A Patient with Cerebral Embolism Related to Trousseau s Syndrome
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1 Journal of Neuroendovascular Therapy 2017; 11: Online July 11, 2017 DOI: /jnet.cr A Patient with Cerebral Embolism Related to Trousseau s Syndrome Yosuke Nishimuta, 1 Tetsuya Nagayama, 2 Takaaki Hiwatari, 1 Mami Yamashita, 1 Dan Kawahara, 1 Takeshi Ishii, 1 Masahiko Yamada, 1 Tetsuzo Tomosugi, 1 Kazuho Hirahara, 1 and Kazunori Arita 3 Objective: We report a patient with acute-phase cerebral embolism related to Trousseau s syndrome (TS) in whom thrombectomy was performed, and white thrombi were captured. Case Presentation: The patient was a 65-year-old female. Sudden-onset dizziness and progressive consciousness disorder were noted. Diagnostic imaging led to a diagnosis of occlusion of the basilar artery (BA). In the acute phase, thrombectomy was performed, and white thrombi were captured, differing from standard-type embolism. After surgery, the symptoms rapidly reduced, but systemic investigation suggested advanced gastric cancer as an etiologic factor for embolism. Subsequently, embolism recurred, and the patient died of hemorrhagic cerebral infarction 31 days after onset. Conclusion: If a white thrombus is captured during thrombectomy, TS should be differentiated as an etiologic factor. Keywords Trousseau s syndrome, embolization, thrombectomy, white thrombus Introduction Previous studies have demonstrated the efficacy and safety of thrombectomy for acute-phase cerebral embolism. 1) We encountered a patient with cerebral embolism related to Trousseau s syndrome (TS). Few studies have reported this disorder. We report the characteristic findings and clinical course, and review the literature. Case Presentation Case: A 65-year-old female. Complaint: Progressive consciousness disorder 1 Department of Neurosurgery, Kagoshima City Hospital, Kagoshima, Kagoshima, Japan 2 Atsuchi Neurosurgical Hospital, Kagoshima, Kagoshima, Japan 3 Department of Neurosurgery, Kagoshima University Graduate School of Medicine and Dental Sciences, Kagoshima, Kagoshima, Japan Received: January 20, 2017; Accepted: June 8, 2017 Corresponding author: Yosuke Nishimuta. Department of Neurosurgery, Kagoshima City Hospital, 37-1 Uearata, Kagoshima, Kagoshima , Japan yosuke-n@m.kufm.kagoshima-u.ac.jp This work is licensed under a Creative Commons Attribution-NonCommercial- NoDerivatives International License The Japanese Society for Neuroendovascular Therapy Medical history: Not contributory. Present illness: The patient had a 1-month history of vertigo. At a local clinic, MRI was performed, but there were no abnormal findings. After she went to bed at 22:00, left occipital headache, dizziness, nausea, and articulation disorder suddenly appeared at 1:00, and she was transported to the local clinic by ambulance. A diagnosis of cerebral infarction was made based on imaging findings, and treatment was started. However, the consciousness level gradually reduced, and she was referred to our hospital at 12:05. Findings on admission: The blood pressure, pulse, body temperature, and respiratory rate were 157/76 mmhg, 64 beats/min, 36.7 C, and 18/min, respectively. Electrocardiography showed sinus rhythm. Neurologic findings on admission: The consciousness level was evaluated as E3V4M6 using the Glasgow Coma Scale (GCS). Concerning the cranial nervous system, right homonymous hemianopsia and dysphemia were noted. Concerning the motor system, left hemiplegia was observed (Manual Muscle test [MMT]: 4/5), and the National Institute of Health Stroke Scale (NIHSS) score was 8 points, but there were no cerebellar symptoms. Hematologic data: The leukocyte count, erythrocyte count, hemoglobin level, platelet count, international normalized ratio of prothrombin time (PT-INR), activated partial thromboplastin time (APTT), fibrin level, D-dimer level, 575
2 Nishimuta Y, et al. Fig. 1 Imaging findings on admission. (A and B) MRI-DWIs of the head showed scattered high-signal-intensity areas, involving the cortex, in the medial areas of the bilateral (especially left) occipital and right frontal lobes (white arrows). (C) MRA revealed occlusion of the basilar (white arrow) and right anterior cerebral arteries (A1) (white arrow head). DWIs: diffusion-weighted images C-reactive protein (CRP) level, and brain natriuretic peptide (BNP) level were 6200/µL, /µl, 11.0 g/dl, /µl, 1.2, 39.6 seconds, 138 mg/dl, 30.3 g/ml, 1.87 mg/dl, and 71.4 pg/ml, respectively, suggesting mild anemia, slight thrombopenia, a slight increase in the CRP level, and a marked increase in the D-dimer level. Neuroradiologic findings: On MRI, diffusion-weighted images (DWIs) showed scattered high-signal-intensity areas, involving the cortex, in the bilateral posterior (especially left) and right anterior cerebral arterial territories. There were no fresh infarcted foci in the brainstem or thalamus (Fig. 1A and 1B). MRA revealed occlusion of the basilar artery (BA), and the bilateral posterior cerebral arteries (PCAs) were not visualized. Furthermore, the right anterior cerebral artery (A1 area) was occluded (Fig. 1C). Arteriosclerosis was not suggested in any other blood vessels, including the cervical blood vessels. The PC-Alberta Stroke Programme Early CT (ASPECT) Score was 8 points. Course after admission: A diagnosis of cerebral embolism was made based on multiple major cerebral artery occlusion, which suddenly occurred. Initially, cardiogenic cerebral embolism was suspected. Although the interval from onset was 8 hours, progressive consciousness disorder related to BA occlusion was noted, and thrombectomy was performed. Under local anesthesia, a 6F FUBUKI (Asahi Intec, Aichi, Japan) was inserted into the left vertebral artery through the right femoral artery at 13:20. On diagnostic angiography, neither the BA end nor its periphery was visualized (Fig. 2A). A Trevo Pro14 (Stryker, Kalamazoo, MI, USA) was promptly inserted into the left P2 area, and a Trevo ProVue Retriever 3 mm 20 mm was developed in the left P2-BA area using the push and fluff method. Two passes led to recanalization. In addition, similarly, a Trevo ProVue Retriever 3 mm 20 mm was developed in the right P2-BA area, and a white, slightly hard thrombus was collected (Fig. 2C) through two passes. However, recanalization at the periphery of the right PCA was not achieved, and surgery was completed, with the Thrombolysis in Cerebral Infarction (TICI) grade being evaluated as 2b (Fig. 2B). After surgery, anticoagulant therapy by the continuous drip infusion of heparin (15000 units/day) and therapy with edaravone were administered. The consciousness level became clear the day after surgery, 576
3 Cerebral Embolism Related to Trousseau s Syndrome Fig. 2 First session of thrombectomy. (A) Preoperative left vertebral arteriography (anterior and posterior views) revealed occlusion of the basilar artery. (B) Postoperative left vertebral arteriography (anterior and posterior views) showed recanalization of the basilar and left posterior cerebral arteries. However, occlusion of the right posterior cerebral artery (P3 or peripheral) (black arrow head) was noted. (C) White thrombi and stent retriever. and only mild right homonymous hemianopsia was observed. The patient became able to walk. For detailed examination of the source of embolism, Holter electrocardiography, continuous electrocardiographic monitoring, transthoracic echocardiography, and lower limb vein echography were performed, but there were no abnormalities. For aortic plaque diagnosis, contrast-enhanced CT of the aorta was performed 10 days after admission. Marked lymph node swelling and thickening of the gastric wall were observed. In addition, tumor marker tests showed increases in the carcinoembryonic antigen (CEA) and carbohydrate antigen 19-9 (CA19-9) levels (193 ng/ml and 111 U/mL, respectively) and a normal soluble IL-2 receptor level (510 U/mL), suggesting advanced gastric cancer. To further investigate the source of embolism, transesophageal echography was scheduled 12 days after admission. While heparin administration was temporarily discontinued (for 1 hour), consciousness disorder (GCS: E4V4M6), right conjugate deviation, left spatial neglect, restlessness, and left hemiplegia (MMT 1/5) suddenly appeared. Although continuous electrocardiographic monitoring was continued, there was no arrhythmia, such as atrial fibrillation. Puncture was performed 1.5 hours after the final pre-disease time, and detailed diagnostic imaging procedures, including DSA, showed a DWI-ASPECT score of 11 points, suggesting re-embolism at the right M2 inferior trunk. Emergency thrombectomy was again performed following DSA. As described above, a Trevo ProVue Retriever 3 mm 20 mm was developed (two passes), but recanalization was not achieved. At this point, early deep venous filling was observed (Fig. 3A and 3B). Considering the risk of hemorrhage and prognosis of a strongly suspected malignant tumor, the procedure was discontinued. Gastric biopsy was performed 17 days after admission. The patient was diagnosed with signet-ring cell carcinoma (poorly differentiated adenocarcinoma), and the life expectancy was estimated to be a few months. Subsequently, left hemiplegia and spatial neglect persisted, but heparin (15000 units/day) was switched to an oral Xa inhibitor (rivaroxaban at 15 mg) 19 days after admission (7 days after the onset of second embolism) to discharge the patient based on her family s wishes. However, consciousness disorder (GCS: E1V1M2) and ataxic respiration related to the second episode of hemorrhage in the infarcted focus (Fig. 4A and 4B) suddenly appeared 26 days after admission. The patient died of hemorrhagic cerebral infarction 31 days after onset. Discussion In 1865, Trousseau reported that TS was a condition in which a latent malignant tumor induces multiple, migrating venous thrombi. 2) Currently, TS is considered to be the state of thrombosis tendency caused by latent or recently diagnosed malignant tumors in the absence of other factors; it may be mediated by several mechanisms. 3) However, its definition remains to be established. Finelli et al. 4) reported that imaging findings of TSrelated cerebral infarction included multiple infarction in most patients, and that it accounted for 22% of patients with a high signal intensity involving 3 blood vessels on DWIs and 75% of those in whom the source of embolism was unclear. 577
4 Nishimuta Y, et al. Fig. 3 (A) MRI-DWIs at the onset of second embolism did not show any high-signal-intensity areas. (B) Preoperative right internal carotid arteriography (lateral view) revealed occlusion of the right inferior trunk (white arrow). (C) Right internal carotid arteriography (lateral view) after two passes did not confirm recanalization of the right inferior trunk. Early deep venous filling (black arrow head) was observed. DWIs: diffusion-weighted images Fig. 4 (A and B) CT revealed extensive hemorrhagic infarction in the second infarcted focus and marked compression. Case reports on thrombectomy for TS-related embolism of the major cerebral artery are rare. To our knowledge, only four patients, 6,7) including the present patient, have been reported. Of these, three had been diagnosed with malignant tumors before the onset of cerebral infarction, but, in the present case, idiopathic, multiple cerebral embolism initially occurred. The hematologic data on admission showed disturbance of the coagulation-fibrinolysis system, but there was no other factor involved in embolism. Systemic investigation led to a diagnosis of an advanced malignant tumor, suggesting TS-related cerebral embolism. Thrombectomy for the first episode of embolism was performed in the acute phase, rapidly reducing the symptoms. However, the thrombi captured were macroscopically white and slightly hard, differing from standard-type (dark) red thrombi. Pathologically, there was no malignancy, and the thrombi consisted of fibrin (Fig. 5). The characteristics of the thrombi were common with those in the three previously reported patients. 6,7) In many cases, white thrombi are related to atherosclerotic cerebral infarction. In the present case, there was no risk factor or arteriosclerosis in other blood vessels; therefore, the possibility of atherosclerotic cerebral infarction was ruled out. Etiologic factors for TS include arterial/venous thrombosis related to the enhancement of the blood coagulation system, microembolism related to disseminated endovascular coagulation, and tumor embolism. 5) However, nonbacterial thrombotic endocarditis (NBTE) may also be involved in hypercoagulation as the source of embolism. 8) A study indicated that NBTE was the most frequent cause of symptomatic cerebral infarction on autopsy in malignant tumor patients with stroke, accounting for 27%. 9) In these patients, white thrombi consisted of fibrin or platelets. 10,11) 578
5 Cerebral Embolism Related to Trousseau s Syndrome Fig. 5 Histopathology of the thrombi captured. Hematoxylin-eosin staining (A) 10-fold, (B) 50-fold. Most fibrins were colored pink with eosin. A small number of leukocytes were detected. There was no erythrocyte. Table 1 Summary of four patients who underwent thrombectomy for Trousseau s syndrome Author Age (years) Sex Occulution site Color of thrombus Initial treatment Reccurence Outcome 1 Matsumoto 5) 67 M BA White Success n.m. n.m. 2 Matsumoto 5) 84 F L.MCA White Success Yes n.m. 3 Inoue 6) 66 M L.MCA White Success Yes Death 4 our case 65 F BA White Success Yes Death BA: basilar artery; F: female; L: left; M: male; MCA: middle cerebral artery; n.m.: no mention Concerning drug therapy for TS-related embolism, there is no evidence regarding selective Xa or thrombin inhibitors. 5) Although heparin is effective, 3) recurrent thrombosis related to the discontinuation of heparin was reported; 3) the administration method and period must be reviewed. In the present case, embolism also recurred after the discontinuation of heparin; the necessity of continuous drip infusion over a long period should be reviewed. In the present case, recurrence could be prevented by orally administering a Xa inhibitor to achieve discharge. However, finally, hemorrhagic infarction occurred on day 26, leading to an unfavorable prognosis. As TS-related abnormalities in the coagulation system were present as a background factor, it was necessary to consider the low-dose administration of the Xa inhibitor or self-injection of heparin calcium. Thus, TS-related occlusion of the major cerebral artery may have the following characteristics based on previous studies: 6,7) 1) white thrombi are captured; 2) thrombectomy may reduce symptoms; 3) several episodes of embolism may occur in a short period; and 4) the prognosis is unfavorable due to the progression of the primary disease or coagulation disorder (Table 1). With advances in treatment for acute-phase cerebral infarction, physicians specializing in endovascular treatment have increasingly encountered patients with TS-related major artery occlusion. If a white thrombus is captured during thrombectomy in the absence of malignant tumor detection before onset, as demonstrated in the present case, the etiology must be investigated, considering TS as a disease to be differentiated. Conclusion We encountered a patient with TS-related major artery occlusion in whom white thrombi were captured. Disclosure Statement There is no conflict of interest for the main author or coauthors. References 1) Berkhemer OA, Fransen PS, Beumer D, et al: A randomized trial of intraarterial treatment for acute ischemic stroke. N Engl J Med 2015; 372: ) Trousseau A: Plegmasia alba dolens. Lectures on clinical medicine. Delivered at the hotel-dieu, Paris; 1865; 5:
6 Nishimuta Y, et al. 3) Varki A: Trousseau s syndrome: multiple definitions and multiple mechanisms. Blood 2007; 110: ) Finelli PF, Nouh A: Three-territory DWI acute infarcts: diagnostic value in cancer-associated hypercoagulation stroke (Trousseau syndrome). AJNR Am J Neuroradiol 2016; 37: ) Matsumoto N, Fukuda H, Handa A, et al: Histological examination of Trousseau syndrome-related thrombus retrieved through acute endovascular thrombectomy: report of 2 cases. J Stroke Cerebrovasc Dis 2016; 25: e227 e230. 6) Inoue S, Fujita A, Mizowaki T, et al: [Successful treatment of repeated bilateral middle cerebral artery occlusion by performing mechanical thrombectomy in a patient with trousseau syndrome]. No Shinkei Geka 2016; 44: (in Japanese) 7) Ikushima S, Ono R, Fukuda K, et al: [Trousseau s syndrome: cancer-associated thrombosis]. Jpn J Clin Oncol 2016; 46: (in Japanese) 8) Lopez JA, Ross RS, Fishbein MC, et al: Nonbacterial thrombotic endocarditis: a review. Am Heart J 1987; 113: ) Graus F, Rogers LR, Posner JB: Cerebrovascular complications in patients with cancer. Medicine (Baltimore) 1985; 64: ) Eiken PW, Edwards WD, Tazelaar HD, et al: Surgical pathology of nonbacterial thrombotic endocarditis in 30 patients, Mayo Clin Proc 2001; 76: ) Sutherland DE, Weitz IC, Liebman HA: Thromboembolic complications of cancer: epidemiology, pathogenesis, diagnosis, and treatment. Am J Hematol 2003; 72:
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