Obstetrics & Gynecology:
Venous Thromboembolism and Use of Prophylaxis Among Women Undergoing Laparoscopic Hysterectomy
Ritch, Jessica M. B. MD; Kim, Jin Hee MD; Lewin, Sharyn N. MD; Burke, William M. MD; Sun, Xuming MS; Herzog, Thomas J. MD; Wright, Jason D. MD
From the Divisions of Gynecologic Oncology and Gynecologic Surgery, Department of Obstetrics and Gynecology, Columbia University College of Physicians and Surgeons, New York, New York; and the Herbert Irving Comprehensive Cancer Center, New York, New York.
Corresponding author: Jason D. Wright, MD, Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Columbia University College of Physicians and Surgeons, 161 Fort Washington Ave, 8th Floor, New York, NY 10032; e-mail: email@example.com.
Financial Disclosure The authors did not report any potential conflicts of interest.
OBJECTIVE: To examine the risk of venous thromboembolism and the use of venous thromboembolism prophylaxis in women undergoing laparoscopic hysterectomy.
METHODS: Results of women recorded in a health outcomes, resource utilization, and quality database from 2003 to 2007 who underwent laparoscopic hysterectomy were analyzed. The rate and predictors of venous thromboembolism as well as patterns of venous thromboembolism prophylaxis were examined. Multivariable logistic regression models were developed to determine the incidence of venous thromboembolism and use of any prophylaxis, as well as pharmacologic prophylaxis.
RESULTS: Among 60,013 women, a total of 579 (1.0%) venous thromboembolism events were noted. Venous thromboembolism was diagnosed in 2.1% of women aged 60 years or older and in 2.3% of those with cancer. Women older than 60 years (OR 1.64, 95% CI 1.19–2.26) and with more medical comorbidities (OR 3.07, 95% CI 2.23–4.23) were most likely to have a venous thromboembolism develop. A total of 23,562 (39.3%) patients received no venous thromboembolism prophylaxis, 29,288 (48.8%) received mechanical prophylaxis, and 7,163 (11.9%) received pharmacologic prophylaxis. Women aged 60 years or older (OR 1.56, 95% CI 1.41–1.73), women with more medical comorbidities (OR 1.93, 95% CI 1.71–2.17), those with cancer (OR 3.08, 95% CI 2.75–3.45), and patients treated by high-volume surgeons (OR 1.42, 95% CI 1.33–1.52) were more likely to receive pharmacologic prophylaxis.
CONCLUSION: Whereas patients undergoing laparoscopic hysterectomy are overall at low risk for venous thromboembolism, older women, those with medical comorbidities, and women with cancer are at substantial risk. Venous thromboembolism prophylaxis is highly variable and often not utilized.
LEVEL OF EVIDENCE: III
Venous thromboembolism is the most common preventable cause of hospital-related death.1 In a study of more than seven million patients discharged from acute care hospitals across the United States, postoperative venous thromboembolism on average resulted in more than a 5-day increased length of stay, more than $20,000 in increased costs, and a more than six-fold increase in mortality.2 Over the course of the past three decades, a number of trials have shown that venous thromboembolism prophylaxis is highly efficacious in the prevention of deep venous thrombosis and pulmonary embolism.1
There is little evidence about the incidence of venous thromboembolism and use of prophylaxis against venous thromboembolism in women undergoing laparoscopic gynecologic surgery. Historically, the rate of venous thromboembolism in patients undergoing major open gynecologic surgery without prophylaxis is reported to range from 4% to 45%.1,3 In general surgery, the risk of venous thromboembolism is higher in open surgery compared with laparoscopic surgery. Patients undergoing open appendectomy are 1.8-times more likely to experience a venous thromboembolism, whereas those undergoing open antireflux surgery are more than 24-times more likely to experience a venous thromboembolism than when the procedure is performed laparoscopically.9
Given the apparent lower risk of venous thromboembolism with laparoscopic surgery, evidenced-based recommendations for prophylaxis in patients undergoing laparoscopic surgery have been inconsistent.1,10,11 The American College of Chest Physicians only recommends early ambulation for patients undergoing laparoscopic surgery, unless they have other risk factors for venous thromboembolism.1 In contrast, the European Association for Endoscopic Surgery recommends use of intermittent pneumatic compression devices for all laparoscopic cases lasting 2 hours or more, whereas the American College of Obstetricians and Gynecologists recommends using prophylaxis based on patient and procedure risk factors regardless of whether the procedure is performed open or laparoscopically.10,11
As more major gynecologic procedures are being performed laparoscopically, it is becoming increasingly important to understand the risk of venous thromboembolism in these patients. The objective of our study was to determine the incidence of venous thromboembolism after laparoscopic hysterectomy and investigate the patterns of use of venous thromboembolism prophylaxis in women undergoing these procedures.
MATERIALS AND METHODS
The Perspective database (health outcomes, resource utilization, and quality database) was used for analysis. The Perspective database is a nationwide, voluntary, fee-supported database developed to measure health outcomes, resource utilization, and quality. More than 500 acute care hospitals throughout the United States contribute data on inpatient hospital admissions. Electronic data updates are submitted on a quarterly basis by each participating institution. Regular audits are performed to ensure the quality and integrity of the source data. In addition to patient demographics, disease characteristics, and procedures, the database collects information on all billed services. As such, the database contains information on all drugs and medications, devices, radiologic tests, laboratory tests, and therapeutic services rendered during a patient's hospital stay. The database used in this study is validated and has been utilized in a number of outcomes studies.12,13 All data were de-identified and approved by the Columbia University Institutional Review Board.
We identified all women who underwent laparoscopic hysterectomy between 2003 and 2007. Patients who underwent laparoscopic subtotal hysterectomy (International Classification of Diseases, 9th Revision, Clinical Modification [ICD-9-CM] code 68.31), total laparoscopic hysterectomy (ICD-9-CM code 68.41), and laparoscopically assisted vaginal hysterectomy (ICD-9-CM code 68.51) were included and are referred to collectively as laparoscopic hysterectomy throughout. Patients who underwent a hysterectomy that was primarily an open procedure and patients who underwent a radical hysterectomy (either open or laparoscopic) were excluded from analysis. The cohort only included patients for whom the operating surgeon and the hospital where the procedure was performed could be identified.
The primary outcomes of interest were the occurrence of venous thromboembolic events and the use of venous thromboembolism prophylaxis. For the analysis of venous thromboembolism, we analyzed the occurrence of deep venous thromboses and pulmonary emboli. Venous thromboembolic events that occurred during the hospitalization of the surgery as well as those requiring readmission during a 60-day postoperative period were recorded.
Venous thromboembolism prophylaxis was stratified as none, mechanical, or pharmacologic. Patients who had either graduated compression stockings or intermittent pneumatic compression devices were coded as mechanical prophylaxis. Patients who received unfractionated heparin, low-molecular-weight heparin (including enoxaparin sodium, tinzaparin sodium, or dalteparin sodium), or fondaparinux sodium were classified as having received pharmacologic prophylaxis. Women who received mechanical prophylaxis in combination with pharmacologic prophylaxis were included in the pharmacologic prophylaxis cohort.
Predictor variables in the analysis included age (younger than 60 compared with 60 years of age or older), race (white, African American, other), year of diagnosis (2003–2005 compared with 2006–2007), primary payer (Medicare, Medicaid, commercial insurance, uninsured), marital status (married compared with single), and area of residence (Midwest, Northeast, South, West). Given the strong association between cancer and venous thromboembolism, we noted the presence of cancer, either of the female reproductive organs (ICD-9-CM codes 179–184.9) or colon and rectum (ICD-9-CM codes 153–154.8) for each patient. The performance of oophorectomy was noted for each patient. Comorbidity was estimated using the Charlson index.14 The Charlson index is a validated system to measure comorbidity in studies of administrative data. The ICD-9-CM coding for calculation of the Charlson index was based on the classification system developed by Deyo et al.15 Hospital characteristics including location (urban compared with rural), teaching status (teaching compared with nonteaching), and size (less than 350, 350–550, more than 550 beds) were analyzed.
The effects of surgeon volume and hospital volume were estimated using annualized procedural volume. Each hospital or surgeon's annual case volume was estimated by dividing the number of patients who underwent surgery by the number of years an individual hospital or surgeon contributed at least one laparoscopic procedure. The distribution of annual surgical volume was inspected visually and cut-points were selected to create tertiles of surgeon and hospital volume, each with similar numbers of patients: low-volume, intermediate-volume, and high-volume, as has been reported in previous work.16,17
The association between clinical and demographic variables and venous thromboembolic events and venous thromboembolism prophylaxis were compared using χ2 tests. Multivariable logistic regression models were developed to determine the clinical and demographic factors associated with the development of venous thromboembolism. For this analysis, thromboembolic events that occurred during the initial hospitalization or during the 60-day postoperative period were analyzed in aggregate. Similar multivariable logistic regression models were developed to determine factors associated with venous thromboembolism prophylaxis. Separate models examining any prophylaxis (mechanical or pharmacologic) and pharmacologic prophylaxis are reported. P<.05 was considered statistically significant. All analyses were performed with SAS 9.2 (SAS Institute).
A total of 60,013 women who underwent laparoscopic hysterectomy were identified. There were 579 (1.0%) total venous thromboembolism events. Deep venous thromboses were documented in 546 (0.9%) patients, whereas 45 women had a pulmonary embolism develop (0.1%). Of the 546 deep venous thromboses, 521 (95.4%) occurred during the initial hospitalization, whereas 25 (4.6%) occurred in the 60-day postoperative period. Of the 45 pulmonary embolisms, 27 (60.0%) occurred during the initial hospitalization, whereas 18 (40.0%) occurred in the 60-day postoperative period (Table 1).
Table 2 displays the association between clinical and demographic characteristics and the development of venous thromboembolism. Advanced age, later year of diagnosis, increased comorbidity, and residence in the Midwest were associated with an increased risk for venous thromboembolism (P<.05 for all). The odds ratio (OR) for venous thromboembolism in patients 60 years of age or older was 1.64 (95% confidence interval [CI] 1.19–2.26) compared with younger women, whereas the OR for patients with the most comorbidities was 3.07 (95% CI 2.23–4.23). Patients treated at teaching hospitals as well as those treated at medium or large hospitals were also at increased risk for the development of venous thromboembolism (P<.05 for all). Neither physician volume nor hospital volume was associated with the risk of a venous thromboembolism developing.
Overall, 23,562 (39.3%) women received no venous thromboembolism prophylaxis, 29,288 (48.8%) received mechanical prophylaxis, and 7,163 (11.9%) received pharmacologic prophylaxis (Table 3). Pharmacologic prophylaxis was more commonly administered to older patients, African American women, patients with Medicare, those with more recent diagnoses, patients residing in the northeast, those treated at urban and teaching hospitals, patients in medium hospitals, those with more comorbidities, patients who underwent oophorectomy, those with cancer, and patients treated by high-volume surgeons (P<.05 for all). Among women younger than 60 years of age, 10.6% received pharmacologic prophylaxis compared with 27.1% of those 60 years of age or older (P<.001). Use of pharmacologic prophylaxis increased from 9.8% between 2003 and 2005 to 14.0% during 2006–2007 (P<.001). Cancer patients received pharmacologic prophylaxis 45.2% of the time, whereas 32.5% of women in the highest comorbidity category received pharmacologic prophylaxis.
Similar findings were noted in the multivariable analysis (Table 4). Patients 60 years of age or older (OR 1.37, 95% CI 1.26–1.48), those in the highest comorbidity strata (OR 1.23, 95% CI 1.11–1.36), and women with cancer (OR 1.60, 95% CI 1.43–1.79) were more likely to receive some form (any) of prophylaxis. In contrast, patients treated at rural hospitals (OR 0.85, 95% CI 0.80–0.89), teaching facilities (OR 0.94, 95% CI 0.90–0.98), and large hospitals (OR 0.81, 95% CI 0.77–0.85) were less likely to receive any prophylaxis. Patients treated by high-volume surgeons (OR 0.85, 95% CI 0.81–0.89) and at high-volume hospitals (OR 0.85, 95% CI 0.81–0.89) were less likely to receive any prophylaxis.
We then specifically examined use of pharmacologic prophylaxis (Table 4). Patients older than 60 years of age (OR 1.56, 95% CI 1.41–1.73), those in the highest comorbidity strata (OR 1.93, 95% CI 1.71–2.17), patients with cancer (OR 3.08, 95% CI 2.75–3.45), and African American women (OR 1.19, 95% CI 1.09–1.30) were more likely to receive pharmacologic prophylaxis. Patients at rural hospitals (OR 1.17, 95% CI 1.08–1.27) were more likely to receive pharmacologic prophylaxis, whereas patients at large hospitals (OR 0.71, 95% CI 0.66–0.77) were less likely to receive pharmacologic prophylaxis. Although high-volume surgeons were more likely to administer pharmacologic prophylaxis (OR 1.42, 95% CI 1.33–1.52), hospital volume had no effect on the allocation of pharmacologic prophylaxis. The overall use of prophylaxis as well as pharmacologic prophylaxis both increased with time from 2003 to 2007.
Our findings demonstrate that venous thromboembolic disease occurs in approximately 1% of women who undergo laparoscopic hysterectomy. Certain subgroups of patients with classic risk factors appear to be at increased risk and have a substantially higher rate of venous thromboembolism. Previous work has generally reported a low incidence of venous thromboembolism after gynecologic laparoscopy.18–22 The Gynecologic Oncology Group's randomized trial of laparoscopic hysterectomy for endometrial cancer documented pulmonary emboli in 1% of women.22 An institutional series of women who underwent laparoscopic gynecologic surgery and received mechanical venous thromboembolism prophylaxis reported a 0.2% venous thromboembolism rate among women with benign disease and a 1.2% rate of venous thromboembolism in patients with cancer. The chance of venous thromboembolism increased with the technical complexity of the case, with no venous thromboembolisms in low-complexity cases, 0.5% in intermediate-complexity cases, and 2.8% in high-complexity cases.21 In our population-based analysis, we noted slightly higher rates of venous thromboembolism, 0.9% for benign procedures and 2.3% for laparoscopic hysterectomy for gynecologic cancer.
Although the overall venous thromboembolism rate in our study was relatively low, we noted several high-risk subgroups. Venous thromboembolic disease was documented in 2.1% of women 60 years of age or older, in 2.9% of patients in the highest comorbidity strata, and in 2.3% of patients with cancer. In general, the risk factors for venous thromboembolism after laparoscopic hysterectomy are similar to risk factors for major open gynecologic surgery.1 Other unexpected factors associated with an increased risk of venous thromboembolism included treatment later in the study period and surgery at teaching hospitals or at a larger hospital. These differences in the risk of venous thromboembolism likely reflect disparities in case mix. The risk profile we noted will be helpful in the development of risk stratification strategies.
Overall, the utilization of venous thromboembolism prophylaxis among women undergoing laparoscopic hysterectomy was relatively low. Nearly 40% of patients received no venous thromboembolism prophylaxis; among those who received prophylaxis, many women received only graduated compression stockings. Whereas the low rates of prophylaxis for laparoscopic hysterectomy may be partly attributable to the fact that clear and consistent recommendations for the appropriate prophylaxis are lacking, even in scenarios in which clear evidence-based recommendations are in place, venous thromboembolism prophylaxis is often underutilized.23–27 In a worldwide analysis, 93% of patients undergoing major surgery were at risk for venous thromboembolism, but only 62% received prophylaxis. In this trial, only 54% of women who underwent gynecologic surgery received prophylaxis.26,28
Despite the fact that the use of venous thromboembolism prophylaxis was low, encouragingly we noted that patients who were at highest risk for venous thromboembolism were more likely to receive prophylaxis. Whereas the type of surgical procedure performed appears to be the most important factor in influencing prophylaxis, a number of studies have suggested that age, race, socioeconomic status, and comorbidities also effect the allocation of prophylaxis.23,25–27,29 In addition to patient attributes, it appears that physician and hospital characteristics also influence the patterns of prophylaxis. In particular, we noted that physician volume was an important factor in prophylaxis; patients treated by high-volume physicians were more likely to receive pharmacologic prophylaxis. Our group has previously demonstrated that among patients undergoing open oncologic surgery, both hospital volume and physician volume strongly influence use of prophylaxis.30
We acknowledge several important limitations in our study. Because the primary purpose of administrative data is billing, it is likely that not all thromboembolic events were captured using ICD-9-CM coding.31 The underreporting of venous thromboembolism may have been further compounded in the 60-day perioperative window because patients who were admitted to other facilities for the treatment of venous thromboembolism would not have been captured in our dataset. Although our results undoubtedly underestimate the true incidence of venous thromboembolism, identification of additional events only would have augmented our findings and would have made a stronger argument for venous thromboembolism prophylaxis. We were unable to capture a number of important venous thromboembolism risk factors, including duration of surgery, weight, and previous venous thromboembolism. Additional limitations of administrative data include the inability to perform complete risk adjustment as well as the inability to separate venous thromboembolism prophylaxis from treatment. Given that venous thromboembolism only occurred in 1% of the cohort, it is unlikely that the miscategorization of venous thromboembolism treatment as prophylaxis would have led to substantially different results.
What is the optimal prophylaxis strategy for women undergoing laparoscopic hysterectomy? Although risk is relatively low, venous thromboembolism is a potentially catastrophic surgical complication and is a preventable cause of mortality, which may warrant the use of low-risk mechanical prophylaxis in all patients undergoing laparoscopic hysterectomy. Although the risk of prophylaxis is low, further comparative effectiveness studies incorporating cost and patient preferences are needed in patients at lower risk. Women with risk factors, such as age 60 years or older, multiple medical comorbidities, and cancer, are at substantial risk for the development of venous thromboembolism. We believe that pharmacologic prophylaxis should be considered in these women.1,32
In conclusion, our findings demonstrate that laparoscopic hysterectomy is associated with a higher risk of venous thromboembolism than reported in many previous studies. Patients with risk factors are at substantial risk for the development of thromboembolic events. Current patterns of venous thromboembolism prevention are highly variable across the United States and many women do not receive any type of venous thromboembolism prophylaxis. Venous thromboembolism prevention has become a major focus of quality improvement initiatives on a national level and prophylaxis should be considered in all women undergoing laparoscopic hysterectomy.
1. Geerts WH, Bergqvist D, Pineo GF, Heit JA, Samama CM, Lassen MR, et al. Prevention of venous thromboembolism: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition). Chest 2008;133:381S–453S.
2. Zhan C, Miller MR. Excess length of stay, charges, and mortality attributable to medical injuries during hospitalization. JAMA 2003;290:1868–74.
3. Greer IA. Epidemiology, risk factors and prophylaxis of venous thrombo-embolism in obstetrics and gynaecology. Baillieres Clin Obstet Gynaecol 1997;11:403–30.
4. Beebe DS, McNevin MP, Crain JM, Letourneau JG, Belani KG, Abrams JA, et al. Evidence of venous stasis after abdominal insufflation for laparoscopic cholecystectomy. Surg Gynecol Obstet 1993;176:443–7.
5. Nguyen NT, Owings JT, Gosselin R, Pevec WC, Lee SJ, Goldman C, et al. Systemic coagulation and fibrinolysis after laparoscopic and open gastric bypass. Arch Surg 2001;136:909–16.
6. Nguyen TN, Hinojosa M, Fayad C, Gray J, Murrell Z, Stamos M. Laparoscopic and thoracoscopic Ivor Lewis esophagectomy with colonic interposition. Ann Thorac Surg 2007;84:2120–4.
7. Rahr HB, Fabrin K, Larsen JF, Thorlacius-Ussing O. Coagulation and fibrinolysis during laparoscopic cholecystectomy. Thromb Res 1999;93:121–7.
8. Schietroma M, Carlei F, Mownah A, Franchi L, Mazzotta C, Sozio A, et al. Changes in the blood coagulation, fibrinolysis, and cytokine profile during laparoscopic and open cholecystectomy. Surg Endosc 2004;18:1090–6.
9. Nguyen NT, Hinojosa MW, Fayad C, Varela E, Konyalian V, Stamos MJ, et al. Laparoscopic surgery is associated with a lower incidence of venous thromboembolism compared with open surgery. Ann Surg 2007;246:1021–7.
10. Committee on Practice Bulletins-Gynecology, American College of Obstetricians and Gynecologists. ACOG Practice Bulletin No. 84: Prevention of deep vein thrombosis and pulmonary embolism. Obstet Gynecol 2007;110:429–40.
11. Neudecker J, Sauerland S, Neugebauer E, Bergamaschi R, Bonjer HJ, Cuschieri A, et al. The European Association for Endoscopic Surgery clinical practice guideline on the pneumoperitoneum for laparoscopic surgery. Surg Endosc 2002;16:1121–43.
12. Rothberg MB, Pekow PS, Lahti M, Brody O, Skiest DJ, Lindenauer PK. Antibiotic therapy and treatment failure in patients hospitalized for acute exacerbations of chronic obstructive pulmonary disease. JAMA 2010;303:2035–42.
13. Lindenauer PK, Rothberg MB, Pekow PS, Kenwood C, Benjamin EM, Auerbach AD. Outcomes of care by hospitalists, general internists, and family physicians. N Engl J Med 2007;357:2589–600.
14. Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987;40:373–83.
15. Deyo RA, Cherkin DC, Ciol MA. Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol 1992;45:613–9.
16. Hollenbeck BK, Wei Y, Birkmeyer JD. Volume, process of care, and operative mortality for cystectomy for bladder cancer. Urology 2007;69:871–5.
17. Birkmeyer JD, Sun Y, Wong SL, Stukel TA. Hospital volume and late survival after cancer surgery. Ann Surg 2007;245:777–83.
18. Ageno W, Manfredi E, Dentali F, Silingardi M, Ghezzi F, Camporese G, et al. The incidence of venous thromboembolism following gynecologic laparoscopy: a multicenter, prospective cohort study. J Thromb Haemost 2007;5:503–6.
19. Feng L, Song J, Wong F, Xia E. Incidence of deep venous thrombosis after gynaecological laparoscopy. Chin Med J (Engl) 2001;114:632–5.
20. Johnston K, Rosen D, Cario G, Chou D, Carlton M, Cooper M, et al. Major complications arising from 1265 operative laparoscopic cases: a prospective review from a single center. J Minim Invasive Gynecol 2007;14:339–44.
21. Nick AM, Schmeler KM, Frumovitz MM, Soliman PT, Spannuth WA, Burzawa JK, et al. Risk of thromboembolic disease in patients undergoing laparoscopic gynecologic surgery. Obstet Gynecol 2010;116:956–61.
22. Walker JL, Piedmonte MR, Spirtos NM, Eisenkop SM, Schlaerth JB, Mannel RS, et al. Laparoscopy compared with laparotomy for comprehensive surgical staging of uterine cancer: Gynecologic Oncology Group Study LAP2. J Clin Oncol 2009;27:5331–6.
23. Amin A, Stemkowski S, Lin J, Yang G. Appropriate thromboprophylaxis in hospitalized cancer patients. Clin Adv Hematol Oncol 2008;6:910–20.
24. Amin AN, Lin J, Ryan A. Need to improve thromboprophylaxis across the continuum of care for surgical patients. Adv Ther 2010;27:81–93.
25. Amin AN, Stemkowski S, Lin J, Yang G. Inpatient thromboprophylaxis use in U.S. hospitals: adherence to the seventh American College of Chest Physician's recommendations for at-risk medical and surgical patients. J Hosp Med 2009;4:E15–21.
26. Cohen AT, Tapson VF, Bergmann JF, Goldhaber SZ, Kakkar AK, Deslandes B, et al. Venous thromboembolism risk and prophylaxis in the acute hospital care setting (ENDORSE study): a multinational cross-sectional study. Lancet 2008;371:387–94.
27. Tapson VF, Decousus H, Pini M, Chong BH, Froehlich JB, Monreal M, et al. Venous thromboembolism prophylaxis in acutely ill hospitalized medical patients: findings from the International Medical Prevention Registry on Venous Thromboembolism. Chest 2007;132:936–45.
28. Kakkar AK, Cohen AT, Tapson VF, Bergmann JF, Goldhaber SZ, Deslandes B, et al. Venous thromboembolism risk and prophylaxis in the acute care hospital setting (ENDORSE survey): findings in surgical patients. Ann Surg 2010;251:330–8.
29. Kahn SR, Panju A, Geerts W, Pineo GF, Desjardins L, Turpie AG, et al. Multicenter evaluation of the use of venous thromboembolism prophylaxis in acutely ill medical patients in Canada. Thromb Res 2007;119:145–55.
30. Wright JD, Shah M, Burke WM, Sun X, Lewin SN, Herzog TJ. Quality of venous thromboembolism prophylaxis in patients undergoing gynecologic cancer surgery. 13th Biennial Meeting of the International Gynecologic Cancer Society. Prague (Czech Republic): International Gynecologic Cancer Society; 2010.
31. Leibson CL, Needleman J, Buerhaus P, Heit JA, Melton LJ 3rd, Naessens JM, et al. Identifying in-hospital venous thromboembolism (VTE): a comparison of claims-based approaches with the Rochester Epidemiology Project VGTE cohort. Med Care 2008;46:127–32.
32. Lyman GH, Khorana AA, Falanga A, Clarke-Pearson D, Flowers C, Jahanzeb M, et al. American Society of Clinical Oncology guideline: recommendations for venous thromboembolism prophylaxis and treatment in patients with cancer. J Clin Oncol 2007;25:5490–505.
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