Download PDF
Semin Thromb Hemost 2009; 35(7): 597-604
DOI: 10.1055/s-0029-1242713
© Thieme Medical Publishers

Unsuspected Triggers of Venous Thromboembolism—Trivial or Not So Trivial?

Giuseppe Lippi1 , Massimo Franchini2 , Emmanuel J. Favaloro3
  • 1U.O. Diagnostica Ematochimica, Dipartimento di Patologia e Medicina di Laboratorio, Azienda Ospadaliero-Universitaria di Parma, Parma, Italy
  • 2Servizio di Immunoematologia e Trasfusione, Azienda Ospedaliero-Universitaria di Parma, Italy
  • 3Department of Haematology, Institute of Clinical Pathology and Medical Research (ICPMR), Westmead Hospital, Westmead, Australia
Further Information

Publication History

Publication Date:
09 December 2009 (online)

    Permissions and Reprints

ABSTRACT

Venous thromboembolism (VTE) can be considered a multifactorial disorder involving a variety of inherited and acquired prothrombotic conditions and events. Although greater emphasis has classically been given to traditional thrombophilic risk factors, there is increasing recognition of less typical precipitating conditions and events. Indeed, the list of plausible but unusual triggers of thrombosis includes sneezing and coughing attacks, eating, migraine, sexual intercourse, strenuous physical exercise, drug abuse, and defecation. Although it is difficult to assert conclusively the true contribution of such events to the etiology of acute episodes of venous thrombosis, it seems reasonable to conclude that the concomitant presence of such trivial elements with one or more additional risk factors for VTE might precipitate an acute thrombotic episode.

KEYWORDS

Deep vein thrombosis - pulmonary embolism - risk factor - thrombosis - trigger - venous thromboembolism

REFERENCES

  • 1 Bernardi E, Pesavento R, Prandoni P. Upper extremity deep venous thrombosis.  Semin Thromb Hemost. 2006;  32(7) 729-736
    Article in Thieme ConnectPubMedGoogle Scholar
  • 2 Lippi G, Franchini M. Pathogenesis of venous thromboembolism: when the cup runneth over.  Semin Thromb Hemost. 2008;  34(8) 747-761
    Article in Thieme ConnectPubMedGoogle Scholar
  • 3 Lussana F, Dentali F, Ageno W, Kamphuisen P W. Venous thrombosis at unusual sites and the role of thrombophilia.  Semin Thromb Hemost. 2007;  33(6) 582-587
    Article in Thieme ConnectPubMedGoogle Scholar
  • 4 Primignani M, Mannucci P M. The role of thrombophilia in splanchnic vein thrombosis.  Semin Liver Dis. 2008;  28(3) 293-301
    Article in Thieme ConnectPubMedGoogle Scholar
  • 5 Ganeshan D, Narlawar R, McCann C, Jones H L, Curtis J. Cerebral venous thrombosis—a pictorial review.  Eur J Radiol. 2009;  , March 16 (Epub ahead of print)
    PubMedGoogle Scholar
  • 6 Franchini M, Lippi G, Favaloro E J. Coagulopathies and thrombosis: usual and unusual causes and associations, part I.  Semin Thromb Hemost. 2009;  35(3) 257-259
    Article in Thieme ConnectPubMedGoogle Scholar
  • 7 Adams M, Williams A, Fell J. Exercise in the fight against thrombosis: friend or foe?.  Semin Thromb Hemost. 2009;  35(3) 261-268
    Article in Thieme ConnectPubMedGoogle Scholar
  • 8 Lippi G, Maffulli N. Biological influence of physical exercise on hemostasis.  Semin Thromb Hemost. 2009;  35(3) 269-276
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 Targher G, Chonchol M, Miele L, Zoppini G, Pichiri I, Muggeo M. Nonalcoholic fatty liver disease as a contributor to hypercoagulation and thrombophilia in the metabolic syndrome.  Semin Thromb Hemost. 2009;  35(3) 277-287
    Article in Thieme ConnectPubMedGoogle Scholar
  • 10 Franchini M, Montagnana M, Manzato F, Vescovi P P. Thyroid dysfunction and hemostasis: an issue still unresolved.  Semin Thromb Hemost. 2009;  35(3) 288-294
    Article in Thieme ConnectPubMedGoogle Scholar
  • 11 Gisondi P, Girolomoni G. Psoriasis and atherothrombotic diseases: disease-specific and non-disease-specific risk factors.  Semin Thromb Hemost. 2009;  35(3) 313-324
    Article in Thieme ConnectPubMedGoogle Scholar
  • 12 Lippi G, Montagnana M, Favaloro E J, Franchini M. Mental depression and cardiovascular disease: a multifaceted, bidirectional association.  Semin Thromb Hemost. 2009;  35(3) 325-336
    Article in Thieme ConnectPubMedGoogle Scholar
  • 13 Lippi G, Franchini M, Favaloro E J. Coagulopathies and thrombosis: usual and unusual causes and associations, part II.  Semin Thromb Hemost. 2009;  35(7) 591-596
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Bousser M G. Cerebral venous thrombosis: diagnosis and management.  J Neurol. 2000;  247(4) 252-258
    CrossrefPubMedGoogle Scholar
  • 15 Röttger C, Trittmacher S, Gerriets T, Kaps M, Stolz E. Sinus thrombosis after a jump from a small rock and a sneezing attack: minor endothelial trauma as a precipitating factor for cerebral venous thrombosis?.  Headache. 2004;  44(8) 812-815
    CrossrefPubMedGoogle Scholar
  • 16 Fonseca A C, Ferreira J J, Albuquerque L, Ferro J M. Sneeze as a precipitating factor of cerebral venous thrombosis.  Eur J Neurol. 2007;  14(10) e7-e8
    PubMedGoogle Scholar
  • 17 Mitchell S, Gorman D. The pathophysiology of cerebral arterial gas embolism.  J Extra Corpor Technol. 2002;  34(1) 18-23
    PubMedGoogle Scholar
  • 18 Kau T, Rabitsch E, Celedin S, Habernig S M, Weber J R, Hausegger K A. When coughing can cause stroke—a case-based update on cerebral air embolism complicating biopsy of the lung.  Cardiovasc Intervent Radiol. 2008;  31(5) 848-853
    CrossrefPubMedGoogle Scholar
  • 19 Rodriguez J F, Liron L, Chambost M, Combe C. Cerebral gas embolism after a cough fit [in French].  Ann Fr Anesth Reanim. 2005;  24(1) 64-67
    PubMedGoogle Scholar
  • 20 Culić V. Acute risk factors for myocardial infarction.  Int J Cardiol. 2007;  117(2) 260-269
    CrossrefPubMedGoogle Scholar
  • 21 Ferguson T, Sansing L H, Herrmann H, Cucchiara B. To close or not to close: PFO, sex and cerebrovascular events.  J Invasive Cardiol. 2006;  18 E292-E293
    PubMedGoogle Scholar
  • 22 Velicu S, Biller J, Hacein-Bey L, Freihage J H, Leya F. Paradoxical embolism to the central nervous system after sexual intercourse in a young woman with a complex atrial septal abnormality.  J Stroke Cerebrovasc Dis. 2008;  17(5) 320-324
    CrossrefPubMedGoogle Scholar
  • 23 Bird V, Krasnokutsky S, Zhou H S, Jarrahy R, Khan S A. Traumatic thrombophlebitis of the superficial dorsal vein of the penis: an occupational hazard.  Am J Emerg Med. 1997;  15(1) 67-69
    CrossrefPubMedGoogle Scholar
  • 24 Katz R, Blachar A. Superficial dorsal penile vein thrombosis (Mondor's disease) [in Hebrew].  Harefuah. 1997;  132(8) 544-545, 607
    PubMedGoogle Scholar
  • 25 Ozkara H, Akkuş E, Alici B, Akpinar H, Hattat H. Superficial dorsal penile vein thrombosis (penile Mondor's disease).  Int Urol Nephrol. 1996;  28(3) 387-391
    CrossrefPubMedGoogle Scholar
  • 26 Sasso F, Gulino G, Basar M, Carbone A, Torricelli P, Alcini E. Penile Mondors' disease: an underestimated pathology.  Br J Urol. 1996;  77(5) 729-732
    PubMedGoogle Scholar
  • 27 Dicuio M, Pomara G, Ales V, Menchini Fabris F, Dahlstrand C, Morelli G. Doppler ultrasonography in a young patient with penile Mondor's disease.  Arch Ital Urol Androl. 2005;  77(1) 58-59
    PubMedGoogle Scholar
  • 28 Shen H L, Liu S P, Wang S M, Tsay W, Hsieh J T. Elevated plasma factor VIII coagulant activity presenting with thrombophlebitis of the deep dorsal vein of the penis.  Int J Urol. 2007;  14(7) 663-664
    CrossrefPubMedGoogle Scholar
  • 29 Kollef M H, Schachter D T. Acute pulmonary embolism triggered by the act of defecation.  Chest. 1991;  99(2) 373-376
    CrossrefPubMedGoogle Scholar
  • 30 Chew G, Liao W B, Hsu T S, Bullard M J. Defecation induced deep venous thrombosis. A case report.  Jpn Heart J. 1996;  37(3) 409-415
    PubMedGoogle Scholar
  • 31 Yamada N, Nakamura M, Ishikura K et al.. Triggers of acute pulmonary thromboembolism developed in hospital, with focusing on toilet activities as triggering acts.  Int J Cardiol. 2005;  98(3) 409-411
    CrossrefPubMedGoogle Scholar
  • 32 Soyuncu S, Cete Y, Nokay A E. Portal vein thrombosis related to Cassia angustifolia .  Clin Toxicol (Phila). 2008;  46(8) 774-777
    CrossrefPubMedGoogle Scholar
  • 33 Kollef M H, Neelon-Kollef R A. Pulmonary embolism associated with the act of defecation.  Heart Lung. 1991;  20(5 Pt 1) 451-454
    PubMedGoogle Scholar
  • 34 Culić V. Triggering of cardiovascular incidents by micturition and defecation.  Int J Cardiol. 2006;  109(2) 277-279
    CrossrefPubMedGoogle Scholar
  • 35 Miller G J. Postprandial lipaemia and haemostatic factors.  Atherosclerosis. 1998;  141(Suppl 1) S47-S51
    CrossrefPubMedGoogle Scholar
  • 36 Anderson R A, Jones C J, Goodfellow J. Is the fatty meal a trigger for acute coronary syndromes.  Atherosclerosis. 2001;  159(1) 9-15
    CrossrefPubMedGoogle Scholar
  • 37 Fukutake T, Shimoe Y, Hattori T. Dizziness when eating: an unusual isolated presentation of cerebral venous thrombosis.  Intern Med. 2001;  40(9) 961-963
    CrossrefPubMedGoogle Scholar
  • 38 Brandão L R, Williams S, Kahr W H, Ryan C, Temple M, Chan A K. Exercise-induced deep vein thrombosis of the upper extremity. 1. Literature review.  Acta Haematol. 2006;  115(3-4) 214-220
    CrossrefPubMedGoogle Scholar
  • 39 Flinterman L E, Van Der Meer F J, Rosendaal F R, Doggen C J. Current perspective of venous thrombosis in the upper extremity.  J Thromb Haemost. 2008;  6(8) 1262-1266
    CrossrefPubMedGoogle Scholar
  • 40 Brandão L R, Williams S, Kahr W H, Ryan C, Temple M, Chan A K. Exercise-induced deep vein thrombosis of the upper extremity. 2. A case series in children.  Acta Haematol. 2006;  115(3-4) 221-229
    CrossrefPubMedGoogle Scholar
  • 41 van Stralen K J, Doggen C J, Lumley T et al.. The relationship between exercise and risk of venous thrombosis in elderly people.  J Am Geriatr Soc. 2008;  56(3) 517-522
    CrossrefPubMedGoogle Scholar
  • 42 Ali M S, Kutty M S, Corea J R. Deep vein thrombosis in a jogger.  Am J Sports Med. 1984;  12(2) 169
    CrossrefPubMedGoogle Scholar
  • 43 Harvey Jr J S. Effort thrombosis in the lower extremity of a runner.  Am J Sports Med. 1978;  6(6) 400-402
    CrossrefPubMedGoogle Scholar
  • 44 Amann W, Fruhwirth J, Schweiger W, Koch G. Isolated pelvic vein thrombosis in a young marathon runner [in German].  Sportverletz Sportschaden. 1997;  11(1) 33-34
    Article in Thieme ConnectPubMedGoogle Scholar
  • 45 Cauley K, Wright P. Iliac vein compression and pulmonary embolism in a long distance runner: computed tomography and magnetic resonance imaging—a case report.  Angiology. 2005;  56(1) 87-91
    CrossrefPubMedGoogle Scholar
  • 46 Papastergiou S G, Koukoulias N E, Tsitouridis I, Natsis C, Parisis C A. Circumflex femoral vein thrombosis misinterpreted as acute hamstring strain.  Br J Sports Med. 2007;  41(7) 460-461
    CrossrefPubMedGoogle Scholar
  • 47 Siegal D S, Wu J S, Brennan D D, Challies T, Hochman M G. Plantar vein thrombosis: a rare cause of plantar foot pain.  Skeletal Radiol. 2008;  37(3) 267-269
    CrossrefPubMedGoogle Scholar
  • 48 Antignani P L, Todini A R, Di Fortunato T, Bartolo M. The syndrome of the “coup de fouet.” Is it always a benign disease?.  Dermatol Surg. 1995;  21(10) 872-875
    CrossrefPubMedGoogle Scholar
  • 49 Disdier P, Harlé , Swiader L, Gambarelli-Mouillac N, Weiller P J. Retinal vein occlusions in a marathon runner.  Presse Med. 1992;  21(12) 582
    PubMedGoogle Scholar
  • 50 Gaudard A, Varlet-Marie E, Monnier J F et al.. Exercise-induced central retinal vein thrombosis: possible involvement of hemorheological disturbances. A case report.  Clin Hemorheol Microcirc. 2002;  27(2) 115-122
    PubMedGoogle Scholar
  • 51 Stang P, Sternfeld B, Sidney S. Migraine headache in a prepaid health plan: ascertainment, demographics, physiological, and behavioral factors.  Headache. 1996;  36(2) 69-76
    CrossrefPubMedGoogle Scholar
  • 52 Schwaiger J, Kiechl S, Stockner H et al.. Burden of atherosclerosis and risk of venous thromboembolism in patients with migraine.  Neurology. 2008;  71(12) 937-943
    CrossrefPubMedGoogle Scholar
  • 53 Bushnell C D, Jamison M, James A H. Migraines during pregnancy linked to stroke and vascular diseases: US population based case-control study.  BMJ. 2009;  338 b664
    CrossrefPubMedGoogle Scholar
  • 54 Bono G, Minonzio G, Mauri M, Clerici A M. Complications of migraine: migrainous infarction.  Clin Exp Hypertens. 2006;  28(3-4) 233-242
    CrossrefPubMedGoogle Scholar
  • 55 Moschiano F, D'Amico D, Ciusani E et al.. Coagulation abnormalities in migraine and ischaemic cerebrovascular disease: a link between migraine and ischaemic stroke?.  Neurol Sci. 2004;  25(Suppl 3) S126-S128
    CrossrefPubMedGoogle Scholar
  • 56 Lippi G, Targher G, Franchini M. Migraine, valproic acid, and lipoprotein(a).  Pediatr Neurol. 2009;  41(1) 78 author reply 78-79
    PubMedGoogle Scholar
  • 57 Pieper B, Kirsner R S, Templin T N, Birk T J. Injection drug use: an understudied cause of venous disease.  Arch Dermatol. 2007;  143(10) 1305-1309
    CrossrefPubMedGoogle Scholar
  • 58 McColl M D, Tait R C, Greer I A, Walker I D. Injecting drug use is a risk factor for deep vein thrombosis in women in Glasgow.  Br J Haematol. 2001;  112(3) 641-643
    CrossrefPubMedGoogle Scholar
  • 59 Pieper B, Templin T. Chronic venous insufficiency in persons with a history of injection drug use.  Res Nurs Health. 2001;  24(5) 423-432
    CrossrefPubMedGoogle Scholar
  • 60 Salmon A M, Dwyer R, Jauncey M, van Beek I, Topp L, Maher L. Injecting-related injury and disease among clients of a supervised injecting facility.  Drug Alcohol Depend. 2009;  101(1-2) 132-136
    CrossrefPubMedGoogle Scholar
  • 61 Wright N M, Martin M, Goff T, Morgan J, Elworthy R, Ghoneim S. Cocaine and thrombosis: a narrative systematic review of clinical and in-vivo studies.  Subst Abuse Treat Prev Policy. 2007;  2 27
    CrossrefPubMedGoogle Scholar
  • 62 Lisse J R, Davis C P, Thurmond-Anderle M. Cocaine abuse and deep venous thrombosis.  Ann Intern Med. 1989;  110(7) 571-572
    PubMedGoogle Scholar
  • 63 Zoghby Z, Sekhon I S, Miller D V, Sethi S. Cocaine, loin pain, and renal vein thrombosis.  Am J Kidney Dis. 2007;  49(6) 859-861
    CrossrefPubMedGoogle Scholar
  • 64 Neynaber S, Mistry-Burchardi N, Rust C et al.. PR3-ANCA-positive necrotizing multi-organ vasculitis following cocaine abuse.  Acta Derm Venereol. 2008;  88(6) 594-596
    PubMedGoogle Scholar
  • 65 Siegel A J, Sholar M B, Mendelson J H et al.. Cocaine-induced erythrocytosis and increase in von Willebrand factor: evidence for drug-related blood doping and prothrombotic effects.  Arch Intern Med. 1999;  159(16) 1925-1929
    CrossrefPubMedGoogle Scholar
  • 66 Jensenius M, Holm B, Calisch T E, Haugen K, Sandset P M. Deep venous thrombosis in intravenous drug addicts [in Norwegian].  Tidsskr Nor Laegeforen. 1996;  116(21) 2556-2558
    PubMedGoogle Scholar
  • 67 Lin D, Reeck J B, Murr A H. Internal jugular vein thrombosis and deep neck infection from intravenous drug use: management strategy.  Laryngoscope. 2004;  114(1) 56-60
    CrossrefPubMedGoogle Scholar
  • 68 Boedeker C C, Ridder G J, Weerda N, Maier W, Klenzner T, Schipper J. Etiology and therapy of the internal jugular vein thrombosis [in German].  Laryngorhinootologie. 2004;  83(11) 743-749
    Article in Thieme ConnectPubMedGoogle Scholar
  • 69 Ghosheh F R, Kathuria S S. Intraorbital heroin injection resulting in orbital cellulitis and superior ophthalmic vein thrombosis.  Ophthal Plast Reconstr Surg. 2006;  22(6) 473-475
    CrossrefPubMedGoogle Scholar
  • 70 Gallus A S. Travel, venous thromboembolism, and thrombophilia.  Semin Thromb Hemost. 2005;  31(1) 90-96
    Article in Thieme ConnectPubMedGoogle Scholar
  • 71 Koton S, Tanne D, Bornstein N M, Green M S. Triggering risk factors for ischemic stroke: a case-crossover study.  Neurology. 2004;  63(11) 2006-2010
    PubMedGoogle Scholar
  • 72 Ferguson T, Sansing L H, Herrmann H, Cucchiara B. To close or not to close: PFO, sex and cerebrovascular events.  J Invasive Cardiol. 2006;  18(12) E292-E293
    PubMedGoogle Scholar

Giuseppe LippiM.D. 

U.O. Diagnostica Ematochimica, Dipartimento di Patologia e Medicina di Laboratorio, Azienda Ospadaliero-Universitaria di Parma, Strada Abbeveratoia

2, 43100 Parma, Italy

Email: giuseppe.lippi@univr.it

Email: ulippi@tin.it