Characteristic images of deeply in ltrating rectosigmoid endometriosis on transvaginal and transrectal ultrasonography
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1 Human Reproduction Vol.18, No.6 pp. 1328±1333, 2003 DOI: /humrep/deg243 Characteristic images of deeply in ltrating rectosigmoid endometriosis on transvaginal and transrectal ultrasonography Kaori Koga 1, Yutaka Osuga 1,3, Tetsu Yano 1, Mikio Momoeda 1, Osamu Yoshino 1, Yasushi Hirota 1, Koji Kugu 1, Osamu Nishii 1, Osamu Tsutsumi 1,2 and Yuji Taketani 1 1 Department of Obstetrics and Gynecology, University of Tokyo, Hongo, Bunkyo-ku, Tokyo and 2 CREST Japan Science and Technology, Honmachi, Kawaguchi , Japan 3 To whom correspondence should be addressed. yutakaos-tky@umin.ac.jp BACKGROUND: To evaluate the usefulness of transvaginal and transrectal ultrasonography for diagnosis and management of deeply in ltrating rectosigmoid endometriosis. METHODS: A series of six patients (aged 32±39 years) with rectosigmoid endometriosis underwent transvaginal and transrectal ultrasonography. In three patients undergoing surgical resection of the intestine, the ultrasonographic ndings were compared with macroscopic and microscopic ndings. In one patient, sequential observations of the lesion using ultrasonography were conducted before and after medical treatment and following childbirth. RESULTS: In all cases, the lesion was detected as a hypoechoic irregular-shaped area surrounded by a hyperechoic rim located posterior to the uterus, with size ranging from to mm in diameter. The comparison of the ultrasonographical ndings with histology revealed that the hypoechoic irregular-shaped area corresponded to a layer of hypertrophic muscularis propria of the lesion, while the hyperechoic rim represented the layer including the, sub and serosa. In one patient, the lesion decreased in size and lost its central hypoechoic area after childbirth in association with pain relief. CONCLUSIONS: Transvaginal and transrectal ultrasonography provides characteristic appearances for rectosigmoid endometriosis that correlate well with its histological ndings. The procedures would be useful in the management of rectosigmoid endometriosis. Key words: endometriosis/rectum/ultrasound Introduction is de ned as the presence of endometrial tissue outside the uterus. The prevalence of this disease is estimated to be ~10% in all women (Olive and Schwartz, 1993). Gastrointestinal involvement by endometriosis is found at surgery in ~12% of patients with this disease, and the rectosigmoid is most commonly affected site (MacAfee and Greer, 1960). Most rectosigmoid involvement is seen within the serosa, and the lesions rarely in ltrate deeply into the intestinal wall and produce a nodular mass. However, the deeply in ltrating type of rectosigmoid endometriosis is of signi cant importance, because it often yields severe intestinal symptoms including haematochezia and dyschezia, and usually requires careful and intensive treatment. Thus, in this paper we use the term `rectosigmoid endometriosis', restricting it to mean the deeply in ltrating type. Various diagnostic techniques for rectosigmoid endometriosis, such as colonoscopy, barium enema (Scarmato et al., 2000), magnetic resonance imaging (MRI) (Kinkel et al., 1999; Dumontier et al., 2000) and endoscopic ultrasonography (EUS) (Chapron et al., 1998; Roseau et al., 2000), have been documented, but to our knowledge, there is only one case report which showed the usefulness of transvaginal (TV) ultrasonography in detecting the disease (Gorell et al., 1989). The aims of this study were to report our initial experience with the use of TV or transrectal (TR) ultrasonography (US) in the management of rectosigmoid endometriosis, and to evaluate the characteristic ndings of obtained images especially in comparison with histological ndings. Materials and methods Six women (mean age 34.8; range 32±39 years) treated for rectosigmoid endometriosis from 1998 to 2001 were included in this study. was con rmed pathologically in ve cases, on biopsied specimens in two cases and on resected specimens in three cases. Although no pathological veri cation was available in one patient, the clinical ndings were compatible with rectosigmoid endometriosis ã European Society of Human Reproduction and Embryology
2 Rectosigmoid endometriosis on ultrasonography Table I. Clinical and imaging ndings in six patients with rectosigmoid endometriosis Patient No. Age (years) Gravida parity Previous operations Symptoms Other endometriotic lesions Colonoscopy Barium enema (lesion location) MRI Operation Pathological Dx of biopsy specimen Pathological Dx of resected specimen 1 38 G2P2 TAH + LSO due to endometriosis Haematochezia, dyschezia 2 39 G2P2 None Haematochezia, dyschezia, diarrhoea 3 33 G0P0 None Haematochezia, dyschezia, diarrhoea 4 35 G0P0 None Haematochezia, dyschezia 5 32 G0P0 Uterine myomectomy 6 32 G0P0 Ovarian endometrial, cystectomy Haematochezia, dyschezia, diarrhoea Haematochezia, dyschezia Pelvis Post-vaginal vault Post-vaginal vault Post-vaginal vault, bladder Pelvis, ovary Pelvis, ovary, bladder mass mass, l oedema Subl tumour mass, l ulcer Subl tumour mass, l ulcer folds (R-S/C) folds, extrinsic mass (R) folds (S/C) folds, extrinsic mass (S/C) NED LAR In amed NED TAH + LAR Normal Lesion was not clearly detected NED T2WI low, CE (6) mass with irregular margin NED HAR + resection of retrovaginal endometriosis In amed (mp-sm) (mp-sm) In amed (ss-sm) (ss-m) (ss-sm) TAH = total abdominal hysterectomy; LSO = left salpingooophorectomy; LAR = low anterior resection; HAR = high anterior resection; MRI = magnetic resonance imaging; T2WI = T 2 -weighted image; CE = contrast enhancement; R = rectum; S/C = sigmoid colon; NED = no evidence of disease; ss = subserosa; sm = sub; m = ; mp = muscularis propria; Dx = diagnosis. US was for all the patients by gynaecologists (Y.O. and K.K.) with Sonovista-Ex (Mochida, Tokyo, Japan) equipped with TV probe of 5±7.5 MHz. The probe, covered with a rubber sheath containing a small amount of gel, was rstly introduced via the vagina (TV US). Scans were obtained in a routine gynaecological work-up manner, with a special attention to the perirectal region. Then, the probe was inserted into the rectum under local anaesthesia using 2% lidocaine gel (Xylocaine jelly; AstraZeneca, Osaka, Japan) and advanced until the midline image of the uterine cervix was visualized on the longitudinal plane (TR US). Other examinations conducted were colonoscopy, biopsy and MRI in all six cases, and barium enema in four. MRI was without special techniques such as contrast enhancement or rectal distension, and the ndings were assessed by radiologists who were aware of the earlier diagnostic examinations but were unaware of the subsequent surgical or histological ndings. The biopsied or resected specimens were reviewed by both pathologists and gynaecologists. With the aim of correlating ultrasonographic appearance with histological architecture of the lesion, in one case, we introduced the TV US probe into the resected intestine from its anal side, placed it onto the lesion and obtained its US image, which was highly suggestive of the presence of endometriosis. The specimen was then incised at the lesion scanned with US and examined macro- and microscopically. In two other patients undergoing bowel resection, the specimens were also reviewed macro- and microscopically. In another patient, we observed sequential changes of US ndings of pathologically diagnosed rectosigmoid endometriosis before and after medical treatment and childbirth. Results The clinical characteristics of the patients are summarized in Table I. Four out of the six women were nulliparous. Three women had a past history of surgery, each having either hysterectomy and left salpingoophorectomy due to endometriosis, uterine myomectomy or laparoscopic ovarian endometrial cystectomy. They all reported hematochezia and dyschezia, and three of them presented with diarrhoea. In three women the bowel symptoms were related to their menstrual cycles. Other symptoms included dysuria in two, dyspareunia in one and dysmenorrhoea in four. All the patients tolerated the TV or TR US procedure well, without any complications. In every case, TV or TR US demonstrated a homogeneous, hypoechoic irregular-shaped area with a hyperechoic rim (Figure 1). Our impression was that TV US yielded images in the whole pelvis cavity including the bladder, the uterus and ovaries, whereas TR US determined the location and structure of the lesion more precisely than TV US. All the lesions were detected posterior to the uterus at the level of the isthmus. The size of the six lesions ranged from to mm. Other ultrasonographic ndings included ovarian cysts in two patients (patients 5 and 6) and bladder endometriosis in two (patients 4 and 6). Colonoscopy visualized l elevation mimicking a subl tumour (two of six) or an extrinsic mass with 1329
3 K.Koga et al. stricture (four of six) in the rectosigmoid colon. The seemed to be intact (three of six) or oedematous (one of six), or ulcerated (two of six). All the lesions were located between 8 and 15 cm from the anal verge. Barium enema was carried out for four patients. The ndings were stricture (four of four), extrinsic mass effect (two of four) and folds (four of four). The location of all the lesions was the rectosigmoid colon. MRI was in all the cases, but none of the six lesions was clearly identi ed. The result of biopsy under colonoscopy was positive for endometriosis in two cases, while the other four cases showed only in amed e. Among these four cases, in three we conducted bowel resection by laparotomy (low anterior resection = 2, high anterior resection = 1), endometriosis being pathologically con rmed in the resected specimens; i.e. ve cases in total were pathologically diagnosed with rectosigmoid endometriosis. The extent of the lesion was as follows; two involving the muscularis propria and sub, two from the subserosa to sub and one from the subserosa to. Figure 2a shows US image of the lesion when the TV probe was put onto the lesion in the resected intestine (patient 1). The image was virtually identical to the preoperative TR US ndings (Figure 2b), showing a typical hypoechoic irregularshaped area with hyperechoic rim. The resected specimen, subsequently being incised at the plane including the lesions, showed subl tumour-like protrusion accompanied by thickening of the muscularis propria and brotic adhesion and convergence of the serosa (Figure 2c,d). The hypoechoic irregular-shaped area in US image seemed identical to the thickened layer of the muscularis propria, where hypertrophic and hyperplastic muscularis propria associated with in ammatory changes and brosis around invading endometriosis was microscopically con rmed (Figure 2e). The hyperechoic rim was almost consistent with the layer of the, sub and serosa, although the correspondence may not be completely identical. In other two patients, macro- and microscopic examinations of the resected specimens also revealed the hyperplastic muscularis propria and brotic adhesion of the serosa around invading endometriosis. Figure 1. US ndings obtained by TV (c and f) ortr(a, b, d, e) US in six patients with rectosigmoid endometriosis (a±f correspond to the patient numbers 1±6 in Table I). In every case, TV or TR US demonstrated a homogeneous, hypoechoic irregular-shaped area surrounded by a hyperechoic rim posterior to the uterus at the level of the isthmus (arrows). The size of the six lesions ranged from to mm. Figure 2. Rectosigmoid endometriosis in a 38-year-old woman who underwent low anterior resection (patient 1 in Table I). (a) US image of the resected specimen. A TV US probe was introduced into the resected intestine from its anal side, put onto the lesion and the image was obtained. This image is virtually identical to pre-operative transrectal US ndings (b). (c) The resected specimen of the rectosigmoid colon. (d) Higher magni cation of the image in (c). The specimen incised at the corresponding plane shows subl tumour-like protrusion accompanied by thickening of muscularis propria and brotic adhesion and convergence of serosal tissues. (e) Photomicrograph of the resected specimen showing endometriosis invasion accompanied by hypertrophy and hyperplasia of muscularis propria, and in ammation and brosis. Haematoxylin±eosin stain; original magni cation 340. Figure 4. A likely pathological mechanism for the formation of an intestinal wall protrusion that can be detected as a typical US pattern. (a) Resected specimen of rectosigmoid endometriosis in a 33-year-old woman (patient 3 in Table I). Transversal sectioned gross pathological specimen (b) and histological specimen (c, haematoxylin±eosin stain, original magni cation 34) are shown. Hyperplastic muscularis propria and brotic adhesion of the serosa around invading endometriosis were observed. (d) Illustration of the mechanism of protrusion formation. Thickening of muscularis propria and brotic adhesion and convergence is suggested to play a cooperative role to create the protrusion. m, ; sm = sub; mp = muscularis propria; s = serosa. 1330
4 Rectosigmoid endometriosis on ultrasonography Figure 2. Legend on facing page. Figure 4. Legend on facing page. 1331
5 K.Koga et al. Figure 3. The sequential US appearance of pathologically diagnosed rectosigmoid endometriosis in a 32-year-old woman who had haematochezia and dyschezia (patient 5 in Table I). TV US image at her rst visit (a), and after 2 months treatment with GnRH agonist (b). The lesion decreased in size and lost its central hypoechoic area after subsequent spontaneous pregnancy and childbirth (c). The change was accompanied by the relief of the patient's symptoms. Figure 3 shows sequential TV US images of pathologically diagnosed rectosigmoid endometriosis during a 3-year followup period (patient 5). The lesion detected with TV US at her rst visit (Figure 3a) appeared similar after 2 months treatment with GnRH agonist (Figure 3b). It decreased in size and lost its central hypoechoic area after subsequent spontaneous pregnancy and childbirth (Figure 3c). The change was accompanied by the relief of the patient's symptoms. Discussion In the present study, we demonstrated that TV or TR US ndings of rectosigmoid endometriosis correlated with histopathological ndings. All the lesions were visualized as homogeneous, hypoechoic irregular-shaped areas with a hyperechoic rim. Figure 4 illustrates a likely pathological mechanism for protrusion formation in rectosigmoid endometriosis, which yields the typical US pattern. It has been reported that intestine affected by endometriosis shows hypertrophy and hyperplasia of the muscularis propria and brosis in the serosa (Yantiss et al., 2001). Theoretically, thickening of the muscularis propria and brotic adhesion and convergence of the serosa seems to be responsible for yielding the protrusion. We also observed the sequential changes of US ndings in long-term follow-up. The effects of GnRH agonist or pregnancy on rectosigmoid endometriosis have not been well documented and seem to be variable between the cases. Our experience suggests that TV or TR US can be useful in monitoring treatment response of rectosigmoid endometriosis as well as in detecting the disease. To date, various techniques such as colonoscopy, barium enema (Scarmato et al., 2000) or MRI (Kinkel et al., 1999; Dumontier et al., 2000) have been introduced for the diagnosis of endometriosis. However, none of them yields speci c ndings in this disease or has much sensitivity (Zwas and 1332 Lyon, 1991). In this study, we did not detect any speci c ndings with colonoscopy or barium enema, and the lesions were not clearly identi ed by MRI; however, contrast enhancement or rectal distension might have provided more precise images (Kinkel et al., 1999; Dumontier et al., 2000). Using TR US, there have been two studies that visualized deep endometriotic lesions; one examined the uterosacral ligaments in ltrated with endometriosis (Ohba et al., 1996) and the other showed the ndings of endometriosis invading the rectovaginal septum (Fedele et al., 1998). In these studies, however, there was no discussion of the feasibility of TV or TR US in the assessment of rectosigmoid endometriosis. On the other hand, a recent study employed EUS to visualize rectosigmoid endometriosis (Chapron et al., 1998; Roseau et al., 2000). The study describes the appearance of rectosigmoid endometriosis as a hypoechoic mass of the fourth layer of the rectal wall, i.e. the muscularis propria. This nding is in accordance with ours in that the muscularis propria of the colon invaded with endometriosis produced a hypoechoic feature on ultrasonography. Certainly, the information obtained by TV or TR US has limitations, and additional examinations such as barium enema, colonoscopy, EUS (Chapron et al., 1998; Roseau et al., 2000) or MRI (Dumontier et al., 2000) would be needed, especially for pre-operative assessment of the lesion. However, TV US is simple and less invasive than other examination, for instance, no bowel preparation is needed and patients rarely complain of pain or discomfort. As the present study was limited to a small number of cases, we cannot determine the sensitivity and speci city of our US technique for diagnosis of rectosigmoid endometriosis. Further investigation is needed to broaden the spectrum of TV or TR US ndings associated with intestinal endometriosis. In conclusion, our study demonstrated that TV and TR US provide characteristic images of rectosigmoid endometriosis
6 Rectosigmoid endometriosis on ultrasonography that relate to its histological features. TV and TR US should be considered a valid and useful diagnostic tool in the detection and management of the disease. References Chapron, C., Dumontier, I., Dousset, B., Fritel, X., Tardif, D., Roseau, G., Chaussade, S., Couturier, D. and Dubuisson, J.B. (1998) Results and role of rectal endoscopic ultrasonography for patients with deep pelvic endometriosis. Hum. Reprod., 13, 2266±2270. Dumontier, I., Roseau, G., Vincent, B., Chapron, C., Dousset, B., Chaussade, S., Moreau, J.F., Dubuisson, J.B. and Couturier, D. (2000) Comparison of endoscopic ultrasound and magnetic resonance imaging in severe pelvic endometriosis. Gastroenterol. Clin. Biol., 24, 1197±1204. Fedele, L., Bianchi, S., Portuese, A., Borruto, F. and Dorta, M. (1998) Transrectal ultrasonography in the assessment of rectovaginal endometriosis. Obstet. Gynecol., 91, 444±448. Gorell, H.A., Cyr, D.R., Wang, K.Y. and Greer, B.E. (1989) Rectosigmoid endometriosis. Diagnosis using endovaginal sonography. J. Ultrasound Med., 8, 459±461. Kinkel, K., Chapron, C., Balleyguier, C., Fritel, X., Dubuisson, J.B. and Moreau, J.F. (1999) Magnetic resonance imaging characteristics of deep endometriosis. Hum. Reprod., 14, 1080±1086. MacAfee, C.H.G. and Greer, H.L.H. (1960) Intestinal endometriosis: a report of 29 cases and survey of the literature. J. Obstet. Gynecol., 67, 539±555. Ohba, T., Mizutani, H., Maeda, T., Matsuura, K. and Okamura, H. (1996) Evaluation of endometriosis in uterosacral ligaments by transrectal ultrasonography. Hum. Reprod., 11, 2014±2017. Olive, D.L. and Schwartz, L.B. (1993). N. Engl. J. Med., 328, 1759±1769. Roseau, G., Dumontier, I., Palazzo, L., Chapron, C., Dousset, B., Chaussade,S., Dubuisson, J.B. and Couturier, D. (2000) Rectosigmoid endometriosis: endoscopic ultrasound features and clinical implications. Endoscopy, 32, 525±530. Scarmato, V.J., Levine, M.S., Herlinger, H., Wickstrom, M., Furth, E.E. and Tureck, R.W. (2000) Ileal endometriosis: radiographic ndings in ve cases. Radiology, 214, 509±512. Yantiss, R.K., Clement, P.B. and Young, R.H. (2001) of the intestinal tract: a study of 44 cases of a disease that may cause diverse challenges in clinical and pathologic evaluation. Am. J. Surg. Pathol., 25, 445±454. Zwas, F.R. and Lyon, D.T. (1991). An important condition in clinical gastroenterology. Dig. Dis. Sci., 36, 353±364. Submitted on September 18, 2002; resubmitted on December 2, 2002; accepted on February 21,
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