Importance of genital endometriosis in pathogenesis of infertility

Cover Page


Cite item

Full Text

Abstract

One of the most common manifestations of endometriosis is infertility. Currently much attention of researchers is lead to pathogenetic mechanisms of infertility in this disease, but there is not common conception of the causal effect of the failure of reproductive function. There is a literature review of mechanisms of fertility disturbance in genital endometriosis in this article. There are data about hormonal, immunological, genetic factors and data about endometrial alterations during implantation, which can influence on pregnancy onset.

About the authors

Maria Igorevna Yarmolinskaya

FSBI «The D. O. Ott Research Institute of Obstetrics and Gynecology» NWB RAMS

Email: m.yarmolinskaya@gmail.com
MD, PhD, Leading Scientific Researcher of the department of reproductive endocrinology

Valentina Mikhailovna Denisova

FSBI «The D. O. Ott Research Institute of Obstetrics and Gynecology» NWB RAMS

Email: valyik@mail.ru
PhD student

References

  1. Баскаков В. П., Цвелев Ю. В., Кира Е. Ф. Эндометриоидная болезнь. СПБ.: Изд-во Н-Л; 2002.
  2. Ярмолинская М. И. Цитокиновый профиль перитонеальной жидкости и периферической крови больных с наружным генитальным эндометриозом. Журнал акушерства и женских болезней. 2008; LVII (3): 30-4.
  3. Ярмолинская М. И. Генитальный эндометриоз: влияние гормональных, иммунологических и генетических факторов на развитие, особенности течения и выбор терапии. Автореф. дис. … докт. мед. наук. СПб.; 2009.
  4. Adamson G. D., Pasta D. J. Endometriosis fertility index: the new, validated endometriosis staging system. Fertil. Steril. 2010; 94: 1609-15.
  5. Aghajanova L., Giudice L. C. Molecular evidence for differences in endometrium in severe versus mild endometriosis. Reprod Sci. 2011; 18 (3): 229-51.
  6. Aghajanova L., Tatsumi K., Horcajadas J. A. et al. Unique transcriptome, pathways, and networks in the human endometrial fibroblast response to progesterone in endometriosis. Biology of reproduction. 2011; 84: 801-15.
  7. Alizadeh Z., Shokrzadeh N., Saidijam M. et al. Semi-quantitative analysis of HOXA11, leukemia inhibitory factor and basic transcriptional element binding protein 1 mRNA expression in the mid-secretory endometrium of patients with endometriosis. Iran Biomed. J. 2011; 15 (3): 66-72.
  8. Barnhart K., Dunsmoor-Su R., Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil. Steril. 2002; 77 (5): 1148-55.
  9. Barragan J. C., Brotons J., Ruiz J. A. et al. Experimentally induced endometriosis in rats: effect on fertility and the effects of pregnancy and lactation on the ectopic endometrial tissue. Fertil. Steril. 1992; 58: 1215-9.
  10. Bilibio J. P., Matte U., de Conto E. et al. Dopamine receptor D2 genotype (3438) is associated with moderate/severe endometriosisin infertile women in Brazil. Fertil. Steril. 2013; 99 (5): 1340-5.
  11. Bilotas M., Meresman G., Buquet R. et al. Effect of vascular endothelial growth factor and interleukin-1beta on apoptosis in endometrial cell cultures from patients with endometriosis and controls. J. Reprod. Immunol. 2010; 84 (2): 193-8.
  12. Brosens J. J., Hodgetts A., Feroze-Zaidi F. et al. Proteomic analysis of endometrium from fertile and infertile patients suggests a role for apolipoprotein A-I in embryo implantation failure and endometriosis. Molecular Human Reproduction. 2010; 16 (4): 273-85.
  13. Bulun S. E. Endometriosis. N. Engl. J. Med. 2009; 360: 268-79.
  14. Bulun S. E., Cheng Y. H., Pavone M. E. et al. 17Beta-hydroxysteroid dehydrogenase-2 deficiency and progesterone resistance inendometriosis. Semin. Reprod. Med. 2010; 28 (1): 44-50.
  15. Bulun S. E., Zeitoun K., Takayama K.et al. Estrogen production in endometriosis and use of aromatase inhibitors to treat endometriosis. Endocrine-Related Cancer. 1999; 6: 293-301.
  16. Carneiro M. M., Morsch D. M., Camargos A. F. et al. Androgen receptor and 5α-reductase are expressed in pelvic andometriosis. BJOG. 2008; 115: 113-7.
  17. Casals G., Ordi J., Creus M. et al. Expression pattern of osteopontin and αvβ3 integrin during the implantation window in infertile patients with early stages of endometriosis. Hum. Reprod. 2012; 27 (3): 805-13.
  18. Chang C. Y.-Y., Chang H.-W., Chen C.-M. et al. MUC4 gene polymorphisms associate with endometriosis development and endometriosis -related infertility. BMC Medicine. 2011, 9: 19
  19. Christofolini D. M., Vilarino F. L., Mafra F. A. et al. Combination of polymorphisms in luteinizing hormone β, estrogen receptor β andprogesterone receptor and susceptibility to infertility and endometriosis. Eur. J. Obstet. Gynecol. Reprod. Biol. 2011; 158 (4): 260-4.
  20. Coccia M. E., Rizzello F., Mariani G. et al. Impact of endometriosis on in vitro fertilization and embryo transfer cycles in young women: a stage-dependent interference. Acta Obstet. Gynecol. Scand. 2011; 90 (11): 1232-8.
  21. Collette T., Maheux R., Mailloux J. et al. Increased expression of matrix metalloproteinase-9 in the eutopic endometrial tissue of women with endometriosis. Hum. Reprod. 2006; 21: 3059-67.
  22. Costa I. R., Silva R. C., Frare A. B. et al. Polymorphism of the progesterone receptor gene associated with endometriosis in patients from Goiás, Brazil. Genet. Mol. Res. 2011; 10 (3): 1364-70.
  23. Cunha-Filho J.S., Gross J. L., Lemos N. A. et al. Hyperprolactinemia and luteal insufficiency in infertile patients with mild and minimal endometriosis. Horm. Metab. Res. 2001; 33 (4): 216-20.
  24. Cunha-Filho J.S., Gross J. L., Lemos N. A. et al. Prolactin and growth hormone secretion after thyrotrophinreleasing hormone infusion and dopaminergic (DA2) blockade in infertile patients with minimal/mild endometriosis. Hum. Reprod. 2002; 17: 960-5.
  25. D’Hooghe T. M., Bambra C. S., Raeymaekers B. M. et al. The cycle pregnancy rate is normal in baboons with stage I endometriosis but decreased in primates with stage II and stage III-IV disease. Fertil. Steril. 1996; 66 (5): 809-13.
  26. Dassen H., Punyadeera C., Kamps R. et al. Estrogen metabolising enzymes in endometrium and endometriosis. Human Reproduction. 2007; 22 (12): 3148-58.
  27. Defrère S., González-Ramos R., Lousse J.-C. et al. Insights into iron and nuclear factor-kappa B (NF-kB) involvement in chronic inflammatory processes in peritoneal endometriosis. Histol. Histopathol. 2011; 26: 1083-92.
  28. Delvoux B., Groothuis P., D’Hooghe T. et al. Increased production of 17β-estradiol in endometriosis lesions is the result of impaired metabolism. J. Clin. Endocrinol. Metabol. 2009; 94 (3): 876-83.
  29. Dimitriadis E., Stoikos C., Stafford-Bell M. et al. Interleukin-11, IL-11 receptoralpha and leukemia inhibitory factor are dysregulated in endometrium of infertile women with endometriosis during the implantation window. J. Reprod. Immunol. 2006; 69: 53-64.
  30. Dimitriadis E., White C. A., Jones R. L. et al. Cytokines, chemokines and growth factors in endometrium related to implantation. Human Reproduction Update. 2005; 11 (6): 613-30.
  31. Ezaki K., Motoyama H., Sasaki H. Immunohistologic localization of estrone sulfatase in uterine endometrium and adenomyosis. Obstet. Gynecol. 2001; 98: 815-9.
  32. Flamini M. I., Sanchez A. M., Goglia L. et al. Differential actions of estrogen and SERMs in regulation of the actin cytoskeleton of endometrial cells. Molecular Human Reproduction. 2009; 15 (10): 675-85.
  33. Gimenes C., Bianco B., Mafra F. A. et al. The progins progesterone receptor gene polymorphism is not related to endometriosis associated infertility or to idiopathic infertility. Clinics. 2010; 65 (11): 1073-6.
  34. Giudice L. C., Evers J. L.H., Healy D. L. Endometriosis: Science and Practice. N.Y.: Wiley-Blackwell; 2012.
  35. Gogacz M., Darmochwal-Kolarz D., Putowski L. et al. The estimation of IL-2 and IL-2 receptors in peritoneal fluid of infertile patients with endometriosis. Centr. Eur. J. Immunol. 2007; 32 (3): 160-3.
  36. Gomez-Torres M.-J., Acien P., Calmpos A. et al. Embryotoxicity of peritoneal fluid in women with endometriosis. Its relation with cytokines and lymphocyte populations. Human Reproduction. 2002; 17 (3): 777-81.
  37. Gregoriou G., Bakas P., Vitoratos N. et al. Evaluation of serum prolactin levels in patients with endometriosis and infertility. Gynecol Obstet Invest 1999; 48: 48-51.
  38. Griffith J. S., Liu Y.-G., Tekmal R. R. et al. Menstrual endometrial cells from women with endometriosis demonstrate increased adherence to peritoneal cells and increased expression of CD44 splice variants. Ferti. Steril. 2010; 93 (6): 1745-9.
  39. Grund E. M., Kagan D., Tran C. A. [et al.] Tumor necrosis factor-α regulates inflammatory and mesenchymal responses via mitogen-activated protein kinase kinase, p38, and nuclear factor κB in human endometriotic epithelial cells. Mol. Pharmacol. 2008; 73: 1394-04.
  40. Hahn D. W., Carraher R. P., Foldesy R. G. et al. Experimental evidence for failure to implant as a mechanism of infertility associated with endometriosis. Am. J. Obstet. Gynecol. 1986; 155: 1109-13.
  41. Haider S., Knöfler M. Human Tumour Necrosis Factor: Physiological and Pathological Roles in Placenta and Endometrium. Placenta. 2009; 30 (2): 111-23.
  42. Harada T., Ohata Y., Deura I. et al. Serum cytokine levels are evaluated in patients with endometriosis. World Endometriosis Society e-Journal. 2008; 10: 5-8.
  43. Huges E. G., Fedorkow D. M., Collins J. A. A quantitative overview of controlled trials in endometriosis-associated infertility. Fertil. Steril. 1993; 59: 963-70.
  44. Jasper M. J., Tremellen K. P., Robertson S. A. Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Molecular Human Reproduction. 2006; 12 (5): 301-8.
  45. Karita M., Yamashita Y., Hayashi A. et al. Does advanced-stage endometriosis affect the gene expression of estrogen andprogesterone receptors in granulosa cells? Fertil. Steril. 2011; 95 (3): 889-94.
  46. Keay S. D., Harlow C. R., Wood P. J. et al. Higher cortisol: cortisone ratios in the preovulatory follicle of completely unstimulated IVF cycles indicate oocytes with increased pregnancypotential. Hum. Reprod. 2002; 17: 2410-4.
  47. Kim K. J., Choi J. S., Kang I. et al. Melatonin suppresses tumor progression by reducing angiogenesis stimulated by HIF-1 in a mouse tumor model. J. Pineal. Res. 2013; 54 (3): 264-70.
  48. Kissler S., Zangos S., Wiegratz I. et al. Utero-tubal sperm transport and its impairment in endometriosis and adenomyosis. Ann. N. Y. Acad. Sci. 2007; 1101: 38-48.
  49. Koc O., Gunduz B., Topcuoglu A. et al. Effects of pinealectomy and melatonin supplementation on endometrial explants in a rat model. Eur. J. Obstet. Gynecol. Reprod. Biol. 2010; 153 (1): 72-6.
  50. Kumbak B., Kahraman S., Karlikaya G. et al. In vitro fertilization in normoresponder patients with endometriomas: comparison with basal simple ovarian cysts. Gynecol. Obstet. Invest. 2008; 65: 212-6.
  51. Kurihara I., Lee D. K., Petit F. G. et al. COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLoS Genet. 2007; 3 (6): 1053-64.
  52. Kwak-Kim J.Y.H., Chung-Bang H.S., Ng S. C. et al. Increased T helper 1 cytokine responses by circulating T cells are present in women with recurrent pregnancy losses and in infertile women with multiple implantation failures. Human Reproduction. 2003; 18 (4): 767-73.
  53. Lampiao F., du Plessis S. S. TNF-alpha and IL-6 affect human sperm function by elevating nitric oxide production. Reprod Biomed Online. 2008; 17 (5): 628-31.
  54. Lima A. P., Moura M. D., Rosa e Silva A. A.M. Prolactin and cortisol levels in women with endometriosis. Brazilian J. Med. Biol. Res. 2006; 39: 1121-7.
  55. Lousse J. C., Langendonckt A. V., Defrere S. et al. Peritoneal endometriosis is an inflammatory disease. Front Biosci. 2012; 4: 23-40.
  56. Matalliotakis I., Panidis D., Vlassis G. et al. PRL, TSH and their response to the TRH test in patients with endometriosis before, during, and after treatment with danazol. Gynecol. Obste.t Invest. 1996; 42: 183-6.
  57. Matsuoka R., Yanaihara A., Saito H. et al. Regulation of estrogen activity in human endometrium: effect of IL-1beta on steroid sulfatase activity in human endometrial stromal cells. Steroids. 2002; 67: 655-9.
  58. Mehasseb M. K., Panchal R., Taylor A. H. et al. Estrogen and progesterone receptor isoform distribution through the menstrual cycle in uteri with and without adenomyosis. Fertil. Steril. 2011; 95 (7): 2228-35.
  59. Mercer F., Kozhaya L., Unutmaz D. Expression and function of TNF and IL-1 receptors on human regulatory T Cells. PLoS ONE. 2010; 5 (1): e8639.
  60. Moeller G., Adamski J. Multifunctionality of human 17beta-hydroxysteroid dehydrogenases. Mol. Cell. Endocrinol. 2006; 248: 47-55.
  61. Nan C.-L., Lei Z.-Z., Zhao Z.-J., Shi L.-H., Ouyang Y.-C., Song X.-F., Sun Q.-Y., Chen D.-Y. Increased Th1/Th2 (IFNγ/IL-4) Cytokine mRNA Ratio of rat embryos in the pregnant mouse uterus. J. Reprod. Dev. 2007; 53: 219-28.
  62. Oehler M. K., Greschik H., Fischer D. C. et al. Functional characterization of somatic point mutations of the human estrogen receptor a (hERa) in adenomyosis uteri. Molecular Human Reproduction. 2004; 10 (12): 853-60.
  63. Petracco R., Grechukhina O., Popkhadze S. et al. MicroRNA 135 Regulates HOXA10 expression in endometriosis. J. Clin. Endocrinol. Metab. 2011; 96 (12): 1925-33.
  64. Podgaec S., Abrao M. S., Dias J. A. et al. Endometriosis: an inflammatory disease with a Th2 immune response component. Human Reproduction. 2007; 22 (5): 1373-9.
  65. Podgaec S., Dias J. A. Junior, Chapron C. et al. Th1 and Th2 immune responses related to pelvic endometriosis. Rev. Assoc. Med. Bras. 2010; 56 (1): 92-8.
  66. Ponce C., Torres M., Galleguillos C. et al. Nuclear factor kB pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Clinical Reproduction. 2009; 137: 727-37.
  67. Ramon L., Gilabert-Estelles J., Castello R. et al. mRNA analysis of several components of the plasminogen activator and matrix metalloproteinase systems in endometriosis using a real-time quantitative RT-PCR assay. Hum. Reprod. 2005; 20: 272-8.
  68. Schenken R. S., Williams R. F., Hodgen G. D. Effect of pregnancy on surgically induced endometriosis in cynomolgus monkeys. Am. J. Obstet. Gynecol. 1987; 157: 1392-6.
  69. Shakiba K., Falcone T. Tumor necrosis factor-α blockers: potential limitations in the management of advanced endometriosis? A case report. Human Reproduction. 2006; 21 (9): 2417-20.
  70. Shi J. Yang Y. Dong Z., Lang J. et al. Morphological analysis on adhesion and invasion involved in endometriosis with tissue culture. Chin. Med. J. 2011; 124 (1): 148-51.
  71. Schwertner A., Conceição Dos Santos C. C., Costa G. D. et al. Efficacy of melatonin in the treatment of endometriosis: a phase II, randomized, double-blind, placebo-controlled trial. Pain. 2013; 154 (6): 874-81.
  72. Smuc T., Pucelj M. R., Sinkovec J. et al. Expression analysis of the genes involved in estradiol and progesterone action in human ovarian endometriosis. Gynecol. Endocrinol. 2007; 23: 105-11.
  73. Stoikos C. J., Salamonsen L. A., Hannan N. J. et al. Activin A regulates trophoblast cell adhesive properties: implications for implantation failure in women with endometriosis-associated infertility. Human Reproduction. 2010; 25 (7): 1767-74.
  74. Toma S. K., Stovall D. W., Hammond M. G. The effect of laparoscopic ablation or danocrine on pregnancy rates in patients with stage I or II endometriosis undergoing donor insemination. Obstet. Gynecol. 1992; 80: 253-6.
  75. Trukhacheva E., Lin Z., Reierstad S. et al. Estrogen receptor (ER) β regulates ERα expression in stromal cells derived from ovarian endometriosis. J. Clin. Endocrinol. Metab. 2009; 94 (2): 615-22.
  76. Tsai S. J., Wu M. H., Lin C. C. et al. Regulation of steroidogenic acute regulatory protein expression and progesterone production in endometriotic stromal cells. J. Clin. Endocrinol. Metab. 2001; 86: 5765-73.
  77. Velasco I., Acién P., Campos A. et al. Interleukin-6 and other soluble factors in peritoneal fluid and endometriomas and their relation to pain and aromatase expression. J. Reprod. Immunol. 2010; 84 (2): 199-205.
  78. Vercellini P., Solmigliana E., Vigano P. et al. Surgery for endometriosis - associated infertility: a pragmatic approach. Human Reproduction. 2009; 24 (2): 254-69.
  79. Wei Q., Clair J. B. St., Fu T. et al. Reduced expression of biomarkers associated with the implantation window in women with endometriosis. Fertil. Steril. 2009; 91 (5): 1686-91.
  80. Weiss G., Goldsmith L. T., Taylor R. N. et al. Inflammation in reproductive disorders. Reprod. Sci. 2009; 16 (2): 216-29.
  81. Yonezawa S., Higashi M., Yamada N. et al. Significance of mucin expression in pancreatobiliary neoplasms. J. Hepatobiliary Pancreat Sci. 2010; 17: 108-24.
  82. Zulli K., Bianco B., Mafra F. A. et al. Polymorphism of the estrogen receptor b gene is related to infertility and infertilityassociated endometriosis. Arq. Bras. Endocrinol. Metab. 2010; 54 (6): 567-71.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2013 Yarmolinskaya M.I., Denisova V.M.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

1. Я (далее – «Пользователь» или «Субъект персональных данных»), осуществляя использование сайта https://journals.rcsi.science/ (далее – «Сайт»), подтверждая свою полную дееспособность даю согласие на обработку персональных данных с использованием средств автоматизации Оператору - федеральному государственному бюджетному учреждению «Российский центр научной информации» (РЦНИ), далее – «Оператор», расположенному по адресу: 119991, г. Москва, Ленинский просп., д.32А, со следующими условиями.

2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».