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Dan C. Martin, MD
UT Medical Group, Inc.

University of Tennessee Health Science Center (UTHSC)

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Daniel Clyde Martin, M.D.
UT Medical Group, Inc.
Infertility and Gynecology
Reproductive Surgery
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Glenn Ann Martin, Ph.D.
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Deep Endometriosis

Adapted from "Recognition of Endometriosis" in
Laparoscopic Appearance of Endometriosis, Lecture Supplement
Martin DC (ed), Resurge Press, Memphis, (c)1991

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Deep endometriosis (adenomyoma) was noted by Cullen, (Cullen, 1896; Cullen, 1919) von Lockyer, (Lockyer, 1913) and Sampson. (Sampson, 1921) This lesion is a combination of fibromuscular scar plus the glands and stroma of endometriosis. (Clement, 1990; Cullen, 1919; Novak & Woodruff, 1974; Stripling, Martin, Chatman, Vander Zwaag, & Poston, 1988; Wharton, 1970) The distribution of the depth of infiltration of peritoneal lesions in referral populations was:

bullet61% and 70% of lesions penetrating greater than 2 mm,
bullet43% and 53% penetrating greater than 3 mm, and
bullet25% and 29% penetrating greater than 5 mm. (Cornillie, Oosterlynck, Lauweryns, & Koninckx, 1990; Martin, Hubert, & Levy, 1989)

The pathogenesis of deep endometriosis has long been a source of debate. (Martin, Koninckx, Batt, & Smith, 1997) Russell (Russell, 1899) and Gruenwald (Gruenwald, 1942) felt that these were related to previous Mullerian remnants. On the other hand, Sampson originally felt that endometriosis came from the ovary (Sampson, 1921) but later concluded that endometriosis was related to retrograde menstruation. (Jacobson, 1922; Sampson, 1922; Sampson, 1927) The different expressions of biochemistry and histology have led Donnez and Nisolle to conclude that peritoneal lesions are related to retrograde menstruation whereas retroperitoneal lesions are from Mullerian remnants. (Donnez, Nisolle, Smoes, Gillet, Beguin, & Casanas-Roux, 1996; Nisolle & Donnez, 1997) But the distribution supports implantation, growth, and infiltration of peritoneum. Furthermore, the finding that most if not all deep paravaginal lesions extend from or to the peritoneum (Martin, 1988) argues for infiltration or implantation into pockets with subsequent growth. Since the Mullerian system is the original source of both endometrium and Mullerian remnant, the biochemical and histologic expression may be related to peritoneal fluid microenvironment, (Koninckx & Martin, 1994) vascularization, (Batt & Smith, 1989; Batt, Smith, Buck, Naples, & Severino, 1989) local immunology, tissue resistance, loose connective tissue characteristics, genetics, or other factors. (Martin, et al., 1997)

Koninckx and Martin have described three types of clinical presentations of deep implants. (Koninckx & Martin, 1992) Type I lesions are infiltrating lesions starting at the surface and have a conical distribution. Type II lesions involve peritoneal retraction and adhesions. Type II lesions may be precursors to type III deep lesions, but these are not Allen-Masters syndrome. (Batt, 1995) Type III lesions are deep spherical lesions. These may be the result of ballooning as infiltration is into deep loose connective tissue, expansion of type II lesions, or metaplasia/growth from Mullerian remnants. (Koninckx & Martin, 1992) A combination of these origins may be needed to account for all findings. (Martin, et al., 1997)

An early publication on unrecognized spherical Type III lesions noted that 3.2% of patients with pelvic pain and 4.5% of patients with both pain and infertility had these lesions. This deep endometriosis is better recognized by palpation and becomes more apparent during excision. The depth does not correlate with the pelvic area in Type I. In two women, nodules were found only by palpation and not visualization; in a third woman, the nodule was found only during menstruation. The incidence of deep endometriosis increases with age although the total incidence remains constant. (Koninckx & Martin, 1992) In a subsequent publication, menstrual examination increased the number of palpable nodules from 4(6%) to 22(33%) in a study of 66 women. (Koninckx, Meuleman, Oosterlynck, & Cornillie, 1996) Menstrual examination is very important in the identification of deep lesions.

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Adamyan has proposed a staging system with retrocervical endometriosis as Stage I with no vaginal involvement while Stage II involves the vagina. (Adamyan, 1993) This observation agrees with other author's observations that deep retrocervical and rectovaginal nodules tend to invade the vagina and not the rectum. (Donnez, Nisolle, Casanas-Roux, Bassil, & Anaf, 1995; Martin, 1988; Nisolle & Donnez, 1997; Perry & Victoria, 1995) Adamyan Stage III involves the vagina and rectum and has cul-de-sac distortion while Stage IV includes cul-de-sac obliteration. Stages I and II have no cul-de-sac distortion and are compatible with deep Mullerian (Donnez, et al., 1996; Nisolle & Donnez, 1997) or Type III endometriosis. (Koninckx & Martin, 1992) Stages III and IV have significant cul-de-sac distortion and/or obliteration. These appear to be type I or a combination of type I and III. (Koninckx & Martin, 1992)

Deep lesions may be easier to palpate than to see. (Koninckx & Cornillie, 1993; Koninckx & Martin, 1992; Martin, 1988; Martin & Diamond, 1986; Martin & Vander Zwaag, 1987; Moore, Binstock, & Growdon, 1988; Weed & Ray, 1987) Attempts to develop visual criteria for distinguishing deep infiltration from superficial disease by surface observation have so far been unsuccessful. These deep lesions are associated with increased tenderness. (Cornillie, et al., 1990; Koninckx & Martin, 1992; Koninckx, Meuleman, Demeyere, Lesaffre, & Cornillie, 1991; Ripps & Martin, 1991; Ripps & Martin, 1992) Palpation and removal of all identifiable disease in addition to medical suppression appear important in treating pain and in decreasing the number of repeat surgeries performed. When nodularity is noted on preoperative exam, this exam should be repeated before finishing surgery. This is in order to rule out persistence of deep nodules. (Martin & Diamond, 1986) In addition, deep infiltrating areas have been noted in the process of excising what appeared to be superficial lesions.

Deep disease is generally suspected for one of three reasons:

bulletPalpable nodules on clinical exam,
bulletFocal tenderness on clinical exam, and
bulletPalpable nodules on examination under anesthesia.

Due to this, careful palpation of the posterior vagina, cul-de-sac, uterosacrals, rectovaginal septum and rectosigmoid junction is needed preoperatively. When endometriosis is seen in the posterior vagina, this generally represents extension from peritoneal disease. (Martin, 1988) This is compatible with Donnez' findings that epithelial glands interconnect. (Donnez, Nisolle, & Casanas-Roux, 1992) A distinction is made between disease in the RV septum posterior to the cervix or vaginal fornix as contrasted with disease in or near the rectum. (Donnez, et al., 1996; Martin, 1988; Martin, 1997; Martin, et al., 1997; Nisolle & Donnez, 1997; Perry & Victoria, 1995) Retrocervical and vaginal lesions that leave the cul-de-sac intact can often be resected without damaging the rectum. On the other hand, when the cul-de-sac is distorted, rectal involvement is common. (Adamyan, 1993) and may require rectal resection. Careful examination during menses is needed to be prepared for this possibility. Suppression with GnRH analogs and bowel prep increases the chance of a successful operation and decreases the chance of complications. (Koninckx, 1996)

Deep endometriosis is hard to dissect due to it's irregular and indistinct planes. Palpation at laparoscopy or laparotomy has been helpful in localizing lesions beneath the peritoneum and around the uterosacral ligaments where visualization could not differentiate between the fibrotic white of scarred endometriosis and the white of the uterosacral ligaments.

Visualization is adequate to differentiate loose connective tissue and fat from the appearance of endometriosis in most other areas. (Daniell & Feste, 1985; Redwine, 1992) The histologic presence of adequate healthy tissue at the margins of these lesions confirmed the ability to make this distinction.

bulletFibrosis surrounding endometriosis is white and firm.
bulletFat is yellow and soft.
bulletLoose connective tissue is easily dissected and spreads freely with a blunt probe.

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Manual palpation at laparotomy increases recognition of deep lesions, subperitoneal nodules, epiploic fat nodules, appendiceal nodules and infiltrating bowel lesions. The distribution of penetration depth of lesions in the patients who had laparotomy (6 to 30 mm) and the laparoscopic appearance of patients with proven, probable or possible bowel involvement suggests that some patients have penetration in the 1 mm to 10 mm range unrecognized at laparoscopy. (Martin, et al., 1989) This is, to some degree, confirmed by my patients with mesenteric endometriosis and with 6 to 20 nodules of the bowel which were found at laparotomy but had not been seen at laparoscopy. (Martin, 1991; Martin, 1995) Appendiceal lesions are also difficult to find. Almost half of those in my series have been found by palpation and not visualization. 60% of those in Pittaway's study were missed on gross inspection. (Pittaway, 1983)

These deep lesions are most common in the pouch of Douglas and uterosacrals. (Cornillie, et al., 1990) From 50%(Damario, Horowitz, & Rock, 1994) to 82%(Koninckx, et al., 1996) are missed using routine untimed clinical exam. Treatment of these deep lesions using coagulation is associated with a lower success rate than other areas. (Hasson, 1979) These lesions can present as Stage 0, Score 0 endometriosis. (Moore, et al., 1988; Nesbitt & Rizk, 1971) These areas can be hidden due to the cervical bulge(Perry & Victoria, 1995) and the cul-de-sac can be intact. (Adamyan, 1993) As an added concern, ovarian cancer and cervical cancer can cause nodularity or be coexistent with nodular endometriosis. Adequate histology is needed in these areas. (Batt & Wheeler, 1992; Walker, Manetta, Mannel, Berman, & DiSaia, 1990)

Deep endometriosis and surgery for this process is associated with increased complications. (Brudenell, 1996; Moore, et al., 1988; Nezhat, Nezhat, Nezhat, Nasserbakht, Rosati, & Seidman, 1996) Koninckx has demonstrated that fewer complications and less operative difficulty is associated with the use of preoperative medical suppression. (Koninckx, 1996) Preoperative recognition of the possibility of deep endometriosis is needed to prepare for this possibility. Menstrual examination, preoperative bowel prep and preoperative medical suppression appear to be associated for improved surgical outcome. (Koninckx, 1996; Koninckx, et al., 1996)

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bulletAdamyan, L. (1993). Additional international perspectives. In D. H. Nichols (Eds.), Gynecologic and Obstetric Surgery (pp. 1167-1182). St. Louis: Mosby Year Book.
bulletBatt, R. E. (1995). Allen-Masters syndrome is caused by trauma, not by endometriosis. J Am Assoc Gynecol Laparoscopists, 2, 245-247.
bulletBatt, R. E., & Smith, R. A. (1989). Embryologic theory of histogenesis of endometriosis in peritoneal pockets. Obstet Gynecol Clin N A, 16, 15-28.
bulletBatt, R. E., Smith, R. A., Buck, G. M., Naples, J. D., & Severino, M. F. (1989). A case series - peritoneal pockets and endometriosis: rudimentary duplications of the Mullerian system. Adolesc Pediatr Gynecol, 2, 47-56.
bulletBatt, R. E., & Wheeler, J. M. (1992). Endometriosis: Surgical Considerations. In R. B. Hunt (Eds.), Atlas of Female Infertility Surgery (pp. 405-421). St. Louis: Mosby Year Book.
bulletBrudenell, M. (1996). Medico-legal aspects of ureteric damage during abdominal hysterectomy. Br J Obstet Gynaecol, 133, 1180-1183.
bulletClement, P. B. (1990). Pathology of Endometriosis. Path Ann, 25 (part 1), 245-295.
bulletCornillie, F. J., Oosterlynck, D., Lauweryns, J. M., & Koninckx, P. R. (1990). Deeply infiltrating pelvic endometriosis: histology and clinical significance. Fertil Steril, 53, 978-983.
bulletCullen, T. S. (1896). Adenomyoma of the round ligament. Johns Hopkins Hospital Bulletin 896, 62-63((May-June)), 896??
bulletCullen, T. S. (1919). The distribution of adenomyomata containing uterine mucosa. Am J Obstet Gynecol, 80, 130-138.
bulletDamario, M. A., Horowitz, I. R., & Rock, J. A. (1994). The role of uterosacral ligament resection in conservative operation for recurrent endometriosis. J Gynecol Surg, 10, 57-61.
bulletDaniell, J. F., & Feste, J. R. (1985). Laser laparoscopy. In W. R. Keye (Eds.), Laser Surgery in Gynecology and Obstetrics (pp. 147-163). Boston: GK Hall.
bulletDonnez, J., Nisolle, M., & Casanas-Roux, F. (1992). Three-dimensional architectures of peritoneal endometriosis. Fertil Steril, 57, 980-983.
bulletDonnez, J., Nisolle, M., Casanas-Roux, F., Bassil, S., & Anaf, V. (1995). Rectovaginal septum, endometriosis or adenomyosis: laparoscopic management in a series of 231 patients. Hum Reprod, 10, 630-635.
bulletDonnez, J., Nisolle, M., Smoes, P., Gillet, N., Beguin, S., & Casanas-Roux, F. (1996). Peritoneal endometriosis and endometriotic nodules of the rectovaginal septum are two different entities. Fertil Steril, 66, 362-368.
bulletGruenwald, P. (1942). Origin of endometriosis from the mesenchyme of the celomic walls. Am J Obstet Gynecol, 44, 470-474.
bulletHasson, H. M. (1979). Electrocoagulation of pelvic endometriotic lesions with laparoscopic control. Am J Obstet Gynecol, 135, 115-121.
bulletJacobson, V. C. (1922). The autotransplantation of endometrial tissue in the rabbit. Arch Surg, 5, 281-300.
bulletKoninckx, P. R. (1996). Complications of C02 laser endoscopic excision of deep endometriosis. Hum Reprod, 11, 2263-2268.
bulletKoninckx, P. R., & Cornillie, F. J. (1993). Infiltrating endometriosis: infiltration, retraction or adenomyosis externa? In D. C. Martin (Eds.), Atlas of Endometriosis (pp. 9.1-9.8). London: Gower Med Publ.
bulletKoninckx, P. R., & Martin, D. C. (1992). Deep endometriosis: a consequence of infiltration or retraction or possibly adenomyosis externa? Fertil Steril, 58, 924-928.
bulletKoninckx, P. R., & Martin, D. C. (1994). Treatment of deeply infiltrating endometriosis. Curr Opinion Obstet Gynecol, 6, 231-241.
bulletKoninckx, P. R., Meuleman, C., Demeyere, S., Lesaffre, E., & Cornillie, F. J. (1991). Suggestive evidence that pelvic endometriosis is a progressive disease, whereas deeply infiltrating endometriosis is associated with pelvic pain. Fertil Steril, 55, 759-765.
bulletKoninckx, P. R., Meuleman, C., Oosterlynck, D., & Cornillie, F. J. (1996). Diagnosis of deep endometriosis by clinical examination during menstruation and plasma CA-125 concentrations. Fertil Steril, 65, 280-287.
bulletLockyer, C. (1913). Adenomyoma in the recto-uterine and recto-vaginal septa. Proc Royal Soc Med (Obstet), 6, 112-120.
bulletMartin, D. C. (1988). Laparoscopic and vaginal colpotomy for the excision of infiltrating cul-de-sac endometriosis. J Reprod Med, 33, 806-808.
bulletMartin, D. C. (1991). Carbon dioxide laser laparoscopy for endometriosis. Obstet Gynecol Clin N A, 18(3(September)), 575-582.
bulletMartin, D. C. (1995). Surgical treatment of endometriosis. Clin Consul Obstet Gynecol, 7, 190-199.
bulletMartin, D. C. (1997). Deep endometriosis (Abstract). Gynaecol Endoscopy, 6 (Sup 1), 16-17.
bulletMartin, D. C., & Diamond, M. P. (1986). Operative laparoscopy: comparison of lasers with other techniques. Curr Probl Obstet Gynecol Fertil, 9, 563-601.
bulletMartin, D. C., Hubert, G. D., & Levy, B. S. (1989). Depth of infiltration of endometriosis. J Gynecol Surg, 5, 55-60.
bulletMartin, D. C., Koninckx, P. R., Batt, R. E., & Smith, R. (1997). Deep endometriosis. In , H. Minaguchi, & O. Sugimoto (Eds.), Endometriosis Today Advances in Research and Practice (pp. 50-57). Lancaster: Parthenon Publishing Group.
bulletMartin, D. C., & Vander Zwaag, R. (1987). Excisional techniques for endometriosis with the CO2 laser laparoscope. J Reprod Med, 32, 753-758.
bulletMoore, J. G., Binstock, M. A., & Growdon, W. A. (1988). The clinical implications of retroperitoneal endometriosis. Am J Obstet Gynecol, 158, 1291-1298.
bulletNesbitt, R. E., & Rizk, P. T. (1971). Uterosacral ligament syndrome. Obstet Gynecol, 37(5), 730-733.
bulletNezhat, C., Nezhat, F., Nezhat, C., Nasserbakht, F., Rosati, M., & Seidman, D. S. (1996). Urinary tract endometriosis treated by laparoscopy. Fertil Steril, 66, 920-924.
bulletNisolle, M., & Donnez, J. (Ed.). (1997). Peritoneal ovarian and rectovaginal endometriosis. Parthenon Publishing.
bulletNovak, E. R., & Woodruff, J. D. (1974). Novak's Gynecologic and Obstetrical Pathology with Clinical and Endocrine Relations (Seventh ed.). Philadelphia: WB Saunders. 
bulletPerry, C. P., & Victoria, M. M. (1995). Occult retrocervical endometriosis. J Reprod Med, 40, 652-654.
bulletPittaway, D. E. (1983). Appendectomy in the surgical treatment of endometriosis. Obstet Gynecol, 61, 421.
bulletRedwine, D. B. (1992). Laparoscopic en bloc resection for treatment of the obliterated cul-de-sac endometriosis. J Reprod Med, 37, 695-698.
bulletRipps, B. A., & Martin, D. C. (1991). Focal pelvic tenderness, pelvic pain and dysmenorrhea in endometriosis. J Reprod Med, 36, 470-472.
bulletRipps, B. A., & Martin, D. C. (1992). Correlation of focal pelvic tenderness with implant dimension and stage of endometriosis. J Reprod Med, 37, 620-624.
bulletRussell, W. W. (1899). Aberrant portions of the Mullerian duct found in an ovary. Johns Hopkins Hosp Bul, 94-96(January, February, March), 8-10.
bulletSampson, J. A. (1921). Perforating hemorrhagic (chocolate) cysts of the ovary. Their importance and especially their relation to pelvic adenomas of the endometrial type ("adenomyoma" of the uterus, rectovaginal septum, sigmoid, etc.). Arch Surg, 3, 245-323.
bulletSampson, J. A. (1922). Ovarian hematomas of endometrial type (perforating hemorrhagic cysts of the ovary) and implantation adenomas of endometrial type. Boston Med Surg J, 186, 445.
bulletSampson, J. A. (1927). Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol, 14, 422-469.
bulletStripling, M. C., Martin, D. C., Chatman, D. L., Vander Zwaag, R., & Poston, W. M. (1988). Subtle appearance of pelvic endometriosis. Fertil Steril, 49, 427-431.
bulletWalker, J. L., Manetta, A., Mannel, R. S., Berman, M. L., & DiSaia, P. J. (1990). The influence of endometriosis on the staging of cervical cancer. Obstet Gynecol, 75, 543-545.
bulletWeed, J. C., & Ray, J. E. (1987). Endometriosis of the bowel. Obstet Gynecol, 69, 727-730.
bulletWharton, L. R. (1970). Endometriosis. In R. W. Te Linde & R. F. Mattingly (Eds.), Operative Gynecology (pp. 192-224). Philadelphia: JB Lippincott.

Adapted from "Recognition of Endometriosis" in
Laparoscopic Appearance of Endometriosis, Lecture Supplement
Martin DC (ed), Resurge Press, Memphis, (c)1991

The color illustrations that accompanied this paper are in the Color Atlas.

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