Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array
Open accessAbstract
BACKGROUND: Preeclampsia is a severe complication of pregnancy characterized by an excessive maternal systemic inflammatory response with activation of both the innate and adaptive arms of the immune system. Cytokines, chemokines and adhesion molecules are central to innate and adaptive immune processes. The purpose of this study was to determine circulating levels of cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia in a comprehensive manner, and to investigate their relationship to the clinical features and laboratory parameters of the study participants, including markers of overall inflammation (C-reactive protein), endothelial activation (von Willebrand factor antigen) and endothelial injury (fibronectin), oxidative stress (malondialdehyde) and trophoblast debris (cell-free fetal DNA). RESULTS: Serum levels of interleukin (IL)-1beta, IL-1 receptor antagonist (IL-1ra), IL-2, IL-4, IL-6, IL-8, IL-10, IL-12p40, IL-12p70, IL-18, interferon (IFN)-gamma, tumor necrosis factor (TNF)-alpha, transforming growth factor (TGF)-beta1, interferon-gamma-inducible protein (IP)-10, monocyte chemotactic protein (MCP)-1, intercellular adhesion molecule (ICAM)-1 and vascular cell adhesion molecule (VCAM)-1 were measured in 60 preeclamptic patients, 60 healthy pregnant women and 59 healthy non-pregnant women by multiplex suspension array and ELISA. In normal pregnancy, the relative abundance of circulating IL-18 over IL-12p70 and the relative deficiency of the bioactive IL-12p70 in relation to IL-12p40 might favour Th2-type immunity. Although decreased IL-1ra, TNF-alpha and MCP-1 concentrations of healthy pregnant relative to non-pregnant women reflect anti-inflammatory changes in circulating cytokine profile, their decreased serum IL-10 and increased IP-10 levels might drive pro-inflammatory responses. In addition to a shift towards Th1-type immunity (expressed by the increased IL-2/IL-4 and IFN-gamma/IL-4 ratios), circulating levels of the pro-inflammatory cytokines IL-6 and TNF-alpha, the chemokines IL-8, IP-10 and MCP-1, as well as the adhesion molecules ICAM-1 and VCAM-1, were raised in preeclampsia compared with healthy pregnancy, resulting in an overall pro-inflammatory systemic environment. Increased IP-10, MCP-1, ICAM-1 and VCAM-1 concentrations of preeclamptic patients showed significant correlations with blood pressure values, renal and liver function parameters, as well as with CRP, malondialdehyde, von Willebrand factor antigen and fibronectin levels. CONCLUSIONS: According to our findings, preeclampsia was associated with an overall pro-inflammatory systemic environment. Elevated amounts of pro-inflammatory cytokines, chemokines and adhesion molecules in the maternal circulation might play a central role in the excessive systemic inflammatory response, as well as in the generalized endothelial dysfunction characteristics of the maternal syndrome of preeclampsia.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Metformin decreased the expression of vascular cell adhesion molecule 1 (VCAM1) expressed by endothelial cells that are dysfunctional or have been stimulated by incubation with tumor necrosis factor alpha (TNF-α).
“Metformin also decreased the expression of vascular cell adhesion molecule 1 (VCAM1), expressed by endothelial cells that are dysfunctional or have been stimulated by incubation with tumor necrosis factor alpha (TNF-α), a cytokine increased in the circulation of patients with preeclampsia(190–195).”
From Metformin, the Aspirin of the 21st Century: Its Role in Gestational Diabetes Mellitus, Prevention of Preeclampsia and Cancer, and the Promotion of Longevity (2017) · cites this paper as [195]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Acute-Phase Proteins and Other Systemic Responses to Inflammation
Gabay, C., & Kushner, I. (1999) · New England Journal of Medicine · doi:10.1056/nejm199902113400607 · Cited by 6,734 · see citing works
Wegmann, T. G., Lin, H., Guilbert, L., & Mosmann, T. R. (1993) · Immunology Today · doi:10.1016/0167-5699(93)90235-d · Cited by 2,852 · see citing works
Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems
Placer, Z., Cushman, L. L., & Johnson, B. C. (1966) · Analytical Biochemistry · doi:10.1016/0003-2697(66)90167-9 · Cited by 2,330 · see citing works
Soluble endoglin contributes to the pathogenesis of preeclampsia
Venkatesha, S., Toporsian, M., Lam, C., Hanai, J.-I., Mammoto, T., Kim, Y. M., Bdolah, Y., Lim, K.-H., Yuan, H.-T., Libermann, T. A., et al. (2006) · Nature Medicine · doi:10.1038/nm1429 · Cited by 1,855 · see citing works
Preeclampsia: An excessive maternal inflammatory response to pregnancy
Redman, C. W. G., Sacks, G. P., & Sargent, I. L. (1999) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(99)70239-5 · Cited by 1,838 · see citing works
Decidual NK cells regulate key developmental processes at the human fetal-maternal interface
Hanna, J. H., Goldman‐Wohl, D., Hamani, Y., Avraham, I., Greenfield, C., Natanson‐Yaron, S., Prus, D., Cohen‐Daniel, L., Arnon, T. I., Manaster, I., et al. (2006) · Nature Medicine · doi:10.1038/nm1452 · Cited by 1,690 · see citing works
Interleukin-18 Regulates Both Th1 and Th2 Responses
Nakanishi, K., Yoshimoto, T., Tsutsui, H., & Okamura, H. (2001) · Annual Review of Immunology · doi:10.1146/annurev.immunol.19.1.423 · Cited by 1,310 · see citing works
Sacks, G. P., Studená, K., Sargent, I. L., & Redman, C. W. G. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70254-6 · Cited by 823 · see citing works
Inflammation, free radicals, and antioxidants
Conner, E. M., & Grisham, M. B. (1996) · Nutrition · doi:10.1016/s0899-9007(96)00000-8 · Cited by 697 · see citing works
Quantitative Abnormalities of Fetal DNA in Maternal Serum in Preeclampsia
Lo, Y. M. D., Leung, T. N., Tein, M., Sargent, I. L., Zhang, J., Lau, T. K., Haines, C. J., & Redman, C. W. G. (1999) · Clinical Chemistry · doi:10.1093/clinchem/45.2.184 · Cited by 480 · see citing works
Saito, S., Sakai, M., Sasaki, Y., Tanebe, K., Tsuda, H., & MICHIMATA, T. (1999) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1999.00997.x · Cited by 424 · see citing works
The role of the immune system in preeclampsia
Saito, S., Shiozaki, A., Nakashima, A., Sakai, M., & Sasaki, Y. (2007) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2007.02.006 · Cited by 352 · see citing works
Expression of Inflammatory Cytokines in Placentas from Women with Preeclampsia1
Benyo, D. F., Smárason, A. K., Redman, C. W. G., Sims, C. J., & Conrad, K. P. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7585 · Cited by 329 · see citing works
Expression of Inflammatory Cytokines in Placentas from Women with Preeclampsia
Benyo, D. F. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.86.6.2505 · Cited by 264 · see citing works
Greer, I. A., Lyall, F., Perera, T., Boswell, F., & Macara, L. (1994) · PubMed · Cited by 262 · see citing works
Cytokine mapping of sera from women with preeclampsia and normal pregnancies
Jonsson, Y., Rubèr, M., Matthiesen, L., Berg, G. E., Nieminen, K., Sharma, S., Ernerudh, J., & Ekerfelt, C. (2006) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2005.10.007 · Cited by 256 · see citing works
Saito, S., Umekage, H., 阪本, 義., Sakai, M., Tanebe, K., Sasaki, Y., & Morikawa, H. (1999) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1999.tb00442.x · Cited by 237 · see citing works
Trophoblast–Macrophage Interactions: a Regulatory Network for the Protection of Pregnancy
Fest, S., Aldo, P. B., Abrahams, V. M., Visintin, I., Alvero, A. B., Chen, R., Chavez, S. L., Romero, R. J., & Mor, G. (2006) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2006.00446.x · Cited by 225 · see citing works
Rusterholz, C., Hahn, S., & Holzgreve, W. (2007) · Seminars in Immunopathology · doi:10.1007/s00281-007-0071-6 · Cited by 196 · see citing works
Tumour necrosis factor-alpha (TNF-α) gene polymorphism and expression in pre-eclampsia
Chen, G., Wilson, R., Wang, S. H., Zheng, H.-E., Walker, J. J., & McKillop, J. H. (1996) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1996.d01-647.x · Cited by 155 · see citing works
Preeclampsia and the systemic inflammatory response
Redman, C. W. G., & Sargent, I. L. (2004) · Seminars in Nephrology · doi:10.1016/s0270-9295(04)00127-5 · Cited by 148 · see citing works
CXCL10/IP-10: A missing link between inflammation and anti-angiogenesis in preeclampsia?
Gotsch, F., Romero, R. J., Friel, L. A., Kusanovic, J. P., Espinoza, J., Erez, O., Than, N. G., Mittal, P., Edwin, S. S., Yoon, B. H., et al. (2007) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767050701483298 · Cited by 141 · see citing works
Preeclampsia and the systemic inflammatory response
Redman, C. W. G., & Sargent, I. L. (2004) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2004.07.005 · Cited by 137 · see citing works
T helper 1- and T helper 2-type cytokine imbalance in pregnant women with pre-eclampsia
Darmochwał-Kolarz, D., Leszczyńska‐Gorzelak, B., Roliński, J., & Oleszczuk, J. (1999) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(99)00065-2 · Cited by 125 · see citing works
Circulating heat shock protein 70 (HSPA1A) in normal and pathological pregnancies
Molvarec, A., Tamási, L., Losonczy, G., Madách, K., Prohászka, Z., & Rigó, J. J. (2009) · Cell Stress and Chaperones · doi:10.1007/s12192-009-0146-5 · Cited by 114 · see citing works
Self-citationMolvarec, A., Rigó, J. J., Lázár, L., Balogh, K., Makó, V., Cervenak, L., Mézes, M., & Prohászka, Z. (2008) · Cell Stress and Chaperones · doi:10.1007/s12192-008-0067-8 · Cited by 106 · see citing works
Self-citationMaternal Cytokine Production Patterns in Women with Pre‐eclampsia
Azizieh, F. Y., Raghupathy, R., & Makhseed, M. (2005) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2005.00278.x · Cited by 100 · see citing works
Cytokine Genotyping in Preeclampsia
Daher, S., Sass, N., Oliveira, L. G., & Mattar, R. (2006) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2005.00341.x · Cited by 99 · see citing works
The Expressions of Intracellular Cytokines in the Lymphocytes of Preeclamptic Patients
Darmochwał-Kolarz, D., Roliński, J., Leszczyńska‐Gorzelak, B., & Oleszczuk, J. (2002) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2002.01089.x · Cited by 90 · see citing works
Visser, N., van Rijn, B. B., Rijkers, G. T., Franx, A., & Bruinse, H. W. (2007) · Obstetrical & Gynecological Survey · doi:10.1097/01.ogx.0000256779.06275.c4 · Cited by 87 · see citing works
Benian, A., Madazl, R., Aksu, F., Uzun, H., & Aydn, S. (2002) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(02)02077-x · Cited by 78 · see citing works
Tumor necrosis factor α, interleukin‐6 and interleukin‐10 polymorphisms in preeclampsia
Vural, P., Değirmencioğlu, S., Saral, N. Y., Demirkan, A., Akgül, C., Yıldırım, G., İşsever, H., & Eroğlu, H. (2010) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2009.01111.x · Cited by 70 · see citing works
Cytokine gene polymorphisms in preeclampsia and eclampsia
de Lima, T. H. B., Sass, N., Mattar, R., Moron, A. F., Torloni, M. R., Franchim, C. S., & Daher, S. (2009) · Hypertension Research · doi:10.1038/hr.2009.58 · Cited by 68 · see citing works
Molvarec, A., Jermendy, Á., Nagy, B., Kovács, M., Várkonyi, T., Hupuczi, P., Prohászka, Z., & Rigó, J. J. (2008) · Clinica Chimica Acta · doi:10.1016/j.cca.2008.03.009 · Cited by 65 · see citing works
Self-citationAssociation between allelic variants in cytokine genes and preeclampsia
Haggerty, C. L., Ferrell, R. E., Hubel, C. A., Marković, N., Harger, G. F., & Ness, R. B. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.11.008 · Cited by 62 · see citing works
Ohkuchi, A., IWASAKI, R., Suzuki, H., Hirashima, C., Takahashi, K., Usui, R., Matsubara, S., Minakami, H., & Suzuki, M. (2006) · Hypertension Research · doi:10.1291/hypres.29.161 · Cited by 58 · see citing works
Endothelial Cell Dysfunction, Injury and Death
Pober, J. S., & Min, W. (2006) · Springer eBooks · doi:10.1007/3-540-36028-x_5 · Cited by 54 · see citing works
Lázár, L., Rigó, J. J., Nagy, B., Balogh, K., Makó, V., Cervenak, L., Mézes, M., Prohászka, Z., & Molvarec, A. (2009) · BMC Medical Genetics · doi:10.1186/1471-2350-10-120 · Cited by 54 · see citing works
Self-citationAggarwal, P. K., Jain, V., & Jha, V. (2010) · Hypertension Research · doi:10.1038/hr.2010.23 · Cited by 54 · see citing works
Sakai, M., Shiozaki, A., Sasaki, Y., Yoneda, S., & Saito, S. (2004) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2004.01.001 · Cited by 44 · see citing works
Rosta, K., Molvarec, A., Énzsöly, A., Nagy, B., Rónai, Z., Fekete, A., Sasvári‐Székely, M., Rigó, J. J., & Vér, Á. (2008) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2008.10.014 · Cited by 41 · see citing works
Self-citationPreeclampsia is associated with decreased serum α2-HS glycoprotein (fetuin-A) concentration
Molvarec, A., Kalabay, L., Derzsy, Z., Szarka, A., Halmos, A., Stenczer, B., Arnaud, P., Karádi, I., Prohászka, Z., & Rigó, J. J. (2009) · Hypertension Research · doi:10.1038/hr.2009.79 · Cited by 38 · see citing works
Self-citationCirculating anti-heat-shock-protein antibodies in normal pregnancy and preeclampsia
Molvarec, A., Derzsy, Z., Kocsis, J., Bőze, T., Nagy, B., Balogh, K., Makó, V., Cervenak, L., Mézes, M., Karádi, I., et al. (2009) · Cell Stress and Chaperones · doi:10.1007/s12192-009-0102-4 · Cited by 30 · see citing works
Self-citationOhkuchi, A., Minakami, H., AOYA, T., HAGA, T., Kimura, H., Suzuki, M., & Sato, I. (2001) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2001.d01-10.x · Cited by 25 · see citing works
Presence of Cell-Free Fetal DNA in Plasma of Women with Ectopic Pregnancies,
Lázár, L., Nagy, B., Bán, Z., Nagy, G., & Papp, Z. (2006) · Clinical Chemistry · doi:10.1373/clinchem.2006.067587 · Cited by 25 · see citing works
Self-citationLeptin gene (TTTC)n microsatellite polymorphism in pre-eclampsia and HELLP syndrome
Nagy, B., Várkonyi, T., Molvarec, A., Lázár, L., Hupuczi, P., Than, N. G., & Rigó, J. J. (2009) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2009.243 · Cited by 12 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Immune responses at the maternal-fetal interface
Ander, S. E., Diamond, M., & Coyne, C. B. (2019) · Science Immunology · doi:10.1126/sciimmunol.aat6114 · Cited by 652 · see citing works
Pre-eclampsia: its pathogenesis and pathophysiolgy
Gathiram, P., & Moodley, J. (2016) · Cardiovascular journal of South Africa/Cardiovascular journal of Southern Africa · doi:10.5830/cvja-2016-009 · Cited by 433 · see citing works
Cotechini, T., Komisarenko, M., Sperou, A., Macdonald-Goodfellow, S. K., Adams, M. A., & Graham, C. H. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20130295 · Cited by 343 · see citing works
Cytokine Research in Depression: Principles, Challenges, and Open Questions
Himmerich, H., Patsalos, O., Lichtblau, N., Ibrahim, M. A. A., & Dalton, B. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00030 · Cited by 313 · see citing works
The role of immune cells and mediators in preeclampsia
Deer, E. M., Herrock, O., Campbell, N., Cornelius, D. C., Fitzgerald, S. J., Amaral, L. M., & LaMarca, B. B. (2023) · Nature Reviews Nephrology · doi:10.1038/s41581-022-00670-0 · Cited by 308 · see citing works
Pathogenesis of Preeclampsia and Therapeutic Approaches Targeting the Placenta
Jena, M. K., Sharma, N. R., Petitt, M., Maulik, D., & Nayak, N. R. (2020) · Biomolecules · doi:10.3390/biom10060953 · Cited by 269 · see citing works
Romero, R., Erez, O., Hüttemann, M., Maymon, E., Panaitescu, B., Conde-Agudelo, A., Pacora, P., Yoon, B. H., & Grossman, L. I. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.06.003 · Cited by 253 · see citing works
Early prediction of preeclampsia in pregnancy with cell-free RNA
Moufarrej, M. N., Vorperian, S. K., Wong, R. J., Campos, A. A. S., Quaintance, C. C., Sit, R. V., Tan, M., Detweiler, A. M., Mekonen, H. E., Neff, N. F., et al. (2022) · Nature · doi:10.1038/s41586-022-04410-z · Cited by 250 · see citing works
Nitric Oxide and Reactive Oxygen Species in the Pathogenesis of Preeclampsia
Matsubara, K., Higaki, T., Matsubara, Y., & Nawa, A. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms16034600 · Cited by 249 · see citing works
Cytokines as Key Players in the Pathophysiology of Preeclampsia
Raghupathy, R. (2013) · Medical Principles and Practice · doi:10.1159/000354200 · Cited by 235 · see citing works
Association of pro‐ and anti‐inflammatory cytokines in preeclampsia
Aggarwal, R., Jain, A. K., Mittal, P., Kohli, M., Jawanjal, P., & Rath, G. (2019) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.22834 · Cited by 233 · see citing works
Lau, S., Guild, S., Barrett, C. J., Chen, Q., McCowan, L. M. E., Jordan, V., & Chamley, L. (2013) · American Journal of Reproductive Immunology · doi:10.1111/aji.12138 · Cited by 212 · see citing works
Tryptophan metabolism, disposition and utilization in pregnancy
Badawy, A. A.-B. (2015) · Bioscience Reports · doi:10.1042/bsr20150197 · Cited by 204 · see citing works
Gestational Hypoxia and Developmental Plasticity
Ducsay, C. A., Goyal, R., Pearce, W. J., Wilson, S. M., Hu, X., & Zhang, L. (2018) · Physiological Reviews · doi:10.1152/physrev.00043.2017 · Cited by 203 · see citing works
Metabolic profiling of pregnancy: cross-sectional and longitudinal evidence
Wang, Q., Würtz, P., Auro, K. M., Mäkinen, V., Kangas, A. J., Soininen, P., Tiainen, M., Tynkkynen, T., Jokelainen, J. J., Santalahti, K., et al. (2016) · BMC Medicine · doi:10.1186/s12916-016-0733-0 · Cited by 199 · see citing works
The integrative roles of chemokines at the maternal–fetal interface in early pregnancy
Du, M., Wang, S., & Li, D. (2014) · Cellular and Molecular Immunology · doi:10.1038/cmi.2014.68 · Cited by 195 · see citing works
The Role of Inflammation in the Pathogenesis of Preeclampsia
Michalczyk, M., Celewicz, A., Celewicz, M., Woźniakowska-Gondek, P., & Rzepka, R. (2020) · Mediators of Inflammation · doi:10.1155/2020/3864941 · Cited by 193 · see citing works
Eiland, E., Nzerue, C. M., & Faulkner, M. L. (2012) · Journal of Pregnancy · doi:10.1155/2012/586578 · Cited by 192 · see citing works
Brantsæter, A. L., Myhre, R., Haugen, M. A., Myking, S., Sengpiel, V., Magnus, P. M., Jacobsson, B., & Meltzer, H. M. (2011) · American Journal of Epidemiology · doi:10.1093/aje/kwr168 · Cited by 185 · see citing works
Vascular Dysfunction in Preeclampsia
Brennan, L., Morton, J. S., & Davidge, S. T. (2013) · Microcirculation · doi:10.1111/micc.12079 · Cited by 173 · see citing works
Ferguson, K. K., Meeker, J. D., McElrath, T. F., Mukherjee, B., & Cantonwine, D. E. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.12.174 · Cited by 152 · see citing works
Fan, Z., Tang, P., Li, C., Yang, Q., Xu, Y., Su, C., & Li, L. (2023) · Journal of Oral Microbiology · doi:10.1080/20002297.2022.2145729 · Cited by 150 · see citing works
Gestational Diabetes: Implications for Cardiovascular Health
Sullivan, S. D., Umans, J. G., & Ratner, R. (2012) · Current Diabetes Reports · doi:10.1007/s11892-011-0238-3 · Cited by 143 · see citing works
Molvarec, A., Szarka, A., Walentin, S., Bekő, G., Karádi, I., Prohászka, Z., & Rigó, J. J. (2011) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-9-124 · Cited by 138 · see citing works
Self-citationThe imbalance of Th17/Treg axis involved in the pathogenesis of preeclampsia
Eghbal‐Fard, S., Yousefi, M., Heydarlou, H., Ahmadi, M., Taghavi, S., Movasaghpour, A., Jadidi‐Niaragh, F., Yousefi, B., Dolati, S., Hojjat‐Farsangi, M., et al. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27315 · Cited by 137 · see citing works
Is inflammation the cause of pre-eclampsia?
Ramma, W., & Ahmed, A. (2011) · Biochemical Society Transactions · doi:10.1042/bst20110672 · Cited by 135 · see citing works
Torjusen, H., Brantsæter, A. L., Haugen, M. A., Alexander, J., Bakketeig, L. S., Lieblein, G., Stigum, H., Næs, T., Swartz, J., Holmboe‐Ottesen, G., et al. (2014) · BMJ Open · doi:10.1136/bmjopen-2014-006143 · Cited by 127 · see citing works
Pinheiro, M. D. B., Martins‐Filho, O. A., Mota, A. P. L., Alpoim, P. N., Godói, L. C., Silveira, A. C. O., Teixeira‐Carvalho, A., Gomes, K. B., & Dusse, L. M. S. (2013) · Cytokine · doi:10.1016/j.cyto.2013.02.027 · Cited by 125 · see citing works
Maternal Serum Cytokine Concentrations in Healthy Pregnancy and Preeclampsia
Spence, T., Allsopp, P. J., Yeates, A. J., Mulhern, M. S., Strain, J., & McSorley, E. M. (2021) · Journal of Pregnancy · doi:10.1155/2021/6649608 · Cited by 123 · see citing works
Cassidy‐Bushrow, A. E., Peters, R. M., Johnson, D. A., & Templin, T. (2012) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2012.01.007 · Cited by 117 · see citing works
Donahue, J. G., Kieke, B. A., King, J. P., Destefano, F. R., Mascola, M. A., Irving, S. A., Cheetham, T. C., Glanz, J. M., Jackson, L. A., Klein, N. P., et al. (2017) · Vaccine · doi:10.1016/j.vaccine.2017.06.069 · Cited by 112 · see citing works
Progesterone: A Unique Hormone with Immunomodulatory Roles in Pregnancy
Raghupathy, R., & Szekeres‐Barthó, J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031333 · Cited by 112 · see citing works
Early pregnancy immune biomarkers in peripheral blood may predict preeclampsia
Garcia, M. D. S., Mobley, Y. R., Henson, J. T., Davies, M., Skariah, A. M., Dambaeva, S. V., Gilman‐Sachs, A., Beaman, K. D., Lampley, E. C., & Kwak-Kim, J. Y.-H. (2017) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2017.10.048 · Cited by 111 · see citing works
A meta-analysis of tumor necrosis factor-alpha, interleukin-6, and interleukin-10 in preeclampsia
Xie, C., Yao, M. Z., Liu, J. B., & Xiong, L. (2011) · Cytokine · doi:10.1016/j.cyto.2011.09.021 · Cited by 110 · see citing works
Evaluation of maternal systemic inflammatory response in preeclampsia
Mihu, D., Ciortea, R., Măluţan, A. M., & Mihaela, C. (2015) · Taiwanese Journal of Obstetrics and Gynecology · doi:10.1016/j.tjog.2014.03.006 · Cited by 107 · see citing works
Cotechini, T., & Graham, C. H. (2015) · Placenta · doi:10.1016/j.placenta.2015.05.016 · Cited by 107 · see citing works
Chronic hypertension and superimposed preeclampsia: screening and diagnosis
Kametas, N. A., Nzelu, D., & Nicolaides, K. H. (2021) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.11.029 · Cited by 105 · see citing works
Choudhury, R., Dunk, C., Lye, S. J., Aplin, J., Harris, L. K., & Jones, R. L. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601175 · Cited by 103 · see citing works
Kim, Y. M., Chaemsaithong, P., Romero, R. J., Shaman, M., Kim, C. J., Kim, J.-S., Qureshi, F., Jacques, S. M., Ahmed, A. I., Chaiworapongsa, T., et al. (2014) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2014.976198 · Cited by 103 · see citing works
Interplay of cytokines in preterm birth
Pandey, M., Chauhan, M., & Awasthi, S. (2017) · The Indian Journal of Medical Research · doi:10.4103/ijmr.ijmr_1624_14 · Cited by 98 · see citing works
Gong, P., Liu, M., Hong, G., Li, Y., Xue, P., Zheng, M., Wu, M., Shen, L., Yang, M., Diao, Z., et al. (2016) · Placenta · doi:10.1016/j.placenta.2016.03.002 · Cited by 96 · see citing works
Xue, P., Zheng, M., Gong, P., Lin, C., Zhou, J., Li, Y., Shen, L., Diao, Z., Yan, G., Sun, H., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0124001 · Cited by 96 · see citing works
Tian, M., Zhang, Y., Liu, Z., Sun, G., Mor, G., & Liao, A. (2016) · Scientific Reports · doi:10.1038/srep27683 · Cited by 96 · see citing works
Vitamin D and Inflammatory Cytokines in Healthy and Preeclamptic Pregnancies
Barrera, D., Dı́az, L., Noyola-Martínez, N., & Halhali, A. (2015) · Nutrients · doi:10.3390/nu7085293 · Cited by 89 · see citing works
Wnt/β-catenin signaling pathway in trophoblasts and abnormal activation in preeclampsia
Zhang, Z., Wang, X., Zhang, L., Shi, Y., Wang, J., & Yan, H. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.6718 · Cited by 87 · see citing works
Rolfo, A., Giuffrida, D., Nuzzo, A. M., Pierobon, D., Cardaropoli, S., Piccoli, E., Giovarelli, M., & Todros, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059403 · Cited by 87 · see citing works
CD74-Downregulation of Placental Macrophage-Trophoblastic Interactions in Preeclampsia
Przybył, Ł., Haase, N., Golić, M., Rugor, J., Solano, M. E., Arck, P., Gauster, M., Huppertz, B., Emontzpohl, C., Stoppe, C., et al. (2016) · Circulation Research · doi:10.1161/circresaha.116.308304 · Cited by 86 · see citing works
Vitamin D Effects on the Immune System from Periconception through Pregnancy
Schröder‐Heurich, B., Springer, C., & von Versen‐Höynck, F. (2020) · Nutrients · doi:10.3390/nu12051432 · Cited by 83 · see citing works
Inflammatory cytokines in aqueous humor of patients with choroidal neovascularization.
Miao, H., Tao, Y. K., & Li, X. (2012) · PubMed Central · Cited by 83 · see citing works
Relationship between Maternal Immunological Response during Pregnancy and Onset of Preeclampsia
Martínez‐Varea, A., Pellicer, B., Alfredo Perales, M., & Pellicer, A. (2014) · Journal of Immunology Research · doi:10.1155/2014/210241 · Cited by 82 · see citing works
Zhao, X., Fang, R., Yu, R., Chen, D., Zhao, J., & Xiao, J. (2017) · Nutrients · doi:10.3390/nu9020138 · Cited by 81 · see citing works
Inflammatory Markers and Preeclampsia
Black, K. D., & Horowitz, J. A. (2018) · Nursing Research · doi:10.1097/nnr.0000000000000285 · Cited by 81 · see citing works
The Role of Oxidative Stress, Adhesion Molecules and Antioxidants in Preeclampsia
Haram, K., Mortensen, J. H. S., Myking, O. L., Magann, E. F., & Morrison, J. C. (2019) · Current Hypertension Reviews · doi:10.2174/1573402115666190119163942 · Cited by 80 · see citing works
Peraçoli, J. C., Castro, C. F. B., Romão‐Veiga, M., Weel, I. C., Ribeiro, V. R., Borges, V. T. M., Rudge, M. V. C., Witkin, S. S., & Peraçoli, M. T. S. (2013) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2013.08.003 · Cited by 78 · see citing works
Increased circulating interleukin-17 levels in preeclampsia
Molvarec, A., Czegle, I., Szijártó, J., & Rigó, J. J. (2015) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2015.05.007 · Cited by 77 · see citing works
Self-citationThe Adaptation of the Cerebral Circulation to Pregnancy: Mechanisms and Consequences
Cipolla, M. J. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2012.210 · Cited by 76 · see citing works
Transforming growth factor β signaling in uterine development and function
Li, Q. (2014) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/2049-1891-5-52 · Cited by 76 · see citing works
Xiao, J., Yin, Y., Gao, Y., Lau, S., Shen, F., Zhao, M., & Chen, Q. (2012) · Cytokine · doi:10.1016/j.cyto.2012.07.039 · Cited by 74 · see citing works
Perucci, L. O., Gomes, K. B., Freitas, L. G., Godói, L. C., Alpoim, P. N., Pinheiro, M. D. B., de Miranda, A. S., Teixeira, A. L., Dusse, L. M. S., & Sousa, L. P. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097632 · Cited by 73 · see citing works
Interleukin-1 family cytokines and their regulatory proteins in normal pregnancy and pre-eclampsia
Southcombe, J. H., Redman, C. W. G., Sargent, I. L., & Granne, I. (2015) · Clinical & Experimental Immunology · doi:10.1111/cei.12608 · Cited by 71 · see citing works
Amash, A., Holcberg, G., Sapir, O., & Huleihel, M. (2012) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2012.0013 · Cited by 70 · see citing works
Noyola-Martínez, N., Dı́az, L., Avila, E., Halhali, A., Larrea, F., & Barrera, D. (2012) · Cytokine · doi:10.1016/j.cyto.2012.10.001 · Cited by 69 · see citing works
Doppler ultrasound evaluation in preeclampsia
Lopez-Mendez, M. A., Martínez-Gaytán, V., Flores, R. C., Ramos-González, R., Ochoa-Torres, M., Veloz, I. G., Martinez-Acuña, M. I., Badillo-Almaraz, J. I., & Martínez‐Fierro, M. L. (2013) · BMC Research Notes · doi:10.1186/1756-0500-6-477 · Cited by 66 · see citing works
The Cerebral Circulation During Pregnancy: Adapting to Preserve Normalcy
Johnson, A. C., & Cipolla, M. J. (2015) · Physiology · doi:10.1152/physiol.00048.2014 · Cited by 66 · see citing works
Placental ABC transporters, cellular toxicity and stress in pregnancy
Aye, I. L. M. H., & Keelan, J. A. (2013) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2013.03.007 · Cited by 66 · see citing works
Murthi, P., Pinar, A. A., Dimitriadis, E., & Samuel, C. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041406 · Cited by 66 · see citing works
The role of arginine, homoarginine and nitric oxide in pregnancy
Khalil, A. A., Hardman, L., & O’Brien, P. (2015) · Amino Acids · doi:10.1007/s00726-015-2014-1 · Cited by 65 · see citing works
Zhang, W., Zhou, Y., & Ding, Y. (2017) · American Journal of Reproductive Immunology · doi:10.1111/aji.12647 · Cited by 63 · see citing works
Maternal ABO blood group and adverse pregnancy outcomes
Phaloprakarn, C., & Tangjitgamol, S. (2012) · Journal of Perinatology · doi:10.1038/jp.2012.73 · Cited by 62 · see citing works
Sun, Y., Gu, J. F., Tan, X. B., WANG, C. F., Jia, X., Feng, L., & Liu, J. P. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.4725 · Cited by 61 · see citing works
Lymphocytes immunotherapy for preserving pregnancy: Mechanisms and Challenges
Hajipour, H., Nejabati, H. R., Latifi, Z., Hamdi, K., Bahrami‐Asl, Z., Fattahi, A., & Nouri, M. (2018) · American Journal of Reproductive Immunology · doi:10.1111/aji.12853 · Cited by 61 · see citing works
Pinheiro, M. D. B., Gomes, K. B., Ronda, C. R. S. C., Guimarães, G. G., Freitas, L. G., Teixeira‐Carvalho, A., Martins‐Filho, O. A., & Dusse, L. M. S. (2014) · Cytokine · doi:10.1016/j.cyto.2014.10.021 · Cited by 60 · see citing works
Guzman, N. A., & Phillips, T. M. (2011) · Electrophoresis · doi:10.1002/elps.201000700 · Cited by 60 · see citing works
MiRNA‐548c‐5p downregulates inflammatory response in preeclampsia via targeting PTPRO
Wang, Z., Wang, P., Wang, Z., Qin, Z., Xiu, X., Xu, D., Zhang, X., & Wang, Y. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27758 · Cited by 60 · see citing works
Monocytes from Pregnant Women with Pre-Eclampsia are Polarized to a M1 Phenotype
de Medeiros, L. T. L., Peraçoli, J. C., Castro, C. F. B., Romão‐Veiga, M., Weel, I. C., Golim, M. D. A., Oliveira, L. G., Kurokawa, C. S., Borges, V. T. M., & Peraçoli, M. T. S. (2014) · American Journal of Reproductive Immunology · doi:10.1111/aji.12222 · Cited by 59 · see citing works
Molvarec, A., Szarka, A., Walentin, S., Bekő, G., Karádi, I., Prohászka, Z., & Rigó, J. J. (2011) · Clinica Chimica Acta · doi:10.1016/j.cca.2011.06.042 · Cited by 58 · see citing works
Self-citationFirst and second trimester immune biomarkers in preeclamptic and normotensive women
Taylor, B. D., Ness, R. B., Klebanoff, M. A., Zoh, R. S., Bass, D. C., HOUGAARD, D. M., Skogstrand, K., & Haggerty, C. L. (2016) · Pregnancy Hypertension · doi:10.1016/j.preghy.2016.09.002 · Cited by 58 · see citing works
Circulating microparticles in severe preeclampsia
Marques, F. K., Campos, F. M. F., Martins‐Filho, O. A., Teixeira‐Carvalho, A., Dusse, L. M. S., & Gomes, K. B. (2012) · Clinica Chimica Acta · doi:10.1016/j.cca.2012.09.023 · Cited by 57 · see citing works
IL-10, TNF-α & IFN-γ: Potential early biomarkers for preeclampsia
Kumar, A., Begum, N., Prasad, S., Agarwal, S., & Sharma, S. B. (2013) · Cellular Immunology · doi:10.1016/j.cellimm.2013.06.012 · Cited by 57 · see citing works
Holtan, S. G., Chen, Y., Kaimal, R., Creedon, D. J., Enninga, E. A. L., Nevala, W. K., & Markovic, S. N. (2015) · Journal of Immunology Research · doi:10.1155/2015/952571 · Cited by 57 · see citing works
Maternal monocytes in pregnancy and preeclampsia in humans and in rats
Faas, M. M., & de Vos, P. (2016) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2016.06.009 · Cited by 57 · see citing works
Immune system activation in the pathogenesis of posterior reversible encephalopathy syndrome
Chen, Z., Shen, G., Lerner, A., & Gao, B. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.03.012 · Cited by 57 · see citing works
Distinct First Trimester Cytokine Profiles for Gestational Hypertension and Preeclampsia
Tangerås, L. H., Austdal, M., Skråstad, R. B., Salvesen, K. Å., Austgulen, R., Bathen, T. F., & Iversen, A. (2015) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.115.305817 · Cited by 56 · see citing works
Mid-pregnancy circulating immune biomarkers in women with preeclampsia and normotensive controls
Taylor, B. D., Tang, G., Ness, R. B., Olsen, J., HOUGAARD, D. M., Skogstrand, K., Roberts, J. M., & Haggerty, C. L. (2015) · Pregnancy Hypertension · doi:10.1016/j.preghy.2015.11.002 · Cited by 56 · see citing works
In vivo immune signatures of healthy human pregnancy: Inherently inflammatory or anti-inflammatory?
Graham, C., Chooniedass, R., Stefura, W. P., Becker, A. B., Sears, M. R., Turvey, S. E., Mandhane, P. J., Subbarao, P., CHILD Study Investigators, & HayGlass, K. T. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177813 · Cited by 56 · see citing works
Relationship between Maternal Serum C-Reactive Protein, Funisitis and Early-Onset Neonatal Sepsis
Lee, S. Y., Park, K. H., Jeong, E. H., Oh, K. J., Ryu, A., & Park, K. U. (2012) · Journal of Korean Medical Science · doi:10.3346/jkms.2012.27.6.674 · Cited by 55 · see citing works
The tryptophan utilization concept in pregnancy
Badawy, A. A. ‐. (2014) · Obstetrics & Gynecology Science · doi:10.5468/ogs.2014.57.4.249 · Cited by 55 · see citing works
Pregnant serum induces neuroinflammation and seizure activity via TNFα
Cipolla, M. J., Pusic, A. D., Grinberg, Y. Y., Chapman, A. C., Poynter, M. E., & Kraig, R. P. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.01.005 · Cited by 53 · see citing works
Li, M., Wu, Z., Yang, H., & Huang, S.-T. J. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0055 · Cited by 53 · see citing works
Equils, O., Kellogg, C., McGregor, J., Gravett, M. G., Neal-Perry, G. S., & Gabay, C. (2020) · Biology of Reproduction · doi:10.1093/biolre/ioaa102 · Cited by 53 · see citing works
Broekhuizen, M., Hitzerd, E., van den Bosch, T. P. P., Dumas, J., Verdijk, R. M., van Rijn, B. B., Danser, A. H. J., van Eijck, C. H. J., Reiss, I. K. M., & Mustafa, D. A. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.780043 · Cited by 52 · see citing works
Guan, X., Fu, Y., Liu, Y., Cui, M., Zhang, C., Zhang, Q., Li, C., Zhao, J., Wang, C., Song, J., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1156039 · Cited by 52 · see citing works
Biomarkers for the management of pre-eclampsia in pregnant women.
Petla, L. T., Chikkala, R., Ratnakar, K. S., Kodati, V., & Sritharan, V. (2013) · Europe PMC (PubMed Central) · Cited by 52 · see citing works
Relationship between ABO blood group and pregnancy complications: a systematic literature analysis.
Franchini, M., Mengoli, C., & Lippi, G. (2016) · Europe PMC (PubMed Central) · doi:10.2450/2016.0313-15 · Cited by 52 · see citing works
Huang, C.-C., Hsueh, Y., Chang, C., Hsu, H.-C., Yang, T., Lin, W.-C., & Chang, H. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1200330 · Cited by 51 · see citing works
Functional Toll-like receptors in primary first-trimester trophoblasts
Tangerås, L. H., Stødle, G. S., Olsen, G. D., Leknes, A.-H., Gundersen, A. S., Skei, B., Vikdal, A. J., Ryan, L., Steinkjer, B., Myklebost, M. F., et al. (2014) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2014.04.004 · Cited by 51 · see citing works
Ramma, W., Buhimschi, I. A., Zhao, G., Dulay, A. T., Nayeri, U. A., Buhimschi, C. S., & Ahmed, A. (2012) · Angiogenesis · doi:10.1007/s10456-012-9261-5 · Cited by 51 · see citing works
Maharaj, N. R., Phulukdaree, A., Nagiah, S., Ramkaran, P., Tiloke, C., & Chuturgoon, A. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170063 · Cited by 51 · see citing works
Neuromyelitis optica spectrum disorders and pregnancy: Interactions and management
Shosha, E., Pittock, S. J., Flanagan, E. P., & Weinshenker, B. G. (2017) · Multiple Sclerosis Journal · doi:10.1177/1352458517740215 · Cited by 51 · see citing works
Adekola, H., Romero, R. J., Chaemsaithong, P., Korzeniewski, S. J., Dong, Z., Yeo, L., Hassan, S. S., & Chaiworapongsa, T. (2014) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2014.964676 · Cited by 50 · see citing works
- Authors
- Szarka, A., Rigó, J., Lázár, L., Bekő, G., & Molvarec, A.
- Affiliations
- Semmelweis University (HU)
- Corresponding author
- Molvarec, Attila
- Venue
- BMC Immunology
- Published
- 2010-12
- Volume
- 11
- Issue
- 1
- Pages
- 59-59
- ISSN
- 1471-2172 (ISSN-L)
- PMC
- PMC3014878
- OpenAlex
- W2079231160
- Cited by
- 516
- References
- 46
- Citations by year
- 2026: 7 · 2025: 29 · 2024: 27 · 2023: 31 · 2022: 28 · 2021: 30 · 2020: 45 · 2019: 31 · 2018: 37 · 2017: 37 · 2016: 33 · 2015: 47 · 2014: 48 · 2013: 34 · 2012: 34
- FWCI
- 37.65
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- BMC Immunology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Semmelweis Egyetem
- Magyar Tudományos Akadémia
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Epidemiology › Preterm Birth and Chorioamnionitis
- Keywords
- preeclampsia, normal pregnancy, serum cytokines, chemokines, adhesion molecules, systemic inflammation, Th1/Th2 balance, IL-18, IL-12p70, CXCL10, MCP-1, ICAM-1, VCAM-1, TNF-α, interleukin-6, oxidative stress, endothelial activation, trophoblast
- MeSH terms
- Adult, C-Reactive Protein, Enzyme-Linked Immunosorbent Assay, Female, Fibronectins, Humans, Inflammation, Pre-Eclampsia, Pregnancy, von Willebrand Factor, Cell Adhesion Molecules, Cytokines, Oxidative Stress, Microarray Analysis, Th1-Th2 Balance
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
