Autoantibodies research in patients with endometriosis: A cross-sectional study

Autoantibodies research in patients with endometriosis: A cross-sectional study | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Short Report Autoantibodies research in patients with endometriosis: A cross-sectional study Cesar Augusto Capellari, Danilo Rahal, Carlos Bezerra Sobrinho, and 3 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3872997/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Background Endometriosis is a common inflammatory disease with an unknown etiology; dysregulation of the immune system appears to play a role in this context. Objective To study the presence of autoantibodies in patients with endometriosis. Methods Two hundred and two females (111 with endometriosis and 91 controls) were studied for the presence of Antinuclear Antibodies (ANA), Extractable Nuclear Antigens (ENA) profile; anti-dsDNA, anticardiolipin (aCl) IgG and IgM and anti endomysial Antibodies (EmA-IgA). Clinical data, obstetric and gynecological history were collected. Results ANA was positive in 26/111 (23.4%) females with endometriosis vs. 5/91 (5.4%) in the control sample (p = 0.0004; OR = 5.26; 95% CI = 1.92–14.30). None of the samples were positive for aCl IgG or IgM; ds-DNA, ENA profile or EMA. No associations between ANA positivity and clinical, obstetrical and gynecological data were found. Conclusion Patients with endometriosis showed high positivity for ANA, but not to the more specific autoantibodies. endometriosis autoimmunity autoantibodies Figures Figure 1 INTRODUCTION Endometriosis is a common cause of pelvic pain and infertility that affects approximately 10% of women of reproductive age. [ 1 ] It is characterized by the presence of endometrial-like tissue outside the uterine cavity, mainly ovaries and peritoneum, but it may also be found in the lungs and pleura, colon, lymph nodes, kidneys, bladder, and abdominal wall. [ 2 ] Endometriosis risk is associated with age between 25 and 45 years, low body mass index (BMI), Caucasian ethnic background and early menarche. [ 3 ] Studies show that altered humoral and cellular immunity favours attachment, persistence, and development of ectopic endometrial tissue. [ 1 ] Decreased natural killer (NK) cell function, increased secretion of adhesion molecules ICAM (intercellular adhesion molecule)-1, and altered expression in the Fas-Fas ligand (Fas-L) system increasing the apoptosis of immune cells are some of the hypotheses to explain the escape of endometriotic cells from local immune surveillance. Macrophages appear to play a central role in this immunobiological process secreting cytokines, chemokines and growth factors, that favor the survival of endometriotic cells. [ 1 ] Autoantibodies recognizing endometrial antigens resulting from polyclonal B cell activation have also been documented in this setting. [ 1 , 4 – 6 ] Other systemic and organ-specific autoimmune diseases associated with endometriosis include systemic lupus erythematosus, [ 7 ] rheumatoid arthritis, [ 8 ] and Hashimoto thyroiditis, [ 9 ] inflammatory bowel disease, [ 10 ] and psoriasis. [ 10 ] The objective of this study was to examine the prevalence of autoantibodies such as antinuclear antibodies (ANA), antiphospholipid antibodies and anti-endomysial autoantibodies in the sera of patients with endometriosis. An association with endometriosis features was also examined. METHODS Ethical Issues This is a cross-sectional study approved by the local Research Ethics Committee under protocol 3.034.734. All included patients were older than 18 years of age and provided signed informed consent. Study Sample and data collection The study sample was from a single gynecological outpatients’ unit at a tertiary hospital in Southern Brazil. Patients were invited to participate in the study in the order of their appointment. All included patients had biopsy-proven endometriosis and were between the age of 18 and 50. Patients with known associated autoimmune disease were excluded. All patients filled out a protocol with demographic data, data on clinical symptoms, gynecological and obstetric history. A 10 ml venous blood sample was collected, aliquoted for autoantibody determination and stored in a -80 o C freezer until tested. A health database was used as the control group, and 91 females paired by age, and reproductive history were selected. They didn’t have autoimmune disease or any clinical symptoms of endometriosis. Determination of autoantibodies. ANA were detected on HEp-2 cells by indirect immunofluorescence, as recommended by the manufacturer (Kallestad® HEp-2 slides–BioRad, USA). The initial dilution was 1:80, and a titer equal to or higher was considered positive for ANA. Fluorescence patterns were classified as fine speckled, coarse speckled, homogeneous, peripheral, or cytoplasmatic according to the International Consensus on ANA Patterns (ICAP) in 2021. [ 11 ] Immunofluorescence test for Crithidia luciliae was used to detect anti-ds-DNA antibodies (ScimedX, USA). Sera that fluoresced brightly in the kinetoplast at a ratio of 1:10 or higher were considered positive. Antibodies to ENA (SS-A/Ro, SS-B/La, Sm, RNP/Sm, Scl-70, and Jo-1) were detected using the ENA-6-Profile kit (Orgentech®, Mainz, Germany), with the cut-off level set at 10 U/mL as recommended by the manufacturer. Only samples with positive ANA were tested for antibodies against extractible nuclear antigens (ENA). Indirect immunofluorescence was used to investigate anti-endomysial antibodies in monkey esophagus with a commercially available kit (Euroimmun®, Denmark); the initial dilution was 1:10. ELISA was used to search for IgG and IgM anticardiolipin antibodies using a commercial kit (Euroimmun®, Denmark). Values greater than 12 U-PL were considered positive. Statistical analysis Nominal data was reported in frequency tables and expressed in percentages. Numerical data had distribution studied by the Shapiro-Wilk test. Comparison between nominal variables was done by chi-squared and Fisher test. For numerical variables, the Mann-Whitney U test was used if the distribution was non-parametric and the unpaired t-test if the distribution was normal. The adopted significance level was 5%. Tests were performed using GraphPad Prism version 8.0.0 for Windows, GraphPad Software, San Diego, California USA, www.graphpad.com ” RESULTS a. Description of the study sample. Two hundred and two females were included: 111 patients with endometriosis (mean age of 36.8 ± 6.8 years) and 91 controls (mean age of 37.8 ± 5.6 years). Patients and controls were paired by age (p = 0.36). Table 1 shows clinical, obstetrical, gynecological and epidemiological data of the endometriosis group. Table 1 Main characteristics of patients with endometriosis studied (n = 111) N (%) Disease duration – (years) Median 3 (2–7) Family history of endometriosis 20 (18.0) Symptoms: (n) Continuous pelvic pain 44 (38.7) Dysmenorrhea 70 (63.1) Amenorrhea- 2 (1.8) Irregular or excessive bleeding 37 (33.3) Dyspareunia 4 (3.6) Asymptomatic 11 (9.9) Gynecological and obstetric history Number of pregnancies (n) Median 1 (0–2) One 33 (49.3) Two 24 (35.8) Three or more 10 (14.9) Number of abortions (n) Median 0 (0–0) One 15 (13.5) Two 4 (3.6) Three or more 2 (1.8) Infertility (n) 43 (38.7) Menstrual cycle (days) Median 28 (23–30) Menses’ duration (days) Median 5 (3–7) Previous sexually transmitted disease Human papillomavirus (HPV) 12 (10.8) Syphilis 1 (0.9) Endometriosis staging Minimal 34 (30.6) Light 29 (26.1) Moderate 27 (24.3) Severe 21 (18.9) In the endometriosis group, 26 (23.4%) females were ANA positive, compared to 5/91(5.4%) in the control group, with p = 0.0004 (OR = 5.26; 95% CI = 1.92–14.30). The observed patterns of immunofluorescence of endometriosis patients and controls are shown in Table 2 . The fine speckled pattern was the most common. The median titer was 1:80 in both groups. Table 2 Characteristics (pattern and titer) of positive ANA in patients with endometriosis and controls Endometriosis sample n = 26 Controls n = 5 Fine speckled 18/26 (69.2%) 1/5 (20%) Nucleolar 3/26 (11.5%) - Dense fine speckled 3/26 (11.5%) 2/5 (24.0%) Homogeneous 1/26 (3.8%) - Coarse speckled 1/26 (3.8%) - Cytoplasmatic 0 2/5 (40%) ANA titer Range − 1/80 to 1/320 Median- 1/80 Range- 1/80 to 1/320 Median 1/80 None of the ANA-positive patients were positive for anti-dsDNA or any antibody from the ENA profile. Moreover, none of the samples was positive for anti-cardiolipin antibodies or anti-endomysial antibodies. Study of endometriosis characteristics according to the ANA presence The study of ANA presence according to endometriosis staging is shown in Fig. 1 . The presence of ANA was not associated with endometriosis. The study of ANA according to endometriosis clinical findings is shown in Table 3 . No associations were found. Table 3 Positive ANA according to clinical findings of patients with endometriosis (n = 26) With the clinical finding- n (%) Without the clinical finding- n (%) p Continuous pelvic pain 10/44 (22.7) 16/67 (23.8) 0.88 Dysmenorrhea 13/70 (18.5) 12/41 (29.2) 0.11 Amenorrhea 3/8 (37.5) 23/103(22.3) 0.38 Irregular or excessive bleeding 6/37 (16.2) 20/74 (27.0) 0.20 Dyspareunia 1/4 (25) 25/107(23.3) 0.99 Asymptomatic 5/11 (45.4) 21/100 (21.0) 0.06 Infertility 9/43 (20.9) 17/68 (25.0) 0.62 At least 1 abortion 5/21 (23.8) 21/90 (23.3) 0.96 Positive familial history 5/20 (25) 21/91 (23.0) 0.85 Discussion The results of the current study show that ANAs were more frequently found in patients with endometriosis than in controls. However, autoantibodies considered more specific for autoimmune diseases were not. Anti-dsDNA and anti-Smith antibody (which belongs to the ENA profile) are considered to be highly specific for systemic lupus [ 12 , 13 ] while anti endomysial antibodies have a nearly 100% specificity for celiac disease. [ 14 ] ANA is one of the most common biomarkers of autoimmunity and may result from polyclonal B cell activation. Therefore, it is an unspecific biomarker of autoimmunity. [ 15 ] ANA may be positive years before the disease develops; therefore, it may be a transitional indicator of autoimmune disease development. [ 15 ] Unexpectedly, a study comparing Systemic Lupus Erythematosus (SLE) and endometriosis patients found that endometriosis patients have a similar rate of musculoskeletal symptoms as SLE patients (articular and fibromyalgic complaints), [ 16 ] suggesting that both serological markers and clinical symptoms, may indicate an underlying autoimmunity. Autoimmunity may not only enable the endometriosis appearance, but it also appears to have an influence on endometriosis findings. According to Almeri et al. [ 10 ] the coexistence of autoimmunity in patients with endometriosis may have an additive role in problems with embryo implantation, favouring infertility in this situation. Infertility is one of the major concerns in endometriosis affecting from 30–50% of women with this disease. [ 3 ] In the present study, it was found in 38% of the sample. Furthermore, females with endometriosis undergoing assisted reproductive technology have a poorer outcome than those without it; lower number of retrieved oocytes, poor embryo quality and altered endometrial receptivity are among the main reasons for this outcome. [ 17 ] Autoimmunity may impair embryo implantation as it creates an abnormal inflammatory microenvironment at the implantation site. [ 18 ] Additionally, they may also affect embryo quality. [ 19 ] In this study it was not possible to link ANA presence to infertility, but the presence of this autoantibody is likely one of the autoimmune findings in this context. The lack of a significant association suggests that additional autoimmune phenomena, including those not linked to B cell dysfunction, should be further investigated. This study is limited by its cross-sectional design and by the limited number of searched autoantibodies. In conclusion, this study showed that ANA is more common in patients with endometriosis than healthy controls, corroborating the existence of autoimmunity in this disease. However, specific autoantibodies tested were shown to be negative. Declarations Author contributions: All authors contributed to the study conception and design. Material preparation, data collection were performed by CAC, DR, CBS and LVB. The data analysis and the first draft of the manuscript was done by TS and RN and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. Conflicts of interest/Competing interests: All authors declare that there are not conflict of interest. Funding: No funding. Ethics approval : All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was approved by the Committee of Ethics in Research from Evangelic Mackenzie School of Medicine under protocol number 3.034.734. Consent to participate All participants signed an informed consent. Consent for publication : Yes. Transparency declaration The authors affirm that this manuscript is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned (and, if relevant, registered) have been explained. References Lebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil Steril. 2001; 75(1):1-10. doi: 10.1016/s0015-0282(00)01630-7. Chauhan S, More A, Chauhan V, Kathane A. Endometriosis: A review of clinical diagnosis, treatment, and pathogenesis. Cureus. 2022; 14(9):e28864. doi: 10.7759/cureus.28864. Smolarz B, Szyłło K, Romanowicz H. Endometriosis: Epidemiology, classification, pathogenesis, treatment and genetics (Review of literature). Int J Mol Sci. 2021; 22(19):10554. doi: 10.3390/ijms221910554. Şerifoğlu H, Arinkan SA, Pasin O, Vural F. Is there an association between endometriosis and thyroid autoimmunity? Rev Assoc Med Bras. 2023; 69(6):e20221679. doi: 10.1590/1806-9282.20221679. Loyau S, Bauters A, Trillot N, Garcia C, Cougoul P, Pol H, et al. Association between endometriosis, infertility and autoimmune antiplatelet glycoprotein VI antibodies in two patients. Platelets. 2023; 34(1):2226756. doi: 10.1080/09537104.2023.2226756. Laudański P, Rogalska G, Warzecha D, Lipa M, Mańka G, Kiecka M, et al. Autoantibody screening of plasma and peritoneal fluid of patients with endometriosis. Hum Reprod. 2023; 38(4):629-643. doi: 10.1093/humrep/dead011. Coloma JL, Martínez-Zamora, Tàssies D, Reverter JC, Espinosa G, Cervera R, et al. Serological autoimmune profile of systemic lupus erythematosus in deep and non-deep endometriosis patients. J Reprod Immunol. 2023; 156:103827. doi: 10.1016/j.jri.2023.103827. Zervou MI, Vlachakis D, Papageorgiou , L, Eliopoulos E, Goulielmos GN. Increased risk of rheumatoid arthritis in patients with endometriosis: genetic aspects. Rheumatology (Oxford). 2022; 61(11):4252-4262. doi: 10.1093/rheumatology/keac143. Porpora MG, Scaramuzzino S, Sangiuliano C, Piacenti I, Bonanni V, Piccioni MG, et al. High prevalence of autoimmune diseases in women with endometriosis: a case-control study. Gynecol Endocrinol. 2020; 36(4):356-359. doi: 10.1080/09513590.2019.1655727. Salmeri N, Gennarelli G, Vanni VS, Ferrari S, Ruffa A, Rovere-Querini P, et al. Concomitant autoimmunity in endometriosis impairs endometrium-embryo crosstalk at the implantation site: A multicenter case-control study. J Clin Med. 2023; 12(10):3557. doi: 10.3390/jcm12103557. Chan EKL, von Mühlen CA, Fritzler MJ, Damoiseaux J, Infantino M, Klotz W, et al. The International Consensus on ANA patterns (ICAP) in 2021-The 6th Workshop and current perspectives. J Appl Lab Med. 2022;7(1):322-30. doi: 10.1093/jalm/jfab140. Wichainun R, Kasitanon N, Wangkaew S, Hongsongkiat S, Sukitawut W, Louthrenoo W. Sensitivity and specificity of ANA and anti-dsDNA in the diagnosis of systemic lupus erythematosus: a comparison using control sera obtained from healthy individuals and patients with multiple medical problems. Asian Pac J Allergy Immunol. 2013;31(4):292-8. doi: 10.12932/AP0272.31.4.2013. Ahn SS, Jung SM, Yoo J, Lee SW, Song JJ, Park YB. Anti-Smith antibody is associated with disease activity in patients with new-onset systemic lupus erythematosus. Rheumatol Int. 2019; 39(11):1937-1944. doi: 10.1007/s00296-019-04445-y. Compilato D, Campisi G, Pastore L, Carroccio A. The production of the oral mucosa of antiendomysial and anti-tissue-transglutaminase antibodies in patients with celiac disease: a review. ScientificWorldJournal. 2010; 10:2385-94. doi: 10.1100/tsw.2010.228. Dinse GE, Parks CG, Weinberg CR, Co CA, Wilkerson J, Zeldin DC, et al. Increasing prevalence of antinuclear antibodies in the United States. Arthritis Rheumatol. 2020; 72(6):1026-35. doi: 10.1002/art.41214. Pasoto SG, Abrao MS, Viana VS, Bueno C, Leon EP, Bonfa E. Endometriosis and systemic lupus erythematosus: a comparative evaluation of clinical manifestations and serological autoimmune phenomena. Am J Reprod Immunol. 2005; 53(2):85-93. doi: 10.1111/j.1600-0897.2005.00252.x. Nada ES, Bordea AE, Bratila E. The impact of endometriosis on in vitro fertilization outcome. Maedica (Bucur). 2022; 17(4):757-761. doi: 10.26574/maedica.2022.17.4.757. Wang Q, Sun Y, Fan R, Wang M, Ren C, Jiang A et al. Role of inflammatory factors in the etiology and treatment of recurrent implantation failure. Reprod. Biol. 2022; 22: 100698. doi: 10.1016/j.repbio.2022.100698. Andrisani A, Sabbadin C, Marin L, Ragazzi E, Dessole F, Armanini D, et al. The influence of thyroid autoimmunity on embryo quality in women undergoing assisted reproductive technology. Gynecol. Endocrinol. 2018; 34:752–755. doi: 10.1080/09513590.2018.1442427. Additional Declarations No competing interests reported. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3872997","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Short Report","associatedPublications":[],"authors":[{"id":267774858,"identity":"5c1a353c-cf4b-4339-a8a2-40a904ba5148","order_by":0,"name":"Cesar Augusto Capellari","email":"","orcid":"","institution":"Federal University of Paraná","correspondingAuthor":false,"prefix":"","firstName":"Cesar","middleName":"Augusto","lastName":"Capellari","suffix":""},{"id":267774859,"identity":"34d544d2-648e-4da0-8555-afc68b6cda5d","order_by":1,"name":"Danilo Rahal","email":"","orcid":"","institution":"Federal University of Paraná","correspondingAuthor":false,"prefix":"","firstName":"Danilo","middleName":"","lastName":"Rahal","suffix":""},{"id":267774860,"identity":"802590f1-04aa-40b4-bd09-710f8e54b276","order_by":2,"name":"Carlos Bezerra Sobrinho","email":"","orcid":"","institution":"Mackenzie Evangelical School of Medicine Paraná","correspondingAuthor":false,"prefix":"","firstName":"Carlos","middleName":"Bezerra","lastName":"Sobrinho","suffix":""},{"id":267774861,"identity":"e5be19e8-76fb-4068-b2fb-e4a042398dc4","order_by":3,"name":"Laura Vilas Boas","email":"","orcid":"","institution":"Mackenzie Evangelical School of Medicine Paraná","correspondingAuthor":false,"prefix":"","firstName":"Laura","middleName":"Vilas","lastName":"Boas","suffix":""},{"id":267774862,"identity":"a6df2c16-d19d-4e11-8eb7-e92b7de4c5e8","order_by":4,"name":"Thelma Skare","email":"","orcid":"","institution":"Mackenzie Evangelical School of Medicine Paraná","correspondingAuthor":false,"prefix":"","firstName":"Thelma","middleName":"","lastName":"Skare","suffix":""},{"id":267774863,"identity":"bb2f1703-0d85-4ec3-a512-a74df03e27d2","order_by":5,"name":"RENATO NISIHARA","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA+ElEQVRIiWNgGAWjYBADHgZmHhBtA8SMjQcIqj+A0JIG0tJAlBawRUBwGEkABzBv7z34+UPFHRn5dt6DnytqztutbT8MtKXGJhqXFpkz55IlDpx5xmNwmC9Z8syx28nbziQCtRxLy23AoUVCIsdA4mDbYR4DZh4DyQa228lmB4BaGBsO49Yi/8b4B0iLfDOP8c+Gf+eSzc4/JKBFgscMbAvDYR4zyca2A3ZmNwjZwpNjZnHmDNBhQC2WjX3JCWY3gLYk4PML+xnjGxUVh+3l+88Y32z4Zmdvdj794YMPNTY4tWCARLDKBGKVg4A9KYpHwSgYBaNgZAAAOJVhmb3/TcAAAAAASUVORK5CYII=","orcid":"","institution":"Federal University of Paraná","correspondingAuthor":true,"prefix":"","firstName":"RENATO","middleName":"","lastName":"NISIHARA","suffix":""}],"badges":[],"createdAt":"2024-01-17 13:15:24","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3872997/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3872997/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":49990998,"identity":"733456c1-194d-4555-a1dd-b87439f91ffd","added_by":"auto","created_at":"2024-01-22 18:45:42","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":33754,"visible":true,"origin":"","legend":"\u003cp\u003ePrevalence of positive antinuclear antibodies (ANA) according to endometriosis staging.\u003c/p\u003e\n\u003cp\u003eNote: Qui-Squared test p = 0.50.\u003c/p\u003e","description":"","filename":"figure1.png","url":"https://assets-eu.researchsquare.com/files/rs-3872997/v1/b3b818c6aa311a005825893f.png"},{"id":49992942,"identity":"044af2b5-d274-4329-846c-e5d58e715119","added_by":"auto","created_at":"2024-01-22 19:01:47","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":346081,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3872997/v1/dde65692-95a3-4919-879a-790365c2c0c8.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Autoantibodies research in patients with endometriosis: A cross-sectional study","fulltext":[{"header":"INTRODUCTION","content":"\u003cp\u003eEndometriosis is a common cause of pelvic pain and infertility that affects approximately 10% of women of reproductive age. [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e] It is characterized by the presence of endometrial-like tissue outside the uterine cavity, mainly ovaries and peritoneum, but it may also be found in the lungs and pleura, colon, lymph nodes, kidneys, bladder, and abdominal wall. [\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e] Endometriosis risk is associated with age between 25 and 45 years, low body mass index (BMI), Caucasian ethnic background and early menarche. [\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e]\u003c/p\u003e \u003cp\u003eStudies show that altered humoral and cellular immunity favours attachment, persistence, and development of ectopic endometrial tissue. [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e] Decreased natural killer (NK) cell function, increased secretion of adhesion molecules ICAM (intercellular adhesion molecule)-1, and altered expression in the Fas-Fas ligand (Fas-L) system increasing the apoptosis of immune cells are some of the hypotheses to explain the escape of endometriotic cells from local immune surveillance. Macrophages appear to play a central role in this immunobiological process secreting cytokines, chemokines and growth factors, that favor the survival of endometriotic cells. [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e] Autoantibodies recognizing endometrial antigens resulting from polyclonal B cell activation have also been documented in this setting. [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e, \u003cspan additionalcitationids=\"CR5\" citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e] Other systemic and organ-specific autoimmune diseases associated with endometriosis include systemic lupus erythematosus, [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e] rheumatoid arthritis, [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e] and Hashimoto thyroiditis, [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e] inflammatory bowel disease, [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e] and psoriasis. [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]\u003c/p\u003e \u003cp\u003eThe objective of this study was to examine the prevalence of autoantibodies such as antinuclear antibodies (ANA), antiphospholipid antibodies and anti-endomysial autoantibodies in the sera of patients with endometriosis. An association with endometriosis features was also examined.\u003c/p\u003e"},{"header":"METHODS","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e\n \u003ch2\u003eEthical Issues\u003c/h2\u003e\n \u003cp\u003eThis is a cross-sectional study approved by the local Research Ethics Committee under protocol 3.034.734. All included patients were older than 18 years of age and provided signed informed consent.\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec4\" class=\"Section2\"\u003e\n \u003ch2\u003eStudy Sample and data collection\u003c/h2\u003e\n \u003cp\u003eThe study sample was from a single gynecological outpatients\u0026rsquo; unit at a tertiary hospital in Southern Brazil. Patients were invited to participate in the study in the order of their appointment. All included patients had biopsy-proven endometriosis and were between the age of 18 and 50. Patients with known associated autoimmune disease were excluded.\u003c/p\u003e\n \u003cp\u003eAll patients filled out a protocol with demographic data, data on clinical symptoms, gynecological and obstetric history. A 10 ml venous blood sample was collected, aliquoted for autoantibody determination and stored in a -80\u003csup\u003eo\u003c/sup\u003e C freezer until tested.\u003c/p\u003e\n \u003cp\u003eA health database was used as the control group, and 91 females paired by age, and reproductive history were selected. They didn\u0026rsquo;t have autoimmune disease or any clinical symptoms of endometriosis.\u003c/p\u003e\n \u003cp\u003e\u003cstrong\u003eDetermination of autoantibodies.\u003c/strong\u003e\u003c/p\u003e\n \u003cp\u003eANA were detected on HEp-2 cells by indirect immunofluorescence, as recommended by the manufacturer (Kallestad\u0026reg; HEp-2 slides\u0026ndash;BioRad, USA). The initial dilution was 1:80, and a titer equal to or higher was considered positive for ANA. Fluorescence patterns were classified as fine speckled, coarse speckled, homogeneous, peripheral, or cytoplasmatic according to the International Consensus on ANA Patterns (ICAP) in 2021. [\u003cspan class=\"CitationRef\"\u003e11\u003c/span\u003e]\u003c/p\u003e\n \u003cp\u003eImmunofluorescence test for \u003cem\u003eCrithidia luciliae\u003c/em\u003e was used to detect anti-ds-DNA antibodies (ScimedX, USA). Sera that fluoresced brightly in the kinetoplast at a ratio of 1:10 or higher were considered positive.\u003c/p\u003e\n \u003cp\u003eAntibodies to ENA (SS-A/Ro, SS-B/La, Sm, RNP/Sm, Scl-70, and Jo-1) were detected using the ENA-6-Profile kit (Orgentech\u0026reg;, Mainz, Germany), with the cut-off level set at 10 U/mL as recommended by the manufacturer. Only samples with positive ANA were tested for antibodies against extractible nuclear antigens (ENA).\u003c/p\u003e\n \u003cp\u003eIndirect immunofluorescence was used to investigate anti-endomysial antibodies in monkey esophagus with a commercially available kit (Euroimmun\u0026reg;, Denmark); the initial dilution was 1:10.\u003c/p\u003e\n \u003cp\u003eELISA was used to search for IgG and IgM anticardiolipin antibodies using a commercial kit (Euroimmun\u0026reg;, Denmark). Values greater than 12 U-PL were considered positive.\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec5\" class=\"Section2\"\u003e\n \u003ch2\u003eStatistical analysis\u003c/h2\u003e\n \u003cp\u003eNominal data was reported in frequency tables and expressed in percentages. Numerical data had distribution studied by the Shapiro-Wilk test. Comparison between nominal variables was done by chi-squared and Fisher test. For numerical variables, the Mann-Whitney U test was used if the distribution was non-parametric and the unpaired t-test if the distribution was normal. The adopted significance level was 5%. Tests were performed using GraphPad Prism version 8.0.0 for Windows, GraphPad Software, San Diego, California USA, \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ewww.graphpad.com\u003c/span\u003e\u003c/span\u003e\u0026rdquo;\u003c/p\u003e\n\u003c/div\u003e"},{"header":"RESULTS","content":"\u003cp\u003e \u003cb\u003ea. Description of the study sample.\u003c/b\u003e \u003c/p\u003e \u003cp\u003eTwo hundred and two females were included: 111 patients with endometriosis (mean age of 36.8\u0026thinsp;\u0026plusmn;\u0026thinsp;6.8 years) and 91 controls (mean age of 37.8\u0026thinsp;\u0026plusmn;\u0026thinsp;5.6 years). Patients and controls were paired by age (p\u0026thinsp;=\u0026thinsp;0.36). Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e shows clinical, obstetrical, gynecological and epidemiological data of the endometriosis group.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eMain characteristics of patients with endometriosis studied (n\u0026thinsp;=\u0026thinsp;111)\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eN (%)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eDisease duration \u0026ndash; (years)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMedian 3 (2\u0026ndash;7)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eFamily history of endometriosis\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e20 (18.0)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"4\" nameend=\"c4\" namest=\"c1\"\u003e \u003cp\u003e\u003cb\u003eSymptoms: (n)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eContinuous pelvic pain\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e44 (38.7)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eDysmenorrhea\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e70 (63.1)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eAmenorrhea-\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2 (1.8)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eIrregular or excessive bleeding\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e37 (33.3)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eDyspareunia\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e4 (3.6)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eAsymptomatic\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e11 (9.9)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"4\" nameend=\"c4\" namest=\"c1\"\u003e \u003cp\u003e\u003cb\u003eGynecological and obstetric history\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eNumber of pregnancies (n)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMedian 1 (0\u0026ndash;2)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eOne\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e33 (49.3)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eTwo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e24 (35.8)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eThree or more\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e10 (14.9)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eNumber of abortions (n)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMedian 0 (0\u0026ndash;0)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eOne\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e15 (13.5)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eTwo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e4 (3.6)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eThree or more\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2 (1.8)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eInfertility (n)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e43 (38.7)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eMenstrual cycle (days)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMedian 28 (23\u0026ndash;30)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003eMenses\u0026rsquo; duration (days)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMedian 5 (3\u0026ndash;7)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c3\" namest=\"c1\"\u003e \u003cp\u003ePrevious sexually transmitted disease\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eHuman papillomavirus (HPV)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e12 (10.8)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eSyphilis\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1 (0.9)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"4\" nameend=\"c4\" namest=\"c1\"\u003e \u003cp\u003e\u003cb\u003eEndometriosis staging\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eMinimal\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e34 (30.6)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eLight\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e29 (26.1)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eModerate\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e27 (24.3)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eSevere\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e21 (18.9)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eIn the endometriosis group, 26 (23.4%) females were ANA positive, compared to 5/91(5.4%) in the control group, with p\u0026thinsp;=\u0026thinsp;0.0004 (OR\u0026thinsp;=\u0026thinsp;5.26; 95% CI\u0026thinsp;=\u0026thinsp;1.92\u0026ndash;14.30).\u003c/p\u003e \u003cp\u003eThe observed patterns of immunofluorescence of endometriosis patients and controls are shown in Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e. The fine speckled pattern was the most common. The median titer was 1:80 in both groups.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eCharacteristics (pattern and titer) of positive ANA in patients with endometriosis and controls\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eEndometriosis sample\u003c/p\u003e \u003cp\u003en\u0026thinsp;=\u0026thinsp;26\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eControls\u003c/p\u003e \u003cp\u003en\u0026thinsp;=\u0026thinsp;5\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFine speckled\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e18/26 (69.2%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1/5 (20%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNucleolar\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3/26 (11.5%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDense fine speckled\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3/26 (11.5%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2/5 (24.0%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHomogeneous\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1/26 (3.8%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCoarse speckled\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1/26 (3.8%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCytoplasmatic\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2/5 (40%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eANA titer\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eRange \u0026minus;\u0026thinsp;1/80 to 1/320\u003c/p\u003e \u003cp\u003eMedian- 1/80\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eRange- 1/80 to 1/320\u003c/p\u003e \u003cp\u003eMedian 1/80\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eNone of the ANA-positive patients were positive for anti-dsDNA or any antibody from the ENA profile. Moreover, none of the samples was positive for anti-cardiolipin antibodies or anti-endomysial antibodies.\u003c/p\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eStudy of endometriosis characteristics according to the ANA presence\u003c/h2\u003e \u003cp\u003eThe study of ANA presence according to endometriosis staging is shown in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e. The presence of ANA was not associated with endometriosis.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eThe study of ANA according to endometriosis clinical findings is shown in Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e. No associations were found.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003ePositive ANA according to clinical findings of patients with endometriosis (n\u0026thinsp;=\u0026thinsp;26)\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eWith the clinical finding- n (%)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eWithout the clinical finding- n (%)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003ep\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eContinuous pelvic pain\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e10/44 (22.7)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e16/67 (23.8)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.88\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDysmenorrhea\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e13/70 (18.5)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e12/41 (29.2)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.11\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAmenorrhea\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3/8 (37.5)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e23/103(22.3)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.38\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eIrregular or excessive bleeding\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e6/37 (16.2)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e20/74 (27.0)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.20\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDyspareunia\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1/4 (25)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e25/107(23.3)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.99\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAsymptomatic\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5/11 (45.4)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e21/100 (21.0)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.06\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eInfertility\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e9/43 (20.9)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e17/68 (25.0)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.62\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAt least 1 abortion\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5/21 (23.8)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e21/90 (23.3)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.96\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePositive familial history\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5/20 (25)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e21/91 (23.0)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.85\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eThe results of the current study show that ANAs were more frequently found in patients with endometriosis than in controls. However, autoantibodies considered more specific for autoimmune diseases were not. Anti-dsDNA and anti-Smith antibody (which belongs to the ENA profile) are considered to be highly specific for systemic lupus [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e, \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e] while anti endomysial antibodies have a nearly 100% specificity for celiac disease. [\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e] ANA is one of the most common biomarkers of autoimmunity and may result from polyclonal B cell activation. Therefore, it is an unspecific biomarker of autoimmunity. [\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e] ANA may be positive years before the disease develops; therefore, it may be a transitional indicator of autoimmune disease development. [\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e] Unexpectedly, a study comparing Systemic Lupus Erythematosus (SLE) and endometriosis patients found that endometriosis patients have a similar rate of musculoskeletal symptoms as SLE patients (articular and fibromyalgic complaints), [\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e] suggesting that both serological markers and clinical symptoms, may indicate an underlying autoimmunity.\u003c/p\u003e \u003cp\u003eAutoimmunity may not only enable the endometriosis appearance, but it also appears to have an influence on endometriosis findings. According to Almeri et al. [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e] the coexistence of autoimmunity in patients with endometriosis may have an additive role in problems with embryo implantation, favouring infertility in this situation. Infertility is one of the major concerns in endometriosis affecting from 30\u0026ndash;50% of women with this disease. [\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e] In the present study, it was found in 38% of the sample. Furthermore, females with endometriosis undergoing assisted reproductive technology have a poorer outcome than those without it; lower number of retrieved oocytes, poor embryo quality and altered endometrial receptivity are among the main reasons for this outcome. [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e] Autoimmunity may impair embryo implantation as it creates an abnormal inflammatory microenvironment at the implantation site. [\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e] Additionally, they may also affect embryo quality. [\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e] In this study it was not possible to link ANA presence to infertility, but the presence of this autoantibody is likely one of the autoimmune findings in this context. The lack of a significant association suggests that additional autoimmune phenomena, including those not linked to B cell dysfunction, should be further investigated.\u003c/p\u003e \u003cp\u003eThis study is limited by its cross-sectional design and by the limited number of searched autoantibodies.\u003c/p\u003e \u003cp\u003eIn conclusion, this study showed that ANA is more common in patients with endometriosis than healthy controls, corroborating the existence of autoimmunity in this disease. However, specific autoantibodies tested were shown to be negative.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthor contributions:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll authors contributed to the study conception and design. Material preparation, data collection were performed by CAC, DR, CBS and LVB. The data analysis and the first draft of the manuscript was done by TS and RN and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflicts of interest/Competing interests:\u003c/strong\u003e All authors declare that there are not conflict of interest.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding:\u003c/strong\u003e\u0026nbsp; No funding.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics approval\u003c/strong\u003e: All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was approved by the Committee of Ethics in Research from Evangelic Mackenzie School of Medicine under protocol number\u0026nbsp;3.034.734.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent to participate\u003c/strong\u003e All participants signed an informed consent.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e: Yes.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eTransparency declaration\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors affirm that this manuscript is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned (and, if relevant, registered) have been explained.\u003c/p\u003e\n"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eLebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil Steril. 2001; 75(1):1-10. doi: 10.1016/s0015-0282(00)01630-7.\u003c/li\u003e\n\u003cli\u003eChauhan S, More A, Chauhan V, Kathane A. Endometriosis: A review of clinical diagnosis, treatment, and pathogenesis. Cureus. 2022; 14(9):e28864. doi: 10.7759/cureus.28864. \u003c/li\u003e\n\u003cli\u003eSmolarz B, Szyłło K, Romanowicz H. Endometriosis: Epidemiology, classification, pathogenesis, treatment and genetics (Review of literature). Int J Mol Sci. 2021; 22(19):10554. doi: 10.3390/ijms221910554.\u003c/li\u003e\n\u003cli\u003eŞerifoğlu H, Arinkan SA, Pasin O, Vural F. Is there an association between endometriosis and thyroid autoimmunity? Rev Assoc Med Bras. 2023; 69(6):e20221679. doi: 10.1590/1806-9282.20221679.\u003c/li\u003e\n\u003cli\u003eLoyau S, Bauters A, Trillot N, Garcia C, Cougoul P, Pol H, et al. Association between endometriosis, infertility and autoimmune antiplatelet glycoprotein VI antibodies in two patients. 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J Appl Lab Med. 2022;7(1):322-30. doi: 10.1093/jalm/jfab140.\u003c/li\u003e\n\u003cli\u003eWichainun R, Kasitanon N, Wangkaew S, Hongsongkiat S, Sukitawut W, Louthrenoo W. Sensitivity and specificity of ANA and anti-dsDNA in the diagnosis of systemic lupus erythematosus: a comparison using control sera obtained from healthy individuals and patients with multiple medical problems. Asian Pac J Allergy Immunol. 2013;31(4):292-8. doi: 10.12932/AP0272.31.4.2013.\u003c/li\u003e\n\u003cli\u003eAhn SS, Jung SM, Yoo J, Lee SW, Song JJ, Park YB. Anti-Smith antibody is associated with disease activity in patients with new-onset systemic lupus erythematosus. Rheumatol Int. 2019; 39(11):1937-1944. doi: 10.1007/s00296-019-04445-y.\u003c/li\u003e\n\u003cli\u003eCompilato D, Campisi G, Pastore L, Carroccio A. The production of the oral mucosa of antiendomysial and anti-tissue-transglutaminase antibodies in patients with celiac disease: a review. ScientificWorldJournal. 2010; 10:2385-94. doi: 10.1100/tsw.2010.228.\u003c/li\u003e\n\u003cli\u003eDinse GE, Parks CG, Weinberg CR, Co CA, Wilkerson J, Zeldin DC, et al. Increasing prevalence of antinuclear antibodies in the United States. Arthritis Rheumatol. 2020; 72(6):1026-35. doi: 10.1002/art.41214.\u003c/li\u003e\n\u003cli\u003ePasoto SG, Abrao MS, Viana VS, Bueno C, Leon EP, Bonfa E. Endometriosis and systemic lupus erythematosus: a comparative evaluation of clinical manifestations and serological autoimmune phenomena. Am J Reprod Immunol. 2005; 53(2):85-93. doi: 10.1111/j.1600-0897.2005.00252.x.\u003c/li\u003e\n\u003cli\u003eNada ES, Bordea AE, Bratila E. The impact of endometriosis on in vitro fertilization outcome. Maedica (Bucur). 2022; 17(4):757-761. doi: 10.26574/maedica.2022.17.4.757.\u003c/li\u003e\n\u003cli\u003eWang Q, Sun Y, Fan R, Wang M, Ren C, Jiang A et al. Role of inflammatory factors in the etiology and treatment of recurrent implantation failure. Reprod. Biol. 2022; 22: 100698. doi: 10.1016/j.repbio.2022.100698.\u003c/li\u003e\n\u003cli\u003eAndrisani A, Sabbadin C, Marin L, Ragazzi E, Dessole F, Armanini D, et al. The influence of thyroid autoimmunity on embryo quality in women undergoing assisted reproductive technology. Gynecol. Endocrinol. 2018; 34:752\u0026ndash;755. doi: 10.1080/09513590.2018.1442427.\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"endometriosis, autoimmunity, autoantibodies","lastPublishedDoi":"10.21203/rs.3.rs-3872997/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3872997/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eBackground\u003c/h2\u003e \u003cp\u003eEndometriosis is a common inflammatory disease with an unknown etiology; dysregulation of the immune system appears to play a role in this context.\u003c/p\u003e\u003ch2\u003eObjective\u003c/h2\u003e \u003cp\u003eTo study the presence of autoantibodies in patients with endometriosis.\u003c/p\u003e\u003ch2\u003eMethods\u003c/h2\u003e \u003cp\u003eTwo hundred and two females (111 with endometriosis and 91 controls) were studied for the presence of Antinuclear Antibodies (ANA), Extractable Nuclear Antigens (ENA) profile; anti-dsDNA, anticardiolipin (aCl) IgG and IgM and anti endomysial Antibodies (EmA-IgA). Clinical data, obstetric and gynecological history were collected.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eANA was positive in 26/111 (23.4%) females with endometriosis vs. 5/91 (5.4%) in the control sample (p\u0026thinsp;=\u0026thinsp;0.0004; OR\u0026thinsp;=\u0026thinsp;5.26; 95% CI\u0026thinsp;=\u0026thinsp;1.92\u0026ndash;14.30). None of the samples were positive for aCl IgG or IgM; ds-DNA, ENA profile or EMA. No associations between ANA positivity and clinical, obstetrical and gynecological data were found.\u003c/p\u003e\u003ch2\u003eConclusion\u003c/h2\u003e \u003cp\u003ePatients with endometriosis showed high positivity for ANA, but not to the more specific autoantibodies.\u003c/p\u003e","manuscriptTitle":"Autoantibodies research in patients with endometriosis: A cross-sectional study","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-01-22 18:45:37","doi":"10.21203/rs.3.rs-3872997/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"55a25d9b-6d2d-4aff-b1a5-97451da7dac8","owner":[],"postedDate":"January 22nd, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-01-22T18:45:40+00:00","versionOfRecord":[],"versionCreatedAt":"2024-01-22 18:45:37","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-3872997","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3872997","identity":"rs-3872997","version":["v1"]},"buildId":"B-jG_2CBjPDmsCi4Wdhf-","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}