Expression of MMIF, HIF-1α and VEGF in Serum and Endometrial Tissues of Patients with Endometriosis

article OA: closed CC0 ⤵ 24 in-corpus citations
AI-generated summary by gemini-2.5-flash-lite+body, 2026-06-28

Serum and endometrial expression of MMIF, HIF-1α, and VEGF are significantly elevated in endometriosis patients and correlate with disease stage and dysmenorrhea severity.

One-sentence paraphrase of the abstract; not a substitute for reading it. No clinical advice. How this works

AI-generated deep summary by claude@2026-06, 2026-06-07 · read from full text

This study measured macrophage migration inhibitory factor (MMIF), hypoxia-inducible factor-1α (HIF-1α), and vascular endothelial growth factor (VEGF) levels in serum using ELISA and in endometrial tissues using Western blotting in 80 patients with endometriosis (staged by R-AFS I–IV) grouped by dysmenorrhea severity, alongside 40 healthy controls. Serum concentrations and tissue expression of all three proteins were significantly higher in endometriosis patients than controls, and increased with both R-AFS stage and dysmenorrhea severity. The authors reported that combining serum MMIF, HIF-1α, and VEGF improved sensitivity and specificity compared with each marker alone. The paper’s main limitation is that it reports associations without establishing causality between these molecular markers and disease progression or symptom severity. This paper is centrally about endometriosis — it focuses on expression patterns of MMIF, HIF-1α, and VEGF in serum and endometrial tissues and their clinical association with disease stage and dysmenorrhea severity.

Read from the paper's body, not the abstract. Not a substitute for reading the paper. No clinical advice. How this works

Abstract

The aim of this study was to investigate the expression of macrophage migration inhibitory factor (MMIF), hypoxia-inducible factor-1 a (HIF-1α) and vascular endothelial growth factor (VEGF) in the serum and endometrial tissues of patients with endometriosis (EM) and the clinical significance. Eighty EM patients [American Reproductive Association stage I (n=20), stage II (n=22), stage III (n=21) and stage IV (n=17)] were enrolled and divided into mild (10-14 points, n=28), moderate (16-24 points, n=27) and severe (26-30 points, n=25) dysmenorrhea groups. The control group included 40 healthy women of childbearing age who underwent routine healthcare examinations in the enrolment period. The expression of MMIF, HIF-1α and VEGF in the serum and endometrial tissues was measured by enzyme-linked immunosorbent assay and Western blotting, respectively. Meanwhile, the sensitivity and specificity of serum MMIF, HIF-1α, and VEGF when separately used as single indexes or jointly used as one index were examined as well. The results showed that serum concentrations of MMIF, HIF-1α, and VEGF were significantly higher in EM patients than in controls (P<0.05). The expression of all three proteins in both serum and endometrial tissues increased significantly with the R-AFS stage (P<0.05) and with dysmenorrheal severity (P<0.05). The sensitivity and specificity of the combined detection of serum MMIF, HIF-1α, and VEGF levels were significantly higher than those of single index detection (P<0.05). In conclusion, the expression of MMIF, HIF-1α, and VEGF in the serum and endometrial tissues may be used to assess the stage of EM and the severity of dysmenorrhea. Combined evaluation of MMIF, HIF-1α, and VEGF significantly improves the diagnostic sensitivity and specificity.
Full text 7,750 characters · extracted from oa-doi-fallback · click to expand
Summary The aim of this study was to investigate the expression of macrophage migration inhibitory factor (MMIF), hypoxia-inducible factor-1 a (HIF-1α) and vascular endothelial growth factor (VEGF) in the serum and endometrial tissues of patients with endometriosis (EM) and the clinical significance. Eighty EM patients [American Reproductive Association stage I (n=20), stage II (n=22), stage III (n=21) and stage IV (n=17)] were enrolled and divided into mild (10-14 points, n=28), moderate (16-24 points, n=27) and severe (26-30 points, n=25) dysmenorrhea groups. The control group included 40 healthy women of childbearing age who underwent routine healthcare examinations in the enrolment period. The expression of MMIF, HIF-1α and VEGF in the serum and endometrial tissues was measured by enzyme-linked immunosorbent assay and Western blotting, respectively. Meanwhile, the sensitivity and specificity of serum MMIF, HIF-1α, and VEGF when separately used as single indexes or jointly used as one index were examined as well. The results showed that serum concentrations of MMIF, HIF-1α, and VEGF were significantly higher in EM patients than in controls (P<0.05). The expression of all three proteins in both serum and endometrial tissues increased significantly with the R-AFS stage (P<0.05) and with dysmenorrheal severity (P<0.05). The sensitivity and specificity of the combined detection of serum MMIF, HIF-1α, and VEGF levels were significantly higher than those of single index detection (P<0.05). In conclusion, the expression of MMIF, HIF-1α, and VEGF in the serum and endometrial tissues may be used to assess the stage of EM and the severity of dysmenorrhea. Combined evaluation of MMIF, HIF-1α, and VEGF significantly improves the diagnostic sensitivity and specificity. Similar content being viewed by others References Psaroudakis D, Hirsch M, Davis C. Review of the management of ovarian endometriosis: paradigm shift towards conservative approaches. Curr Opin Obstet Gynecol, 2014,26(4):266–274 Dancet EA, Apers S, Kremer JA, et al. The patientcenteredness of endometriosis care and targets for improvement: a systematic review. Gynecol Obstet Invest, 2014,78(2): 69–80 Veillat V, Sengers V, Metz CN, et al. Macrophage migration inhibitory factor is involved in a positive feedback loop increasing aromatase expression in endometriosis. Am J Pathol, 2012,181(3):917–927 Serrano-Oviedo L, Giménez-Bachs JM, Nam-Cha SY, et al. Implication of VHL, ERK5, and HIF-1 alpha in clear cell renal cell carcinoma: Molecular basis. Urol Oncol, 2017,35(3):el5–e22 Xu H, Zhang T, Man GC, et al. Vascular endothelial growth factor C is increased in endometrium and promotes endothelial functions, vascular permeability and angiogenesis and growth of endometriosis. Angiogenesis, 2013,16(3):541–551 Stilley JA, Birt JA, Sharpe-Timms KL. Cellular and molecular basis for endometriosis-associated infertility. Cell Tissue Res, 2012,349(3):849–862 Gregoric P, Doklestic K, Pandurovic M, et al. Distal ideal endometriosis as a cause of ileus: a case report. Srp Arh Celok Lek, 2012,140(3-4):225–228 Mei J, Xie XX, Li MQ, et al. Indoleamine 2, 3-dioxygenase-l (IDOl) in human endometrial stromal cells induces macrophage tolerance through interleukin-33 in the progression of endometriosis. Int J Clin Exp Pathol, 2014,7(6):2743–2757 Pirdel L, Pirdel M. Role of iron overload-induced macrophage apoptosis in the pathogenesis of peritoneal endometriosis. Reproduction, 2014,147(6):R199–R207 Lin W, Chen S, Li M, et al. Expression of macrophage migration inhibitory factor in human endometriosis: relation to disease stage, menstrual cycle and infertility. J Obstet Gynaecol Res, 2010,36(2):344–351 Pan X, Mao X, Cheng T, et al. Macrophage migration inhibitiory factor: a regular of MMP13 and inflammation in titanium particles stimulated air pouch in vivo. Mol Cell Biochem, 2011,357(1-2):313–321 Baron N, Deuster O, Noelker C, et al. Role of macrophage migration inhibitory factor in primary glioblastoma multiforme cells. J Neurosci Res, 2011,89(5):711–717 Ajdukovic J. HIF-l-a big chapter in the cancer tale. Exp Oncol, 2016,38(1):9–12 Eslavath RK, Sharma D, Bin Omar NA, et al. P-N-oxalyl-L-a, P-diaminopropionic acid induces HRE expression by inhibiting HIF-prolyl hydroxylase-2 in normoxic conditions. Eur J Pharmacol, 2016,791:405–411 Li J, Mi C, Ma J, et al. Dihydrotanshinone I inhibits the translational expression of hypoxia-inducible factor-la. Chem Biol Interact, 2015,240(5):48–58 El-Naggar AM, Veinotte CJ, Cheng H, et al. Translational activation of HIF1α by YB-1 promotes sarcoma metastasis. Cancer Cell, 2015,27(5):682–697 Critchley HO, Osei J, Henderson TA, et al. Hypoxiainducible factor-1 alpha expression in human endometrium and its regulation by prostaglandin E-series prostanoid receptor 2(EP2). Endocrinology, 2006,147(2):744–753 Goteri G, Lucarini G, Zizzi A, et al. Proangiogenetic molecules, hypoxia-inducible factor-1 alpha and nitric oxide synthase isoforms in ovarian endometriotic cysts. Virchows Arch, 2010,456(6):703–710 Wu MH, Lu CW, Chang FM, et al. Estrogen receptor expression affected by hypoxia inducible factor-la in stromal cells from patients with endometriosis. Taiwan J Obstet Gynecol, 2012,51(2):50–54 Kim KH, Kim HY, Kim HH, et al. Hypoxia induces expression of COX-2 through the homeodomain transcription factor CDX1 and orphan nuclear receptor SHP in human endometrial cells. Mol Hum Reprod, 2011,17(3):710–719 Hsiao KY, Chang N, Lin SC, et al. Inhibition of dual specificity phosphatase-2 by hypoxia promotes interleukin-8-mediated angiogenesis in endometriosis. Hum Reprod, 2014,29(2):2747–2755 Courtnay R, Ngo DC, Malik N, et al. Cancer metabolism and the Warburg effect: the role of HIF-1 and PI3K. Mol Biol Rep, 2015,42(5):841–851 Denko NC. Hypoxia HIFI and glucose metabolism in the solid tumour. Nat Rev Cancer, 2008,8(2):705–713 Cho S, Choi YS, Jeon YE, et al. Expression of vascular endothelial growth factor (VEGF) and its soluble receptor-1 inendometriosis. Microvasc Res, 2012,83(2):237–242 Leone R Maggiore U, Ferrero S. Methodological concerns regarding levels of vascular endothelial growth factor (VEGF) in serum of women with endometriosis. Int J Fertil Steril, 2015,8(4):485–486 Fang F, Gong L, Wang X, et al. The association between vascular endothelial growth factor (VEGF) +405G>C genetic polymorphism and endometriosis. Exp Biol Med, 2015,240(9): 1177–1182 Gonçalves GA, Camargo-Kosugi CM, Bonetti TC, etal. p27kipl overexpression regulates VEGF expression, cell proliferation and apoptosis in cell culture from eutopic endometrium of women with endometriosis. Apoptosis, 2015,20(3):327–335 Huang F, Wang H, Zou Y, et al. Effect of GnRH-II on the ESC proliferation, apoptosis and VEGF secretion in patients withendometriosis in vitro. Int J Clin Exp Pathol, 2013,6(ll):2487–2496 Li YZ, Wang LJ, Li X, et al. Vascular endothelial growth factor gene polymorphisms contribute to the risk of endometriosis: an updated systematic review and meta-analysis of 14 case-control studies. Genet Mol Res, 2013,12(2): 1035–1044 Barcz E, Milewski L, Dziunycz P, et al. Peritoneal cytokines and adhesion formation in endometriosis: an inverse association with vascular endothelial growth factor concentration. Fertil Steril, 2012,97(6): 1380–1386 Author information Authors and Affiliations Corresponding author Rights and permissions About this article Cite this article Zhang, F., Liu, Xl., Wang, W. et al. Expression of MMIF, HIF-1α and VEGF in Serum and Endometrial Tissues of Patients with Endometriosis. CURR MED SCI 38, 499–504 (2018). https://doi.org/10.1007/s11596-018-1906-1 Received: Revised: Published: Version of record: Issue date: DOI: https://doi.org/10.1007/s11596-018-1906-1

Text is read by the "Ask this paper" AI Q&A widget below. Extraction quality varies by source — PMC NXML preserves structure cleanly, OA-HTML may include some navigation residue, and OA-PDF can have broken hyphenation. The publisher copy (via DOI) is the canonical version.

My notes (saved in your browser only)

Ask this paper AI returns verbatim quotes from the full text · source: oa-doi-fallback

Answers must be backed by verbatim quotes from this paper's full text. Hallucinated quotes are dropped automatically; if no verbatim passage answers the question, we say so. How this works

Condition tags

endometriosis

MeSH descriptors

Endometriosis Endometrium Endometrium Hypoxia-Inducible Factor 1, alpha Subunit Intramolecular Oxidoreductases Macrophage Migration-Inhibitory Factors Vascular Endothelial Growth Factor A Adult Case-Control Studies Endometriosis Endometrium Female Humans Hypoxia-Inducible Factor 1, alpha Subunit Intramolecular Oxidoreductases Macrophage Migration-Inhibitory Factors Sensitivity and Specificity Vascular Endothelial Growth Factor A

Citation neighborhood

Papers in the corpus that this work cites (lower rings, blue) and that cite this one (upper rings, green). Dot size scales with the paper's in-corpus citation count — bigger dot = more influential within the endo/adeno field. Click a dot to open that paper. [ expand to 2 hops ] — adds papers reached through this work's immediate citers/citees. Heavier; up to 60 extra dots.

References (30)

Cited by (30)

Source provenance

europepmc
last seen: 2026-09-11T06:15:56.568227+00:00
openalex
last seen: 2026-06-10T17:14:06.276822+00:00
pubmed
last seen: 2026-05-13T22:19:37.156494+00:00
License: CC0 · commercial use OK