Deep venous thrombosis (DVT) occurs annually in one in 1000 people among the general U.S. population (6,8,13). DVT, with its associated complications, is a significant source of morbidity and mortality. While physical activity and exercise appear to be protective against thromboembolic disorders, case reports of DVT in athletes do exist (1). Examples from published literature include lower extremity DVT (LEDVT) in triathletes (19,25), soccer players (6), runners (13), and a military cadet (8), as well as cases of upper extremity DVT (UEDVT) in football linemen (23), weight lifters (13), and baseball pitchers (9). Despite case reports, no estimates are available for the incidence of thromboembolic disorders in competitive athletes. While anticoagulation treatment guidelines are well established for DVT, no return-to-play guidelines currently exist for athletes with venous thrombosis. Additionally, no randomized controlled trials (RCT) or large cohort studies exist that document the safe timing of exercise in the DVT recovery process. This article discusses the evidence for safe return-to-exercise and competition for athletes with DVT.
DVT affects more than 250,000 people in the United States each year. At least 116,000 people are diagnosed with their first DVT each year (8). The estimated incidence of DVT from all causes is 0.5 to 1.6·1000−1·year−1, a number that may be underestimated because of the number of asymptomatic DVT and inaccuracies of clinical diagnosis (6). In the general population, the majority of DVT occur in the lower extremity. UEDVT is rare, occurring in approximately 2·100,000−1 persons·yr−1 but is the most common vascular condition among athletes (8).
Delayed presentation with DVT is not uncommon. More than 50% of outpatients diagnosed with DVT wait at least 3 d before seeking medical attention (8). Complications of DVT include death, pulmonary embolus (PE), recurrent DVT, and postthrombotic syndrome (PTS). Morbidity and mortality can be high. One to five percent of patients presenting with DVT will die from all-cause complications, mainly pulmonary embolism (25). In one study, 30% of patients presenting with their first DVT died within 30 d (8). Up to 50% of patients with DVT develop a PE (2). Despite optimal anticoagulant therapy, DVT symptoms such as leg swelling can take up to several weeks to subside. As many as 40% of patients with DVT develop PTS, symptoms of which include chronic leg pain, leg heaviness, leg swelling, and leg cramping aggravated with standing and alleviated with recumbence and elevation (21). PTS usually occurs in the first 6 months following DVT diagnosis, but its effects can last for years (27). Approximately 20% to 50% of patients with LEDVT and 15% to 25% of patients with UEDVT develop PTS (6,9,10,23). PTS can be difficult to distinguish from recurrent occult thrombosis. The severity of symptoms may vary over time, and the most extreme manifestation is venous ulcers of the lower leg.
Thrombosis development is summarized by Virchow's Triad of endothelial injury, blood stasis, and increased blood viscosity. These three clot-predisposing factors initiate a cascade of procoagulant reactions that culminate with the formation of a thrombus. Endothelial injury has been highlighted as a primary factor in case reports of athletes with LEDVT involving acute traumatic knee dislocation and repetitive cyclist leg motion over a bicycle seat (6,8,13). Muscle hypertrophy impinging on blood vessels, causing both blood stasis and endothelial injury, has been implicated in both LEDVT and UEDVT (6,8,9,13,23). Compression of the subclavian vein by cervical ribs, clavicular anomalies, and musculofascial bands also have been reported in cases of UEDVT (also termed "effort thrombosis" or Paget Schroetter Syndrome). Increased blood viscosity, traditionally implicated in patients with hypercoagulable disorders, also plays a role in patients with erythrocytosis and marked dehydration (13).
Standard risk factors for DVT are immobilization, pregnancy, recent surgery, malignancy, older age, smoking, hypercoagulable states, connective tissue disorders, sex steroid administration, severe dehydration, and major trauma (6,13). Competitive athletes often are placed under conditions where they are exposed to several risk factors. These risk factors can include orthopedic trauma, postinjury immobilization, frequent and prolonged travel, hemoconcentration after exertion, and polycythemia as seen with altitude training and exogenous Epo administration (13). While cast immobilization, hypoxic training, air travel, doping, misuse of nutritional supplements, and pathologic training potentially may contribute to an increased risk of thrombosis, there is no strong evidence to suggest that these factors clearly predispose the competitive athlete to thrombosis (1,10,13). Case reports have described athletes presenting with UEDVT after pitching and following heavy upper-body workouts involving repetitive arm abduction (9,23). Literature also describes athletes who presented with LEDVT following popliteal contusion, car rides longer than 3 h, and elective abortion (6,8,13). However, there is no consensus that elite athletes as a whole are at higher risk for venous thromboembolism (VTE). More study is needed.
Published case reports describe athletes presenting with DVT following heavy bouts of exertion, after competition travel, and orthopedic injury sustained during competition (6,13,19,23,25). Some cases have reported DVT in athletes following only mild to moderate activity (6). Patients with VTE typically present with complaints of limb edema and pain that is increased with provocative maneuvers. Low-grade fever, venous distension, increased limb circumference, extremity cyanosis, and tender palpable cords may be noticed (6,7,11,23).
Clinical examination has low sensitivity (11%) and a low predictive value (25%) for DVT; however, it has demonstrated moderate to high specificity (76%-85%) (8). History and physical exam findings alone have a predictive value of only 15% (18). Clinical prediction algorithms, which rely on the initial risk stratification of athletes based on pretest probability, have been developed to facilitate the diagnosis of VTE (9a). Pretest probability of DVT may be estimated by a well-validated clinical prediction rule, such as the Wells model, which takes into account the clinical features of active cancer (1 point), lower extremity paralysis, paresis, or immobilization (1 point), recent surgery with bed rest for 3 d (1 point), localized deep vein tenderness (1 point), full length leg swelling (1 point), unilateral calf swelling >3 cm (1 point), pitting edema (1 point), collateral superficial veins (1 point), and probable alternative diagnosis (−2 points) (26). A score of zero is considered low risk, while a score of one point or higher is considered moderate or high. Athletes with a moderate to high probability should undergo duplex venous ultrasound with compression to rule out LEDVT. Athletes with a low pretest probability may be screened first with a highly sensitive D-dimer assay. DVT is ruled out in low-risk athletes with a negative D-dimer assay. Those low-risk athletes with a positive D-dimer must have DVT ruled out via compression duplex ultrasound (18). Ultrasound is the initial test of choice because it is noninvasive, and it has high sensitivity (93% for proximal LEDVT, 96% for UEDVT) and specificity (98% for proximal LEDVT, 93.5% for UEDVT) in the investigation of peripheral DVT (14,17). If initial ultrasound results are negative and DVT is strongly suspected, ultrasound should be repeated in 3 to 7 d (18). Additionally, computed tomography (CT) venography (sensitivity 89%-100%; specificity 94%-100%) or magnetic resonance (MR) angiography (sensitivity 100%; specificity 100%) can be used to confirm the diagnosis (13,14,18).
Anticoagulation remains the mainstay of VTE therapy whether the patient is a competitive athlete or a member of the general population. It maintains the patency of venous collaterals, reduces thrombus propagation, and reduces the incidence of thrombus embolization (11,13). Anticoagulation is begun with subcutaneous low molecular weight heparin (LMWH) or unfractionated heparin (UFH), and concurrent initiation of a vitamin K antagonist (VKA) like warfarin. LMWH or UFH is continued for at least 5 d and discontinued once a therapeutic international normalized ratio (INR) range of 2.0 to 3.0 has been achieved for 24 h (8). In patients with DVT, the dose of VKA should be adjusted to maintain an INR range of 2.0 to 3.0 (target of 2.5) for all treatment durations. For patients with DVT secondary to a transient risk factor, anticoagulation with VKA is continued for 3 months (11). Patients with unprovoked (i.e., idiopathic) DVT should be anticoagulated with a VKA for at least 3 months, then undergo risk-to-benefit ratio evaluation for long-term therapy. Patients with a first unprovoked VTE that is a proximal DVT, and in whom risk factors for bleeding are absent and for whom good anticoagulation monitoring is achievable, should undergo long-term anticoagulation when this is consistent with patient preference. For patients with a first unprovoked distal DVT, 3 months of anticoagulation is sufficient (11). In patients with extensive acute proximal DVT (e.g., iliofemoral DVT with symptoms <14 d) who have a low bleeding risk, CDT followed by balloon angioplasty and stent placement may be used to reduce acute symptoms and postthrombotic morbidity, provided adequate expertise and resources are available (11).
Although no RCT have evaluated the use of anticoagulation for the initial treatment of UEDVT, several small prospective cohort studies have reported low rates of recurrent DVT, PE, and major bleeds using treatment protocols for UEDVT similar to those for patients with LEDVT (11,13,23). Thus, for patients with acute UEDVT, the American College of Chest Physicians (ACCP) recommends anticoagulation treatment as described for LEDVT. Although some studies report good success of thrombolytic therapy in establishing early and maintaining late venous patency, the overall quality of evidence remains low (11). It has been suggested that catheter-directed thrombolysis (CDT) may reduce PTS in athletes with UEDVT. It also has been suggested that CDT may yield higher rates of clot resolution and reduces risk of serious bleeding compared with systemic thrombolysis (11,13). However, the largest prospective study examining CDT reported a substantial follow-up recurrence rate of 23% (11). More study is needed to determine whether thrombolytic therapy is superior to anticoagulation in important clinical end points such as PE, recurrent VTE, bleeding, and PTS. The ACCP recommends against routine use of systemic or CDT therapy for most patients with UEDVT. However, in select patients with acute UEDVT who present with severe symptoms of recent onset (i.e., less than 7 d) and who pose a low risk of bleeding, CDT may be used for initial treatment, provided appropriate expertise and resources are available (11).
A number of surgical reviews have advocated for thrombolysis and angioplasty or stent placement followed by early or late surgical decompression of thoracic outlet syndrome. However, the data and safety of these approaches are limited and derived from small, uncontrolled case series (9,11,23). For most patients with acute UEDVT, the ACCP recommends against the routine use of catheter extraction, surgical thrombectomy, transluminal angioplasty, stent placement, staged approach of lysis followed by interventional or surgical procedure, or superior vena cava filter placement. These interventions, however, including surgical decompression in cases of obstruction to thoracic vascular structures, may be considered in athletes with acute UEDVT and severe persistent symptoms who have failed conservative measures, including anticoagulation, structured physical therapy, weight loss, and nonsteroidal antiinflammatory drugs (NSAID) (11,13).
Venous compression devices long have been used in the initial treatment of LEDVT, despite a paucity of evidence-based literature to support their use. However, combined data from five trials over the last 10 yr suggest that the use of venous compression reduces the incidence of PTS (2,10,15). Mild to moderate PTS decreased from 37% to 22%, and severe PTS decreased from 12% to 5% (15). Overall, the number needed to treat with venous compression to prevent one episode of PTS was five (15). Given the potentially debilitating effects of PTS and the low potential for harm, the ACCP recommends elastic compression stockings with an ankle pressure gradient of 30 to 40 mm Hg for the prevention of PTS in patients with symptomatic proximal LEDVT. Compression therapy should be started as soon as possible after initiating anticoagulation and should be continued for a minimum of 2 yr. The treatment of PTS has been evaluated only in small or methodologically flawed trials. Based on limited data, for patients with severe edema of the leg due to PTS, a course of intermittent pneumatic compression is suggested. For patients with mild edema, elastic compression stockings are recommended (11).
Unlike lower extremity PTS, no controlled studies have evaluated the effectiveness of elastic bandages or compression sleeves in the prevention of upper extremity PTS. Thus the routine use of elastic compression is not recommended for the prevention of PTS after UEDVT (11). Likewise for treatment of upper extremity PTS, there exist no controlled studies evaluating the effectiveness of elastic bandages or compression sleeves. Anecdotal evidence, however, exists suggesting that patients with upper extremity PTS may derive symptomatic relief from elastic bandages or compression sleeves. Since their use is unlikely to cause harm, elastic bandages and compression sleeves are recommended in patients with UEDVT who have persistent pain and edema (11).
Patients with VTE who undergo anticoagulation experience marked reductions in complications of VTE compared with those who remain untreated. Although radiographically demonstrable clot lysis occurs in only 50% of anticoagulated patients (6), heparin (UFH or LMWH) significantly reduces clot propagation, recurrent PE, and mortality (11). Mortality is high when anticoagulation is not used. Weight-appropriate unmonitored LMWH administered subcutaneously is as effective and as safe as intravenous UFH. In fact, a recent analysis of 17 studies demonstrated that LMWH was associated with fewer thrombotic complications and less major bleeding than UFH (11).
While many previously active patients with LEDVT attempt return to an active lifestyle, the long-term clinical outcomes often are complicated by persistent symptoms. One study found that 82% of patients with their first DVT suffered from recurrent symptoms at a mean follow-up of 6.6 yr (27). As previously mentioned, early ambulation and compression therapy may mitigate these symptoms. The general knowledge concerning quality of life and burden of illness in these patients is not known. More study is needed.
For patients with UEDVT, the overall prognosis is good. Of patients treated with thrombolysis, 80% to 90% returned to a long-term asymptomatic state (13). It also appears that the prognosis with anticoagulation is favorable. In a literature review of more than 2,500 patients, no superiority of treatment was found between anticoagulation alone and thrombolysis for the general treatment of UEDVT (23).
In cases of external compression such as thoracic outlet syndrome or clavicular impingement, patients appear to benefit from acute correction of the anatomy. One study reported that all patients who underwent first rib resection were free of long-term symptoms. Another study that examined UEDVT in elite baseball players found that four players who underwent first rib resection were able to return-to-play at previous levels or better (11). While the overall data are positive, they are admittedly limited. Thus, it is suggested that surgical decompression be reserved for patients with severe persistent symptoms after failing conservative therapy (11,23).
Traditionally, patients with active DVT were hospitalized and placed on bed rest for 7 to 10 d for fear of PE development in those who remain active. Soreness often precluded a return to daily activities in the first few weeks after DVT, especially in patients entering their sixth and seventh decades of life. Thus, sedentary patients generally followed a gradual 6-wk return to daily activities. Over the last two decades, however, this plan of care has been challenged, particularly for athletes. The early treatment of acute DVT with bed rest and anticoagulation has given way to anticoagulation with early mobilization (2,10,11,22).
Randomized trials and observational studies suggest that a majority of patients with DVT may begin ambulation within 24 hours of anticoagulation provided they have adequate cardiopulmonary reserve and no clinical evidence of active pulmonary embolism (2,10,21). Evidence suggests that these patients who ambulate early are not at higher risk for developing PE, nor does it aggravate acute DVT symptoms. In fact, early walking may reduce the risk of DVT extension, improve the resolution of DVT symptoms, and reduce the long-term symptoms of PTS. Provided that immediate rest, elevation, and anticoagulation have reduced the initial edema and inflammation, it thus seems prudent to permit, and even encourage, the athlete with DVT to engage in light ambulation as tolerated within the first 1 to 2 d after beginning anticoagulation.
While data for anticoagulation and early mobilization exist, data guiding return to physical activity are sparse. There are no RCT investigating when it is safe to return to sport following VTE. There are no expert consensus-derived clinical practice guidelines on the topic.
In their case report of a female triathlete with acute LEDVT, Roberts and Christie suggested a gradual progressive return to training program (Table 1) (19). At the start, they recommend the gradual introduction of activities of daily living (ADL) over the first 3 wk of anticoagulation. This is based off animal models of the natural history of venous thrombosis, which demonstrate that thrombus endothelialization and adhesion to vessel wall begin early in the first 3 wk after clot formation. Once endothelialization and adhesion take place, the potential for clot migration and embolism decreases. Thus, during the first 3 wk of anticoagulation, athletes should engage in gradual return to ADL.
By weeks 4 to 6, clot lysis and recanalization have occurred. It is during weeks 4 through 6 of anticoagulation that Roberts and Christie suggest a gradual return-to-training regimen that begins with nonweight-bearing exercise (e.g., swimming) in week 4, then nonimpact-loading exercise (e.g., swimming and cycling) in week 5, followed by the gradual introduction of impact-loading exercise (e.g., running) in week 6. While a template for the gradual introduction of running is not specified, such might be accomplished by use of an 8-wk return-to-running protocol as outlined by O'Connor and Wilder (16) (Table 2). Athletes should be instructed to discontinue any activity that results in return of symptoms or signs and report any blood loss or bruising. While on warfarin, athletes will need weekly INR labs until a stable INR has been reached, at which point lab monitoring can be performed on a monthly basis (11).
Individuals with acute VTE should not participate in collision or contact sports. Individuals in noncontact sports may participate after appropriate counseling, unless that sport is a suspected cause for VTE or has additional environmental risks (e.g., SCUBA diving) (11).
Those with UEDVT who are determined to have an underlying cause for thrombus should not participate in aggravating activities until any structural abnormalities have been corrected (13).
If individuals have completed a course of anticoagulation and a hypercoagulability laboratory evaluation (as needed for a positive family history of VTE or personal history of recurrent idiopathic VTE) is negative, return-to-play with gradual increase in intensity is recommended with careful monitoring for recurrent VTE and management of PTS. Strong recommendations should be given to the athlete about the possible instigating factors that may have led to the initial event so that appropriate preventative measures can be instituted (13).
Multiple studies have demonstrated the effectiveness of graduated compression stockings in the prevention of DVT in hospitalized patients (20). The study of graduated compression stockings in athletes is limited to a few small treadmill studies of healthy runners. Two studies found no significant physiologic benefit, while a third found that running performance was improved at anabolic and metabolic thresholds (4,5,12). Significantly decreased incidence of delayed onset muscle soreness and greater subjective comfort in runners wearing low-grade compression stockings were benefits noted in other studies (3,4). None of the studies involving athletes, however, evaluated the role of compression stockings in the primary prevention of DVT.
The role of exercise in the prevention of VTE has been the subject of much scrutiny. Chronic sports participation or endurance training is associated with overall decrease in risk of venous thrombosis and a reduction in various markers of coagulation. Light to moderate exercise thus is likely to be of benefit. However, there is enhanced platelet reactivity and coagulation in response to vigorous exercise (1). Since vigorous exercise is an integral part of the elite athlete's training regimen, some suggest that this may place elite athletes at a higher risk for thrombosis.
While there is not conclusive evidence that properly hydrated athletes have a decreased incidence of VTE, there is evidence of increased incidence of VTE in hemoconcentrated or polycythemic individuals. When combined with the observation that there is enhanced platelet reactivity and coagulation in response to vigorous exercise, it would seem prudent to recommend sufficient oral intake, particularly for those engaging in high-intensity workouts.
Those who suffer competition injury requiring immobilization greater than 3 d should receive early prophylactic anticoagulation in addition to physical antithrombotic measures (13). For athletes with a history of DVT using air travel, LMWH should be considered for prevention of DVT recurrence. In addition, Eichner has recommended eight strategies for prevention of clots. These include sitting in seats that allow leg extension, hourly aisle walks, not crossing legs, wearing of loose clothing, hydration with water or juices, consuming low-fat meals, fidgeting, and thinning blood with aspirin or LMWH if prone to clotting (7).
Venous thromboembolism can occur in athletes following strenuous exertion, prolonged air or automobile travel, and orthopedic injury. While it is not known whether elite athletes are at higher risk for VTE, the nature of their training and competition schedules exposes them to various risk factors. A high index of suspicion is needed to diagnosis VTE in the athlete, as many patients do not exhibit hallmark signs, and the rates of short- and long-term complications are high (6,8,18). Those athletes diagnosed with VTE should undergo anticoagulation therapy. Selected cases may warrant alternate additional therapies or procedures. Compression therapy and rapid mobilization are crucial to shorter recovery times and decreased long-term complications. Return-to-play should follow a structured program of gradual increased activity as tolerated by the patient. More study, preferably RCT or large cohort studies, is needed to examine the safe timing of return-to-play in the VTE recovery process.
1. Adams M, Williams A, Fell J. Exercise in the fight against thrombosis: friend or foe? Semin. Thromb. Hemost
. 2009; 35(3):261-8.
2. Aldrich D, Hunt DP. When can the patient with deep venous thrombosis begin to ambulate? Phys. Ther
. 2004; 84(3):268-73.
3. Ali A, Caine M, Snow B. Graduated compression stockings: physiological and perceptual responses during and after exercise. J. Sports Sci
. 2007; 25(4):413-9.
4. Ali A, Creasy R, Edge J. Physiologic effects of wearing graduated compression stockings during running. Eur. J. Appl. Physiol
. 2010; 109(6):1017-25.
5. Berry M, Bailey S, Simpkins L, TeWinkle J. The effects of elastic tights on the post-exercise response. Can. J. Sport Sci
. 1990; 15(4):244-8.
6. Echlin P, Upshur R, McKeag D, Jayatilake H. Traumatic deep vein thrombosis in a soccer player: a case study. Thrombosis J
. 2004; 2:8.
7. Eichner R. Athletes in airplanes: some are born to clot. Sports Med. Dig
. 2000; 22:140-42.
8. Fink M, Stoneman P. Deep vein thrombosis in an athletic military cadet. J. Orthop. Sports. Phys. Ther
. 2006; 36(9):386-97.
9. Hurley W, Comins S, Green R, Canizzaro J. A traumatic subclavian vein thrombosis in a collegiate baseball player. J. Athl. Train
. 2006; 41(2):198-200.
10. Kahn SR, Shrier I, Kearon C. Physical activity in patients with deep venous thrombosis: a systematic review. Thromb. Res
. 2008; 122(6):763-73.
11. Kearon C, Kahn S, Agnelli G, et al
. Antithrombotic therapy for venous thromboembolic disease: American College of Chest Physicians evidenced-based clinical practice guidelines (8th edition). Chest
. 2008; 133:454-545.
12. Kemmler W, von Stengel S, Köckritz C, et al
. Effect of compression stockings on running performance in men runners. J. Strength Cond. Res
. 2009; 23(1):101-5.
13. Meyering C, Howard T. Hypercoagulability in athletes. Curr. Sports Med. Rep
. 2004; 3(2):77-83.
14. Miller JC. Diagnosis of lower extremity deep venous thrombosis. Radiol. Rounds
. 2005; 3(5):1-3.
15. Musani MH, Matta F, Yaekoub AY, et al
. Venous compression for prevention of postthrombotic syndrome: a meta-analysis. Am. J. Med
. 2010; 123(8):735-40.
16. O'Connor F, Wilder R. Textbook of Running Medicine
. New York: McGraw-Hill; 2001. p. 696.
17. Prandoni P, Polistena P, Bernardi E, et al
. Upper-extremity deep vein thrombosis: risk factors, diagnosis and complications. Arch. Intern. Med
. 1997; 157:57-62.
18. Ramzi DW, Leeper KV. DVT and pulmonary embolism: part I - diagnosis. Am. Fam. Phys
. 2004; 69(12):2829-36.
19. Roberts WO, Christie DM. Return to training and competition after deep venous calf thrombosis. Med. Sci. Sports Exerc
. 1992; 24(1):2-5.
20. Sachdeva A, Dalton M, Amaragiri S, Lees T. Elastic compression stockings for prevention of deep vein thrombosis. Coch. Data. Syst. Rev
. 2010; 7(7):CD001484.
21. Shrier I, Kahn SR. Effect of physical activity after recent deep venous thrombosis: a cohort study. Med. Sci. Sports Exerc
. 2005; 37(4):630-4.
22. Shrier I, Kahn SR, Steele RJ. Effect of early physical activity on long-term outcome after venous thrombosis. Clin. J. Sport Med
. 2009; 19(6):487-93.
23. Snead D, Marberry K, Rowdon G. Unique treatment regimen for effort thrombosis in the nondominant extremity of an overhead athlete. J. Athl. Train
. 2009; 44(1):94-7.
24. Stinar T, O'Connor F. DeWitt Army Community Hospital Sports Medicine Clinic Return to Running Program [Handout]. 2001.
25. Tao K, Davenport M. Deep venous thromboembolism in a triathlete. J. Emerg. Med
. 2010; 38(3):351-53.
26. Wells PS, Anderson DR. Value of assessment of pretest probability of deep-vein thrombosis in clinical management. Lancet
. 1997; 350(9094):1795-98.
27. Ziegler S, Schillinger M, Maca T, Minar E. Post-thrombotic syndrome after the primary event of deep venous thrombosis 10 to 20 years ago. Thromb. Res
. 2001; 101:23-33.