Semin Reprod Med 2003; 21(2): 135-144
DOI: 10.1055/s-2003-41320
Copyright © 2003 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

Endometriosis: Interaction of Immune and Endocrine Systems

Emre Seli, Aydin Arici
  • Division of Reproductive Endocrinology Department of Obstetrics Gynecology, Yale University School of Medicine New Haven Connecticut
Weitere Informationen

Publikationsverlauf

Publikationsdatum:
14. August 2003 (online)

ABSTRACT

Endometriosis is a common gynecologic disorder characterized by the presence of endometrial tissue outside the uterine cavity. Although no single theory can explain all cases of endometriosis, the most commonly accepted theory is Sampson's theory of retrograde menstruation. Retrograde menstruation occurs in 76 to 90% of women. The much lower prevalence of endometriosis suggests that additional factors determine susceptibility to endometriosis. Endometriosis is associated with changes in both cell-mediated and humoral immunity. Impaired natural killer cell activity resulting in inadequate removal of refluxed menstrual debris may play a role in the development of endometriotic implants. Moreover, although the peritoneal fluid of women with endometriosis contains increased numbers of immune cells, these seem to facilitate rather than inhibit the development of endometriosis. Macrophages that would be expected to clear endometrial cells from the peritoneal cavity appear to enhance their proliferation by secreting growth factors and cytokines. Although it is unclear whether these immunologic alterations induce endometriosis or are a consequence of its presence, they appear to play an important role in allowing endometriosis implants to persist and progress and contribute to the development of associated infertility and pelvic pain. Danazol and gonadotropin-releasing hormone (GnRH) agonists are commonly used for the medical treatment of endometriosis. These medications seem to down-regulate cellular and humoral immune responses concomitant with their effect on endometriotic implants. Immunomodulatory effects of danazol and GnRH agonists are likely to contribute to the observed clinical improvement associated with their use.

REFERENCES

  • 1 Sampson J A. Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity.  Am J Obstet Gynecol . 1927;  14 422-469
  • 2 Beyth Y, Yaffe H, Levij S. et al . Retrograde seeding of endometrium: a sequela of tubal flushing.  Fertil Steril . 1975;  26 1094-1097
  • 3 Bartosik D, Jacobs S L, Kelly L J. Endometrial tissue in peritoneal fluid.  Fertil Steril . 1986;  46 796-800
  • 4 TeLinde R W, Scott R B. Experimental endometriosis.  Am J Obstet Gynecol . 1950;  60 1147-1173
  • 5 Ridley J H, Edwards I K. Experimental endometriosis in the human.  Am J Obstet Gynecol . 1958;  76 783-790
  • 6 Jenkins S, Olive D L, Haney A F. Endometriosis: pathogenic implications of the anatomic distribution.  Obstet Gynecol . 1986;  67 335-338
  • 7 Blumenkrantz J M, Gallagher N, Bashore R A. et al . Retrograde menstruation in women undergoing chronic peritoneal dialysis.  Obstet Gynecol . 1981;  57 667-670
  • 8 Halme J, Hammond M G, Hulka J F. et al . Retrograde menstruation in healthy women and in patients with endometriosis.  Obstet Gynecol . 1984;  64 151-154
  • 9 Houston D E, Noller K L, Melton 3rd J L. et al . Incidence of pelvic endometriosis in Rochester, Minnesota, 1970-1979.  Am J Epidemiol . 1987;  125 959-969
  • 10 Kjerulff K H, Erickson B A, Langenberg P W. Chronic gynecological conditions reported by US women: findings from the National Health Interview Survey, 1984 to 1992.  Am J Public Health . 1996;  86 195-199
  • 11 vanFurth R, Raeburn J A, vanZwet T I. Characteristics of human mononuclear phagocytes.  Blood . 1979;  54 485-500
  • 12 Haney A F, Muscato J J, Weinberg J B. Peritoneal fluid cell populations in infertility patients.  Fertil Steril . 1981;  35 696-698
  • 13 Olive D L, Weinberg J B, Haney A F. Peritoneal macrophages and infertility: the association between cell number and pelvic pathology.  Fertil Steril . 1985;  44 772-777
  • 14 Halme J, Becher S, Hammond M G. et al . Increased activation of pelvic macrophages in infertile women with mild endometriosis.  Am J Obstet Gynecol . 1983;  145 333-337
  • 15 Zeller J M, Henig I, Radwanska E. et al . Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis.  Am J Reprod Immunol . 1987;  13 78-82
  • 16 Dunselman G A, Hendrix M G, Bouckaert P X. et al . Functional aspects of peritoneal macrophages in endometriosis of women.  J Reprod Fertil . 1988;  1988 707-710
  • 17 Hill J A, Faris H MP, Schiff I. et al . Characterization of leukocyte subpopulations in the peritoneal fluid of women with endometriosis.  Fertil Steril . 1988;  50 216-222
  • 18 Lebovic D I, Mueller M D, Taylor R N. Immunobiology of endometriosis.  Fertil Steril . 2001;  75 1-10
  • 19 Ramprasad M P, Fischer W, Witztum J L. et al . The 94- to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68.  Proc Natl Acad Sci U S A . 1995;  92 9580-9584
  • 20 Ottnad E, Parthasarathy S, Sambrano G R. et al . A macrophage receptor for oxidized low density lipoprotein distinct from the receptor for acetyl low density lipoprotein: partial purification and role in recognition of oxidatively damaged cells.  Proc Natl Acad Sci USA . 1995;  92 1391-1395
  • 21 Stanton L W, White R T, Bryant C M. et al . A macrophage Fc receptor for IgG is also a receptor for oxidized low density lipoprotein.  J Biol Chem . 1992;  267 22446-22451
  • 22 Endemann G, Stanton L W, Madden K S. et al . CD36 is a receptor for oxidized low density lipoprotein.  J Biol Chem . 1993;  268 11811-11816
  • 23 Moulton K S, Wu H, Barnett J. et al . Regulated expression of the human acetylated low density lipoprotein receptor gene and isolation of promoter sequences.  Proc Natl Acad Sci USA . 1992;  89 8102-8106
  • 24 Wu H, Moulton K, Horvai A. et al . Combinatorial interactions between AP-1 and ets domain proteins contribute to the developmental regulation of the macrophage scavenger receptor gene.  Mol Cell Biol . 1994;  14 2129-2139
  • 25 de Villiers J W, Fraser I P, Gordon S. Cytokine and growth factor regulation of macrophage scavenger receptor expression and function.  Immunol Lett . 1994;  43 73-79
  • 26 Sidell N, Han S W, Parthasarathy S. Regulation and modulation of abnormal immune responses in endometriosis.  Ann NY Acad Sci . 2002;  955 159-406
  • 27 Kim J G, Keshava C, Murphy A A. et al . Fresh mouse peritoneal macrophages have low scavenger receptor activity.  J Lipid Res . 1997;  38 2207-2215
  • 28 Surrey E S, Halme J. Effect of peritoneal fluid from endometriosis patients on endometrial stromal cell proliferation in vitro.  Obstet Gynecol . 1990;  76 792-797
  • 29 Braun D P, Muriana A, Gebel H. et al . Monocyte-mediated enhancement of endometrial cell proliferation in women with endometriosis.  Fertil Steril . 1994;  61 78-84
  • 30 Holmberg L A, Ault K A. Characterization of natural killer cells induced in the peritoneal exudates of mice infected with Listeria monocytogenes: a study of their tumor target specificity and their expression of murine differentiation antigens and human NK-associated antigens.  Cell Immunol . 1984;  89 151-168
  • 31 Voogt P J, Falkenburg J H, Fibbe W E. et al . Normal hematopoietic progenitor cells and malignant lymphohematopoietic cells show different susceptibility to direct cell-mediated MHC-non-restricted lysis by T cell receptor-/ CD3-, T cell receptor gamma delta+/CD3+ and T cell receptor-alpha beta+/CD3+ lymphocytes.  J Immunol . 1989;  142 1774-1780
  • 32 Moretta A, Sivori S, Vitale M. et al . Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells.  J Exp Med . 1995;  182 875-884
  • 33 Kikuchi Y, Ishikawa N, Hirata J. et al . Changes of peripheral blood lymphocyte subsets before and after operation of patients with endometriosis.  Acta Obstet Gynecol Scand . 1993;  72 157-161
  • 34 Oosterlynck D J, Cornillie F J, Waer M. et al . Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium.  Fertil Steril . 1991;  56 45-51
  • 35 Wilson T J, Hertzog P J, Angus D. et al . Decreased natural killer cell activity in endometriosis patients: relationship to disease pathogenesis.  Fertil Steril . 1994;  62 1086-1088
  • 36 Ho H N, Chao K H, Chen H F. et al . Peritoneal natural killer cytotoxicity and CD25+ CD3+ lymphocyte subpopulation are decreased in women with stage III-IV endometriosis.  Hum Reprod . 1995;  10 2671-2675
  • 37 Kanzaki H, Wang H-S, Kariya M. et al . Suppression of natural killer cell activity by sera from patients with endometriosis.  Am J Obstet Gynecol . 1992;  167 257-261
  • 38 Oosterlynck D J, Meuleman C, Waer M. et al . Immunosuppressive activity of peritoneal fluid in women with endometriosis.  Obstet Gynecol . 1993;  82 206-212
  • 39 Ho H N, Wu M Y, Yang Y S. Peritoneal cellular immunity and endometriosis.  Am J Reprod Immunol . 1997;  38 400-412
  • 40 Wu M Y, Yang J H, Chao K H. et al . Increase in the expression of killer cell inhibitory receptors on peritoneal natural killer cells in women with endometriosis.  Fertil Steril . 2000;  74 1187-1191
  • 41 Maeda N, Izumiya C, Yamamoto Y. et al . Increased killer inhibitory receptor KIR2DL1 expression among natural killer cells in women with pelvic endometriosis.  Fertil Steril . 2002;  77 297-302
  • 42 Garzetti G G, Ciavattini A, Provinciali M. et al . Natural cytotoxicity and GnRH agonist administration in advanced endometriosis: positive modulation on natural killer activity.  Obstet Gynecol . 1996;  88 234-240
  • 43 Hsu C C, Lin Y S, Wang S T. et al . Immunomodulation in women with endometriosis receiving GnRH agonist.  Obstet Gynecol . 1997;  89 993-998
  • 44 Vigano P, Di Blasio M A, Busacca M. et al . Danazol suppresses both spontaneous and activated human lymphocyte-mediated cytotoxicity.  Am J Reprod Immunol . 1992;  28 38-42
  • 45 Dmowski W P, Steele R W, Baker G F. Deficient cellular immunity in endometriosis.  Am J Obstet Gynecol . 1981;  141 377-383
  • 46 Steele R W, Dmowski W P, Marmer D J. Immunologic aspects of human endometriosis.  Am J Reprod Immunol . 1984;  6 33-36
  • 47 Dmowski W P, Gebel H M, Braun D P. The role of cell-mediated immunity in pathogenesis of endometriosis.  Acta Obstet Gynecol Scand . 1994;  159 7-14
  • 48 Gleicher N, Dmowski W P, Siegel I. et al . Lymphocyte subsets in endometriosis.  Obstet Gynecol . 1984;  63 463-466
  • 49 Badawy S ZA, Cuenca V, Stitzel A. et al . Immune rosettes of T and B lymphocytes in infertile women with endometriosis.  J Reprod Med . 1987;  32 194-197
  • 50 Mettler L, Volkov N I, Kulakov V I. et al . Lymphocyte subsets in the endometrium of patients with endometriosis throughout the menstrual cycle.  Am J Reprod Immunol . 1996;  36 342-348
  • 51 Witz C A, Montoya I A, Dey T D. et al . Characterization of lymphocyte subpopulations and T cell activation in endometriosis.  Am J Reprod Immunol . 1994;  32 173-179
  • 52 Hill J A, Barbieri R L, Anderson D J. Immunosuppressive effects of danazol in vitro.  Fertil Steril . 1987;  48 414-418
  • 53 Braun D P, Gebel H, Dmowski W P. Effect of danazol in vitro and in vivo on monocyte-mediated enhancement of endometrial cell proliferation in women with endometriosis.  Fertil Steril . 1994;  62 89-95
  • 54 Weed J C, Arquembourg P C. Endometriosis: can it produce an autoimmune response resulting in infertility?.  Clin Obstet Gynecol . 1980;  23 885-893
  • 55 Mathur S, Peress M R, Williamson H O. et al . Autoimmunity to endometrium and ovary in endometriosis.  Clin Exp Immunol . 1982;  50 259-266
  • 56 Gleicher N, el-Roeiy A, Confino E. et al . Is endometriosis an autoimmune disease?.  Obstet Gynecol . 1987;  70 115-122
  • 57 Pillai S, Zhou G X, Arnaud P. et al . Antibodies to endometrial transferrin and alpha 2-Heremans Schmidt (HS) glycoprotein in patients with endometriosis.  Am J Reprod Immunol . 1996;  35 483-494
  • 58 Lang G A, Yeaman G R. Autoantibodies in endometriosis sera recognize a Thomsen-Friedenreich-like carbohydrate antigen.  J Autoimmun . 2001;  16 151-161
  • 59 Yeaman G R, Collins J E, Lang G A. Autoantibody responses to carbohydrate epitopes in endometriosis.  Ann NY Acad Sci . 2002;  955 174-406
  • 60 Gleicher N, el-Roeiy A, Confino E. et al . Reproductive failure because of autoantibodies: unexplained infertility and pregnancy wastage.  Am J Obstet Gynecol . 1989;  160 1375-1380
  • 61 Glinoer D, Soto M F, Bourdoux P. et al . Pregnancy in patients with mild thyroid abnormalities: maternal and neonatal repercussions.  J Clin Endocrinol Metab . 1991;  73 421-427
  • 62 el-Roeiy A, Dmowski W P, Gleicher N. et al . Danazol but not gonadotropin-releasing hormone agonists suppresses autoantibodies in endometriosis.  Fertil Steril . 1988;  50 864-871
  • 63 Kennedy S H, Starkey P M, Sargent I L. et al . Antiendometrial antibodies in endometriosis measured by an enzyme-linked immunosorbent assay before and after treatment with danazol and nafarelin.  Obstet Gynecol . 1990;  75 914-918
  • 64 Ota H, Igarashi S, Hayakawa M. et al . Effect of danazol on the immunocompetent cells in the eutopic endometrium in patients with endometriosis: a multicenter cooperative study.  Fertil Steril . 1996;  65 545-551
  • 65 Dmowski W P, Rana N, Michalowska J. et al . The effect of endometriosis, its stage and activity, and of autoantibodies on in vitro fertilization and embryo transfer success rates.  Fertil Steril . 1995;  63 555-562
  • 66 Nothnick W B. Treating endometriosis as an autoimmune disease.  Fertil Steril . 2001;  76 223-231
  • 67 Hang L, Slack J H, Amundson C. et al . Induction of murine autoimmune disease by chronic polyclonal B cell activation.  J Exp Med . 1983;  157 874-883
  • 68 Prud'homme G J, Balderas R S, Dixon F J. et al . B cell dependence on and response to accessory signals in murine lupus strains.  J Exp Med . 1983;  157 1815-1827
  • 69 Rose N R, Bona C. Defining criteria for autoimmune diseases (Witebsky's postulates revised).  Immunol Today . 1993;  14 426-430
  • 70 Hill J A, Anderson D J. Lymphocyte activity in the presence of peritoneal fluid from fertile women and infertile women with and without endometriosis.  Am J Obstet Gynecol . 1989;  161 861-864
  • 71 Fakih H, Bagget B, Holtz G. et al . Interleukin-1: possible role in the infertility associated with endometriosis.  Fertil Steril . 1987;  47 213-217
  • 72 Mori H, Sawairi M, Nakagawa M. et al . Peritoneal fluid interleukin-1 beta and tumor necrosis factor in patients with benign gynecologic disease.  Am J Reprod Immunol . 1991;  26 62-67
  • 73 Keenan J A, Chen T T, Chadwell N L. et al . IL-1β, TNF-α, and IL-2 in peritoneal fluid and macrophage conditioned media of women with endometriosis.  Am J Reprod Immunol . 1995;  34 381-385
  • 74 Lebovic D I, Bentzien F, Chao V A. et al . Induction of an angiogenic phenotype in endometriotic stromal cell cultures by interleukin-1beta.  Mol Hum Reprod . 2000;  6 269-275
  • 75 Vigano P, Gaffuri B, Somigliana E. et al . Expression of intercellular adhesion molecule (ICAM)-1 mRNA and protein is enhanced in endometriosis versus endometrial stromal cells in culture.  Mol Hum Reprod . 1998;  4 1150-1156
  • 76 Hill J A, Haimovici F, Politch J. et al . Effect of soluble products of activated lymphocytes and macrophages (lymphokines and monokines) on human sperm motion parameters.  Fertil Steril . 1987;  47 460-465
  • 77 Hill J A, Haimovici F, Anderson D J. Products of activated lymphocytes and macrophages inhibit mouse embryo development in vitro.  J Immunol . 1987;  139 2250-2254
  • 78 Sueldo C E, Kelly E, Montoro L. et al . Effect of interleukin-1 on gamete interaction and mouse embryo development.  J Reprod Med . 1990;  35 868-872
  • 79 Koumantakis E, Matalliotakis I, Neonaki M. et al . Soluble serum interleukin-2 receptor, interleukin-6 and interleukin-1a in patients with endometriosis and in controls.  Arch Gynecol Obstet . 1994;  255 107-112
  • 80 Mori H, Nakagawa M, Itoh N. et al . Danazol suppresses the production of interleukin-1 beta and tumor necrosis factor by human monocytes.  Am J Reprod Immunol . 1990;  24 45-50
  • 81 Taketani Y, Kuo T M, Mizuno M. Comparison of cytokine levels and embryo toxicity in peritoneal fluid in infertile women with untreated or treated endometriosis.  Am J Obstet Gynecol . 1992;  167 265-270
  • 82 Arici A, Head J R, MacDonald P C. et al . Regulation of interleukin-8 gene expression in human endometrial cells in culture.  Mol Cell Endocrinol . 1993;  94 195-204
  • 83 Arici A, Tazuke S I, Attar E. et al . Interleukin-8 concentration in peritoneal fluid of patients with endometriosis and modulation of interleukin-8 expression in human mesothelial cells.  Mol Hum Reprod . 1996;  2 40-45
  • 84 Arici A, Seli E, Senturk L M. et al . Interleukin-8 in the human endometrium.  J Clin Endocrinol Metab . 1998;  83 1783-1787
  • 85 Ryan I P, Tseng J F, Schriock E D. et al . Interleukin-8 concentrations are elevated in peritoneal fluid of women with endometriosis.  Fertil Steril . 1995;  63 929-932
  • 86 Akoum A, Lawson C, McColl S. et al . Ectopic endometrial cells express high concentrations of interleukin (IL)-8 in vivo regardless of the menstrual cycle phase and respond to oestradiol by up-regulating IL-1-induced IL-8 expression in vitro.  Mol Hum Reprod . 2001;  7 859-866
  • 87 Garcia-Velasco J A, Arici A. Interleukin-8 stimulates the adhesion of endometrial stromal cells to fibronectin.  Fertil Steril . 1999;  72 336-340
  • 88 Garcia-Velasco J A, Arici A. Interleukin-8 expression in endometrial stromal cells is regulated by integrin-dependent cell adhesion.  Mol Hum Reprod . 1999;  5 1135-1140
  • 89 Spuijbroek M E H D, Dunselman G AJ, Menheere P J A P. et al . Early endometriosis invades the extracellular matrix.  Fertil Steril . 1992;  58 929-933
  • 90 Arici A. Local cytokines in endometrial tissue: the role of interleukin-8 in the pathogenesis of endometriosis.  Ann NY Acad Sci . 2002;  955 101-406
  • 91 Arici A, Seli E, Zeyneloglu H B. et al . Interleukin-8 induces proliferation of endometrial stromal cells: a potential autocrine growth factor.  J Clin Endocrinol Metab . 1998;  83 1201-1205
  • 92 Arici A, Oral E, Attar E. et al . Monocyte chemotactic protein-1 concentration in peritoneal fluid of women with endometriosis and its modulation of expression in mesothelial cells.  Fertil Steril . 1997;  67 1065-1072
  • 93 Jolicoeur C, Boutouil M, Drouin R. et al . Increased expression of monocyte chemotactic protein-1 in the endometrium of women with endometriosis.  Am J Pathol . 1998;  152 125-133
  • 94 Akoum A, Jolicoeur C, Boucher A. Estradiol amplifies interleukin-1-induced monocyte chemotactic protein-1 expression by ectopic endometrial cells of women with endometriosis.  J Clin Endocrinol Metab . 2000;  85 896-904
  • 95 Akoum A, Lemay A, Brunet C. et al . Secretion of monocyte chemotactic protein-1 by cytokine-stimulated endometrial cells of women with endometriosis. Le groupe d'investigation en gynecologie.  Fertil Steril . 1995;  63 322-328
  • 96 Akoum A, Lemay A, Brunet C. et al . Cytokine-induced secretion of monocyte chemotactic protein-1 by human endometriotic cells in culture.  Am J Obstet Gynecol . 1995;  172 594-600
  • 97 Boucher A, Mourad W, Mailloux J. et al . Ovarian hormones modulate monocyte chemotactic protein-1 expression in endometrial cells of women with endometriosis.  Mol Hum Reprod . 2000;  6 618-626
  • 98 Boucher A, Lemay A, Akoum A. Effect of hormonal agents on monocyte chemotactic protein-1 expression by endometrial epithelial cells of women with endometriosis.  Fertil Steril . 2000;  74 969-975
  • 99 Jolicoeur C, Lemay A, Akoum A. Comparative effect of danazol and a GnRH agonist on monocyte chemotactic protein-1 expression by endometriotic cells.  Am J Reprod Immunol . 2001;  45 86-93
  • 100 Khorram O, Taylor R N, Ryan I P. et al . Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis.  Am J Obstet Gynecol . 1993;  169 1545-1549
  • 101 Hornung D, Ryan I P, Chao V A. et al . Immunolocalization and regulation of the chemokine RANTES in human endometrial and endometriosis tissues and cells.  J Clin Endocrinol Metab . 1997;  82 1621-1628
  • 102 Philippeaux M M, Piguet P F. Expression of tumor necrosis factor-alpha and its mRNA in the endometrial mucosa during the menstrual cycle.  Am J Pathol . 1993;  143 480-486
  • 103 Laird S M, Tuckerman E M, Saravelos H. et al . The production of tumour necrosis factor alpha (TNF-alpha) by human endometrial cells in culture.  Hum Reprod . 1996;  11 1318-1323
  • 104 Eisermann J, Gast M J, Pineda J. et al . Tumor necrosis factor in peritoneal fluid of women undergoing laparoscopic surgery.  Fertil Steril . 1988;  50 573-579
  • 105 Zhang R, Wild R, Ojago J. Effect of tumor necrosis factor-α on adhesion of human endometrial stromal cells to peritoneal mesothelial cells: an in vitro system.  Fertil Steril . 1993;  59 1196-1201
  • 106 Shifren J L, Tseng J F, Zaloudek C J. et al . Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis.  J Clin Endocrinol Metab . 1996;  81 3112-3118
  • 107 Li X F, Gregory J, Ahmed A. Immunolocalisation of vascular endothelial growth factor in human endometrium.  Growth Factors . 1994;  11 277-282
  • 108 McLaren J, Prentice A, Charnock-Jones D S. et al . Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids.  J Clin Invest . 1996;  98 482-489
  • 109 Brogi E, Wu T, Namiki A. et al . Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only.  Circulation . 1994;  90 649-652
  • 110 Ben-Av P, Crofford L J, Wilder R L. et al . Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: a potential mechanism for inflammatory angiogenesis.  FEBS Lett . 1995;  372 83-87
  • 111 Donnez J, Smoes P, Gillerot S. et al . Vascular endothelial growth factor (VEGF) in endometriosis.  Hum Reprod . 1998;  13 1686-1690