Role of imaging in endometriosis

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Transvaginal ultrasonography and magnetic resonance imaging are essential for confirming endometriosis diagnosis and guiding surgical treatment.

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This review article evaluates the diagnostic utility of imaging techniques, primarily transvaginal ultrasonography and magnetic resonance imaging, for detecting endometriosis. The authors emphasize that while clinical examination and serum CA-125 levels have limited predictive value, advanced imaging is essential for confirming presumptive diagnoses and mapping the location and depth of lesions prior to surgical intervention. A significant caveat noted is that the accuracy of these modalities heavily depends on operator skill, particularly for ultrasound, and may require bowel preparation or additional studies like MRI to fully assess deeply infiltrating disease. This paper is centrally about endometriosis — specifically the role of radiologic imaging in diagnosing and characterizing the extent of pelvic lesions.

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Abstract

Endometriosis--the presence of endometrial tissue outside the uterine cavity--is first suspected on the basis of its signs and symptoms. The diagnosis is confirmed by imaging and surgery. Imaging, particularly transvaginal ultrasonography and magnetic resonance imaging, is essential to confirm the diagnosis and guide surgical treatment.
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GIUSEPPE LO MONTE, MD Department of Morphology, Surgery and Experimental Medicine, University of Ferrara, Ferrara, Italy JEAN MARIE WENGER, MD Department of Gynecology and Obstet- rics, Division of Gynecology, Geneva University Hospitals, Geneva, Switzerland PATRICK PETIGNAT, MD Department of Gynecology and Obstet- rics, Division of Gynecology, Geneva University Hospitals, Geneva, Switzerland ROBERTO MARCI, PhD Department of Morphology, Surgery and Experimental Medicine, University of Ferrara, Ferrara, Italy Imaging in Practice Role of imaging in endometriosis ABSTRACT Endometriosis—the presence of endometrial tissue outside the uterine cavity—is first suspected on the basis of its signs and symptoms. The diagnosis is confirmed by imaging and surgery. Imaging, particularly transvaginal ultrasonography and magnetic resonance imaging, is essential to confirm the diagnosis and guide surgical treatment. KEY POINTS The diagnostic evaluation should always start with trans- vaginal ultrasonography of the pelvic structures followed by magnetic resonance imaging, especially if deeply infiltrating endometriosis is suspected. An inaccurate imaging evaluation may lead to an incom- plete excision of lesions if the patient undergoes surgery. Transvaginal ultrasonography and magnetic resonance imaging allow the assessment of the size, location, and extent of the lesions. Given the multifocal nature of the disease, a thorough evaluation of all pelvic structures, including the bowel, the bladder, and the ureters, is always recommended. CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 81 • NUMBER 6 JUNE 2014 361 A 32-year-old woman presents with a his- tory of pelvic pain, dysmenorrhea, dys- pareunia, dyschezia, and dysuria, with exacer - bation of the symptoms during her menstrual cycles. Her menarche occurred at the age of 13 and her menses are regular. She has never undergone surgery and has no relevant patho- logic processes. She also reports that for the past 18 months she has been unsuccessfully trying to conceive. T wo months ago, she went to the emergen- cy department because of an acute episode of severe pelvic pain associated with abdominal cramps, vomiting, and dyschezia, occurring at the beginning of her menstrual cycle. At that time, her vital signs were within normal limits, but deep palpation of the right iliac fossa was painful. On that occasion, acute abdomen and bowel obstruction were excluded. Now, vaginal examination reveals a bluish, painful, bulky induration in the posterior for - nix. Digital rectal examination reveals a circu- lar infiltrated area in the anterior rectal wall. Her cancer antigen 125 (CA 125) level is 230 U/mL (normal range 0–35 U/mL). ■ MENSES-RELATED SYMPTOMS AND THE DIAGNOSIS OF ENDOMETRIOSIS The diagnosis of endometriosis should be con- sidered in the patient described above. Many of her signs and symptoms can be associated with several diseases. However, the diagnostic hypothesis points strongly toward endometrio- sis, since her symptoms recur at the beginning of every menstrual cycle. 1 Endometriosis is the presence of endome- trial tissue outside the uterine cavity. The af- fected organs usually include the ovaries, fallo- pian tubes, 2 peritoneal surface, vagina, cervix, IMAGING IN PRACTICE doi:10.3949/ccjm.81a.13032 EDUCATIONAL OBJECTIVE: Readers will order appropriate imaging if patients present with symptoms that suggest endometriosisCREDIT CME 362 CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 81 • NUMBER 6 JUNE 2014 IMAGING IN ENDOMETRIOSIS abdominal wall,3 scar tissue, pouch of Douglas, urinary tract, and bowel. However, any organ can be involved. So-called deeply infiltrating endometriosis is an endometriotic lesion penetrating into the retroperitoneal space (most often affecting the uterosacral ligaments and the rectovaginal septum) or the pelvic-organ wall to a depth of at least 5 mm and involving structures such as the rectum, vagina, ureters, and bladder. 4 Its clinical presentation is highly variable, rang- ing from no symptoms to severe pain and dys- function of pelvic organs. Endometriosis can be diagnosed with cer - tainty only when the endometriotic lesions are observed by laparoscopy or laparotomy and after the histologic examination of sur - gically resected lesions ( FIGURE 1 ).1 However, a presumptive diagnosis can be made on the basis of imaging findings, which can be useful in the differential diagnostic process (TABLE 1). ■ EXAMINATION AND BLOOD MARKERS PROVIDE LIMITED INFORMATION Knowing the history of the patient, along with a physical examination that includes speculum and bimanual vaginal and rectal examination, can be helpful in the diagnostic process even if nothing abnormal is found. Pelvic examination has a poor predictive value, as demonstrated in a study conducted by Nezhat et al 5 in 91 patients with surgically confirmed endometriosis, 47% of whom had a normal bimanual examination. CA 125 is the serologic marker most often used for diagnosing endometriosis. Levels are usually high in the sera of patients with endo- metriosis, especially in the advanced stages. 6 However, levels increase both in the physi- ologic menstrual cycle and in epithelial ovar - ian cancers.7 Thus, the diagnostic value of CA 125 is limited in terms of both sensitivity and specificity. ■ INCLUDE IMAGING IN THE DIAGNOSTIC WORKUP Surgical treatment is frequently offered to pa- tients who have severe pelvic pain that does not respond to medical treatment, or in cases of infertility. Imaging investigations are man- datory both to ascertain the diagnosis and to assess involvement of internal organs before surgery. Moreover, imaging helps minimize the surgical risks. The primary aim of the radiologic exami- nation is to describe the precise location, the depth, and the number of pelvic endometri- otic lesions. Furthermore, imaging is useful to check for endometriotic foci in pelvic organs such as the bowel, ureters, and bladder, which are often involved in the pathologic process. Transvaginal ultrasonography and magnet- ic resonance imaging (MRI) can accurately delineate deeply infiltrating lesions of endo- metriosis that are not easily accessible laparo- scopically. Transvaginal ultrasonography Transvaginal ultrasonography is the first-line imaging study when endometriosis is suspect- ed: it is powerful, simple, widely available, and cost-effective. In particular, it is recom- mended for diagnosing endometriotic ovarian cysts (endometriomas) 8,9 and endometriosis of the bladder.10 However, its value for the assess- ment of superficial peritoneal lesions, ovarian foci, and deeply infiltrating endometriosis is questionable. Although uncomfortable for the patient, transvaginal ultrasonography should be per - formed during menses, or when the pain reaches its highest level. In fact, during men- strual bleeding the endometrial implants grow and become easier to detect. Endometriosis can involve any organ Medical history Physical examination Serologic markers (eg, cancer antigen 125) Presumptive diagnosis of pelvic endometriosis Transvaginal ultrasonography Symptoms or radiologic signs suggesting concomitant bowel or bladder endometriosis Magnetic resonance imaging Double-contrast barium enema Multislice computed tomography Cystoscopy Transrectal ultrasonography Laparoscopy and biopsy Definitive diagnosis of endometriosis FIGURE 1. Diagnostic algorithm for endometriosis. CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 81 • NUMBER 6 JUNE 2014 363 LO MONTE AND COLLEAGUES Mais et al 8 reported that transvaginal ul- trasonography has a sensitivity of 88% in dif- ferentiating endometriomas from other ovar - ian masses, and a specificity of 90% (FIGURE 2). Furthermore, its specificity is as high as that of MRI. 8,9 Endometriotic nodules detected in the uterosacral ligaments, rectovaginal sep- tum, vagina, vesicouterine pouch, bladder (FIGURE 3 ), and ureters can be signs of deeply infiltrating endometriosis. Pelvic adhesions can be suspected when pelvic organs appear fixed to each other, when hyperechogenic plaques are found between the serosal sur - faces of the different organs, and when the pouch of Douglas is partially or completely obliterated. The accuracy of transvaginal ultrasonogra- phy strongly depends on the operator’s skill. Furthermore, lesions of the sigmoid colon are impossible to visualize by transvaginal ultrasonography; hence, further diagnostic procedures are required. Transvaginal ultra- sonography is the most accurate technique in detecting endometriotic nodules of the blad- der wall in patients with urinary symptoms. Transvaginal ultrasonography combined with color Doppler can also demonstrate the flow of urine through the ureters to the blad- der, thereby ascertaining the patency of the ureters and clarifying the anatomic relation- ship between the ureters and any endometri- otic lesions in the detrusors. 10 Hydronephrosis can arise from ureteral restriction caused by TABLE 1 Differential diagnosis of endometriotic lesions detected at imaging according to location Location Differential diagnosis Additional information Bladder Urachal remnant Epithelial tumor Mesenchymal tumor Cystoscopic evaluation may provide additional information Perimetrium and round ligaments Subserosal leiomyoma Other neoplasm At laparoscopy, endometriosis appears as red/black/white scarred lesions associated or not with adhesions Retrocervical region Peritoneal metastasis (ie, gastrointestinal cancer) Ovarian malignancy Ascites and tumor mass detected elsewhere in the abdominal cavity guide the diagnosis to metastatic malignancies At laparoscopy, retrocervical deeply infiltrating endometriosis is easily recognized Rectovaginal space Bladder cancer Vaginal cancer Anorectal cancer The region is not easily accessible for endoscopic viewing Rectosigmoid colon Bowel-constricting neoplasm Metastatic implants to the bowel Colonoscopy easily detects epithelial colon cancers; unlike colon cancer, deeply infiltrating endometriosis starts at the serosal layer and rarely affects the mucosa Ureters Ureteral cancer Extrinsic ureteral obstruction due to gastrointestinal or gynecologic malignancies Correct diagnosis requires detection of the epicenter of the mass Renal ultrasonography is useful to reveal hydronephrosis Ovaries Hemorrhagic corpus luteum Dermoid cyst Ovarian cancer Transvaginal ultrasonography, magnetic resonance imaging, or computed tomography usually provides sufficient information 364 CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 81 • NUMBER 6 JUNE 2014 IMAGING IN ENDOMETRIOSIS endometriotic nodules. Thus, transabdominal ultrasonography of the kidneys is always rec- ommended when deeply infiltrating endome- triosis is suspected. Some centers use a bowel-preparation pro- tocol consisting of a laxative taken 24 hours be- fore the procedure, combined with a low-residue diet and an enema 1 hour before the examina- tion to cleanse the rectosigmoid colon of fecal content and gas, which can interfere with the visual examination of the pelvic structures. 11 Transabdominal ultrasonography Transabdominal ultrasonography can be used instead of transvaginal ultrasonography, eg, in young girls and women who have never been sexually active. When transabdominal ultra- sonography is selected, the patient should have a full bladder to maximize the visualiza- tion of the pelvic structures. However, trans- vaginal ultrasonography is generally more sensitive than transabdominal in detecting adnexal masses and pelvic nodules. 12 Magnetic resonance imaging MRI has been recently introduced in the di- agnosis of endometriosis. MRI is less operator- dependent than transvaginal ultrasonography and is more sensitive for detecting foci of deeply infiltrating endometriosis, because of its ability to completely survey the anterior and posterior compartments of the pelvis. How- ever, its diagnostic value in cases of bladder endometriosis, superficial peritoneal lesions, and ovarian foci is still controversial. 13–16 On MRI, lesions of deeply infiltrating en- dometriosis mainly appear as areas or nodules with regular, irregular, indistinct, or stellate margins. A distortion of the normal pelvic anatomy or the detection of a loculated fluid collection can indirectly signal the presence of adhesions. MRI has high specificity for the diagnosis of endometriomas as a result of its ability to detect aged hemorrhagic content ( FIGURE 4).17 Despite the many studies that point to the limits of MRI in detecting small endometri- otic lesions, recent studies demonstrated that MRI also has good sensitivity for small peri- toneal implants and adhesions. 18,19 The injec- tion of gadolinium contrast is still a debatable measure, because contrast-enhanced imaging cannot differentiate infiltrating lesions from other normal fibromuscular pelvic anatomic structures. 15,20 Bowel preparation can be done with an oral laxative the day before imaging, comple- mented by a low-residue diet. A single dose of a ready-to-use enema is given 30 minutes before the examination to cleanse the termi- nal section of the intestinal tract. To avoid motion artifacts caused by bowel peristalsis, images are obtained after intramuscular injec- tions of a myorelaxant are given, if there is no contraindication. Bowel preparation is useful to eliminate fecal residue and gas, thereby al- lowing proper visualization of lesions of deeply infiltrating endometriosis, but it is not rou- tinely prescribed in all centers. 11 FIGURE 2. Endometriotic ovarian cysts (endometriomas) (ar- row) on transvaginal ultrasonography. FIGURE 3. Transvaginal ultrasonography in the sagittal plane shows an endometriotic nodule in the posterior wall of the bladder (arrow). CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 81 • NUMBER 6 JUNE 2014 365 LO MONTE AND COLLEAGUES In most cases, endometriotic lesions have an MRI signal intensity that comes very close to that of the surrounding fibromuscular struc- tures. In this regard, vaginal and rectal disten- tion and opacification using ultrasonographic gel clearly help to delineate the cervix, vagi- nal fornices, and vaginal wall, as well as the rectum and wall of the rectosigmoid junction ( FIGURE 5).20 ■ PRESURGICAL IMAGING Rectal endoscopic ultrasonography Even though it should not be included in the routine diagnostic workup, rectal endoscopic ul- trasonography, using a flexible echoendoscope, is suitable in certain presurgical cases. The aim of this imaging technique is to assess the depth of bowel wall infiltration thanks to the visual- ization of the different layers. 21 Double-contrast barium enema and multislice computed tomography Double-contrast barium enema is extensively used for the diagnosis of bowel endometriosis, once the decision to perform surgery has been made. It allows evaluation of the degree and length of the bowel occlusion at the level of the sigmoid or high rectosigmoid tract, but it does not permit differentiation of bowel en- dometriosis from other pathologies. Multislice computed tomography offers the opportunity to evaluate the depth of the lesions with excellent precision. 22 The most relevant disadvantage of both procedures is the exposure of women of repro- ductive age to ionizing radiation. In addition, multislice computed tomography requires the administration of an intravenous iodinated contrast medium and a retrograde colonic dis- tention with about 2 L of water. ■ ■ REFERENCES 1. Attaran M, Falcone T, Goldberg J. Endometriosis: still tough to diag- nose and treat. Cleve Clin J Med 2002; 69:647–653. 2. Wenger JM, Soave I, Lo Monte G, Petignat P , Marci R. Tubal en- dometrioma within a twisted fallopian tube: a clinically complex diagnosis. J Pediatr Adolesc Gynecol 2013; 26:e1–e4. 3. Marci R, Lo Monte G, Soave I, Bianchi A, Patella A, Wenger JM. Rectus abdominis muscle endometriotic mass in a woman affected by multiple sclerosis. J Obstet Gynaecol Res 2013; 39:462–465. 4. Vercellini P , Frontino G, Pietropaolo G, Gattei U, Daguati R, Crosig- nani PG. Deep endometriosis: definition, pathogenesis, and clinical management. J Am Assoc Gynecol Laparosc 2004; 11:153–161. 5. Nezhat C, Santolaya J, Nezhat FR. Comparison of transvaginal sonography and bimanual pelvic examination in patients with lapa- roscopically confirmed endometriosis. J Am Assoc Gynecol Laparosc 1994; 1:127–130. 6. Barbieri RL, Niloff JM, Bast RC Jr, Scaetzl E, Kistner RW, Knapp RC. Elevated serum concentrations of CA-125 in patients with advanced endometriosis. Fertil Steril 1986; 45:630–634. 7. Bon GG, Kenemans P , Dekker JJ, et al. Fluctuations in CA 125 and CA 15-3 serum concentrations during spontaneous ovulatory cycles. Hum Reprod 1999; 14:566–570. 8. Mais V, Guerriero S, Ajossa S, Angiolucci M, Paoletti AM, Melis GB. The efficiency of transvaginal ultrasonography in the diagnosis of endometrioma. Fertil Steril 1993; 60:776–780. 9. Guerriero S, Mais V, Ajossa S, et al. The role of endovaginal ultra- sound in differentiating endometriomas from other ovarian cysts. Clin Exp Obstet Gynecol 1995; 22:20–22. FIGURE 4. Ovarian endometrioma on magnetic resonance imaging. (A) On a fat-saturation transverse T1-weighted image, the endometrioma has high signal intensity. (B) On transverse T2-weighted image, blood-degraded product content has intermediate to low signal intensity. FIGURE 5. Posterior deep infiltrating endometriotic nodule on magnetic resonance imaging. (A) On a T2- weighted image with no opacification of the vagina and rectum with ultrasonographic gel, a retrocervical endometriotic nodule (white oval) has a signal intensity very close to that of the surrounding fibromuscular anatomic structures such as the rectal wall (arrow), vagina, and cervical stroma (asterisk). (B) A T2- weighted image shows the endometriotic nodule (oval) extending downward to the vaginal fornix, which appears obliterated. Only the right vaginal fornix (asterisk) is distended. Between the nodule and the anterior rectal wall, interposing fat tissue (arrowhead) is likely to repre- sent a safety margin and a plane of dissection. * * 366 CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 81 • NUMBER 6 JUNE 2014 IMAGING IN ENDOMETRIOSIS 10. Fedele L, Bianchi S, Raffaelli R, Portuese A. Pre-operative assessment of bladder endometriosis. Hum Reprod 1997; 12:2519–2522. 11. Chamié LP , Blasbalg R, Pereira RM, Warmbrand G, Serafini PC. Find- ings of pelvic endometriosis at transvaginal US, MR imaging, and laparoscopy. Radiographics 2011; 31:E77–E100. 12. Fleischer AC. Transabdominal and transvaginal sonography of ovar- ian masses. Clin Obstet Gynecol 1991; 34:433–442. 13. Zawin M, McCarthy S, Scoutt L, Comite F. Endometriosis: appear- ance and detection at MR imaging. Radiology 1989; 171:693–696. 14. Togashi K, Nishimura K, Kimura I, et al. Endometrial cysts: diagnosis with MR imaging. Radiology 1991; 180:73–78. 15. Balleyguier C, Chapron C, Dubuisson JB, et al. Comparison of magnetic resonance imaging and transvaginal ultrasonography in diagnosing bladder endometriosis. J Am Assoc Gynecol Laparosc 2002; 9:15–23. 16. Siegelman ES, Oliver ER. MR imaging of endometriosis: ten imaging pearls. Radiographics 2012; 32:1675–1691. 17. Takeuchi M, Matsuzaki K, Kubo H, Nishitani H. Magnetic resonance manifestations of endometrial cysts at 3 T compared with 1.5 T. J Comput Assist Tomogr 2008; 32:369–271. 18. Zanardi R, Del Frate C, Zuiani C, Del Frate G, Bazzocchi M. Staging of pelvic endometriosis using magnetic resonance imaging compared with the laparoscopic classification of the American Fertility Society: a prospective study. Radiol Med 2003; 105:326–338. 19. Takahashi K, Okada M, Okada S, Kitao M, Imaoka I, Sugimura K. Studies on the detection of small endometrial implants by magnetic resonance imaging using a fat saturation technique. Gynecol Obstet Invest 1996; 41:203–206. 20. Loubeyre P , Copercini M, Frossard JL, Wenger JM, Petignat P. Pictori- al review: rectosigmoid endometriosis on MRI with gel opacification after rectosigmoid colon cleansing. Clin Imaging 2012; 36:295–300. 21. Bahr A, de Parades V, Gadonneix P , et al. Endorectal ultrasonogra- phy in predicting rectal wall infiltration in patients with deep pelvic endometriosis: a modern tool for an ancient disease. Dis Colon Rectum 2006; 49:869–875. 22. Biscaldi E, Ferrero S, Remorgida V, Rollandi GA. Bowel endometrio- sis: CT-enteroclysis. Abdom Imaging 2007; 32:441–450. ADDRESS: Roberto Marci, PhD, Department of Morphology, Surgery and Experimental Medicine, University of Ferrara, Corso Giovecca 183, 44100, Ferrara, Italy; e-mail: [email protected]

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endometriosis

MeSH descriptors

Endometriosis Endosonography Magnetic Resonance Imaging Adult Barium Sulfate CA-125 Antigen CA-125 Antigen Endometriosis Enema Female Humans Magnetic Resonance Imaging Multidetector Computed Tomography Multidetector Computed Tomography

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