The DOI matches its Crossref record; 45 of the 46 references it cites were found in a registry or an index.
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.
Overview
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
Figures
Verification
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?
In the citing paper
“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.
Citations
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
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
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
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
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
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
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 1,319
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
Inflammation, free radicals, and antioxidants
Conner, E. M., & Grisham, M. B. (1996) · Nutrition · doi:10.1016/s0899-9007(96)00000-8 · Cited by 707
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
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
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
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
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
Greer, I. A., Lyall, F., Perera, T., Boswell, F., & Macara, L. (1994) · PubMed · Cited by 262
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
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
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
Rusterholz, C., Hahn, S., & Holzgreve, W. (2007) · Seminars in Immunopathology · doi:10.1007/s00281-007-0071-6 · Cited by 198
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 167
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
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 144
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
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
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
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
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
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
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
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
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 68
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
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
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
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
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
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
Self-citationAggarwal, P. K., Jain, V., & Jha, V. (2010) · Hypertension Research · doi:10.1038/hr.2010.23 · Cited by 54
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
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
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
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
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
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
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
Self-citation
Research works printed but not linked: 1
- Joubert K: Standards of the body mass and body length of birth in Hungary on the basis of the 1990-1996 nation-wide liveborn data. Magy Noorv L. 2000, 63: 155-163.
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 662
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 444
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
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
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 316
Metadata
- 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 › Obstetrics and Gynecology › 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
