Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis
Open accessAbstract
Objective To evaluate basal (constitutive) and stimulated synthesis of tumor necrosis factor alpha (TNF alpha), interleukin (IL)-8, IL-10 by peritoneal macrophages (PM) in women with endometriosis.Design Peritoneal macrophages were cultured in the presence or absence of lipopolysaccharide (LPS) for 24 hours. Peritoneal fluids (PF) and PM supernatants were assayed for cytokines using ELISA.Setting Institute for the Study and Treatment of Endometriosis and university-based research laboratories.Subjects Fertile controls undergoing tubal ligation (n = 8) and women with endometriosis (n = 17).Intervention Peritoneal fluid samples were obtained at the time of diagnostic laparoscopy (endometriosis group) or laparoscopy for tubal ligation; both were performed in the midluteal phase of the cycle.Results Both basal and LPS stimulated production of TNF alpha, IL-8, and IL-10 by the PM were elevated significantly in women with endometriosis as compared with the fertile controls.Conclusions This study demonstrated that cytokines TNF alpha, IL-8, and IL-10 are synthesized at greater than normal levels by basal and stimulated PM from women with endometriosis. The levels of TNF alpha and IL-8 correlated with the levels in the PF, suggesting that PM are the principal source of these cytokines in the PF.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Implantation in the peritoneum is explained by a local disorder of the mechanisms that prevent adhesion, with increased production of cytokine macrophages including tumor necrosis factor α and interleukin.
“Implantation in the peritoneum is explained by a local disorder of the mechanisms that prevent adhesion. The consequence is an increased production of cytokine macrophages, including tumor necrosis factor α (TNF-α) and interleukin [55].”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [55]
Cites
Interleukin-10-deficient mice develop chronic enterocolitis
Kühn, R., Löhler, J., Rennick, D. M., Rajewsky, K., & Müller, W. (1993) · Cell · doi:10.1016/0092-8674(93)80068-p · Cited by 4,248 · see citing works
de Waal Malefyt, R., Abrams, J., Bennett, B., Figdor, C. G., & de Vries, J. E. (1991) · The Journal of experimental medicine · doi:10.1084/jem.174.5.1209 · Cited by 3,762 · see citing works
Interleukin-8 as a macrophage-derived mediator of angiogenesis
Koch, A. E., Polverini, P. J., Kunkel, S. L., Harlow, L. A., DiPietro, L. A., Elner, V. M., Elner, S. G., & Strieter, R. M. (1992) · Science · doi:10.1126/science.1281554 · Cited by 2,135 · see citing works
Revised American Fertility Society Classification of Endometriosis: 1985
(1985) · Fertility and Sterility · doi:10.1016/s0015-0282(16)48430-x · Cited by 1,803 · see citing works
The Biology Of Cachectin/TNF: A Primary Mediator Of The Host Response
Beutler, B., & Cerami, A. (1989) · Annual Review of Immunology · doi:10.1146/annurev.iy.07.040189.003205 · Cited by 1,684 · see citing works
Cachectin and tumour necrosis factor as two sides of the same biological coin
Beutler, B., & Cerami, A. (1986) · Nature · doi:10.1038/320584a0 · Cited by 1,633 · see citing works
Properties and Functions of Interleukin-10
Mosman, T. R. (1994) · Advances in immunology · doi:10.1016/s0065-2776(08)60449-6 · Cited by 495 · see citing works
Interleukin‐1: A possible role in the infertility associated with endometriosis
Fakih, H., Baggett, B., & Holtz, G. (1988) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(88)90224-x · Cited by 319 · see citing works
Halme, J. K., Becker, S., & Haskill, S. (1987) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(87)90333-4 · Cited by 289 · see citing works
Interleukin-1: a possible role in the infertility associated with endometriosis
Fakih, H., Baggett, B., Holtz, G., Tsang, K.-Y., Lee, J. C., & Williamson, H. O. (1987) · Fertility and Sterility · doi:10.1016/s0015-0282(16)49993-0 · Cited by 285 · see citing works
Tumor necrosis factor in peritoneal fluid of women undergoing laparoscopic surgery
Eisermann, J., Gast, M. J., Pineda, J. A., Odem, R. R., & Collins, J. L. (1988) · Fertility and Sterility · doi:10.1016/s0015-0282(16)60185-1 · Cited by 276 · see citing works
TABIBZADEH, S. S., Santhanam, U., Sehgal, P. B., & May, L. T. (1989) · The Journal of Immunology · doi:10.4049/jimmunol.142.9.3134 · Cited by 261 · see citing works
Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis
Khorram, O., Taylor, R. N., Ryan, I. P., Schall, T. J., & LANDERS, D. V. (1993) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(93)90433-j · Cited by 244 · see citing works
Interleukin-8 concentrations are elevated in peritoneal fluid of women with endometriosis
Ryan, I. P., Tseng, J. F., Schriock, E. D., Khorram, O., Landers, D. V., & Taylor, R. N. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57506-2 · Cited by 222 · see citing works
Peritoneal Macrophages From Patients With Endometriosis Release Growth Factor Activityin Vitro*
Halme, J. K., WHITE, C., Kauma, S. W., Estes, J. E., & Haskill, S. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-66-5-1044 · Cited by 179 · see citing works
Cytokines and the response to infection
van Deuren, M., Dofferhoff, A. S. M., & van der Meer, J. W. M. (1992) · The Journal of Pathology · doi:10.1002/path.1711680403 · Cited by 156 · see citing works
Release of tumor necrosis factor-α by human peritoneal macrophages in vivo and in vitro
Halme, J. K. (1989) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(89)90957-5 · Cited by 155 · see citing works
Betjes, M. G. H., Tuk, C. W., Struijk, D. G., Krediet, R. T., Arisz, L., Hart, M. H. L., & Beelen, R. H. J. (1993) · The Journal of Infectious Diseases · doi:10.1093/infdis/168.5.1202 · Cited by 123 · see citing works
Elevated interleukin-6 levels in peritoneal fluid of patients with pelvic pathology
Buyalos, R. P., Funari, V. A., Azziz, R., Watson, J. M., & Martı́nez-Maza, O. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55216-9 · Cited by 102 · see citing works
Hill, J. A., & Anderson, D. J. (1989) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(89)90736-9 · Cited by 101 · see citing works
Cytokines in the peritoneal fluid of patients with endometriosis
Koyama, N., Matsuura, K., & Okamura, H. (1993) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(93)90273-y · Cited by 76 · see citing works
Mononuclear phagocytes : biology of monocytes and macrophages
van Furth, R. (1992) · Kluwer Academic Publishers eBooks · Cited by 45 · see citing works
Braun, D. P., & Harris, J. E. (1981) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/67.4.809 · Cited by 40 · see citing works
Human resident peritoneal macrophages: phenotype and biology
Eischen, A., Duclos, B., Schmitt‐Goguel, M., Rouyer, N., Jp, B., Hummel, M., Oskam, R., & Oberling, F. (1994) · British Journal of Haematology · doi:10.1111/j.1365-2141.1994.tb05109.x · Cited by 38 · see citing works
Interleukin-8: a chemotactic cytokine produced by macrophages and tissue cells
Baggiolini, M. (1992) · Springer eBooks · doi:10.1007/978-94-015-8070-0_45 · Cited by 4 · see citing works
Tumor necrosis factor. Induction and biological effects in humans
van Leenen, D., van der Poll, T., & van Deventer, S. J. H. (1992) · Springer eBooks · doi:10.1007/978-94-015-8070-0_46 · Cited by 2 · see citing works
Flagged first, then by citations
1 of the 27 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Pathogenesis and pathophysiology of endometriosis
Burney, R. O., & Giudice, L. C. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.06.029 · Cited by 1,590 · see citing works
“In women with endometriosis, the peritoneal fluid is remarkable for an increased number of activated macrophages and important differences in the cytokine/chemokine profile (78).”
Nisolle, M., & Donnez, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00191-x · Cited by 1,279 · see citing works
Endometriosis and infertility: pathophysiology and management
de Ziegler, D., Borghese, B., & Chapron, C. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60490-4 · Cited by 836 · see citing works
Endometriosis: epidemiology and aetiological factors
Viganò, P., Parazzini, F., Somigliana, E., & Vercellini, P. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.01.007 · Cited by 718 · see citing works
Role of cytokines in endometriosis
Harada, T., Iwabe, T., & Terakawa, N. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01816-7 · Cited by 567 · see citing works
Smolarz, B., Szyłło, K., & Romanowicz, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910554 · Cited by 560 · see citing works
Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial
Bedaiwy, M. A. (2002) · Human Reproduction · doi:10.1093/humrep/17.2.426 · Cited by 485 · see citing works
“Several studies have shown that TNF-α levels are increased in the PF of women with endometriosis (Eisermann et al., 1988; Mori et al., 1991; Taketani et al., 1992; Overton et al., 1996; Rana et al., 1996).”
BackgroundPeritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis
Gazvani, R., & Templeton, A. (2002) · Reproduction · doi:10.1530/rep.0.1230217 · Cited by 393 · see citing works
The 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
Angiogenic Factors in Endometriosis
Taylor, R. N., Lebovic, D. I., & Mueller, M. D. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02769.x · Cited by 304 · see citing works
Vinatier, D., Orazi, G., Cosson, M., & Dufour, P. (2001) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00405-x · Cited by 299 · see citing works
Behaviour of Cytokine Levels in Serum and Peritoneal Fluid of Women with Endometriosis
Pizzo, A., Salmeri, F. M., Ardita, F. V., Sofo, V., Tripepi, M., & Marsico, S. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000067717 · Cited by 285 · see citing works
Zeitvogel, A., Baumann, R., & Starzinski‐Powitz, A. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63030-1 · Cited by 275 · see citing works
Qazi, B. S., Tang, K., & Qazi, A. S. (2011) · International Journal of Inflammation · doi:10.4061/2011/908468 · Cited by 271 · see citing works
“The concentration of IL-8 in the peritoneal fluid was higher in women with endometriosis compared to women without, and that difference was statistically significant as has been reported previously [106, 107].”
BackgroundResultEndometriotic disease: the role of peritoneal fluid
Koninckx, P. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.741 · Cited by 252 · see citing works
Potential involvement of the immune system in the development of endometriosis
Kyama, C. M., Debrock, S., Mwenda, J. M., & D'Hooghe, T. M. (2003) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-1-123 · Cited by 244 · see citing works
The relationship of endometriosis and ovarian malignancy: a review
Nezhat, F. R., Datta, M., Hanson, V., Pejovic, T. B., Nezhat, C., & NEZHAT, C. R. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.08.007 · Cited by 246 · 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
Immune 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
“Specifically, a decrease in NK cell cytotoxicity [41,42] and an enhanced activation state of monocytes and peritoneal macrophages has been documented in endometriosis patients [43–45].”
BackgroundDairy-food, calcium, magnesium, and vitamin D intake and endometriosis: a prospective cohort study
Harris, H. R., Chavarro, J. E., Malspeis, S., Willett, W. C., & Missmer, S. A. (2013) · American Journal of Epidemiology · doi:10.1093/aje/kws247 · Cited by 223 · see citing works
Dmowski, W. P., & Braun, D. P. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.02.001 · Cited by 225 · see citing works
Uterine Chemokines in Reproductive Physiology and Pathology
Kayisli, U. A., MAHUTTE, N. G., & Arici, A. M. (2002) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2002.01075.x · Cited by 222 · see citing works
Endometriosis and Mechanisms of Pelvic Pain
Howard, F. M. (2009) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2009.06.017 · Cited by 218 · see citing works
Lin, Y., Lai, M.-D., Lei, H.-Y., & Wing, L.-Y. C. (2005) · Endocrinology · doi:10.1210/en.2005-0790 · Cited by 218 · see citing works
The link between immunity, autoimmunity and endometriosis: a literature update
Zhang, T., De Carolis, C., Man, G. C. W., & Wang, C. C. (2018) · Autoimmunity Reviews · doi:10.1016/j.autrev.2018.03.017 · Cited by 196 · see citing works
Endometriosis: A dysfunction and disease of the archimetra
Leyendecker, G. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.752 · Cited by 199 · see citing works
“Attracted and activated monocytes/ macrophages secrete many angiogenic and other growth factors and stimulate stromal proliferation and the production of pro-inflammatory molecules (Halme et al., 1988; Olive et al., 1991; Braun et al., 1996; McLaren et al., 1996; Rana et al., 1996).”
Regulation of Inflammation Pathways and Inflammasome by Sex Steroid Hormones in Endometriosis
García-Gómez, E., Vázquez-Martínez, E. R., Reyes-Mayoral, C., Cruz-Orozco, O., Camacho‐Arroyo, I., & Cerbón, M. A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00935 · Cited by 198 · see citing works
Escherichia coli contamination of menstrual blood and effect of bacterial endotoxin on endometriosis
Khan, K. N., Kitajima, M., Hiraki, K., Yamaguchi, N., Katamine, S., Matsuyama, T., Nakashima, M., Fujishita, A., Ishimaru, T., & Masuzaki, H. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.04.053 · Cited by 195 · see citing works
Involvement of the nuclear factor-κB pathway in the pathogenesis of endometriosis
González-Ramos, R., Van Langendonckt, A., Defrère, S., Lousse, J.-C., Colette, S., Devoto, L., & Donnez, J. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.01.013 · Cited by 179 · see citing works
Endometriosis-Associated Ovarian Cancer: A Review of Pathogenesis
Worley, M. J., Welch, W., Berkowitz, R. S., & Ng, S. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14035367 · Cited by 175 · see citing works
“In women with endometriosis, the peritoneal fluid often contains an increased number of activated macrophages [61].”
BackgroundFiligheddu, N., Gregnanin, I., Porporato, P. E., Surico, D., Perego, B., Galli, L., Patrignani, C., Graziani, A., & Surico, N. (2010) · Journal of Biomedicine and Biotechnology · doi:10.1155/2010/369549 · Cited by 162 · see citing works
Peritoneal Cellular Immunity and Endometriosis
Ho, H., Wu, M., & Yang, Y. (1997) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1997.tb00319.x · Cited by 160 · see citing works
Differential macrophage infiltration in early and advanced endometriosis and adjacent peritoneum
Khan, K. N., Masuzaki, H., Fujishita, A., Kitajima, M., Sekine, I., & Ishimaru, T. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.07.037 · Cited by 161 · see citing works
Chemokines and human reproduction
García-Velasco, J. A., & Arici, A. M. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00120-x · Cited by 160 · see citing works
Current Concepts in the Pathogenesis of Endometriosis
Witz, C. A. (1999) · Clinical Obstetrics & Gynecology · doi:10.1097/00003081-199909000-00013 · Cited by 151 · see citing works
González-Ramos, R., Defrère, S., & Devoto, L. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.06.021 · Cited by 148 · see citing works
Current concepts of the pathogenesis of endometriosis
Osuga, Y. (2009) · Reproductive Medicine and Biology · doi:10.1007/s12522-009-0031-z · Cited by 147 · see citing works
Kyama, C. M., Overbergh, L., Debrock, S., Valckx, D., Perre, S. V., Meuleman, C., Mihalyi, A., Mwenda, J. M., Mathieu, C., & D’Hooghe, T. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.11.060 · Cited by 146 · see citing works
Guo, S. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000096047 · Cited by 140 · see citing works
Montagna, P., Capellino, S., Villaggio, B., Remorgida, V., Ragni, N., Cutolo, M., & Ferrero, S. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.11.200 · Cited by 135 · see citing works
Akoum, A. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)84754-1 · Cited by 132 · see citing works
Imbalance between sympathetic and sensory innervation in peritoneal endometriosis
Arnold, J., Barcena de Arellano, M. L., Rüster, C., Vercellino, G. F., Chiantera, V., Schneider, A., & Mechsner, S. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2011.08.004 · Cited by 132 · see citing works
New considerations for the pathogenesis of endometriosis
Gazvani, R., & Templeton, A. (2002) · International Journal of Gynecology & Obstetrics · doi:10.1016/s0020-7292(01)00577-x · Cited by 127 · see citing works
Tsudo, T., Harada, T., Iwabe, T., Tanikawa, M., Nagano, Y., Ito, M., Taniguchi, F., & Terakawa, N. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00496-3 · Cited by 124 · see citing works
Angiogenesis and antiangiogenic therapy in endometriosis
Becker, C. M., & D’Amato, R. J. (2007) · Microvascular Research · doi:10.1016/j.mvr.2007.04.008 · Cited by 122 · see citing works
Endometriosis: abnormal endometrium and dysfunctional immune response
Braun, D. P., & Dmowski, W. P. (1998) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-199810000-00003 · Cited by 123 · see citing works
The Role of the Lymphatic System in Endometriosis: A Comprehensive Review of the Literature1
Jerman, L. F., & Hey-Cunningham, A. J. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.114.124313 · Cited by 122 · see citing works
The M2a macrophage subset may be critically involved in the fibrogenesis of endometriosis in mice
Duan, J., Liu, X., Wang, H., & Guo, S.-W. (2018) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2018.05.017 · Cited by 121 · see citing works
D'Antonio, M., Martelli, F., Peano, S., Papoian, R., & Borrelli, F. (2000) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(00)00073-5 · Cited by 119 · see citing works
“Therefore IL-8, with its proinflammatory, growth-promoting and angiogenic properties, might be an important factor responsible for neo-vascularization and, along with TNF-a, for the inflammation in and around the ectopic endometrial lesions (Rana et al., 1996; Gazvani et al., 1998).”
BackgroundResultSikora, J., Smycz‐Kubańska, M., Mielczarek‐Palacz, A., & Kondera‐Anasz, Z. (2017) · American Journal of Reproductive Immunology · doi:10.1111/aji.12622 · Cited by 118 · see citing works
Is endometriosis an endometrial disease?
Vinatier, D., Cosson, M., & Dufour, P. (2000) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(99)00263-8 · Cited by 115 · see citing works
Gazvani, M. R., Christmas, S. E., Quenby, S. M., Kirwan, J. P., Johnson, P. M., & Kingsland, C. R. (1998) · Human Reproduction · doi:10.1093/humrep/13.7.1957 · Cited by 114 · see citing works
Immunological aspects of endometriosis
Vinatier, D. (1996) · Human Reproduction Update · doi:10.1093/humupd/2.5.371 · Cited by 113 · see citing works
“Furthermore, peritoneal fluid concentrations of IL-8 in women with endometriosis correlate with IL-8 production by peritoneal macrophages (Rana et al., 1996).”
BackgroundRole of inflammation in benign gynecologic disorders: from pathogenesis to novel therapies†
AlAshqar, A., Reschke, L. D., Kirschen, G. W., & Borahay, M. A. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab054 · Cited by 121 · see citing works
Endometriosis and Infertility: New Concepts
Ryan, I. P., & Taylor, R. N. (1997) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-199706000-00021 · Cited by 106 · see citing works
Suen, J., Chang, Y., Chiu, P.-R., Hsieh, T., Hsi, E., Chen, Y., Chen, Y., & Tsai, E. (2013) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.10.023 · Cited by 103 · see citing works
Can chemokines be used as biomarkers for endometriosis? A systematic review
Borrelli, G. M., Abrao, M. S., & Mechsner, S. (2014) · Human Reproduction · doi:10.1093/humrep/det401 · Cited by 102 · see citing works
Said, T. M., Agarwal, A. K., Falcone, T., Sharma, R. K., Bedaiwy, M. A., & Li, L. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.11.068 · Cited by 102 · see citing works
Role of eutopic endometrium in pelvic endometriosis
Carvalho, L., Podgaec, S., Bellodi-Privato, M., Falcone, T., & Abrão, M. S. (2011) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2011.03.009 · Cited by 99 · see citing works
“These inflammatory factors may form part of the pathogenesis of endometriosis [78,79].”
BackgroundDmowski, W. P. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.696 · Cited by 101 · see citing works
“It is relevant that the PM, while unable to mediate destruction of ectopic endometrial cells, can serve as a principal source of TNF-α and possibly other growth-enhancing signals (Rana et al., 1996).”
BackgroundBain, C. C., Gibson, D. A., Steers, N. J., Boufea, K., Louwe, P. A., Doherty, C., González-Huici, V., Gentek, R., Magalhaes-Pinto, M., Shaw, T., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abc4466 · Cited by 97 · see citing works
“3 clusters of resident 30 macrophages (3-5) could be identified on the basis of their high expression of Adgre1 (F4/80) and Icam2 31 (CD102).”
BackgroundSiristatidis, C. S., Nissotakis, C., Chrelias, C., Iacovidou, H., & Salamalekis, E. (2006) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2006.00373.x · Cited by 93 · see citing works
RetractedNematian, S., Mamillapalli, R., Kadakia, T. S., Zolbin, M. M., Moustafa, S. M., & Taylor, H. S. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-01199 · Cited by 94 · see citing works
“Consistent with that finding, peritoneal macrophages secrete more IL-8, IL-10, and TNF-a in patients with endometriosis compared with healthy controls (25, 27).”
BackgroundResultSakr, S., Naqvi, H., Komm, B., & Taylor, H. S. (2014) · Endocrinology · doi:10.1210/en.2013-1977 · Cited by 91 · see citing works
Cao, W. G., Morin, M., Metz, C. N., Maheux, R., & Akoum, A. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.104.038331 · Cited by 91 · see citing works
“These inflammatory cells were shown to overproduce IL1 compared with that of cells from normal women [19].”
BackgroundEndometriosis and human infertility: a new investigation into the role of eutopic endometrium
Minici, F., Tiberi, F., Tropea, A., Orlando, M., Gangalè, M. F., Romani, F., Campo, S., Bompiani, A., Lanzone, A., & Apa, R. (2007) · Human Reproduction · doi:10.1093/humrep/dem399 · Cited by 89 · see citing works
“Finally, we tested whether sTNFR-1 could modify the effect of EPF on normal ESC differentiation, since TNF-a is secreted at increased amounts in EPF (Rana et al., 1996) and is able to decrease PRL secretion from stromal cells during in vitro decidualization (Inoue et al.”
BackgroundInfluentialOutcome of IVF in Patients with Endometriosis in Comparison with Tubal-Factor Infertility
Bergendal, A., Naffah, S., Nagy, C., Bergqvist, A., Sjöblom, P., & Hillensjø, T. (1998) · Journal of Assisted Reproduction and Genetics · doi:10.1023/a:1022526002421 · Cited by 86 · see citing works
“level of these cytokines, as well as interferon-r and transforming growth factor-B, has been shown in peritoneal fluid in women with endometriosis (20).”
Pathogenesis of Endometriosis: The Role of Peritoneal Fluid
Koninckx, P. R., Kennedy, S., & Barlow, D. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000052856 · Cited by 85 · see citing works
Akoum, A., Kong, J., Metz, C. N., & Beaumont, M.-C. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03082-0 · Cited by 84 · see citing works
Compartmentalization of Tolerance to Endotoxin
Fitting, C., Dhawan, S., & Cavaillon, J. (2004) · The Journal of Infectious Diseases · doi:10.1086/382657 · Cited by 84 · see citing works
“However, when the cells were derived from other compartments, an enhanced responsiveness was usually observed by use of peritoneal macrophages during infectious peritonitis [29], inflammatory bowel diseases [30], and endometriosis [31, 32] or by use of alveolar macrophages during acute respiratory distress syndrome [3…”
BackgroundEffect of peritoneal fluid from women with endometriosis on implantation in the mouse model
Illera, M. J., Juan, L., Stewart, C. L., Cullinan, E. B., Ruman, J. I., & Lessey, B. A. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)00552-5 · Cited by 83 · see citing works
Environmental Dioxins and Endometriosis
Rier, S. (2002) · Toxicological Sciences · doi:10.1093/toxsci/70.2.161 · Cited by 119 · see citing works
The biology of serous cavity macrophages
Bain, C. C., & Jenkins, S. J. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.01.003 · Cited by 78 · see citing works
“In addition to increases in their numbers, peritoneal macrophages obtained from women with endometriosis have heightened basal production of pro-inflammatory cytokines, including TNFa, IL-1b and IL-8, and exaggerated responses to stimulation with TLR ligands, such as LPS [109,110].”
BackgroundInfluentialTumor necrosis factor alpha secretion by peritoneal macrophages in patients with endometriosis
Richter, O. N., Dorn, C., R�sing, B., Flaskamp, C., & Ulrich, U. A. (2004) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-003-0591-9 · Cited by 79 · see citing works
“As previously noted, a large number of immunoactive and proliferation-promoting substances such as cytokines and growth factors were determined as secretion products of the macrophages in the peritoneal secretion of endometriosis patients [10, 43].”
BackgroundAkoum, 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
Akoum, A., Metz, C. N., Al-Akoum, M., & Kats, R. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.10.073 · Cited by 78 · see citing works
Dioxin-like PCBs and Endometriosis
Bruner‐Tran, K. L., & Osteen, K. G. (2010) · Systems Biology in Reproductive Medicine · doi:10.3109/19396360903381023 · Cited by 77 · see citing works
“1994] and an enhanced activation state of monocytes and peritoneal macrophages [Braun et al. 1996; Rana et al. 1996; Zeller et al. 1987].”
Mülayim, N., Savlu, A., Guzeloglu‐Kayisli, O., Kayisli, U. A., & Arici, A. M. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.11.015 · Cited by 78 · see citing works
The gut microbiota and endometriosis: From pathogenesis to diagnosis and treatment
Qin, R., Tian, G., Liu, J., & Cao, L. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.1069557 · Cited by 77 · see citing works
“Other studies have shown that macrophages can promote the release of inflammatory mediators under lipopolysaccharide stimulation, thereby promoting the inflammatory infiltration, proliferation and angiogenesis observed in endometriosis (Rana et al., 1996; Jeljeli et al., 2020).”
BackgroundMAP kinases and the inflammatory signaling cascade as targets for the treatment of endometriosis?
Santulli, P., Marcellin, L., Tosti, C., Chouzenoux, S., Cerles, O., Borghese, B., Batteux, F., & Chapron, C. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2015.1090974 · Cited by 75 · see citing works
“Peritoneal fluids of women with endometriosis contain a large number of activated macrophages and exhibit pronounced differences in their cytokine/chemokine profiles [24].”
BackgroundAkoum, A., Jolicoeur, C., & Boucher, A. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.2.6348 · Cited by 75 · see citing works
Witz, C. A. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000049425 · Cited by 73 · see citing works
Ho, H., Wu, M., Chen, S., Chao, K., Chen, C., & Yang, Y. (1997) · Human Reproduction · doi:10.1093/humrep/12.12.2810 · Cited by 73 · see citing works
“Previously we and others have reported raised concentrations of cytokines from immune cells — most likely from activated macrophages — in the peritoneal fluid of women with endometriosis (Oosterlynck et al., 1994; Sharpe-Timms et al., 1994; Keenan et al., 1995; Skrzypczak et al., 1995; Ho et al., 1996; Overton et al.,…”
BackgroundFaserl, K., Golderer, G., Kremser, L., Lindner, H. H., Sarg, B., Wildt, L., & Seeber, B. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-1532 · Cited by 71 · see citing works
Cao, W. G., Morin, M., Sengers, V., Metz, C. N., Roger, T., Maheux, R., & Akoum, A. (2005) · Human Reproduction · doi:10.1093/humrep/dei315 · Cited by 68 · see citing works
“Elevated concentrations of TNF-α were found in the peritoneal fluid of women with endometriosis (Rana et al., 1996; Barcz et al., 2000; Iwabe et al., 2000; Bedaiwy et al., 2002; Bullimore, 2003; Darai et al., 2003).”
BackgroundAkoum, A., Lemay, A., & Maheux, R. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020106 · Cited by 67 · see citing works
Interleukin-8 stimulates the adhesion of endometrial stromal cells to fibronectin
García-Velasco, J. A., & Arici, A. M. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00223-x · Cited by 65 · see citing works
Endometriosis is sustained by tumour necrosis factor-α
Bullimore, D. W. (2002) · Medical Hypotheses · doi:10.1016/s0306-9877(02)00336-5 · Cited by 63 · see citing works
Toll-like receptor 4-mediated growth of endometriosis by human heat-shock protein 70
Khan, K. N., Kitajima, M., Imamura, T., Hiraki, K., Fujishita, A., Sekine, I., Ishimaru, T., & Masuzaki, H. (2008) · Human Reproduction · doi:10.1093/humrep/den195 · Cited by 62 · see citing works
Zhang, X., Hei�, P., Deng, L., & Lin, J. (2006) · Molecular Human Reproduction · doi:10.1093/molehr/gal106 · Cited by 62 · see citing works
“Interestingly, some authors have reported that protein levels of IL-10 in PF are significantly increased in patients with endometriosis compared with controls (Punnonen et al., 1996; Ho et al., 1997b), although this has not been found in all studies (Rana et al., 1996; McLaren et al., 1997).”
BackgroundResultPathophysiology of Endometriosis-Associated Infertility
Burns, W. N., & Schenken, R. S. (1999) · Clinical Obstetrics & Gynecology · doi:10.1097/00003081-199909000-00014 · Cited by 61 · see citing works
Premenstrual and Menstrual Changes in the Macaque and Human Endometrium: Relevance to Endometriosis
BRENNER, R. M., NAYAK, N. R., SLAYDEN, O. D., CRITCHLEY, H. O. D., & KELLY, R. W. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02766.x · Cited by 59 · see citing works
Endometriosis-Related Chronic Pelvic Pain
Song, S. Y., Jung, Y. W., Shin, W., Park, M., Lee, G. W., Jeong, S., An, S., Kim, K.-M., Ko, Y. B., Lee, K. H., et al. (2023) · Biomedicines · doi:10.3390/biomedicines11102868 · Cited by 67 · see citing works
Alpinetin ameliorates inflammatory response in LPS-induced endometritis in mice
Liang, Y., Shen, T., Qi, M., Han, G., Zhang, Y., Liang, J., & Zhu, D. (2018) · International Immunopharmacology · doi:10.1016/j.intimp.2018.07.010 · Cited by 58 · see citing works
Alborzi, S., Ghotbi, S. H., Parsanezhad, M. E., Dehbashi, S., Alborzi, S., & Alborzi, M. (2007) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2006.06.024 · Cited by 56 · see citing works
Future Perspectives in the Medical Treatment of Endometriosis
Ferrero, S., Abbamonte, L. H., Anserini, P., Remorgida, V., & Ragni, N. (2005) · Obstetrical & Gynecological Survey · doi:10.1097/01.ogx.0000189153.87365.dc · Cited by 56 · see citing works
Nothnick, W. B., & Alali, Z. (2016) · F1000Research · doi:10.12688/f1000research.7504.1 · Cited by 55 · see citing works
Impact of endometriosis on surgical outcomes and complications of total laparoscopic hysterectomy
Uccella, S., Marconi, N., Casarin, J., Ceccaroni, M., Boni, L., Sturla, D., Serati, M., Carollo, S., Alluvion, C. P., & Ghezzi, F. (2016) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-016-4115-9 · Cited by 54 · see citing works
Morin, M., Bellehumeur, C., Therriault, M., Metz, C. N., Maheux, R., & Akoum, A. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.10.039 · Cited by 53 · see citing works
Wu, M., Ho, H., Chen, S., Chao, K., Chen, C., & Yang, Y. (1999) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1999.tb00082.x · Cited by 52 · see citing works
- Authors
- Rana, N., Braun, D. P., House, R., Gebel, H., Rotman, C., & Dmowski, W. P.
- Affiliations
- Rush University Medical Center (US)
- ORCID
- Gebel, Howard
- Venue
- Fertility and Sterility
- Publisher
- Elsevier BV
- Published
- 1996-05
- Volume
- 65
- Issue
- 5
- Pages
- 925-930
- ISSN
- 0015-0282 (ISSN-L)
- OpenAlex
- W98713221
- Cited by
- 264
- References
- 27
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 12 · 2023: 9 · 2022: 5 · 2021: 8 · 2020: 6 · 2019: 5 · 2018: 6 · 2017: 9 · 2016: 6 · 2015: 4 · 2014: 4 · 2013: 8 · 2012: 9
- FWCI
- 11.33
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Fertility and Sterility (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ca058922-03)
- National Cancer Institute (CA 58922)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Surgery › Diagnosis and treatment of tuberculosis
- Keywords
- endometriosis, peritoneal macrophages, cytokine production, TNF-α, interleukin-8, IL-10, lipopolysaccharide stimulation, peritoneal fluid
- MeSH terms
- Ascitic Fluid, Cells, Cultured, Endometriosis, Female, Humans, Lipopolysaccharides, Tumor Necrosis Factor-alpha, Cytokines, Interleukin-8, Interleukin-10, Macrophages, Peritoneal
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
