The DOI matches its Crossref record; 64 of the 66 references it cites were found in a registry or an index.
Lupus anticoagulants are stronger risk factors for thrombosis than anticardiolipin antibodies in the antiphospholipid syndrome: a systematic review of the literature
Abstract
To formally establish the risk of lupus anticoagulants and anticardiolipin antibodies for arterial and venous thrombosis, we ran a MEDLINE search of the literature from 1988 to 2000. Studies were selected for their case-control (11), prospective (9), cross-sectional (3), and ambispective (2) design. They provided or enabled us to calculate the odds ratio with 95% confidence interval (CI) of lupus anticoagulants and/or anticardiolipin antibodies for thrombosis in 4184 patients and 3151 controls. Studies were grouped according to the antibody investigated. Five studies compared lupus anticoagulants with anticardiolipin antibodies: the odds ratio with 95% CI of lupus anticoagulants for thrombosis was always significant. None of them found anticardiolipin antibodies were associated with thrombosis. Four studies analyzed only lupus anticoagulants: the odds ratio with 95% CI was always significant. The risk of lupus anticoagulants was independent of the site and type of thrombosis, the presence of systemic lupus erythematosus, and the coagulation tests employed to detect them. Sixteen studies served to assess 28 associations between anticardiolipin antibodies and thrombosis: the odds ratio with 95% CI was significant in 15 cases. Anticardiolipin titer correlated with the odds ratio of thrombosis. In conclusion, the detection of lupus anticoagulants and, possibly, of immunoglobulin G (IgG) anticardiolipin antibodies at medium or high titers helps to identify patients at risk for thrombosis. However, to take full advantage of the conclusions provided by the available evidence, there is an urgent need to harmonize investigational methods.
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In the citing paper
“These results confirm and validate several previous reports that have implicated these antibodies in the pathogenesis of APS [9, 10, 12, 13, 29, 30], but they also add to the growing body of evidence that shows inconsistent associations between aPL-associated autoantibodies and anamnestic thrombotic risk [3, 16].”
From Cardiovascular risk factors are major determinants of thrombotic risk in patients with the lupus anticoagulant (2017) · cites this paper as [29]
In the citing paper
“It is now clear that LA positivity is associated with TEs.22”
From Incidence of a first thromboembolic event in asymptomatic carriers of high-risk antiphospholipid antibody profile: a multicenter prospective study (2011) · cites this paper as [22]
In the citing paper
“It is well known that LA positivity is more strongly associated with both arterial and venous thrombosis than either aCL or anti-β2-glycoprotein I antibodies [8, 9].”
From Antiphospholipid patterns predict risk of thrombosis in systemic lupus erythematosus (2021) · cites this paper as [9]
In the citing paper
“Large studies found that IgM aCL and IgM anti-β2-glycoprotein I are not associated with thrombotic events [9–13].”
From Antiphospholipid patterns predict risk of thrombosis in systemic lupus erythematosus (2021) · cites this paper as [9]
In the citing paper
“Similarly, in a systematic review, aCL IgM was not predictive for thrombosis [9].”
From Antiphospholipid patterns predict risk of thrombosis in systemic lupus erythematosus (2021) · cites this paper as [9]
In the citing paper
“In most studies, it has been shown that in SLE, LA is the main predictor of thrombosis [9, 27–29].”
From Antiphospholipid patterns predict risk of thrombosis in systemic lupus erythematosus (2021) · cites this paper as [9]
In the citing paper
“Patients with persistent aPL with or without APS are at increased risk of future thrombotic events, LA positivity having the strongest association with these events.3”
From Lupus anticoagulant test persistence over time and its associations with future thrombotic events (2022) · cites this paper as [3]
In the citing paper
“Patients with persistent aPL with or without APS are at increased risk of future thrombotic events, LA positivity having the strongest association with these events.3”
From Lupus anticoagulant test persistence over time and its associations with future thrombotic events (2022) · cites this paper as [3]
In the citing paper
“Additional antibodies, most notably anticardiolipin antibodies (aCL) and anti–glycoprotein-I antibodies (aβ2GPI), were later identified and associated with thrombosis and recurrent spontaneous abortions.2-4”
From Lupus anticoagulant test persistence over time and its associations with future thrombotic events (2022) · cites this paper as [3]
In the citing paper
“Notably, most prior efforts to risk-stratify patients for future thrombotic events have used the patients’ aPL status from the first measurement or early in the observation period and have not analyzed changes over time.3,7,8”
From Lupus anticoagulant test persistence over time and its associations with future thrombotic events (2022) · cites this paper as [3]
In the citing paper
“This contention is supported by meta-analyses showing that the presence of aCL and ab2GPI alone are poorly associated with thromboembolic events [6,7].”
From Clinical course of high‐risk patients diagnosed with antiphospholipid syndrome (2010) · cites this paper as [6]
In the citing paper
“Although a positive LAC is considered to be a strong risk factor for thrombosis in APS, 10,11”
From Clinical Relevance of Isolated Lupus Anticoagulant Positivity in Patients with Thrombotic Antiphospholipid Syndrome (2021) · cites this paper as [10]
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“The LA test correlates better with clinical events than do aCL and anti-β2GPI tests.(20)†”
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“Furthermore, a recent systematic review has questioned the association between isolated aCL and thrombosis.(7) We systematically reviewed laboratory testing, diagnostic criteria, and treatment of thrombosis in patients with antiphospholipid antibodies.”
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“Positive LA has been demonstrated to be the aPL test most strongly related to thrombosis [33,34], while isolated ab2-GPI areweakly associatedwith vascularmanifestations [15,33].”
BackgroundHow we diagnose the antiphospholipid syndrome
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“N40 GPL units) resulted significantly associated with arterial thrombosis (first cerebral stroke or MI) [9].”
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“[37], in an attempt to reduce the possible over-diagnosis of the syndrome, argued in favour of maintaining antiβ2GPI and also suggested that aCL should be dropped from the diagnostic laboratory panel owing to the lack of association with clinical APS-related disorders.”
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ResultTincani, A., Allegri, F., Balestrieri, G., Reber, G., Sanmarco, M., Meroni, P. L., & Boffa, M. (2004) · Thrombosis Research · doi:10.1016/j.thromres.2004.06.035 · Cited by 128
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“Although several clinical studies and systematic reviews suggested that LA is a stronger risk factor for the development of thrombosis (Galli et al, 2003; de Groot et al, 2005), other studies have shown that the presence of LA alone is not associated with thromboembolic events (Pengo et al, 2005;…”
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Antiphospholipid Syndrome during pregnancy: the state of the art.
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“This approach has been previously reported and validated [10, 11].”
MethodLupus Anticoagulant-Hypoprothrombinemia Syndrome
Mazodier, K., Arnaud, L., Mathian, A., Costedoat-Chalumeau, N., Haroche, J., Francès, C., Harlé, J., Pernod, G., Lespessailles, É., Gaudin, P., et al. (2012) · Medicine · doi:10.1097/md.0b013e31826b971f · Cited by 112
Antiphospholipid antibodies in COVID-19: a meta-analysis and systematic review
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Arnout, J., & Vermylen, J. (2003) · Journal of Thrombosis and Haemostasis · doi:10.1046/j.1538-7836.2003.00125.x · Cited by 107
Gris, J., Bouvier, S., Molinari, N., Galanaud, J. ‐., Cochery-Nouvellon, É., Mercier, É., Fabbro-Péray, P., Balducchi, J.-P., Marès, P., Quéré, I., et al. (2011) · Blood · doi:10.1182/blood-2011-09-381913 · Cited by 108
“Age, y 30 (5) [17-44] 29 (4) [18-44] 29 (4) [16-41] .”
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“The first was a meta-analysis including 18 studies in adult patients with SLE demonstrating that LA shows stronger association with TEs than ACLAs.1 A more recent systematic review included 25 studies in adult patients with or without SLE.10 The review confirmed LAs as a strong risk factor for TEs but did not find une…”
BackgroundInfluentialA protocol for determination of anticardiolipin antibodies by ELISA
Pierangeli, S. S., & Harris, E. N. (2008) · Nature Protocols · doi:10.1038/nprot.2008.48 · Cited by 106
“The main reason of such statement is based on the results of a large meta-analysis study showing that LA is a strong risk factor for thrombosis at variance of the aCL assa”
ResultLim, W. (2013) · Hematology · doi:10.1182/asheducation-2013.1.675 · Cited by 107
Landolfi, R., Cipriani, M. C., & Novarese, L. (2006) · Best Practice & Research Clinical Haematology · doi:10.1016/j.beha.2005.07.011 · Cited by 99
Antiphospholipid antibody testing and standardization
Devreese, K. M. J. (2014) · International Journal of Laboratory Hematology · doi:10.1111/ijlh.12234 · Cited by 98
“[63, 64], while for pregnancy morbidity the role of IgM should be further established [57, 58].”
BackgroundCerebral Manifestations in the Antiphospholipid (Hughes) Syndrome
Sanna, G., D’Cruz, D. P., & Cuadrado, M. J. (2006) · Rheumatic Disease Clinics of North America · doi:10.1016/j.rdc.2006.05.010 · Cited by 95
Diagnosis and management of non-criteria obstetric antiphospholipid syndrome
Machin, S. J., Mackie, I. J., Cohen, H., & Arachchillage, D. J. (2014) · Thrombosis and Haemostasis · doi:10.1160/th14-05-0416 · Cited by 97
“A meta-analysis of the association between aPL and recurrent fetal loss in women without autoimmune disease, reported that LA, which appears to have the strongest association with thrombosis (23), was associated with late recurrent pregnancy loss (odds ratio [OR] 7.”
BackgroundSurvey of lupus anticoagulant diagnosis by central evaluation of positive plasma samples
Pengo, V., Biasiolo, A., Gresele, P., Marongiu, F., Erba, N., Veschi, F., Ghirarduzzi, A., Candia, E. D., Montaruli, B., Testa, S., et al. (2007) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2007.02454.x · Cited by 95
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Mechanisms of Disease: antiphospholipid antibodies—from clinical association to pathologic mechanism
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“The consequence of the low specificity of the assays is the suboptimal treatment of patients”
BackgroundCatastrophic antiphospholipid syndrome: how to diagnose a rare but highly fatal disease
Aguiar, C. L., & Erkan, D. (2013) · Therapeutic Advances in Musculoskeletal Disease · doi:10.1177/1759720x13502919 · Cited by 91
“…diagnostic purposes [Miyakis et al. 2006]; (b) a positive LA test is a better predictor of aPLrelated thrombotic events compared with other aPL tests [Galli et al. 2003]; (c) whenever possible, LA test should be tested off anticoagulation as both false-negative and false-positive results can occur…”
ResultIncidence of a first thromboembolic event in carriers of isolated lupus anticoagulant
Pengo, V., Testa, S., Martinelli, I., Ghirarduzzi, A., Legnani, C., Gresele, P., Passamonti, S. M., Bison, E., Denas, G., Jose, S. P., et al. (2015) · Thrombosis Research · doi:10.1016/j.thromres.2014.10.013 · Cited by 89
Detection of lupus anticoagulant in the presence of rivaroxaban using Taipan snake venom time
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Chayoua, W., Kelchtermans, H., Gris, J., Moore, G. W., Musiał, J., Wahl, D., de Groot, P. G., de Laat, B., & Devreese, K. M. J. (2020) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.14633 · Cited by 89
Secondary immune thrombocytopenic purpura
Liebman, H. A., & Stasi, R. (2007) · Current Opinion in Hematology · doi:10.1097/moh.0b013e3282ab9904 · Cited by 85
How I treat the antiphospholipid syndrome
Giannakopoulos, B., & Krilis, S. A. (2009) · Blood · doi:10.1182/blood-2009-05-220756 · Cited by 83
Laboratory Investigation of Thrombophilia: The Good, the Bad, and the Ugly
Favaloro, E. J., McDonald, D., & Lippi, G. (2009) · Seminars in Thrombosis and Hemostasis · doi:10.1055/s-0029-1242723 · Cited by 84
The Aetiology of Deep Venous Thrombosis
Malone, P. C., & Agutter, P. S. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6650-4 · Cited by 88
When Direct Oral Anticoagulants Should Not Be Standard Treatment
Bejjani, A., Khairani, C. D., Assi, A. A., Piazza, G., Sadeghipour, P., Talasaz, A. H., Fanikos, J. R., Connors, J. M., Siegal, D. M., Barnes, G. D., et al. (2024) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2023.10.038 · Cited by 89
The aetiology of deep venous thrombosis
Malone, P. C. (2006) · QJM · doi:10.1093/qjmed/hcl070 · Cited by 83
Invitation to a debate on the serological criteria that define the antiphospholipid syndrome
GALLI, M., REBER, G., DE MOERLOOSE, P., & DE GROOT, P. G. (2008) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2008.02862.x · Cited by 85
Self-citationRintelen, C., Vormittag, R., Sailer, T., Lehr, S., Quehenberger, P., Rumpold, H., Male, C., & Pabinger, I. (2005) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2005.01394.x · Cited by 82
Pediatric Antiphospholipid Syndrome
Cimaz, R., & Descloux, É. (2006) · Rheumatic Disease Clinics of North America · doi:10.1016/j.rdc.2006.05.005 · Cited by 81
Svenungsson, E., Gustafsson, J., Leonard, D., Sandling, J. K., Gunnarsson, I., Nordmark, G., Jönsen, A., Bengtsson, A. A., Sturfelt, G. K., Rantapää‐Dahlqvist, S., et al. (2009) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2009.115535 · Cited by 82
Challenges in the Diagnosis of the Antiphospholipid Syndrome
Devreese, K. M. J., & Hoylaerts, M. (2010) · Clinical Chemistry · doi:10.1373/clinchem.2009.133678 · Cited by 82
Venous Thrombosis in the Antiphospholipid Syndrome
Farmer-Boatwright, M. K., & Roubey, R. A. S. (2009) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.182204 · Cited by 82
Laboratory Testing for Lupus Anticoagulants: A Review of Issues Affecting Results
Tripodi, A. (2007) · Clinical Chemistry · doi:10.1373/clinchem.2007.089524 · Cited by 81
Thrombophilia screening revisited: an issue of personalized medicine
Colucci, G., & Tsakiris, D. Α. (2020) · Journal of Thrombosis and Thrombolysis · doi:10.1007/s11239-020-02090-y · Cited by 85
Management of antiphospholipid syndrome
Tuthill, J. I., & Khamashta, M. A. (2009) · Journal of Autoimmunity · doi:10.1016/j.jaut.2009.05.002 · Cited by 78
Laboratory diagnosis of the antiphospholipid syndrome: a plethora of obstacles to overcome
Devreese, K., & Hoylaerts, M. F. (2009) · European Journal Of Haematology · doi:10.1111/j.1600-0609.2009.01243.x · Cited by 78
“Since LAC show the strongest correlation with thrombosis and pregnancy morbidity, LAC-detection seems to be the assay of choice to detect functional aPL antibodies (25, 26, 89).”
BackgroundInfluentialPhenotyping the haemostatic system by thrombography—potential for the estimation of thrombotic risk
Regnault, V., Hemker, H. C., Wahl, D. G., et al. (2004) · Thrombosis Research · doi:10.1016/j.thromres.2004.06.017 · Cited by 78
Metadata
- Authors
- Galli, M., Luciani, D., Bertolini, G., & Barbui, T.
- Affiliations
- From the Division of Hematology, Ospedali Riuniti, Bergamo, Italy; and Laboratory of Clinical Epidemiology, Mario Negri Institute, Ranica (Bergamo), Italy.
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2003-03-01
- Volume
- 101
- Issue
- 5
- Pages
- 1827-1832
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- OpenAlex
- W2044043417
- Cited by
- 972
- References
- 66
- Citations by year
- 2026: 23 · 2025: 22 · 2024: 32 · 2023: 28 · 2022: 34 · 2021: 40 · 2020: 37 · 2019: 39 · 2018: 30 · 2017: 41 · 2016: 57 · 2015: 36 · 2014: 40 · 2013: 41 · 2012: 50
- FWCI
- 8.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Blood (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
- Health Sciences › Medicine › Hematology › Blood Coagulation and Thrombosis Mechanisms
- Health Sciences › Medicine › Hematology › Heparin-Induced Thrombocytopenia and Thrombosis
- Keywords
- lupus anticoagulant, anticardiolipin antibodies, antiphospholipid syndrome, thrombosis, arterial thrombosis, venous thrombosis, thrombosis risk factors, systemic lupus erythematosus, antibody titers
- MeSH terms
- Arterial Occlusive Diseases, Autoantigens, Autoimmune Diseases, Cross-Sectional Studies, Glycoproteins, Humans, Myocardial Infarction, Prospective Studies, Prothrombin, Research Design, Risk Factors, Thrombosis, Confidence Intervals, Odds Ratio, Case-Control Studies, Lupus Coagulation Inhibitor, Antiphospholipid Syndrome, Antibodies, Anticardiolipin, Thrombophilia, Venous Thrombosis, Stroke, beta 2-Glycoprotein I
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