The Double Engines and Single Checkpoint Theory of Endometriosis
Open accessPublished version of a preprint
Abstract
Endometriosis is a chronic disease characterized by the ectopic localization of the endometrial tissue in the peritoneal cavity. Consequently, it causes local pathological changes and systemic symptoms, affecting at least one in every ten women. This disease is difficult to diagnose early, it is prone to dissemination, is difficult to eradicate, tends to recur, and is regarded as “a cancer of no kill”. Indeed, the development of endometriosis closely resembles that of cancer in the way of mutagenesis, pelvic spreading, and immunological adaptation. While retrograde menstruation has been regarded as the primary cause of endometriosis, the role of ovulation and menstrual stimuli in the development of endometriosis has long been overlooked. The development of ovarian and peritoneal endometrioses, similar to the development of high-grade serous carcinoma in the fallopian tube fimbriae with intraperitoneal metastasis, depends highly on the carcinogens released during ovulation. Moreover, endometriosis carries an extremely hypermutated genome, which is non-inferior to the ultra-mutated endometrial cancer. The hypermutation would lead to an overproduction of new proteins or neoantigens. Because of this, the developing endometriosis may have to turn on the PD-1/PDL-1 “self-tolerance” checkpoint to evade immune surveillance, leaving an Achilles tendon for an immune checkpoint blockade. In this review, we present the double engines and single checkpoint theory of the genesis of endometriosis, provide the current pieces of evidence supporting the hypothesis, and discuss the new directions of prevention and treatment.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Yousif, N. G. (2013) · Cell Biology International · doi:10.1002/cbin.10184 · Cited by 109 · see citing works
RetractedIntegrated genomic characterization of endometrial carcinoma
The Cancer Genome Atlas Research Network, & Levine, D. A. (2013) · Nature · doi:10.1038/nature12113 · Cited by 5,784 · see citing works
Patterns of somatic mutation in human cancer genomes
Greenman, C. D., Stephens, P., Smith, R., Dalgliesh, G. L., Hunter, C., Bignell, G. R., Davies, H. R., Teague, J. W., Butler, A. P., Stevens, C., et al. (2007) · Nature · doi:10.1038/nature05610 · Cited by 3,062 · see citing works
Zondervan, K. T., Becker, C. M., & Missmer, S. A. (2020) · New England Journal of Medicine · doi:10.1056/nejmra1810764 · Cited by 2,249 · see citing works
Hundreds of variants clustered in genomic loci and biological pathways affect human height
Lango Allen, H., Estrada, K., Lettre, G., Berndt, S. I., Weedon, M. N., Rivadeneira, F., Willer, C. J., Jackson, A. U., Vedantam, S., Raychaudhuri, S., et al. (2010) · Nature · doi:10.1038/nature09410 · Cited by 1,945 · see citing works
A comprehensive catalogue of somatic mutations from a human cancer genome
Pleasance, E. D., Cheetham, R. K., Stephens, P. J., McBride, D. J., Humphray, S. J., Greenman, C. D., Varela, I., Lin, M.-L., Ordóñez, G. R., Bignell, G. R., et al. (2010) · Nature · doi:10.1038/nature08658 · Cited by 1,696 · see citing works
A decade of immune-checkpoint inhibitors in cancer therapy
Robert, C. (2020) · Nature Communications · doi:10.1038/s41467-020-17670-y · Cited by 1,608 · see citing works
Zondervan, K. T., Becker, C. M., Koga, K., Missmer, S. A., Taylor, R. N., & Viganò, P. (2018) · Nature Reviews Disease Primers · doi:10.1038/s41572-018-0008-5 · Cited by 1,257 · see citing works
(1927) · PubMed Central · Cited by 1,008 · see citing works
(1984) · PubMed · Cited by 997 · see citing works
Clinical diagnosis of endometriosis: a call to action
Agarwal, S. K., Chapron, C., Giudice, L. C., Laufer, M. R., Leyland, N., Missmer, S. A., Singh, S. S., & Taylor, H. S. (2019) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2018.12.039 · Cited by 843 · see citing works
Risk for and consequences of endometriosis: A critical epidemiologic review
Shafrir, A. L., Farland, L. V., Shah, D. K., Harris, H. R., Kvaskoff, M., Zondervan, K., & Missmer, S. A. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.06.001 · Cited by 823 · see citing works
Cancer-associated mutations in endometriosis without cancer
Anglesio, M. S., Papadopoulos, N., Ayhan, A., Nazeran, T. M., Noë, M., Horlings, H. M., Lum, A., Jones, S., Senz, J., Seckin, T., et al. (2017) · New England Journal of Medicine · doi:10.1056/nejmoa1614814 · Cited by 628 · see citing works
Zhang, Y., Xia, M., Jin, K., Wang, S., Wei, H., Fan, C., Wu, Y., Li, X., Li, X., Li, G., et al. (2018) · Molecular Cancer · doi:10.1186/s12943-018-0796-y · Cited by 577 · see citing works
Sunshine, J. C., & Taube, J. M. (2015) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2015.05.011 · Cited by 562 · see citing works
Smolarz, B., Szyłło, K., & Romanowicz, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910554 · Cited by 560 · cited 2× · see citing works
“Epidemiological studies have revealed multiple risk factors for endometriosis [3,10], which can be grouped into two categories, both associate with ovulation.”
BackgroundPhysiology of the Endometrium and Regulation of Menstruation
Critchley, H., Maybin, J. A., Armstrong, G. M., & Williams, A. R. W. (2020) · Physiological Reviews · doi:10.1152/physrev.00031.2019 · Cited by 552 · see citing works
The mutational landscape of normal human endometrial epithelium
Moore, L., Leongamornlert, D., Coorens, T. H. H., Sanders, M. A., Ellis, P., Dentro, S. C., Dawson, K. J., Butler, T., Rahbari, R., Mitchell, T. J., et al. (2020) · Nature · doi:10.1038/s41586-020-2214-z · Cited by 499 · see citing works
Suda, K., Nakaoka, H., Yoshihara, K., Ishiguro, T., Tamura, R., Mori, Y., Yamawaki, K., Adachi, S., Takahashi, T., Kase, H., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.037 · Cited by 414 · see citing works
Oxidative stress and peritoneal endometriosis
Van Langendonckt, A., Casanas-Roux, F., & Donnez, J. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)02959-x · Cited by 391 · see citing works
Petta, C. A., Ferriani, R. A., Abrao, M. S., Hassan, D., Rosa e Silva, J. C., Podgaec, S., & Bahamondes, L. (2005) · Human Reproduction · doi:10.1093/humrep/deh869 · Cited by 363 · see citing works
Vercellini, P., Trespidi, L., Colombo, A., Vendola, N., Marchini, M., & Crosignani, P. G. (1993) · Fertility and Sterility · doi:10.1016/s0015-0282(16)56039-7 · Cited by 311 · see citing works
Risk and prognosis of ovarian cancer in women with endometriosis: a meta-analysis
Kim, H. S., Kim, T. H., Chung, H. H., & Song, Y. S. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.29 · Cited by 307 · see citing works
Epidemiology of endometriosis among parous women
Sangi‐Haghpeykar, H., & POINDEXTERIII, A. (1995) · Obstetrics and Gynecology · doi:10.1016/0029-7844(95)00074-2 · Cited by 288 · see citing works
Periostin: A Matricellular Protein With Multiple Functions in Cancer Development and Progression
González‐González, L., & Alonso, J. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00225 · Cited by 286 · see citing works
Mismatch Repair Pathway, Genome Stability and Cancer
Pećina-Šlaus, N., Kafka, A., Salamon, I., & Bukovac, A. (2020) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2020.00122 · Cited by 247 · see citing works
Leuprolide Acetate Depot and Hormonal Add-Back in Endometriosis: A 12-Month Study
Hornstein, M. D. (1998) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(97)00620-0 · Cited by 244 · see citing works
Endometrial regeneration and endometrial stem/progenitor cells
Gargett, C. E., Nguyen, P. H., & Ye, L. (2012) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-012-9221-9 · Cited by 243 · see citing works
Incidence of symptom recurrence after hysterectomy for endometriosis
Namnoum, A. B., Hickman, T. N., Goodman, S. B., Gehlbach, D. L., & Rock, J. A. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57899-6 · Cited by 238 · see citing works
Reproductive History and Endometriosis Among Premenopausal Women
Missmer, S. A., Hankinson, S. E., Spiegelman, D., Barbieri, R. L., Malspeis, S., Willett, W. C., & Hunter, D. J. (2004) · Obstetrics & Gynecology · doi:10.1097/01.aog.0000142714.54857.f8 · Cited by 237 · see citing works
Proteins of Human Follicular Fluid: The Blood-Follicle Barrier
Shalgi, R., Kraicer, P. F., Rimon, A., Pinto, M., & Soferman, N. (1973) · Fertility and Sterility · doi:10.1016/s0015-0282(16)39730-8 · Cited by 231 · see citing works
Effects of GH/IGF axis on bone and cartilage
Dixit, M., Poudel, S. B., & Yakar, S. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.111052 · Cited by 207 · see citing works
Potential involvement of iron in the pathogenesis of peritoneal endometriosis
Defrere, S., Lousse, J. C., Gonzalez-Ramos, R., Colette, S., Donnez, J., & Van Langendonckt, A. (2008) · Molecular Human Reproduction · doi:10.1093/molehr/gan033 · Cited by 204 · see citing works
Medical treatment of endometriosis-related pain
Vercellini, P., Buggio, L., Frattaruolo, M. P., Borghi, A., Dridi, D., & Somigliana, E. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.01.015 · Cited by 188 · see citing works
Oral contraceptives and risk of endometriosis: a systematic review and meta-analysis
Vercellini, P., Eskenazi, B., Consonni, D., Somigliana, E., Parazzini, F., Abbiati, A., & Fedele, L. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmq042 · Cited by 176 · see citing works
Forster, R., Sarginson, A., Velichkova, A. N., Hogg, C., Dorning, A., Horne, A. W., Saunders, P. T. K., & Greaves, E. (2019) · The FASEB Journal · doi:10.1096/fj.201900797r · Cited by 175 · see citing works
ORIGIN OF PERITONEAL FLUID IN WOMEN: AN OVARIAN EXUDATION PRODUCT
Koninckx, P. R., Renaer, M., & Brosens, I. A. (1980) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1980.tb04514.x · Cited by 172 · see citing works
Greaves, E., Cousins, F., Murray, A., Esnal-Zufiaurre, A., Fassbender, A., Horne, A., & Saunders, P. (2014) · American Journal of Pathology · doi:10.1016/j.ajpath.2014.03.011 · Cited by 170 · see citing works
Insulin-like growth factor system gene expression in human endometrium during the menstrual cycle
Zhou, J., Dsupin, B. A., Giudice, L. C., & Bondy, C. A. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.6.7527408 · Cited by 170 · see citing works
Dienogest in the treatment of endometriosis: systematic review
Andres, M. P., Lopes, L. A., Baracat, E. C., & Podgaec, S. (2015) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-015-3681-6 · Cited by 166 · see citing works
Epidemiologic determinants of endometriosis: A hospital-based case-control study
Signorello, L. B., Harlow, B. L., Cramer, D. W., Spiegelman, D. L., & Hill, J. A. (1997) · Annals of Epidemiology · doi:10.1016/s1047-2797(97)00017-3 · Cited by 163 · see citing works
Shao, C., Li, G., Huang, L., Pruitt, S. K., Castellanos, E. H., Frampton, G. M., Carson, K. R., Snow, T., Singal, G., Fabrizio, D. A., et al. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.25109 · Cited by 155 · see citing works
Menstruation pulls the trigger for inflammation and pain in endometriosis
Laux-Biehlmann, A., d’Hooghe, T., & Zollner, T. M. (2015) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2015.03.004 · Cited by 150 · see citing works
A Review of Immune Checkpoint Blockade Therapy in Endometrial Cancer
Green, A. K., Feinberg, J., & Makker, V. (2020) · American Society of Clinical Oncology Educational Book · doi:10.1200/edbk_280503 · Cited by 146 · see citing works
Muzii, L., Di Tucci, C., Achilli, C., Di Donato, V., Musella, A., Palaia, I., & Panici, P. B. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.08.074 · Cited by 142 · see citing works
Use of integrins to date the endometrium
Lessey, B. A., Castelbaum, A. J., Wolf, L., Greene, W., Paulson, M., Meyer, W. R., & Fritz, M. A. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00604-4 · Cited by 138 · see citing works
Peritoneal endometriosis is an inflammatory disease.
Lousse, J., van Langendonckt, A., Defrère, S., Ramos, R. G., Colette, S., & Donnez, J. (2012) · Frontiers in Bioscience · doi:10.2741/358 · Cited by 137 · see citing works
Ricinoleic acid-based biopolymers
Teomim, D., Nyska, A., & Domb, A. J. (1999) · Journal of Biomedical Materials Research · doi:10.1002/(sici)1097-4636(19990605)45:3 · Cited by 135 · see citing works
KOBAYASHI, H., HIGASHIURA, Y., SHIGETOMI, H., & KAJIHARA, H. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2013.1755 · Cited by 133 · see citing works
Proteomic analysis of human follicular fluid from fertile women
Zamah, A. M., Hassis, M. E., Albertolle, M. E., & Williams, K. E. (2015) · Clinical Proteomics · doi:10.1186/s12014-015-9077-6 · Cited by 132 · see citing works
Endometriosis-associated ovarian neoplasia
Matías‐Guiu, X., & Stewart, C. J. R. (2017) · Pathology · doi:10.1016/j.pathol.2017.10.006 · Cited by 131 · see citing works
Peritoneal endometriosis is an inflammatory disease
Donnez, J. (2012) · Frontiers in Bioscience · doi:10.2741/e358 · Cited by 127 · see citing works
Sugawara, J., Fukaya, T., Murakami, T., Yoshida, H., & Yajima, A. (1997) · Biology of Reproduction · doi:10.1095/biolreprod57.4.936 · Cited by 110 · see citing works
Apter, D. L., Gemzell‐Danielsson, K., Hauck, B., Rosén, K., & Zurth, C. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.03.004 · Cited by 109 · see citing works
Periostin promotes ovarian cancer angiogenesis and metastasis
Zhu, M., Fejzo, M. S., Anderson, L. A., Dering, J., Ginther, C., Ramos, L., Gasson, J. C., Karlan, B. Y., & Slamon, D. J. (2010) · Gynecologic Oncology · doi:10.1016/j.ygyno.2010.07.008 · Cited by 109 · see citing works
Parity and endometrial cancer risk: a meta-analysis of epidemiological studies
Wu, Q., Li, Y., Tu, C., Zhu, J., Qian, K., Feng, T., Li, C., Wu, L., & Ma, X. (2015) · Scientific Reports · doi:10.1038/srep14243 · Cited by 108 · see citing works
Characteristics Related to the Prevalence of Minimal or Mild Endometriosis in Infertile Women
Bérubé, S., Marcoux, S., & Maheux, R. (1998) · Epidemiology · doi:10.1097/00001648-199809000-00006 · Cited by 104 · see citing works
Recurrence of endometriosis after hysterectomy.
(2014) · Europe PMC (PubMed Central) · Cited by 104 · see citing works
Biochemical characterization of peritoneal fluid in women during the menstrual cycle
KONINCKX, P. R., VERHOEVEN, G., VAN BAELEN, H., LISSENS, W. D., DE MOOR, P., & BROSENS, I. A. (1980) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-51-6-1239 · Cited by 101 · see citing works
The Blood-Follicle Barrier (BFB) In Disease and in Ovarian Function
Siu, M. K. Y., & Cheng, C. Y. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-4711-5_9 · Cited by 100 · see citing works
Cancer-associated mutations in endometriosis: shedding light on the pathogenesis and pathophysiology
Guo, S.-W. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmz047 · Cited by 96 · see citing works
The effect of pregnancy on endometriosis-facts or fiction?
Leeners, B., Damaso, F., Ochsenbein-Kölble, N., & Farquhar, C. (2018) · Human Reproduction Update · doi:10.1093/humupd/dmy004 · Cited by 95 · see citing works
Gram, I. T., Norat, T., Rinaldi, S., Dossus, L., Lukanova, A., Téhard, B., Clavel‐Chapelon, F., van Gils, C. H., van Noord, P. A. H., Peeters, P. H. M., et al. (2006) · International Journal of Obesity · doi:10.1038/sj.ijo.0803324 · Cited by 94 · see citing works
Lafay Pillet, M.-C., Schneider, A., Borghese, B., Santulli, P., Souza, C., Streuli, I., de Ziegler, D., & Chapron, C. (2012) · Human Reproduction · doi:10.1093/humrep/der346 · Cited by 91 · see citing works
Surrey, E. S. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00500-7 · Cited by 90 · see citing works
Huang, H.-S., Chu, S., Hsu, C., Chen, P., Ding, D., Chang, M.-Y., & Chu, T. (2015) · Carcinogenesis · doi:10.1093/carcin/bgv132 · Cited by 89 · see citing works
Self-citationIncessant ovulation and ovarian cancer - a hypothesis re-visited.
Fathalla, M. F. (2013) · PubMed · Cited by 87 · see citing works
Sengupta, S., Xiao, Y., & Xu, Y. (2003) · The FASEB Journal · doi:10.1096/fj.02-1145fje · Cited by 83 · see citing works
Hapangama, D. K., Drury, J. A., Silva, L. D., Al‐Lamee, H., Earp, A., Valentijn, A., Edirisinghe, D. P., Murray, P. A., Fazleabas, A. T., & Gargett, C. E. (2018) · Human Reproduction · doi:10.1093/humrep/dey336 · Cited by 82 · see citing works
Khan, K. N., Masuzaki, H., Fujishita, A., Kitajima, M., Sekine, I., & Ishimaru, T. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(02)04535-1 · Cited by 78 · see citing works
Human menstrual blood: a renewable and sustainable source of stem cells for regenerative medicine
Lv, H., Hu, Y., Cui, Z., & Jia, H. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-1067-y · Cited by 78 · see citing works
Independent development of endometrial epithelium and stroma within the same endometriosis
Noë, M., Ayhan, A., Wang, T., & Shih, I. (2018) · The Journal of Pathology · doi:10.1002/path.5082 · Cited by 77 · see citing works
Nilsson, C. G., Lähteenmäki, P., & Luukkainen, T. (1980) · Contraception · doi:10.1016/0010-7824(80)90003-7 · Cited by 76 · see citing works
Li, X., Zhang, Y., Zhao, L., Wang, L., Wu, Z., Mei, Q., Nie, J., Li, X., Li, Y., Fu, X., et al. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu330 · Cited by 74 · see citing works
Principe, N., Kidman, J., Goh, S., Tilsed, C. M., Fisher, S. A., Fear, V. S., Forbes, C. A., Zemek, R. M., Chopra, A., Watson, M. W., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.584423 · Cited by 74 · see citing works
Gonadotropin-releasing hormone agonist and add-back therapy: what do the data show?
Surrey, E. S. (2010) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e32833b35a7 · Cited by 64 · see citing works
Chen, Y.-J., Hsu, T.-F., Huang, B.-S., Tsai, H.-W., Chang, Y.-H., & Wang, P.-H. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.02.008 · Cited by 64 · see citing works
Yoshida, S., Harada, T., Mitsunari, M., Iwabe, T., Sakamoto, Y., Tsukihara, S., Iba, Y., Horie, S., & Terakawa, N. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030874 · Cited by 63 · see citing works
Wu, L., Lv, C., Su, Y.-F., Li, C., Zhang, H., Zhao, X., & Li, M. (2018) · Gynecological Endocrinology · doi:10.1080/09513590.2018.1519787 · Cited by 60 · see citing works
Kauma, S. W., Clark, M. R., White, C., & Halme, J. K. (1988) · PubMed · Cited by 55 · see citing works
Koninckx, P., Ussia, A., Tahlak, M., Adamyan, L. V., Wattiez, A., Martin, D. C., & Gomel, V. (2019) · PubMed Central · Cited by 52 · see citing works
(1982) · PubMed · Cited by 52 · see citing works
IGF-axis confers transformation and regeneration of fallopian tube fimbria epithelium upon ovulation
Hsu, C., Huang, H.-S., Chen, P., Ding, D., & Chu, T. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.01.061 · Cited by 51 · see citing works
Self-citationWu, N., Fang, C., Huang, H.-S., Wang, J., & Chu, T. (2019) · Modern Pathology · doi:10.1038/s41379-019-0370-1 · Cited by 51 · see citing works
Self-citationZhou, Y., Zeng, C., Li, X., Wu, P., Yin, L., Yu, X., Zhou, Y., & Xue, Q. (2016) · Journal of Molecular Medicine · doi:10.1007/s00109-016-1396-1 · Cited by 44 · see citing works
Huang, H., Hsu, C., Chu, S., Chen, P., Ding, D., Chang, M., & Chu, T. (2016) · The Journal of Pathology · doi:10.1002/path.4807 · Cited by 38 · see citing works
Self-citationKHAN, K. N., MASUZAKI, H., FUJISHITA, A., KITAJIMA, M., HIRAKI, K., MIURA, S., SEKINE, I., & ISHIMARU, T. (2006) · Acta Obstetricia et Gynecologica Scandinavica · doi:10.1080/00016340500432556 · Cited by 36 · see citing works
Koninckx, P. R., Ussia, A., Tahlak, M., Adamyan, L., Wattiez, A., Martin, D. C., & Gomel, V. (2019) · Lirias · Cited by 34 · see citing works
Hsu, C., Chen, P., Seenan, V., Ding, D., & Chu, T. (2021) · Cancers · doi:10.3390/cancers13030468 · Cited by 32 · see citing works
Self-citationIncreased levels of laminin in ascitic fluid of patients with ovarian cancer
Byers, L. J., Osborne, J. L., Carson, L. F., Carter, J. R., Haney, A. F., Weinberg, J. B., & Ramakrishnan, S. (1995) · Cancer Letters · doi:10.1016/0304-3835(94)03625-s · Cited by 29 · see citing works
Peritoneal fluid progesterone and progesterone resistance in superficial endometriosis lesions
Koninckx, P. R., Ussia, A., Adamyan, L. V., Gomel, V., & Martin, D. C. (2021) · Human Reproduction · doi:10.1093/humrep/deab258 · Cited by 28 · see citing works
Koninckx, P. R., Ussia, A., Adamyan, L. V., Wattiez, A., Gomel, V., & Martin, D. C. (2019) · Europe PMC (PubMed Central) · Cited by 27 · see citing works
Postoperative desogestrel for pelvic endometriosis-related pain: a randomized controlled trial
Tanmahasamut, P., Saejong, R., Rattanachaiyanont, M., Angsuwathana, S., Techatraisak, K., & Sa‐nga‐areekul, N. (2017) · Gynecological Endocrinology · doi:10.1080/09513590.2017.1296124 · Cited by 22 · see citing works
Bone marrow-derived stem cells contribute to regeneration of the endometrium
Lee, Y. J., & Yi, K. W. (2018) · Daehan saengsik uihak hoeji/Clinical and experimental reproductive medicine · doi:10.5653/cerm.2018.45.4.149 · Cited by 22 · see citing works
Determination of HGF concentration in serum and peritoneal fluid in women with endometriosis.
Zong, L., Li, Y., & Ha, X.-Q. (2003) · PubMed · Cited by 20 · see citing works
Huang, H.-S., Chen, P., Chu, S., Lee, M., Huang, C.-Y., & Chu, T. (2021) · Neoplasia · doi:10.1016/j.neo.2021.09.006 · Cited by 19 · see citing works
Self-citationGuo, Q., Zhu, L., Wang, C., Wang, S., Nie, X., Liu, J., Liu, Q., Hao, Y., Li, X., & Lin, B. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00954 · Cited by 19 · see citing works
Kavoussi, S. K., Odenwald, K. C., As‐Sanie, S., & Lebovic, D. I. (2017) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2017.06.028 · Cited by 17 · see citing works
Determination of follicular fluid estradiol levels by enzyme-linked immunosorbent assay
Silván, G., Illera, J. C., & Illera, M. (1993) · Steroids · doi:10.1016/0039-128x(93)90092-2 · Cited by 17 · see citing works
Age-Parity-Season Adjustment Factors for Milk and Fat Yields of Dairy Goats
Finley, C. M., Thompson, J. R., & Bradford, G. E. (1984) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(84)81516-7 · Cited by 16 · see citing works
Letrozole promotes the expression of integrin αvβ3 and HOXA10 in endometrium of endometriosis
Zhang, J., Wang, L., Li, C., Zhang, H., Li, R., & Li, M. (2021) · Systems Biology in Reproductive Medicine · doi:10.1080/19396368.2021.2013577 · Cited by 15 · see citing works
Evaluation of fibronectin as a marker of malignant ascites
SIDDIQUI, R. A., Kochhar, R. K., Singh, V., Rajwanshi, A., Goenka, M. K., & Mehta, S. K. (1992) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.1992.tb00955.x · Cited by 15 · see citing works
Preoperative imaging of deep endometriosis: pitfalls of a diagnostic test before surgery.
Koninckx, P. R., Deslandes, A., Ussia, A., Giovanni, A. D., Hanan, G., Tahlak, M., Адамян, Л. В., Keckstein, J., & Wattiez, A. (2021) · PubMed Central · Cited by 15 · see citing works
HGF and c-Met in pathogenesis of endometrial carcinoma
Wang, H. (2015) · Frontiers in bioscience · doi:10.2741/4328 · Cited by 14 · see citing works
Arici, A. M., Matalliotakis, I., Goumenou, A. G., Koumantakis, G. E., Fragouli, Y. G., & MAHUTTE, N. G. (2003) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2003.01164.x · Cited by 13 · see citing works
Honda, T., Fujiwara, H., Yoshioka, S., Yamada, S., Nakayama, T., Egawa, M., Nishioka, Y., Takahashi, A., & Fujii, S. (2004) · Reproductive Medicine and Biology · doi:10.1111/j.1447-0578.2004.00051.x · Cited by 13 · see citing works
Origin of Peritoneal Fluid in Women: An Ovarian Exudation Product
Koninckx, P. R., Renaer, M., & Brosens, I. A. (1980) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-198010000-00015 · Cited by 12 · see citing works
Şahin, N., Toylu, A., Gülekli, B., Doğan, E., Kovalı, M., & Atabey, N. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.08.059 · Cited by 12 · see citing works
Tanaka, T., Mizuno, K., Umesaki, N., & Ogita, S. (1998) · PubMed · Cited by 11 · see citing works
Schneider, G., Suszyńska, M., Kakar, S. S., & Ratajczak, M. Z. (2016) · Journal of Cancer Stem Cell Research · doi:10.14343/jcscr.2016.4e1005 · Cited by 10 · see citing works
Plaino, L., Stomati, M., Casarosa, E., Artini, P. G., Santuz, M., D’Ambrogio, G., Cobellis, L., Luisi, M., Genazzani, A. R., & Petraglia, F. (2000) · Gynecological Endocrinology · doi:10.3109/09513590009167686 · Cited by 8 · see citing works
Clinical significance of serum laminin levels in patients with lung cancer
Taş, F., Bilgin, E., Taştekin, D., Ertürk, K., & Duranyıldız, D. (2016) · Biomedical Reports · doi:10.3892/br.2016.612 · Cited by 7 · see citing works
Nishihira, H., & Kigasawa, H. (1981) · British Journal of Haematology · doi:10.1111/j.1365-2141.1981.tb07264.x · Cited by 6 · see citing works
Eiden, L. E., Rausch, D. M., da Cunha, A., Murray, E. A., Heyes, M. P., Sharer, L. R., Nöhr, D., & Weihe, E. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb26271.x · Cited by 6 · see citing works
Řežábek, K., Moosová, M., Pavelková, J., Moos, J., & Filova, V. (2009) · PubMed · Cited by 3 · see citing works
Association of IGF axis hormones with waist-to-hip ratio varies by physical activity.
Schmitz, K. H., Xie, D., Teal, V. L., Ballard-Barbash, R. R., & Berrigan, D. A. (2011) · PubMed · Cited by 2 · see citing works
Kwasniewski, W., Stupak, A., Wolun-Cholewa, M., Fronczek, A., Kwasniewska, A., Kotarski, J., Polak, G., & Gozdzicka-Jozefiak, A. (2021) · Ginekologia Polska · doi:10.5603/gp.a2021.0210 · Cited by 1 · see citing works
Flagged first, then by citations
4 of the 121 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Epigenetic regulation and T-cell responses in endometriosis – something other than autoimmunity
Szukiewicz, D. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.943839 · Cited by 64 · see citing works
Endometriosis and ovulatory menstruation: beyond the Sampson principle
Bulun, S. E. (2025) · Journal of Clinical Investigation · doi:10.1172/jci188787 · Cited by 28 · see citing works
Heme induced progesterone-resistant profiling and promotion of endometriosis in vitro and in vivo
Ma, X.-Q., Liu, Y.-Y., Zhong, Z.-Q., Chen, S., Hu, W., Sheng, Y., Liu, Y., Wei, C., Li, M., & Zhu, X. (2023) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2023.166761 · Cited by 15 · see citing works
Divergent Immune–Metabolic Profiles in Endometriosis and Ovarian Cancer: A Cross-Sectional Analysis
Neri, M., Sanna, E., Ferrari, P. A., Madeddu, C., Lai, E., Vallerino, V., & Macciò, A. (2025) · Cancers · doi:10.3390/cancers17142325 · Cited by 11 · see citing works
CCL2/CCR4 participates in mast cell-mediated epithelial mesenchymal transition in endometriosis
Ding, S., Mao, X., Zhu, L., Xu, X., Chen, S., Zou, G., Xu, P., Wang, J., & Zhang, X. (2025) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2025.104796 · Cited by 5 · see citing works
Hsu, C., Seenan, V., Manickam, S. P., Wang, L.-Y., Chang, Y.-C., Chen, Y.-H., Ding, D., Chen, P., & Chu, T. (2025) · Tzu Chi Medical Journal · doi:10.4103/tcmj.tcmj_90_25 · Cited by 1 · see citing works
Self-citationPeripheral blood leukocyte Telomere length and endometriosis: A Mendelian randomization study
Wang, Y., Sun, F., Yue, C., & Man, Q. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e33854 · Cited by 1 · see citing works
Peng, Y., Wang, L., Tan, A., Wang, S., Zou, W., Li, X., & Yang, J. (2025) · Current Medical Science · doi:10.1007/s11596-025-00125-0 · Cited by 1 · see citing works
Machine Learning-Based Diagnosis And Modeling Research in EndometriosisPreprint
Yang, Y., Huang, Y., Wang, Y., & Li, R. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4874442
Associations between granulysin and ovarian endometriosis: A 2-sample Mendelian randomization study
Lai, B., Yu, M., Liao, Y., Zhou, G., Liu, L., Shan, Z., & Fan, J. (2026) · Medicine · doi:10.1097/md.0000000000049618
Li, X., Wang, Z., He, Y., Wang, S., Liu, P., Wu, J., & Yu, S. (2026) · Clinical and Experimental Obstetrics & Gynecology · doi:10.31083/ceog48963
Phytochemicals Modulating Receptor Tyrosine Kinase Signaling Networks in Endometriosis
Hsu, C., & Weng, C. (2026) · Pharmaceuticals · doi:10.3390/ph19091413
Self-citation
- Authors
- Hsu, C.-F., Khine, A. A., Huang, H.-S., & Chu, T.-Y.
- Affiliations
- Tzu Chi Foundation (TW)
- Tzu Chi University (TW)
- Corresponding author
- Hsu, Che-Fang
- Venue
- Biomedicines
- Publisher
- MDPI AG
- Published
- 2022-06-14
- Volume
- 10
- Issue
- 6
- Pages
- 1403
- ISSN
- 2227-9059 (ISSN-L)
- PMC
- PMC9219825
- OpenAlex
- W4282914803
- Cited by
- 12
- References
- 121
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 2 · 2023: 1 · 2022: 1
- FWCI
- 0.36
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Biomedicines (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Ministry of Science and Technology, Taiwan, ROC (MOST 107-2314-B-303-013-MY3, MOST 110-2314-B-303-008, TCMMP108-01-01)
- Buddhist Tzu Chi General Hospital, Taiwan, ROC (MOST 107-2314-B-303-013-MY3, MOST 110-2314-B-303-008, TCMMP108-01-01)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, retrograde menstruation, ovulation, endometrioma, peritoneal endometriosis, hypermutation, neoantigens, PD-1/PD-L1 immune checkpoint, immune evasion, immune checkpoint blockade, carcinogenesis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review