Noninvasive diagnostic imaging of pelvic venous disorders

Abstract

It is estimated that chronic pelvic pain (CPP) may affect up to 24% of women. Unfortunately, very often, despite extensive diagnostics, the cause of CPP remains unknown. The pathophysiology of CPP could be explained to a large extent by the occurrence of pelvic venous disorders (PVD). Although pelvic venography is still considered the gold standard for the diagnosis of PVD, noninvasive diagnostic imaging techniques seem to be instrumental in the initial identification of patients with PVD. This literature review aimed to analyze and evaluate the usefulness of noninvasive diagnostic imaging techniques like transvaginal ultrasonography, transabdominal ultrasonography, magnetic resonance, and computed tomography in the diagnosis and identification of patients with PVD. Forty-one articles published between 1984 and 2023 were included in this literature review. Based on this literature review, we conclude that the clinical application of noninvasive diagnostic techniques in the diagnosis of PVD seems to be very promising. Future studies investigating the role of noninvasive diagnostic imaging techniques in the diagnosis of PVD are required.

Zusammenfassung

Schätzungen zufolge sind bis zu 24% aller Frauen von chronischen Beckenschmerzen (CPP: „Chronic Pelvic Pain“) betroffen. Leider bleibt die Ursache von CPP trotz umfassender Diagnostik sehr oft unbekannt. Die Pathophysiologie von CPP könnte zu einem großen Teil durch das Auftreten von Beckenvenen-Erkrankungen (PVD: „Pelvic Venous Disorders“) erklärt werden. Obwohl die Beckenvenografie nach wie vor als Goldstandard für die Diagnose der PVD gilt, scheinen nicht invasive diagnostische Bildgebungstechniken bei der Erstidentifizierung von Patienten mit PVD hilfreich zu sein.

Diese Literaturrecherche zielte darauf ab, den Nutzen nicht invasiver diagnostischer Bildgebungstechniken wie transvaginaler Ultraschall, transabdominaler Ultraschall, Magnetresonanztomografie und Computertomografie bei der Diagnose und Identifizierung von Patienten mit PVD zu analysieren und zu bewerten.

In diese Literaturübersicht wurden 41 Artikel einbezogen, die zwischen 1984 und 2023 veröffentlicht wurden. Basierend auf dieser Literaturrecherche kommen wir zu dem Schluss, dass die klinische Anwendung nicht invasiver Diagnosetechniken bei der Diagnose von PVD sehr vielversprechend zu sein scheint.

Zukünftige Studien, die die Rolle nicht invasiver diagnostischer Bildgebungstechniken bei der Diagnose von PVD untersuchen, sind erforderlich.

Keywords

Pelvic Venous Disorders - Chronic Pelvic Pain - Ultrasonography - MRI - Noninvasive diagnostic imaging

Introduction

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.

Material and Methods

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.

Results

Forty-one articles published between 1984 and 2023 were included in this literature review.

Ultrasonography

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].

Fig. 1 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).

Fig. 2 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].

Fig. 3 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].

Magnetic Resonance

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).

Fig. 4 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.

Fig. 5 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.

Fig. 6 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].

Computed Tomography

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].

Discussion

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.

Conclusion

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]).

Table 1 Diagnostic criteria, main advantages, and disadvantages of conventional venography, TVUS, TAUS, CT, and MR [7] [11] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [28] [29] [30] [31] [33] [34] [35] [36] [37].

	Conventional venography	TVUS	TAUS	MR	CT
Diagnostic criteria	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 Visualization of reflux	Reflux (>1 s) 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	Dilatation (> 5 mm) of the ovarian vein with the reversed caudal flow Dilatation of arcuate veins and pelvic venous plexus (tortuous aspects) Variable duplex waveform in the varicoceles during the Valsalva	Grade I – venous reflux in the left ovarian vein and/or left parauterine veins Grade II – includes additional venous reflux in the right ovarian vein and iliac vein (left/right)	Identification of at least four ipsilateral pelvic veins (with a diameter of at least one vein greater than 4 mm) Ovarian vein diameter greater than 8 mm Obstructing mass lesions are absent
Advantages	Gold standard Detailed image of the anatomy of the veins Simultaneous intervention through pelvic vein embolization possible	First-choice/screening method of PVD examination performed in a gynecologist’s clinical practice Cheap No exposure to radiation Exclusion of other causes of CPP	First-choice/screening method for PVD examination performed in a gynecologist’s clinical practice Cheap No exposure to radiation Exclusion of other causes of CPP	Precise assessment of pelvis and abdomen exclusion of other causes of CPP No exposure to radiation	Precise assessment of pelvis and abdomen exclusion of other causes of CPP
Disadvantages	Invasive technique Exposure to radiation	Technically difficult Results may vary depending on the examiner’s experience Distortion due to body habitus or inadequate preparation for test	Technically difficult results may vary depending on the examiner’s experience Distortion due to body habitus or inadequate preparation to test	Results may vary depending on the examiner’s experience Expensive	Results may vary depending on the examiner’s experience Expensive

Future studies investigating the role of noninvasive imaging techniques in diagnosing PVD are required.

Conflict of Interest

The authors declare that they have no conflict of interest.

• References

• 1 Royal College of Obstetricians and Gynaecologists. The initial management of chronic pelvic pain: Green Top Guideline No. 41. (May 2012). Zugriff am 13. Oktober 2022 unter: https://www.rcog.org.uk/globalassets/documents/guidelines/gtg_41.pdf
• 2 Khilnani NM, Winokur RS, Scherer KL. et al. Clinical Presentation and Evaluation of Pelvic Venous Disorders in Women. Tech Vasc Interv Radiol 2021; 24 (01) 100730 DOI: 10.1016/j.tvir.2021.100730. (PMID: 34147196)
• 3 Phillips D, Deipolyi AR, Hesketh RL. et al. Pelvic congestion syndrome: etiology of pain, diagnosis, and clinical management. J Vasc Interv Radiol 2014; 25 (05) 725-733 DOI: 10.1016/j.jvir.2014.01.030. (PMID: 24745902)
• 4 Meissner MH, Khilnani NM, Labropoulos N. et al. The Symptoms-Varices-Pathophysiology classification of pelvic venous disorders: A report of the American Vein & Lymphatic Society International Working Group on Pelvic Venous Disorders. J Vasc Surg Venous Lymphat Disord 2021; 9 (03) 568-584 DOI: 10.1016/j.jvsv.2020.12.084. (PMID: 33529720)
• 5 Zondervan KT, Yudkin PL, Vessey MP. et al. The community prevalence of chronic pelvic pain in women and associated illness behaviour. Br J Gen Pract 2001; 51 (468) 541-547 (PMID: 11462313)
• 6 Latthe P, Latthe M, Say L. et al. WHO systematic review of prevalence of chronic pelvic pain: a neglected reproductive health morbidity. BMC Public Health 2006; 6: 177 DOI: 10.1186/1471-2458-6-177. (PMID: 16824213)
• 7 Borghi C, Dell’Atti L. Pelvic congestion syndrome: the current state of the literature. Arch Gynecol Obstet 2016; 293 (02) 291-301 DOI: 10.1007/s00404-015-3895-7. (PMID: 26404449)
• 8 Szymanski J, Jakiel G, Slabuszewska-Jozwiak A. Pelvic venous insufficiency – an often-forgotten cause of chronic pelvic pain. Ginekol Pol 2020; 91 (11) 704-708 DOI: 10.5603/GP.a2020.0093. (PMID: 33301167)
• 9 Xholli A, Londero AP, Cavalli E. et al. The Benefit of Transvaginal Elastography in Detecting Deep Endometriosis: A Feasibility Study. Ultraschall in Med 2023; DOI: 10.1055/a-2028-8214. (PMID: 36746396)
• 10 Cohen Ben-Meir L, Soriano D, Zajicek M. et al. The Association Between Gastrointestinal Symptoms and Transvaginal Ultrasound Findings in Women Referred for Endometriosis Evaluation: A Prospective Pilot Study. Ultraschall in Med 2022; 43 (05) e81-e89 DOI: 10.1055/a-1300-1887.
• 11 Beard RW, Highman JH, Pearce S. et al. Diagnosis of pelvic varicosities in women with chronic pelvic pain. Lancet 1984; 2: 946-949 DOI: 10.1016/s0140-6736(84)91165-6.
• 12 Clark MR, Taylor AC. Pelvic Venous Disorders: An Update in Terminology, Diagnosis, and Treatment. Semin Intervent Radiol 2023; 40 (04) 362-371 DOI: 10.1055/s-0043-1771041. (PMID: 37575340)
• 13 Tanaka ME, Kutsenko O, Salazar G. Choosing the Most Appropriate Treatment Option for Pelvic Venous Disease: Stenting versus Embolization. Semin Intervent Radiol 2021; 38 (02) 182-188 DOI: 10.1055/s-0041-1727104. (PMID: 34108804)
• 14 Arnoldussen CW, de Wolf MA, Wittens CH. Diagnostic imaging of pelvic congestive syndrome. Phlebology 2015; 30 (Suppl. 01) 67-72 DOI: 10.1177/0268355514568063. (PMID: 25729070)
• 15 Herrera-Betancourt AL, Villegas-Echeverri JD, López-Jaramillo JD. et al. Sensitivity and specificity of clinical findings for the diagnosis of pelvic congestion syndrome in women with chronic pelvic pain. Phlebology 2018; 33 (05) 303-308 DOI: 10.1177/0268355517702057.
• 16 Hansrani V, Dhorat Z, McCollum CN. Diagnosing of pelvic vein incompetence using minimally invasive ultrasound techniques. Vascular 2017; 25 (03) 253-259 DOI: 10.1177/1708538116670499. (PMID: 27688293)
• 17 Valero I, Garcia-Jimenez R, Valdevieso P. et al. Identification of Pelvic Congestion Syndrome Using Transvaginal Ultrasonography. A Useful Tool. Tomography 2022; 8 (01) 89-99 DOI: 10.3390/tomography8010008. (PMID: 35076614)
• 18 Knuttinen MG, Xie K, Jani A. et al. Pelvic venous insufficiency: imaging diagnosis, treatment approaches, and therapeutic issues. AJR Am J Roentgenol 2015; 204 (02) 448-458 DOI: 10.2214/AJR.14.12709. (PMID: 25615769)
• 19 Park SJ, Lim JW, Ko YT. et al. Diagnosis of pelvic congestion syndrome using transabdominal and transvaginal sonography. AJR Am J Roentgenol 2004; 182 (03) 683-688 DOI: 10.2214/ajr.182.3.1820683. (PMID: 14975970)
• 20 Topper SR, Winokur RS. Imaging of Pelvic Venous Disorders (PeVD); Should Every Patient Get an MRI?. Tech Vasc Interv Radiol 2021; 24 (01) 100731 DOI: 10.1016/j.tvir.2021.100731. (PMID: 34147189)
• 21 Whiteley MS, Dos Santos SJ, Harrison CC. et al. Transvaginal duplex ultrasonography appears to be the gold standard investigation for the haemodynamic evaluation of pelvic venous reflux in the ovarian and internal iliac veins in women. Phlebology 2015; 30 (10) 706-713 DOI: 10.1177/0268355514554638. (PMID: 25324278)
• 22 Labropoulos N, Jasinski PT, Adrahtas D. et al. A standardized ultrasound approach to pelvic congestion syndrome. Phlebology 2017; 32 (09) 608-619 DOI: 10.1177/0268355516677135. (PMID: 27799418)
• 23 Steenbeek MP, van der Vleuten CJM, Schultze Kool LJ. et al. Noninvasive diagnostic tools for pelvic congestion syndrome: a systematic review. Acta Obstet Gynecol Scand 2018; 97 (07) 776-786 DOI: 10.1111/aogs.13311.
• 24 Dos Santos SJ, Holdstock JM, Harrison CC. et al. Ovarian Vein Diameter Cannot Be Used as an Indicator of Ovarian Venous Reflux. Eur J Vasc Endovasc Surg 2015; 49 (01) 90-94 DOI: 10.1016/j.ejvs.2014.10.013. (PMID: 25457295)
• 25 Metzger PB, Rossi FH, Kambara AM. et al. Criteria for detecting significant chronic iliac venous obstructions with duplex ultrasound. J Vasc Surg Venous Lymphat Disord 2016; 4 (01) 18-27 DOI: 10.1016/j.jvsv.2015.07.002.
• 26 Kim SH, Cho SW, Kim HD. et al. Nutcracker syndrome: diagnosis with Doppler US. Radiology 1996; 198 (01) 93-97 DOI: 10.1148/radiology.198.1.8539413.
• 27 Malgor RD, Adrahtas D, Spentzouris G. et al. The role of duplex ultrasound in the workup of pelvic congestion syndrome. J Vasc Surg Venous Lymphat Disord 2014; 2 (01) 34-38 DOI: 10.1016/j.jvsv.2013.06.004. (PMID: 26992966)
• 28 Lombardi P, Carr JC, Allen BD. et al. Updates in Magnetic Resonance Venous Imaging. Semin Intervent Radiol 2021; 38 (02) 202-208 DOI: 10.1055/s-0041-1729152. (PMID: 34108807)
• 29 Kim CY, Miller Jr MJ, Merkle EM. Time-resolved MR angiography as a useful sequence for assessment of ovarian vein reflux. AJR Am J Roentgenol 2009; 193 (05) W458-463 DOI: 10.2214/AJR.09.2557. (PMID: 19843728)
• 30 Yang DM, Kim HC, Nam DH. et al. Time-resolved MR angiography for detecting and grading ovarian venous reflux: comparison with conventional venography. Br J Radiol 2012; 85: e117-122 DOI: 10.1259/bjr/79155839.
• 31 Dick EA, Burnett C, Anstee A. et al. Time-resolved imaging of contrast kinetics three-dimensional (3D) magnetic resonance venography in patients with pelvic congestion syndrome. Br J Radiol 2010; 83: 882-887 DOI: 10.1259/bjr/82417499.
• 32 Asciutto G, Mumme A, Marpe B. et al. MR venography in the detection of pelvic venous congestion. Eur J Vasc Endovasc Surg 2008; 36 (04) 491-496 DOI: 10.1016/j.ejvs.2008.06.024. (PMID: 18718774)
• 33 Ganeshan A, Upponi S, Hon LQ. et al. Chronic pelvic pain due to pelvic congestion syndrome: the role of diagnostic and interventional radiology. Cardiovasc Intervent Radiol 2007; 30 (06) 1105-1111 DOI: 10.1007/s00270-007-9160-0. (PMID: 17805925)
• 34 Osman AM, Mordi A, Khattab R. Female pelvic congestion syndrome: how can CT and MRI help in the management decision?. Br J Radiol 2021; 94: 20200881 DOI: 10.1259/bjr.20200881. (PMID: 33252986)
• 35 Desimpelaere JH, Seynaeve PC, Hagers YM. et al. Pelvic congestion syndrome: demonstration and diagnosis by helical CT. Abdom Imaging 1999; 24 (01) 100-102 DOI: 10.1007/s002619900451. (PMID: 9933685)
• 36 Kim KW, Cho JY, Kim SH. et al. Diagnostic value of computed tomographic findings of nutcracker syndrome: correlation with renal venography and renocaval pressure gradients. Eur J Radiol 2011; 80 (03) 648-654 DOI: 10.1016/j.ejrad.2010.08.044.
• 37 Baldt MM, Zontsich T, Stümpflen A. et al. Deep venous thrombosis of the lower extremity: efficacy of spiral CT venography compared with conventional venography in diagnosis. Radiology 1996; 200 (02) 423-428 DOI: 10.1148/radiology.200.2.8685336.
• 38 Kowalczyk K, Kowalczyk D, Klimek M. et al. A comprehensive use of ultrasound examination in infertility workup. Ginekol Pol 2021; DOI: 10.5603/GP.a2021.0086. (PMID: 33914311)
• 39 Watanabe Y, Dohke M, Okumura A. et al. Dynamic subtraction contrast-enhanced MR angiography: technique, clinical applications, and pitfalls. Radiographics 2000; 20 (01) 135-152 DOI: 10.1148/radiographics.20.1.g00ja10135. (PMID: 10682778)
• 40 Pandey T, Shaikh R, Viswamitra S. et al. Use of time resolved magnetic resonance imaging in the diagnosis of pelvic congestion syndrome. J Magn Reson Imaging 2010; 32 (03) 700-704 DOI: 10.1002/jmri.22288. (PMID: 20815070)
• 41 Huang YK, Tseng YH, Lin CH. et al. Evaluation of venous pathology of the lower extremities with triggered angiography non-contrast-enhanced magnetic resonance imaging. BMC Med Imaging 2019; 19 (01) 96 DOI: 10.1186/s12880-019-0395-4.

Publikationsverlauf

Eingereicht: 16. April 2023

Angenommen nach Revision: 25. Januar 2024

Accepted Manuscript online:
07. Februar 2024

Artikel online veröffentlicht:
06. Mai 2024