Noninvasive diagnostic imaging of pelvic venous disorders.

Forty-one articles published between 1984 and 2023 were included in this literature review. In the clinical practice of a gynecologist, TVUS, in conjunction with TAUS, is the first method of screening/examination performed in patients with symptoms of CPP. PVD in TVUS may manifest as dilatation or tortuous aspects of ovarian veins, low blood flow (<3 cm/s) or reflux in ovarian veins and dilated arcuate vein in the myometrium communicating to pelvic varicosities 14 17 18 19 . Generally accepted imaging criteria that should be taken into consideration during diagnosis of PVD by TVUS include reflux (>1 s) and dilatation of the venous trunks on Valsalva, ipsilateral siphoning or contralateral dilation and syphon effects between the ovarian and internal iliac trunks, flow reversal in and distention of associated varices on Valsalva ( Fig. 1 a,b,c) ( Fig. 2 a,b,c) 20 21 . TVUS examination of a 44-year-old woman with CPP syndrome: Dilated arcuate veins in the myometrium with enhanced blood flow ( a ; arrows); dilated and tortuous ovarian vein with reversed caudal flow ( b ; arrow); dilated arcuate vein in the myometrium communicating with pelvic varicosities ( c ; arrow). Examples of TVUS imaging of dilated ovarian veins in various patients with PVD. The ovarian veins are marked with arrows ( a : diameter: 0.89 cm; b : diameter: 1.48 cm). In the case of TVUS, when appropriate imaging criteria are applied, it has a sensitivity of 92.3% and a specificity of 75% with false-positive and false-negative rates of 7.69% and 25%, respectively, for the detection of PVD 17 . Imaging criteria that should be considered during diagnosis of PVD by TAUS include dilatation (> 5 mm) of the ovarian vein with reversed caudal flow, dilatation of the arcuate veins and pelvic venous plexus (tortuous aspects) and variable duplex waveform in the varicoceles during the Valsalva 19 22 23 . Nonetheless, it should be noted that the diameter of the ovarian vein as an indicator of PVD remains debatable for researchers. A large-caliber ovarian vein may not show features of reflux, thus being asymptomatic. On the other hand, a small-diameter ovarian vein may show features of reflux, thus causing the typical symptoms of PVD described above 24 . Therefore, the assessment of reflux remains very important ( Fig. 3 a,b). According to Steenbeek et al., in TAUS reversed, caudal flow in the ovarian vein accounted for a sensitivity of 100% for detecting PVD 23 . Furthermore, when appropriate imaging criteria are applied, TAUS has a sensitivity of 76% and a specificity of 100% in the diagnosis of iliac vein obstruction and a sensitivity of 80% and a specificity of 94% in the diagnosis of renal vein obstruction 25 26 . Dilated ovarian vein (arrow) with a diameter of 0.90 cm in the TVUS examination a . On power Doppler b evidence of reflux (arrow: retrograde flow component below the baseline). According to Malgor et al., TAUS demonstrates a sensitivity of 100% and a specificity of 57% in the diagnosis of dilatation of the left ovarian vein and a sensitivity of 67% and a specificity of 90% in the diagnosis of dilatation of the right ovarian vein 27 . The diagnosis of PVD is challenging. Delayed or incorrect diagnosis affects treatment efficiency and significantly reduces patient quality of life, increasing the rate of patient morbidity and the incidence of recurrence. Noninvasive diagnostic imaging techniques like MRI and CT play an essential role in diagnosis and appropriate management selection for patients with PVD. Exclusion of other potential causes of CPP mentioned above should be the primary goal of a proper diagnosis of PVD. The accurate diagnosis of pelvic venous insufficiency is the secondary goal. The management strategy decision is complex and depends on the causes of PVD, the severity of PVD and finally radiological findings 28 . PVD in conventional MR manifests as tortuous, dilated and enhancing tubular structures around the uterus, ovaries, ovarian veins, vaginal venous plexus, adnexa, and broad ligament 7 28 29 30 31 . Generally accepted imaging criteria for diagnosing PVD by MR venography have been described. Grade I includes venous reflux in the left ovarian vein and/or left parauterine veins, and Grade II additionally includes venous reflux in the right ovarian vein and iliac vein (left/right) 29 30 31 . In addition, MR and CT enable the evaluation of structures for which evaluation in TVUS or TAUS may be limited, such as the left common iliac vein or the left renal vein 20 ( Fig. 4 a,b) ( Fig. 5 a,b,c,d) ( Fig. 6 a,b). Depiction of a dilated and divided left ovarian vein (arrows) in a 38-year-old PVD patient on MRI a and in the corresponding conventional venography b . Depiction of massive pelvic varices on both sides of the uterus in pelvic MRI (T2 FatSat sequences): coronal views show the tortuous vascular convolutions (arrows) on both sides of the uterus and vagina a , which continue anteriorly b . The axial view shows that the findings are more pronounced on the left c and that the pelvic varices extend from the bladder deep into the pelvis d . Depiction of dilated parauterine veins (arrows) on the right side in a 36-year-old PVD patient on MRI a; b . According to Asciutto et al., MR venography has a sensitivity of 88% and a specificity of 67% for the detection of diseases located in ovarian veins, a sensitivity of 100% and a specificity of 38% for the detection of diseases located in internal iliac veins and sensitivity of 91% and a specificity of 42% for the detection of diseases located in the pelvic venous plexus 32 . Furthermore, Young et al. found no significant difference between time-resolved MR angiography and conventional venography for grading ovarian vein reflux 30 . Compared to TVUS, TAUS and MR, CT is less frequently used for diagnosing PVD. Due to ionizing radiation, CT scans should be used cautiously in premenopausal patients. Furthermore, CT is more expensive than TVUS or TAUS. Despite that, CT provides detailed anatomical information about the pelvis and abdomen and allows the exclusion of some of the other causes of CPP 7 . PVD on conventional CT manifests as tortuous, dilated, and enhancing tubular structures around the uterus, ovaries, ovarian veins, vaginal venous plexus, adnexa, and broad ligament 33 . The diagnostic criteria of PVD in CT examination include identifying at least four ipsilateral pelvic veins (with a diameter of at least one vein greater than 4 mm) and ovarian vein diameter greater than 8 mm. Obstructing mass lesions are absent 34 . Visualization of reflux (like in the Valsalva maneuver) is possible during CT. Deep breath hold increases intraabdominal pressure in the supine position, inducing reflux 35 . Furthermore, it is possible to assess structures in which evaluation in TVUS or TAUS may be limited, such as the left common iliac vein or left renal vein 20 . According to Osman et al., CT has a sensitivity of 94.8% for the diagnosis of PVD. Furthermore, during the assessment of the diameter of the ovarian vein and the number and diameter of the pelvic varicose, no statistically significant differences were found between CT and conventional venography 34 . When appropriate imaging criteria are applied, CT has a sensitivity of 91.7% and a specificity of 88.9% for detecting left renal vein obstruction 36 . Moreover, lower doses of contrast medium are required to perform CT venography 37 .

Analysis of the available literature in the PubMed, Cochrane and MEDLINE databases (original articles and reviews published between 1969 and 2023) was conducted between August 2022 and November 2023 using the following search term combinations: pelvic venous disorders OR chronic pelvic pain OR pelvic venous incompetence OR pelvic venous insufficiency OR pelvic congestion syndrome OR ovarian venous reflux OR pelvic venous reflux OR nutcracker syndrome OR May–Thurner, AND diagnostic imaging OR minimally invasive imaging techniques OR ultrasonography OR computed tomography OR magnetic resonance OR venography. English-language abstracts analyzing CPP (etiology, differential diagnosis, diagnostic methods, and management strategy) were included in the literature analysis. Case studies, studies with insufficient/overlapping data, and irrelevant outcomes were excluded from the literature review. After the review of 1460 abstracts, full versions of scientific papers related to the topic were assessed for eligibility. The final sample was chosen from the 295 reviewed English-language full-text articles.

Noninvasive imaging techniques seem to be crucial for diagnosing PVD. Currently, PVD-induced CPP is a treatable disease in the vast majority of patients. Delayed or incorrect diagnosis affects treatment efficiency and significantly reduces patient quality of life. It should be kept in mind that all noninvasive imaging techniques require significant experience, and the results may vary depending on the examiner’s experience 23 . These noninvasive diagnostic imaging techniques should be performed according to standardized protocols considering generally accepted criteria. Undoubtedly, such management increases the sensitivity and specificity of tests. As presented above, the diagnostic criteria of PVD are not equal and vary between techniques. Firstly, the diagnostic criteria were based on various studies. Moreover, these differences may result from the way the tests are performed. The test result is influenced by, among other things, the patient’s position and the patient’s ability to cooperate (to induce reflux). Diagnostic criteria and the main advantages/disadvantages of all methods described above have been summarized in the form of a table ( Table 1 ). Future studies investigating the role of noninvasive imaging techniques in diagnosing PVD are required.

In conjunction with TAUS, TVUS is the first-choice method of PVD examination performed in a gynecologist’s clinical practice. These are cheap and noninvasive imaging techniques that can be performed during the same visit. Both TVUS and TAUS allow the evaluation of multiple pathologies that may contribute to CPP, like ovarian tumors, endometriosis, adenomyosis, or uterine fibroids 17 38 . TVUS could be performed both in supine and semi-erect positions, offering more detailed imaging of anatomical structures involved in PVD 14 16 . In the case of disease at the more central level (inferior vena cava, iliac veins and renal veins), the image obtained by the TVUS may be less accurate compared to TAUS 14 . Furthermore, TAUS also allows exclusion of some of the other causes of CPP described above that cannot be excluded using TVUS 14 22 . Unfortunately, the image obtained in the ultrasound examination may be distorted due to the body habitus and the presence of bowel gas obstructing venous structures despite adequate preparation for the test (at the clinic of the authors of the manuscript, the test is performed in the morning after 6 hours of fasting. Patients are asked not to eat fatty meals, dairy products, and carbonated drinks the day before, and not to chew gum or smoke on the day of the procedure). As described above, Valero et al. found that TVUS has a sensitivity of 92.3% and a specificity of 75% with false-positive and false-negative rates of 7.69% and 25%, respectively, for the detection of PVD. The main limitations of this study were the small sample size and lack of intra- and interobserver reproducibility. Furthermore, patients were not adequately prepared for the test 17 . It was found that TAUS has a sensitivity of 100% and a specificity of 57% for the diagnosis of dilatation of the left ovarian vein, a sensitivity of 67% and a specificity of 90% for the diagnosis of dilatation of the right ovarian vein, a sensitivity of 76% and a specificity of 100% for the diagnosis of iliac vein obstruction and a sensitivity of 80% and a specificity of 94% for the diagnosis of renal vein obstruction. The main limitation of the cited studies was the small sample size. Furthermore, the study performed by Metzger et al. was cross-sectional and the study performed by Malgor et al. was retrospective 25 26 27 . Both TVUS and TAUS require significant experience, and the results obtained may vary depending on the examiner’s experience 23 . As the first-choice method of PVD detection in gynecologists’ clinical practice, TVUS and TAUS are very helpful and complement each other. Although MR is more expensive than CT, it is used more extensively in diagnosing PVD in many centers. Compared to CT, it does not unnecessarily expose patients to ionizing radiation, allowing precise assessment of pelvic and abdominal structures. Furthermore, MR enables the exclusion of some of the other causes of CPP. Unfortunately, due to the performance of the examination in the supine position, MR may underestimate venous pathology 7 32 . MR provides exquisite soft-tissue contrast and allows excellent evaluation of the pelvic organs including visualization of the pelvic, perineal, vulval/labial, and thigh varices as well as dilatation of the ovarian vein 7 32 33 . Moreover, thanks to multiplanar imaging capability and high-quality soft-tissue contrast, secondary causes of PVD can be detected 39 . Tortuous veins with blood stasis can be visualized in high quality using the T2 Fat-Sat Spin echo sequence. MR venography with time-resolved imaging is a noninvasive and fast imaging technique that allows for the visualization of flow disturbances, which are often key to making the diagnosis. Data on pelvic anatomy as well as flow disturbances are also useful in developing the details of the embolization procedure. MR is reproducible, less expensive than conventional venography, and non-irradiating in these young female patients 20 29 40 41 . MR enables clarification of any diagnostic ambiguities on TVUS or TAUS without exposing the patient to ionizing radiation. However, it should be kept in mind that MR is a method that requires significant reading experience (more than CT), and the results obtained may vary depending on the experience of the operator 23 . It was found that MR has a sensitivity of 88% and a specificity of 67% for the detection of diseases located in ovarian veins, a sensitivity of 100% and a specificity of 38% for the detection of diseases located in internal iliac veins and a sensitivity of 91% and a specificity of 42% for the detection of diseases located in the pelvic venous plexus. Moreover, Young et al. found no significant difference between time-resolved MR angiography and conventional venography for grading ovarian vein reflux. Both studies have a small sample size. Furthermore, the study design by Young et al. was retrospective and there was no control group 30 32 . Compared to MR, CT is a lower-cost and more available imaging technique and, therefore, it is considered to be the method of choice by some for the diagnosis of PVD due to its highest temporal and spatial resolution with the advantages of 3D reconstruction images and post-imaging processing in the form of multiplanar reformatting. CT also enables precise assessment of pelvic and abdominal structures, whose evaluation with TAUS or TVUS may be limited. Furthermore, lower doses of contrast medium are required to perform CT venography 37 . Unfortunately, CT does not allow for a detailed distinction of veins in the case of massive parametrial varicose veins and for dynamic evaluation of the venous flow 34 . It was found that CT has a sensitivity of 94.8% for the diagnosis of PVD, and a sensitivity of 91.7% and a specificity of 88.9% for detecting left renal vein obstruction and that no statistically significant differences were found between CT and conventional venography. However, both of these studies were retrospective and there were problems with a control group 34 36 . In some cases, the use of CT may be appropriate. If it is not possible to perform MR, CT also allows clarification of any diagnostic ambiguities on TVUS or TAUS. However, due to ionizing radiation, the application of CT in PVD diagnosis is limited.

According to the Royal College of Obstetricians and Gynecologists, chronic pelvic pain (CPP) can be defined as a condition in which intermittent or constant pain (dull ache or fullness) in the lower abdomen or pelvis lasts at least six months, and the occurrence of pain is not related to pregnancy, sexual intercourse, or menstrual cycle 1 . However, pain could be aggravated by menstruation, sexual intercourse, pregnancy, prolonged standing, or overexertion. Other non-specific symptoms could include vulvar swelling, vaginal discharge, urinary urgency, rectal discomfort, back pain, hip pain, varicose veins of the vulva, perineum and lower extremity, persistent genital arousal disorder, flatulence, nausea, headache, apathy, and depression 2 3 4 . It is estimated that CPP may affect up to 24% of women 5 6 . CPP differential diagnosis should consider gynecological, gastrointestinal, urological, neurological, musculoskeletal, and mental health disorders. Unfortunately, despite extensive diagnostics, the cause of CPP often remains unknown 7 8 9 10 . The pathophysiology of CPP can be explained to a large extent by the occurrence of pelvic venous disorders (PVDs) 4 11 . PVDs include a group of disease entities whose common feature is the occurrence of the symptoms of CPP listed above, and varices located in the pelvis and abdomen. The nomenclature update has changed historically used terms such as pelvic congestion syndrome, nutcracker syndrome and May-Thurner syndrome, resulting in a more precise diagnosis that is based on anatomy and underlying pathophysiology 4 12 13 . Venography is an invasive method requiring the administration of contrast. Diagnostic criteria of PVD using pelvic venography include ovarian vein diameter greater than 6 mm, contrast retention for longer than 20 seconds, stasis (of blood flow) in the ovary, pelvis, vulva and vagina or thigh, and visualization of reflux. Pelvic venography makes it possible to obtain a detailed image of the anatomy of the veins before the embolization procedure. Moreover, it allows for the observation of reflux, which is not always possible in noninvasive imaging techniques, and most importantly, it allows for simultaneous intervention through pelvic vein embolization 13 14 . When appropriate imaging criteria are applied, conventional venography has a sensitivity of 91% and a specificity of 89% in PVD diagnosis 11 15 . As premenopausal women constitute the majority of CPP patients, consideration should be given to their unnecessary exposure to ionizing radiation 7 16 . Although pelvic venography is still considered the gold standard for diagnosing PVD, noninvasive diagnostic imaging is instrumental in identifying patients with PVD 17 . This literature review aimed to evaluate the usefulness of noninvasive diagnostic imaging techniques like transvaginal ultrasonography (TVUS), transabdominal ultrasonography (TAUS), magnetic resonance (MR), and computed tomography (CT) in the identification of patients with PVD.