Endometriosis, recurrent miscarriage and implantation failure: is there an immunological link?
Abstract
Endometriosis is more frequently diagnosed in patients with infertility than in a normal population. The goal of this paper is to give an overview of the clinical and fundamental evidence for a possible link between endometriosis and (recurrent) miscarriage or implantation failure after treatment with assisted reproductive technology. According to the literature, there is insufficient evidence for an association between endometriosis and (recurrent) miscarriage, but there is, however, epidemiological evidence to support the link between endometriosis and recurrent implantation failure after assisted reproduction. This can possibly be explained by alterations in humoral and cell-mediated immunity in women with endometriosis. Humoral immunological changes include increased formation of antibodies against endometrial antigens, anti-laminin-1 auto-antibodies and other auto-immune antibodies (e.g. antiphospholipid). Cell-mediated immunological changes include alterations in peritoneal and follicular fluid immune cells and cytokines. The possible negative effect of these immunological changes on folliculogenesis, ovulation, oocyte quality, early embryonic development and implantation in women with endometriosis suggests that infertility in endometriosis patients may be related to alterations within the follicle or oocyte, resulting in embryos with decreased ability to implant.
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Retrospective studies have suggested that women with endometriosis may have higher rates of maternal complications and fetal problems such as preeclampsia and miscarriage, though these associations need further study.
“Retrospective studies have suggested that women with endometriosis may have higher rates of maternal complications and fetal problems such as preeclampsia and miscarriage (46–50), though these associations need further study.”
Cites
Laparoscopic Surgery in Infertile Women with Minimal or Mild Endometriosis
Marcoux, S., Maheux, R., & Bérubé, S. (1997) · New England Journal of Medicine · doi:10.1056/nejm199707243370401 · Cited by 948 · see citing works
Immunobiology of endometriosis
Lebovic, D. I., Mueller, M. D., & Taylor, R. N. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01630-7 · Cited by 857 · see citing works
Effect of endometriosis on in vitro fertilization
Barnhart, K. T., Dunsmoor-Su, R. F., & Coutifaris, C. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03112-6 · Cited by 798 · see citing works
Kao, L. C., Germeyer, A., Tulac, S., Lobo, S., Yang, J. P., Taylor, R. N., Osteen, K., Lessey, B. A., & Giudice, L. C. (2003) · Endocrinology · doi:10.1210/en.2003-0043 · Cited by 696 · see citing works
Lessey, B. A., Damjanovich, L., Coutifaris, C., Castelbaum, A. J., Albelda, S. Μ., & Buck, C. A. (1992) · Journal of Clinical Investigation · doi:10.1172/jci115835 · Cited by 640 · see citing works
Simón, C., Gutiérrez, A., Vidal, A., de los Santos, M. J., Tarín, J. J., Remohí, J., & Pellicer, A. (1994) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a138578 · Cited by 374 · see citing works
HOX gene expression is altered in the endometrium of women with endometriosis
Taylor, H. S. (1999) · Human Reproduction · doi:10.1093/humrep/14.5.1328 · Cited by 372 · see citing works
dell'Endometriosi, G. I. P. L. S. (1999) · Human Reproduction · doi:10.1093/humrep/14.5.1332 · Cited by 370 · see citing works
Endometriosis and Subfertility: Is the Relationship Resolved?
D’Hooghe, T. M., Debrock, S., Hill, J. A., & Meuleman, C. (2003) · Seminars in Reproductive Medicine · doi:10.1055/s-2003-41330 · Cited by 320 · see citing works
Self-citationThe role of cytokines in endometriosis
Wu, M., & Ho, H. (2003) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2003.01207.x · Cited by 317 · see citing works
High Risk Pregnancy: Management Options
Robson, S. C. (1995) · BMJ · doi:10.1136/bmj.310.6983.882a · Cited by 289 · see citing works
Aromatase: a key molecule in the pathophysiology of endometriosis and a therapeutic target
Zeitoun, K. M., & Bulun, S. E. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00393-3 · Cited by 256 · see citing works
Antiangiogenic Agents Are Effective Inhibitors of Endometriosis
Hull, M. L., Jones, D. S., Chan, C. L. K., Bruner‐Tran, K. L., Osteen, K. G., Tom, B. D. M., Fan, T. D., & Smith, S. K. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021912 · Cited by 243 · see citing works
Is Endometriosis Associated with Systemic Subclinical Inflammation?
Agic, A., Xu, H., Finas, D., Banz, C., Diedrich, K., & Hornung, D. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000093121 · Cited by 231 · see citing works
ENRIQUE B. DEL CASTILLO 1897-1969
Tramezzani, J. H. (1970) · Reproduction · doi:10.1530/jrf.0.0220001 · Cited by 223 · see citing works
Autoimmunity to endometrium and ovary in endometriosis.
MATHUR, S. P., Peress, M. R., Williamson, H. O., YOUMANS, C. D., MANEY, S. A., Garvin, A. J., Rust, P. F., & Fudenberg, H. H. (1982) · PubMed Central · Cited by 213 · see citing works
Oosterlynck, D. J., Meuleman, C., Waer, M., & Koninckx, P. R. (1994) · PubMed · Cited by 205 · see citing works
Self-citationPellicer, A., Oliveira, N., Ruiz, A., Remohi, J., & Simón, C. (1995) · Human Reproduction · doi:10.1093/humrep/10.suppl_2.91 · Cited by 202 · see citing works
Pellicer, A., Albert, C., Mercader, A., Bonilla-Musoles, F. M., Remohi, J., Sr., & Simón, C. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00204-0 · Cited by 192 · see citing works
Autoimmunity to Endometrium and Ovary in Endometriosis
MATHUR, S. P., Peress, M. R., Williamson, H. O., YOUMANS, C. D., MANEY, S. A., Garvin, A. J., Rust, P. F., & Fudenberg, H. H. (1983) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-198309000-00022 · Cited by 167 · see citing works
Endometriosis and Inflammation in Infertility
Halis, G., & Arici, A. M. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1335.032 · Cited by 163 · see citing works
Dmowski, W. P., Rana, N., Michalowska, J., Friberg, J., Papierniak, C. K., & El-Roeiy, A. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57425-1 · Cited by 161 · see citing works
Bulun, S. E., Simpson, E. R., & Word, R. A. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.78.3.8126151 · Cited by 152 · see citing works
Immunodiagnostic Evaluation in Women with Reproductive Failure
Kaider, A. S., Kaider, B. D., Janowicz, P. B., & Roussev, R. G. (1999) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1999.tb00110.x · Cited by 136 · see citing works
Carlberg, M., Nejaty, J., Fröysa, B., Guan, Y.-M., Söder, O., & Bergqvist, A. (2000) · Human Reproduction · doi:10.1093/humrep/15.6.1250 · Cited by 132 · see citing works
D’Hooghe, T. M., Nugent, N. P., Cuneo, S., Chai, D. C., Deer, F., Debrock, S., Kyama, C. M., Mihalyi, A., & Mwenda, J. M. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.043349 · Cited by 132 · see citing works
Self-citationLee, K. S., Joo, B. S., Na, Y. J., Yoon, M. S., Choi, O. H., & Kim, W. W. (2000) · Journal of Assisted Reproduction and Genetics · doi:10.1023/a:1009495913119 · Cited by 130 · see citing works
Donnez, J., Donnez, O., Orellana, R., Binda, M. M., & Dolmans, M. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.01.019 · Cited by 112 · see citing works
Paracrine Regulation of Matrix Metalloproteinase Expression in the Normal Human Endometrium
Osteen, K. G., Keller, N. R., Feltus, F. A., & Melner, M. H. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000052863 · Cited by 108 · see citing works
The Molecular Basis for Implantation Failure in Endometriosis
Giudice, L. C., Telles, T. L., Lobo, S. C., & Kao, L. C. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02786.x · Cited by 108 · see citing works
Urman, B., Yakın, K., & Balaban, B. (2005) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60846-2 · Cited by 101 · see citing works
Pituitary-ovarian dysfunction and endometriosis
Cahill, D. J. (2000) · Human Reproduction Update · doi:10.1093/humupd/6.1.56 · Cited by 98 · see citing works
Reduced preovulatory granulosa cell steroidogenesis in women with endometriosis.
Harlow, C. R., Cahill, D. J., Maile, L. A., Talbot, W. M., Mears, J., Wardle, P. G., & Hull, M. G. R. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.1.8550788 · Cited by 95 · see citing works
High Risk Pregnancy: Management Options
Williamson, C., & Girling, J. (1999) · Cited by 93 · see citing works
Implantation Defects in Infertile Women with Endometriosis
Lessey, B. A. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02787.x · Cited by 92 · see citing works
Omland, A. K., Åbyholm, T., Fedorcsák, P., Ertzeid, G., Oldereid, N. B., Bjercke, S., & Tanbo, T. G. (2005) · Human Reproduction · doi:10.1093/humrep/deh664 · Cited by 91 · see citing works
Endometriosis: Associations with Menorrhagia, Infertility and Oral Contraceptives
Sensky, T. E., & Liu, D. T. Y. (1980) · International Journal of Gynecology & Obstetrics · doi:10.1002/j.1879-3479.1980.tb00210.x · Cited by 90 · see citing works
Autoimmunity in Endometriosis: Relevance to Infertility
MATHUR, S. P. (2000) · American Journal of Reproductive Immunology · doi:10.1111/j.8755-8920.2000.440204.x · Cited by 88 · see citing works
Brizek, C. L., Schlaff, S., Pellegrini, V. A., Frank, J. B., & Worrilow, K. C. (1995) · Journal of Assisted Reproduction and Genetics · doi:10.1007/bf02211378 · Cited by 86 · see citing works
Reproductive and menstrual factors and risk of peritoneal and ovarian endometriosis
Candiani, G. B., Danesino, V., Gastaldi, A., Parazzini, F., & Ferraroni, M. (1991) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54477-x · Cited by 81 · see citing works
Bulun, S. E., Mahendroo, M., & Simpson, E. R. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.76.6.7684741 · Cited by 77 · see citing works
Endometriosis and Oocyte Quality
Saito, H., Seino, T., Kaneko-Tarui, T., Nakahara, K., Toya, M., & Kurachi, H. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000049424 · Cited by 74 · see citing works
Lachapelle, M.-H., Hemmings, R., Roy, D., Falcone, T., & Miron, P. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58327-7 · Cited by 71 · see citing works
Urman, B., Yakın, K., & Balaban, B. (2005) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60847-4 · Cited by 68 · see citing works
Is the endometrium or oocyte/embryo affected in endometriosis?
Garcia-Velasco, J. A., & Arici, A. (1999) · Human Reproduction · doi:10.1093/humrep/14.suppl_2.77 · Cited by 68 · see citing works
An association of IgG anti-laminin-1 autoantibodies with endometriosis in infertile patients
Inagaki, J. (2003) · Human Reproduction · doi:10.1093/humrep/deg148 · Cited by 67 · see citing works
TABIBZADEH, S. S., Mason, J. M., Shea, W., Cai, Y., Murray, M. J., & Lessey, B. A. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.7.6674 · Cited by 63 · see citing works
Endometrial antigens involved in the autoimmunity of endometriosis
MATHUR, S. P., Chihal, H. J., Homm, R. J., Garza, D. E., Rust, P. F., & Williamson, H. O. (1988) · Fertility and Sterility · doi:10.1016/s0015-0282(16)60362-x · Cited by 62 · see citing works
Tanbo, T. G., Omland, A. K., Dale, P. O., & Åbyholm, T. (1995) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349509024386 · Cited by 61 · see citing works
Taranissi, M., El‐Toukhy, T., & Verlinsky, Y. (2005) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61670-7 · Cited by 57 · see citing works
TABIBZADEH, S. S. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.7.2526 · Cited by 53 · see citing works
Martínez‐Román, S., Balasch, J., Creus, M. T., Fábregues, F., Carmona, F., Vilella, R., & Vanrell, J. A. (1997) · Human Reproduction · doi:10.1093/humrep/12.8.1794 · Cited by 49 · see citing works
Reduced preovulatory granulosa cell steroidogenesis in women with endometriosis
Harlow, C. R. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.1.426 · Cited by 49 · see citing works
Bükülmez, O., Yaralı́, H., & Gürgan, T. (2001) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00379-1 · Cited by 44 · see citing works
IgG Anti‐laminin‐1 Autoantibody and Recurrent Miscarriages
Inagaki, J., Matsuura, E., Kaihara, K., Kobayashi, K., Yasuda, T., Nomizu, M., SUGIURA‐OGASAWARA, M., Katano, K., & Aoki, K. (2001) · American Journal of Reproductive Immunology · doi:10.1111/j.8755-8920.2001.450406.x · Cited by 42 · see citing works
Endometriosis and spontaneous abortion rate: a cohort study in infertile women
Matorras, R., Rodrı́guez, F., de Terán, G. G., Pijoán, J. I., Ramón, O., & Rodrı́guez-Escudero, F. J. (1998) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(97)00181-4 · Cited by 41 · see citing works
Spontaneous abortions in women with endometriosis
Pittaway, D. E., Vernon, C., & Fayez, J. A. (1988) · Fertility and Sterility · doi:10.1016/s0015-0282(16)60303-5 · Cited by 40 · see citing works
Endometriosis and Recurrent Pregnancy Loss
Vercammen, E., & D’Hooghe, T. M. (2000) · Seminars in Reproductive Medicine · doi:10.1055/s-2000-13726 · Cited by 39 · see citing works
Self-citationMı́nguez, Y., Rubio, C., Bernal, A., Gaitán, P., Remohí, J., Simón, C., & Pellicer, A. (1997) · Human Reproduction · doi:10.1093/humrep/12.10.2282 · Cited by 39 · see citing works
Levels of Transferrin and Alpha 2-HS Glycoprotein in Women with and without Endometriosis
MATHUR, S. P., Lee, J. H., Jiang, H., Arnaud, P., & Rust, P. F. (1999) · Autoimmunity · doi:10.3109/08916939908995381 · Cited by 39 · see citing works
Bulun, S. E. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.76.6.1458 · Cited by 37 · see citing works
Future Directions in Endometriosis Research
D’Hooghe, T. M., Kyama, C. M., Debrock, S., Meuleman, C., & Mwenda, J. M. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1335.034 · Cited by 36 · see citing works
Self-citationKaláb, P., Schultz, R. M., & Kopf, G. S. (1993) · Biology of Reproduction · doi:10.1095/biolreprod49.3.561 · Cited by 35 · see citing works
Spontaneous abortion and endometriosis
Fitzsimmons, J., Stahl, R., Gocial, B., & Shapiro, S. S. (1987) · Fertility and Sterility · doi:10.1016/s0015-0282(16)59124-9 · Cited by 27 · see citing works
Abae, M., Glassberg, M., Majercik, M., Yoshida, H., Vestal, R., & Puett, D. (1994) · Fertility and Sterility · doi:10.1016/s0015-0282(16)56760-0 · Cited by 26 · see citing works
Endometriosis and subfertility treatment: a review.
Hondt, A. D., Peeraer, K., Meuleman, C., Meeuwis, L., Loecker, P. D., & D’Hooghe, T. M. (2005) · PubMed · Cited by 19 · see citing works
Self-citationPreclinical abortions and endometriosis
Pittaway, D. E., Ellington, C. P., & Klimek, M. (1988) · Fertility and Sterility · doi:10.1016/s0015-0282(16)59705-2 · Cited by 14 · see citing works
Lack of endometriosis in patients with repeated abortion
Balasch, J. C., Creus, M. T., & Vanrell, J. A. (1988) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136690 · Cited by 5 · see citing works
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Vitonis, A. F., Vincent, K., Rahmioglu, N., Fassbender, A., Buck Louis, G. M., Hummelshoj, L., Giudice, L. C., Stratton, P., Adamson, G. D., Becker, C. M., et al. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.07.1244 · Cited by 236 · see citing works
Self-citationImmune interactions in endometriosis
Herington, J. L., Bruner‐Tran, K. L., Lucas, J. A., & Osteen, K. G. (2011) · Expert Review of Clinical Immunology · doi:10.1586/eci.11.53 · Cited by 226 · see citing works
Rahmioglu, N., Fassbender, A., Vitonis, A. F., Tworoger, S. S., Hummelshoj, L., D'Hooghe, T. M., Adamson, G. D., Giudice, L. C., Becker, C. M., Zondervan, K. T., et al. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.07.1208 · Cited by 227 · see citing works
Self-citationBacterial contamination hypothesis: a new concept in endometriosis
Khan, K. N., Fujishita, A., Hiraki, K., Kitajima, M., Nakashima, M., Fushiki, S., & Kitawaki, J. (2018) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12083 · Cited by 176 · see citing works
Cytokine Networks and the Regulation of Uterine Function in Pregnancy and Parturition
Orsi, N. M., & Tribe, R. M. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01668.x · Cited by 181 · see citing works
Is there an association between autoimmunity and endometriosis?
Eisenberg, V. H., Zolti, M., & Soriano, D. (2012) · Autoimmunity Reviews · doi:10.1016/j.autrev.2012.01.005 · Cited by 164 · see citing works
In vitro fertilization is a successful treatment in endometriosis-associated infertility
Opøien, H. K., Fedorcsák, P., Omland, A. K., Åbyholm, T., Bjercke, S., Ertzeid, G., Oldereid, N. B., Mellembakken, J. R., & Tanbo, T. G. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.01.112 · Cited by 154 · see citing works
Plants as source of new therapies for endometriosis: a review of preclinical and clinical studies
Meresman, G. F., Götte, M., & Laschke, M. W. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa039 · Cited by 158 · see citing works
Cellular and molecular basis for endometriosis-associated infertility
Stilley, J. A. W., Birt, J. A., & Sharpe-Timms, K. L. (2012) · Cell and Tissue Research · doi:10.1007/s00441-011-1309-0 · Cited by 151 · see citing works
Vercellini, P., Parazzini, F., Pietropaolo, G., Cipriani, S., Frattaruolo, M., & Fedele, L. (2012) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2012.03466.x · Cited by 134 · see citing works
Oocyte vitrification for fertility preservation in women with endometriosis: an observational study
Cobo, A., Giles, J., Paolelli, S., Pellicer, A., Remohí, J., & García-Velasco, J. A. (2020) · Fertility and Sterility · doi:10.1016/j.fertnstert.2019.11.017 · Cited by 127 · see citing works
Opøien, H. K., Fedorcsak, P., Åbyholm, T., & Tanbo, T. (2011) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2011.06.002 · Cited by 120 · see citing works
Can Endometriosis-Related Oxidative Stress Pave the Way for New Treatment Targets?
Cacciottola, L., Donnez, J., & Dolmans, M.-M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22137138 · Cited by 118 · see citing works
Exacoustos, C., Lauriola, I., Lazzeri, L., De Felice, G., & Zupi, E. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.06.024 · Cited by 100 · see citing works
Kolańska, K., Alijotas‐Reig, J., Cohen, J., Cheloufi, M., Selleret, L., d’Argent, E. M., Kayem, G., Esteve‐Valverde, E., Fain, O., Bornes, M., et al. (2020) · American Journal of Reproductive Immunology · doi:10.1111/aji.13384 · Cited by 98 · see citing works
Khan, K. N., Kitajima, M., Hiraki, K., Fujishita, A., Sekine, I., Ishimaru, T., & Masuzaki, H. (2009) · Gynecologic and Obstetric Investigation · doi:10.1159/000212061 · Cited by 94 · see citing works
Akoum, A., Al-Akoum, M., Lemay, A., Maheux, R., & Leboeuf, M. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.06.019 · Cited by 78 · see citing works
REVIEW ARTICLE: NK Cell Tolerance and the Maternal–Fetal Interface
Riley, J. K., & Yokoyama, W. M. (2008) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2008.00593.x · Cited by 76 · see citing works
Immunological Aspects of Endometriosis: An Update
Olovsson, M. (2011) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2011.01045.x · Cited by 74 · see citing works
Barrier, B. F. (2010) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181db7c33 · Cited by 72 · see citing works
Socolov, R. V., Buţureanu, S., Angioni, S. L., Sindilar, A., Boiculese, L. V., Cozma, L. G., & Socolov, D. G. (2010) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2010.10.008 · Cited by 65 · see citing works
Quenby, S. M., Anim-Somuah, M., Kalumbi, C., Farquharson, R. G., & Aplin, J. (2007) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60791-2 · Cited by 61 · see citing works
Circulating cell-free DNA as a potential biomarker for minimal and mild endometriosis
Zachariah, R., Schmid, S., Radpour, R., Buerki, N., Fan, A. X.-C., Hahn, S., Holzgreve, W., & Zhong, X. Y. (2009) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60100-9 · Cited by 59 · see citing works
Braundmeier, A. G., Jackson, K. S., Hastings, J. M., Koehler, J., Nowak, R. A., & Fazleabas, A. T. (2012) · Human Reproduction · doi:10.1093/humrep/des083 · Cited by 58 · see citing works
Huang, Y., Zhao, X., Chen, Y., Wang, J., Zheng, W., & Cao, L. (2020) · BioMed Research International · doi:10.1155/2020/4381346 · Cited by 55 · see citing works
Do endometriomas induce an inflammatory reaction in nearby follicles?
Opøien, H. K., Fedorcsák, P., Polec, A., Stensen, M. H., Åbyholm, T., & Tanbo, T. G. (2013) · Human Reproduction · doi:10.1093/humrep/det087 · Cited by 53 · see citing works
Toll‐like receptor system and endometriosis
Khan, K. N., Kitajima, M., Fujishita, A., Nakashima, M., & Masuzaki, H. (2013) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.12117 · Cited by 52 · see citing works
Ma, C., Yan, L., Qiao, J., Sha, W., Li, L., Chen, Y., & Sun, Q. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.01.131 · Cited by 49 · see citing works
Disorders of implantation – are there diagnostic and therapeutic options?
Tóth, B., Würfel, W., Germeyer, A., Hirv, K., Makrigiannakis, A., & Strowitzki, T. (2011) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2011.05.002 · Cited by 47 · see citing works
Kabut, J., Kondera‐Anasz, Z., Sikora, J., & Mielczarek‐Palacz, A. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.12.061 · Cited by 42 · see citing works
Immunopathological insights into endometriosis: from research advances to future treatments
Dai, Y., Ye, Z., Lin, X., & Zhang, S. (2025) · Seminars in Immunopathology · doi:10.1007/s00281-025-01058-5 · Cited by 40 · see citing works
CAUSES OF FEMALE INFERTILITY: A CROSS- SECTIONAL STUDY
Sudha, G. (2013) · Cited by 38 · see citing works
Carli, C., Leclerc, P., Metz, C. N., & Akoum, A. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.04.002 · Cited by 37 · see citing works
Targeting Mast Cells in Endometriosis with Janus Kinase 3 Inhibitor, JANEX‐1
D’Cruz, O. J., & Uckun, F. M. (2007) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2007.00502.x · Cited by 35 · see citing works
Is there a role of autoimmunity in implantation failure after in-vitro fertilization?
Cline, A. M., & Kutteh, W. H. (2009) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e3283294879 · Cited by 35 · see citing works
Obstetrical complications and outcome in patients with endometriosis
Borisova, A. V., Konnon, S. R., Tosto, V., Gerli, S., & Radzinsky, V. E. (2020) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2020.1793326 · Cited by 32 · see citing works
Endometriosis is associated with pregnancy loss: a nationwide historical cohort study
Boje, A. D., Egerup, P., Westergaard, D., Bertelsen, M.-L. M. F., Nyegaard, M., Hartwell, D., Lidegaard, Ø., & Nielsen, H. S. (2023) · Fertility and Sterility · doi:10.1016/j.fertnstert.2022.12.042 · Cited by 31 · see citing works
Disturbed progesterone signalling in an advanced preclinical model of endometriosis
Esfandiari, F., Khoei, H. H., Saber, M., Favaedi, R., Piryaei, A., Moini, A., Shahhoseini, M., Ramezanali, F., Ghaffari, F., & Baharvand, H. (2021) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2020.12.011 · Cited by 30 · see citing works
Salmeri, N., Gennarelli, G., Vanni, V. S., Ferrari, S. M., Ruffa, A., Rovere, P. Q., Pagliardini, L., Candiani, M., & Papaleo, E. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12103557 · Cited by 28 · see citing works
Devesa-Peiró, A., Sebastián-León, P., Pellicer, A., & Díaz-Gimeno, P. (2021) · Molecular Human Reproduction · doi:10.1093/molehr/gaab011 · Cited by 25 · see citing works
Endometriosis, need for a multidisciplinary clinical setting: the internist’s point of view
Montalto, M., Santoro, L., D’Onofrio, F., Gallo, A., Campo, S., Campo, V., Gasbarrini, A., & Gasbarrini, A. (2010) · Internal and Emergency Medicine · doi:10.1007/s11739-010-0404-7 · Cited by 25 · see citing works
Carvalho, L. F. P., Rossener, R., Azeem, A., Malvezzi, H., Abrão, M. S., & Agarwal, A. K. (2013) · PubMed · Cited by 25 · see citing works
Ruiz, L. A., Dutil, J., Ruiz, A., Fourquet, J., Abac, S., Laboy, J., & Flores, I. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.06.001 · Cited by 24 · see citing works
Matteo, M., Cicinelli, E., Neri, M., Carrubba, R., Carpagnano, F. A., Romeo, F., Scutiero, G., Greco, P., Garlanda, C., Vendemiale, G., et al. (2017) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2017.08.014 · Cited by 23 · see citing works
Postgestational effects of macrophage migration inhibitory factor on embryonic implantation in mice
Bondza, P. K., Metz, C. N., & Akoum, A. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.08.046 · Cited by 20 · see citing works
Possible effects of endometriosis-related immune events on reproductive function
Kökçü, A. (2013) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-013-2767-2 · Cited by 20 · see citing works
Endometriosis and assisted reproduction: the role for reproductive surgery?
Hondt, A. D., Meuleman, C., Tomassetti, C., Peeraer, K., & D’Hooghe, T. M. (2006) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/01.gco.0000233929.27145.f3 · Cited by 19 · see citing works
Self-citationThe Role of Peritoneal Immunity in Peritoneal Endometriosis and Related Infertility
Huang, Q., Yu, Y., Xu, W., Li, S., Zhou, Y., & Shu, J. (2023) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2808166 · Cited by 19 · see citing works
Michaud, N., Al-Akoum, M., Gagnon, G., Girard, K., Blanchet, P., Rousseau, J. A., & Akoum, A. (2011) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2011.08.001 · Cited by 14 · see citing works
Kilic, S., Evsen, M. S., Taşdemir, N., Yılmaz, N., Yuksel, B., Dogan, M., & Batıoğlu, S. (2007) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60345-8 · Cited by 13 · see citing works
A panoramic view to relationships between reproductive failure and immunological factors
Kökçü, A., Yavuz, E., Çelik, H., & Bıldırcın, D. (2012) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-012-2480-6 · Cited by 12 · see citing works
THE EFFECT OF MORPHINE ADMINISTRATION ON STRUCTURE AND ULTRASTRUCTURE OF UTERUS IN PREGNANT MICE
Dehghan, M. M., Mokhtar, J., & Mahmoudian, A. (2010) · TSpace (University of Toronto) · Cited by 11 · see citing works
AN OVERVIEW OF AUTOIMMUNITY IN IMPLANTATION FAILURE: A LITERATURE REVIEW
Berestoviy, V. O., Mahmood, A. A., Berestoviy, O. O., Гінзбург, В. Г., & Говсєєв, Д. О. (2021) · Wiadomości Lekarskie · doi:10.36740/wlek202103240 · Cited by 11 · see citing works
Genes Downregulated in Endometriosis Are Located Near the Known Imprinting Genes
Kobayashi, H., Higashiura, Y., Koike, N., Akasaka, J., Uekuri, C., Iwai, K., Niiro, E., Morioka, S., & Yamada, Y. (2014) · Reproductive Sciences · doi:10.1177/1933719114526473 · Cited by 10 · see citing works
Germeyer, A., von Wolff, M., Jauckus, J., Strowitzki, T., Sharma, T., & Grazul‐Bilska, A. T. (2010) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-8-67 · Cited by 10 · see citing works
Induction of Endometriosis by implantation of endometrial fragments in female rats
Mohammadzadeh, A., Heidari, M., Haleh, S. G., Zarnani, A., Novin, M. G., Akhondi, M. M., Jarahi, A. M., & Mohammadzadeh, F. (2006) · TSpace (University of Toronto) · Cited by 10 · see citing works
Birt, J. A., Taylor, K. H., Davis, J., & Sharpe-Timms, K. L. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.07.007 · Cited by 9 · see citing works
Polycystic ovary syndrome and immune deregulation: what do hormones want to say?
Johnson, B. S., & Laloraya, M. (2022) · Exploration of Immunology · doi:10.37349/ei.2022.00058 · Cited by 8 · see citing works
Mohammadzadeh, A., Heidari, M., Soltanghoraee, H., Jeddi‐Tehrani, M., Novin, M. G., Akhondi, M. M., Zeraati, H., & Mohammadzadeh, F. (2008) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2008.00745.x · Cited by 8 · see citing works
RetractedHe, Y., Su, X., Li, H., Tang, R., Ju, Y., Chen, S., & Wang, X. (2024) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2024.104250 · Cited by 8 · see citing works
Silva, A. C. J. D. S. R. E., Mamillapalli, R., Silva, J. C. R. E., Ucar, A., Schwartz, J., & Taylor, H. S. (2022) · F&S Science · doi:10.1016/j.xfss.2022.10.003 · Cited by 7 · see citing works
Dose-Dependent Decreased Fertility in Response to the Burden of Endometriosis in a Murine Model
Rosa-e-Silva, A. C. J. S., Silva, J. C. R. E., Mamillapalli, R., & Taylor, H. S. (2019) · Reproductive Sciences · doi:10.1177/1933719119859438 · Cited by 8 · see citing works
Sun, Y., Cai, J., Ding, S., & Bao, S. (2022) · Reproductive Sciences · doi:10.1007/s43032-022-01102-x · Cited by 7 · see citing works
Linehan, L. A., Hennessy, M., & O’Donoghue, K. (2021) · HRB Open Research · doi:10.12688/hrbopenres.13397.1 · Cited by 6 · see citing works
Marron, K., Kennedy, J. F., & Harrity, C. (2018) · Fertility Research and Practice · doi:10.1186/s40738-018-0046-4 · Cited by 6 · see citing works
An Investigation of Molecular Targeting of MMP-9 for Endometriosis Using Algal Bioactive Molecules
Nabiya, F., Chenniappan, A. D., Rajamiriyam, M., MubarakAli, D., & Kim, J. (2021) · Phyton · doi:10.32604/phyton.2022.017390 · Cited by 5 · see citing works
Adur, M. K., Braundmeier‐Fleming, A., Lessey, B. A., & Nowak, R. A. (2021) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/22840265211018544 · Cited by 5 · see citing works
Role of hysterosalpingography and diagnostic laparoscopy in infertility
Sachdeva, P., & Kaur, N. (2016) · International Journal of Reproduction Contraception Obstetrics and Gynecology · doi:10.18203/2320-1770.ijrcog20163836 · Cited by 5 · see citing works
Guha, P., Roychoudhury, S., Singha, S., Kalita, J. C., Kolesárová, A., Jamal, Q. M. S., Jha, N. K., Kumar, D., Ruokolainen, J., & Kesari, K. K. (2021) · Applied Sciences · doi:10.3390/app11083349 · Cited by 4 · see citing works
A case of spontaneous abortion related to ovarian endometriosis in a Golden Retriever dog.
Ma, D. (2017) · Europe PMC (PubMed Central) · Cited by 4 · see citing works
Orief, Y. I., Karkor, T. A. E., Saleh, H. A., Elhadidy, A., & Badr, N. (2013) · Middle East Fertility Society Journal · doi:10.1016/j.mefs.2013.06.002 · Cited by 4 · see citing works
Ma, R., Qin, J., Wang, S., Guan, S., Jia, F., Deng, Y., Bai, J., & Wang, S. (2025) · Taiwanese Journal of Obstetrics and Gynecology · doi:10.1016/j.tjog.2025.01.004 · Cited by 3 · see citing works
Góźdź, A., Żeberkiewicz, M., Janiuk, I. R., Hyc, A., Iwan, A., Zwierzchowska, A., Maksym, R., Shevchenko, K., Wlodarski, P. K., Barcz, E., et al. (2025) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-025-01486-w · Cited by 3 · see citing works
The diagnostic role of cervico-vaginal fluid interleukins-1α in endometriosis: A case-control study.
Mardanian, F., & Sheikhsoleimani, Z. (2014) · Europe PMC (PubMed Central) · Cited by 3 · see citing works
Rahmioğlu, N., Fassbender, A., Vitonis, A. F., Hummelshøj, L., Adamson, G. D., Becker, C. M., Missmer, S. A., & Zondervan, K. T. (2017) · Springer eBooks · doi:10.1007/978-3-319-59856-7_11 · Cited by 3 · see citing works
Endometriosis and autoimmunity
Abisror, N., Kolańska, K., Cheloufi, M., Selleret, L., d’Argent, E. M., Kayem, G., & MEKINIAN, A. (2022) · Exploration of Immunology · doi:10.37349/ei.2022.00034 · Cited by 3 · see citing works
Poorasamy, J., Garg, D., Bharti, J., Nambirajan, A., Patil, A., Sengupta, J., & Ghosh, D. (2022) · Reproductive Medicine · doi:10.3390/reprodmed3040022 · Cited by 3 · see citing works
Caesarean section in a case of systemic lupus erythematosus
Shukla, D., Vyas, V. H., Patil, S., & Mohite, S. N. (2014) · Indian Journal of Anaesthesia · doi:10.4103/0019-5049.130827 · Cited by 3 · see citing works
Yarmolinskaya, M. I., & Михайловна, Д. В. (2015) · Journal of obstetrics and women s diseases · doi:10.17816/jowd64381-91 · Cited by 2 · see citing works
Ananyeva, M. A., Shilova, N. A., Валентиновна, Ч. Т., Kharlamova, N. V., & Назаров, С. Б. (2016) · Russian Bulletin of Obstetrician-Gynecologist · doi:10.17116/rosakush201616571-75 · Cited by 2 · see citing works
Autoimmunity and Female Infertility: Fact vs. Fiction
Odom, L. N., Cline, A. M., & Kutteh, W. H. (2011) · Springer eBooks · doi:10.1007/978-1-4419-8456-2_1 · Cited by 2 · see citing works
Молотков, А. С., & Yarmolinskaya, M. I. (2015) · Russian Bulletin of Obstetrician-Gynecologist · doi:10.17116/rosakush201515642-47 · Cited by 2 · see citing works
Baştuğ, E. (2013) · Turkish Journal of Immunology · doi:10.5606/tji.2013.195 · Cited by 2 · see citing works
Peripheral Biomarkers as Predictive Indicators of Endometriosis: A Prospective Case Control Study
Deo, S., Jaiswar, S., Shankhwar, P. L., Iqbal, B., & Jhirwar, M. (2017) · SSR Institute of International Journal of Life Sciences · doi:10.21276/ijlssr.2017.3.5.18 · Cited by 1 · see citing works
Recurrent Implantation Failure: History, Etiology, Advances and Ongoing Challenges
George, S. K. (2025) · doi:10.38124/ijisrt/25mar1152 · Cited by 1 · see citing works
侯, 梦. (2023) · Traditional Chinese Medicine · doi:10.12677/tcm.2023.128321 · Cited by 1 · see citing works
Harby, I. K. A., Ahmed, O. I., Zaki, W. K., Faris, M. A., & El-Deen, N. N. S. (2022) · Journal of Pure and Applied Microbiology · doi:10.22207/jpam.16.2.59 · Cited by 1 · see citing works
Shu, M., Zhou, Y., Hong, L., Han, H., Zhong, W., Yao, S., Ruan, Z., Yu, D., & Shang, W. (2023) · Clinical and Experimental Obstetrics & Gynecology · doi:10.31083/j.ceog5007137 · Cited by 1 · see citing works
THE EFFECT OF PENTOXIFYLLINE ON THE GROWTH OF ENDOMETRIAL IMPLANTS AND LEUKOCYTES IN RATS
Mohammadzadeh, A., Heidari, M., Haleh, S. G., Novin, M. G., Jeddi‐Tehrani, M., Akhondi, M. M., Zeraati, H., Mohammadzadeh, F., & Ebadi, P. (2007) · TSpace (University of Toronto) · Cited by 1 · see citing works
Role of Endometriosis in Infertility and Embryonic Loss: More than Anatomical Reasons
Wilde, R. L. D. (2017) · Journal of Gynecology and Womens Health · doi:10.19080/jgwh.2017.03.555612 · Cited by 1 · see citing works
Pregnancy and live birth rates in women with endometriosis related infertility in Latvia
Avdotina, J., Mezecka-Oleinika, A., Siliņa, V., & Vitina, Z. (2019) · International Journal of Reproduction Contraception Obstetrics and Gynecology · doi:10.18203/2320-1770.ijrcog20190495 · Cited by 1 · see citing works
Re: Preventing recurrent miscarriage of unknown aetiology
Sathiyathasan, S. (2014) · The Obstetrician & Gynaecologist · doi:10.1111/tog.12069_1
Germeyer, A., von Wolff, M., Jauckus, J., Strowitzki, T., Sharma, T., & Grazul‐Bilska, A. T. (2010)
Clinical assessment of the endometrium
Holoch, K., & Lessey, B. A. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511777851.019
Protein markers for external genital endometriosis
Linde, V. A., Томай, Л. Р., Викторовна, Е. Н., Gunko, V. O., & Pogorelova, T. N. (2016) · Russian Bulletin of Obstetrician-Gynecologist · doi:10.17116/rosakush201616432-35
Prospective evaluation of causes of infertility at a tertiary care hospital
Soni, M. L., & Kumari, S. (2018) · International Journal of Research in Medical Sciences · doi:10.18203/2320-6012.ijrms20184895
Herlambang Herlambang1, F. F. W. (2021) · Medico-Legal Update · doi:10.37506/mlu.v21i1.2331
Morley, L. C., Shillito, J., & Tang, T. H. (2014) · The Obstetrician & Gynaecologist · doi:10.1111/tog.12069_2
Thrombophilia, antiphospholipid antibodies, and anticoagulation in recurrent implantation failure
Cavalcante, M. B., & Barini, R. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-90805-4.00020-1
- Authors
- Tomassetti, C., Meuleman, C., Pexsters, A., Mihalyi, A., Kyama, C., Simsa, P., & D'Hooghe, T.
- Affiliations
- Universitair Ziekenhuis Leuven (BE)
- Venue
- Reproductive BioMedicine Online
- Publisher
- Elsevier BV
- Published
- 2006-01
- Volume
- 13
- Issue
- 1
- Pages
- 58-64
- ISSN
- 1472-6483 (ISSN-L)
- OpenAlex
- W2085072288
- Cited by
- 106
- References
- 67
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 3 · 2023: 6 · 2022: 7 · 2021: 9 · 2020: 5 · 2019: 3 · 2018: 3 · 2017: 5 · 2016: 4 · 2015: 2 · 2014: 7 · 2013: 8 · 2012: 6
- FWCI
- 0.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Reproductive BioMedicine Online (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Keywords
- endometriosis, recurrent pregnancy loss, implantation failure, assisted reproduction, autoantibodies, antiphospholipid antibodies, cell-mediated immunity, humoral immunity, follicular fluid, peritoneal fluid, cytokines, oocyte quality, folliculogenesis, ovulation, infertility
- MeSH terms
- Abortion, Habitual, Autoantibodies, Endometriosis, Endometrium, Female, Fertilization in Vitro, Humans, Immunity, Cellular, Infertility, Female, Embryo Implantation, Pregnancy, Gene Expression, Cytokines, Treatment Failure, Reproductive Techniques, Assisted, Embryonic Development
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