Adnexal Torsion: Review of Radio- Logic Appearances

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WOMEN’S IMAGING - - - - - 609 ------rather rather adnexal torsion [email protected] Introduction (5). However, these terms are generally used However, (5). radiographics.rsna.org is defined as the twisting of an organ or part of an organ ovarian torsion RSNA, 2021 • RSNA, of the affected ovary. Hemorrhage internal and absence of or flow of the affected ovary. condi Pertinent infarction. of ovarian enhancement are suggestive are a rupturedtions to consider in the differential diagnosis hemor hyperstimula ovarian edema, ovarian massive rhagic cyst, ovarian leiomyoma. and a degenerating tion, this article. for Online supplemental material is available © abdomen, and the diagnosis is often made clinically with corrobora and the diagnosis abdomen, the symptoms of adnexal torsion can be variable However, US. tive an early diagnosis challenging making unless this and nonspecific, When adnexal torsion is not clini condition is clinically suspected. Imaging be performed. has an CT or MRI may cally suspected, important role in identifying adnexal torsion de and accelerating particularlynot in cases in which the diagnosis is treatment, finitive imaging are characteristic features Several an early consideration. of adnexal torsion can be seen to varying and degrees across differ ovary migrated edematous to the midline; a massive, ent modalities: peripherally follicles resembling a string displaced ovarian of pearls; surrounding inflam mass; lesion acting as a lead a benign ovarian and the uterus the side matory pulled toward fluid; change or free Adnexal torsion is the twisting of the ovary, and often of the fal and often Adnexal torsionthe ovary, is the twisting of com resulting in vascular supports, on its ligamental lopian tube, is management definitive The infarction. promise and ovarian diagnosis facilitates and prompt surgical preservation detorsion, which is particularly importantthis condi because of the ovary, The majority affects premenopausal women. tion predominantly and a surgical vomiting, pain, acute present with severe of patients diagnostic challenge. To avoid ovarian infarction ovarian and the possibility avoid To diagnostic challenge. early detection is critical. subfertility, of associated Torsion of the adnexa is a gynecologic emer- Torsion axis (1). along its own 2%–3% of females who present gency affects approximately that Both the ovary and the fallopian tube with acute pelvic pain (2–4). the preferred term hence, typically are involved; than ovaryThe and fallopian tube interchangeably in clinical practice. causing interrupted and ligamental supports, twist on their vascular conges- and lymphatic is initially due to venous perfusion that Less tion and subsequently caused by compromise to arterial flow. torsion of the fallopian or torsion tube in isolation of commonly, Despite cysts or paraovarian) also can occur. (paratubal extraovarian adnexal torsion is an important uncommon, cause being relatively to be a can prove and its nonspecific manifestations of morbidity,

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M.T.D. (e- M.T.D.

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LEARNING OBJECTIVES Stewart, BMedSci, BMBS, BMBS, BMedSci, Stewart, Rockall, MBBS, MRCP, MRCP, MBBS, Rockall, Adnexal Torsion: Review of Review Adnexal Radio Torsion: Appearances logic

Sudderuddin, BSc, MBBS, MBBS, BSc, Sudderuddin, Naik, BSc, MBBS, MRCP, MRCP, MBBS, BSc, Naik, Bharwani, BSc, MBBS, MRCP, MRCP, MBBS, BSc, Bharwani, See rsna.org/learning-center-rg. Address correspondence to [email protected] activity, participants will be able to: FRCR FRCR MRCP, FRCR FRCR MRCP, MRCP, FRCR MRCP, FRCR Discuss important differential diag- Summarize the typical clinical manifes- List the imaging of adnexal features

RSNA, 2021 RSNA, SA-CME After completing this journal-based SA-CME the author A.G.R. has provided disclosures (see disclosures has provided A.G.R. the author and the editor, all other authors, end of article); relation disclosed no relevant the reviewers have ships. mail: Trust, Praed Street, London W2 1NY, England W2 1NY, London Praed Street, Trust, V.R.S.); A.G.R., S.A.S., N.B., M.N., (M.T.D., Department of Surgeryand Division of Cancer, London, Imperial London, College and Cancer, Presented as an educa A.G.R.). England (N.B., Annual Meeting. the 2019 RSNA tion exhibit at revision requested June 2020; 11, May Received accepted Septem 9; September 25 and received this journal-based SA-CME activity, For ber 21. From the Department of Radiology, St Mary’s From the Department of Radiology, Imperial Healthcare NHS College Hospital, noses based on imaging appearances to potential misinterpretations. avoid tation of adnexal torsion.tation and MRI. CT, torsion US, seen at © RadioGraphics 2021; 41:609–624 RadioGraphics 2021; https://doi.org/10.1148/rg.2021200118 Content Codes: Siham A. G. Andrea R. Victoria M. Taufiq Dawood, BSc, MBBS, MBBS, BSc, Dawood, Taufiq M. Mitesh Nishat 610 March-April 2021 radiographics.rsna.org

TEACHING POINTS The massively enlarged ovary is often too big to be contained within the pelvis and thus migrates superiorly and toward the midline, usually lying in front of the uterus. This adnexal movement pulls the uterus out of its usual position and toward the side of the affected ovary. The altered position and relationship of the ovary and uterus are highly suggestive of adnexal torsion. Ovarian enlargement increases the tendency of the ovary to twist on its ligaments, and the presence of a benign ovarian Figure 1. Schematic diagram of the ovaries (Ov) and uterus lesion is the single greatest risk factor for adnexal torsion. (U). The left side of the image shows the normal relationships Nausea and vomiting occur in 70% of patients with adnexal among the structures attached to the ovary: suspensory liga- torsion; this is higher than the frequency with which these ment of the ovary (1), which contains the ovarian artery and symptoms manifest with other gynecologic causes of pelvic vein; broad ligament (2); ovarian ligament (3); and fallopian pain. When these symptoms are present, torsion should al- tube (4). The right side of the image shows how these relation- ways be considered as a likely diagnosis. ships change in the setting of adnexal torsion, with the twisted Although the findings of abnormal or reduced ovarian blood pedicle (arrow) consisting of the suspensory ligament and fallopian tube and resulting in a congested enlarged ovary. flow are sensitive for torsion, it is important not to be falsely reassured by normal vascularity, as arterial perfusion can be maintained until relatively late in the course of torsion. (also known as the infundibulopelvic ligament), The pedicle twist appreciated at US and MRI can be difficult to visualize on CT images. Rather, the thickened vascular pedicle which contains the ovarian artery and vein. can appear as elongated or triangular enhancing soft tissue Finally, the fallopian tube drapes over the broad at the anterolateral margin of the uterus, between the uterus ligament, attaching the ovary to the lateral wall and involved ovary. of the uterine fundus. The ovaries and fallopian tubes receive a dual blood supply from the ovarian and uterine arteries (7). The majority of patients present with severe In adnexal torsion, the ovary rotates on its axis acute pain, vomiting, and a surgical abdomen (ie, to cause a twist in the suspensory ligament that an acute intra-abdominal condition that requires contains the vascular pedicle (Fig 2, Movie 1). surgery). The diagnosis of adnexal torsion is often While adnexal torsion involves both the ovary made clinically with corroborative US. However, and the fallopian tube in up to 67% of cases because the symptoms are nonspecific, making an (8,9), isolated ovarian torsion also can occur, early diagnosis of adnexal torsion can be challeng- with sparing of the fallopian tube. However, ing unless the condition is clinically suspected. cases of isolated ovarian torsion are rare owing Imaging has a fundamental role in early identifica- to the wide attachment between the ovary and tion, particularly given its routine use in the acute the broad ligament (10). In practice, these two setting to triage patients with abdominopelvic pathologic entities are very challenging to distin- pain. Imaging features that support a diagnosis of guish with imaging alone, as both of them cause adnexal torsion must be correctly interpreted to a twisted vascular pedicle and secondary changes enable expeditious patient management. in the adjacent ovary. Isolated fallopian tube tor- In this article, we review the pathophysiology sion also has been described, with similar features of adnexal torsion, making reference to prin- of an adnexal twist but sparing of changes in the cipal anatomic features. We define the clinical ovary itself (11). manifestations of this pathologic entity, discuss The twist in the ovarian suspensory ligament the relative merits of different imaging modali- causes compression of the relatively low-pres- ties in the diagnosis, and review typical imaging sure ovarian vein and lymphatics, which become features. In addition, we highlight key differen- engorged, with massive enlargement of the ovary tial diagnoses to be considered during image and vascular pedicle. During this early period of interpretation and associated pitfalls that may ovarian expansion, the arterial supply is pre- cause confusion. served because arterial pressures are higher than venolymphatic pressures and owing to a more Anatomy and Pathophysiology muscular arterial vessel wall. Changes are re- In a premenopausal woman, the normal ovary versible during this time, and the ovary remains can measure up to 20 cm3 (6) and is held in place potentially salvageable. If left uncorrected, the by a series of ligamental supports (Fig 1). The arterial supply to the ovary can become compro- ovarian ligament attaches the ovary to the uterus. mised owing to marked luminal narrowing that The broad ligament, a broad-based peritoneal causes ischemia and subsequent infarction (10). fold, attaches the uterus to the pelvic sidewall The severity of vascular impairment depends on and encases the suspensory ligament of the ovary the degree of rotation of the adnexum about its RG • Volume 41 Number 2 Dawood et al 611

Figure 2. Adnexal torsion in a 41-year-old woman who presented with right-sided loin pain. (a) Focused transvaginal US image depicts an enlarged right ovary (RO) measuring 7 cm in length, with increased central echogenicity and normal follicles (arrowhead) within. (b) US image shows a whirlpool (curved arrow) with twisted hypoechoic vessels, which was confirmed as being continuous with the ovary and uterus at dynamic US assessment (see Movie 1). Find- ings of subsequent MRI (not shown), ordered because the medical history was not believed to be convincing for torsion, confirmed a twisted pedicle.

Figure 3. Adnexal torsion and associated hemorrhage in a 36-year-old woman who presented with severe abdominal pain and vomiting. (a) Axial contrast-enhanced CT image shows a right adnexal mass (solid arrow) with intrinsic high attenuation, adnexal soft tissue (dashed arrow), and surrounding free fluid *( ). (b, c) Axial (b) and coronal (c) T2-weighted MR images show an enlarged right ovary (arrowhead in b) and a twisted thickened pedicle (arrow in c), consistent with adnexal torsion. (d) Axial T1-weighted fat-saturated MR image shows high signal intensity (arrow) at the periphery of the right ovary, corresponding to the high attenuation seen in a, in keeping with hemorrhage and suggestive of ovarian infarction. There is a well-defined cyst in the ovary, which is likely to have predisposed it to torsion. axis (12) and whether there is some preservation rhagic infarction occurs within the ovary (Fig of arterial flow to the ovary from its dual supply. 3). The presence of hemorrhage is predictive of As the arterial supply is compromised, hemor- ovarian nonviability and necrosis (13,14). 612 March-April 2021 radiographics.rsna.org

Figure 4. Adnexal torsion of a benign ovarian cyst, with a migrated ovary and pulled uterus, in a 52-year-old woman. (a) Coronal contrast-enhanced CT image shows an adnexal mass that has a large cystic component (solid arrow) and has “flipped” superiorly to the uterus at the midline. Note the intrauterine contraceptive device. There is free fluid (dashed arrow) adjacent to the mass.(b) Axial T2-weighted MR image shows an unusual and complex right ovarian mass (arrowhead) with a large cystic component and a smooth internally thickened wall. (c) Coronal T2-weighted MR image shows a twisted thickened pedicle (curved arrow) and the uterus (U) pulled to the right. Despite the complex imaging appearances, histopathologic analysis confirmed the presence of a hemorrhagic necrotic benign cyst. This case illustrates how benign masses can have altered and unusual appearances in torsion.

The massively enlarged ovary is often too fat and/or hyperattenuating calcification may be big to be contained within the pelvis and thus seen, and the characteristic presence of fat can migrates superiorly and toward the midline, be confirmed at MRI by using fat-suppression usually lying in front of the uterus. This adnexal or chemical shift techniques (23). movement pulls the uterus out of its usual posi- Ovulation induction for infertility stimu- tion and toward the side of the affected ovary lates the production of multiple follicular cysts, (Fig 4). The altered position and relationship resulting in ovarian enlargement and increased of the ovary and uterus are highly suggestive susceptibility for torsion (24). Additional risk of adnexal torsion (15,16) and can be helpful factors include pregnancy, particularly in the in differentiating torsion from other adnexal first trimester when corpus luteum cysts may or ovarian conditions, which are more likely to develop (25), and prior pelvic surgery (26) (Fig push the uterus posteriorly or toward the con- 6). Adhesions related to malignant lesions and tralateral side owing to mass effect. endometriosis are believed to be protective (27). Specific risk factors for isolated fallopian tube Risk Factors torsion include pelvic inflammatory disease, Ovarian enlargement increases the tendency tubal ligation, and other specific tubal surgical of the ovary to twist on its ligaments, and procedures (28). the presence of a benign ovarian lesion is the Although adnexal torsion is most prevalent in single greatest risk factor for adnexal torsion women of childbearing age (3), it can also arise (3). Masses greater than 5 cm in diameter are in premenarchal and postmenopausal patients. believed to be associated with a particularly In premenarchal patients who are diagnosed increased risk for adnexal torsion (17,18), with adnexal torsion, the underlying patho- although masses of any size are susceptible. genic process may be related to elongation of Benign lesions more commonly undergo tor- the utero-ovarian ligaments (29), and the ovary sion and are present in more than 80% of cases itself is more likely to be normal compared with (Fig 5) (18). Simple ovarian cysts are most the ovaries in older women (30). In postmeno- frequently involved and have a typical US ap- pausal women, torsion is more commonly as- pearance of a thin-walled hypoechoic mass with sociated with a malignant mass, but this occurs no internal vascularity (19). On CT and MR in a relative minority of patients, reportedly in images, these cysts have uncomplicated fluid at- 9% of postmenopausal women (compared with tenuation and signal intensity, respectively. 0.4% of premenopausal women) diagnosed with The other commonly involved lesions are torsion in a single-center study (31). mature cystic teratomas. At US, these lesions contain hyperechoic sebaceous or fatty material Clinical Examination and with discrete, markedly hyperechoic regions of Manifestations calcification identified owing to the presence of The clinical manifestation of adnexal torsion can posterior acoustic shadowing (9,20–23). Cor- be variable, with commonly described symptoms responding CT appearances of hypoattenuating that include nausea, vomiting, and acute lower RG • Volume 41 Number 2 Dawood et al 613

Figure 5. Adnexal torsion of a right ovarian cyst acting as a lead mass in a 60-year-old woman who presented with acute lower abdominal pain and vomiting. (a) Axial contrast-enhanced CT image shows a cystic pelvic mass (solid arrow) with a smooth wall, and a triangle of adnexal soft tissue (dashed arrow). (b) Axial contrast-enhanced CT image shows the uterus (U) pulled to the right and a normal left ovary (arrow). A complex large mass and free fluid *( ) should not deter the reader from considering torsion. (c) Sagittal T2-weighted MR image shows ovarian tissue (arrowhead) stretched around a benign-appearing thin-walled cyst with no wall irregularity. (d) Axial T2-weighted MR image shows that the adnexal soft tissue seen in a corresponds to a twisted pedicle (dashed arrow). Surgery revealed a torsed benign simple ovarian cyst.

Figure 6. Adnexal torsion in a 29-year-old woman with a history of hysterectomy for cervical cancer who presented acutely with right-sided abdominal pain and vomiting. (a) Axial noncontrast CT image shows a right iliac fossa mass (arrow) and surrounding free fluid (arrowhead).(b) Sagittal T2-weighted MR image shows typical features of adnexal torsion: an enlarged ovary with peripherally placed follicles, edema (*), and pelvic free fluid (arrowhead).(c) Sagittal T2-weighted MR image shows a pedicular twist (arrow). Successful surgical detorsion was performed, and the ovary was preserved. abdominal pain (Table 1) (17,32–35). Nausea symptoms are present, torsion should always and vomiting occur in 70% of patients with be considered as a likely diagnosis. Pain can be adnexal torsion; this is higher than the frequency intermittent as a result of episodic twisting and with which these symptoms manifest with other untwisting, and alteration in the tension placed gynecologic causes of pelvic pain. When these on the supporting structures (5). Less common 614 March-April 2021 radiographics.rsna.org

Table 1: Clinical Signs and Symptoms in Patients with Confirmed Adnexal Torsion

Symptom or Sign Occurrence Rate (%) Reference Numbers Acute pain 44–97 17,20,30,32–34 Nausea and/or vomiting 59–70 17,20,26,30,32,34 Fever 2–20 17,20,30,32,34 Palpable abdominal mass 20–47 17,20,34,35

Figure 7. Diagram illustrates an algorithmic approach to appropriate radiologic examinations in women who present to the emer- gency department with abdominopelvic pain and nausea. manifestations include fever and a palpable ab- Acute appendicitis is also a differential, along dominal mass. Owing to these nonspecific mani- with other nongynecologic causes of pain such festations, the diagnosis of adnexal torsion can be as enterocolitis, diverticulitis, inflammatory difficult, delaying appropriate management and bowel disease, urolithiasis, and urinary tract increasing the likelihood of irreversible ischemia infection. and necrosis (36). A pregnancy test is crucial for excluding Imaging Features ectopic pregnancy (37); otherwise, laboratory Imaging has an important role in the diagnosis of tests are of limited value. Elevated inflammatory adnexal torsion. An approach to guide appropri- markers or leukocytosis may be present, even in ate imaging examinations is outlined in Figure the absence of a fever (3,34). 7. Key imaging features are common across There is a wide differential for acute ab- imaging modalities and include massive ovar- dominopelvic pain, with gynecologic causes that ian enlargement, abnormal displacement of the include hemorrhagic or ruptured ovarian cysts, involved ovary superiorly into the midline and of ectopic pregnancy, endometriosis with acute the uterus toward the affected side, and a thick- hemorrhage or rupture, leiomyoma degeneration ened twisted pedicle. Additional features are a or torsion, infection, and pelvic inflammatory benign lead mass and acute inflammatory change disease. In adnexal torsion, the right ovary is within or around the adnexa. The relative rates involved more frequently than the left, probably of these findings across imaging modalities and owing to the increased mobility of the ileum and their correlations to viability or nonviability of the cecum compared to that of the rectosigmoid, involved ovary and fallopian tube are summarized which may help to anchor the left adnexa (38). in Table 2. RG • Volume 41 Number 2 Dawood et al 615

Table 2: Imaging Features of Adnexal Torsion and Nonviability in Confirmed Cases of Adnexal Torsion

Reference General Features* Features Suggesting Nonviability* Numbers US Ovary: Ovary: absent central vascularity (100%) 4, 9,20–22,39 Enlarged (53%–85%) Increased central echogenicity (40%–85%) Peripheral small follicles (string of pearls) (12%–38%) Benign lead mass (40%–65%) Tube and pedicle: … 4, 9,20,21,39 Twisted pedicle whirlpool (79%) Abnormal blood flow (35%–85%) Peritoneum: free fluid (20%–72%) … 20–22,39 CT Ovary: Ovary: 15,21,40–42 Enlarged; may be midline (87%–100%) Lead mass with eccentric or irregular wall Benign lead mass with smooth regular wall thickening thickening (52%–93%) High-attenuating hemorrhagic foci Absent enhancement Tube and pedicle: 15,21,40–43 Twisted pedicle whirlpool (31%–100%) Pedicle soft-tissue thickening (17%–97%) Uterus: pulled to involved side (36%–68%) … 14,15,21, 40–43 Peritoneum: surrounding fat stranding and/ Peritoneum: hemoperitoneum, rather than 4,14,15,21, or small volume of free fluid (40%–73%) simple fluid, in the context of adnexal torsion 40–42 suggests ovarian infarction MRI Ovary: Ovary: 13,44–47 Enlarged; may be midline (100%) Lead mass with eccentric or irregular wall Increased central signal intensity at T2W thickening (>10 mm) (50%) imaging (32%–86%) Stromal hemorrhage (high signal intensity at Peripheral high T2W follicles (string of T1W and T1W FS imaging, intermedi- pearls) (27%–86%) ate or low signal intensity at T2W imaging) Benign-appearing lead mass with smooth (66%–91%) wall thickening (27%–70%) Absent enhancement (17%) Tube and pedicle: … 13,44,45 Twisted pedicle whirlpool (14%–70%) Pedicle soft-tissue thickening (59%) Uterus: pulled to involved side (41%–70%) … 13,45 Peritoneum: surrounding fat stranding and/ Peritoneum: hemoperitoneum, rather than 13,44,45 or small volume of free fluid (40%–71%) simple fluid, in the context of adnexal torsion suggests ovarian infarction Note.—FS = fat saturated, T1W = T1 weighted, T2W = T2 weighted. *Numbers in parentheses are percentage rates at which the feature is seen at the given imaging examination.

US Assessment ing to perform in patients with significant pain. US should be the first-line examination when Despite these challenges, in a systematic review torsion is suspected, particularly in premeno- of 663 cases of adnexal torsion (20), the overall pausal women, owing to the lack of ionizing diagnostic accuracy of US was 79%, compared radiation and the widespread availability (48). with 42% for CT. Transabdominal and transvaginal US scanning The primary and sometimes only US finding of provide excellent dynamic imaging of the ovaries, adnexal torsion is a massively enlarged ovary, typi- uterus, and associated anatomy, whereas Doppler cally at the midline (9,22). Central ovarian edema US enables real-time assessment of vascularity. appears as a hypoechoic heterogeneous central US is operator dependent and can be challeng- medulla and is present in up to 79% of cases (39) 616 March-April 2021 radiographics.rsna.org

Figure 8. Left adnexal torsion with massive ovarian enlargement in a 20-year-old woman who presented with acute pelvic pain. (a) Transabdominal US image shows a large heterogeneously echogenic pelvic mass (between calipers) that contains an anechoic cyst (C). These findings were believed to represent a benign ovarian mass, and MRI was performed.(b) Axial T2-weighted MR image shows a massive centrally migrated left ovary with peripherally placed high-signal-intensity follicles, creating a “string of pearls” appearance (arrowheads). Note the ill-defined central edema *( ). (c) Coronal T2-weighted MR image shows the uterus to be pulled (curved arrow) toward the side of the affected left ovary by a thickened pedicle (dashed arrow). A benign left ovarian cyst (C), which probably acted as a lead mass, and a normal-sized right ovary (solid straight arrow) also are seen.

Figure 9. Adnexal torsion in a 32-year-old woman who presented with right-sided abdominal pain and nausea. (a) Trans- vaginal US image shows an enlarged ovary measuring 6.39 cm (between calipers), with central edema (*) and peripheral hypoechoic follicles (arrowheads) consistent with torsion. (b) Color Doppler US image shows globally preserved blood flow consistent with a viable ovary. Surgical detorsion was performed, and the ovary was preserved. (Case courtesy of Joseph Yaz- bek, MD, MRCOG, London, England.)

(Fig 8). Intervening regions of increased echo- a color Doppler signal) or “target” (concentric genicity may indicate hemorrhagic infarction (49). alternating hypo- and hyperechoic rings) sign if it The follicle-containing cortex becomes stretched is visualized perpendicular to the rotational axis around the periphery of the medulla, creating a (Figs 2, 10). Although this sign is present in more thin layer of follicles that resembles a string of than 90% of confirmed cases of adnexal torsion pearls, which is visible as multiple hypoechoic (39), it can be subtle, depending on the number avascular cystic structures (Fig 9) (39). An addi- of twists and structures involved (51). tional sonographic finding is that of a hyperechoic Isolated fallopian tube torsion is rare, but rim surrounding peripherally displaced antral fol- its typical reported US appearance is that of a licles, known as the “follicular ring” sign, with the dilated tube with thickened echogenic walls. The rim measuring 1–2 mm in thickness (50). This is dilated tube can be found medial to a normal seen with greater clarity at transvaginal US. ipsilateral ovary, tapering toward either end in a A twisted vascular pedicle, which includes configuration known as the “beak” sign (11,52). the ligamental support and often the fallopian Doppler US can be used to assess the vas- tube, manifests as a thickened tubular structure cularity of the ovary, although the findings of adjacent to the uterus. US facilitates dynamic adnexal torsion are variable and the utility of assessment in multiple planes to identify this this modality in this setting is controversial. finding as the characteristic “whirlpool” (twist- Although the findings of abnormal or reduced ing of the hypoechoic vessels with or without ovarian blood flow are sensitive for torsion (4), it RG • Volume 41 Number 2 Dawood et al 617

Figure 10. Right ovarian torsion in a 36-year-old woman who presented with acute lower abdominal pain and vomiting. (a) Transvaginal US image shows an asymmetrically enlarged right ovary measuring 9.4 cm, with peripheral follicles (arrowheads) and an echogenic medulla (*). (b) Doppler US image of the right ovary shows two avascular cystic lesions: a simple cyst (C) and a more complex cyst (arrow) with layered hyperechogenic components and interposed low-level (ground-glass) echoes, consistent with a hemorrhagic cyst. (c) Sagittal T2-weighted MR image shows an enlarged right ovary with peripheral follicles (arrowheads), central edema (*), and a thickened edematous right pedicle (arrow). (d) Coronal T2-weighted MR image shows the characteristic whirlpool sign of a twisted right pedicle (arrow), which with multiplanar sequences appears as an edematous heterogeneous tubelike structure that lies between and connects the uterus and ovary (see Movie 2). A multicystic left ovary (LO) also is seen. (e) Axial T2-weighted MR image shows a heterogeneous cystic lesion (arrow) with partially low signal intensity. (f) Axial T1-weighted fat-saturated MR image shows high signal intensity in the lesion in e, confirming the presence of a hemorrhagic cyst (solid arrow), which probably acted as a lead mass.

is important not to be falsely reassured by normal of 47 positive cases (4) showed that, together vascularity, as arterial perfusion can be main- with ovarian enlargement, free fluid is a sensitive tained until relatively late in the course of tor- sign for torsion. However, is it not specific and sion (Fig 9) (53–55). A venous flow abnormality, therefore needs to be correlated with clinical and defined as a noncontinuous flow pattern, can be other US findings. present in up to 100% of cases (54). Abnormal or absent venous flow occurs earlier than does an CT Assessment arterial flow abnormality and could suggest im- Although CT is not indicated when torsion is pending or early torsion. Arterial flow can show suspected, it is often performed in women who high impedance before becoming absent (56), the present with nonspecific abdominal pain and caveat being that there can be cyclical variability vomiting. The radiologist may be the first mem- in arterial flow owing to the menstrual cycle (57). ber of the team to suspect adnexal torsion if Similar findings were described in a case series of ancillary features are present in the setting of an 13 patients (53), in which surgical findings were adnexal mass. Because uncomplicated adnexal compared with the results of Doppler US assess- masses rarely cause acute pain, the diagnosis of ment of viability. In that study, central venous adnexal torsion should be suggested to aid early flow was present in surgically confirmed viable detection, as it is unlikely that the clinicians ovaries but absent in most nonviable ovaries (53). suspect torsion if CT has been performed. Ow- Some of the nonviable ovaries did have sustained ing to the lack of anatomic definition of adnexal peripheral arterial flow, which may have been the structures, diagnosing adnexal torsion with CT result of the dual arterial supply and relative pres- can be difficult (21), particularly if the presenta- ervation of flow within the uterine artery. tion is subacute; the accuracy rate can be as low While the presence of pelvic free fluid is seen as 42% (20). Normal CT results have a high in a variety of abdominopelvic diseases, a study negative predictive value, especially when both 618 March-April 2021 radiographics.rsna.org

Figure 11. Left ovarian necrosis following adnexal torsion of a benign spindle cell tumor in a 61-year-old woman with left iliac fossa pain. (a) Axial contrast-enhanced CT image shows a triangular mass of soft tissue (dashed outline) adjacent to the enlarged left ovary (arrow). (b) Axial T2-weighted MR image shows increased signal intensity within the soft tissue (arrow), consistent with edema. (c) Coronal T2- weighted MR image findings clarify the structure of the soft tissue, convincingly demonstrating the presence of a twisted thickened pedicle (dashed arrow). Also note the surrounding free fluid *( ) and the uterus (curved arrow) pulled toward the side of torsion. (d) Sagittal T2-weighted MR image findings confirm the presence of a benign-appearing right ovarian mass (solid arrow) acting as a lead mass, with the twisted pedicle (dashed arrow) again seen.

ovaries are visualized (58); however, adnexal frequently than the triangle of soft tissue or the torsion with no positive imaging findings has twist itself. It is usually not possible to distinguish been reported (4). the vascular structures from the fallopian tube With adnexal torsion, the primary abnormality involved in torsion. seen at CT is a large pelvic mass that is typically Because contrast-enhanced abdominal CT is superior to the uterus at the midline; this finding generally performed in the acute setting without is present in almost all cases (15). Multiplanar noncontrast image acquisition, internal hemor- reconstruction is particularly helpful for assess- rhage can be mistaken for enhancing soft tissue ing the relative positions of the ovary and uterus, and lead to a false-positive diagnosis of malig- with the uterus typically pulled toward the side of nancy (Fig 12). In addition, the appearance of torsion (15). A study of 52 adnexal torsion cases an underlying benign ovarian lesion may change (40) showed that the addition of coronal recon- following torsion. The inflammatory changes can structions to standard axial images significantly erroneously be attributed to a “malignant” process increased the sensitivity of CT for diagnosing rather than acute changes within a benign lesion adnexal torsion, from 28% to 79%. (Fig 4). When a cyst acts as a lead mass, smooth The pedicle twist appreciated at US and concentric cyst wall thickening is suggestive of MRI can be difficult to visualize on CT images simple edema, while eccentric or irregular thicken- (16,41). Rather, the thickened vascular pedicle ing may indicate hemorrhagic infarction (14,46). can appear as elongated or triangular enhanc- Peritoneal changes are nonspecific (5,21). ing soft tissue at the anterolateral margin of the Free fluid and inflammatory stranding of the uterus, between the uterus and involved ovary surrounding fat can be present, particularly if (Fig 11) (40). This appearance can be over- the torsion is chronic, and should not be misin- looked and mistaken for enhancing tissue that is terpreted as peritoneal disease associated with part of an adnexal mass. malignancy (Fig 13). Such misinterpretation can The described engorgement of the ovarian lead to delayed treatment for salvaging the ovary. artery and vein can sometimes be observed as contrast material–opacified serpiginous distended MRI Assessment vessels on contrast-enhanced CT images (59). MRI is reserved for problem solving in complex However, these engorged vessels are seen less gynecologic cases because of the capability to dif- RG • Volume 41 Number 2 Dawood et al 619

Figure 12. Adnexal torsion in a 56-year-old woman who presented with lower abdominal pain. (a) Axial contrast-enhanced CT image shows a large complex septated mass (arrow), with areas of high attenuation (arrowhead) that were believed to be enhancing soft tissue. MRI was performed to characterize the mass, given its complex appearance. (b) Axial T2-weighted MR image shows a septated cystic right ovarian mass (solid arrow) with a pedicle twist (dashed arrow). (c) Axial T1-weighted fat-saturated MR image shows the mass with intrinsic high signal intensity (arrowhead) consistent with hemorrhage. (d) Axial T1-weighted contrast-enhanced subtraction MR image shows a complete absence of enhancement (arrow) within the mass. All of these findings are suggestive of torsion. Histologic findings confirmed the presence of a torsed benign mucinous cystadenoma. This case illustrates why MRI is sometimes needed to problem solve, as the appearances of torsion, especially those seen at CT, can mimic malignancy.

Figure 13. Torsed infarcted benign right ovarian cyst, with surrounding peritoneal inflammation, in a 50-year-old woman who presented with acute abdominal pain. (a) Axial T2-weighted MR image shows a cystic right ovarian mass (RO), which appears simple, smooth walled, and with edematous ovarian stroma (*) stretched around it. (b) Axial T1-weighted MR image shows a rim of increased T1 signal intensity (arrowhead) consistent with hemorrhage, and surrounding fat stranding (arrow). In comparison, a partially imaged simple left-sided ovarian cyst (LO) has no surrounding fat stranding or cyst wall thickening. (c) Sagittal T2-weighted MR image better depicts a twisted right pedicle (arrow) and pelvic free fluid(FF). ferentiate viscera and tissue types. MRI is often been misdiagnosed as a complex adnexal mass unavailable in the acute setting and is primarily with other imaging modalities. used in atypical cases to clarify equivocal findings As with other modalities, with MRI, peripher- seen with other modalities, aid anatomic local- ally displaced follicles appearing as the string of ization (13,48), and/or characterize lead masses pearls sign are often present (60). The central if there is concern for malignancy. MRI may be medulla of the enlarged edematous ovary yields used to diagnose unexpected torsion in cases in high signal intensity at T2-weighted MR imaging. which intermittent pain has resolved as a result Hemorrhage may be visible as areas of of spontaneous detorsion or ovarian torsion has increased signal intensity on T1-weighted MR 620 March-April 2021 radiographics.rsna.org

Figure 14. Ruptured hemorrhagic ovarian cyst in a 57-year-old woman who presented with lower abdominal pain and vomiting. (a) Axial contrast-enhanced CT image shows a pelvic mass with high attenuation along its lateral aspect (arrow). The uterus (U) is pushed to the right. (b) Transvaginal US image shows an avascular left ovarian cyst with increased dependent echogenicity (arrow) and layered content, correlating with the high signal intensity seen in a and consistent with blood products. There are no ancillary features of torsion. (c) Axial T2-weighted MR image obtained 6 weeks later shows that the left ovarian mass has decreased in size since the images in a and b were obtained. The T2 shading (arrowhead) is in keeping with hemorrhage, which was confirmed with other MRI sequences (not shown). There is no adnexal soft tissue or pedicle twist. U = uterus. images. Hemorrhage into the ovary can be very ovarian infarction. Overall salvage rates are low restricted at diffusion-weighted imaging and owing to diagnostic uncertainty (62), but they could be mistaken for malignant tissue. There- can be improved by reducing the time between fore, it is important to correlate regions of re- presentation and surgery (36). Laparoscopic stricted diffusion on T1-weighted and contrast- exploration can be used to assess the viability of enhanced MR images. the ovary and remaining adnexa to guide defini- Absence of enhancement is strongly suspicious tive management. for ischemia, necrosis, and nonviability of the Conventional surgical management involves ovary (53). This feature is more easily discernible intraoperative assessment of the color and fri- at MRI, where subtraction imaging is often in- ability of the ovary to determine whether it valuable, especially if internal hemorrhage is seen should be detorsed or excised. It is accepted that on noncontrast images (Fig 11) (47). nonviability is overestimated at surgical assess- The edematous twisted pedicle is readily ment, particularly in children (63). Severe isch- visible on MR images as a swirling heteroge- emia and necrosis can be suspected on the basis neous structure with increased T2 signal inten- of a dark or dusky ovary, but even then, some sity extending from the uterus to the centrally ovaries may reperfuse following detorsion, which migrated enlarged ovary (Movie 2). Even subtle is therefore performed in all cases, irrespec- twists can be appreciated on MR images, given tive of the patient’s age, before oophorectomy the superior spatial resolution. The whirlpool is considered (64). In addition to detorsion, sign at MRI has been found to be a key feature, additional management is dependent on other reported in up to 69% of cases (13). The rela- findings identified at surgery (26). In a pre- tive positions of the uterus and ovary are again menopausal woman, cystectomy or resection is relevant, with displacement of the uterus toward performed if a benign lesion is present. If there the side of the abnormality (61). is suspicion for malignancy or definite necrosis, MRI is superior for the characterization of salpingo-oophorectomy is performed instead adnexal masses associated with torsion. However, (65). In postmenopausal women, salpingo-oo- if necrosis is present and the torsion is chronic, the phorectomy may be offered routinely because of appearance of a mass may become more complex, the risk of recurrent torsion, and malignancy is a and it may not be possible to definitively exclude greater consideration (26). malignancy. As described with US and CT, signs of peritoneal inflammation and free fluid often Differential Diagnoses coexist at MRI in cases of torsion and should not The pertinent differential diagnoses of adnexal deter the radiologist from making the diagnosis. torsion are briefly reviewed in the following sec- tions. It is worth emphasizing that the clinical Management of Adnexal Torsion history is vital when considering these differential Adnexal torsion is managed surgically, and diagnoses. With adnexal torsion, there is almost prompt decision making is required to avoid certainly an acute history. RG • Volume 41 Number 2 Dawood et al 621

Figure 15. Massive ovarian edema in a 46-year-old woman with bilateral Krukenberg tumors from metastatic signet ring cancer of the stomach. (a) Axial contrast-enhanced CT image obtained at the time of the initial cancer diagnosis shows bilateral ovarian me- tastases (arrows) with solid enhancing tissue and smaller cystic components, which were the only sites of disease. Two months later the patient presented with worsening pelvic pain. (b) Sagittal T2-weighted MR image shows a markedly edematous right ovary (arrow) that has rapidly increased in size. (c) Axial contrast-enhanced T1-weighted fat-saturated MR image shows an absence of central enhancement (*) in this ovary, confirming that the expansion is secondary to edema rather than tumor growth. Avid enhancement (arrowhead) is preserved in the smaller solid left ovarian tumor.

Ruptured Hemorrhagic Cyst ian lesion within a nontorsed ovary. The clinical A ruptured hemorrhagic ovarian cyst or corpus presentation can also be helpful. Adnexal torsion luteum is the most likely differential diagnosis causes intermittent severe pain, and vomiting can to mirror the clinical manifestation of torsion, be severe. Meanwhile, the pain from cyst rupture with sudden-onset lower abdominal pain. As and/or hemorrhage is often maximal at symptom the manifestation of this hemorrhaging is acute, onset and can wane thereafter, with vomiting a the first-line modality is likely to be US or less marked feature (66). contrast-enhanced CT, either of which depicts an adnexal mass and surrounding inflammatory Massive Ovarian Edema change (Fig 14) (66). Very rarely, particularly following menarche, tor- The hemorrhagic component can be visual- sion and spontaneous detorsion can occur before ized at US as internal complexity or dependent ischemia develops (70,71). This condition can low-level echoes (ground-glass appearance) that manifest more indolently, but there is a risk of later organize into a lacy fibrinous web (67). further episodic torsion and detorsion, which can These echoes are distinguishable from true septa cause tumor-like edematous enlargement of the owing to their thin morphology, absence of flow ovary, referred to as massive ovarian edema. The at color Doppler US, and incomplete extension appearances of the ovary are similar to those of across the cyst (19). A solid heterogeneous avas- adnexal torsion, but there is no pedicle twist or cular mass with concave outer margins within adnexal soft tissue. the cyst indicates the development of a retracted While most cases of massive ovarian edema clot, which can change shape when pressure is are caused by intermittent torsion and associated applied with the probe. A fluid-fluid or fluid- venolymphatic obstruction, a small proportion debris level also may be present. Adjacent hyper- of cases in older women are caused by lymphatic echoic free fluid containing internal echoes can infiltration from metastatic ovarian neoplasms suggest hemoperitoneum, with the ruptured (70). In such cases, there is gradually increasing cyst adopting an angulated or crenated appear- lymphatic obstruction that results in edema and ance (68). Hemorrhage within both the cyst massive ovarian enlargement (Fig 15). and the peritoneal cavity has high attenuation at CT (69) and typically high signal intensity Ovarian Hyperstimulation at T1-weighted MRI, without suppression on Ovarian hyperstimulation, an iatrogenic side images obtained with T1-weighted fat-saturated effect of follicle stimulation therapy for subfertil- sequences. ity, results in excessive follicle production and While inflammation and hemorrhage also ovarian enlargement. At imaging, distinguish- can be seen in adnexal torsion, the absence of ing features of ovarian hyperstimulation include the other typical signs of torsion suggest hemor- enlarged follicles in a spoke-wheel distribution rhagic ovarian cyst as the more likely anomaly. and normal central ovarian tissue (72) (Fig 16). The identification of a thin rim of nonedematous In contrast, adnexal torsion usually involves small surrounding ovarian stroma also can facilitate peripherally placed follicles encircling a markedly diagnosis of a ruptured cyst or other intraovar- expanded edematous central medulla. 622 March-April 2021 radiographics.rsna.org

Figure 16. Ovarian hyperstimulation in a 37-year- old woman who was 11 weeks pregnant following Figure 17. Torsed degenerating leiomyoma in a ovulation induction and presented with right iliac 67-year-old woman who presented with a pelvic fossa pain. Transabdominal US image shows ovarian mass and pain. Axial T2-weighted MR image shows enlargement with multiple large peripheral follicles a large central pelvic mass adjacent to but separate (arrowheads) in a spoke-wheel distribution. While from the left ovary. The left ovary (solid arrow) con- hyperstimulated ovaries are a risk factor for adnexal tains a small simple cyst and is not enlarged; there- torsion, there is no pedicle twist or central edema to fore, this is not adnexal torsion. The pelvic mass has suggest this as the cause. a lacy cobweb pattern of low signal intensity (arrowhead) on a background of high signal intensity. This appearance is consistent with a leiomyoma undergoing cystic degeneration. A thickened twisted The ovarian features of hyperstimulation are pedicle (dashed arrow) connects the lesion to the usually bilateral and arise in combination with broad ligament. a history of follicle stimulation therapy, making ovarian hyperstimulation relatively easy to diagnose. In addition, large-volume ascites and pleural separate from the mass enables the exclusion of effusions are often present. However, enlarged ovarian torsion, although isolated fallopian tube hyperstimulated ovaries are at increased risk of torsion remains a rare possibility (75). torsion; therefore, if an ovary is asymmetrically enlarged or symptoms become more unilateral, Conclusion torsion should always be considered (24). Adnexal torsion eventually leads to ovarian and possibly fallopian tube infarction; thus, prompt Degenerating Leiomyoma diagnosis is critical to salvage the ovary. A high A pedunculated degenerating leiomyoma may index of clinical suspicion is required in cases of torse and can be difficult to differentiate from ad- sudden-onset pelvic pain when it is associated nexal torsion on contrast-enhanced CT images, with nausea or vomiting, particularly in premeno- particularly since the clinical manifestations of pausal patients, and the radiologist may be the these two conditions may be similar, resulting in first to consider this diagnosis. acute pain (73). Both diseases manifest as large Systematic assessment of the pelvic viscera pelvic masses adjacent to but separate from the with all imaging modalities assists in making a uterus (Fig 17). prompt diagnosis. Typical findings of adnexal tor- The MRI appearances of degenerating leio- sion include an enlarged abnormally positioned myoma are variable and wide ranging, in part ovary positioned superiorly and toward the mid- because of the different types of degeneration line, with the uterus pulled to the side of the tor- that they can undergo (74), which are beyond sion. Additional features include central ovarian the scope of this article. It is important to note edema with peripherally displaced follicles that that a primary ovarian lesion such as a fibro form a string of pearls appearance. The diagnosis thecoma may undergo torsion and thus have an should be made by using US, which is the imag- appearance that is similar to that of a degenerating examination of choice in this setting. Multi- ing leiomyoma. Often when undergoing cystic planar reconstructions at cross-sectional imag- degeneration, leiomyomas can have a relatively ing are invaluable for demonstrating a twisted characteristic pattern of thin low-T2 signal bands pedicle, which often confirms the diagnosis. At within a cystic mass, which can add confidence contrast-enhanced CT, a triangle of adnexal soft to the diagnosis. Identification of the ovaries tissue is a suggestive sign. RG • Volume 41 Number 2 Dawood et al 623

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