Chapter 3 Theories on Endometriosis

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1 Chapter 3 Theories on Endometriosis Sajal Gupta, Avi Harlev, Ashok Agarwal, and Elizabeth Pandithurai 3.1 Sampson s Theory There are several theories as to how endometriosis develops, but the most widely accepted one is Sampson s theory. First hypothesized in 1927, Sampson s theory [ 1 ] states that three elements are required to cause endometriosis: retrograde menstruation, the presence of viable cells within the retrograde menstruation, and the implantation of these viable endometrial cells, which continue to grow and form peritoneal lesions [ 1 ]. Retrograde menstruation refers to the regression of menstrual blood backwards through the fallopian tubes into the peritoneal cavity, with subsequent attachment and implantation of endometrial fragments [ 2 ]. Several studies conducted over the last six decades have suggested that retrograde menstruation occurs in most females [ 3 5 ]. According to Sampson s theory, some part of the endometrial lining refluxes back through the fallopian tubes into the peritoneal cavity during menstruation. Here, the endometrial cells can attach to local tissues and form their own nerve endings and blood supply. Although most women of reproductive age have some amount of retrograde menstrual flow, [ 6 ] their immune systems are usually able to clear the implanted cells and prevent their growth. When this does not occur, however, the patient develops endometriosis. Up to 20 % of women diagnosed with idiopathic infertility have endometrial implants as seen via laparoscopic examination [ 7 ]. Many factors that have yet to be studied further may play a role in the development of endometriosis, such as a damaged immune system, genetics, or exogenous factors [ 8 ]. There are many points that can be argued in favor of Sampson s theory. The site of occurrence of several observed peritoneal endometrial or endometriotic lesions corresponds to a tubal reflux pathway. Also, endometrial cells recovered post menstruation are viable and have the capacity to grow rapidly. These cells also have integrins on their surface that allows them to attach to the peritoneal cavity. In The Author(s) 2015 S. Gupta et al., Endometriosis: A Comprehensive Update, SpringerBriefs in Reproductive Biology, DOI / _3 17

2 18 3 Theories on Endometriosis addition, the endometrium can produce certain angiogenic factors that enable the creation of neo-angiogenesis. 3.2 Coelomic Metaplasia The oldest alternative theory to retrograde menstruation is coelomic metaplasia. Coelomic metaplasia describes the ability of normal cell derivatives of primitive parietal peritoneum to transform into endometrial tissue [ 9 ]. The metaplasia theory is used to explain endometriosis in females with absence of menstruation, such as those who are prepubescent or have a history of total abdominal hysterectomy, in premenopausal women, and in rare cases of endometriosis in males [ ]. The theory of coelomic metaplasia is based on the fact that the ovaries and Mullerian ducts are derived from the coelomic epithelium. This epithelium may undergo metaplastic transformation to form tissue much like that of the endometrium. The coelomic epithelium is a common ancestor to both peritoneal and endometrial cells, and it may transform into the latter by means of chronic inflammation [ 7 ]. The metaplasia theory is viable because it can explain the presence of endometriosis in the absence of menstruation, such as in men who undergo estrogen therapy for prostate cancer, pre-menarche women, and post-menopausal females [ 13, 14 ]. However, there are many points that argue against the idea. If the metaplasia theory is true, endometriosis would be possible without the presence of an endometrium, such as in women with a congenital absence of the uterus or in healthy males through the potential of peritoneal metaplasia. Coelomic metaplasia would then also be expected to occur anywhere in the body where tissue derived from the coelomic epithelium is found. Hence, most scientific institutions continue to cite the retrograde menstruation theory instead [ 7 ]. 3.3 Embryonic Rest Theory This theory proposes that the presence of cells of Mullerian origin within the peritoneal cavity can be induced to form endometrial tissue when subjected to the appropriate stimuli [ 15 ]. This hypothesis could account for the presence of endometriosis of the rectovaginal septum as well as in any location along the migration pathway of the embryonic Mullerian system. Furthermore, this theory could account for the presence of rare endometriosis in men because the male embryo initially develops femalespecific embryological structures that regress with activation of the male genome. This theory remains speculative, as it would require the assumption that these embryological rests persist to adulthood. Again, this theory remains unproven and purely hypothetical.

3 3.7 Stem Cell Theory Lymphatic and Vascular Metastasis Theory Endometrial tissue is usually spread through the fallopian tubes. However, the presence of endometrial tissue in remote locations may be explained by possible transport through the vasculature and lymph nodes [ 1, 16 ]. Because endometriosis most commonly occurs in the ovary, spread through the lymph nodes is likely. Results from many studies support the dissemination of endometrial tissue to distal locations in the body via detection of endometriosis in atypical locations suggesting hematogenous and/or lymphatic transport of endometrial tissue. This theory may explain why endometriosis can be found in areas outside the peritoneal cavity such as the pleura and pericardium [ 17 ]. 3.5 TIAR (Tissue Injury and Repair) Theory The TIAR theory postulates that endometriosis is caused by trauma. Either a normal chronic peristalsis or a state of hyper-peristalsis caused by an event during reproductive life leads to microtraumatizations. These microtraumatizations lead to tissue injury and repair, increasing production of local estrogen. Estrogen acts as a positive feedback for the hyper-peristalsis, resulting in self-perpetuation of the disease. This auto traumatization, together with high motility, allows endometrium to implant outside the uterine cavity [ 18 ]. 3.6 Quinn s Denervation-Reinnervation Theory According to Quinn, endometrial cells are deposited outside the uterine cavity as a result of nerve injuries. These injuries cause denervation and can occur in response to some process, such as straining during defecation or vaginal delivery, leading to an alteration of fundo-cervical polarity. The ectopic endometrial cells from the retrograde menstruation adhere to the injured tissue in the peritoneal cavity and uterosacral ligaments. Re-innervation then occurs causing pelvic pain [ 19 ]. 3.7 Stem Cell Theory According to this theory, stem cells in shedding endometrium may play a role in the pathogenesis of early onset endometriosis [ 20 ], possibly due to retrograde neonatal uterine bleeding. Some of the elements that support this hypothesis include the manifestation of overt vaginal bleeding in 5 % of neonates, which is attributed to the fact that during later stages of pregnancy, the endometrium of the fetus transforms

4 20 3 Theories on Endometriosis in to a decidualized layer that desquamates after birth. The hypothesis is further supported by the presence of functional obstruction in the endocervical canal in neonates, which leads to the regurgitation of endometrial cells into the peritoneal cavity. These endometrial cells later implant and survive long term as endometrial stem cells/progenitor cells. This is similar to the theory of retrograde menstruation proposed by Sampson explaining the pathogenesis of endometriosis in adolescent and adult population [ 21 ]. 3.8 Key Points and Summary The pathogenesis of endometriosis is multi-factorial. There are several theories including retrograde menstruation, coelomic metaplasia, lymphatic and vascular metastasis, embryonic rest, TIAR, Quinn s denervation-re-innervation theory, and stem cell theory. The most widely accepted theory is retrograde menstruation proposed by Sampson in References 1. Sampson, J. A. (1927). Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. The American Journal of Pathology, 3 (2): Giudice, L. C., & Kao, L. C. (2004). Endometriosis. Lancet, 364 (9447), Halme, J., Hammond, M. G., Hulka, J. F., Raj, S. G., & Talbert, L. M. (1984). Retrograde menstruation in healthy women and in patients with endometriosis. Obstetrics and Gynecology, 64 (2), Kruitwagen, R. F., Poels, L. G., Willemsen, W. N., de Ronde, I. J., Jap, P. H., & Rolland, R. (1991). Endometrial epithelial cells in peritoneal fluid during the early follicular phase. Fertility and Sterility, 55 (2), Liu, D. T., & Hitchcock, A. (1986). Endometriosis: Its association with retrograde menstruation, dysmenorrhoea and tubal pathology. British Journal of Obstetrics and Gynaecology, 93 (8), (1983). Retrograde menstruation. Lancet, 2 (8340): Vinatier, D., Orazi, G., Cosson, M., & Dufour, P. (2001). Theories of endometriosis. European Journal of Obstetrics, Gynecology, and Reproductive Biology, 96 (1), Vigano, P., Parazzini, F., Somigliana, E., & Vercellini, P. (2004). Endometriosis: Epidemiology and aetiological factors. Best Practice & Research. Clinical Obstetrics & Gynaecology, 18 (2), El-Mahgoub, S., & Yaseen, S. (1980). A positive proof for the theory of coelomic metaplasia. American Journal of Obstetrics and Gynecology, 137 (1), Suginami, H. (1991). A reappraisal of the coelomic metaplasia theory by reviewing endometriosis occurring in unusual sites and instances. American Journal of Obstetrics and Gynecology, 165 (1), Schrodt, G. R., Alcorn, M. O., & Ibanez, J. (1980). Endometriosis of the male urinary system: A case report. The Journal of Urology, 124 (5), Martin, J. D., Jr., & Hauck, A. E. (1985). Endometriosis in the male. The American Surgeon, 51 (7),

5 References Dictor, M., Nelson, C. E., & Uvelius, B. (1988). Priapism in a patient with endometrioid prostatic carcinoma. A case report. Urologia Internationalis, 43 (4), Pinkert, T. C., Catlow, C. E., & Straus, R. (1979). Endometriosis of the urinary bladder in a man with prostatic carcinoma. Cancer, 43 (4), Longo, L. D. (1979). Classic pages in obstetrics and gynecology. Aberrant portions of the mullerian duct found in an ovary: William Wood Russell Johns Hopkins Hospital Bulletin, vol. 10, pp. 8 10, American Journal of Obstetrics and Gynecology, 134 (2), Ueki, M. (1991). Histologic study of endometriosis and examination of lymphatic drainage in and from the uterus. American Journal of Obstetrics and Gynecology, 165 (1), Cassina, P. C., Hauser, M., Kacl, G., Imthurn, B., Schroder, S., & Weder, W. (1997). Catamenial hemoptysis. Diagnosis with MRI. Chest, 111 (5), Leyendecker, G., Wildt, L., & Mall, G. (2009). The pathophysiology of endometriosis and adenomyosis: Tissue injury and repair. Archives of Gynecology and Obstetrics, 280 (4), Quinn, M. J. (2011). Endometriosis: The consequence of uterine denervation-reinnervation. Archives of Gynecology and Obstetrics, 284 (6), Maruyama, T., & Yoshimura, Y. (2012). Stem cell theory for the pathogenesis of endometriosis. Frontiers in Bioscience (Elite Edition), 4, Gargett, C. E., Schwab, K. E., Brosens, J. J., Puttemans, P., Benagiano, G., & Brosens, I. (2014). Potential role of endometrial stem/progenitor cells in the pathogenesis of early-onset endometriosis. Molecular Human Reproduction, 20 (7),

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