Thromboembolic Complications After Splenectomy for Hematologic Diseases
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1 American Journal of Hematology 76: (2004) Thromboembolic Complications After Splenectomy for Hematologic Diseases Martin Mohren, 1 * Ilka Markmann, 1 Ulrike Dworschak, 1 Astrid Franke, 1 Christian Maas, 1 Sabine Mewes, 1 Günter Weiss, 2 and Kathleen Jentsch-Ullrich 1 Thromboembolic complications following splenectomy for hematologic diseases occur in up to 10% of patients and may range from portal vein thrombosis (PVT) to pulmonary embolism (PE) and deep vein thrombosis (DVT). Up to now there exist no recommendations for the duration and intensity of prophylactic anticoagulation, which usually follows local institutional protocols. We report on three consecutive patients with severe portal vein thrombosis and/or pulmonary embolism one with fatal outcome 7 to 35 days after splenectomy for autoimmune hemolytic anemia, immunothrombocytopenia, and indolent lymphoma, respectively. Incidence and pathophysiology of thromboembolic events (TE) in this patient group as well as prophylactic anticoagulation will be discussed, including a review of the current literature on this topic. Am. J. Hematol. 76: , ª 2004 Wiley-Liss, Inc. Key words: splenectomy; hematologic diseases; thromboembolism; prophylactic anticoagulation INTRODUCTION Splenectomy is performed for diagnosis or treatment of a variety of hematologic diseases such as immune cytopenia, indolent non-hodgkin s lymphoma (NHL), and, rarely, for myeloproliferative diseases (MPD) [1]. Within the recent years, laparoscopic splenectomy has been increasingly employed when possible and is associated with a decreased rate of intraoperative organ damage and quicker postoperative recuperation of the patient [2]. Postoperative complications most often comprise infections, particularly with encapsulated organisms such as pneumococci or haemophilus influenzae type B following a sometimes fulminant course, thus preoperative vaccination has become standard practice [2]. Additionally, patients with immunethrombocytopenia and low platelet counts may have an increased perioperative bleeding risk. In contrast to the former, thromboembolic risk has so far attracted considerably less attention in this patient group, and published reports of thromboembolism (TE) so far have come from surgeons rather than hematologists. Within a period of 6 months we saw severe TE in 3 patients several days to weeks after splenectomy for various hematologic disorders. All 3 patients had received anticoagulation with low molecular weight ª 2004 Wiley-Liss, Inc. heparin until complete mobilization, had no prior history of thrombophilia, and exhibited no further obvious clinical risk factors for TE, such as prolonged immobilization, infection, or heart failure except for smoking in patient I. PATIENTS Patient I A 24-year-old female patient with a 2-year history of autoimmune hemolytic anemia of the warm antibody type had been successfully treated with prednisone and relapsed under a maintenance dose of 5 mg daily. The hemoglobin normalized when steroids were increased to 100 mg/day, and the patient was referred for splenectomy after the dose was tapered to <40 mg/day. Laparoscopic splenectomy (spleen weight 395 g) was performed, and after quick recovery she was *Correspondence to: Dr. Martin Mohren, Klinik fu r Ha matologie/ Onkologie, Universität Magdeburg, Leipziger Str. 44, Magdeburg, Germany. Martin.Mohren@medizin.uni-magdeburg.de Received for publication 26 May 2003; Accepted 17 October 2003 Published online in Wiley InterScience ( DOI: /ajh.20018
2 144 Case Report: Mohren et al. Fig. 1. Portal vein thrombosis with Perfusion defects in the liver. Fig. 2. Inferior cava vein thrombosis. discharged on day 7 after the operation with a platelet count of 519 G/l. Anticoagulation with low molecular weight heparin was carried out until discharge. The next day, the patient collapsed at home and was found to have extensive pulmonary embolism as well as portal vein thrombosis (Fig. 1) on CT scan. Platelets were at 499 G/l. Although anticoagulation with fulldose heparin was started immediately, the further course was complicated by mesenteric vein thrombosis with severe bowel ischemia, subsequently leading to death from multiorgan failure. Fig. 3. Right pulmonary embolism. Patient II A 21-year-old male patient with chronic immunethrombocytopenia first diagnosed 8 years prior to admission had received a short course of therapy with immunoglobulins and steroids, whereafter the platelet count had remained stable at 70 G/l with no further medication. At relapse, high steroid doses were necessary to maintain platelets above 40 G/l, and splenectomy was recommended. Laparoscopic splenectomy (spleen weight 350 g) was carried out at a platelet count of 60 G/l with no bleeding complications. He received anticoagulation with low molecular weight heparin until discharge on day 5 postsplenectomy. By that time, platelets were at 360 G/l. Two days later the patient complained of acute-onset shortness of breath and left-sided upper abdominal pain. The platelet count was at 1,013 G/l. Embolism of the right pulmonary artery and portal and inferior cava vein thrombosis (Fig. 2 and 3) were diagnosed, and full-dose heparin was begun immediately followed by oral anticoagulation for 1 year. He is currently well with no further anti-coagulation and/or immunosuppressive medication. Patient III A 63-year-old male patient presented to our clinic because of left-sided upper abdominal pain secondary to splenomegaly. Bone marrow histology revealed infiltration by indolent lymphoma, and open splenectomy was performed, yielding a massively enlarged organ, of size cm and weight 1,660 g. Histologic findings were consistent with marginal zone lymphoma. There was also involvement of abdominal lymph nodes. The postoperative course was uneventful, and he received prophylactic anticoagulation with low molecular weight heparin for 30 days due to our previous experience. However, on day 35 postsplenectomy, this patient experienced chest pain and dyspnoea of sudden onset; ventilation and perfusion scintigraphy revealed pulmonary embolism in segment 2 in both lungs. The platelet count was at 1,158 G/l. Full-dose heparin was started and was later switched to a vitamin K antagonist for a period of 6 months. DISCUSSION We saw 3 patients with severe thromboembolic events (TE) after splenectomy for hematologic
3 Case Report: Thromboembolic Complications After Splenectomy 145 diseases within a short period of time. TE is a rare complication of splenectomy that usually does not receive as much attention as secondary infections or hemorrhage. However, an increased incidence of TE, portal vein thrombosis in particular, following splenectomy has been reported in patients with hematologic diseases. A Dutch study of 563 splenectomies published in 2000 found postoperative portal vein thrombosis in 9 patients (2%). The latter was more likely to occur in patients with hematologic diseases, such as autoimmune hemolytic anemia and myeloproliferative syndrome (incidence 10%) [3]. In a recently published report investigating portal vein thrombosis after splenectomy, an incidence of 8% was found among 101 patients, 74% of whom had hematologic disease [4]. Among 8 patients who developed PVT, 4 had a myeloproliferative disorder. Interestingly PVT occurred as late as 3 years following splenectomy [4]. Another report of 223 splenectomies in patients with myeloid metaplasia, however, detected thrombosis (location not further specified) in 7.2% only. Postsplenectomy thrombocytosis in these patients was associated with postoperative thrombosis. Unfortunately, platelet numbers are not provided by the authors [5]. An additional analysis of 26 splenectomized patients with myelofibrosis revealed venous thrombosis in 12% [6]. In an American investigation carried out with 50 splenectomized patients whose underlying disease was not further specified, 5 of 50 patients (10%) were found to develop PVT that was then successfully treated with anticoagulation [7]. In an Italian report on patients undergoing splenectomy for treatment of thalassemia, an incidence of TE as high as 29% was seen [8]. One of 12 patients with immunethrombocytopenia developed PVT without any further complications in another Italian report [9]. A French group performed repeat Doppler ultrasound studies in 60 consecutive splenectomized patients on days 7 and 30 postoperatively and found 1 symptomatic and 3 asymptomatic PVT (8%) in this patient cohort [10]. Thus asymptomatic PVT may occur more frequent than clinically apparent TE. A review of imaging findings in postsplenectomy patients revealed PVT in 12 of 123 patients (9,8%), all of whom had hematologic disease [11]. A small number of TE (1%) was reported by a French group that performed laparoscopic splenectomy in 275 patients with hematologic disease [12], and a lower rate of TE was also found in another report on laparoscopic splenectomy [5]. In contrast to these findings, 2 of our patients with severe TE had undergone laparoscopic splenectomy. There is little data on the incidence of TE other than PVT, such as DVT and/or PE in splenectomized patients [13]. In one report, 4 of 8 patients with postsplenectomy PVT developed TE later in the course [5], whereas 2 of our patients had both, PVT and PE at the same time. So far the pathogenesis of TE after splenectomy is poorly understood. Portal vein thrombosis may result from local factors, such as intraoperative manipulation of visceral vessels, the splenic vein in particular [14], and may account for the particular risk in patients with massively enlarged organs. Five of 31 patients (16%) with mesenteric venous thrombosis (MVT) a rare complication of PVT had previously undergone splenectomy, whereas 13 (42%) of these patients had a hypercoagulable state (protein C, protein S, and ATIII deficiency) without local risk factors [15]. Mesenteric thrombosis, as was also seen in patient I of our report, is associated with a poor prognosis due to subsequent bowel ischemia and multiorgan failure [4,15,16]. Thrombocytosis that accompanies splenectomy in most cases may, although poorly defined, play an etiologic role. In several reports, large spleen size, thrombocytosis, and a myeloproliferative disease (MPD) as the underlying disease were described as risk factors for TE [4,7]. Patients with MPD and a large spleen (>3,000 g) had a 75% incidence of PVT [4]. Splenic weight >1,000 g was found to be associated with significant morbidity after laparoscopic splenectomy [17], yet none of our patients with severe TE had MPD and only one patient had a massively enlarged spleen. The association of postsplenectomy thrombocytosis and PVT is unclear, particularly in patients without MPD, since not all patients with thrombocytosis develop PVT and PVT also occurs in patients with normal platelets [4]. Patient I in our report, for example, had slightly elevated platelets only (499 G/l), and not all of the reported patients with MVT following splenectomy had thrombocytosis [15]. In a study of 129 patients with extreme thrombocytosis (>1,000 G/l), 72 in MPD and 57 with reactive thrombocytosis, thrombosis was found in 3 4% [18], but a prospective observational study of patients with essential thrombocythemia (ET) and a platelet count <1,500 G/l as compared to an age- and sex-matched control group failed to show an increased risk for thrombosis in ET patients [19]. A recent study investigating etiology and clinical significance of thrombocytosis found a higher incidence of venous and arterial thrombosis in patients with primary thrombocytosis as compared to patients with secondary thrombocytosis (12.4% vs. 1.6%). The authors conclude that postsplenectomy thrombocytosis is not associated with an increased risk for hemostatic complications [20]. Thus
4 146 Case Report: Mohren et al. thrombocytosis by itself does not seem an indication to initiate anti-coagulation or antiplatelet or plateletlowering therapy unless it is being used as secondary prophylaxis. There exists little data on activation of plasmatic coagulation and/or lack of coagulation inhibitors, such as protein C or S deficiency after splenectomy or the presence of the factor V Leiden mutation or antiphospholipid antibodies. Few reports demonstrated a systemic hypercoaguable state in patients with PVT [14,15], but these reports focused on the etiology of PVT and MVT without special attention to the postsplenectomy state. Disseminated intravascular coagulation was not found in splenectomized patients in a systemic evaluation [5]. approach may not be sufficient in preventing TE in splenectomized patients with hematologic disease. In concordance with our findings, the majority of patients (approximately 70%) developed PVT while receiving prophylactic anticoagulation with low-dose heparin [4,8]. Although a combination of heparin and antiplatelet agents or even vitamin K antagonists has been suggested in high-risk splenectomized patients [4], its use is problematic due to an increased risk of bleeding in the postoperative period and the abnormal platelet function seen in some patients with hematologic disease [5]. However, routine postoperative surveillance ultrasound imaging may be of benefit in patients with myeloproliferative disease and a large spleen [11] for prompt diagnosis of PVT. How can TE be prevented in splenectomized patients? Preventive measures still rely preferentially on personal experience, because accumulated data is inconclusive and general recommendations for duration and intensity of anticoagulation after splenectomy do not exist [2,21]. So far there is little evidence indicating that the method of splenectomy has an impact on subsequent thromboembolic complications. General prophylactic measures such as early mobilization and refraining from smoking may be of some help. Until now, prophylactic low-dose anticoagulation has failed to show sufficient effect [4] to prevent PVT but may reduce the risk for TE in other locations, such as deep venous thrombosis and pulmonary embolism. However, 3 of our patients had pulmonary embolism 2 of whom also had portal vein and inferior cava vein and/or mesenteric vein thrombosis although they had received prophylactic anticoagulation with low molecular weight heparin until complete mobilization and discharge from the hospital. Antiplatelet agents such as aspirin in postsplenectomy thrombocytosis have not been thoroughly looked at most experience of aspirin use in thrombocytosis stemming from patients with ET, a disease with a different impact on platelet function and may increase bleeding complications as has been shown in patients with ET [22]. However, antiplatelet agents may be of benefit in patients with extreme thrombocytosis (>1,500 G/l) particularly if there are additive cardiovascular risk factors [22]. Although extension of prophylactic anticoagulation with low molecular weight heparin until day 30 postsplenectomy was started after we saw TE in the first 2 patients, patient III developed pulmonary embolism on day 35, which was 5 days after cessation of anticoagulation. Thus even our newly established CONCLUSIONS Although it does not receive as much attention as infectious complications, TE occurs in approximately 10% of splenectomized patients, and prophylactic anticoagulation is warranted in patients undergoing splenectomy for hematologic diseases. Duration and intensity of mandatory anticoagulation has yet to be established. At our institution, patients currently receive low molecular weight heparin for a period of 30 days after splenectomy. However, as has been shown in one of our patients and in further previous reports, TE may occur ever after a prolonged time interval after surgery, thus physicians as well as patients should be alert to symptoms of TE in splenectomized patients, even years after the operation to ensure rapid diagnosis and proper treatment. REFERENCES 1. Xiros N, Economopoulos T, Christodoulidis C, et al. Splenectomy in patients with malignant non-hodgkin s lymphoma. Eur J Haematol 2000;64(3): Marcaccio MJ. Laparoscopic splenectomy in chronic idiopathic thrombocytopenic purpura. Semin Hematol 2000;37(3): van t Riet M, Burger JW, van Muiswinkel JM, Kazemier G, Schipperus MR, Bonjer HJ. Diagnosis and treatment of portal vein thrombosis following splenectomy. Br J Surg 2000;87(9): Winslow ER, Brunt LM, Drebin JA, Soper NJ, Klingensmith ME. Portal vein thrombosis after splenectomy. Am J Surg 2002;184(6): Tefferi A, Mesa RA, Nagorney DM, Schroeder G, Silverstein MN. Splenectomy in myelofibrosis with myeloid metaplasia: a singleinstitution experience with 223 patients Blood 2000;95(7): Akpek G, McAneny D, Weintraub L. Risk and benefits of splenectomy in myelofibrosis with myeloid metaplasia: a retrospective analysis of 26 cases. J Surg Oncol 2001;77(1): Hassn AM, Al-Fallouji MA, Ouf TI, Saad R. Portal vein thrombosis following splenectomy. Br J Surg 2000;87(3):
5 Case Report: Thromboembolic Complications After Splenectomy Cappellini MD, Robbiolo L, Bottasso BM, Coppola R, Fiorelli G, Manucci AP. Venous thromboembolism and hypercoagulabiliy in splenectomized patients with halassaemia intermedia. Br J Hematol 2000;111(2): Valeri A, Venneri F, Presenti L, Grossi A, Borelli D. Portal thrombosis. A rare complication of laparoscopic splenectomy. Surg Endosc 1998;12(9): Chaffanjon PC, Brichon P-Y. Portal vein thrombosis following splemectomy for hematologic disease: prospective study with Doppler color flow imaging. World J Surg 1998;22: Loring LA, Panicek DM, Karpeh MS. Portal system thrombosis after splenectomy for neoplasm or chronic hematologic disorder: is routine surveillance imaging necessary? J Comput Assist Tomogr 1998;22(6): Delaitre B, Champault G, Barrat C, et al. Laparoscopic splenectomy for hematologic diseases. Study of 275 cases Ann Chir 2000; 125(6): Stephens BJ, Justice JL, Sloan DA, Yoder JA. Elective laparoscopic splenectomy for hematologic disorders. 1997;63(8): Valla DC, Condat B. Portal vein thrombosis in adults: pathophyiology, pathogenesis and management. J Hepatol 2000;32: Morasch M, Ebaugh MD, Chiou AC, Matsamura J, Pearce W, Yao J. Masenteric venous thrombosis: a changing clinical entity. Vasc Surg 2001;34(4): Balz J, Minton JP. Mesenteric thrombosis following splenectomy. Ann Surg 1975;181(1): Patel AG, Parker JE, Wallwork B, et al. Massive splenomegaly is associated with significant morbidity after laparoscopic splenectomy. Ann Surg 2003;238(2): Buss DH, Stuart JJ, Lipscomb GE. The incidence of thrombotic and hemorrhagic disorders in association with extreme thrombocytosis: an analysis of 129 cases. Am J Hematol 1985;20(4): Ruggeri M, Finazzi G, Tosetto A, Riva S, Rodeghiero F, Barbui T. No treatment for low-risk thrombocythaemia: results from a prospective study Br J Haematol 1998;103(3): Griesshammer M, Bangerter M, Sauer T, Wennauer R. Bergmann L, Heimpel H. Aetiology and clinical significance of thrombocytosis: analysis of 732 patients with an elevated platelet count. J Intern Med 1999;245: Benoist S. Median and long-term complications of splenectomy Ann Chir 2000;125(4): Schafer A. Thrombocytosis and thrombocythemia. Blood Rev 2001;15:
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