Preeclampsia and the Antiphospholipid Syndrome
Abstract
:1. Introduction
2. Discussion
2.1. Association of APS and Preeclampsia
2.1.1. Pathophysiology of APS and Preeclampsia
2.1.2. Prevalance of aPLs in Women with Preeclampsia
2.2. Clinical Phenotypes of OAPS
Spontaneous Preterm Delivery
2.3. Other Forms of OAPS
2.4. Sequela of Preeclampsia, i.e., Prematurity
2.5. Management of “Classic APS”
2.6. Management of Refractory APS
Hydroxychloroquin
2.7. Supplementation as a Potential Additional Treatment
2.7.1. Vitamin D
2.7.2. Curcumin
3. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Miyakis, S.; Lockshin, M.D.; Atsumi, T.; Branch, D.W.; Brey, R.L.; Cervera, R.; Derksen, R.H.; De Groot, P.G.; Koike, T.; Meroni, P.L.; et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J. Thromb. Haemost. 2006, 4, 295–306. [Google Scholar] [CrossRef] [PubMed]
- ACOG Practice Bulletin No. 118: Antiphospholipid syndrome. Obstet. Gynecol. 2011, 117, 192–199. [CrossRef] [PubMed]
- Alijotas-Reig, J.; Esteve-Valverde, E.; Anunciación-Llunell, A.; Marques-Soares, J.; Pardos-Gea, J.; Miró-Mur, F. Pathogenesis, Diagnosis and Management of Obstetric Antiphospholipid Syndrome: A Comprehensive Review. J. Clin. Med. 2022, 11, 675. [Google Scholar] [CrossRef] [PubMed]
- Alijotas-Reig, J.; Esteve-Valverde, E.; Ferrer-Oliveras, R.; Sáez-Comet, L.; Lefkou, E.; Mekinian, A.; Belizna, C.; Ruffatti, A.; Hoxha, A.; Tincani, A.; et al. Comparative study of obstetric antiphospholipid syndrome (OAPS) and non-criteria obstetric APS (NC-OAPS): Report of 1640 cases from the EUROAPS registry. Rheumatology 2020, 59, 1306–1314. [Google Scholar] [CrossRef]
- Alijotas-Reig, J.; Esteve-Valverde, E.; Ferrer-Oliveras, R.; Sáez-Comet, L.; Lefkou, E.; Mekinian, A.; Belizna, C.; Ruffatti, A.; Tincani, A.; Marozio, L.; et al. The European Registry on Obstetric Antiphospholipid Syndrome (EUROAPS): A survey of 1000 consecutive cases. Autoimmun. Rev. 2019, 18, 406–414. [Google Scholar] [CrossRef]
- Andreoli, L.; Chighizola, C.B.; Banzato, A.; Pons-Estel, G.J.; Ramire de Jesus, G.; Erkan, D. Estimated frequency of antiphospholipid antibodies in patients with pregnancy morbidity, stroke, myocardial infarction, and deep vein thrombosis: A critical review of the literature. Arthritis Care Res. 2013, 65, 1869–1873. [Google Scholar] [CrossRef]
- Page, J.M.; Christiansen-Lindquist, L.; Thorsten, V.; Parker, C.B.; Reddy, U.M.; Dudley, D.J.; Saade, G.R.; Coustan, D.; Rowland Hogue, C.J.; Conway, D.; et al. Diagnostic Tests for Evaluation of Stillbirth: Results From the Stillbirth Collaborative Research Network. Obstet. Gynecol. 2017, 129, 699–706. [Google Scholar] [CrossRef]
- Helgadottir, L.B.; Skjeldestad, F.E.; Jacobsen, A.F.; Sandset, P.M.; Jacobsen, E.M. The association of antiphospholipid antibodies with intrauterine fetal death: A case-control study. Thromb. Res. 2012, 130, 32–37. [Google Scholar] [CrossRef]
- Silver, R.M.; Parker, C.B.; Reddy, U.M.; Goldenberg, R.; Coustan, D.; Dudley, D.J.; Saade, G.R.; Stoll, B.; Koch, M.A.; Conway, D.; et al. Antiphospholipid antibodies in stillbirth. Obstet. Gynecol. 2013, 122, 641–657. [Google Scholar] [CrossRef]
- Lees, C.C.; Stampalija, T.; Baschat, A.; da Silva Costa, F.; Ferrazzi, E.; Figueras, F.; Hecher, K.; Kingdom, J.; Poon, L.C.; Salomon, L.J.; et al. ISUOG Practice Guidelines: Diagnosis and management of small-for-gestational-age fetus and fetal growth restriction. Ultrasound Obstet. Gynecol. 2020, 56, 298–312. [Google Scholar] [CrossRef]
- Miller, S.L.; Huppi, P.S.; Mallard, C. The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome. J. Physiol. 2016, 594, 807–823. [Google Scholar] [CrossRef] [PubMed]
- Francis, J.H.; Permezel, M.; Davey, M.A. Perinatal mortality by birthweight centile. Aust. N. Z. J. Obstet. Gynaecol. 2014, 54, 354–359. [Google Scholar] [CrossRef] [PubMed]
- ACOG Practice Bulletin No. 202: Gestational Hypertension and Preeclampsia. Obstet. Gynecol. 2019, 133, 1. [CrossRef]
- von Dadelszen, P.; Magee, L.A.; Roberts, J.M. Subclassification of preeclampsia. Hypertens. Pregnancy 2003, 22, 143–148. [Google Scholar] [CrossRef] [PubMed]
- American College of Obstetricians and Gynecologists’ Committee on Practice Bulletins—Obstetrics. Practice Bulletin No. 171: Management of Preterm Labor. Obstet. Gynecol. 2016, 128, e155–e164. [Google Scholar] [CrossRef]
- Clark, E.A.; Silver, R.M.; Branch, D.W. Do antiphospholipid antibodies cause preeclampsia and HELLP syndrome? Curr. Rheumatol. Rep. 2007, 9, 219–225. [Google Scholar] [CrossRef]
- Mayer-Pickel, K.; Stern, C.; Cervar-Zivkovic, M.; Schöll, W.; Moertl, M. Preeclampsia before fetal viability in women with primary antiphospholipid syndrome- materno-fetal outcomes in a series of 7 cases. J. Reprod. Immunol. 2020, 138, 103101. [Google Scholar] [CrossRef]
- Appenzeller, S.; Souza, F.H.; Wagner Silva de Souza, A.; Shoenfeld, Y.; de Carvalho, J.F. HELLP syndrome and its relationship with antiphospholipid syndrome and antiphospholipid antibodies. Semin. Arthritis Rheum. 2011, 41, 517–523. [Google Scholar] [CrossRef]
- Le Thi Thuong, D.; Tieulie, N.; Costedoat, N.; Andreu, M.R.; Wechsler, B.; Vauthier-Brouzes, D.; Aumaitre, O.; Piette, J.C. The HELLP syndrome in the antiphospholipid syndrome: Retrospective study of 16 cases in 15 women. Ann. Rheum. Dis. 2005, 64, 273–278. [Google Scholar] [CrossRef]
- Alsulyman, O.M.; Castro, M.A.; Zuckerman, E.; McGehee, W.; Goodwin, T.M. Preeclampsia and liver infarction in early pregnancy associated with the antiphospholipid syndrome. Obstet. Gynecol. 1996, 88, 644–646. [Google Scholar] [CrossRef]
- Branch, D.W.; Andres, R.; Digre, K.B.; Rote, N.S.; Scott, J.R. The association of antiphospholipid antibodies with severe preeclampsia. Obstet. Gynecol. 1989, 73, 541–545. [Google Scholar] [PubMed]
- Lassere, M.; Empson, M. Treatment of antiphospholipid syndrome in pregnancy--a systematic review of randomized therapeutic trials. Thromb. Res. 2004, 114, 419–426. [Google Scholar] [CrossRef] [PubMed]
- Bouvier, S.; Cochery-Nouvellon, E.; Lavigne-Lissalde, G.; Mercier, E.; Marchetti, T.; Balducchi, J.P.; Mares, P.; Gris, J.C. Comparative incidence of pregnancy outcomes in treated obstetric antiphospholipid syndrome: The NOH-APS observational study. Blood 2014, 123, 404–413. [Google Scholar] [CrossRef]
- Ruffatti, A.; Tonello, M.; Favaro, M.; Del Ross, T.; Calligaro, A.; Ruffatti, A.T.; Gervasi, M.T.; Hoxha, A. The efficacy and safety of second-line treatments of refractory and/or high risk pregnant antiphospholipid syndrome patients. A systematic literature review analyzing 313 pregnancies. Semin. Arthritis Rheum. 2021, 51, 28–35. [Google Scholar] [CrossRef]
- Ruffatti, A.; Tonello, M.; Hoxha, A.; Sciascia, S.; Cuadrado, M.J.; Latino, J.O.; Udry, S.; Reshetnyak, T.; Costedoat-Chalumeau, N.; Morel, N.; et al. Effect of Additional Treatments Combined with Conventional Therapies in Pregnant Patients with High-Risk Antiphospholipid Syndrome: A Multicentre Study. Thromb. Haemost. 2018, 118, 639–646. [Google Scholar] [CrossRef] [PubMed]
- Radin, M.; Cecchi, I.; Rubini, E.; Foddai, S.G.; Barinotti, A.; Menegatti, E.; Roccatello, D.; Sciascia, S. Treatment of antiphospholipid syndrome. Clin. Immunol. 2020, 221, 108597. [Google Scholar] [CrossRef]
- Alijotas-Reig, J.; Esteve-Valverde, E.; Llurba, E.; Gris, J.M. Treatment of refractory poor aPL-related obstetric outcomes with TNF-alpha blockers: Maternal-fetal outcomes in a series of 18 cases. Semin. Arthritis Rheum. 2019, 49, 314–318. [Google Scholar] [CrossRef]
- Andreoli, L.; Piantoni, S.; Dall’Ara, F.; Allegri, F.; Meroni, P.L.; Tincani, A. Vitamin D and antiphospholipid syndrome. Lupus 2012, 21, 736–740. [Google Scholar] [CrossRef]
- Cohen, H.; Cuadrado, M.J.; Erkan, D.; Duarte-Garcia, A.; Isenberg, D.A.; Knight, J.S.; Ortel, T.L.; Rahman, A.; Salmon, J.E.; Tektonidou, M.G.; et al. 16th International Congress on Antiphospholipid Antibodies Task Force Report on Antiphospholipid Syndrome Treatment Trends. Lupus 2020, 29, 1571–1593. [Google Scholar] [CrossRef]
- Cyprian, F.; Lefkou, E.; Varoudi, K.; Girardi, G. Immunomodulatory Effects of Vitamin D in Pregnancy and Beyond. Front. Immunol. 2019, 10, 2739. [Google Scholar] [CrossRef]
- De Carolis, S.; Tabacco, S.; Rizzo, F.; Giannini, A.; Botta, A.; Salvi, S.; Garufi, C.; Benedetti Panici, P.; Lanzone, A. Antiphospholipid syndrome: An update on risk factors for pregnancy outcome. Autoimmun. Rev. 2018, 17, 956–966. [Google Scholar] [CrossRef] [PubMed]
- García-Carrasco, M.; Jiménez-Herrera, E.A.; Gálvez-Romero, J.L.; Mendoza-Pinto, C.; Méndez-Martínez, S.; Etchegaray-Morales, I.; Munguía-Realpozo, P.; Vázquez de Lara-Cisneros, L.; Santa Cruz, F.J.; Cervera, R. The anti-thrombotic effects of vitamin D and their possible relationship with antiphospholipid syndrome. Lupus 2018, 27, 2181–2189. [Google Scholar] [CrossRef] [PubMed]
- Tranquilli, A.L.; Dekker, G.; Magee, L.; Roberts, J.; Sibai, B.M.; Steyn, W.; Zeeman, G.G.; Brown, M.A. The classification, diagnosis and management of the hypertensive disorders of pregnancy: A revised statement from the ISSHP. Pregnancy Hypertens. 2014, 4, 97–104. [Google Scholar] [CrossRef]
- Roberts, J.M.; Hubel, C.A. The two stage model of preeclampsia: Variations on the theme. Placenta 2009, 30 (Suppl. A), S32–S37. [Google Scholar] [CrossRef] [PubMed]
- Ness, R.B.; Roberts, J.M. Heterogeneous causes constituting the single syndrome of preeclampsia: A hypothesis and its implications. Am. J. Obstet. Gynecol. 1996, 175, 1365–1370. [Google Scholar] [CrossRef]
- Lisonkova, S.; Joseph, K.S. Incidence of preeclampsia: Risk factors and outcomes associated with early- versus late-onset disease. Am. J. Obstet. Gynecol. 2013, 209, e541–e544. [Google Scholar] [CrossRef]
- Firkin, B.G.; Howard, M.A.; Radford, N. Possible relationship between lupus inhibitor and recurrent abortion in young women. Lancet 1980, 2, 366. [Google Scholar] [CrossRef]
- Hughes, G.R. Thrombosis, abortion, cerebral disease, and the lupus anticoagulant. Br. Med. J. (Clin. Res. Ed.) 1983, 287, 1088–1089. [Google Scholar] [CrossRef]
- Branch, D.W.; Scott, J.R.; Kochenour, N.K.; Hershgold, E. Obstetric complications associated with the lupus anticoagulant. N. Engl. J. Med. 1985, 313, 1322–1326. [Google Scholar] [CrossRef]
- Lockshin, M.D.; Druzin, M.L.; Goei, S.; Qamar, T.; Magid, M.S.; Jovanovic, L.; Ferenc, M. Antibody to cardiolipin as a predictor of fetal distress or death in pregnant patients with systemic lupus erythematosus. N. Engl. J. Med. 1985, 313, 152–156. [Google Scholar] [CrossRef]
- Branch, D.W.; Silver, R.M.; Blackwell, J.L.; Reading, J.C.; Scott, J.R. Outcome of treated pregnancies in women with antiphospholipid syndrome: An update of the Utah experience. Obstet. Gynecol. 1992, 80, 614–620. [Google Scholar] [PubMed]
- Caruso, A.; De Carolis, S.; Ferrazzani, S.; Valesini, G.; Caforio, L.; Mancuso, S. Pregnancy outcome in relation to uterine artery flow velocity waveforms and clinical characteristics in women with antiphospholipid syndrome. Obstet. Gynecol. 1993, 82, 970–977. [Google Scholar] [CrossRef] [PubMed]
- Lima, F.; Khamashta, M.A.; Buchanan, N.M.; Kerslake, S.; Hunt, B.J.; Hughes, G.R. A study of sixty pregnancies in patients with the antiphospholipid syndrome. Clin. Exp. Rheumatol. 1996, 14, 131–136. [Google Scholar] [PubMed]
- Willis, R.; Harris, E.N.; Pierangeli, S.S. Pathogenesis of the antiphospholipid syndrome. Semin. Thromb. Hemost. 2012, 38, 305–321. [Google Scholar] [CrossRef] [PubMed]
- Meroni, P.L.; Raschi, E.; Grossi, C.; Pregnolato, F.; Trespidi, L.; Acaia, B.; Borghi, M.O. Obstetric and vascular APS: Same autoantibodies but different diseases? Lupus 2012, 21, 708–710. [Google Scholar] [CrossRef] [PubMed]
- D’Ippolito, S.; Di Simone, N.; Di Nicuolo, F.; Castellani, R.; Caruso, A. Antiphospholipid antibodies: Effects on trophoblast and endothelial cells. Am. J. Reprod. Immunol. 2007, 58, 150–158. [Google Scholar] [CrossRef]
- Di Simone, N.; Luigi, M.P.; Marco, D.; Fiorella, D.N.; Silvia, D.; Clara, D.M.; Alessandro, C. Pregnancies complicated with antiphospholipid syndrome: The pathogenic mechanism of antiphospholipid antibodies: A review of the literature. Ann. N. Y. Acad. Sci. 2007, 1108, 505–514. [Google Scholar] [CrossRef]
- Young, B.C.; Levine, R.J.; Karumanchi, S.A. Pathogenesis of preeclampsia. Annu. Rev. Pathol. 2010, 5, 173–192. [Google Scholar] [CrossRef]
- Burton, G.J.; Redman, C.W.; Roberts, J.M.; Moffett, A. Pre-eclampsia: Pathophysiology and clinical implications. BMJ 2019, 366, l2381. [Google Scholar] [CrossRef]
- Redman, C.W.; Sargent, I.L. Placental stress and pre-eclampsia: A revised view. Placenta 2009, 30 (Suppl. A), S38–S42. [Google Scholar] [CrossRef]
- Redman, C.W.; Staff, A.C. Preeclampsia, biomarkers, syncytiotrophoblast stress, and placental capacity. Am. J. Obstet. Gynecol. 2015, 213 (Suppl. S4), S9.e1–S9.e4. [Google Scholar] [CrossRef] [PubMed]
- Roberts, J.M.; Redman, C.W. Pre-eclampsia: More than pregnancy-induced hypertension. Lancet 1993, 341, 1447–1451. [Google Scholar] [CrossRef] [PubMed]
- McNally, R.; Alqudah, A.; Obradovic, D.; McClements, L. Elucidating the Pathogenesis of Pre-eclampsia Using In Vitro Models of Spiral Uterine Artery Remodelling. Curr. Hypertens. Rep. 2017, 19, 93. [Google Scholar] [CrossRef] [PubMed]
- Redman, C.W.; Sargent, I.L.; Staff, A.C. IFPA Senior Award Lecture: Making sense of pre-eclampsia—Two placental causes of preeclampsia? Placenta 2014, 35, S20–S25. [Google Scholar] [CrossRef]
- Tannetta, D.; Masliukaite, I.; Vatish, M.; Redman, C.; Sargent, I. Update of syncytiotrophoblast derived extracellular vesicles in normal pregnancy and preeclampsia. J. Reprod. Immunol. 2017, 119, 98–106. [Google Scholar] [CrossRef]
- Brosens, I.; Pijnenborg, R.; Vercruysse, L.; Romero, R. The “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am. J. Obstet. Gynecol. 2011, 204, 193–201. [Google Scholar] [CrossRef]
- Robillard, P.Y.; Dekker, G.; Scioscia, M.; Saito, S. Progress in the understanding of the pathophysiology of immunologic maladaptation related to early-onset preeclampsia and metabolic syndrome related to late-onset preeclampsia. Am. J. Obstet. Gynecol. 2022, 226, S867–S875. [Google Scholar] [CrossRef]
- McLaughlin, K.; Zhang, J.; Lye, S.J.; Parker, J.D.; Kingdom, J.C. Phenotypes of Pregnant Women Who Subsequently Develop Hypertension in Pregnancy. J. Am. Heart Assoc. 2018, 7, e009595. [Google Scholar] [CrossRef]
- Pauzner, R.; Dulitzki, M.; Langevitz, P.; Livneh, A.; Kenett, R.; Many, A. Low molecular weight heparin and warfarin in the treatment of patients with antiphospholipid syndrome during pregnancy. Thromb. Haemost. 2001, 86, 1379–1384. [Google Scholar]
- Huong, D.L.; Wechsler, B.; Bletry, O.; Vauthier-Brouzes, D.; Lefebvre, G.; Piette, J.C. A study of 75 pregnancies in patients with antiphospholipid syndrome. J. Rheumatol. 2001, 28, 2025–2030. [Google Scholar]
- Alijotas-Reig, J.; Ferrer-Oliveras, R.; Ruffatti, A.; Tincani, A.; Lefkou, E.; Bertero, M.T.; Coloma-Bazan, E.; de Carolis, S.; Espinosa, G.; Rovere-Querini, P.; et al. The European Registry on Obstetric Antiphospholipid Syndrome (EUROAPS): A survey of 247 consecutive cases. Autoimmun. Rev. 2015, 14, 387–395. [Google Scholar] [CrossRef] [PubMed]
- Cervera, R.; Piette, J.C.; Font, J.; Khamashta, M.A.; Shoenfeld, Y.; Camps, M.T.; Jacobsen, S.; Lakos, G.; Tincani, A.; Kontopoulou-Griva, I.; et al. Antiphospholipid syndrome: Clinical and immunologic manifestations and patterns of disease expression in a cohort of 1000 patients. Arthritis Rheum. 2002, 46, 1019–1027. [Google Scholar] [CrossRef] [PubMed]
- Cervera, R. Antiphospholipid syndrome. Thromb. Res. 2017, 151 (Suppl. S1), S43–S47. [Google Scholar] [CrossRef] [PubMed]
- Duckitt, K.; Harrington, D. Risk factors for pre-eclampsia at antenatal booking: Systematic review of controlled studies. BMJ 2005, 330, 565. [Google Scholar] [CrossRef]
- Katano, K.; Aoki, A.; Sasa, H.; Ogasawara, M.; Matsuura, E.; Yagami, Y. beta 2-Glycoprotein I-dependent anticardiolipin antibodies as a predictor of adverse pregnancy outcomes in healthy pregnant women. Hum. Reprod. 1996, 11, 509–512. [Google Scholar] [CrossRef]
- Nodler, J.; Moolamalla, S.R.; Ledger, E.M.; Nuwayhid, B.S.; Mulla, Z.D. Elevated antiphospholipid antibody titers and adverse pregnancy outcomes: Analysis of a population-based hospital dataset. BMC Pregnancy Childbirth 2009, 9, 11. [Google Scholar] [CrossRef]
- van Pampus, M.G.; Dekker, G.A.; Wolf, H.; Huijgens, P.C.; Koopman, M.M.; von Blomberg, B.M.; Büller, H.R. High prevalence of hemostatic abnormalities in women with a history of severe preeclampsia. Am. J. Obstet. Gynecol. 1999, 180, 1146–1150. [Google Scholar] [CrossRef]
- Yamamoto, T.; Yoshimura, S.; Geshi, Y.; Sasamori, Y.; Okinaga, S.; Kobayashi, T.; Mori, H. Measurement of antiphospholipid antibody by ELISA using purified beta 2-glycoprotein I in preeclampsia. Clin. Exp. Immunol. 1993, 94, 196–200. [Google Scholar] [CrossRef]
- Yasuda, M.; Takakuwa, K.; Tokunaga, A.; Tanaka, K. Prospective studies of the association between anticardiolipin antibody and outcome of pregnancy. Obstet. Gynecol. 1995, 86, 555–559. [Google Scholar] [CrossRef]
- Heilmann, L.; Schorsch, M.; Hahn, T.; Fareed, J. Antiphospholipid syndrome and pre-eclampsia. Semin. Thromb. Hemost. 2011, 37, 141–145. [Google Scholar] [CrossRef]
- Marchetti, T.; de Moerloose, P.; Gris, J.C. Antiphospholipid antibodies and the risk of severe and non-severe pre-eclampsia: The NOHA case-control study. J. Thromb. Haemost. 2016, 14, 675–684. [Google Scholar] [CrossRef] [PubMed]
- Cervera, R.; Serrano, R.; Pons-Estel, G.J.; Ceberio-Hualde, L.; Shoenfeld, Y.; de Ramon, E.; Buonaiuto, V.; Jacobsen, S.; Zeher, M.M.; Tarr, T.; et al. Morbidity and mortality in the antiphospholipid syndrome during a 10-year period: A multicentre prospective study of 1000 patients. Ann. Rheum. Dis. 2015, 74, 1011–1018. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Liang, M. Risk factors for pregnancy morbidity in women with antiphospholipid syndrome. J. Reprod. Immunol. 2021, 145, 103315. [Google Scholar] [CrossRef] [PubMed]
- Deguchi, M.; Yamada, H.; Sugiura-Ogasawara, M.; Morikawa, M.; Fujita, D.; Miki, A.; Makino, S.; Murashima, A. Factors associated with adverse pregnancy outcomes in women with antiphospholipid syndrome: A multicenter study. J. Reprod. Immunol. 2017, 122, 21–27. [Google Scholar] [CrossRef] [PubMed]
- Ye, S.L.; Gu, X.K.; Tao, L.Y.; Cong, J.M.; Wang, Y.Q. Efficacy of Different Treatment Regimens for Antiphospholipid Syndrome-related Recurrent Spontaneous Abortion. Chin. Med. J. 2017, 130, 1395–1399. [Google Scholar] [CrossRef]
- Saccone, G.; Berghella, V.; Maruotti, G.M.; Ghi, T.; Rizzo, G.; Simonazzi, G.; Rizzo, N.; Facchinetti, F.; Dall’Asta, A.; Visentin, S.; et al. Antiphospholipid antibody profile based obstetric outcomes of primary antiphospholipid syndrome: The PREGNANTS study. Am. J. Obstet. Gynecol. 2017, 216, 525.e1–525.e12. [Google Scholar] [CrossRef]
- Cervera, R.; Khamashta, M.A.; Shoenfeld, Y.; Camps, M.T.; Jacobsen, S.; Kiss, E.; Zeher, M.M.; Tincani, A.; Kontopoulou-Griva, I.; Galeazzi, M.; et al. Morbidity and mortality in the antiphospholipid syndrome during a 5-year period: A multicentre prospective study of 1000 patients. Ann. Rheum. Dis. 2009, 68, 1428–1432. [Google Scholar] [CrossRef]
- Chaiworapongsa, T.; Romero, R.; Tarca, A.; Kusanovic, J.P.; Mittal, P.; Kim, S.K.; Gotsch, F.; Erez, O.; Vaisbuch, E.; Mazaki-Tovi, S.; et al. A subset of patients destined to develop spontaneous preterm labor has an abnormal angiogenic/anti-angiogenic profile in maternal plasma: Evidence in support of pathophysiologic heterogeneity of preterm labor derived from a longitudinal study. J. Matern. Fetal Neonatal Med. 2009, 22, 1122–1139. [Google Scholar] [CrossRef]
- Salomon, L.J.; Diaz-Garcia, C.; Bernard, J.P.; Ville, Y. Reference range for cervical length throughout pregnancy: Non-parametric LMS-based model applied to a large sample. Ultrasound Obstet. Gynecol. 2009, 33, 459–464. [Google Scholar] [CrossRef]
- Iams, J.D.; Goldenberg, R.L.; Meis, P.J.; Mercer, B.M.; Moawad, A.; Das, A.; Thom, E.; McNellis, D.; Copper, R.L.; Johnson, F.; et al. The length of the cervix and the risk of spontaneous premature delivery. National Institute of Child Health and Human Development Maternal Fetal Medicine Unit Network. N. Engl. J. Med. 1996, 334, 567–572. [Google Scholar] [CrossRef]
- Evaluating Progestogens for Preventing Preterm birth International Collaborative (EPPPIC): Meta-analysis of individual participant data from randomised controlled trials. Lancet 2021, 397, 1183–1194. [CrossRef] [PubMed]
- Dodd, J.M.; Grivell, R.M.; CM, O.B.; Dowswell, T.; Deussen, A.R. Prenatal administration of progestogens for preventing spontaneous preterm birth in women with a multiple pregnancy. Cochrane Database Syst. Rev. 2017, 10, Cd012024. [Google Scholar] [CrossRef] [PubMed]
- Crowther, C.A.; Ashwood, P.; McPhee, A.J.; Flenady, V.; Tran, T.; Dodd, J.M.; Robinson, J.S. Vaginal progesterone pessaries for pregnant women with a previous preterm birth to prevent neonatal respiratory distress syndrome (the PROGRESS Study): A multicentre, randomised, placebo-controlled trial. PLoS Med. 2017, 14, e1002390. [Google Scholar] [CrossRef]
- Meis, P.J.; Klebanoff, M.; Thom, E.; Dombrowski, M.P.; Sibai, B.; Moawad, A.H.; Spong, C.Y.; Hauth, J.C.; Miodovnik, M.; Varner, M.W.; et al. Prevention of recurrent preterm delivery by 17 alpha-hydroxyprogesterone caproate. N. Engl. J. Med. 2003, 348, 2379–2385. [Google Scholar] [CrossRef] [PubMed]
- Ashoush, S.; El-Kady, O.; Al-Hawwary, G.; Othman, A. The value of oral micronized progesterone in the prevention of recurrent spontaneous preterm birth: A randomized controlled trial. Acta Obstet. Gynecol. Scand. 2017, 96, 1460–1466. [Google Scholar] [CrossRef] [PubMed]
- Saling, E.; Schumacher, E. Total surgical cervical occlusion. Conclusions from data of several clinica, which use total surgical cervical occlusion. Z. Geburtshilfe Neonatol. 1996, 200, 82–87. [Google Scholar]
- Berghella, V.; Ciardulli, A.; Rust, O.A.; To, M.; Otsuki, K.; Althuisius, S.; Nicolaides, K.H.; Roman, A.; Saccone, G. Cerclage for sonographic short cervix in singleton gestations without prior spontaneous preterm birth: Systematic review and meta-analysis of randomized controlled trials using individual patient-level data. Ultrasound Obstet. Gynecol. 2017, 50, 569–577. [Google Scholar] [CrossRef]
- Berger, R.; Abele, H.; Bahlmann, F.; Doubek, K.; Felderhoff-Müser, U.; Fluhr, H.; Garnier, Y.; Grylka-Baeschlin, S.; Hayward, A.; Helmer, H.; et al. Prevention and Therapy of Preterm Birth. Guideline of the DGGG, OEGGG and SGGG (S2k Level, AWMF Registry Number 015/025, September 2022)—Part 2 with Recommendations on the Tertiary Prevention of Preterm Birth and on the Management of Preterm Premature Rupture of Membranes. Geburtshilfe Frauenheilkd 2023, 83, 569–601. [Google Scholar] [CrossRef]
- Berger, R.; Abele, H.; Bahlmann, F.; Doubek, K.; Felderhoff-Müser, U.; Fluhr, H.; Garnier, Y.; Grylka-Baeschlin, S.; Hayward, A.; Helmer, H.; et al. Prevention and Therapy of Preterm Birth. Guideline of the DGGG, OEGGG and SGGG (S2k-Level, AWMF Registry Number 015/025, September 2022)—Part 1 with Recommendations on the Epidemiology, Etiology, Prediction, Primary and Secondary Prevention of Preterm Birth. Geburtshilfe Frauenheilkd 2023, 83, 547–568. [Google Scholar] [CrossRef]
- Alijotas-Reig, J.; Esteve-Valverde, E.; Ferrer-Oliveras, R.; LLurba, E.; Ruffatti, A.; Tincani, A.; Lefkou, E.; Bertero, M.T.; Espinosa, G.; de Carolis, S.; et al. Comparative study between obstetric antiphospholipid syndrome and obstetric morbidity related with antiphospholipid antibodies. Med. Clin. 2018, 151, 215–222. [Google Scholar] [CrossRef]
- Conti, F.; Andreoli, L.; Crisafulli, F.; Mancuso, S.; Truglia, S.; Tektonidou, M.G. Does seronegative obstetric APS exist? “pro” and “cons”. Autoimmun. Rev. 2019, 18, 102407. [Google Scholar] [CrossRef] [PubMed]
- Zohoury, N.; Bertolaccini, M.L.; Rodriguez-Garcia, J.L.; Shums, Z.; Ateka-Barrutia, O.; Sorice, M.; Norman, G.L.; Khamashta, M. Closing the Serological Gap in the Antiphospholipid Syndrome: The Value of “Non-criteria” Antiphospholipid Antibodies. J. Rheumatol. 2017, 44, 1597–1602. [Google Scholar] [CrossRef] [PubMed]
- Arachchillage, D.R.; Machin, S.J.; Mackie, I.J.; Cohen, H. Diagnosis and management of non-criteria obstetric antiphospholipid syndrome. Thromb. Haemost. 2015, 113, 13–19. [Google Scholar] [CrossRef]
- Hughes, G.R.; Khamashta, M.A. Seronegative antiphospholipid syndrome. Ann. Rheum. Dis. 2003, 62, 1127. [Google Scholar] [CrossRef]
- Litvinova, E.; Darnige, L.; Kirilovsky, A.; Burnel, Y.; de Luna, G.; Dragon-Durey, M.A. Prevalence and Significance of Non-conventional Antiphospholipid Antibodies in Patients with Clinical APS Criteria. Front. Immunol. 2018, 9, 2971. [Google Scholar] [CrossRef] [PubMed]
- Pires da Rosa, G.; Ferreira, E.; Sousa-Pinto, B.; Rodríguez-Pintó, I.; Brito, I.; Mota, A.; Cervera, R.; Espinosa, G. Comparison of non-criteria antiphospholipid syndrome with definite antiphospholipid syndrome: A systematic review. Front. Immunol. 2022, 13, 967178. [Google Scholar] [CrossRef]
- Arabin, B.; Baschat, A.A. Pregnancy: An Underutilized Window of Opportunity to Improve Long-term Maternal and Infant Health-An Appeal for Continuous Family Care and Interdisciplinary Communication. Front. Pediatr. 2017, 5, 69. [Google Scholar] [CrossRef]
- Epstein, F.H. Late vascular effects of toxemia of pregnancy. N. Engl. J. Med. 1964, 271, 391–395. [Google Scholar] [CrossRef]
- Hermes, W.; Franx, A.; van Pampus, M.G.; Bloemenkamp, K.W.; Bots, M.L.; van der Post, J.A.; Porath, M.; Ponjee, G.A.; Tamsma, J.T.; Mol, B.W.; et al. Cardiovascular risk factors in women who had hypertensive disorders late in pregnancy: A cohort study. Am. J. Obstet. Gynecol. 2013, 208, 474.e1–474.e8. [Google Scholar] [CrossRef]
- Veerbeek, J.H.; Hermes, W.; Breimer, A.Y.; van Rijn, B.B.; Koenen, S.V.; Mol, B.W.; Franx, A.; de Groot, C.J.; Koster, M.P. Cardiovascular disease risk factors after early-onset preeclampsia, late-onset preeclampsia, and pregnancy-induced hypertension. Hypertension 2015, 65, 600–606. [Google Scholar] [CrossRef]
- Melchiorre, K.; Sutherland, G.R.; Baltabaeva, A.; Liberati, M.; Thilaganathan, B. Maternal cardiac dysfunction and remodeling in women with preeclampsia at term. Hypertension 2011, 57, 85–93. [Google Scholar] [CrossRef] [PubMed]
- Kristensen, J.H.; Basit, S.; Wohlfahrt, J.; Damholt, M.B.; Boyd, H.A. Pre-eclampsia and risk of later kidney disease: Nationwide cohort study. BMJ 2019, 365, l1516. [Google Scholar] [CrossRef] [PubMed]
- Prick, B.W.; Bijlenga, D.; Jansen, A.J.; Boers, K.E.; Scherjon, S.A.; Koopmans, C.M.; van Pampus, M.G.; Essink-Bot, M.L.; van Rhenen, D.J.; Mol, B.W.; et al. Determinants of health-related quality of life in the postpartum period after obstetric complications. Eur. J. Obstet. Gynecol. Reprod. Biol. 2015, 185, 88–95. [Google Scholar] [CrossRef] [PubMed]
- Blom, E.A.; Jansen, P.W.; Verhulst, F.C.; Hofman, A.; Raat, H.; Jaddoe, V.W.; Coolman, M.; Steegers, E.A.; Tiemeier, H. Perinatal complications increase the risk of postpartum depression. The Generation R Study. BJOG 2010, 117, 1390–1398. [Google Scholar] [CrossRef] [PubMed]
- Poel, Y.H.; Swinkels, P.; de Vries, J.I. Psychological treatment of women with psychological complaints after pre-eclampsia. J. Psychosom. Obstet. Gynaecol. 2009, 30, 65–72. [Google Scholar] [CrossRef]
- Jacobsson, B.; Ahlin, K.; Francis, A.; Hagberg, G.; Hagberg, H.; Gardosi, J. Cerebral palsy and restricted growth status at birth: Population-based case-control study. BJOG 2008, 115, 1250–1255. [Google Scholar] [CrossRef]
- Paz, I.; Gale, R.; Laor, A.; Danon, Y.L.; Stevenson, D.K.; Seidman, D.S. The cognitive outcome of full-term small for gestational age infants at late adolescence. Obstet. Gynecol. 1995, 85, 452–456. [Google Scholar] [CrossRef]
- Rich-Edwards, J.W.; Stampfer, M.J.; Manson, J.E.; Rosner, B.; Hankinson, S.E.; Colditz, G.A.; Willett, W.C.; Hennekens, C.H. Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ 1997, 315, 396–400. [Google Scholar] [CrossRef]
- Lithell, H.O.; McKeigue, P.M.; Berglund, L.; Mohsen, R.; Lithell, U.B.; Leon, D.A. Relation of size at birth to non-insulin dependent diabetes and insulin concentrations in men aged 50-60 years. BMJ 1996, 312, 406–410. [Google Scholar] [CrossRef]
- Law, C.M.; de Swiet, M.; Osmond, C.; Fayers, P.M.; Barker, D.J.; Cruddas, A.M.; Fall, C.H. Initiation of hypertension in utero and its amplification throughout life. BMJ 1993, 306, 24–27. [Google Scholar] [CrossRef]
- Paulson, K.R.; Kamath, A.M.; Alam, T.; Bienhoff, K.; Abady, G.G.; Abbas, J.; Abbasi-Kangevari, M.; Abbastabar, H.; Abd-Allah, F.; Abd-Elsalam,, S.M.; et al. Global, regional, and national progress towards Sustainable Development Goal 3.2 for neonatal and child health: All-cause and cause-specific mortality findings from the Global Burden of Disease Study 2019. Lancet 2021, 398, 870–905. [Google Scholar] [CrossRef] [PubMed]
- Goldenberg, R.L.; Culhane, J.F.; Iams, J.D.; Romero, R. Epidemiology and causes of preterm birth. Lancet 2008, 371, 75–84. [Google Scholar] [CrossRef] [PubMed]
- Saigal, S.; Doyle, L.W. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet 2008, 371, 261–269. [Google Scholar] [CrossRef]
- Esteve-Valverde, E.; Ferrer-Oliveras, R.; Alijotas-Reig, J. Obstetric antiphospholipid syndrome. Rev. Clin. Esp. 2016, 216, 135–145. [Google Scholar] [CrossRef] [PubMed]
- Alijotas-Reig, J. Treatment of refractory obstetric antiphospholipid syndrome: The state of the art and new trends in the therapeutic management. Lupus 2013, 22, 6–17. [Google Scholar] [CrossRef]
- Bramham, K.; Thomas, M.; Nelson-Piercy, C.; Khamashta, M.; Hunt, B.J. First-trimester low-dose prednisolone in refractory antiphospholipid antibody-related pregnancy loss. Blood 2011, 117, 6948–6951. [Google Scholar] [CrossRef] [PubMed]
- Sher, G.; Maassarani, G.; Zouves, C.; Feinman, M.; Sohn, S.; Matzner, W.; Chong, P.; Ching, W. The use of combined heparin/aspirin and immunoglobulin G therapy in the treatment of in vitro fertilization patients with antithyroid antibodies. Am. J. Reprod. Immunol. 1998, 39, 223–225. [Google Scholar] [CrossRef]
- Branch, D.W.; Peaceman, A.M.; Druzin, M.; Silver, R.K.; El-Sayed, Y.; Silver, R.M.; Esplin, M.S.; Spinnato, J.; Harger, J. A multicenter, placebo-controlled pilot study of intravenous immune globulin treatment of antiphospholipid syndrome during pregnancy. The Pregnancy Loss Study Group. Am. J. Obstet. Gynecol. 2000, 182 (Pt 1), 122–127. [Google Scholar] [CrossRef]
- Tenti, S.; Cheleschi, S.; Guidelli, G.M.; Galeazzi, M.; Fioravanti, A. Intravenous immunoglobulins and antiphospholipid syndrome: How, when and why? A review of the literature. Autoimmun. Rev. 2016, 15, 226–235. [Google Scholar] [CrossRef]
- Triolo, G.; Ferrante, A.; Ciccia, F.; Accardo-Palumbo, A.; Perino, A.; Castelli, A.; Giarratano, A.; Licata, G. Randomized study of subcutaneous low molecular weight heparin plus aspirin versus intravenous immunoglobulin in the treatment of recurrent fetal loss associated with antiphospholipid antibodies. Arthritis Rheum. 2003, 48, 728–731. [Google Scholar] [CrossRef]
- Tincani, A.; Scarsi, M.; Franceschini, F.; Cattaneo, R. Intravenous immunoglobulin in pregnancy: A chance for patients with an autoimmune disease. Isr. Med. Assoc. J. 2007, 9, 553–554. [Google Scholar] [PubMed]
- Christiansen, O.B.; Pedersen, B.; Rosgaard, A.; Husth, M. A randomized, double-blind, placebo-controlled trial of intravenous immunoglobulin in the prevention of recurrent miscarriage: Evidence for a therapeutic effect in women with secondary recurrent miscarriage. Hum. Reprod. 2002, 17, 809–816. [Google Scholar] [CrossRef] [PubMed]
- Dendrinos, S.; Sakkas, E.; Makrakis, E. Low-molecular-weight heparin versus intravenous immunoglobulin for recurrent abortion associated with antiphospholipid antibody syndrome. Int. J. Gynaecol. Obstet. 2009, 104, 223–225. [Google Scholar] [CrossRef]
- Urban, M.L.; Bettiol, A.; Serena, C.; Comito, C.; Turrini, I.; Fruttuoso, S.; Silvestri, E.; Vannacci, A.; Ravaldi, C.; Petraglia, F.; et al. Intravenous immunoglobulin for the secondary prevention of stillbirth in obstetric antiphospholipid syndrome: A case series and systematic review of literature. Autoimmun. Rev. 2020, 19, 102620. [Google Scholar] [CrossRef] [PubMed]
- Kaplan, Y.C.; Ozsarfati, J.; Nickel, C.; Koren, G. Reproductive outcomes following hydroxychloroquine use for autoimmune diseases: A systematic review and meta-analysis. Br. J. Clin. Pharmacol. 2016, 81, 835–848. [Google Scholar] [CrossRef]
- Mekinian, A.; Costedoat-Chalumeau, N.; Masseau, A.; Tincani, A.; De Caroli, S.; Alijotas-Reig, J.; Ruffatti, A.; Ambrozic, A.; Botta, A.; Le Guern, V.; et al. Obstetrical APS: Is there a place for hydroxychloroquine to improve the pregnancy outcome? Autoimmun. Rev. 2015, 14, 23–29. [Google Scholar] [CrossRef]
- Mekinian, A.; Cohen, J.; Alijotas-Reig, J.; Carbillon, L.; Nicaise-Roland, P.; Kayem, G.; Daraï, E.; Fain, O.; Bornes, M. Unexplained Recurrent Miscarriage and Recurrent Implantation Failure: Is There a Place for Immunomodulation? Am. J. Reprod. Immunol. 2016, 76, 8–28. [Google Scholar] [CrossRef]
- Sciascia, S.; Branch, D.W.; Levy, R.A.; Middeldorp, S.; Pavord, S.; Roccatello, D.; Ruiz-Irastorza, G.; Tincani, A.; Khamashta, M.; Schreiber, K.; et al. The efficacy of hydroxychloroquine in altering pregnancy outcome in women with antiphospholipid antibodies. Evidence and clinical judgment. Thromb. Haemost. 2016, 115, 285–290. [Google Scholar] [CrossRef]
- Mekinian, A.; Lazzaroni, M.G.; Kuzenko, A.; Alijotas-Reig, J.; Ruffatti, A.; Levy, P.; Canti, V.; Bremme, K.; Bezanahary, H.; Bertero, T.; et al. The efficacy of hydroxychloroquine for obstetrical outcome in anti-phospholipid syndrome: Data from a European multicenter retrospective study. Autoimmun. Rev. 2015, 14, 498–502. [Google Scholar] [CrossRef]
- Belizna, C.; Pregnolato, F.; Abad, S.; Alijotas-Reig, J.; Amital, H.; Amoura, Z.; Andreoli, L.; Andres, E.; Aouba, A.; Apras Bilgen, S.; et al. HIBISCUS: Hydroxychloroquine for the secondary prevention of thrombotic and obstetrical events in primary antiphospholipid syndrome. Autoimmun. Rev. 2018, 17, 1153–1168. [Google Scholar] [CrossRef]
- Mekinian, A.; Vicaut, E.; Cohen, J.; Bornes, M.; Kayem, G.; Fain, O. Hydroxychloroquine to obtain pregnancy without adverse obstetrical events in primary antiphospholipid syndrome: French phase II multicenter randomized trial, HYDROSAPL. Gynecol. Obstet. Fertil. Senol. 2018, 46, 598–604. [Google Scholar] [CrossRef] [PubMed]
- Schreiber, K.; Breen, K.; Cohen, H.; Jacobsen, S.; Middeldorp, S.; Pavord, S.; Regan, L.; Roccatello, D.; Robinson, S.E.; Sciascia, S.; et al. HYdroxychloroquine to Improve Pregnancy Outcome in Women with AnTIphospholipid Antibodies (HYPATIA) Protocol: A Multinational Randomized Controlled Trial of Hydroxychloroquine versus Placebo in Addition to Standard Treatment in Pregnant Women with Antiphospholipid Syndrome or Antibodies. Semin. Thromb. Hemost. 2017, 43, 562–571. [Google Scholar] [CrossRef] [PubMed]
- Ruffatti, A.; Favaro, M.; Hoxha, A.; Zambon, A.; Marson, P.; Del Ross, T.; Calligaro, A.; Tonello, M.; Nardelli, G.B. Apheresis and intravenous immunoglobulins used in addition to conventional therapy to treat high-risk pregnant antiphospholipid antibody syndrome patients. A prospective study. J. Reprod. Immunol. 2016, 115, 14–19. [Google Scholar] [CrossRef]
- Frampton, G.; Cameron, J.S.; Thom, M.; Jones, S.; Raftery, M. Successful removal of anti-phospholipid antibody during pregnancy using plasma exchange and low-dose prednisolone. Lancet 1987, 2, 1023–1024. [Google Scholar] [CrossRef]
- El-Haieg, D.O.; Zanati, M.F.; El-Foual, F.M. Plasmapheresis and pregnancy outcome in patients with antiphospholipid syndrome. Int. J. Gynaecol. Obstet. 2007, 99, 236–241. [Google Scholar] [CrossRef]
- Costantine, M.M. Pravastatin to prevent obstetrical complications in women with antiphospholipid syndrome. J. Clin. Investig. 2016, 126, 2792–2794. [Google Scholar] [CrossRef]
- Lefkou, E.; Mamopoulos, A.; Fragakis, N.; Dagklis, T.; Vosnakis, C.; Nounopoulos, E.; Rousso, D.; Girardi, G. Clinical improvement and successful pregnancy in a preeclamptic patient with antiphospholipid syndrome treated with pravastatin. Hypertension 2014, 63, e118–e119. [Google Scholar] [CrossRef] [PubMed]
- Alijotas-Reig, J.; Esteve-Valverde, E.; Ferrer-Oliveras, R.; Llurba, E.; Gris, J.M. Tumor Necrosis Factor-Alpha and Pregnancy: Focus on Biologics. An Updated and Comprehensive Review. Clin. Rev. Allergy Immunol. 2017, 53, 40–53. [Google Scholar] [CrossRef]
- Berman, J.; Girardi, G.; Salmon, J.E. TNF-alpha is a critical effector and a target for therapy in antiphospholipid antibody-induced pregnancy loss. J. Immunol. 2005, 174, 485–490. [Google Scholar] [CrossRef]
- van Hoorn, M.E.; Hague, W.M.; van Pampus, M.G.; Bezemer, D.; de Vries, J.I. Low-molecular-weight heparin and aspirin in the prevention of recurrent early-onset pre-eclampsia in women with antiphospholipid antibodies: The FRUIT-RCT. Eur. J. Obstet. Gynecol. Reprod. Biol. 2016, 197, 168–173. [Google Scholar] [CrossRef]
- Rodger, M.A.; Hague, W.M.; Kingdom, J.; Kahn, S.R.; Karovitch, A.; Sermer, M.; Clement, A.M.; Coat, S.; Chan, W.S.; Said, J.; et al. Antepartum dalteparin versus no antepartum dalteparin for the prevention of pregnancy complications in pregnant women with thrombophilia (TIPPS): A multinational open-label randomised trial. Lancet 2014, 384, 1673–1683. [Google Scholar] [CrossRef] [PubMed]
- Mastrolia, S.A.; Novack, L.; Thachil, J.; Rabinovich, A.; Pikovsky, O.; Klaitman, V.; Loverro, G.; Erez, O. LMWH in the prevention of preeclampsia and fetal growth restriction in women without thrombophilia. A systematic review and meta-analysis. Thromb. Haemost. 2016, 116, 868–878. [Google Scholar] [CrossRef] [PubMed]
- Robertson, L.; Wu, O.; Langhorne, P.; Twaddle, S.; Clark, P.; Lowe, G.D.; Walker, I.D.; Greaves, M.; Brenkel, I.; Regan, L.; et al. Thrombophilia in pregnancy: A systematic review. Br. J. Haematol. 2006, 132, 171–196. [Google Scholar] [CrossRef] [PubMed]
- de Jong, P.G.; Goddijn, M.; Middeldorp, S. Testing for inherited thrombophilia in recurrent miscarriage. Semin. Reprod. Med. 2011, 29, 540–547. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Chen, Y.; Ye, C.; Xing, D.; Wu, R.; Li, F.; Chen, L.; Wang, T. Hereditary thrombophilia and recurrent pregnancy loss: A systematic review and meta-analysis. Hum. Reprod. 2021, 36, 1213–1229. [Google Scholar] [CrossRef] [PubMed]
- Rodger, M.A.; Betancourt, M.T.; Clark, P.; Lindqvist, P.G.; Dizon-Townson, D.; Said, J.; Seligsohn, U.; Carrier, M.; Salomon, O.; Greer, I.A. The association of factor V leiden and prothrombin gene mutation and placenta-mediated pregnancy complications: A systematic review and meta-analysis of prospective cohort studies. PLoS Med. 2010, 7, e1000292. [Google Scholar] [CrossRef]
- Quenby, S.; Booth, K.; Hiller, L.; Coomarasamy, A.; de Jong, P.G.; Hamulyák, E.N.; Scheres, L.J.; van Haaps, T.F.; Ewington, L.; Tewary, S.; et al. Heparin for women with recurrent miscarriage and inherited thrombophilia (ALIFE2): An international open-label, randomised controlled trial. Lancet 2023, 402, 54–61. [Google Scholar] [CrossRef] [PubMed]
- Fanouriakis, A.; Kostopoulou, M.; Alunno, A.; Aringer, M.; Bajema, I.; Boletis, J.N.; Cervera, R.; Doria, A.; Gordon, C.; Govoni, M.; et al. 2019 Update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann. Rheum. Dis. 2019, 78, 736–745. [Google Scholar] [CrossRef]
- Kerschbaumer, A.; Sepriano, A.; Smolen, J.S.; Van Der Heijde, D.; Dougados, M.; Van Vollenhoven, R.; McInnes, I.B.; Bijlsma, J.W.J.; Burmester, G.R.; De Wit, M.; et al. Efficacy of pharmacological treatment in rheumatoid arthritis: A systematic literature research informing the 2019 update of the EULAR recommendations for management of rheumatoid arthritis. Ann. Rheum. Dis. 2020, 79, 744–759. [Google Scholar] [CrossRef]
- Brito-Zerón, P.; Ramos-Casals, M. Advances in the understanding and treatment of systemic complications in Sjögren’s syndrome. Curr. Opin. Rheumatol. 2014, 26, 520–527. [Google Scholar] [CrossRef]
- Demarchi, J.; Papasidero, S.; Medina, M.A.; Klajn, D.; Chaparro del Moral, R.; Rillo, O.; Martiré, V.; Crespo, G.; Secco, A.; Catalan Pellet, A.; et al. Primary Sjögren’s syndrome: Extraglandular manifestations and hydroxychloroquine therapy. Clin. Rheumatol. 2017, 36, 2455–2460. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.Q.; Zhang, L.W.; Wei, P.; Hua, H. Is hydroxychloroquine effective in treating primary Sjogren’s syndrome: A systematic review and meta-analysis. BMC Musculoskelet. Disord. 2017, 18, 186. [Google Scholar] [CrossRef] [PubMed]
- Abarientos, C.; Sperber, K.; Shapiro, D.L.; Aronow, W.S.; Chao, C.P.; Ash, J.Y. Hydroxychloroquine in systemic lupus erythematosus and rheumatoid arthritis and its safety in pregnancy. Expert Opin. Drug Saf. 2011, 10, 705–714. [Google Scholar] [CrossRef]
- Clowse, M.E.B.; Eudy, A.M.; Balevic, S.; Sanders-Schmidler, G.; Kosinski, A.; Fischer-Betz, R.; Gladman, D.D.; Molad, Y.; Nalli, C.; Mokbel, A.; et al. Hydroxychloroquine in the pregnancies of women with lupus: A meta-analysis of individual participant data. Lupus Sci. Med. 2022, 9, e000651. [Google Scholar] [CrossRef] [PubMed]
- Sciascia, S.; Hunt, B.J.; Talavera-Garcia, E.; Lliso, G.; Khamashta, M.A.; Cuadrado, M.J. The impact of hydroxychloroquine treatment on pregnancy outcome in women with antiphospholipid antibodies. Am. J. Obstet. Gynecol. 2016, 214, 273.e271–273.e278. [Google Scholar] [CrossRef] [PubMed]
- Gerde, M.; Ibarra, E.; Mac Kenzie, R.; Fernandez Suarez, C.; Heer, C.; Alvarez, R.; Iglesias, M.; Balparda, J.; Beruti, E.; Rubinstein, F. The impact of hydroxychloroquine on obstetric outcomes in refractory obstetric antiphospholipid syndrome. Thromb. Res. 2021, 206, 104–110. [Google Scholar] [CrossRef]
- Nuri, E.; Taraborelli, M.; Andreoli, L.; Tonello, M.; Gerosa, M.; Calligaro, A.; Argolini, L.M.; Kumar, R.; Pengo, V.; Meroni, P.L.; et al. Long-term use of hydroxychloroquine reduces antiphospholipid antibodies levels in patients with primary antiphospholipid syndrome. Immunol. Res. 2017, 65, 17–24. [Google Scholar] [CrossRef]
- Kravvariti, E.; Koutsogianni, A.; Samoli, E.; Sfikakis, P.P.; Tektonidou, M.G. The effect of hydroxychloroquine on thrombosis prevention and antiphospholipid antibody levels in primary antiphospholipid syndrome: A pilot open label randomized prospective study. Autoimmun. Rev. 2020, 19, 102491. [Google Scholar] [CrossRef]
- Palli, E.; Kravvariti, E.; Tektonidou, M.G. Type I Interferon Signature in Primary Antiphospholipid Syndrome: Clinical and Laboratory Associations. Front. Immunol. 2019, 10, 487. [Google Scholar] [CrossRef]
- Do, S.C.; Rizk, N.M.; Druzin, M.L.; Simard, J.F. Does Hydroxychloroquine Protect against Preeclampsia and Preterm Delivery in Systemic Lupus Erythematosus Pregnancies? Am. J. Perinatol. 2020, 37, 873–880. [Google Scholar] [CrossRef]
- Hu, Z.; Gao, R.; Huang, W.; Wang, H.; Qin, L. Effect of Hydroxychloroquine on Lupus Activity, Preeclampsia and Intrauterine Growth Restriction in Pregnant Women with Systemic Lupus Erythematosus and/or Antiphospholipid Syndrome: A Systematic Review and Meta-Analysis. J. Clin. Med. 2023, 12, 485. [Google Scholar] [CrossRef] [PubMed]
- Latino, J.O.; Udry, S.; Aranda, F.; Wingeyer, S.P.; Romero, D.S.F.; Belizna, C.; Larranaga, G. Risk factors for early severe preeclampsia in obstetric antiphospholipid syndrome with conventional treatment. The impact of hydroxychloroquine. Lupus 2020, 29, 1736–1742. [Google Scholar] [CrossRef] [PubMed]
- Pasquier, E.; de Saint-Martin, L.; Marhic, G.; Chauleur, C.; Bohec, C.; Bretelle, F.; Lejeune-Saada, V.; Hannigsberg, J.; Plu-Bureau, G.; Cogulet, V.; et al. Hydroxychloroquine for prevention of recurrent miscarriage: Study protocol for a multicentre randomised placebo-controlled trial BBQ study. BMJ Open 2019, 9, e025649. [Google Scholar] [CrossRef] [PubMed]
- Andreoli, L.; Bertsias, G.K.; Agmon-Levin, N.; Brown, S.; Cervera, R.; Costedoat-Chalumeau, N.; Doria, A.; Fischer-Betz, R.; Forger, F.; Moraes-Fontes, M.F.; et al. EULAR recommendations for women’s health and the management of family planning, assisted reproduction, pregnancy and menopause in patients with systemic lupus erythematosus and/or antiphospholipid syndrome. Ann. Rheum. Dis. 2017, 76, 476–485. [Google Scholar] [CrossRef]
- Yang, C.Y.; Leung, P.S.; Adamopoulos, I.E.; Gershwin, M.E. The implication of vitamin D and autoimmunity: A comprehensive review. Clin. Rev. Allergy Immunol. 2013, 45, 217–226. [Google Scholar] [CrossRef]
- Aranow, C. Vitamin D and the immune system. J. Investig. Med. 2011, 59, 881–886. [Google Scholar] [CrossRef]
- Rolf, L.; Muris, A.H.; Hupperts, R.; Damoiseaux, J. Vitamin D effects on B cell function in autoimmunity. Ann. N. Y. Acad. Sci. 2014, 1317, 84–91. [Google Scholar] [CrossRef]
- Chen, S.; Sims, G.P.; Chen, X.X.; Gu, Y.Y.; Chen, S.; Lipsky, P.E. Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J. Immunol. 2007, 179, 1634–1647. [Google Scholar] [CrossRef]
- Morgan, J.W.; Kouttab, N.; Ford, D.; Maizel, A.L. Vitamin D-mediated gene regulation in phenotypically defined human B cell subpopulations. Endocrinology 2000, 141, 3225–3234. [Google Scholar] [CrossRef]
- Cantorna, M.T.; Snyder, L.; Lin, Y.D.; Yang, L. Vitamin D and 1,25(OH)2D regulation of T cells. Nutrients 2015, 7, 3011–3021. [Google Scholar] [CrossRef]
- Bhalla, A.K.; Amento, E.P.; Clemens, T.L.; Holick, M.F.; Krane, S.M. Specific high-affinity receptors for 1,25-dihydroxyvitamin D3 in human peripheral blood mononuclear cells: Presence in monocytes and induction in T lymphocytes following activation. J. Clin. Endocrinol. Metab. 1983, 57, 1308–1310. [Google Scholar] [CrossRef] [PubMed]
- Marinho, A.; Carvalho, C.; Boleixa, D.; Bettencourt, A.; Leal, B.; Guimarães, J.; Neves, E.; Oliveira, J.C.; Almeida, I.; Farinha, F.; et al. Vitamin D supplementation effects on FoxP3 expression in T cells and FoxP3(+)/IL-17A ratio and clinical course in systemic lupus erythematosus patients: A study in a Portuguese cohort. Immunol. Res. 2017, 65, 197–206. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Eapen, M.S.; Zosky, G.R. Vitamin D both facilitates and attenuates the cellular response to lipopolysaccharide. Sci. Rep. 2017, 7, 45172. [Google Scholar] [CrossRef] [PubMed]
- Iruretagoyena, M.; Hirigoyen, D.; Naves, R.; Burgos, P.I. Immune Response Modulation by Vitamin D: Role in Systemic Lupus Erythematosus. Front. Immunol. 2015, 6, 513. [Google Scholar] [CrossRef]
- Tetlow, L.C.; Smith, S.J.; Mawer, E.B.; Woolley, D.E. Vitamin D receptors in the rheumatoid lesion: Expression by chondrocytes, macrophages, and synoviocytes. Ann. Rheum. Dis. 1999, 58, 118–121. [Google Scholar] [CrossRef]
- Piantoni, S.; Andreoli, L.; Scarsi, M.; Zanola, A.; Dall’Ara, F.; Pizzorni, C.; Cutolo, M.; Airò, P.; Tincani, A. Phenotype modifications of T-cells and their shift toward a Th2 response in patients with systemic lupus erythematosus supplemented with different monthly regimens of vitamin D. Lupus 2015, 24, 490–498. [Google Scholar] [CrossRef]
- Zhao, M.; Duan, X.H.; Wu, Z.Z.; Gao, C.C.; Wang, N.; Zheng, Z.H. Severe vitamin D deficiency affects the expression of autophagy related genes in PBMCs and T-cell subsets in active systemic lupus erythematosus. Am. J. Clin. Exp. Immunol. 2017, 6, 43–51. [Google Scholar]
- Munger, K.L.; Levin, L.I.; Hollis, B.W.; Howard, N.S.; Ascherio, A. Serum 25-hydroxyvitamin D levels and risk of multiple sclerosis. JAMA 2006, 296, 2832–2838. [Google Scholar] [CrossRef]
- Åivo, J.; Hänninen, A.; Ilonen, J.; Soilu-Hänninen, M. Vitamin D3 administration to MS patients leads to increased serum levels of latency activated peptide (LAP) of TGF-beta. J. Neuroimmunol. 2015, 280, 12–15. [Google Scholar] [CrossRef]
- Lee, C.L.; Ng, B.K.; Wu, L.L.; Cheah, F.C.; Othman, H.; Ismail, N.A.M. Vitamin D deficiency in pregnancy at term: Risk factors and pregnancy outcomes. Horm. Mol. Biol. Clin. Investig. 2017, 31, 20170005. [Google Scholar] [CrossRef]
- Fernández-Alonso, A.M.; Dionis-Sánchez, E.C.; Chedraui, P.; González-Salmerón, M.D.; Pérez-López, F.R. First-trimester maternal serum 25-hydroxyvitamin D₃ status and pregnancy outcome. Int. J. Gynaecol. Obstet. 2012, 116, 6–9. [Google Scholar] [CrossRef] [PubMed]
- Agmon-Levin, N.; Blank, M.; Zandman-Goddard, G.; Orbach, H.; Meroni, P.L.; Tincani, A.; Doria, A.; Cervera, R.; Miesbach, W.; Stojanovich, L.; et al. Vitamin D: An instrumental factor in the anti-phospholipid syndrome by inhibition of tissue factor expression. Ann. Rheum. Dis. 2011, 70, 145–150. [Google Scholar] [CrossRef] [PubMed]
- Bodnar, L.M.; Catov, J.M.; Simhan, H.N.; Holick, M.F.; Powers, R.W.; Roberts, J.M. Maternal vitamin D deficiency increases the risk of preeclampsia. J. Clin. Endocrinol. Metab. 2007, 92, 3517–3522. [Google Scholar] [CrossRef]
- Aggarwal, B.B.; Kumar, A.; Bharti, A.C. Anticancer potential of curcumin: Preclinical and clinical studies. Anticancer Res. 2003, 23, 363–398. [Google Scholar]
- Mahady, G.B.; Pendland, S.L.; Yun, G.; Lu, Z.Z. Turmeric (Curcuma longa) and curcumin inhibit the growth of Helicobacter pylori, a group 1 carcinogen. Anticancer Res. 2002, 22, 4179–4181. [Google Scholar]
- Reddy, R.C.; Vatsala, P.G.; Keshamouni, V.G.; Padmanaban, G.; Rangarajan, P.N. Curcumin for malaria therapy. Biochem. Biophys. Res. Commun. 2005, 326, 472–474. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.G.; Kunnumakkara, A.B.; Nair, A.; Merritt, W.M.; Han, L.Y.; Armaiz-Pena, G.N.; Kamat, A.A.; Spannuth, W.A.; Gershenson, D.M.; Lutgendorf, S.K.; et al. Curcumin inhibits tumor growth and angiogenesis in ovarian carcinoma by targeting the nuclear factor-kappaB pathway. Clin. Cancer Res. 2007, 13, 3423–3430. [Google Scholar] [CrossRef]
- Marchiani, A.; Rozzo, C.; Fadda, A.; Delogu, G.; Ruzza, P. Curcumin and curcumin-like molecules: From spice to drugs. Curr. Med. Chem. 2014, 21, 204–222. [Google Scholar] [CrossRef]
- Aggarwal, B.B.; Harikumar, K.B. Potential therapeutic effects of curcumin, the anti-inflammatory agent, against neurodegenerative, cardiovascular, pulmonary, metabolic, autoimmune and neoplastic diseases. Int. J. Biochem. Cell Biol. 2009, 41, 40–59. [Google Scholar] [CrossRef]
- Panahi, Y.; Hosseini, M.S.; Khalili, N.; Naimi, E.; Simental-Mendía, L.E.; Majeed, M.; Sahebkar, A. Effects of curcumin on serum cytokine concentrations in subjects with metabolic syndrome: A post-hoc analysis of a randomized controlled trial. Biomed. Pharmacother. 2016, 82, 578–582. [Google Scholar] [CrossRef]
- Panahi, Y.; Khalili, N.; Sahebi, E.; Namazi, S.; Karimian, M.S.; Majeed, M.; Sahebkar, A. Antioxidant effects of curcuminoids in patients with type 2 diabetes mellitus: A randomized controlled trial. Inflammopharmacology 2017, 25, 25–31. [Google Scholar] [CrossRef] [PubMed]
- Lao, C.D.; Ruffin, M.T.t.; Normolle, D.; Heath, D.D.; Murray, S.I.; Bailey, J.M.; Boggs, M.E.; Crowell, J.; Rock, C.L.; Brenner, D.E. Dose escalation of a curcuminoid formulation. BMC Complement. Altern. Med. 2006, 6, 10. [Google Scholar] [CrossRef] [PubMed]
- Basnet, P.; Skalko-Basnet, N. Curcumin: An anti-inflammatory molecule from a curry spice on the path to cancer treatment. Molecules 2011, 16, 4567–4598. [Google Scholar] [CrossRef] [PubMed]
- Gupta, S.C.; Patchva, S.; Aggarwal, B.B. Therapeutic roles of curcumin: Lessons learned from clinical trials. AAPS J. 2013, 15, 195–218. [Google Scholar] [CrossRef]
- Kocaadam, B.; Sanlier, N. Curcumin, an active component of turmeric (Curcuma longa), and its effects on health. Crit. Rev. Food Sci. Nutr. 2017, 57, 2889–2895. [Google Scholar] [CrossRef] [PubMed]
- Menon, V.P.; Sudheer, A.R. Antioxidant and anti-inflammatory properties of curcumin. Adv. Exp. Med. Biol. 2007, 595, 105–125. [Google Scholar] [CrossRef]
- Panahi, Y.; Alishiri, G.H.; Parvin, S.; Sahebkar, A. Mitigation of Systemic Oxidative Stress by Curcuminoids in Osteoarthritis: Results of a Randomized Controlled Trial. J. Diet. Suppl. 2016, 13, 209–220. [Google Scholar] [CrossRef]
- Jurenka, J.S. Anti-inflammatory properties of curcumin, a major constituent of Curcuma longa: A review of preclinical and clinical research. Altern. Med. Rev. 2009, 14, 141–153. [Google Scholar]
- Lopez-Candales, A.; Hernandez Burgos, P.M.; Hernandez-Suarez, D.F.; Harris, D. Linking Chronic Inflammation with Cardiovascular Disease: From Normal Aging to the Metabolic Syndrome. J. Nat. Sci. 2017, 3, e341. [Google Scholar]
- Phumsuay, R.; Muangnoi, C.; Dasuni Wasana, P.W.; Hasriadi; Vajragupta, O.; Rojsitthisak, P.; Towiwat, P. Molecular Insight into the Anti-Inflammatory Effects of the Curcumin Ester Prodrug Curcumin Diglutaric Acid In Vitro and In Vivo. Int. J. Mol. Sci. 2020, 21, 5700. [Google Scholar] [CrossRef]
- Lestari, M.L.; Indrayanto, G. Curcumin. Profiles Drug Subst. Excip. Relat. Methodol. 2014, 39, 113–204. [Google Scholar] [CrossRef] [PubMed]
- Vitoratos, N.; Economou, E.; Iavazzo, C.; Panoulis, K.; Creatsas, G. Maternal serum levels of TNF-alpha and IL-6 long after delivery in preeclamptic and normotensive pregnant women. Mediat. Inflamm. 2010, 2010, 908649. [Google Scholar] [CrossRef]
- Xia, L.; Xie, H.; Yu, Y.; Zhou, H.; Wang, T.; Yan, J. The Effects of NF-κB and c-Jun/AP-1 on the Expression of Prothrombotic and Proinflammatory Molecules Induced by Anti-β2GPI in Mouse. PLoS ONE 2016, 11, e0147958. [Google Scholar] [CrossRef] [PubMed]
- Maalouly, G.; Ward, C.; Smayra, V.; Saliba, Y.; Aftimos, G.; Haddad, F.; Farès, N. Fish oil attenuates neurologic severity of antiphospholipid syndrome in a mice experimental model. Nutr. Neurosci. 2017, 20, 563–570. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mayer-Pickel, K.; Nanda, M.; Gajic, M.; Cervar-Zivkovic, M. Preeclampsia and the Antiphospholipid Syndrome. Biomedicines 2023, 11, 2298. https://doi.org/10.3390/biomedicines11082298
Mayer-Pickel K, Nanda M, Gajic M, Cervar-Zivkovic M. Preeclampsia and the Antiphospholipid Syndrome. Biomedicines. 2023; 11(8):2298. https://doi.org/10.3390/biomedicines11082298
Chicago/Turabian StyleMayer-Pickel, Karoline, Manurishi Nanda, Maja Gajic, and Mila Cervar-Zivkovic. 2023. "Preeclampsia and the Antiphospholipid Syndrome" Biomedicines 11, no. 8: 2298. https://doi.org/10.3390/biomedicines11082298
APA StyleMayer-Pickel, K., Nanda, M., Gajic, M., & Cervar-Zivkovic, M. (2023). Preeclampsia and the Antiphospholipid Syndrome. Biomedicines, 11(8), 2298. https://doi.org/10.3390/biomedicines11082298