{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T01:20:50Z","timestamp":1760059250482,"version":"build-2065373602"},"reference-count":76,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2025,6,3]],"date-time":"2025-06-03T00:00:00Z","timestamp":1748908800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathophysiology"],"abstract":"<jats:p>Background\/Objectives: Normal remodeling of the extracellular matrix of the endometrium is a necessary condition for the implantation of a blastocyst. We evaluated whether the use of histochemical reticulin\u2013collagen staining can improve the assessment of the extracellular matrix of the mid-secretory endometrium in recrudescent clinical\/biochemical pregnancy losses in comparison with ultrasound and routine histological examination. Methods: We compared the histochemical pattern of reticulin\u2013collagen endometrial biopsy (21st day of the cycle) with ultrasonography and standard histological examination of the endometrium in the following groups: (1) fertile women with gravidity \u2265 2, (gravidity = parity) and (2) women with two or more clinical\/biochemical pregnancy losses. Results: A normal pattern (NP) with ordered reticulin fibers forming cellular structures was determined in 92% of biopsies with physiological reproductive status and 44% of biopsies with recrudescent reproductive failure (p &lt; 0.05), despite the fact that there were no differences in ultrasonography and standard histological examination between the groups (p &gt; 0.05). A histochemical pattern of insufficient secretory endometrial transformation with abnormal noodle-like pattern (aNP) collagen fibers was more common in recrudescent reproductive failure (56%) than in women with physiological reproductive status (8%) (p &lt; 0.001), despite the fact that insufficient secretory endometrial transformation with an abnormal noodle-like pattern with collagenization (aNPC) was detected only in recrudescent reproductive failure, and it was not detected in women with physiological reproductive status (p &lt; 0.00001). Conclusions: We determined the histochemical pattern of the extracellular matrix of the endometrium in terms of the type of reticulin\u2013collagen, associated in our study with recrudescent clinical\/biochemical pregnancy loss, with improved predictability compared to ultrasonography and standard histological examination. We propose to use the method of histochemical evaluation of the reticulin\u2013collagen pattern in order to stratify groups of women of fertile age at risk of reproductive failure.<\/jats:p>","DOI":"10.3390\/pathophysiology32020024","type":"journal-article","created":{"date-parts":[[2025,6,3]],"date-time":"2025-06-03T11:55:52Z","timestamp":1748951752000},"page":"24","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Histochemical Assessment of Reticulin\u2013Collagen Patterns in the Mid-Secretory Endometrium Predicts Recurrent Pregnancy Loss"],"prefix":"10.3390","volume":"32","author":[{"ORCID":"https:\/\/orcid.org\/0009-0000-5033-623X","authenticated-orcid":false,"given":"Nazerke","family":"Oshakhtiyeva","sequence":"first","affiliation":[{"name":"Institute of Life Sciences, Karaganda Medical University, Karaganda 100008, Kazakhstan"},{"name":"Department of Obstetrics and Gynecology, Karaganda Medical University, Karaganda 100008, Kazakhstan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2012-2227","authenticated-orcid":false,"given":"Dmitriy","family":"Klyuyev","sequence":"additional","affiliation":[{"name":"Institute of Life Sciences, Karaganda Medical University, Karaganda 100008, Kazakhstan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhanna","family":"Amirbekova","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Karaganda Medical University, Karaganda 100008, Kazakhstan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rinat","family":"Gatin","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Karaganda Medical University, Karaganda 100008, Kazakhstan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anar","family":"Turmukhambetova","sequence":"additional","affiliation":[{"name":"Institute of Life Sciences, Karaganda Medical University, Karaganda 100008, Kazakhstan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-4789-5872","authenticated-orcid":false,"given":"Kamilya","family":"Makhambetova","sequence":"additional","affiliation":[{"name":"Institute of Life Sciences, Karaganda Medical University, Karaganda 100008, Kazakhstan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7173-3138","authenticated-orcid":false,"given":"Irina","family":"Kadyrova","sequence":"additional","affiliation":[{"name":"Institute of Life Sciences, Karaganda Medical University, Karaganda 100008, Kazakhstan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yevgeniy","family":"Kamyshanskiy","sequence":"additional","affiliation":[{"name":"Clinic of Medical University, Karaganda Medical University, Karaganda 100000, Kazakhstan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,6,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"dev201507","DOI":"10.1242\/dev.201507","article-title":"Human embryo implantation","volume":"150","author":"Muter","year":"2023","journal-title":"Development"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1530\/REP-09-0158","article-title":"Comparative aspects of implantation","volume":"138","author":"Bazer","year":"2009","journal-title":"Reproduction"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Benagiano, G., Mancuso, S., Guo, S.W., and Di Renzo, G.C. (2023). Events Leading to the Establishment of Pregnancy and Placental Formation: The Need to Fine-Tune the Nomenclature on Pregnancy and Gestation. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms242015420"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1177\/1535370220938741","article-title":"The role of extracellular matrix in normal and pathological pregnancy: Future applications of microphysiological systems in reproductive medicine","volume":"245","author":"Pope","year":"2020","journal-title":"Exp. Biol. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"13661","DOI":"10.1073\/pnas.94.25.13661","article-title":"Cell locomotion and focal adhesions are regulated by substrate flexibility","volume":"94","author":"Pelham","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1095\/biolreprod65.1.240","article-title":"Effects of matrix proteins on the expression of matrix metalloproteinase-2, -9, and -14 and tissue inhibitors of metalloproteinases in human cytotrophoblast cells during the first trimester","volume":"65","author":"Xu","year":"2001","journal-title":"Biol. Reprod."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s42825-022-00087-2","article-title":"The role of extracellular matrix on unfavorable maternal\u2013fetal interface: Focusing on the function of collagen in human fertility","volume":"4","author":"Liu","year":"2022","journal-title":"J. Leather Sci. Eng."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1007\/BF00221758","article-title":"An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy","volume":"253","author":"Aplin","year":"1988","journal-title":"Cell Tissue Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.lfs.2019.04.042","article-title":"What is the role of peptide fragments of collagen I and IV in health and disease?","volume":"228","author":"Kisling","year":"2019","journal-title":"Life Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1002\/ar.1092180408","article-title":"Immunolocalization of extracellular matrix proteins and collagen synthesis in first-trimester human decidua","volume":"218","author":"Kisalus","year":"1987","journal-title":"Anat. Rec."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.1091\/mbc.E19-12-0709","article-title":"Collagen, stiffness, and adhesion: The evolutionary basis of vertebrate mechanobiology","volume":"31","author":"Tang","year":"2020","journal-title":"Mol. Biol. Cell."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1167\/iovs.07-0956","article-title":"Substrate rigidity modulates cell matrix interactions and protein expression in human trabecular meshwork cells","volume":"49","author":"Schlunck","year":"2008","journal-title":"Invest. Ophthalmol. Vis. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Sternberg, A.K., Buck, V.U., Classen-Linke, I., and Leube, R.E. (2021). How Mechanical Forces Change the Human Endometrium during the Menstrual Cycle in Preparation for Embryo Implantation. Cells, 10.","DOI":"10.3390\/cells10082008"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1999","DOI":"10.1093\/humrep\/dez139","article-title":"Tissue stiffness at the human maternal-fetal interface","volume":"34","author":"Abbas","year":"2019","journal-title":"Hum. Reprod."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1002\/rmb2.12088","article-title":"Decidualization of the human endometrium","volume":"17","author":"Okada","year":"2018","journal-title":"Reprod. Med. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Ma, Z., Sagrillo-Fagundes, L., Mok, S., Vaillancourt, C., and Moraes, C. (2020). Mechanobiological regulation of placental trophoblast fusion and function through extracellular matrix rigidity. Sci. Rep., 10.","DOI":"10.1038\/s41598-020-62659-8"},{"key":"ref_17","first-page":"2925","article-title":"Decreased type IV collagen expression by human decidual tissues in spontaneous abortion","volume":"81","author":"Iwahashi","year":"1996","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e12769","DOI":"10.1111\/aji.12769","article-title":"Involvement of the JAK-STAT pathway in collagen regulation of decidual NK cells","volume":"78","author":"Fu","year":"2017","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Yoshii, N., Hamatani, T., Inagaki, N., Hosaka, T., Inoue, O., Yamada, M., Machiya, R., Yoshimura, Y., and Odawara, Y. (2013). Successful implantation after reducing matrix metalloproteinase activity in the uterine cavity. Reprod. Biol. Endocrinol., 11.","DOI":"10.1186\/1477-7827-11-37"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1111\/aji.12211","article-title":"Trophoblasts and decidual stromal cells regulate decidual NK cell functions via interaction between collagen and LAIR-1","volume":"71","author":"Fu","year":"2014","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1002\/stem.2222","article-title":"Loss of Endometrial Plasticity in Recurrent Pregnancy Loss","volume":"34","author":"Lucas","year":"2016","journal-title":"Stem Cells"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Salker, M., Teklenburg, G., Molokhia, M., Lavery, S., Trew, G., Aojanepong, T., Mardon, H.J., Lokugamage, A.U., Rai, R., and Landles, C. (2010). Natural selection of human embryos: Impaired decidualization of endometrium disables embryo-maternal interactions and causes recurrent pregnancy loss. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0010287"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Salker, M.S., Nautiyal, J., Steel, J.H., Webster, Z., Su\u0107urovi\u0107, S., Nicou, M., Singh, Y., Lucas, E.S., Murakami, K., and Chan, Y.-W. (2012). Disordered IL-33\/ST2 activation in decidualizing stromal cells prolongs uterine receptivity in women with recurrent pregnancy loss. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0052252"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Potiris, A., Alyfanti, E., Drakaki, E., Mavrogianni, D., Karampitsakos, T., Machairoudias, P., Topis, S., Zikopoulos, A., Skentou, C., and Panagopoulos, P. (2024). The Contribution of Proteomics in Understanding Endometrial Protein Expression in Women with Recurrent Implantation Failure. J. Clin. Med., 13.","DOI":"10.3390\/jcm13072145"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Ticconi, C., Pietropolli, A., Di Simone, N., Piccione, E., and Fazleabas, A. (2019). Endometrial Immune Dysfunction in Recurrent Pregnancy Loss. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20215332"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"You, S., Zhu, Y., Li, H., He, F., Liu, S., Yang, X., Wang, L., Zeng, H., Dai, J., and Hu, L. (2023). Recombinant humanized collagen remodels endometrial immune microenvironment of chronic endometritis through macrophage immunomodulation. Regen. Biomater., 10.","DOI":"10.1093\/rb\/rbad033"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1038\/nrm3620","article-title":"Role of the extracellular matrix in regulating stem cell fate","volume":"14","author":"Watt","year":"2013","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1080\/14737159.2024.2375235","article-title":"Are we closer to robust predictors of recurrent pregnancy loss by means of integrating different types of omics data?","volume":"24","author":"Wei","year":"2024","journal-title":"Expert. Rev. Mol. Diagn."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/s40738-019-0059-7","article-title":"15 years of transcriptomic analysis on endometrial receptivity: What have we learnt?","volume":"5","author":"Messaoudi","year":"2019","journal-title":"Fertil. Res. Pract."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1186\/s12958-024-01263-1","article-title":"Varied cellular abnormalities in thin vs. normal endometrium in recurrent implantation failure by single-cell transcriptomics","volume":"22","author":"Fu","year":"2024","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/biolre\/ioae134","article-title":"Decoding recurrent pregnancy loss: Insights from comparative proteomics studies","volume":"112","author":"Davalieva","year":"2025","journal-title":"Biol Reprod."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"4530","DOI":"10.1002\/jcp.26259","article-title":"Potential roles of metalloproteinases of endometrium-derived exosomes in embryo-maternal crosstalk during implantation","volume":"233","author":"Latifi","year":"2018","journal-title":"J. Cell Physiol."},{"key":"ref_33","first-page":"1786","article-title":"The International Glossary on Infertility and Fertility Care, 2017","volume":"32","author":"Adamson","year":"2017","journal-title":"Hum. Reprod."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2805","DOI":"10.2147\/DDDT.S317545","article-title":"Comparison of Stimulated Cycles with Low Dose r-FSH versus Hormone Replacement Cycles for Endometrial Preparation Prior to Frozen-Thawed Embryo Transfer in Young Women with Polycystic Ovarian Syndrome: A Single-Center Retrospective Cohort Study from China","volume":"15","author":"Li","year":"2021","journal-title":"Drug Des. Devel Ther."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Chow, S.-C., Wang, H., and Shao, J. (2003). Sample Size Calculations in Clinical Research, Marcel Dekker.","DOI":"10.1201\/9780203911341"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"17","DOI":"10.3352\/jeehp.2021.18.17","article-title":"Sample size determination and power analysis using the G*Power software","volume":"18","author":"Kang","year":"2021","journal-title":"J. Educ. Eval. Health Prof."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1016\/S0015-0282(16)60916-0","article-title":"Endometrial thickness and growth during ovarian stimulation: A possible predictor of implantation in in vitro fertilization","volume":"52","author":"Gonen","year":"1989","journal-title":"Fertil. Steril."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Zhao, J., Zhang, Q., and Li, Y. (2012). The effect of endometrial thickness and pattern measured by ultrasonography on pregnancy outcomes during IVF-ET cycles. Reprod. Biol. Endocrinol., 10.","DOI":"10.1186\/1477-7827-10-100"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Ma, N.Z., Chen, L., Dai, W., Bu, Z.Q., Hu, L.L., and Sun, Y.P. (2017). Influence of endometrial thickness on treatment outcomes following in vitro fertilization\/intracytoplasmic sperm injection. Reprod. Biol. Endocrinol., 15.","DOI":"10.1186\/s12958-016-0222-5"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.fertnstert.2006.11.089","article-title":"Changes in measured endometrial thickness predict in vitro fertilization success","volume":"88","author":"McWilliams","year":"2007","journal-title":"Fertil. Steril."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/j.rbmo.2014.05.011","article-title":"Endometrial pattern, thickness and growth in predicting pregnancy outcome following 3319 ivf cycle","volume":"29","author":"Zhao","year":"2014","journal-title":"Reprod. BioMed. Online"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"907874","DOI":"10.3389\/fendo.2022.907874","article-title":"An endometrial receptivity scoring system basing on the endometrial thickness, volume, echo, peristalsis, and blood flow evaluated by ultrasonography","volume":"13","author":"Zhang","year":"2022","journal-title":"Front Endocrinol"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1148\/radiology.167.1.3279455","article-title":"Cyclic endometrial changes: US assessment with histologic correlation","volume":"167","author":"Forrest","year":"1988","journal-title":"Radiology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/oxfordjournals.humrep.a137538","article-title":"How well does ultrasonographic measurement of endometrial thickness predict the results of histological dating?","volume":"7","author":"Li","year":"1992","journal-title":"Hum. Reprod."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"29","DOI":"10.4103\/0974-1208.82357","article-title":"Predictive value of endometrial thickness, pattern and sub-endometrial blood flows on the day of hCG by 2D doppler in in-vitro fertilization cycles: A prospective clinical study from a tertiary care unit","volume":"4","author":"Singh","year":"2011","journal-title":"J. Hum. Reprod. Sci."},{"key":"ref_46","first-page":"77","article-title":"The possibilities of adverse pregnancy outcomes predicting based on laboratory markers of reproductive losses","volume":"113","author":"Taizhanova","year":"2024","journal-title":"Med. Ecol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1016\/S0015-0282(16)46636-7","article-title":"Morphometric analysis of the human endometrium in relation to peripheral hormone levels","volume":"38","author":"Johannisson","year":"1982","journal-title":"Fertil. Steril."},{"key":"ref_48","unstructured":"(2025, March 25). Masson\u2019s Trichrome Staining Protocol for Collagen Fibers. Available online: https:\/\/ihcworld.com\/2024\/01\/26\/massons-trichrome-staining-protocol-for-collagen-fibers\/."},{"key":"ref_49","unstructured":"Reticulum Stain Kit (Modified Gomori\u2019s) For the Histological Visualization of Reticular Fibers (2025, March 25). Version 1 Last Updated 27 June 2018 ab236473. Available online: https:\/\/www.abcam.com\/ps\/products\/236\/ab236473\/documents\/ab236473%20-%20Reticulum%20Stain%20Kit%20(Modified%20Gomori's)%20v1a%20(website).pdf?srsltid=AfmBOordg8pj-ElMRK_eVCflx47RUjSyI7Cx2mc1eQAPUgjKyV6tzW6I."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/S0002-9378(16)33500-1","article-title":"Dating the endometrial biopsy","volume":"122","author":"Noyes","year":"1975","journal-title":"Am. J. Obs. Obstet. Gynecol."},{"key":"ref_51","unstructured":"Benningtoon, J.L. (1980). Decision tree for endometrial dating. Surgical Pathology of the Uterine Corpus, WB Saunders."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1016\/j.fertnstert.2003.11.030","article-title":"A critical analysis of the accuracy, reproducibility, and clinical utility of histologic endometrial dating in fertile women","volume":"81","author":"Murray","year":"2004","journal-title":"Fertil. Steril."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1016\/S0344-0338(84)80084-9","article-title":"The endometrium of infertility. A review","volume":"178","year":"1984","journal-title":"Pathol. Res. Pract."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1016\/S0015-0282(99)00605-6","article-title":"Endometrial dating and determination of the window of implantation in healthy fertile women","volume":"73","author":"Acosta","year":"2000","journal-title":"Fertil. Steril."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2394","DOI":"10.1093\/humrep\/dex312","article-title":"Pinopode score around the time of implantation is predictive of successful implantation following frozen embryo transfer in hormone replacement cycles","volume":"32","author":"Jin","year":"2017","journal-title":"Hum. Reprod."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1016\/S0015-0282(00)00717-2","article-title":"Detection of endometrial pinopodes by light microscopy","volume":"74","author":"Develioglu","year":"2000","journal-title":"Fertil. Steril."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1111\/j.1749-6632.2000.tb06244.x","article-title":"Surface morphology of the human endometrium. Basic and clinical aspects","volume":"900","author":"Nikas","year":"2000","journal-title":"Ann. N. Y Acad. Sci."},{"key":"ref_58","first-page":"37","article-title":"Endometrial receptivity and expression of apoptosis and proliferation factors in the endometrium of women with hyperplasia and infertility","volume":"19","author":"Grishkina","year":"2019","journal-title":"Bull. Gynecol. Obstet. Perinatol."},{"key":"ref_59","first-page":"671","article-title":"Microscopic Colitis: A Review of Collagenous and Lymphocytic Colitis","volume":"13","author":"Boland","year":"2017","journal-title":"Gastroenterol. Hepatol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/0046-8177(89)90198-6","article-title":"Lymphocytic (\u201cmicroscopic\u201d) colitis: A comparative histopathologic study with particular reference to collagenous colitis","volume":"20","author":"Lazenby","year":"1989","journal-title":"Hum. Pathol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.humpath.2022.06.027","article-title":"Microscopic colitis: Lymphocytic colitis, collagenous colitis, and beyond","volume":"132","author":"Yuan","year":"2023","journal-title":"Hum. Pathol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1136\/jcp.51.1.44","article-title":"Decreased type V collagen expression in human decidual tissues of spontaneous abortion during early pregnancy","volume":"51","author":"Iwahashi","year":"1998","journal-title":"J. Clin. Pathol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.yexcr.2017.03.012","article-title":"PRL-3\/PTP4A3 phosphatase regulates integrin \u03b21 in adhesion structures during migration of human ocular melanoma cells","volume":"353","author":"Foy","year":"2017","journal-title":"Exp. Cell Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"2220","DOI":"10.7150\/ijbs.45586","article-title":"Collagen at the maternal-fetal interface in human pregnancy","volume":"16","author":"Shi","year":"2020","journal-title":"Int. J. Biol. Sci."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1016\/j.molimm.2011.09.006","article-title":"Tumor-expressed collagens can modulate immune cell function through the inhibitory collagen receptor LAIR-1","volume":"49","author":"Rygiel","year":"2011","journal-title":"Mol. Immunol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/j.hjc.2017.12.006","article-title":"The dynamic changes in myocardial collagen metabolism in experimental autoimmune myocarditis rats","volume":"59","author":"Lv","year":"2018","journal-title":"Hell. J. Cardiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1111\/jog.13936","article-title":"Dysregulation of collagen expression in peri-implantation endometrium of women with high ovarian response","volume":"45","author":"Li","year":"2019","journal-title":"J. Obs. Obstet. Gynaecol. Res."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/BF00221122","article-title":"The villous stroma of the human placenta. I. The ultrastructure of fixed connective tissue cells","volume":"177","author":"Kaufmann","year":"1977","journal-title":"Cell Tissue Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1055\/s-2001-14063","article-title":"Studies on the mechanism of edematous changes at the endometrial stroma for implantation","volume":"27","author":"Okada","year":"2001","journal-title":"Semin. Thromb. Hemost."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.fertnstert.2003.11.050","article-title":"Accelerated endometrial maturation in the luteal phase of cycles utilizing controlled ovarian hyperstimulation: Impact of gonadotropin-releasing hormone agonists versus antagonists","volume":"82","author":"Saadat","year":"2004","journal-title":"Fertil. Steril."},{"key":"ref_71","first-page":"203","article-title":"Effects of steroid hormone levels on the ultrasound appearance of the preovulatory endometrium in controlled ovarian hyperstimulation cycles","volume":"5","author":"Corbacioglu","year":"2012","journal-title":"Int. J. Fertil. Steril."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"2571","DOI":"10.1016\/j.bbagen.2014.03.007","article-title":"Matrix metalloproteinases in inflammation","volume":"1840","author":"Nissinen","year":"2014","journal-title":"Biochim. Biophys. Acta."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Lee, H.S., and Kim, W.J. (2022). The Role of Matrix Metalloproteinase in Inflammation with a Focus on Infectious Diseases. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms231810546"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1007\/s13770-023-00536-x","article-title":"Development of Matrix Metalloproteinases-Mediated Extracellular Matrix Remodeling in Regenerative Medicine: A Mini Review","volume":"20","author":"Chen","year":"2023","journal-title":"Tissue Eng. Regen. Med."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"217","DOI":"10.12968\/bjom.2018.26.4.217","article-title":"Hypermobile Ehlers-Danlos syndrome during pregnancy, birth and beyond","volume":"26","author":"Pezaro","year":"2018","journal-title":"Br. J. Midwifery"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1739","DOI":"10.1093\/humrep\/deac148","article-title":"Pregnancy complications and placental histology following embryo transfer with a thinner endometrium","volume":"37","author":"Cui","year":"2022","journal-title":"Hum. 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