| | Thrombosis in unusual sites of the lower extremity veinsPresented at the Nineteenth Annual Meeting of the American Venous Forum, San Diego, Calif, Feb 14-17, 2007. Received 3 August 2007; accepted 16 December 2007. published online 25 March 2008. BackgroundThrombosis in unusual locations in the lower extremity veins has not been assessed. These veins are not imaged routinely and therefore information about them is lacking. MethodsThis study was designed to evaluate the natural history of deep vein thrombosis (DVT) in unusual sites. Patients with DVT in all thigh veins but the femoral vein were included. Patients with thrombi in any other vein in the first examination and those with history of DVT were excluded. Duplex ultrasound (DU) examination was performed to exclude thrombosis in the lower extremity in patients with signs and symptoms of venous thromboembolism and also in high-risk, asymptomatic patients. All veins from the distal external iliac vein to the lower calf were imaged. The deep femoral, femoropopliteal, lateral thigh, sciatic, and muscular thigh veins were examined. These patients were followed at 1 week, 1 month, 6 months, 1 year, and yearly thereafter, for thrombus propagation, resolution, and reflux. ResultsAmong the 15,850 DU performed in the vascular laboratory at Loyola University Medical Center, in a 10-year period to rule out DVT, 2568 (16.2%) were positive and 14 cases (7 males, 0.54% among the patients with DVT and 0.088% among the entire population) involved thromboses in unusual locations. Ten cases involved the left lower extremity and four the right. The unusual DVT cases were associated with medical and surgical conditions or were idiopathic in 11 patients, whereas three had Klippel-Trenaunay syndrome (KTS). The veins involved in the first group of patients were the deep femoral (8), the femoropopliteal (2), and the deep external pudendal (1). The patients with KTS had involvement of muscular thigh veins (1), and the lateral thigh vein and the sciatic vein (2). Thrombi propagation with extension to the common femoral vein was seen in four of the 14 patients: two from the deep femoral vein, one from the femoropopliteal vein, and one from the deep external pudendal vein. There were two incidences of pulmonary embolism (PE) one of which was fatal. At final follow-up, two patients developed recurrent DVT and nine had signs and symptoms of chronic venous disease. ConclusionsThe involvement of the studied veins in DVT is extremely rare. Thrombosis in these veins can follow the natural course of thrombosis in the more usual locations and is associated with lethal incidences of PE. Therefore, the association of these veins with all the grave sequelae of thromboembolic disease suggests that inclusion of these veins in routine lower extremity duplex scans would be beneficial. Deep vein thrombosis (DVT) and pulmonary embolism (PE) occur at an annual incidence of 1 per 1000 adults1 and has a great toll in inpatient and outpatient morbidity and mortality. Despite the associated large costs of DVT to society, the precise knowledge of the anatomic distribution of venous thrombosis in “unusual locations” such as the thigh veins has been rarely addressed. Ouriel and colleagues2 reported that most cases of DVT are associated with specific anatomic sites, with increasing frequency from the proximal to the distal venous segments.2 However, their work and that of others have not precisely described the occurrence of DVT in unusual sites or established their clinical significance. Our current work was designed to provide insights into the natural history of DVT affecting rarely reported veins in the thigh. Methods  Patients with thrombosis in the deep femoral and other unusual thigh veins were included in the study. Patients with thrombi in any other vein in the first examination and those with a previous DVT were excluded. All these patients were referred for a duplex ultrasound (DU) examination between 1995 and 2005 to rule out thrombosis in the lower extremity either because they had signs and symptoms of venous thromboembolism or were asymptomatic but a high risk for DVT, ie, patients that underwent complex neurosurgery procedures. All veins from the distal external iliac vein to the lower calf were imaged with DU. Low flow settings with a pulse repetition frequency ≤ 1500 Hz and color gain adjusted to the vessel size, flow, and depth were used. Multifrequency linear array transducers were used when the veins were located within 6 cm depth from the skin. For veins found in deeper locations a curvilinear 2-3 MHz array was used. Compression in transverse view in B-mode and augmentation with color view was applied in all veins. For obese patients and in those with significant edema, an active dorsi-plantar flexion was performed to augment the venous flow. The veins examined were the deep external pudendal vein which is seen uniting the common femoral vein opposite to saphenofemoral junction. The deep femoral vein and its tributaries were imaged from its union with the femoral vein to at least 10 cm distally. The deep femoral vein unites the femoral vein 2-3 cm below saphenofemoral junction to make the common femoral vein. The third vein examined was the femoropopliteal. This is an uncommon vein that unites the popliteal and the deep femoral veins and is also known as axial transformation from popliteal vein to deep femoral vein. It is more apparent in chronic obstruction of the femoral vein, where it dilates for compensation.3 In a few patients, it can be seen in the absence of femoral vein thrombosis. Other atypical veins in patients with venous malformations were also studied. It included the lateral thigh vein, muscular thigh veins, and the sciatic veins. The sciatic veins could be those of the sciatic nerve or the persistent sciatic vein which is much larger than the veins of the nerve. When there is a sciatic vein, the femoral vein often is hypoplastic. Because of the unusual location of thrombosis, these patients were followed up at 1 week, 1 month, 6 months, 1 year, and yearly thereafter. They were seen earlier if new symptoms of venous thromboembolism were present. In case of PE symptoms a spiral CT was performed. At follow-up, the veins were examined for thrombus propagation, resolution, and reflux. A second group of 100 selected patients were included for comparison. All of them had a first episode of acute DVT from the popliteal vein and above and were anticoagulated. The involvement of the veins at unusual sites for thrombosis was assessed. Patients with isolated calf DVT were not included in order to match this group of patients to our study cohort. The CEAP classification system was used to grade the clinical severity of the disease.4 Reflux was considered to be present if the retrograde flow was >0.5 s in the superficial veins, deep thigh veins, and deep calf veins; >1.0 s in the common femoral, femoral, and popliteal veins; and >0.35 s in the perforator veins.5 Reflux was elicited was manual compression distal to the site of imaging followed by sudden release. In obese patients and those that had significant edema, a forced dorsi-plantar flexion was performed. At the baseline examination, the distribution and extent of thrombosis was recorded in detail by reporting the precise location and length of the thrombus. This was very important for determining the propagation and recurrence of thrombosis. Acute thrombus was detected by the dilatation of the lumen, the echolucent texture, and the thin and smooth vessel wall. The presence of chronic thrombus was determined by a normal or reduced vein diameter, the echogenic texture, and the thick and irregular wall. During compression of the vein, the acute thrombus is spongy, and the chronic one is firm. With the use color mode confluent flow channels are seen in the acute thrombus compared with multiple irregular channels in the chronic thrombus. In addition, the fresh thrombus may have a free-floating tail. DVT propagation in the thigh veins was diagnosed when the thrombi extended to a new vein segment, ie, from the deep femoral to common femoral vein. Diagnosis of recurrent DVT was made if thrombus developed in a new location or in a previously recanalized segment. Also, presence of echolucent material, dilation of the vein lumen of >2 mm compared with previous examination, and a double echogenic line in the outer rim of the thrombus were used for detecting recurrent thrombosis.6, 7, 8 These unusual vein sites are not routinely imaged and many investigators do not even know of their existence with the exception of the deep femoral vein. Our center has a vast experience with the anatomy and pathology of these veins and their study is part of the routine DU examination of the lower extremity veins. The first author (NL) either performed or supervised all the examinations included in this study. Often, other ultrasound windows than the medial were used to image these veins such as the lateral, posterior-lateral, posterior, and posterior-medial. These windows allowed better imaging and compressibility of the veins. Anatomic landmarks such as the saphenofemoral junction, the union of the femoral with the deep femoral vein, the femoral bone, and the sciatic nerve were used to locate these veins. Results Prevalence and patient characteristics During the period of observation, 15,850 patients were examined in the vascular laboratory at Loyola University Medical Center to rule out DVT. From these patients, 2568 (16.2%) had DVT. Thrombosis in unusual sites occurred in 14 patients giving a prevalence of 0.088% among all patients or 0.54% in patients with DVT. There were seven men and seven women with a mean age of 48 ± 13.5 years (range 26-71). Thrombosis involved the left lower extremity in 10 patients and the right in four. The etiology of DVT was variable with 2 spontaneous thromboses, 2 cancer-related thromboses (one ovarian and one pancreatic cancer), 3 surgery-related thromboses (2 major abdominal operations and one thoracic spine surgery), 2 thromboses associated with multiple traumatic injuries (1 after a motor vehicle accident and one after a fall), 2 critically ill medical patients (1 with septic shock and one with multiple organ dysfunction syndrome), and 3 patients with Klippel-Trenaunay syndrome (KTS). The patients presented with signs and symptoms of DVT (n = 9) or were high-risk asymptomatic (n = 5). Of the symptomatic patients, three presented with lower extremity pain, two had lower extremity swelling, and four had both pain and swelling. Distribution The thrombi distribution was as follows: 8 cases of deep femoral vein thromboses, 2 thromboses in the femoropopliteal vein, 1 in the deep external pudendal vein, 1 in a muscular thigh vein, and 2 patients with thromboses in the lateral thigh vein, one of which had associated thigh perforator vein thrombi and another with an associated sciatic vein thrombosis (Fig 1, Fig 2). Complications Among the 14 patients, there were three with clinical suspicion of PE, none of which belonged to the KTS group. From these, one tested positive and one negative for PE by spiral computed tomography (CT), and one patient died of PE, as it was later confirmed at autopsy. One of the patients with KTS developed intestinal bleeding for which he underwent colon resection, and he had a filter placed in his inferior vena cava. Follow-up The follow-up period for the 13 patients that were still alive varied from 11 to 37 months. From all 14 patients, 10 received anticoagulation with low-molecular or unfractionated heparin, followed by warfarin for the therapy of DVT immediately after the diagnosis was made. Two patients, both with diagnosis of KTS, did not receive anticoagulation. One of them was diagnosed with thrombus in a muscular thigh vein, for which he was only prescribed aspirin. The other patient developed intestinal bleeding and therefore heparin or warfarin was considered contraindicated. A patient with thrombus in the deep external pudendal vein did not receive anticoagulation at the moment of DVT diagnosis. However, on ultrasound follow-up 4 days later, extension of thrombosis into the common femoral vein was documented and therefore heparin was started, subsequently continued with Warfarin. An additional patient with diagnosis of DVT affecting the femoropopliteal vein was started on Heparin IV immediately after her diagnosis. However, she died about 4 hours after initiation of anticoagulation due to PE found on autopsy. At follow-up, there was thrombus propagation with extension to the common femoral vein in 2 of the deep femoral vein thromboses, in one of the femoropopliteal vein thromboses and in the patient with deep external pudendal vein thrombosis. During the same period, recurrent DVT was observed in two patients. The first patient developed ipsilateral common femoral vein, femoral vein, and popliteal vein thrombosis at 7 months, and the second developed contralateral calf thrombosis (soleal and peroneal veins) at 13 months of follow-up. These patients stopped their anticoagulation therapy at 6 months. Both patients belonged to the group that presented initially with deep femoral vein involvement. At final follow-up, five patients had no signs of venous insufficiency, four presented with edema (class 3 venous insufficiency), and one presented with skin changes (class 4). In the group of patients with KTS, two patients presented with class 4 and one with class 4-6 venous insufficiency. Four patients reported symptoms at final follow-up in the affected limbs. One complained of burning sensation, one with burning pain and itching and two of aching. Analysis of the comparison group The analysis of the second group of 100 selected patients with a first episode of acute DVT proximal to, or including the popliteal vein, revealed only three cases of deep femoral vein involvement. In all three cases, the common femoral vein was also involved. In two of them, the femoral vein was additionally implicated and in the remaining case, thrombus was also seen in the external iliac vein. These three patients clinically presented with impressive lower extremity edema and pain, but without meeting diagnostic criteria for phlegmasia. None of the other unusual vein segments reported in this group were involved. Discussion Lower extremity DVT has a high prevalence in hospitalized patients and is associated with significant short and long-term morbidity and mortality. DVT affects 2.5 million people annually in the United States and is associated with 50,000 to 200,000 deaths each year.9 The magnitude of the problem shows that DVT has a large negative impact on human and economic resources. The standard method to examine patients with symptoms of acute or chronic thromboembolic disease of the lower extremity attributes little significance to unusually affected veins of the lower extremity. The only vein thromboses, from those studied, for which there are reported incidences in the literature are the ones involving the deep femoral 2, 10 and the persistent sciatic veins.11 In their study, Ouriel et al2 reported that the prevalence of deep femoral vein thrombosis studied by phlebography is 0.9%. However, given the fact that phlebography can only recognize deep femoral vein thrombosis if there is simultaneous proximal thrombosis of the ipsilateral common femoral vein or the iliac vein,3 we can infer that the true incidence of isolated deep femoral vein thrombosis is much lower. Other, less frequently reported deep veins in the thigh include the femoropopliteal vein. Raju and colleagues3 reported, in a subset of consecutive severe venous stasis cases, that the deep femoral vein enlarges to a variable extent (ie, axial transformation) in some cases, to compensate for severe post-thrombotic changes in the accompanying femoral vein. It is also our experience that this vein is seen most often accompanying femoral vein thrombosis, but, as it is shown in the current series, this vein can also be seen without associated femoral vein thrombi in rare occasions. The persistent sciatic vein is a rare anomaly most often associated with KTS.11 However, it is currently diagnosed with more frequency due to the improvement of diagnostic methodologies, especially magnetic resonance imaging. Cherry et al11 have previously described this condition and identified a number of cases where PE was associated to their presence, including lethal cases. The persistent sciatic vein has to be carefully differentiated from varices affecting the sciatic nerve vein.12, 13 These veins are inside the nerve and in close proximity with a smaller diameter than the persistent sciatic vein. The deep external pudendal14 and the lateral or marginal thigh veins15 have been previously recognized in the literature, but no cases of thrombosis affecting those veins have been reported up to date. Our current work is the first report of such instances. DVT at unusual sites in combination with axial veins is expectedly to be much more common than isolated DVT in unusual sites. Certainly, deep femoral vein involvement is not rare in chronic post-thrombotic venograms. Similarly, combined involvement intuitively would have more severe acute and chronic symptomatology. In order to analyze such combined involvement, a second group was included. Our analysis indicates that the combined involvement is six times more common and their presentation appeared to be more severe than isolated unusual vein sites affliction. This observation supports the argument for routine screening of unusual vein sites, particularly the deep femoral vein, and treating them aggressively when DVT is detected. The patients presenting with thrombi in the unusual locations studied in this report were both healthy individuals with no significant medical history related to their presentation and patients with severe medical and surgical problems. These patients were selected to have thrombi in unusual sites only, because otherwise the clinical presentation would have been affected by thrombi in the other more usual locations, or it would have been impossible to know where the thrombi originally started. Therefore, thrombi do develop in these veins irrespective of the associated risk factors for thrombosis. The natural history of the thromboembolic disease in these veins mirrors that of the most commonly observed veins. In large series, it has been established that thrombi in the deep veins of the lower extremities tend to propagate in 15% of the limbs16, 17, 18, 19 and that this tendency is associated with the morbidity and mortality related to DVT.20, 21 In our series, there was propagation of the thrombi in four cases that involved all the unusual veins studied. PE is a potentially lethal complication of DVT and it has been established that from the 100 cases of PE secondary to DVT only four will be clinically important and one or two from these may be fatal.19, 21 At the same time, both the deep femoral and the persistent sciatic vein have been associated with life threatening PE in the literature.2, 10, 11 In accordance with these data, in the current report, two patients developed overt PE, which was fatal in one patient. At follow-up, there were two patients in the study group that presented with recurrent DVT of the lower extremities, a finding that agrees with the reported course of the disease in the literature. As it is expected, the cumulative risk of recurrent DVT is 11% at 1 year22 and 24.3% at 5 years.23 In addition, five patients developed evidence of post-thrombotic syndrome in concordance with the natural course of venous thromboembolic disease in the usually examined veins of the lower extremity, in which we expect an incidence of post-thrombotic syndrome of 17% after 2 years.23 Besides the development of thrombosis in unusual veins of the lower extremities in patients from the general population, we reported the development of thrombosis in unusual locations in patients with KTS. This syndrome is diagnosed by the triad of varicose veins, cutaneous hemangiomas, and hypertrophy of soft tissue and bone.24 The existence of dysplastic blood vessels predisposes these patients' blood to stasis, which results in an increased incidence of thrombosis. Baskerville et al24 reported a 17% incidence of radiographically proven DVT in a series of 49 patients with KTS. In comparison the incidence of autopsy proven DVT in nonhospitalized patients is estimated to be 5%.20 In addition, the incidence of PE in patients with KTS is estimated to be 14% to 22%.25 Therefore, DVT is a major morbidity and mortality factor associated with this syndrome. In fact these patients, in accordance to what is presented in this report, have an increased risk of developing venous insufficiency.26 The recognition of thrombosis in the veins that we report (lateral thigh, perforators, sciatic, and muscular thigh veins) is of heightened importance as we prove that these veins are associated with the complications cited in the literature27 for the usually examined veins in patients with KTS. The literature reports thrombotic involvement of unusual vein sites most often in association with hypercoagulable states. Most patients in our study had a well-recognized risk factor for the development of a thromboembolic event, such as a major medical illness, recent major surgical intervention, trauma, neoplasms, or KTS. Therefore, those patients did not undergo further work-up for hypercoagulability. However, there were two patients with spontaneous thrombosis, in whom decision was left to the referring physician to pursue additional testing, which seems intuitively advisable. Our limited data cannot provide guidelines for when is right to perform test for hypercoagulability. Given the rarity and the unusual sites of thrombosis test for thrombophilia should be performed until more concrete data are available. The ideal therapy for this cohort of patients is unknown at this time, given that the current work is the first addressing such cases. Most of the veins affected are considered to be deep veins, except for the marginal thigh vein which is superficial. However, this vein has a large diameter and connects with multiple deep veins in the thigh and with pelvic veins, where it usually terminates. It appears wise to provide anticoagulation if proximal deep vein involvement is confirmed, following the same parameters of the femoral and popliteal vein thrombosis. It is important to note, however, that the two events of PE in our series developed after deep femoral vein thrombosis. Cherry and colleagues11 reported lethal PE cases associated with persistent sciatic vein, which may speak of the need for anticoagulation when involvement of those two veins is noted. Thrombosis of the remaining thigh veins was associated with PE but as the prevalence is low and the natural history is unknown close monitoring should be done if anticoagulation is not given. Conclusions The prevalence of DVT of the thigh veins studied is extremely rare. The presentation of our patients, both initially and at follow-up, spanned the whole spectrum of the natural history of DVT, as reported in the literature for the more usual sites of thrombosis. Since it was not possible to leave these patients untreated, this work reflects the natural history of patients with treated DVT in unusual sites. There were incidences of thrombus propagation, PE, recurrent DVT, and post-thrombotic syndrome. The association of these veins with all the complications of thromboembolic disease suggests that imaging of these veins would be beneficial. Author contributions Conception and design: NL, KB, LL Analysis and interpretation: NL, KB, LL Data collection: NL, KB, LL Writing the article: NL, KB, LL Critical revision of the article: NL, LL Final approval of the article: NL, KB, LL Statistical analysis: Not applicable Obtained funding: Not applicable Overall responsibility: NL References 1. 1Cushman M. Epidemiology and risk factors for venous thrombosis. 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a Department of Surgery, Stony Brook University Medical Center, Stony Brook, NY b Division of Vascular Surgery, Loyola University Medical Center (LUMC), Maywood, Ill c University of Arizona Health Science Center (AHSC), and Southern Arizona Veteran Affairs Health Care System (SAVAHCS)-Vascular Surgery Section, Tucson, Ariz.  Reprint requests: Nicos Labropoulos, Professor of Surgery and Radiology, Director, Vascular Laboratory, Department of Surgery, HSC T19 Rm90, Stony Brook University Medical Center, Stony Brook, NY 11794-8191.
Competition of interest: none. PII: S0741-5214(07)02118-0 doi:10.1016/j.jvs.2007.12.044 © 2008 The Society for Vascular Surgery. Published by Elsevier Inc. All rights reserved. | |
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