{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,6]],"date-time":"2026-11-06T18:59:30Z","timestamp":1793991570496,"version":"4.8.0"},"reference-count":36,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2022,7,12]],"date-time":"2022-07-12T00:00:00Z","timestamp":1657584000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Background and Objectives: Endometriosis is a benign, chronic disease, that negatively influences the quality of life of affected women and is responsible for a remarkable amount of infertility. The pathophysiology of the disease is still not clarified, but the insufficient immune surveillance plays a significant role in it. The phagocyte function of innate immune cells may play a role in the elimination of ectopic endometrium. The purpose of this study is to examine the phagocyte function of neutrophil granulocytes and monocytes, incubated in heat-inactivated and not-inactivated plasma samples from healthy women and from women with endometriosis before and after the surgical treatment. Materials and Methods: Blood samples were collected from eight preoperative and eight postoperative patients with endometriosis before and after the surgical treatment, and from 16 healthy patients as controls. Neutrophil granulocytes, monocytes and blood plasma samples were isolated. Cells were incubated in different plasma samples, and the phagocytic index was determined with a fluorescence microscope. Results: The phagocytic index of granulocytes and monocytes isolated from patients with endometriosis was significantly decreased compared to healthy women after the cells were incubated in their own plasma. Preoperatively isolated cells from patients with endometriosis demonstrated an improved phagocyte function after incubating them in plasma samples from healthy controls. In contrast, the phagocytic activity of cells from healthy women significantly reduced after being incubated in the plasma of preoperative endometriosis patients. The heat-inactivation of plasma samples did not affect the results. Conclusions: Active endometriosis lesions may produce heat-stable systemic immunomodulatory factors, which reduced the phagocyte function of peripheral monocytes and neutrophil granulocytes. The phagocyte function of these cells can be normalized after the complete surgical removal of endometriosis, which then demonstrates similar values as in healthy women.<\/jats:p>","DOI":"10.3390\/medicina58070925","type":"journal-article","created":{"date-parts":[[2022,7,12]],"date-time":"2022-07-12T20:52:41Z","timestamp":1657659161000},"page":"925","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Evaluating the Phagocytic Index of Peripheral Leukocytes in Endometriosis by Plasma Experiments"],"prefix":"10.3390","volume":"58","author":[{"given":"Luca","family":"Luk\u00e1cs","sequence":"first","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Medicine, University of Debrecen, 4031 Debrecen, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna Rebeka","family":"Kov\u00e1cs","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Medicine, University of Debrecen, 4031 Debrecen, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"L\u00e1szl\u00f3","family":"P\u00e1l","sequence":"additional","affiliation":[{"name":"Department of Public Health and Epidemiology, Faculty of Medicine, University of Debrecen, 4028 Debrecen, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4672-4066","authenticated-orcid":false,"given":"S\u00e1ndor","family":"Sz\u0171cs","sequence":"additional","affiliation":[{"name":"Department of Public Health and Epidemiology, Faculty of Medicine, University of Debrecen, 4028 Debrecen, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8230-7692","authenticated-orcid":false,"given":"Rudolf","family":"Lamp\u00e9","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Medicine, University of Debrecen, 4031 Debrecen, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,7,12]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1382","DOI":"10.1111\/j.1471-0528.2008.01878.x","article-title":"Can symptomatology help in the diagnosis of endometriosis? Findings from a national case-control study-Part 1","volume":"115","author":"Ballard","year":"2008","journal-title":"BJOG"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1038\/nrendo.2013.255","article-title":"Endometriosis: Pathogenesis and treatment","volume":"10","author":"Vercellini","year":"2013","journal-title":"Nat. Rev. Endocrinol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1426","DOI":"10.1556\/OH.2013.29699","article-title":"The impact of endometriosis on quality of life in Hungary","volume":"154","author":"Bokor","year":"2013","journal-title":"Orv. Hetil."},{"key":"ref_4","first-page":"349","article-title":"Endometriosis still a challenge","volume":"7","author":"Mehedintu","year":"2014","journal-title":"J. Med. Life"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s10397-021-01096-5","article-title":"Medical and surgical interventions to improve the quality of life for endometriosis patients: A systematic review","volume":"18","author":"Saponara","year":"2021","journal-title":"Gynecol. Surg."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/s00404-021-06243-z","article-title":"Impact of endometriosis on obstetric outcome after natural conception: A Multicenter Italian study","volume":"305","author":"Berlanda","year":"2021","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_7","first-page":"31","article-title":"Endometriosis and adverse pregnancy outcome\u2014Minerva","volume":"74","author":"Sorrentino","year":"2022","journal-title":"Obstet. Gynecol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1007\/s43032-020-00370-9","article-title":"Metabolic Profile of Patients with Severe Endometriosis: A Prospective Experimental Study","volume":"28","author":"Murgia","year":"2020","journal-title":"Reprod. Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1016\/S0015-0282(98)00355-0","article-title":"The performance of CA-125 measurement in the detection of endometriosis: A meta-analysis","volume":"70","author":"Mol","year":"1998","journal-title":"Fertil. Steril."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Ottolina, J., Bartiromo, L., Dolci, C., Salmeri, N., Schimberni, M., Villanacci, R., Vigan\u00f2, P., and Candiani, M. (2020). Assessment of coagulation parameters in women affected by endometriosis: Validation study and systematic review of the literature. Diagnostics, 10.","DOI":"10.3390\/diagnostics10080567"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1016\/j.fertnstert.2012.06.029","article-title":"Pathogenesis and pathophysiology of endometriosis","volume":"98","author":"Burney","year":"2012","journal-title":"Fertil. Steril."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Angioni, S., D\u2019Alterio, M.N., Coiana, A., Anni, F., Gessa, S., and Deiana, D. (2020). Genetic characterization of endometriosis patients: Review of the literature and a prospective cohort study on a mediterranean population. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21051765"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1010","DOI":"10.1080\/09513590.2020.1766440","article-title":"How is small bowel permeability in endometriosis patients? A case control pilot study","volume":"36","author":"Zara","year":"2020","journal-title":"Gynecol. Endocrinol."},{"key":"ref_14","first-page":"193","article-title":"Possible role of microbiome in the pathogenesis of endometriosis","volume":"73","author":"Giuliani","year":"2021","journal-title":"Minerva Gynecol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"158","DOI":"10.4274\/jtgga.2018.0090","article-title":"New Insights on the pathogenesis of endometriosis and novel non-surgical therapies","volume":"19","author":"Suardika","year":"2018","journal-title":"J. Turk. Ger. Gynecol. Assoc."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1368","DOI":"10.3389\/fimmu.2017.01368","article-title":"Control of phagocytosis by microbial pathogens","volume":"8","author":"Rosales","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/j.jri.2011.01.019","article-title":"Granulocyte superoxide anion production and regulation by plasma factors in normal and preeclamptic pregnancy","volume":"89","year":"2011","journal-title":"J. Reprod. Immunol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"101796","DOI":"10.1016\/j.jogoh.2020.101796","article-title":"Phagocyte function of peripheral neutrophil granulocytes and monocytes in endometriosis before and after surgery","volume":"50","year":"2021","journal-title":"J. Gynecol. Obstet. Hum. Reprod."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1016\/S0015-0282(97)81391-X","article-title":"Revised American Society for Reproductive Medicine Classification of Endometriosis: 1996","volume":"67","author":"Canis","year":"1997","journal-title":"Fertil. Steril."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/0022-1759(87)90224-9","article-title":"The use of fluorescence quenching in flow cytofluorometry to measure the attachment and ingestion phases in phagocytosis in peripheral blood without prior cell separation","volume":"101","author":"Hed","year":"1987","journal-title":"J. Immunol. Methods"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1111\/j.1365-3083.1976.tb03851.x","article-title":"Isolation of lymphocytes, granulocytes and macrophages","volume":"5","year":"1976","journal-title":"Scand. J. Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1097\/FJC.0b013e31812378fb","article-title":"Modulating role of alcohol and acetaldehyde on neutrophil and monocyte functions in vitro","volume":"50","author":"Vrsalovic","year":"2007","journal-title":"J. Cardiovasc. Pharmacol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1244","DOI":"10.1056\/NEJMra1810764","article-title":"Endometriosis","volume":"382","author":"Zondervan","year":"2020","journal-title":"N. Engl. J. Med."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.1016\/S0140-6736(04)17403-5","article-title":"Endometriosis","volume":"364","author":"Giudice","year":"2004","journal-title":"Lancet"},{"key":"ref_25","first-page":"153","article-title":"Immunological aspects of endometriosis: A review","volume":"3","author":"Vetvicka","year":"2015","journal-title":"Ann. Transl. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1007\/s00404-010-1583-1","article-title":"Effects of peritoneal fluid from endometriosis patients on the release of monocyte-specific chemokines by leukocytes","volume":"283","author":"Na","year":"2010","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2389","DOI":"10.1056\/NEJMcp1000274","article-title":"Endometriosis","volume":"362","author":"Giudice","year":"2010","journal-title":"N. Eng. J. Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/j.rbmo.2021.04.012","article-title":"Functional changes of immune cells: Signal of immune tolerance of the ectopic lesions in endometriosis?","volume":"43","author":"Halben","year":"2021","journal-title":"Reprod. BioMed. Online"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Ram\u00edrez-Pavez, T.N., Mart\u00ednez-Esparza, M., Ruiz-Alcaraz, A.J., Mar\u00edn-S\u00e1nchez, P., Machado-Linde, F., and Garc\u00eda-Pe\u00f1arrubia, P. (2021). The role of peritoneal macrophages in endometriosis. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms221910792"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1186\/s13578-021-00613-5","article-title":"Cell subtypes and immune dysfunction in peritoneal fluid of endometriosis revealed by single-cell RNA-sequencing","volume":"11","author":"Zou","year":"2021","journal-title":"Cell Biosci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.jri.2008.04.001","article-title":"Effect of normal and preeclamptic plasma on superoxide-anion production of neutrophils from healthy non-pregnant women","volume":"79","author":"Ormos","year":"2008","journal-title":"J. Reprod. Immunol."},{"key":"ref_32","first-page":"11","article-title":"Endometriosis and ovarian cancer: An integrative review (endometriosis and ovarian cancer)","volume":"18","author":"Brilhante","year":"2017","journal-title":"Asian Pac. J. Cancer Prev."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e2773","DOI":"10.1097\/MD.0000000000002773","article-title":"Increased risk of endometriosis in patients with lower genital tract infection","volume":"95","author":"Lin","year":"2016","journal-title":"Medicine"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1186\/s13048-020-00642-7","article-title":"Ovarian endometrioma infiltrating neutrophils orchestrate immunosuppressive microenvironment","volume":"13","author":"Xu","year":"2020","journal-title":"J. Ovarian Res."},{"key":"ref_35","first-page":"7","article-title":"The role of cell-mediated immunity in pathogenesis of endometriosis","volume":"159","author":"Dmowski","year":"1994","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"103371","DOI":"10.1016\/j.jri.2021.103371","article-title":"The roles of polymorphonuclear myeloid-derived suppressor cells in endometriosis","volume":"148","author":"Satake","year":"2021","journal-title":"J. Reprod. Immunol."}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/58\/7\/925\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:48:42Z","timestamp":1760140122000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/58\/7\/925"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,12]]},"references-count":36,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2022,7]]}},"alternative-id":["medicina58070925"],"URL":"https:\/\/doi.org\/10.3390\/medicina58070925","relation":{},"ISSN":["1648-9144"],"issn-type":[{"value":"1648-9144","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,12]]}}}