Thrombocytopenia Due to Acute Venous Thromboembolism and Its Role in Expanding the Differential Diagnosis of Heparin-Induced Thrombocytopenia

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1 American Journal of Hematology 76:69 73 (2004) Thrombocytopenia Due to Acute Venous Thromboembolism and Its Role in Expanding the Differential Diagnosis of Heparin-Induced Thrombocytopenia Craig S. Kitchens* Division of Hematology, Department of Medicine, University of Florida and Medical Service, Department of Veterans Affairs Medical Center, Gainesville, Florida Thrombocytopenia is an uncommon but serious consequence of heparin administration. Occasionally patients with massive acute venous thromboembolism (VTE) will develop. As heparin or some thrombin inhibitor is strongly indicated in acute VTE, it is important to distinguish this event from heparin-induced (HIT). Four patients are presented who developed so early in their course of VTE and/or therapy with heparin that HIT was considered unlikely. The mean nadir platelet count for these four patients was 60,000/ml occurring at a mean time of 18 hr after the initiation of heparin therapy. Because of strong indications to continue heparin for their acute VTE in the face of a very low likelihood that they did have HIT, heparin was continued with excellent results and resolution of the. The literature of this subject is reviewed. Thrombocytopenia following VTE is actually rather common, but it is usually milder than in these four cases. In some cases such as these four, the can be sudden and rather severe causing diagnostic confusion with HIT. Am. J. Hematol. 76:69 73, ª 2004 Wiley-Liss, Inc. Key words: ; heparin; venous thromboembolism Heparin remains a highly efficacious drug in the clinician s armamentarium. It is active in either preventing or treating thromboembolic disease. Despite its usefulness, heparin is associated with several side effects, most notably. Great concern has been raised over the devastating syndrome known as heparin-induced with thrombosis (HIT), also known as Type II heparin-induced. A common nonimmune heparinassociated may be referred to as heparin-induced without thrombosis or heparin-induced Type I. This nonthrombotic normally occurs prior to the fifth day of heparin therapy with a nadir platelet count rarely under 100,000/ml. The condition abates even if heparin therapy is continued. HIT typically begins after the fifth day of heparin therapy unless the patient had been exposed to heparin within the last several months and therefore had pre-existing antiheparin antibodies from previous exposure, in which ª 2004 Wiley-Liss, Inc. case HIT may occur on the first or second day following renewed heparin exposure. The concern for HIT complicating the course of patients who are administered heparin, despite the strongest of indications, has become so pervasive that the use of this efficacious drug may be stopped unnecessarily. As a result, some patients may be exposed to high thrombotic risk without benefit of anticoagulant therapy. Despite excellent recent reviews regarding HIT [1 3], the differential diagnosis of HIT often receives *Correspondence to: Craig S. Kitchens, M.D., Chief, Medical Service (111), Department of Veterans Affairs Medical Center, 1601 SW Archer Road, Gainesville, FL craig.kitchens@med.va.gov Received for publication 16 October 2003; Accepted 17 October 2003 Published online in Wiley InterScience ( DOI: /ajh.20009

2 70 Concise Review: Kitchens little attention. Most clinicians have encountered the unpleasant dilemma characterized by possible severe complications of heparin on the one hand but strong indications for anticoagulant therapy on the other with relatively few therapeutic alternatives in between [4]. We have seen four patients (Table I) over the past several years with that in our opinion is primarily due to acute venous thromboembolism (VTE) with large fresh deep vein thrombosis (DVT), with or without pulmonary emboli (PE), a condition that carries a strong indication for heparin administration. Even though these patients presented with or developing very early in the course of their anticoagulation, heparin administration was considered contraindicated by their practitioners. On the basis of these four cases, we would like to add the term acute thrombosisassociated to the modest differential diagnosis of HIT. CASE 1 A 41-year-old man sustained traumatic fractures including T1 and T8. He underwent thoracic spine fusion with a preoperative platelet count of 156,000/ml. Neither preoperative nor postoperative anticoagulants were employed. Three days later, his platelet count fell to 60,000/ml. That same day he underwent duplex imaging for a swollen leg, which demonstrated extensive venous thrombosis. He was placed on therapeutic doses of unfractionated heparin. Within days, the platelet count rapidly increased. He experienced neither bleeding nor new thrombosis while on therapeutic doses of heparin for the next 3 weeks, during which time his platelet count stabilized at 300,000/ml. CASE 2 Two days after a long automobile trip, an 81-yearold man with a 3-year history of prostate cancer developed a large red, tender, swollen right leg. The clinical diagnosis of DVT was confirmed by ultrasonography, which showed near-total occlusion of the entire venous circulation of the leg. He had never been administered heparin before. He required 40,000 50,000 units of heparin per day over the next hr to achieve a therapeutic aptt. By the end of the first day, his platelet count had decreased from an admission count of 100,000/ml to 53,000/ml. Twelve hours later, that platelet count was 33,000/ml and the heparin requirements decreased from 1,600 units/hr to 800 units/hr. The platelet count increased to 60,000/ml on the third day. Warfarin therapy had been started on admission, and on the fourth day his INR was therapeutic and the platelet count had risen to 90,000/ml. On the sixth day, his platelet count was 150,000/ml and the heparin-associated antiplatelet antibody assay done by the ELISA method of Amiral [5] returned negative. CASE 3 This 41-year-old man suffered an L1 burst fracture with incomplete cord injury and bilateral lower extremity paralysis after an automobile accident. His original platelet count was 194,000/ml, and he underwent an L1 corpectomy and stabilization. On the fifth postoperative day, he was placed on unfractionated heparin, 5,000 units twice daily for prophylaxis. His platelet count dropped to 88,000/ml on the sixth day of hospitalization. The Neurosurgery Service discontinued heparin therapy, and he was then discharged to a rehabilitation unit. Two days later, it was noticed that he had an enlarged painful right leg, and enoxaparin 30 mg twice daily by subcutaneous injection was initiated. Duplex imaging showed total venous thrombosis to all the veins of the right leg. His platelet count then was 322,000/ml. Because he had never been exposed to heparin before this accident and had developed the after only 1 day of exposure during the first admission, it was thought unlikely that he had HIT. He was continued on enoxaparin therapy after the dose was increased to 60 mg twice daily. His platelet counts remained normal. Tests for the heparin-associated antiplatelet antibody were TABLE I. Features of Acute Thrombosis-Associated Thrombocytopenia* Lowest platelet count Case no. Primary diagnosis Thrombosis diagnosis K/ml Hr after primary diagnosis Hr after heparin therapy Antibody test Outcome 1 Massive trauma with paralysis Extensive DVT ND Good 2 Prostate cancer, prolonged travel Extensive DVT Negative Good 3 Massive trauma with paralysis Extensive DVT Indeterminate Good 4 Antiphospholipid syndrome Extensive PE 60 NA 12 Negative Good *Abbreviations: DVT, deep venous thrombosis; PE, pulmonary embolus; ND, not done; NA, not applicable.

3 Concise Review: Thrombocytopenia in Acute VTE 71 indeterminate. Because he was improving without further, enoxaparin was continued until his INR target was reached. The heparin-associated antiplatelet antibody test was not repeated. CASE 4 A 22-year-old woman developed syncope, shortness of breath, and chest pain. A large PE was found, and appropriate therapy was instituted with intravenous unfractionated heparin. Her initial platelet count was 90,000/ml, yet after only a few hours of heparin therapy it decreased to 60,000/ml. There was concern that this could represent HIT, but her treating physicians thought that the onset was too rapid considering she had never been given heparin previously. Nonetheless, she was switched to danaparoid therapy. She was found to have markedly positive assays for antiphospholipid and anticardiolipin antibodies. She was diagnosed as having antiphospholipid syndrome. Her heparin-associated antiplatelet antibody assay subsequently returned negative. Within 5 days, her platelet count returned to normal. DISCUSSION The clinical course of these four patients demonstrates several key relevant points. Of note, none was receiving or had received heparin prophylaxis for orthopedic surgery, heparin therapy for unstable angina, or any invasive cardiovascular procedures, as is seen in most patients who develop HIT. They had all suffered major acute VTE, and the initial platelet counts were obtained very early in the course of their illness. We hypothesize that these large fresh clots consume platelets on their surface, likely due to the exudation of thromboplastic substances [6,7]. This process can be regarded as a form of disseminated intravascular coagulation (DIC) [8,9]. Thrombocytopenia was seen in these patients early in their course of heparin administration or even prior to any heparin administration. The fact that occurred so early fits Warkentin s [3] exclusionary criteria of HIT. Nevertheless, in each case the clinicians caring for these patients not only considered the diagnosis of HIT but, in three of the four cases the patients were also tested for the heparin-associated antiplatelet antibody. We as others [4] wrestled with the implication of the differential diagnosis. We chose to continue heparin therapy because of the strong indication for effective anticoagulation therapy in these cases. Over 100 years ago, Welch [10] showed that platelets quickly accrete on fresh thrombi with the youngest thrombi being coated with the largest number of platelets. These mature into what are now known as the lines of Zahn on histologic examination of thrombotic material. Adelson and colleagues, in 1961 [11], demonstrated that when thromboses were produced acutely in the IVC in an experimental canine model, up to 60% of the circulating platelets adhered to the clot within a matter of hours with resultant. It took approximately 3 days for the circulating platelet count to return to normal. Review of the Urokinase Pulmonary Embolism Trial database [12] reveals that 10% of all acute PE patients exhibited a platelet count of less than 150,000/ml at initial evaluation. The mean of all their patients platelet counts was 293,000/ml with a standard deviation of 134,000/ml. More recently, a comprehensive study of PE determined that the admission platelet count was 221,000/ml with a standard deviation of 73,600/ml, implying that 2.5% had platelet counts 75,000/ml [13]. Warkentin estimates that 3.5% of patients who receive heparin experience a decrease in platelet count while up to 1% experience thrombosis [3]. Warkentin states that occurring before to the fifth day of heparin administration in a patient without prior heparin exposure likely is not HIT but the more common and less serious nonimmune heparin-associated. Others [14] have stated that there is no established standard of care for this difficult situation. In addition, very important medicolegal issues remain, as HIT appears to be the most commonly litigated complication in hematology. To assist the practitioner in distinguishing HIT from other types of, Warkentin [3] promotes the use of a clinical triad in the diagnosis of HIT: (1) occurring between the fifth to the tenth day after initial exposure to heparin; (2) the platelet count should almost always be less than 150,000/ml or at least show a drop of 50,000/ml or 50% of the initial platelet count; and (3) there should be evidence of new or worsening thrombosis. Patients who receive heparin therapy may be thrombocytopenic before receiving heparin or they may become thrombocytopenic soon thereafter. Not all will meet criteria for HIT and some are described as having pseudo-hit [15]. Although venous thromboembolism is occasionally mentioned in the differential diagnosis of HIT [3] as pseudo-hit, very few reports document this underreported occurrence. Thienopyridine (ticlopidine or clopidogrel)-induced thrombotic purpura (TTP) [16,17] also requires consideration in the differential diagnosis of HIT in the appropriate clinical setting that includes the use of heparin.

4 72 Concise Review: Kitchens TABLE II. Differential Diagnosis of Acute Thrombocytopenia in Patients Subject of Heparin Administration* Nonimmune heparin-associated Heparin-induced with thrombosis (HIT) Thienopyridine-induced Drug-induced TTP a Disseminated intravascular coagulation Acute thrombosis-associated Clinical setting Any patient receiving heparin Patients receiving heparin, esp. cardiac and orthopaedic surgery patients Neurologic or cardiovascular patients receiving a thienopyridine Many drugs Patients with a severe underlying illness Platelet count, K/ml <10K Days after heparin therapy started NA NA NA 0 1 Patients with large, fresh VTE Bleeding tendency None None None Major Moderate None Thrombotic tendency None Major Major None Moderate Pre-existing Clinical clues Platelet count slowly drifts down then back up even on heparin New and/or worsening thromboses Treatment Observe Stop heparin and consider alternative therapies Schistocytes, renal impairment, and CNS manifestations Plasmapheresis; stop offending drug Petechial bleeding Stop or change all drugs Obvious underlying disorders and increased FDP, d-dimers Treat underlying illness Large, fresh VTE Continue heparin therapy *Abbreviations: TTP, thrombotic ; VTE, venous thromboembolism; PE, pulmonary embolus; PTT, partial thromboplastin time; CNS, central nervous system; FDP, fibrin degradation products; NA, not applicable. a Thienopyridines include ticlopidine and clopidogrel.

5 Concise Review: Thrombocytopenia in Acute VTE 73 Table II presents a brief differential diagnosis of in clinical settings that may include patients with HIT. Severely ill patients, often requiring admission to intensive care units, may also develop drug-induced s not due to TTP or caused by sepsis or disseminated intravascular coagulation. The clinical manifestations, the duration of heparin therapy prior to, the degree of itself, and other clinical clues assist in the differential diagnosis. A patient receiving heparin therapy who experiences a decrease in platelet count should not reflexively be deprived of treatment with this efficacious agent. Fortunately, the availability of lepirudin and argatroban often eases decision-making as these agents appear to be safe thrombin inhibitors in patients who have HIT yet still need anticoagulation therapy. Laboratory testing for heparin-associated antiplatelet antibodies has been thoroughly reviewed [5]. Although these assays are much improved over previous tests, they are still imperfect. Results are usually returned some days after crucial decisions regarding therapy had to be made, and, unfortunately, there is no direct correlation between the positivity of tests and what one sees clinically; accordingly, HIT remains predominantly a clinical diagnosis. Acute VTE may occasionally present not only with, but the platelet count may also fall further in the first hr. Because these patients require the use of an active thrombin-inhibiting anticoagulant, practitioners should be aware of acute thrombosis-associated in the differential diagnosis of HIT. Note Added in Proof: We are aware of a report from Lubenow and colleagues [18] regarding 4 patients with post-transfusion purpura (PTP). The course of these patients as well as their degree of also caused consideration of heparin-induced as a diagnostic possibility. REFERENCES 1. Warkentin TE, Chong BH, Greinacher A. Heparin-induced : towards consensus. Thromb Haemost 1998;79: Kelton JG, Sheridan D, Santos A, et al. Heparin-induced : laboratory studies. Blood 1988;72: Warkentin TE. Heparin-induced. In: Kitchens, CS, Alving BM, Kessler CM, editors. Consultative hemostasis and thrombosis. Philadelphia: W.B. Saunders; p Alving BM, Krishnamurti C. Recognition and management of heparin-induced (HIT) and thrombosis. Semin Thromb Hemost 1997;23: Amiral J, Bridey F, Dreyfus M, et al. Platelet factor 4 complexed to heparin is the target for antibodies generated in heparininduced. Thromb Haemost 1992;68: Kitchens CS. Thrombotic storm: when thrombosis begets thrombosis. Am J Med 1998;104: Mutch NJ, Robbie LA, Booth NA. Human thrombi contain an abundance of active thrombus. Thromb Haemost 2001;86: Stahl RL, Javid JP, Lackner H. Unrecognizable pulmonary embolism presenting as disseminated intravascular coagulation. Am J Med 1984;76: Mustafa MH, Mispireta LA, Pierce LE. Occult pulmonary embolism presenting with and elevated fibrin split products. Am J Med 1989;86: Welch WH. The structure of white thrombi. Trans Pathol Soc Philadelphia 1887;13: Adelson E, Rheingold JJ, Parker O, et al. Platelet and fibrinogen survival in normal and abnormal states of coagulation. Blood 1961;17: Urokinase pulmonary embolism trial. Circulation 1973;47 (Suppl II): Konstantinides S, Geibel A, Heuel G, et al. Heparin plus alteplase compared with heparin alone in patients with submassive pulmonary embolism. N Engl J Med 2002;347: Blakeman B. Management of heparin-induced : a cardiovascular surgeon s perspective. Semin Hematol 1999;36 (Suppl 1): Warkentin TE. Pseudo-heparin-induced. In: Warkentin TE, Greinacher A, editors. Heparin-induced. 2 nd edition. New York: Marcel Dekker; p Bennett CL, Weinberg PD, Rozenberg-Ben-Dror K. Thrombotic thrombocytopenic purpura associated with ticlopidine. A review of 60 cases. Ann Intern Med 1998;128: Bennett CL, Connors JM, Carwile JM, et al. Thrombotic thrombocytopenic purpura associated with clopidogrel. N Engl J Med 2000;342: Lubenow N, Eichler P, Albrecht D, et al. Very low platelet counts in post-transfusion purpura falsely diagnosed as heparin-induced. Report of four cases and review of literature. Thromb Res 2000;100:

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