Venous Thromboembolism and Atherothrombosis An Integrated Approach
2010; Lippincott Williams & Wilkins; Volume: 121; Issue: 19 Linguagem: Inglês
10.1161/circulationaha.110.951236
ISSN1524-4539
AutoresGregory Piazza, Samuel Z. Goldhaber,
Tópico(s)Cerebrovascular and Carotid Artery Diseases
ResumoHomeCirculationVol. 121, No. 19Venous Thromboembolism and Atherothrombosis An Integrated Approach Free AccessReview ArticlePDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessReview ArticlePDF/EPUBVenous Thromboembolism and Atherothrombosis An Integrated Approach Gregory Piazza, MD and Samuel Z. Goldhaber, MD Gregory PiazzaGregory Piazza From the Cardiovascular Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Mass. and Samuel Z. GoldhaberSamuel Z. Goldhaber From the Cardiovascular Division, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Mass. Originally published18 May 2010https://doi.org/10.1161/CIRCULATIONAHA.110.951236Circulation. 2010;121:2146–2150Case presentation 1: A 45-year-old man with a history of obesity, hypertension, dyslipidemia, deep vein thrombosis (DVT) complicated by pulmonary embolism (PE) 12 years earlier, and non–ST-elevation myocardial infarction treated with angioplasty and stenting of the left anterior descending coronary artery 4 years earlier presented to the emergency department with sudden onset of substernal chest pain. His ECG showed anterolateral ST-segment elevation, and emergent coronary angiography demonstrated in-stent thrombosis of his left anterior descending coronary artery (Figure 1A). Download figureDownload PowerPointFigure 1. Coronary angiography of the left coronary system, anterior-posterior cranial view. Total occlusion of the left anterior descending artery (arrow) was observed at the origin of the previously stented midsegment and was consistent with in-stent thrombosis (A). The occlusion was treated successfully with angioplasty and stenting (B).Case Presentation 2: A 39-year-old man with a history of cigarette smoking, hypertension, dyslipidemia, and non–ST-elevation myocardial infarction 3 years earlier presented with progressive dyspnea and several hours of chest pressure. His ECG was unchanged, but his cardiac troponin I was elevated at 1.33 ng/mL (normal <0.1 ng/mL). Contrast-enhanced chest computed tomography demonstrated a large saddle PE (Figure 2). Download figureDownload PowerPointFigure 2. Contrast-enhanced chest computed tomography demonstrating a large saddle PE straddling the bifurcation of the main pulmonary artery and extending into the right main pulmonary artery and lobar branches (A). Extensive thrombus (arrows) occluding the left main pulmonary artery and distal right pulmonary artery branches was observed (B).OverviewVenous thromboembolism (VTE), including DVT and PE, is the third most common cardiovascular disorder after coronary artery disease and stroke. Furthermore, patients with acute coronary syndromes or stroke have an increased risk of VTE as a complication of hospitalization.1 Many risk factors for VTE, such as obesity, hypertension, dyslipidemia, diabetes, and smoking, overlap with those for atherothrombosis. Data from registry analyses and clinical trials suggest that clinicians should abandon "silo thinking" regarding VTE risk factors and integrate cardiovascular risk reduction strategies from coronary artery disease and stroke into the prevention of DVT and PE. As a novel paradigm, VTE is best considered as part of a pan-cardiovascular syndrome that includes coronary artery disease, peripheral artery disease, and cerebrovascular disease.Risk FactorsThe association of atherothrombosis and VTE was first suggested by Prandoni and colleagues,2 who found that the presence of carotid artery plaque was associated with a doubling in the risk of VTE. A subsequent study demonstrated that the risk of acute myocardial infarction is 4-fold higher among patients with a prior history of VTE than among those without such a history.3 Similarly, the risk of stroke is also increased after an initial VTE event.4Shared risk factors help explain the increased risk of VTE in patients with atherothrombosis and the greater frequency of myocardial infarction and stroke in patients who have had DVT or PE. Established cardiovascular risk factors, including obesity, hypertension, dyslipidemia, diabetes mellitus, the metabolic syndrome, and tobacco use, also increase the risk of VTE. In addition, postmenopausal hormone replacement and hormonal contraceptive therapy increase the risk of atherothrombosis and VTE.Obesity, a well-established risk factor for atherothrombosis, increases the risk of VTE. In a meta-analysis of 63 552 patients from 21 studies, obesity was associated with a doubling in VTE risk.5 In a cohort study from the US National Hospital Discharge Survey, obese women had a greater risk of DVT than obese men.6 In the all-female Nurses' Health Study, obesity tripled the risk of unprovoked PE.7Hypertension predisposes to both atherothrombosis and VTE. Hypertension is associated with a 50% increase in the risk of VTE.5 In the Nurses' Health Study, hypertension was associated with a 2-fold increase in the risk of unprovoked PE.7HDL cholesterol levels in particular are significantly lower in patients who experience VTE.5 Diabetes mellitus has been associated with a 42% increase in the risk of DVT or PE.5 A case-control study of 208 VTE patients and 300 control subjects from Korea demonstrated that both low levels of HDL cholesterol and elevated fasting glucose correlated with a doubling in the risk of VTE.8The metabolic syndrome has emerged as a potent risk factor for atherothrombosis that affects up to 45% of the US population over 50 years old.9 Recent data also implicate the metabolic syndrome as a risk factor for VTE. A registry of 20 374 patients demonstrated that the metabolic syndrome increased the risk of VTE by 84%.10 However, abdominal adiposity, a prominent feature of the metabolic syndrome, accounted for the majority of the increased risk in men and was associated with a significantly increased risk of VTE in women.10 The metabolic syndrome was associated with a 50% increase in the risk of any VTE and a 70% greater risk of an unprovoked event in a large Korean population.8Although a heart-healthy diet constitutes an important component of risk reduction in atherothrombosis, the contribution of nutritional factors to the risk of VTE has received scant attention. In a prospective study conducted over 12 years, 14 962 patients underwent assessments of dietary intake and were followed up for incident VTE.11 Greater daily consumption of fruits and vegetables was associated with a declining risk of VTE.11 Eating fish at least once weekly was associated with a 30% to 45% reduction in the incidence of VTE.11 The risk of VTE increased with greater consumption of red and processed meats.11 The top quintile of meat eaters had double the risk of DVT or PE compared with the bottom quintile.11Hormonal contraception and replacement therapy have been linked to VTE and atherothrombotic events. Oral contraceptive pills, especially those that contain third-generation progestins, increase the risk of VTE.12 In the Women's Health Initiative, women receiving estrogen-plus-progestin hormone replacement therapy demonstrated a 2-fold increase in the risk of VTE compared with those in the placebo group.13Additional atherothrombotic risk factors of tobacco use and stress also increase the risk of VTE. Smoking is a particularly potent VTE risk factor among women, doubling the risk of unprovoked PE for those who smoke 25 to 34 cigarettes daily and tripling the risk for those who smoke 35 or more cigarettes daily compared with never-smokers.7 In a prospective cohort study of 6958 Swedish men followed up for 28 years, persistent stress was independently associated with an increased frequency of PE.14PathophysiologyIn addition to having risk factors in common, VTE and atherothrombosis demonstrate shared pathophysiology (Figure 3). Inflammation, systemic and local hypercoagulability, and endothelial injury play integral mechanistic roles in the pathophysiology of atherothrombosis. An improved understanding of VTE integrates these same pathophysiological processes. Download figureDownload PowerPointFigure 3. A common pathophysiology of VTE and atherothrombosis.The role of inflammation in the pathogenesis of VTE has long been suspected on the basis of the observation of an increased frequency of DVT and PE in patients with chronic inflammatory disorders such as inflammatory bowel disease and systemic vasculitis. Elevations in C-reactive protein, a sensitive marker of systemic inflammation, have been linked to an increased risk of VTE. In an analysis of 10 505 participants in the Atherosclerosis Risk In Communities (ARIC) Study followed up for incident DVT or PE over 8.3 years, elevated C-reactive protein above the 90th percentile was associated with a 76% increase in the risk of VTE versus lower percentiles.15 Elevations in systemic inflammatory markers, including C-reactive protein, fibrinogen, and factor VIII, are particularly prevalent in patients who experience unprovoked DVT or PE compared with those with secondary VTE.16 Polymorphisms in genes encoding factor VII, interleukin-1β, and interleukin-10 modify the risk of unprovoked VTE.17 In an analysis of the randomized, controlled JUPITER study (Justification for the Use of statins in Prevention: an Intervention Trial Evaluating Rosuvastatin), rosuvastatin (20 mg orally daily) reduced the rate of symptomatic VTE by 43% in patients with elevated C-reactive protein and LDL cholesterol levels <130 mg/dL compared with placebo.18Hypercoagulability has been well established in the pathogenesis of VTE. Inherited thrombophilias, including activated protein C resistance due to factor V Leiden mutation, prothrombin gene mutation, and deficiencies of protein C, protein S, and antithrombin III, increase the risk of VTE. Although hyperhomocysteinemia may be inherited due to a deficiency in methylenetetrahydrofolate reductase, it is most often acquired because of dietary folate deficiency and has been associated with both VTE and atherothrombosis. Antiphospholipid antibody syndrome is an acquired thrombophilia that increases the risk for both VTE and arterial thromboembolism.Endothelial injury plays a pathophysiological role in the development of VTE. Traumatic injury to the extremity may result in DVT due to a combination of local endothelial injury and immobility. However, even minor lower-extremity injuries that are not associated with surgery, limb casting, or immobility may increase the risk of DVT up to 5 times that of subjects without such trauma.19 Local endothelial injury from pacemaker and internal cardiac defibrillator leads and long-term indwelling central venous catheters increase the risk of upper-extremity DVT.20PreventionPreventive efforts should begin with lifestyle measures to reduce the risk of VTE and atherothrombotic events. Overweight and obese patients should be counseled regarding diet and exercise to achieve sustained weight reduction. We advise our coronary heart disease and VTE patients to reduce their intake of red and processed meats and to increase consumption of fish, fruits, and vegetables.11 We counsel them regarding tobacco cessation and offer prescription of pharmacological aids and referral to support groups. Finally, referral for stress management and relaxation techniques may be beneficial.Pharmacotherapeutic interventions for prevention of cardiovascular events in patients with VTE or atherothrombosis include treatment of risk factors and anticoagulation. Cardiovascular risk factors of hypertension, dyslipidemia, and diabetes should be treated according to goals set forth by guideline recommendations. In the JUPITER trial, rosuvastatin decreased the frequency of VTE events among nondyslipidemic patients with elevated C-reactive protein levels, which suggests that statins may reduce risk through modulation of inflammatory pathways.18Anticoagulation should be considered in patients who have had VTE according to the risk for recurrence. Patients who have had unprovoked, or idiopathic, VTE benefit from indefinite-duration anticoagulation because of a high rate of recurrent events.21–23 Patients with a history of provoked events due to trauma, surgery, or immobilization usually receive time-limited anticoagulation (often for 6 months) but require meticulous attention to VTE prophylaxis during subsequent high-risk situations such as hospitalization for medical illness. Although antiplatelet agents are not effective in reducing the risk of VTE, they do help prevent atherothrombosis. Some patients will require "triple therapy" with warfarin, aspirin, and clopidogrel or prasugrel.Patients who have experienced atherothrombotic events represent an underrecognized population at risk for VTE. In an analysis of the Healthcare Cost and Utilization Project Nationwide Inpatient Sample database, more than 1 million patients with atherothrombotic cardiovascular disease, including myocardial infarction and stroke, were at risk for VTE, which constitutes one of the largest proportions of hospitalized medical patients.1 Despite guideline recommendations for prevention of DVT and PE in hospitalized medical patients,24,25 including those with atherothrombotic cardiovascular disease, VTE prophylaxis remains underutilized.26,27 Implementation of computerized and "human"-based decision support strategies can improve VTE prophylaxis use in this vulnerable patient population.28–30Policy ImplicationsThe link between atherothrombosis and VTE has public healthcare policy implications. In 2008, the US Surgeon General issued the "Call to Action to Prevent Deep Vein Thrombosis and Pulmonary Embolism" and estimated that 100 000 to 180 000 PE deaths occur annually in the United States alone.31 He cited PE as the most preventable cause of death among hospitalized patients.Identification of individuals with established atherothrombotic cardiovascular disease or with risk factors for atherothrombotic cardiovascular disease provides additional targets for VTE prevention efforts. VTE complicating hospitalization for medical illness such as myocardial infarction and stroke burdens the healthcare system.32 Medicare has classified DVT and PE that occur after total knee or hip replacement as a "never event" and has stopped reimbursing hospitals for the additional costs incurred by this complication.33 A similar policy eventually could be applied to VTE that complicates a hospitalization for common medical illnesses such as myocardial infarction and stroke. Furthermore, the Joint Commission has placed increasing emphasis on VTE prevention as a critical patient safety issue. An improved understanding of the link between atherothrombotic cardiovascular disease and VTE provides clinicians with the ability to identify a previously underrecognized patient population at risk for DVT and PE. Fortunately, effective strategies can be implemented to reduce the frequency of these common cardiovascular illnesses.Case ResolutionsCasepresentation 1: This patient was treated successfully with emergent coronary angioplasty and stent placement in the left anterior descending coronary artery (Figure 1B). Aspirin and clopidogrel were added to his medication regimen, along with continued warfarin.Case presentation 2: This patient was treated successfully for acute PE (Figure 2) with intravenous unfractionated heparin as a "bridge" to warfarin. Because his PE was idiopathic and unprovoked, warfarin was continued for indefinite duration.Case presentations 1 and 2: Both patients were treated for pan-cardiovascular disease with aggressive risk factor reduction, including weight reduction, hypertension control, smoking cessation, lipid lowering, and counseling about diet and exercise. They were educated that a heart-healthy lifestyle is critical for the prevention of both myocardial infarction and PE.Guest Editor for this article was Elliott M. Antman, MD.Sources of FundingDr Piazza is supported by a Research Career Development Award (K12 HL083786) from the National Heart, Lung, and Blood Institute.DisclosuresNone.FootnotesCorrespondence to Gregory Piazza, MD, Cardiovascular Division, Brigham and Women's Hospital, 75 Francis St, Boston, MA 02115. E-mail [email protected] References 1 Piazza G, Fanikos J, Zayaruzny M, Goldhaber SZ. Venous thromboembolic events in hospitalised medical patients. Thromb Haemost. 2009; 102: 505–510.CrossrefMedlineGoogle Scholar2 Prandoni P, Bilora F, Marchiori A, Bernardi E, Petrobelli F, Lensing AW, Prins MH, Girolami A. An association between atherosclerosis and venous thrombosis. N Engl J Med. 2003; 348: 1435–1441.CrossrefMedlineGoogle Scholar3 Spencer FA, Ginsberg JS, Chong A, Alter DA. The relationship between unprovoked venous thromboembolism, age, and acute myocardial infarction. J Thromb Haemost. 2008; 6: 1507–1513.MedlineGoogle Scholar4 Sorensen HT, Horvath-Puho E, Pedersen L, Baron JA, Prandoni P. Venous thromboembolism and subsequent hospitalisation due to acute arterial cardiovascular events: a 20-year cohort study. Lancet. 2007; 370: 1773–1779.CrossrefMedlineGoogle Scholar5 Ageno W, Becattini C, Brighton T, Selby R, Kamphuisen PW. Cardiovascular risk factors and venous thromboembolism: a meta-analysis. Circulation. 2008; 117: 93–102.LinkGoogle Scholar6 Stein PD, Beemath A, Olson RE. Obesity as a risk factor in venous thromboembolism. Am J Med. 2005; 118: 978–980.CrossrefMedlineGoogle Scholar7 Goldhaber SZ, Grodstein F, Stampfer MJ, Manson JE, Colditz GA, Speizer FE, Willett WC, Hennekens CH. A prospective study of risk factors for pulmonary embolism in women. JAMA. 1997; 277: 642–645.CrossrefMedlineGoogle Scholar8 Jang MJ, Choi WI, Bang SM, Lee T, Kim YK, Ageno W, Oh D. Metabolic syndrome is associated with venous thromboembolism in the Korean population. Arterioscler Thromb Vasc Biol. 2009; 29: 311–315.LinkGoogle Scholar9 Dentali F, Squizzato A, Ageno W. The metabolic syndrome as a risk factor for venous and arterial thrombosis. Semin Thromb Hemost. 2009; 35: 451–457.CrossrefMedlineGoogle Scholar10 Steffen LM, Cushman M, Peacock JM, Heckbert SR, Jacobs DR Jr, Rosamond WD, Folsom AR. Metabolic syndrome and risk of venous thromboembolism: Longitudinal Investigation of Thromboembolism Etiology. J Thromb Haemost. 2009; 7: 746–751.CrossrefMedlineGoogle Scholar11 Steffen LM, Folsom AR, Cushman M, Jacobs DR Jr, Rosamond WD. Greater fish, fruit, and vegetable intakes are related to lower incidence of venous thromboembolism: the Longitudinal Investigation of Thromboembolism Etiology. Circulation. 2007; 115: 188–195.LinkGoogle Scholar12 Vandenbroucke JP, Rosing J, Bloemenkamp KW, Middeldorp S, Helmerhorst FM, Bouma BN, Rosendaal FR. Oral contraceptives and the risk of venous thrombosis. N Engl J Med. 2001; 344: 1527–1535.CrossrefMedlineGoogle Scholar13 Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA. 2002; 288: 321–333.CrossrefMedlineGoogle Scholar14 Rosengren A, Freden M, Hansson PO, Wilhelmsen L, Wedel H, Eriksson H. Psychosocial factors and venous thromboembolism: a long-term follow-up study of Swedish men. J Thromb Haemost. 2008; 6: 558–564.CrossrefMedlineGoogle Scholar15 Folsom AR, Lutsey PL, Astor BC, Cushman M. C-reactive protein and venous thromboembolism: a prospective investigation in the ARIC cohort. Thromb Haemost. 2009; 102: 615–619.CrossrefMedlineGoogle Scholar16 Luxembourg B, Schmitt J, Humpich M, Glowatzki M, Dressler D, Seifried E, Lindhoff-Last E. Cardiovascular risk factors in idiopathic compared to risk-associated venous thromboembolism: a focus on fibrinogen, factor VIII, and high-sensitivity C-reactive protein (hs-CRP). Thromb Haemost. 2009; 102: 668–675.CrossrefMedlineGoogle Scholar17 Zee RY, Glynn RJ, Cheng S, Steiner L, Rose L, Ridker PM. An evaluation of candidate genes of inflammation and thrombosis in relation to the risk of venous thromboembolism: the Women's Genome Health Study. Circ Cardiovasc Genet. 2009; 2: 57–62.LinkGoogle Scholar18 Glynn RJ, Danielson E, Fonseca FA, Genest J, Gotto AM Jr, Kastelein JJ, Koenig W, Libby P, Lorenzatti AJ, MacFadyen JG, Nordestgaard BG, Shepherd J, Willerson JT, Ridker PM. A randomized trial of rosuvastatin in the prevention of venous thromboembolism. N Engl J Med. 2009; 360: 1851–1861.CrossrefMedlineGoogle Scholar19 van Stralen KJ, Rosendaal FR, Doggen CJ. Minor injuries as a risk factor for venous thrombosis. Arch Intern Med. 2008; 168: 21–26.CrossrefMedlineGoogle Scholar20 Joffe HV, Kucher N, Tapson VF, Goldhaber SZ. Upper-extremity deep vein thrombosis: a prospective registry of 592 patients. Circulation. 2004; 110: 1605–1611.LinkGoogle Scholar21 Schulman S, Wahlander K, Lundstrom T, Clason SB, Eriksson H. Secondary prevention of venous thromboembolism with the oral direct thrombin inhibitor ximelagatran. N Engl J Med. 2003; 349: 1713–1721.CrossrefMedlineGoogle Scholar22 Ridker PM, Goldhaber SZ, Danielson E, Rosenberg Y, Eby CS, Deitcher SR, Cushman M, Moll S, Kessler CM, Elliott CG, Paulson R, Wong T, Bauer KA, Schwartz BA, Miletich JP, Bounameaux H, Glynn RJ. Long-term, low-intensity warfarin therapy for the prevention of recurrent venous thromboembolism. N Engl J Med. 2003; 348: 1425–1434.CrossrefMedlineGoogle Scholar23 Kearon C, Ginsberg JS, Kovacs MJ, Anderson DR, Wells P, Julian JA, MacKinnon B, Weitz JI, Crowther MA, Dolan S, Turpie AG, Geerts W, Solymoss S, van Nguyen P, Demers C, Kahn SR, Kassis J, Rodger M, Hambleton J, Gent M. Comparison of low-intensity warfarin therapy with conventional-intensity warfarin therapy for long-term prevention of recurrent venous thromboembolism. N Engl J Med. 2003; 349: 631–639.CrossrefMedlineGoogle Scholar24 Geerts WH, Bergqvist D, Pineo GF, Heit JA, Samama CM, Lassen MR, Colwell CW. Prevention of venous thromboembolism: American College of Chest Physicians evidence-based clinical practice guidelines (8th edition). Chest. 2008; 133: 381S–453S.CrossrefMedlineGoogle Scholar25 Cardiovascular Disease Educational and Research Trust; Cyprus Cardiovascular Disease Educational and Research Trust; European Venous Forum; International Surgical Thrombosis Forum; International Union of Angiology; Union Internationale de Phlébologie. Prevention and treatment of venous thromboembolism: International Consensus Statement (guidelines according to scientific evidence). Int Angiol. 2006; 25: 101–161.MedlineGoogle Scholar26 Piazza G, Seddighzadeh A, Goldhaber SZ. Double trouble for 2,609 hospitalized medical patients who developed deep vein thrombosis: prophylaxis omitted more often and pulmonary embolism more frequent. Chest. 2007; 132: 554–561.CrossrefMedlineGoogle Scholar27 Cohen AT, Tapson VF, Bergmann JF, Goldhaber SZ, Kakkar AK, Deslandes B, Huang W, Zayaruzny M, Emery L, Anderson FA Jr. Venous thromboembolism risk and prophylaxis in the acute hospital care setting (ENDORSE study): a multinational cross-sectional study. Lancet. 2008; 371: 387–394.CrossrefMedlineGoogle Scholar28 Piazza G, Rosenbaum EJ, Pendergast W, Jacobson JO, Pendleton RC, McLaren GD, Elliott CG, Stevens SM, Patton WF, Dabbagh O, Paterno MD, Catapane E, Li Z, Goldhaber SZ. Physician alerts to prevent symptomatic venous thromboembolism in hospitalized patients. Circulation. 2009; 119: 2196–2201.LinkGoogle Scholar29 Piazza G, Goldhaber SZ. Computerized decision support for the cardiovascular clinician: applications for venous thromboembolism prevention and beyond. Circulation. 2009; 120: 1133–1137.LinkGoogle Scholar30 Kucher N, Koo S, Quiroz R, Cooper JM, Paterno MD, Soukonnikov B, Goldhaber SZ. Electronic alerts to prevent venous thromboembolism among hospitalized patients. N Engl J Med. 2005; 352: 969–977.CrossrefMedlineGoogle Scholar31 The surgeon general's call to action to prevent deep vein thrombosis and pulmonary embolism. US Department of Health and Human Services; 2008. Available at: www.surgeongeneral.gov/topics/deepvein/calltoaction/call-to-action-on-dvt-2008.pdf. Accessed November 30, 2008.Google Scholar32 MacDougall DA, Feliu AL, Boccuzzi SJ, Lin J. Economic burden of deep-vein thrombosis, pulmonary embolism, and post-thrombotic syndrome. Am J Health Syst Pharm. 2006; 63: S5–S15.CrossrefGoogle Scholar33 Sutedjo JL, Ng RK, Piazza G, Goldhaber SZ. Medicare's new regulations for deep vein thrombosis as a "never event": wise or worrisome? Am J Med. 2009; 122: 975–976.CrossrefMedlineGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Hu S, Tan J, Hu M, Guo T, Chen L, Hua L and Cao J (2023) The Causality between Diabetes and Venous Thromboembolism: A Bidirectional Two-Sample Mendelian Randomization Study, Thrombosis and Haemostasis, 10.1055/a-2040-4850 Jaiswal V, Batra N, Dagar M, Butey S, Huang H, Chia J, Naz S, Endurance E, Raj N, Patel S, Maroo D, Ang S, Hanif M, Mukherjee D, Sarfraz Z, Shrestha A and Song D (2023) Inflammatory bowel disease and associated cardiovascular disease outcomes: A systematic review, Medicine, 10.1097/MD.0000000000032775, 102:6, (e32775), Online publication date: 10-Feb-2023. Migita S, Okumura Y, Fukuda I, Nakamura M, Yamada N, Takayama M, Maeda H, Yamashita T, Ikeda T, Mo M, Yamazaki T and Hirayama A (2023) Relationship between baseline D-dimer and prognosis in Japanese patients with venous thromboembolism: Insights from the J'xactly study, Frontiers in Cardiovascular Medicine, 10.3389/fcvm.2023.1074661, 10 Turpie A, Farjat A, Haas S, Ageno W, Weitz J, Goldhaber S, Goto S, Angchaisuksiri P, Kayani G, Lopes R, Chiang C, Gibbs H, Tse E, Verhamme P, ten Cate H, Muntaner J, Schellong S, Bounameaux H, Prandoni P, Maheshwari U, Kakkar A, Loualidi A, Colak A, Bezuidenhout A, Abdool-Carrim A, Azeddine A, Beyers A, Dees A, Mohamed A, Aksoy A, Abiko A, Watanabe A, Krichell A, Fernandez A, Tosetto A, Khotuntsov A, Oropallo A, Slocombe A, Kelly A, Clark A, Gad A, Arouni A, Schmidt A, Berni A, Kleiban A, Machowski A, Kazakov A, Galvez A, Lockman A, Falanga A, Chauhan A, Riera-Mestre A, Mazzone A, D'Angelo A, Herdy A, Kato A, Salem A, Husin A, Erdelyi B, Jacobson B, Amann-Vesti B, Battaloglu B, Wilson B, Cosmi B, Francois B, Toufek B, Hunt B, Natha B, Mustafa B, Kho B, Carine B, Zidel B, Dominique B, Christophe B, Trimarco B, Luo C, Cuneo C, Diaz C, Schwencke C, Cader C, Yavuz C, Zaidman C, Lunn C, Wu C, Toh C, Chiang C, Elisa C, Hsia C, Huang C, Kwok C, Wu C, Huang C, Ward C, Opitz C, Jeanneret-Gris C, Ha C, Huang C, Bidi C, Smith C, Brauer C, Lodigiani C, Francis C, Wu C, Staub D, Theodoro D, Poli D, Acevedo D, Adler D, Jimenez D, Keeling D, Scott D, Imberti D, Creagh D, Helene D, Hagemann D, Le Roux D, Skowasch D, Belenky D, Dorokhov D, Petrov D, Zateyshchikov D, Prisco D, Møller D, Kucera D, Esheiba E, Panchenko E, Dominique E, Dogan E, Kubat E, Diaz E, Tse E, Yeo E, Hashas E, Grochenig E, Tiraferri E, Blessing E, Michèle E, Usandizaga E, Porreca E, Ferroni F, Nicolas F, Ayala-Paredes F, Koura F, Henry F, Cosmi F, Erdkamp F, Kamalov G, Dalmau G, Damien G, Klein G, Shah G, Hollanders G, Merli G, Plassmann G, Platt G, Poirier G, Sokurenko G, Haddad G, Ali G, Agnelli G, Gan G, Kaye-Eddie G, Le Gal G, Allen G, Esperón G, Jean-Paul G, Gerofke H, Elali H, Burianova H, Ohler H, Wang H, Darius H, Gogia H, Striekwold H, Gibbs H, Hasanoglu H, Turker H, Franow H, Bounameaux H, De Raedt H, Schroe H, ElDin H, Zidan H, Nakamura H, Kim H, Lawall H, Zhu H, Tian H, Yhim H, ten Cate H, Hwang H, Shim H, Kim I, Libov I, Sonkin I, Suchkov I, Song I, Kiris I, Staroverov I, Looi I, De La Azuela Tenorio I, Savas I, Gordeev I, Podpera I, Lee J, Sathar J, Welker J, Beyer-Westendorf J, Kvasnicka J, Vanwelden J, Kim J, Svobodova J, Gujral J, Marino J, Galvar J, Kassis J, Kuo J, Shih J, Kwon J, Joh J, Park J, Kim J, Yang J, Krupicka J, Lastuvka J, Pumprla J, Vesely J, Souto J, Correa J, Duchateau J, Fletcher J, del Toro J, del Toro J, Paez J, Nielsen J, Filho J, Saraiva J, Peromingo J, Lara J, Fedele J, Surinach J, Chacko J, Muntaner J, Benitez J, Abril J, Humphrey J, Bono J, Kanda J, Boondumrongsagoon J, Yiu K, Chansung K, Boomars K, Burbury K, Kondo K, Karaarslan K, Takeuchi K, Kroeger K, Zrazhevskiy K, Svatopluk K, Shyu K, Vandenbosch K, Chang K, Chiu K, Jean-Manuel K, Wern K, Ueng K, Norasetthada L, Binet L, Chew L, Zhang L, Cristina L, Tick L, Schiavi L, Wong L, Borges L, Botha L, Capiau L, Timmermans L, López L, Ria L, Blasco L, Guzman L, Cervera L, Isabelle M, Bosch M, de los Rios Ibarra M, Fernandez M, Carrier M, Barrionuevo M, Gamba M, Cattaneo M, Moia M, Bowers M, Chetanachan M, Berli M, Fixley M, Faghih M, Stuecker M, Schul M, Banyai M, Koretzky M, Myriam M, Gaffney M, Hirano M, Kanemoto M, Nakamura M, Tahar M, Emmanuel M, Kovacs M, Leahy M, Levy M, Munch M, Olsen M, De Pauw M, Gustin M, Van Betsbrugge M, Boyarkin M, Homza M, Koto M, Abdool-Gaffar M, Nagib M, El-Dessoki M, Khan M, Mohamed M, Kim M, Lee M, Soliman M, Ahmed M, el Bary M, Moustafa M, Hameed M, Kanko M, Majumder M, Zubareva N, Mumoli N, Abdullah N, Makruasi N, Paruk N, Kanitsap N, Duda N, Nordin N, Nyvad O, Barbarash O, Gurbuz O, Vilamajo O, Flores O, Gur O, Oto O, Marchena P, Angchaisuk
Referência(s)