The rare adnexal torsion (AT) accounts for 2–3% of gynaecologic emergencies, involves partial or complete rotation of the ovarian vascular pedicle in the suspensory ligament and preferentially occurs on the right side because of contralateral protection from the sigmoid colon. It may affect the ovary, the fallopian tube or both, concomitant ovarian and tubal torsion being the most common event (up to 67% of cases) [42]. AT occurs in the first four decades of life and is uncommon in normal ovaries and in prepubertal girls with markedly mobile fallopian tubes. In reproductive age females, 50% to 90% of AT cases have an underlying ovarian mass (usually greater than 5 cm in diameter) that acts as a lead point for torsion, such as a large cyst, endometrioma, hyperstimulated ovary or benign tumour: a mature cystic teratoma represents the most common aetiology. Conversely, endometriomas and adnexal malignancies occasionally cause torsion because of fixation to adjacent structures [9, 43, 44].
The usual presentation is abrupt-onset lower abdominal pain radiating to the ipsilateral flank or groin, with adnexal tenderness. Alternatively, presentation is often nonspecific with intermittent pain, low-grade fever, nausea and vomiting. Recurrent attacks may be due to episodes of torsion and detorsion. In the early phase of AT, the low-pressure venous and lymphatic outflow is compromised, causing ovarian oedema, congestion and enlargement. If torsion persists, over time, the arterial circulation is impaired, thus resulting in ischaemia and haemorrhagic infarction. Therefore, the extent of imaging findings depends on the duration of torsion [42, 45].
In this respect, it is important to remember that the ovary has a dual blood supply:( a) from the ovarian artery (arising from the abdominal aorta), contained in the infundibulopelvic ligament that extends from the pelvic sidewall to the ovary; and (b) from the ovarian branch of the uterine artery (arising from the iliac internal artery), contained in the utero-ovarian ligament that connects the ovary to the uterus. Ovarian torsion occurs when an ovary twists on its ligamentous supports (both the infundibulopelvic ligament and the utero-ovarian ligament) [46].
US represents the primary imaging modality to assess ovarian torsion. During ovarian torsion, due to the abovementioned dual blood supply, colour Doppler US may still demonstrate some arterial vascular flow. Nevertheless, in the presence of suggestive clinical and imaging findings, this persistence of adnexal vascularisation does not rule out torsion [47].
After inconclusive US (lesion not clearly depicted or ambiguous findings), in premenopausal women, MRI represents the better technique to assess suspected AT, but CT is often performed in patients with alternative presumptive diagnoses. At CT, the unilaterally enlarged ovary (usually greater than 5 cm) is displaced from its expected site and often located on the midline, and the uterus is attracted towards the ipsilateral side by the shortened adnexal ligament. The oedematous ovary may show eccentric or concentric wall thickening or a ‘target-like’ pattern corresponding to peripheral displacement of follicles. Congested, enhancing ovarian blood vessels are generally seen; in this regard, it should be recalled that the pathognomonic twisted pedicle usually shows a spiral configuration, but may also present as a solid-like component adjacent to the ovarian mass. Pelvic free fluid and inflammatory fat stranding are generally present. In full-blown AT, haemorrhage appears as a hyperattenuating area and adnexal contrast enhancement is minimal or absent. When present, a mature cystic teratoma shows calcifications, foci of fat attenuation and enhancing mural nodules (Fig. 18) [9, 42, 45, 47,48,49].
Also in acute and in subacute settings, MRI may depict more clearly both direct and indirect findings of AT. The twisted pedicle, containing the thickened fallopian tube and the ligamentous support with its vascular structures, presents as a beak-like protrusion adjacent to the ovarian mass or to the enlarged ovary. In the early stage, when vascular congestion and oedematous changes prevail, the thickened (diameter > 10 mm) fallopian tube appears hypointense on T1-weighted images and hyperintense on T2-weighted images. In this stage, contrast agent administration allows to demonstrate the characteristic thickened swirling configuration of vascular structures. When ischaemic alterations and haemorrhagic infarction occur, the thickened fallopian tube may show high signal intensity on T1-weighted images. Post-contrast MRI sequences with post-processing subtraction techniques can demonstrate minimal or absent enhancement of the mass presenting high signal intensity on unenhanced T1-weighted fat-saturated images. An enlarged oedematous ovary with central afollicular stroma hyperintense on T2-weighted images and peripherally displaced follicles in a string-like appearance (‘pearl string sign’) is a quite specific sign of ovarian torsion; corpus luteum may be seen in the second half of the menstrual cycle (Fig. 19). In this early stage, ovarian stroma shows enhancement after contrast agent administration [9, 42, 45, 47,48,49,50].
At a later stage, haemorrhagic alterations develop, highly associated with infarction and secondary necrosis. Subacute haemorrhage shows high signal intensity on fat-saturated T1-weighted images and may involve the periphery of the enlarged ovary, as T1-hyperintense rim, or the central stroma. In this stage, heterogeneous, minimal or absent enhancement on gadolinium-enhanced subtraction of fat-saturated T1-weighted images confirm the evolution towards infarction [9, 42, 45, 47,48,49,50]..
Petkovska et al. described a perifollicular T2 hypointense rim correlating with perifollicular haemorrhage; the absence of this finding should be useful as a predictor of ovarian viability [51].
DWI, with both visual assessment and quantitative ADC measurement, may be useful in the diagnosis of ovarian torsion. In patients with ovarian torsion, the ADC value of the torsed ovary is significantly lower than that of the nonaffected side [52]. Kato et al. found that ADC values in swollen ovarian stroma of torsed ovaries were significantly lower in patients with haemorrhagic infarction than in those without. The cytotoxic oedema and haemorrhage that occur in ovarian torsion with haemorrhagic infarction would explain the restricted diffusion and low ADC values [53].
In patients with torsed ovarian masses, at visual assessment, higher signal intensity of the wall of the ovarian lesion on DWI significantly correlates with haemorrhagic infarction. Moreover, the high-contrast resolution of DW images may be useful to detect the twisted pedicle, reflecting in some cases of fallopian tube necrosis [54]. The contribution of DWI in the early diagnosis of ovarian torsion could avoid contrast media administration especially in some categories of patients, such as children and pregnant women [52]. Timely diagnosis of AT is crucial because the likelihood of preserving a viable ovary decreases over time. Surgical treatment should be performed within 48 h from the onset of pain to improve the outcome. Nowadays, laparoscopic detorsion is the treatment of choice in reproductive age females. In postmenopausal women and in presence of ovarian tumours, oophorectomy is required [44].
Isolated fallopian tube torsion and paraovarian/paratubal cysts torsion
Isolated fallopian tube torsion without ovarian torsion is exceptionally rare and requires surgical intervention too. Predisposing factors are hydrosalpinx, tubal ligation, tubal or paratubal cystic and solid masses [9].
CT, better if with multiplanar reformatted images, may show an adnexal structure distinct from the ovary. MRI usually shows a distended dilated fallopian tube with thickened walls; the tube may demonstrate a vortex-like appearance (due to more twists) distant from the ipsilateral ovary, and the latter appears normal. Thick and twisted pedicle can also be observed (whirlpool sign) [19, 50].
Paraovarian or paratubal cysts are unilocular cystic structures located in the broad ligament, between the fallopian tube and the ovary. Isolated torsion of paraovarian/paratubal cysts rarely occurs and its prevalence is higher in children than in adults. MR imaging generally demonstrates a unilocular cyst distinct from the ipsilateral ovary, hyperintense on T2-weighted images and hypointense on T1-weighted images. The signal intensity of the cystic content may be slightly high on T1-weighted images due to haemorrhagic changes related to torsion [9].
Differential diagnosis
The differential diagnosis of AT includes massive ovarian oedema and ovarian hyperstimulation syndrome (OHSS). The former entity is a rare, benign condition thought to result from intermittent or partial torsion of the mesovary compromising the venous and lymphatic drainage but with preserved arterial supply [55].
The imaging appearance of massive ovarian oedema is similar to that of AT: an enlarged ovary with oedematous stroma and multiple nonovulatory follicles pressed towards the periphery of the cortex (Fig. 20) [56]. However, patients’ clinical history generally records self-limiting episodes of abdominal pain of different durations. The features of pain vary (acute pain or progressive and profound diffuse pain) depending on the rapidity of the torsion; menstrual irregularities, infertility, abdominal distension, signs of virilisation and precocious puberty are also reported [57, 58].
OHSS is an iatrogenic complication of assisted reproduction techniques, characterised by bilaterally enlarged ovaries with several, peripherally located cysts accompanied by fluid shift from the intravascular to third space from increased capillary permeability that may cause the development of ascites, pleural effusions and oliguria in severe forms [59]. Typical imaging findings at CT and MRI include bilateral symmetric enlargement of ovaries due to the presence of multiple cysts representing enlarged follicles or corpus luteum cysts. Cystic content can be fluid-like or haemorrhagic; in the latter case, cysts demonstrate higher attenuation at CT and high T1 signal intensity at MRI. The characteristic peripheral location of the follicles, separated by thin septa and surrounding a central core of ovarian stroma, has been referred to as ‘wheel spoke’ appearance [60]. Differently from cystic neoplasms, OHSS lacks abnormal enhancing solid components within the cystic lesions; in addition, follow-up imaging should demonstrate resolution. It should also be remembered that enlarged hyperstimulated ovaries are themselves at risk for torsion [61]. If torsion occurs in hyperstimulated ovaries, the latter may demonstrate asymmetrical augmentation, abnormal enhancement, twisted pedicle and eventually haemorrhage [50].
Other features of OHSS include free fluid in the peritoneal, pleural and pericardial cavity; the free fluid seen in OHSS is generally simple ascites, although it may display slightly higher attenuation due to ruptured haemorrhagic cysts. The modified Golan classification categorises OHSS as mild, moderate or severe on the basis of symptoms severity and radiologic findings [62].
Pelvic congestion syndrome
Congested pelvic veins without AT are the hallmark of the pelvic congestion syndrome (PCS), an underdiagnosed condition that affects 9% of premenopausal women and may be exacerbated by intra-abdominal pressure. The multifactorial pathogenesis involves a family history of varicose veins, previous pelvic surgery, multiple pregnancies, hormonal influences and retroverted uterus. Although the key symptom is chronic dull pelvic pain that worsens in the premenstrual phase, acute and severe pain may also occur. Flow reduction, thrombosis and mass effect on nerves may lead to worsening pelvic pain. Other clinical manifestations may include dyspareunia, postcoital ache, dysmenorrhoea and perineal pain [63, 64].
Similarly to male varicocele, dilatation of the gonadal veins and pelvic venous plexus more commonly occurs on the left side because of left ovarian vein draining into left renal vein before reaching the inferior vena cava. Mechanical extrinsic compression of drainage veins such as in retroaortic left renal vein, in May-Thurner syndrome (left common iliac vein compression against the lumbar spine by the right common iliac artery) or in nutcracker syndrome (left renal vein compression between superior mesenteric artery and aorta), may lead to venous congestion and engorgement of the ovarian vein [65]. In this latter syndrome, the abrupt narrowing, with a triangular shape, of the proximally dilated left renal vein between the abdominal aorta and the superior mesenteric artery is referred to as the ‘beak sign’. It is one of the most useful CT findings for the diagnosis of nutcracker syndrome, with a sensitivity of 91.7% and a specificity of 88.9% according to the literature [66, 67]. MR angiography provides findings similar to those of CT with the advantage of being less invasive and without radiation exposure in comparison with retrograde venography [68].
At CT, tortuous and dilated (> 4 mm) tubular structures nearby the ovary and uterus show slow blood flow and enhancement synchronous with veins. The diagnostic criteria for PCS require at least four ipsilateral parauterine veins of varying calibre, at least one measuring more than 4 mm in diameter, or an ovarian vein diameter greater than 8 mm (Fig. 21). Similarly, MRI depicts pelvic varices as multiple dilated vessels lying on uterus (and within the myometrium such as arcuate veins), ovaries and pelvic sidewall that can extend inferiorly to communicate with paravaginal and thigh venous plexus [64, 69,70,71]. Dilated veins are hyperintense on gradient-echo T1-weighted images; on T2-weighted MR images, they may show no signal intensity due to flow-void artefacts or mixed low and high signal intensity because of the relatively slow flow inside the vessels. Gradient-echo fat-suppressed T1-weighted sequences after intravenous administration of contrast material demonstrate vascular enhancement of pelvic varices, thus confirming the diagnosis (Figs. 22 and 23) [64]. Asciutto et al. reported MRI to have levels of sensitivity and specificity for PGS respectively of 88% and 67% for ovarian veins, 100% and 38% for iliac veins and 91 and 42% for pelvic plexus [72].
Additionally, up to 50% of women with PVI present cystic formations in the ovary, ranging from scant cysts to classic polycystic ovary aspect (Fig. 24) [64]. The mechanism underlying these cystic changes in the ovary is not completely known, although a relationship with increased oestrogen levels has been reported [73].