Dementia associated with the antiphospholipid syndrome: clinical and radiological characteristics of 30 patients
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1 Rheumatology 2005;44:95 99 Advance Access publication 14 eptember 2004 Concise Report Dementia associated with the antiphospholipid syndrome: clinical and radiological characteristics of 30 patients J. A. Go mez-puerta, R. Cervera, L. M. Calvo, B. Gómez-Ansón 1, G. Espinosa, G. Claver,. Bucciarelli, A. Bové, M. Ramos-Casals, M. Ingelmo and J. Font doi: /rheumatology/keh408 Objective. To analyse the clinical and radiological characteristics of patients with dementia associated with the antiphospholipid syndrome (AP). Methods. Twenty-five patients were identified by a computer-assisted (MEDLINE, National Library of Medicine, Bethesda, MD) search of the literature to locate all cases of dementia associated with AP published in English, panish and French from 1983 to Additionally, we included five patients from our clinics. Results. There were 21 (70%) females and 9 (30%) males. The mean age of patients was 4915 yr (range yr). Fourteen (47%) of the patients suffered from primary AP, 9 (30%) had systemic lupus erythematosus and 7 (23%) had lupus-like syndrome. Ten (33%) patients had neddon s syndrome and 2 (7%) had cerebral lesions described as Binswanger s disease. Other AP-related manifestations included thrombocytopenia in 12 (40%) patients, cerebrovascular accidents in 11 (37%), heart valve lesions in 8 (27%), deep vein thrombosis in 7 (28%), migraine in 7 (23%), seizures in 4 (13%); five of the 21 (24%) female patients had nine spontaneous abortions. Lupus anticoagulant was present in 21/29 (72%) patients and anticardiolipin antibodies were present in 24/29 (83%) patients. Cortical infarcts were found in 19 (63%) patients, subcortical infarcts in 9 (30%), basal ganglia infarcts in 7 (23%) and signs of cerebral atrophy in 11 (37%). Anticoagulation was used in 14/25 (56%) patients, steroids in 12/25 (48%), aspirin in 6/25 (24%) and dypiridamole in 5/25 (20%). Conclusions. Dementia is an unusual manifestation of AP but one which has a high disability impact in a patient s daily life. In order to prevent these consequences, an echocardiographic and cerebral CT or MRI evaluation are recommended in all patients with AP. Furthermore, ruling out AP should be recommended in the clinical approach to dementia, especially in young patients. KEY WORD: Antiphospholipid syndrome, Dementia, Vascular dementia, Multi-infarct dementia, neddon s syndrome, Binswanger s disease. Dementia is being increasingly diagnosed in clinical practice and has a high disability impact in a patient s daily life. Alzheimer s disease is the main cause of dementia, followed by vascular multi-infarct dementia, Parkinson s disease, frontal lobe dementia and, less commonly, other metabolic and reversible causes of dementia [1]. The antiphospholipid syndrome (AP) is an autoimmune prothrombotic condition characterized by venous and/or arterial thrombosis and pregnancy morbidity in the presence of antiphospholipid antibodies (apl), i.e. lupus anticoagulant (LA) and anticardiolipin antibodies (acl) [2]. Involvement of cerebral large vessels is frequent in AP and patients usually present clinically with transient ischaemic attacks (TIA) and strokes. However, a wide spectrum of other neurological features has been described, including chorea, epilepsy, multiple sclerosis-like lesions, psychiatric features, migraine and also dementia, among others [2, 3]. A relationship between dementia and AP has been proposed by several authors [2 7]. Although most studies have focused on patients with dementia and cerebral vascular lesions, less severe cognitive impairment has also been associated with the presence of apl in the absence of imaging lesions in the brain [7]. Furthermore, the ischaemic stroke in neddon s syndrome may overlap with AP and some of these patients suffer from severe vascular dementia. The objective of this study was to analyse the clinical and radiological features of patients with dementia associated with AP, highlighting the importance of early diagnosis of this condition. Patients and methods Patients were identified by a computer-assisted (MEDLINE, National Library of Medicine, Bethesda, MD) search of the Department of Autoimmune Diseases, Institut Clı nic de Medicina i Dermatologia, per la Imatge, Hospital Clı nic, Barcelona, Catalonia, pain. 1 Department of Neuroradiology, Centre Clı nic de Diagnòstic ubmitted 8 July 2004; revised version accepted 10 August Correspondence to: R. Cervera, ervei de Malalties Autoimmunes, Hospital Clı nic, Villarroel, 170, Barcelona, Catalonia, pain. rcervera@clinic.ub.es 95 Rheumatology Vol. 44. No. 1 ß British ociety for Rheumatology 2004; all rights reserved
2 96 J. A. Go mez-puerta et al. TABLE 1. General characteristics of 30 patients with dementia and AP Author Gender/ age Diagnosis Associated neddon a Other manifestation Dementia diagnosis apl CN imaging Treatment 1. Asherson et al. [12] F/52 Lupus-like LR, migraine, DVT imultaneously LA, aclþ CT: multiple hemispheric cortical infarcts,, D,, D 2. Asherson et al. [12] F/33 LE þ LR, migraine, DVT, AHA, TIA, chorea, VL 3. Asherson et al. [12] F/32 LE þ Migraine, LR, CVA DVT, thrombocytopenia 4. Asherson et al. [12] F/43 LE Migraine, A (2), sup. thrombophlebitis 7 yr later LA, aclþ CT: multiple cortical infarcts and thalamic lacunar infarct 7 yr later LA, aclþ CT: multiple cortical infarcts, D, AA 1.5 yr later acl IgG CT: multiple bilateral small lacunar and subcortical infarcts in the frontal cand occipitalwhite matter 5. Coull et al. [13] b M/59 PAP CVA, AHA, MI imultaneously aclþ CT: bilateral cortical cerebral infarcts 6. Coull et al. [13] M/43 PAP CVA, thrombocytopenia imultaneously aclþ CT: multiple cortical and subcortical infarctions 7. Coull et al. [13] M/69 PAP CVA 6 yr later aclþ CT: multiple small cortical infarctions AA, D 8. Coull et al. [13] F/28 PAP CVA 2.5 yr later aclþ CT: multiple cortical and subcortical AA, D infarctions 9. Montalba n et al. [14] M/47 Lupus-like Migraine, thrombocytopenia retinal vein occlusion, VL 10 yr later LA acl CT: multiple cortical infarcts 10. Montalba n et al. [14] F/37 LE-like A, seizure, CVA 5 yr later LA acl CT: one cerebral cortical infarction AA 11. Asherson et al. [15] M/42 Lupus-like þ LR, MI, skin ulcers, thrombocytopenia, VL, thrombotic glaucoma 3 yr later LA, aclþ CT: multiple bilateral occipital and parietotemporal infarcts 12. Asherson et al. [15] F/45 PAP Migraine 5 yr later aclþ CT: multiple cortical and small subcortical infarcts 13. Asherson et al. [15] F/42 Lupus-like þ PE (2), LR, CVA, A (3), VL imultaneously LA, acl CT: multiple small cortical infarcts, 14. Westerman et al. [16] b M/54 Lupus-like Thrombocytopenia imultaneously acl IgG MRI: multiple cortical and subcortical hyperintense areas 15. Charles et al. [17] F/16 PAP þ Thrombocytopenia, LR,VL imultaneously aclþ MRI: bilateral thalamic lesions of high signal intensity (infarctions) 16. Kurita et al. [18] M/39 PAP CVA imultaneuosly LAþ CT: multiple brain infarcts 17. Robin et al. [19] F/62 LE Optic neuritis 2 yr later LA, aclþ CT: atrophy and subcortical low-attenuation areas MRI: hyperintensities in periventricular white matter 18. Robin et al. [19] F/63 LE kin ulcers 2 yr later LAþ CT: atrophy and subcortical low-attenuation areas. MRI: hyperintensities in periventricular white matter 19. erra-mestres [20] M/68 PAP þ LR 5yr later aclþ MRI: diffuse white matter hyperintensitities 20. van-horn et al. [21] F/22 Lupus-like up. thrombophlebitis, chorea 1 yr later LA MRI: caudate and white matter hyperintensities., AA PECT: bilaterally decreased perfusion 21. Tomimoto et al. (22) F/60 PAP imultaneously LAþ MRI: diffuse patchy hyperintensities in basal ganglia and cerebral white matter 22. Rich et al. [23] F/34 PAP þ LR, thrombocytopenia, A, VL imultaneously LA, aclþ CT: atrophy. MRI: lacunar hyperintensities consistent with infarcts 23. Fukui et al. [24] F/50 LE Thrombocytopenia, retinal vein thrombosis, seizures 3 yr later LA, aclþ MRI: generalized and progressive, multiple hyperintensities. PECT: defects in bilateral temporoparietal regions 24. Hilker et al. [25] M/55 PAP DVT, thrombocytopenia 5 yr later LA, aclþ MRI: non-specific lacunar lesions in 25. Rodríguez Campello et al. [26] basal ganglia and hyperintensities in periventricular white matter, atrophy F/50 PAP þ Thrombocytopenia, LR imultaneously LA, aclþ CT: cortical and subcortical infarcts. MRI: cortical infarcts and white matter hyperintensities 26. PC 1 F/79 PAP Thrombocytopenia, CVA DVT, PE, A (2), migraine, seizures 1 yr later LA MRI: cortical, subcortical and basal ganglia infarcts, atrophy 27. PC 2 F/49 Lupus-like Thrombocytopenia, VL, seizures imultaneously LA, aclþ MRI: cortical and subcortical infarcts and periventricular white matter hyperintensities 28. PC 3 F/69 LE MI, DVT, CVA 2 yr later LA MRI: cortical infarct in right parietal lobe 29. PC 4 F/72 LE þ LR, thrombocytopenia, CVA, DVT, TIA 4 yr later LA, acl MRI: cortical infarct in occipital lobe 30. PC 5 F/52 PAP Thrombocytopenia, VL 4 yr later LA, aclþ CT: cortical infarcts,, AA, a Associated neddon s syndrome (the co-existence of hypertension, livedo reticularis and stroke). b Microthrombosis in cerebral biopsy. Abbreviations:, anticoagulation; AHA, autoimmune haemolytic anaemia; AA, aspirin; acl, anticardiolipin antibodies; apl, antiphospholipid antibodies; AP, antiphospholipid syndrome; CN, central nervous system; CT, computed tomography; CVA, cerebrovascular accident; D, dypiridamole; F, female; LA, lupus anticoagulant; LR, livedo reticularis; M, male; MI, myocardial infarction; MRI, magnetic resonance imaging;, none reported; PAP, primary antiphospholipid syndrome; PC, present case; PE, pulmonary embolism;, steroids; A, spontaneous abortions; LE, systemic lupus erythematosus; PECT, single-photon emission computed tomography; TIA, transient ischaemic attack; VL, valve lesions.
3 Dementia and antiphospholipid syndrome 97 literature to locate all cases of AP published in English, panish and French from 1983 (when AP was first defined) to December 2003 (keywords used were: anticardiolipin antibodies, lupus inhibitor, cardiolipin, coagulation inhibitor, lupus anticoagulant, antiphospholipid syndrome, antiphospholipid antibodies, multiinfarct dementia, vascular dementia, neddon s syndrome, Alzheimer s disease and Binswanger s disease). Cases having neddon s syndrome with dementia but without apl were not included. Only cases with well-documented clinical summaries and relevant information were included in this review. Data from these cases were summarized using a standardized data form, including gender, age, diagnosis of the underlying condition, the major thrombotic clinical manifestations, immunological features, time of the evolution since the diagnosis of AP until the development of dementia, imaging features and treatment. Five new cases with dementia and AP from our clinics were added to the review. Those patients diagnosed as having dementia who were included in large AP series, but in whom no well-documented clinical data were recorded, were not considered for analysis in the present study. Patients were defined as having dementia according to the Diagnostic and tatistical Manual of Mental Disorders (DM-IV) [8]. They were classified as having systemic lupus erythematosus (LE) if they met four or more criteria of the American College of Rheumatology [9, 10], as lupus-like syndrome if they met only two or three criteria and as primary AP if they met criteria of the International Consensus tatement on Preliminary Classification Criteria for definite AP, and did not meet any of the above described criteria for LE or lupus-like syndrome [11]. Ethical approval and informed patient consent were not required because the study was an analysis of patients that were located by means of a computer-assisted (MEDLINE, National Library of Medicine, Bethesda, MD) search of the literature. Results A total of 25 patients with dementia associated with AP were found in the literature search [12 26]. We did not include those cases where clinical, immunological and imaging characteristics were not described in detail. Five additional patients from our clinics were also reviewed. General characteristics General clinical features of these 30 patients are shown in Table 1. There were 21 (70%) females and 9 (30%) males. The mean age of patients was yr (range yr). Fourteen (47%) of the patients suffered from primary AP, 9 (30%) had LE and 7 (23%) patients had lupus-like syndrome. Ten (33%) patients had neddon s syndrome and 2 (7%) had cerebral lesions described as Binswanger s disease. Clinical presentation Dementia was the presenting manifestation of the AP in 11 (37%) patients. A clinically evident past history of CVA was detected in 11 (37%) patients. Other neurological features included migraine in 7 (23%) patients, seizures in 4 (13%), TIA in 2 (7%), chorea in 2 (7%), and retinal thrombosis in 2 (7%) patients. Thrombotic glaucoma and optic neuritis were present in 1 (3%) case each. kin involvement in the form of livedo reticularis (as a manifestation of neddon s syndrome) was reported in 10 (33%) patients, and skin ulcers in 3 (10%). Other AP-related manifestations were as follows: 8 (27%) patients had heart valve lesions, 7 (23%) deepvein thrombosis (DVT), 2 (7%) pulmonary embolism, 3 (10%) myocardial infarction and 2 (7%) superficial thrombophlebitis. Previous spontaneous abortions (n ¼ 9) were reported in 5 of the 21 (24%) female patients. Laboratory profile Twelve (40%) patients had thrombocytopenia and 2 (7%) had autoimmune haemolytic anaemia. LA was present in 21/29 (72%) patients, whilst acl was present in 24/29 (83%) patients. Neuroimaging features Most patients exhibited several types of lesions on cerebral computed tomography (CT) scan or magnetic resonance imaging (MRI). Cortical infarcts were detected in 19 (63%) patients, subcortical infarcts in 9 (30%), basal ganglia infarcts in 7 (23%) and cerebral atrophy in 11 (37%). ilent brain infarcts (cerebral ischaemic lesions without any focal neurological features) were found in 14 (47%) patients. Treatment and evolution towards dementia Anticoagulation was used in 14/25 (56%) patients, steroids in 12/25 (48%), aspirin in 6/25 (24%) and dypiridamole in 5/25 (20%). Treatment was not reported for five cases. In the 19 (63%) patients who presented AP manifestations previous to the diagnosis of dementia, anticoagulation had been used in 7 (37%) patients, steroids in 6 (32%), aspirin in 5 (26%) and dypiridamole in 4 (21%). The mean time of evolution from the initial AP manifestations to the diagnosis of dementia in these 19 patients was 3.5 yr (range, 1 10 yr). Discussion The relationship between dementia and AP has been proposed in several studies. Mosek et al. [6] studied 87 patients diagnosed as having dementia and compared them with 69 elderly healthy controls. They found higher levels of apl in patients with dementia than in controls. Juby et al. [27] analysed the prevalence of acl in 218 elderly patients. They disclosed that 34 patients suffered from dementia and a significant association between acl and both vascular dementia and Alzheimer s disease was noted. Recently, Chapman et al. [4] studied 23 patients with primary AP and found that 13 (56%) fulfilled criteria for dementia using the Hachinski Ischemia core (HI). Patients with dementia were older, had more CT scan abnormalities and more electroencephalography changes than those without dementia. However, the Euro-Phospholipid consortium, in their cohort of 1000 AP patients, described the presence of vascular dementia in only 25 (2.5%) cases [2]. It is possible that the higher prevalence of dementia in the Chapman et al. series [4] could be merely due to the small and probably highly selected group of patients studied, but it could also be due to the exclusion of LE patients as it is know that in AP associated with LE the incidence of neurological manifestations is higher than in primary AP [28]. The presence of apl in patients with cognitive problems seems to be more than an epiphenomenon, as it has been demonstrated in experimental studies. hrot et al. [29] performed an elegant study with BALB/c mice using a staircase test and a T maze alternation test as cognitive assessment tools. Mice immunized with anti-2- glycoprotein I antibodies developed a higher degree of behavioural and cognitive abnormalities than those that had not been immunized. One-third of the patients from our series had neddon s syndrome. France` s et al. [30] described a specific subset of patients with this syndrome having apl who presented more thrombocytopenia, mitral regurgitation and irregular livedo reticularis than
4 98 J. A. Go mez-puerta et al. patients without apl. There is controversy concerning whether patients with neddon s syndrome without apl could be a special group of transient seronegative AP patients. In the present study, almost one-third of patients had valve disease. It is well known that a high proportion of cerebral infarcts have a cardiac embolic origin and that patients with apl have higher prevalence of valvular abnormalities [31]. Thickening of the valve leaflets is the most common lesion detected by echocardiography in both LE and primary AP patients. The mitral valve is involved most commonly, followed by the aortic valve [32]. Epilepsy is a common neurological manifestation in AP [2]. Recent studies by hoenfeld et al. [33] have confirmed a link between this manifestation and cerebrovascular involvement, heart valve lesions and livedo reticularis. In the present series, 13% of the patients with dementia presented seizures, thus reinforcing the role of focal brain ischaemic lesions in the pathogenesis of AP-related epilepsy. Patients with dementia exhibit a wide variety of cerebral lesions on CT or MRI studies. Cortical and subcortical infarcts are the more frequent findings. Other ischaemic lesions such as lacunar and periventricular infarcts are not uncommon. Cerebral atrophy and white matter lesions (leukoaraiosis), similar to the lesions found in Binswanger s disease, are often seen, specially in elderly AP patients [15]. In LE, these findings have been shown to be in close association with the presence of AP, but other factors, e.g. hypertension, could also contribute to their presence [34]. The continuous improvement and development of new CN imaging techniques [i.e. positron emission tomography (PET) or singlephoton emission computed tomography (PECT)] will allow to us differentiate the distinct perfusion patterns on these cerebral disorders. Kao et al. [35] studied 22 patients with primary AP with only mild neuropsychiatric manifestations (headache, depression, personality disorders, memory loss and cognitive function deficits) and normal brain MRI. They found that 16 (73%) of the patients had abnormal PECT findings, mainly diffuse hypoperfusion lesions in cerebral cortex. It is not only those patients with evident cerebral lesions and cognitive impairment who deserve special attention, but also those patients with an asymptomatic course or subtle decline in cerebral functions having cerebral ischaemic lesions on MRI (silent brain infarcts). Vermeer et al. [36] followed 1077 elderly patients without dementia over 5 yr, with periodical MRI evaluation. Two hundred and seventeen (21%) patients had silent brain infarcts at baseline, with a global cognitive function significantly worse than in those patients without brain infarcts. During the follow-up, 30 (3%) of these patients developed dementia. Erkan et al. [5], in a 10-yr follow-up study of 66 patients with primary AP, found that 3 patients (<30 yr old) developed dementia, independently of the presence of CVA. In the present series, previous history of CVA and/or TIA was present in only 11 and 2 patients, respectively; however, silent brain infarcts were present in 14 (47%) patients. everal strategies have been suggested for the treatment of dementia. The management of atherogenic risk factors (i.e. diabetes, hypertension, hyperlipidaemia) is crucial. However, there is still no evidence that aspirin alone is effective in treating patients with a diagnosis of dementia. In dementia associated with AP, anticoagulant treatment is required, with special care in possible everyday situations with the risk of bleeding. Furthermore, the compliance of demented patients is usually poor, which requires special thought and attention. On the other hand, prevention of dementia should be of paramount importance in those patients with a diagnosis of AP. Unfortunately, it is difficult from the present study to recommend any therapeutic strategy because patients were previously treated with a variety of medications. However, it is worth noting that the majority of patients were not on anticoagulants when the first manifestations of dementia appeared. Therefore, this reinforces the need for active antithrombotic prophylaxis once the diagnosis of AP is made. In conclusion, dementia can be present in patients with AP in multiple scenarios, such as primary AP, neddon s syndrome or with white matter lesions similar to Binswanger s disease. Due to the high disability impact and prognostic consequences, we consider that an echocardiographic and cerebral CT or MRI evaluation should be recommended in all patients with AP. Also, it is important to rule out an AP in young subjects with no explicable cause of dementia, and therefore apl should be tested in these patients in order to prevent disease progression and enable adequate treatment to begin. Rheumatology The authors have declared no conflicts of interest. References Key messages An echocardiographic and cerebral CT or MRI evaluation are recommended in all patients with AP. Ruling out AP should be recommended in the clinical approach to dementia. 1. Roman GC. Vascular dementia: distinguishing characteristics, treatment, and prevention. J Am Geriatr oc 2003;51: Cervera R, Piette JC, Font J et al. Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum 2002;46: Chapman J, Rand JH, Brey RL et al. Non-stroke neurological syndromes associated with antiphospholipid antibodies: evaluation of clinical and experimental studies. Lupus 2003;12: Chapman J, Abu-Katash M, Inzelberg R et al. Prevalence and clinical features of dementia associated with the antiphospholipid syndrome and circulating anticoagulants. J Neurol ci 2002; : Erkan D, Yazici Y, obel R, Lockshin MD. Primary antiphospholipid syndrome: functional outcome after 10 years. J Rheumatol 2000;27: Mosek A, Yust I, Treves TA, Vardinon N, Korczyn AD, Chapman J. Dementia and antiphospholipid antibodies. Dement Geriatr Cogn Disord 2000;11: astre-garriga J, Montalban X. AP and the brain. Lupus 2003; 12: American Psychiatric Association. Diagnostic and tatistical Manual of Mental Disorders, 4th edition (DM-IV), Washington, Tan EM, Cohen A, Fries JF et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25: Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997;40: Wilson WA, Gharavi AE, Koike T et al. International consensus statement on preliminary classification criteria for definite antiphospholipid syndrome: report of an international workshop. Arthritis Rheum 1999;42: Asherson RA, Mercey D, Philips G et al. Recurrent stroke and multiinfarct dementia in systemic lupus erythematosus: association with antiphospholipid antibodies. Ann Rheum Dis 1987;46: Coull B, Bourdette DN, Goodnight H Jr, Briley DP, Hart R. Multiple cerebral infarctions and dementia associated with anticardiolipin antibodies. troke 1987;18: Montalbán J, Fernández J, Arderiu A et al. Demencia multiinfártica asociada a anticuerpos antifosfolı pido. Presentacio n de dos casos. Med Clin (Barc) 1989;93:424 6.
5 Dementia and antiphospholipid syndrome Asherson RA, Khamashta MA, Gil A et al. Cerebrovascular disease and antiphospholipid antibodies in systemic lupus erythematosus, lupus-like disease, and the primary antiphospholipid syndrome. Am J Med 1989;86: Westerman EM, Miles JM, Backnova M, undst W. Neuropathologic findings in multi-infarct dementia associated with anticardiolipin antibody. Arthritis Rheum 1992;35: Charles PD, Fenichel GM. neddon and antiphospholipid antibody syndromes causing bilateral thalamic infarction. Pediatr Neurol 1994;10: Kurita A, Hasunuma T, Mochio, himada T, Isogai Y, Kurahashi T. A young case with multi-infarct dementia associated with lupus anticoagulant. Intern Med 1994;33: Robin C, Gonnaud PM, Durieu I et al. Progressive lupus dementia. 2 cases with or without antiphospholipid antibodies. Rev Neurol (Paris) 1995;151: erra-mestres J. Antiphospholipid antibodies and Binswanger s disease. Neurology 1996;46: van Horn G, Arnett FC, Dimachkie MM. Reversible dementia and chorea in a young woman with the lupus anticoagulant. Neurology 1996;46: Tomimoto H, Akiguchi I, Ohtani R, Yagi H, Ogura, Wakita H. Effects of an antithrombin drug in patients with subacute exacerbations of Binswanger disease. Intern Med 2000;39: Rich MW. neddon syndrome and dementia. Mayo Clin Proc 1999;74: Fukui T, Kawamura M, Hasegawa Y, Kato T, Kaga E. Multiple cognitive impairments associated with systemic lupus erythematosus and antiphospholipid antibody syndrome: a form of progressive vascular dementia? Eur Neurol 2000;43: Hilker R, Thiel A, Geisen C, Rudolf J. Cerebral blood flow and glucose metabolism in multi-infarct-dementia related to primary antiphospholipid antibody syndrome. Lupus 2000;9: Rodríguez Campello A, Roquer J, Munteis E, Gomis M, Pou A. neddon syndrome presenting with dementia. Neurología 2002;17: Juby A, David JA, Genge T, McElhaney J. Anticardiolipin antibodies in two elderly subpopulations. Lupus 1995;4: oltész P, Veres K, Lakos G, Kiss E, Muszbek L, zegedi G. Evaluation of clinical and laboratory features of antiphospholipid syndrome: a retrospective study of 637 patients. Lupus 2003;12: hrot, Katzav A, Korczyn AD et al. Behavioral and cognitive deficits occur only after prolonged exposure of mice to antiphospholipid antibodies. Lupus 2002;11: Francès C, Papo T, Wechsler B, Laporte JL, Biousse V, Piette JC. neddon syndrome with or without antiphospholipid antibodies. A comparative study in 46 patients. Medicine 1999;78: Khamashta MA, Cervera R, Asherson RA et al. Association of antibodies against phospholipids with heart valve disease in systemic lupus erythematosus. Lancet 1990;335: Cervera R. Recent advances in antiphospholipid antibody-related valvulopathies. J Autoimmun 2000;15: hoenfeld Y, Lev, Blatt I et al. Features associated with epilepsy in the antiphospholipid syndrome. J Rheumatol 2004;31: Csépa ny T, Bereczki D, Kollar J, ikula J, Kiss E, Csiba L. MRI findings in central nervous system systemic lupus erythematosus are associated with immunoserological parameters and hypertension. J Neurol 2003;250: Kao CH, Lan JL, Hsieh JF et al. Evaluation of regional cerebral blood flow with 99mTc-HMPAO in primary antiphospholipid antibody syndrome. J Nucl Med 1999;40: Vermeer E, Prins ND, den Heijer T, Hofman A, Koudstaal PJ, Breteler MM. ilent brain infarcts and the risk of dementia and cognitive decline. N Engl J Med 2003;348:
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