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Vascular and Interventional Radiology |
1 From the Department of Radiology, Kings College Hospital, Denmark Hill, London SE5 9RS, England (D.J.Q., P.G., P.S.S.); and Academic Department of Surgery, Guys Kings and St Thomas School of Medicine, London, England (R.A.) From the 2000 RSNA scientific assembly. Received April 5, 2002; revision requested June 12; revision received November 10; accepted December 10. Address correspondence to D.J.Q. (e-mail: dan.quinlan@consultoberon.com).
| ABSTRACT |
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MATERIALS AND METHODS: A retrospective review of 404 bilateral (808 limbs) lower limb venograms obtained from medical patients participating in a thromboprophylaxis clinical trial and found to be free of thrombus was performed. Venograms were evaluated according to predetermined criteria for the presence of duplication of vessels and inter- and intraindividual variations in venous anatomy. Variations were assessed with analysis of variance and
2 tests.
RESULTS: Two vessels were seen in the popliteal fossa on 337 (42%) of 808 venograms, and 41 (5%) were true duplicated popliteal veins. There were 253 (31%) duplicated superficial femoral veins (SFVs), with 12 (1.5%) being complex duplicated systems. Of 265 duplicated SFVs, 138 (52%) began in the midthigh region and 80 (30%), in the adductor canal region. The duplicated vessel was medial to the main SFV in 122 (46%), lateral in 131 (49%), and both (ie, triplications) in 12 (4.5%). The length of the duplicated SFV ranged from 1 to 35 cm; 615 cm was the most common length in 162 (62%) SFVs. There was no significant association between the incidence of anatomic variations and age or sex (P > .1). The presence of multiple vessels in one leg was strongly correlated with the probability of occurrence in the other leg (P < .001).
CONCLUSION: Variations in lower limb venous anatomy are common and have important implications for the US diagnosis of deep vein thrombosis.
© RSNA, 2003
Index terms: Veins, anatomy, 93.92 Veins, thrombosis, 93.751 Venography, 93.124
| INTRODUCTION |
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Variations in the anatomy of the lower limb venous system have been studied with use of cadavers, venography, and US, with differing results. In most traditional anatomy textbooks, the venous system of the lower limb is described as consisting of a continuous flow of veins without duplication (4). It has, however, been demonstrated that only one in six patients will have this normal venous anatomy (5). The major variation is seen in the superficial femoral vein (SFV) where, according to previous study findings, between 6% and 46% of patients have duplicated or multiple vessels (610). The next most common variation is with the popliteal vein (4). By having performed a large number of US andvenographic studies in our department, it is apparent that many patients have two or more vessels in the popliteal fossa, and a number of these are true duplications but many represent a high confluence of the tibial veins.
With the current reliance on US for the diagnosis of DVT, we believed there was a need for an extensive review of the venous anatomy of the lower limb. The availability of bilateral lower limb venograms, obtained in a standard manner from asymptomatic medical patients during a recent clinical trial, allowed the opportunity to assess the true anatomic variation of lower limb veins (11). Therefore, the purpose of our study was to retrospectively review bilateral venograms that were free of thrombus by evaluating the frequency and types of variations seen in venous anatomy.
| MATERIALS AND METHODS |
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Local ethics committee approval for the MEDENOX study was obtained in all participating centers (n = 60), and a detailed standard protocol for patient inclusion was followed. Patients with a history of DVT were excluded from the study. All patients provided informed consent to participate in the study and to the performance of bilateral venography. Ethics committee approval or informed consent was not required for the retrospective review of images, as the images were free of patient identification.
Venography
All venograms, although obtained at different centers, were obtained in a standardized manner, as defined by the protocol, by using the technique described by Rabinov and Paulin (12). A distal foot vein was cannulated, and contrast material was injected to opacify the deep veins. Images of the calf veins were obtained in three views: two oblique and one anteroposterior. Two views of the popliteal vein and one view each of the SFV, common femoral vein, and external and common iliac veins were also acquired. All centers used only nonionic iodinated contrast media, with no specific type stipulated in the protocol except that the iodine concentration had to be a minimum of 200 mg/mL and that the injected volume had to be a minimum of 60 mL per limb.
Only those bilateral venograms that were evaluable and found to be free of thrombus by the clinical trial central radiology reading committee (consisting of three experienced physicians) were included and assessed for variations in anatomy. To be classified as evaluable, the venogram had to demonstrate adequate contrast material filling of all the major veins. Venograms depicting thrombus were excluded from our study for two reasons. First, thrombus may potentially cause obstruction, which would result in a failure of contrast material to fill the veins and therefore not be visualized. Second, thrombus may cause formation of collateral vessels and, as a consequence, potentially giving the impression of vessel duplication. Venography is acceptable for the assessment of the anatomic position of vessels as long as adequate filling of the major vessels is achieved. In view of this, only high-quality venograms characterized by full and adequate contrast material filling of all the deep veins were evaluated.
Venogram Interpretation
Two teams of two readers (D.J.Q., P.S.S. and R.A., P.G.), each experienced in performing and interpreting venographic studies, reviewed all of the studies at a central reading station over a 4-day period. The final interpretation was reached by consensus of each pair of observers, with a four-reviewer consensus with respect to any particularly difficult interpretation. Prior to commencement of the study, a defined protocol was established according to anatomic definitions used in previous studies to correctly and consistently define the vessels. The observers underwent a period of training to develop a uniform standard definition of lower limb venous anatomy (8). For descriptive purposes, proximal implied a central (cranial or cephalad) location, whereas distal implied a peripheral (caudal) location. The proximal deep leg veins were defined as those central to the popliteal vein and the distal veins, as those peripheral to the popliteal vein.
Calf Veins
All calf (eg, peroneal, anterior and posterior tibial veins, gastrocnemius or muscular veins) and proximal vessels had to be clearly visualized in both limbs for the venogram to be eligible for inclusion in the study. In particular, we did not evaluate venograms that showed only partial filling of the calf veins. For each of the calf vessels, a record was made of whether they were paired (as is the classic appearance), triplicated, or single. The drainage of each calf vessel into other calf or popliteal vessels and the position of this confluence in relation to other vessels were recorded. Using this information, we classified how the calf vessels joined to form the trifurcation prior to the formation of the popliteal vein. The popliteal vein is described as a single vessel formed by the confluence of the anterior and posterior tibial veins, often at the distal border of the popliteus muscle, which become the SFV proximal to the adductor opening (4). We recorded visualization of the gastrocnemius vein and the position of drainage.
Popliteal Vein
For the popliteal vein, we recorded the number of vessels present in the popliteal fossa by counting the number crossing the knee joint space to be able to relate this to sonographic visualization during a routine US examination. Second, using the knee joint space as a reference point, we recorded the formation of the popliteal vein (as defined previously) as arising either distal to, proximal to, or at the level of the knee joint (Fig 1).
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Statistical Analysis
The age and sex of the patients were recorded. Variations in the anatomy of the lower limb veins were assessed centrally and recorded in a statistical database (SPSS 9.0 for Windows; SPSS, Chicago, Ill) and presented in a table form. The frequency distribution of multiple vessels was listed according to sex, and the mean age with SD was listed according to the number of vessels. To show the correlation between two legs in the presence of multiple vessels, data from two legs were listed in a paired format.
The probability of variations in venous anatomy was compared between limbs, sex, and age. The
2 test was used in the assessment of the association of sex with the variation of venous anomalies and the correlation between two legs in the presence of multiple vessels in the same patient. When the expected numbers of some cells were less than five, the neighbor categories were combined to avoid invalid comparison with the
2 test. The association between age and venous anomalies was tested by using analysis of variance. P values less than .05 were considered to indicate a significant difference (or association).
| RESULTS |
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Demographics
The mean age of the patients was 73.8 years (age range, 4193 years). There were 199 (49%) female patients, and there was no statistical difference in the incidence of venous anomalies attributable to age or sex (P > .1). Analysis of variations in the calf and popliteal and SFVs showed a strong correlation between the presence of multiple vessels in one leg and the probability of this occurring in the other leg in the same patient (all P < .001).
Calf Veins
The majority of anterior tibial, posterior tibial, and peroneal veins were paired, with values of 68% (455 of 672), 76% (645 of 792), and 76% (689 of 808), respectively. Single veins were seen in 33% (225 of 672), 17% (132 of 792), and 6% (50 of 808) of the veins, respectively. Three or more peroneal veins were seen in 8% (64 of 808) of patients. Drainage of the peroneal veins into the trifurcation occurred 59% (449 of 756) of the time; into the posterior tibial vein, 32% (243 of 756) of the time; and into the anterior tibial vein, 8% (63 of 756) of the time. Gastrocnemius veins were only visualized 64% (432 of 808) of the time, and in 76% (315 of 414) of cases the drainage was above the knee joint. A variable number of gastrocnemius veins (one to six) were visualized.
Popliteal Vein
Data on the popliteal vein are presented in Table 1. The popliteal vein commenced at the knee joint or proximal to it in 279 (35%) and distal to the knee joint in 529 (65%) of the 808 limbs. Within the popliteal fossa, a single vessel was identified in 452 (56%) venograms, and two or more vessels were identified in 356 (44%) of 808 limbs. True embryological duplication of the popliteal vein was present in 41 (5%) of 808 limbs (Fig 2).
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Symmetry between the Limbs
Symmetry between the two sides was seen 14% (55 of 404) of the time, with the main areas of asymmetry being popliteal veins (32%, 129 of 404) and SFVs (48%, 195 of 404).
| DISCUSSION |
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We believe the present study has a number of strengths compared with those in previous studies (7,8,13). All patients did not undergo surgery and were free of thrombus, with visualization of the entire deep venous system of both lower limbs (8). None of the patients included in this study was at high risk of developing DVT and, therefore, the sample chosen is representative of a normal population. Inclusion of high-risk patients in this study could potentially bias any results, with a particular anatomic variation being more prone to produce symptomatic thrombus, which would lead to further investigation. Venography rather than US was used to delineate the anatomy, despite its infrequent current use for initial DVT imaging (2). Although US studies have included larger numbers of patients, they have consistently demonstrated lower rates of venous anomalies (9,10,13) compared with venographic studies (7,8). US will not produce the same anatomic venous "map" and tends to be a subjective assessment that is dependent on operator skill, especially in examinations below the knee (2). For these reasons, a US anatomic study of the lower limb veins will have limitations.
The majority of pulmonary emboli arise from the proximal deep venous system of the lower limbs (14,15), and therefore, accurate assessment of this area is of particular importance, more so when the incidence of duplication of the SFV is as high as 30%, as suggested by findings of the present study. Our findings are in keeping with those of Screaton et al (8), who examined 381 venograms and concluded that as many as 46% of patients have duplicated and/or multiple SFVs. This figure was higher than that in previous studies, which had shown an incidence of 20%25% (6,9,16). This variation may reflect differences in sampling techniques (US or venography) (9), smaller sample sizes of earlier studies, and the fact that many studies reviewed patients with a symptomatic DVT (7).
Duplication of the SFV is a recognized antecedent of missed proximal thrombus at US (7,8,17), with the incidence being twice as high in patients with a duplicated SFV compared with those with a single SFV (7). The reason for this may result from a decrease in blood flow velocity and the subsequent pooling of blood in the duplicated vein, which stimulates the formation of thrombus (7,13). Furthermore, less than half of patients with thrombus in a duplicated SFV are symptomatic compared with almost two-thirds with thrombus in a single SFV, which is likely due to the presence of collaterals (7). An additional important point is whether a duplicated SFV is an independent risk factor for DVT. Further studies are required to assess this potential association.
We demonstrated that the majority of duplicated SFVs arise at the adductor canal or just above it in the midthigh region, with an equal chance of lying medial or lateral to the native vessel. There was a wide range of variation in the size of the duplicated vein. The adductor canal is accessible to US over the anterior aspect of the thigh, and it should be technically possible to visualize duplicated femoral veins when the vessels are assessed in the transverse plane. This will also depend on the transducer footprint length. A linear-array multifrequency probe (15L8w; Acuson Sequoia, Mountain View, Calif) may have a footprint size of up to 5.5 cm, which allows a broad view either side of the native SFV. Although in the present study we did not document the distance of any duplicated vein from the native vein, the impression was that a large number would be seen in this manner. Size is also an important factor, with only 4% of duplicated vessels being the same size as the native vessel; the smaller the vessel, the more difficult US visualization becomes.
The finding of multiple vessels within the popliteal fossa in 44% of patients is of importance for imaging this region. Although there is evidence of an increase in the incidence of DVT in patients with duplicated SFV, this has not been demonstrated in previous studies in which patients with duplicated popliteal veins were examined (13). At present, we are aware of only several cases highlighting the presence of thrombus in one of two veins in patients with congenital duplication of the popliteal vein (18,19). Nevertheless, our study highlights the high incidence of multiple vessels but not duplication in the popliteal fossa. This may increase the likelihood of a missed thrombus at US if only a single vein is visualized. Our findings are similar to those of other authors who reported rates of 36% (19) and 44% (20) in their series, with most popliteal vessel duplications resulting from the high confluence of the posterior tibial and peroneal veins within the popliteal space.
Multiple vessels in the popliteal fossa or duplication of the SFV in one limb strongly correlated with the incidence of venous anomalies in the other limb. This result differs from conclusions in two other studies (9,10), both of which were conducted with US. Therefore, the implications of this observation are that if duplications are visualized in one leg, the other leg should be scanned for the presence of these anomalies.
Little variation was seen in the anatomy of the calf veins, with the majority of calf vessels being paired. Greater variation was seen, however, with respect to the position of confluence of veins that formed the popliteal vein.
Our findings present implications for routine imaging of the SFV, a finding not shared by all authors. There are advocates for the minimal use of US (2123), which suggests that US venous studies can be safely limited to the popliteal and common femoral veins. However, at least 20% of proximal thrombi are isolated to the SFV (2426), and this finding may be more common when the SFV is duplicated (7). In a review of 269 cases of acute lower limb proximal DVT, Maki et al (25) showed that 22% of thrombi were isolated to the SFV, with the remaining 78% having thrombus extending into the common femoral or popliteal veins or both. Thus, assessment of the SFV is often of great importance in the establishment of more than 20% of all lower limb DVT (7). Therefore, like other authors (25,27), we cannot support the suggestion that it is safe to exclude SFV in US assessment of the lower limb.
Our study has several potential limitations. First, by selecting high-quality venograms with full opacification, we may have missed some variations that lend themselves to poor contrast material filling. This may be of importance in multiple SFVs, some of which might not have filled with contrast material. Second, in a review of this nature, where numerous investigators in different countries have performed examinations, individual venographic techniques may have influenced outcomes. Third, our calculations of SFV length should be regarded as estimates, but we attempted to minimize errors in size calculations by classifying the length into groups. Our aim was to show whether duplications of SFV were focal or covered a large field of view of the femoral vein, which is of importance to the sonographer. Finally, venography is not necessarily the standard technique for assessment of detailed anatomy, since it depends on adequate filling of all vessels, which is often not possible because of technical problems. It also causes the assumption that any vessels that do not fill with contrast material are not necessarily present.
Our results demonstrate that variations in lower limb venous anatomy are common and have important implications for diagnostic US imaging of suspected DVT. The results are in concordance with those of previous venographic studies in demonstrating a high degree of variation in lower limb venous anatomy (7,8). However, the present study differs with regard to the population studied and the availability of a large number of bilateral lower limb venograms. The fact that US studies have demonstrated lower frequency rates is a matter of concern and may highlight an important difference in the sensitivity and specificity of these two examination techniques. This has considerable implications for physician confidence in US as a reliable imaging modality for the exclusion of DVT. Unless an assessor-blinded study is performed to directly compare US and venography with regard to the ability to identify venous anomalies, we would recommend to all who perform US for the diagnosis of DVT to look for two vessels in the popliteal fossa and for a duplicated SFV; the examination should start at the adductor canal and extend to the midthigh, and the sonographer should look both medial and lateral to the main SFV. This will prolong an already time-consuming examination, but it will ensure that a potential venous thrombus is not missed.
| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, P.S.S.; study concepts and design, D.J.Q., R.A., P.S.S.; literature research, D.J.Q., R.A., P.S.S.; clinical studies, all authors; data acquisition, D.J.Q., R.A., P.S.S.; data analysis/interpretation, D.J.Q., R.A.; statistical analysis, R.A.; manuscript preparation, definition of intellectual content, and revision/review, D.J.Q., R.A., P.S.S.; manuscript editing and final version approval, all authors.
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