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Antiphospholipid syndrome: Clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients
Open accessAbstract
OBJECTIVE: To analyze the clinical and immunologic manifestations of antiphospholipid syndrome (APS) in a large cohort of patients and to define patterns of disease expression. METHODS: The clinical and serologic features of APS (Sapporo preliminary criteria) in 1,000 patients from 13 European countries were analyzed using a computerized database. RESULTS: The cohort consisted of 820 female patients (82.0%) and 180 male patients (18.0%) with a mean +/- SD age of 42 +/- 14 years at study entry. "Primary" APS was present in 53.1% of the patients; APS was associated with systemic lupus erythematosus (SLE) in 36.2%, with lupus-like syndrome in 5.0%, and with other diseases in 5.9%. A variety of thrombotic manifestations affecting the majority of organs were recorded. A catastrophic APS occurred in 0.8% of the patients. Patients with APS associated with SLE had more episodes of arthritis and livedo reticularis, and more frequently exhibited thrombocytopenia and leukopenia. Female patients had a higher frequency of arthritis, livedo reticularis, and migraine. Male patients had a higher frequency of myocardial infarction, epilepsy, and arterial thrombosis in the lower legs and feet. In 28 patients (2.8%), disease onset occurred before age 15; these patients had more episodes of chorea and jugular vein thrombosis than the remaining patients. In 127 patients (12.7%), disease onset occurred after age 50; most of these patients were men. These patients had a higher frequency of stroke and angina pectoris, but a lower frequency of livedo reticularis, than the remaining patients. CONCLUSION: APS may affect any organ of the body and display a broad spectrum of manifestations. An association with SLE, the patient's sex, and the patient's age at disease onset can modify the disease expression and define specific subsets of APS.
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In the citing paper
“We had more male patients (29% vs. 18%) and primary APS cases (62% vs. 53%).”
From Clinical course of high‐risk patients diagnosed with antiphospholipid syndrome (2010) · cites this paper as [25]
In the citing paper
“Less than half of the patients reported by Cervera et al. were LA positive.”
From Clinical course of high‐risk patients diagnosed with antiphospholipid syndrome (2010) · cites this paper as [25]
In the citing paper
“This selected cohort of patients differed from the large cohort described by Cervera et al. [25,26] in several aspects.”
From Clinical course of high‐risk patients diagnosed with antiphospholipid syndrome (2010) · cites this paper as [25]
In the citing paper
“Our data come close to the data from Cervera et al., if we only considered primary APS patients (female/male ratio drops to 3.5:1) [25].”
From Clinical course of high‐risk patients diagnosed with antiphospholipid syndrome (2010) · cites this paper as [25]
In the citing paper
“These recurrences not only influence morbidity but are also the most common cause of death in APS [25].”
From Clinical course of high‐risk patients diagnosed with antiphospholipid syndrome (2010) · cites this paper as [25]
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“The catastrophic APS (CAPS) is a rare disease that affects around 1 % (0.4-1.6 %) of patients with APS [ 2 ] but is associated with a high rate of mortality [ 3 ] .”
BackgroundInfluentialUpdated assessment of the prevalence, spectrum and case definition of autoimmune disease
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“these patients when entered in the study have been previously reported.(2) Since then, this cohort of patients has been followed up by the same doctors during the ensuing 5 years.”
BackgroundMethodResultInfluentialCardiovascular disease in autoimmune rheumatic diseases
Hollan, I., Meroni, P. L., Ahearn, J. M., Tervaert, J. W. C., Curran, S., Goodyear, C. S., Hestad, K. A., Kahaleh, B., Riggio, M. P., Shields, K. J., et al. (2013) · Autoimmunity Reviews · doi:10.1016/j.autrev.2013.03.013 · Cited by 278
“A significant morbidity andmortality related to central nervous system andmyocardial arterial vessel involvement has been reported both at the presentation and during the follow-up of the aPL syndrome in large epidemiological studies [16,17].”
BackgroundAntiphospholipid syndrome: advances in diagnosis, pathogenesis, and management
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“Evidence suggests that the molecular mimicry mechanism between 2GPI and TT is one of the possible causes for APS.”
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Cervera, R., Font, J., Gómez-Puerta, J. A., Espinosa, G., Cucho, M., Bucciarelli, S., Ramos‐Casals, M., Ingelmo, M., Pietté, J. C., Shoenfeld, Y., et al. (2005) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2004.025759 · Cited by 252
“Fortunately, this is an unusual form of presentation that represents fewer than 1% of the APS cases.”
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“aCL 60 49 (82) 60 48 (80) 120 97 (81) IgG and IgM 54 15 (28) 52 22 (42) 106 37 (35) IgG alone 59 22 (37) 60 20 (33) 119 42 (35) IgM alone 55 12 (22) 52 6 (12) 107 18 (17) Anti- 2GPI 23 16 (70) 25 16 (64) 48 32 (67) IgG and IgM 23 4 (17) 23 5 (22) 46 9 (20) IgG alone 23 8 (35) 25 5 (20) 48 13 (27) IgM alone 23 4 (17) 2…”
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“events such as venous thrombosis (the most common manifestation of APS) (11).”
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Population-Level Evidence for an Autoimmune Etiology of Epilepsy
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BackgroundInfluentialAdenosine receptor agonism protects against NETosis and thrombosis in antiphospholipid syndrome
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MethodAutoantibodies against the fibrinolytic receptor, annexin 2, in antiphospholipid syndrome
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“leading cause of strokes in people under 50 years old [8].”
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Childhood systemic lupus erythematosus in Latin America. The GLADEL experience in 230 children
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Rubin, J. B., & Borden, W. B. (2012) · Current Atherosclerosis Reports · doi:10.1007/s11883-012-0226-3 · Cited by 157
“8% in a large study of APLS patients [57].”
BackgroundMoroni, G. L., Ventura, D., Riva, P., Panzeri, P., Quaglini, S., Banfi, G., Simonini, P., Bader, R., Meroni, P. L., & Ponticelli, C. E. (2004) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2003.09.011 · Cited by 153
Zuily, S., Cohen, H., Isenberg, D. A., Woller, S. C., Crowther, M. A., Dufrost, V., Wahl, D. G., Doré, C. J., Cuker, A. C., Carrier, M., et al. (2020) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.14935 · Cited by 160
Streiff, M. B., Holmstrom, B., Angelini, D. E., Ashrani, A. A., Elshoury, A., Fanikos, J. R., Fertrin, K. Y., Fogerty, A. E., Gao, S., Goldhaber, S. Z., et al. (2021) · PubMed · doi:10.6004/jnccn.2021.0047 · Cited by 149
Alijotas‐Reig, J., Ferrer‐Oliveras, R., Ruffatti, A., Tincani, A., Lefkou, E. E., Bertero, M. T., Coloma, E., Carolis, S. D., Espinosa, G., Rovere, P. Q., et al. (2014) · Autoimmunity Reviews · doi:10.1016/j.autrev.2014.12.010 · Cited by 152
Alén, J. C., Toloza, S., Fernández, M., Bastian, H. M., Fessler, B. J., Roseman, J. M., McGwin, G., Vilá, L. M., Reveille, J. D., Alarcón, G. S., et al. (2005) · Arthritis & Rheumatism · doi:10.1002/art.21149 · Cited by 147
Antiphospholipid syndrome: an overview.
Hanly, J. G. (2003) · Europe PMC (PubMed Central) · Cited by 141
The significance of autoantibodies against β2-glycoprotein I
de Groot, P. G., & Urbanus, R. T. (2012) · Blood · doi:10.1182/blood-2012-03-378646 · Cited by 146
Abdel‐Wahab, N., Talathi, S., Lopez-Olivo, M. A., & Suarez-Almazor, M. E. (2017) · Lupus · doi:10.1177/0961203317731532 · Cited by 148
Demyelination in rheumatic diseases
Theodoridou, A., & Settas, L. (2006) · Postgraduate Medical Journal · doi:10.1136/jnnp.2005.075861 · Cited by 145
Cohen, H., Cuadrado, M. J., Erkan, D., Duarte‐García, A., Isenberg, D. A., Knight, J. S., Ortel, T. L., Rahman, A., Salmon, J. E., Tektonidou, M. G., et al. (2020) · Lupus · doi:10.1177/0961203320950461 · Cited by 170
“The overall prevalence of APS has been estimated at 50 per 100,000 people,(2) with a female-to-male ratio of approximately 5:1.(3) Thrombosis, a cardinal disease manifestation, may be venous, arterial, or microvascular.”
BackgroundAntiphospholipid Syndrome Infectious Origin
Blank, M., Asherson, R. A., Cervera, R., & Shoenfeld, Y. (2004) · Journal of Clinical Immunology · doi:10.1023/b:joci.0000018058.28764.ce · Cited by 141
Cognitive Deficits in Patients With Antiphospholipid Syndrome
Tektonidou, M. G. (2006) · Archives of Internal Medicine · doi:10.1001/archinte.166.20.2278 · Cited by 139
Systematic review of case reports of antiphospholipid syndrome following infection
Abdel‐Wahab, N., Lopez-Olivo, M. A., Pinto-Patarroyo, G. P., & Suarez-Almazor, M. E. (2016) · Lupus · doi:10.1177/0961203316640912 · Cited by 137
Gómez-Puerta, J. A., Cervera, R., Espinosa, G., Aguiló, S., Bucciarelli, S., Ramos‐Casals, M., Ingelmo, M., Asherson, R. A., & Font, J. (2006) · Seminars in Arthritis and Rheumatism · doi:10.1016/j.semarthrit.2005.07.003 · Cited by 138
Gibbs, M., English, J. C., & Zirwas, M. (2005) · Journal of the American Academy of Dermatology · doi:10.1016/j.jaad.2004.11.051 · Cited by 138
Multiple sclerosis, neuropsychiatric lupus and antiphospholipid syndrome: where do we stand?
Ferreira, S. (2005) · British journal of rheumatology · doi:10.1093/rheumatology/keh532 · Cited by 137
“In the Euro-Phospholipid Project cohort of 1000 European APS patients (primary and secondary), myelopathy and optic neuropathy were rare manifestations (0.4 and 1%, respectively) [ 36 ].”
BackgroundInfluentialTreatment of catastrophic antiphospholipid syndrome
Kazzaz, N. M., McCune, W. J., & Knight, J. S. (2016) · Current Opinion in Rheumatology · doi:10.1097/bor.0000000000000269 · Cited by 134
Ioannou, Y., Pericleous, C., Giles, I., Latchman, D. S., Isenberg, D. A., & Rahman, A. (2006) · Arthritis & Rheumatism · doi:10.1002/art.22306 · Cited by 131
“The clinical features of patients in the APS group were representative of the features of patients in larger epidemiologic studies of APS (35).”
ResultHo, K. T., Ahn, C. W., Alarcón, G. S., Baethge, B. A., Tan, F. K., Roseman, J., Bastian, H. M., Fessler, B. J., McGwin, G., Vilá, L. M., et al. (2005) · Rheumatology · doi:10.1093/rheumatology/kei014 · Cited by 128
“Contrary to what we had hypothesized based on the published literature [2, 9, 39–41], an association between aPL antibodies (each one individually or all taken together) was not found in either the univariable or the multivariable analyses even when a second assay was performed in a selected number of patient samples…”
ResultCardiac Manifestations of Antiphospholipid Syndrome With Focus on Its Primary Form
Kolitz, T., Shiber, S., Sharabi, I., Winder, A., & Zandman‐Goddard, G. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00941 · Cited by 135
Cardiac pathology of systemic lupus erythematosus
Jain, D., & Halushka, M. K. (2009) · Journal of Clinical Pathology · doi:10.1136/jcp.2009.064311 · Cited by 127
Diagnosis and management of the antiphospholipid syndrome
Cohen, D. B., Berger, S. P., Steup‐Beekman, G. M., Bloemenkamp, K. W. M., & Bajema, I. M. (2010) · BMJ · doi:10.1136/bmj.c2541 · Cited by 127
“Antiphospholipid syndrome is a systemic autoimmune disorder characterised by arterial and venous thrombosis, adverse outcomes in pregnancy (for mother and fetus), and raised titres of antiphospholipid antibodies. It occurs in isolation (primary antiphospholipid syndrome) in more than 50% of patients, but it can be ass…”
BackgroundAlijotas‐Reig, J., Esteve‐Valverde, E., Anunciación-Llunell, A., Marques-Soares, J. R., Pardos‐Gea, J., & Miró‐Mur, F. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11030675 · Cited by 132
Chronic Inflammatory Placental Disorders Associated With Recurrent Adverse Pregnancy Outcome
Cornish, E. F., McDonnell, T. C. R., & Williams, D. J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.825075 · Cited by 118
The Hematologic Manifestations of the Antiphospholipid Syndrome
Uthman, I. W., Godeau, B., Taher, A. T., & Khamashta, M. A. (2008) · Blood Reviews · doi:10.1016/j.blre.2008.03.005 · Cited by 118
Antiphospholipid syndrome and recurrent thrombosis in children
Berkun, Y., Padeh, S., Barash, J., Uziel, Y., Harel, L., Mukamel, M., Revel‐Vilk, S., & Kenet, G. (2006) · Arthritis Care & Research · doi:10.1002/art.22360 · Cited by 118
Neurological manifestations of antiphospholipid syndrome
Rodrigues, C. E. M., de Carvalho, J. F., & Shoenfeld, Y. (2010) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2010.02263.x · Cited by 116
The antiphospholipid syndrome: from pathophysiology to treatment
Negrini, S. M., Pappalardo, F., Murdaca, G., Indiveri, F., & Puppo, F. (2016) · Clinical and Experimental Medicine · doi:10.1007/s10238-016-0430-5 · Cited by 117
“Venous thromboembolism is the most frequent manifestation in APS patients, and differently from thrombosis in congenital thrombophilias, all segments of the vascular bed (both venous and arterial) can be involved in any combination of occlusive events [2].”
BackgroundInfluentialAntiphospholipid Syndrome during pregnancy: the state of the art.
Prima, F. A. F. D., Valenti, O., Hyseni, E., Giorgio, E., Faraci, M., Renda, E., Domenico, R. D., & Monte, S. (2011) · PubMed Central · Cited by 111
Management of antiphospholipid syndrome
Uthman, I. W., Noureldine, M. H. A., Ruiz‐Irastorza, G., & Khamashta, M. A. (2018) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2018-213846 · Cited by 114
“In an attempt to assess the risk of developing the clinical manifestations related to vascular thrombosis and pregnancy morbidity in patients with APS, the first Risk Scale for the diagnosis of APS was proposed in 2011.”
InfluentialGómez-Puerta, J. A., Cervera, R., Espinosa, G., Asherson, R. A., García‐Carrasco, M., da Costa, I. P., ANDRADE, D. C. O. D., Borba, E. F., Makatsaria, A. D., Bucciarelli, S., et al. (2007) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2006.061671 · Cited by 112
“The antiphospholipid syndrome (APS) is a systemic autoimmune disorder characterised by a combination of arterial and/or venous thrombosis, pregnancy morbidity, usually accompanied by a mild-to-moderate thrombocytopenia, and raised titres of antiphospholipid antibodies (aPL)—namely, the lupus anticoagulant (LA) and/or…”
BackgroundEspinosa, G., Mendizábal, A., Mínguez, S., Ramo-Tello, C. M., Capellades, J., Olivé, A., & Cervera, R. (2008) · Seminars in Arthritis and Rheumatism · doi:10.1016/j.semarthrit.2008.09.002 · Cited by 112
Metadata
- Authors
- Cervera, R., Piette, J., Font, J., Khamashta, M. A., Shoenfeld, Y., Camps, M. T., Jacobsen, S., Lakos, G., Tincani, A., Kontopoulou‐Griva, I., Galeazzi, M., Meroni, P. L., Derksen, R. H. W. M., de Groot, P. G., Gromnica‐Ihle, E., Baleva, M., Mosca, M., Bombardieri, S., Houssiau, F., Gris, J., Quéré, I., Hachulla, E., Vasconcelos, C., Roch, B., Fernández‐Nebro, A., Boffa, M., Hughes, G. R. V., & Ingelmo, M.
- Affiliations
- Hospital Clínic de Barcelona (ES)
- St Thomas' Hospital (GB)
- Sheba Medical Center (IL)
- Hospital Regional Universitario de Málaga (ES)
- University of Debrecen (HU)
- Hippocration General Hospital (GR)
- Ospedale Santa Maria alle Scotte (IT)
- University of Milan (IT)
- University Medical Center Utrecht (NL)
- Immanuel Krankenhaus (DE)
- Medical University of Sofia (BG)
- University of Pisa (IT)
- Cliniques Universitaires Saint-Luc (BE)
- Centre Hospitalier Universitaire de Nîmes (FR)
- Hôpital Claude Huriez (FR)
- Hospital de Santo António (PT)
- University Hospital Carl Gustav Carus (DE)
- Pitié-Salpêtrière Hospital (FR)
- Corresponding author
- Cervera, Ricard
- ORCID
- Venue
- Arthritis & Rheumatism
- Publisher
- Wiley
- Published
- 2002-04
- Volume
- 46
- Issue
- 4
- Pages
- 1019-1027
- ISSN
- 0004-3591 (ISSN-L)
- 1529-0131
- OpenAlex
- W2042958596
- Cited by
- 2,156
- References
- 42
- Citations by year
- 2026: 60 · 2025: 82 · 2024: 110 · 2023: 93 · 2022: 106 · 2021: 130 · 2020: 92 · 2019: 110 · 2018: 99 · 2017: 95 · 2016: 84 · 2015: 94 · 2014: 96 · 2013: 82 · 2012: 85
- FWCI
- 43.59
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Arthritis & Rheumatism (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- University of Debrecen Electronic Archive (University of Debrecen) (submittedVersion, other-oa)
- Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion)
- Institutional Research Information System (Università degli Studi di Brescia) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Use Siena air (University of Siena) (submittedVersion)
- Funders
- Comissió Interdepartamental per a la Recerca i la Tecnologia of Catalonia, Spain ((FI/FIAP 1999/00684))
- Fondo de Investigaciones Sanitarias of Spain ((FIS 1999/280))
- IRCCS Istituto Auxologico Italiano of Italy (Ricerca Corrente 2000)
- Institut Electricité-Santé of France
- Topics
- Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
- Health Sciences › Medicine › Rheumatology › Vasculitis and related conditions
- Health Sciences › Medicine › Rheumatology › Systemic Sclerosis and Related Diseases
- Keywords
- antiphospholipid syndrome, systemic lupus erythematosus, thrombosis, catastrophic antiphospholipid syndrome, sex differences, age of onset, livedo reticularis, thrombocytopenia, leukopenia, stroke, myocardial infarction, arterial thrombosis, lupus-like syndrome, chorea, migraine, epilepsy, angina pectoris
- MeSH terms
- Adolescent, Adult, Aged, Aged, 80 and over, Autoantibodies, Child, Child, Preschool, Diagnosis, Differential, Female, Humans, Infant, Infant, Newborn, Male, Middle Aged, Cohort Studies, Prevalence, Antiphospholipid Syndrome, Age Distribution, Sex Distribution, Lupus Vasculitis, Central Nervous System
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