nevertheless, results obtained from these interpretations are consistent with most of the previously published observations.

At the inferior mesenteric artery level, contradictory results are found from the literature with regard to the participation of this artery to the pelvic circulation (9, 18, 21). The median sacral artery is reported as a cause of endoleak after endovascular repair of aortic aneurysms (12) or as a collateral route to the occlusion of the common iliac artery (24). We observed an inverse, but nonsignificant, relationship between the LMD of both the inferior mesenteric and median sacral pathways and DROPbuttock in the present study. The observation by Lin et al. (21) that no correlation was found between the contralateral hypogastric artery patency and the occurrence of pelvic clinical ischemia seems contradictory with the observed increase in risk of claudication after bilateral compared with unilateral embolization of hypogastric arteries (23, 26). The contralateral hypogastric pathway did not reach statistical significance in the multivariate model, suggesting that, on average, it does not participate in the normal buttocks circulation.

Reversal of flow through patent infrarenal lumbar arteries is recognized as a frequent cause for acute endoleak in endoluminal treatment of aortic aneurysms (13), and these arteries are suggested (9) as efficient collateral pathways to internal iliac arterial occlusion. Our results confirm that ipsilateral infrarenal lumbar arteries play a functional role in providing blood to the buttock circulation in normal condition (a low LMD being significantly associated to buttock DROP) and thus are likely to protect against ischemia in the acute setting when patent. This is consistent with the radioanatomic observations of Hassen-Khodja et al. (14).

Multiple studies have documented the importance of arteries distal to the internal iliac artery in compensation for lesions in the ipsilateral internal iliac artery (10, 16, 19, 21, 25). Contrary to these results, arteries distal to the internal iliac trunk do not play a statistically significant role in our model. This might result from 1) the fact that we rarely observed isolated lesions of these arteries in our group, thus resulting in lesions in these arteries being eventually masked by the effect of lesions located in other pathways; 2) the acute vs. chronic setting of blood flow impairment; 3) the presence of lesions in the common and external iliac arteries in many patients of our group; and 4) the fact that we tested exercise-induced blood flow impairment and not resting stump pressure. Indeed, it cannot be excluded that these collateral pathways could contribute to the buttock blood flow supply at rest in the absence of lesions on the common and external iliac arteries but would preferentially participate to the distal circulation to thigh and calf in case of common or external iliac artery stenoses and during exercise. This latter point should be analyzed in perspective with the unexpected role of DROPcalf in the model. Our hypothesis was that severe distal RBFI (when present) would lead to early ending of the walking test and then would preclude the occurrence of buttock RBFI, but an inverse relationship between DROPbuttock and DROPcalf was not observed. It cannot be excluded that the positive relationship between DROPbuttock and ipsilateral DROPcalf is nothing more than an insight into the diffusion and severity of arterial lesions in the patients. Our hypothesis is that during walking, ipsilateral distal oxygen consumption increases (and thus blood flow requirement) and diverts flow away from the buttock to the exercising calf and thigh muscles through external iliac collaterals. This would be consistent with the apparent absence of a role of these collaterals in the pelvic blood flow supply found in our model, contrary to previous published results. This would also be consistent with the steal phenomenon observed in mongrel dogs by Takebe et al. (30) under exercise loading.

Study limitations.   From a technical point of view, PtcO2 reflects neither muscle ischemia nor intra-arterial pressure. Indeed, the oxygen demand of the skin at exercise is unchanged (except for thermoregulation with prolonged exercise). Thereafter, assuming the PtcO2 changes rely on changes in the oxygen demand/supply ratio, and although the gluteal arteries are terminal branches providing blood to both the muscles and skin at the buttock level, changes at the skin level may underestimate muscle changes. Penile pressure (11, 21) rectal oximetry (20), whole body thallium scintigraphy (27), or near-infrared spectroscopy (4, 29) could be suggested as alternative techniques. However, the two former choices would not allow for the differentiation of ipsilateral to contralateral collateral pathways, and the two latter cannot be used routinely.

Finally, the fact that the gluteal and ischiatic arteries were not included in the model to limit the number of observations can also have interfered with our results. Indeed, these arteries were previously suggested to "worsen pelvic arterial insufficiency by disrupting the collateral perfusion" (19) in case of occlusion of the internal iliac artery. As for the distal branches of the circumflex arteries, the inferior mesenteric artery, the lumbar arteries, or the median sacral artery, it was almost impossible to integrate the complex arterial anastomoses that can be observed in the pelvic anatomy.

The use of minimal diameter and not percent stenosis can appear as a pitfall for our approach. Normalization to the diameter of the catheter was expected to account for radiological enlargement and improve the accuracy of our measurements. Nevertheless, even using 6-Fr pigtail catheters, normalization to catheter diameter still results in a 15–20% variability in arterial diameter measurement (28). Variability is expected to be higher with smaller catheter diameters. At the aortic level, SDs of maximal diameters in our patients were, respectively, 19% and 26% of the mean. This is likely resulting from differences in patient body size. This is also in the same range as the variability expected as a result of the normalization to catheter size.

The choice of a linear regression model could be questioned due to the well-known nonlinear relationship between arterial stenosis and pressure drop through a single stenosis. A low LMD does not necessarily depend on a stenosis, but can result from a small or hypoplasic artery; on the other hand, affected pathways may present multiple severe consecutive lesions rather than a single lesion. In either case, it has not been proved that a nonlinear model is preferable. As a support to this assumption, we have tested the log transformation of the DROP values instead of raw data in the model. This has resulted in no improvement in the monovariate analyses and a lower correlation of the multivariate model (data not shown).

A population bias cannot be excluded. On the one hand, the proportion of men in the study is high. Thus it is not certain whether these results are as applicable to women where vessels are typically smaller. On the other hand, almost all the patients included in the model suffered from stage 2 claudication. It is possible that chronic development of major collateral pathways results in patients remaining asymptomatic. Studying only symptomatic patients could miss the more efficient pathways. This cannot be totally ruled out, and the regression model would require validation in another group of patients. Possibly related to the selection criteria, the prevalence of lesions on each studied pathway was not the same. This might result in one pathway associated to a high beta coefficient but remaining nonstatistically significant. It must be kept in mind that the present approach is only an estimation of the average role of the studied pathways. It is possible that in some patients "atypical" anatomic distribution may occur and that a specific pathway may play a major role at the individual level, although not reaching significance on a population study.

Perspectives.   These observations may have interesting clinical consequences. While deliberate or incidental occlusion of one or both of the internal iliac arteries during surgical or endovascular procedures may result in buttock claudication, deep organ ischemia such as colonic ischemia (20), or buttock cutaneous necrosis (15, 17, 22), it may also result in no complications (23, 31). Therefore, there still is controversy about whether deliberate occlusion of internal iliac arteries (as for pelvic hemorrhage or iliac aneurysms) is functionally deleterious (3, 6–9, 17). On the other hand, whether systematic revascularization of one or both of the internal iliac arteries is required during aorto-iliac or aorto-femoral bypass surgery is still under debate. Because of the aggravating role of DROPcalf on DROPbuttock observed in the present study, a steal phenomenon of distal over proximal circulation is likely during walking exercise. Thus it could be expected that, in patients suffering proximal and distal claudication with occlusion of either the common and internal iliac arteries or of the external and internal iliac arteries, aorto-femoral revascularization (without direct hypogastric revascularization) may improve the buttock's circulation in most cases. A better knowledge of the respective functional participation of the different possible pathways is helpful for planning the surgical or endoluminal approach of the pelvic arteries during vascular, gynecological, or oncological surgery. Whether the model could predict the risk of buttock ischemia and claudication or the benefit of surgery or angioplasty toward the hypogastric circulation will require further prospective experiments.


   GRANTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
ACKNOWLEDGMENTS
 REFERENCES
 
P. Abraham received a grant from the Centre National de la Recherche Scientifique. The study was promoted by the Centre Hospitalier Universitaire d'Angers and in part by PHRC03/01, Bourse Starter de la Société Française de Médicine Vasculaire, and the Bourse de Recherche en Angiologie supported by Sanofi-Aventis-BMS.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
REFERENCES
 
We thank Dr. P. Benharash (Stanford University) and S. Boyé (Radiometer) for help in correcting the grammar and style of the manuscript, Dr. B. Vielle for statistical advice, Drs. P. L'Hoste and P. Bouyé for advice, and W. Buisan and S. Desmas for technical help.


   FOOTNOTES
 

Address for reprint requests and other correspondence: P. Abraham, Physiologie, Explorations Fonctionnelles Vasculaires et d'Effort and Laboratoire de Physiologie, UMR-CNRS 6214-INSERM 771, Centre Hospitalier Universitaire, 2 rue Larrey, 49933 Angers Cedex 9, France (e-mail: piabraham{at}chu-angers.fr)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 

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