Journal of Clinical Medicine Article Hemodynamic and Radiological Classification of Ovarian Veins System Insufficiency Cezary Szary 1,2,*, Justyna Wilczko 1, Michal Zawadzki 1,3 and Tomasz Grzela 1,4 1 Clinic of Phlebology, Wawelska 5, 02-034 Warsaw, Poland; justyna.wilczko@klinikaflebologii.pl (J.W.); michal.zawadzki@klinikaflebologii.pl (M.Z.); tomasz.grzela@klinikaflebologii.pl (T.G.) 2 Diagnostic Imaging Center MRI&CT, Center of Sports Medicine, Wawelska 5, 02-034 Warsaw, Poland 3 Department of Radiology, Centre of Postgraduate Medical Education, 01-813 Warsaw, Poland 4 Department of Histology and Embryology, Medical University of Warsaw, 02-022 Warsaw, Poland * Correspondence: cezary.szary@klinikaflebologii.pl Abstract: Ovarian veins system insufficiency is one of the most common reasons for pelvic venous insufficiency (PVI). PVI is a hemodynamic phenomenon responsible for the occurrence of venous insufficiency of the lower extremities and recurrent varicose veins in nulliparous and parous women, as well as for a set of symptoms described as pelvic congestion syndrome (PCS). In the years 2017–2019, 535 patients admitted to our center with symptoms of venous insufficiency of the lower extremities, underwent complete ultrasound diagnostics (color-duplex ultrasound) of the venous system of the abdomen, pelvis and lower limbs, as well as extended imaging diagnostics using computed tomography (CT) or magnetic resonance (MR) venography. On the basis of the obtained results, the authors proposed a 4-grade hemodynamic and radiological classification (grades I-IV) defining the stratification of ovarian veins insufficiency. Using the above mentioned classification approx. 32% patients were identified as Grade I and I/II, approximately 35% revealed morphological and hemodynamic changes corresponding to Grade II and II/III, approximately 25% were classified Citation: Szary, C.; Wilczko, J.; as Grade III, whereas the remaining 8% were assessed as Grade IV. The described classification allows Zawadzki, M.; Grzela, T. for the grading of ovarian veins insufficiency based on transparent radiological criteria, making Hemodynamic and Radiological it easy to use in everyday clinical practice. According to the authors, the proposed classification Classification of Ovarian Veins could facilitate communication between diagnostic physicians, specialists dealing with the treatment System Insufficiency. J. Clin. Med. of venous insufficiency and gynecologists, who admit patients with symptoms suggesting venous 2021, 10, 646. https://doi.org/ insufficiency of the pelvis. 10.3390/jcm10040646 Keywords: ovarian veins; pelvic veins insufficiency; color-duplex ultrasound; venography Academic Editor: Attilio Cavezzi Received: 30 December 2020 Accepted: 4 February 2021 Published: 8 February 2021 1. Introduction Publisher’s Note: MDPI stays neutral Pelvic venous insufficiency (PVI) is a very common hemodynamic phenomenon with regard to jurisdictional claims in (estimated to be present in 20–43% of the population in women) [1–3], most often resulting published maps and institutional affil- from the reversal of venous blood flow, which occurs in the mechanism of outflow disorders, iations. or excessive dilatation of the main venous axes (VAX) located within the abdomen and pelvis. The abovementioned pathophysiological phenomenon results in overloading of the capacitive venous vessels in the pelvis, most often the para-uterine and peri-vaginal venous plexuses (Figure1), thus generating so-called venous leaks from the pelvis and Copyright: © 2021 by the authors. vulvo-perineal varicosities. Licensee MDPI, Basel, Switzerland. The phenomenon of pelvic venous insufficiency is most frequently caused by the This article is an open access article hemodynamic dysfunction of the ovarian veins [4–7], leading to the retention of venous distributed under the terms and blood in the para-uterine venous plexuses, which through anatomical anastomoses, in- conditions of the Creative Commons cluding uterine veins, overloads the internal iliac veins. This phenomenon is particularly Attribution (CC BY) license (https:// evident in multiparous women who develop chronic insufficiency of both ovarian veins creativecommons.org/licenses/by/ after delivery and widening of the branches of the internal iliac veins. 4.0/). J. Clin. Med. 2021, 10, 646. https://doi.org/10.3390/jcm10040646 https://www.mdpi.com/journal/jcm J. Clin. Med. 2021, 10, x FOR PEER REVIEW 2 of 21 J. Clin. Med. 2021, 10, 646 2 of 19 Figure 1. Illustration of abdominal and pelvic venous system in women. Figure 1. Illustration of abdominal and pelvic venous system in women. In the light of our recent studies [8], growing evidence indicates that PVI resulting from theIn the incompetence light of our ofrecent the ovarianstudies [8], veins growing is responsible evidence in indicates part for that primary PVI resulting venous insufficiencyfrom the incompetence of the lower of extremities, the ovarian asveins well is as responsible for the formation in part for of recurrentprimary venous varicose in- veins.sufficiency As we of know the fromlower the extremities, latest literature as well of patientsas for the with formation recurrent of varices recurrent of the varicose lower extremities,veins. As we PVI know is found from inthe over latest half literature of studied of patients women with [7–13 recurrent]. varices of the lower extremities,Pelvic venous PVI is insufficiencyfound in over can half cause of studied a number women of clinical [7–13]. symptoms. Some of them, limitedPelvic to the venous pelvis insufficiency and genital areascan cause (most a number often perineum of clinical and symptoms. vulva), are Some defined of them, as pelviclimited congestion to the pelvis syndrome and genital (PCS). areas Typical (most PCS often is characterized perineum and by vulva), gravitational are defined pelvic as painpelvic or discomfortcongestion thatsyndrome is worse (PCS). in the Typical upright PCS and is sitting characterized position andby gravitational is associated pelvic with pelvicpain or and discomfort vulvo-pudendal that is worse varicosities in the as upright well as and symptoms sitting position of dyspareunia and is associated and postcoital with painpelvic [9, 10and]. vulvo-pudendal varicosities as well as symptoms of dyspareunia and post- coitalThe pain first [9,10]. attempts to systematize the diagnostic approach to pelvic venous insuffi- ciencyThe began first in attempts the 1990s. to Forsystematize many years, the thediagnostic gold standard approach of imaging to pelvic in venous PVI has insuffi- been classicalciency began retrograde in the phlebography, 1990s. For many performed years, the by percutaneousgold standard access of imaging with directin PVI catheteri- has been zationclassical and retrograde contrasting phlebogr of potentiallyaphy, performed failing vessels, by percutaneous such as ovarian access veins with or internal direct cathe- iliac veinsterization[14–16 and]. The contrasting development of potentially of ultrasonography, failing vessels, and such especially as ovarian the improvement veins or internal of duplexiliac veins ultrasound [14–16]. techniques, The development enabled of the ultras useonography, of transvaginal and ultrasound especially the (TVU), improvement and later ofof transabdominal duplex ultrasound ultrasound techniques, (TAU) enabled in the diagnosis the use of of transvaginal PVI. Numerous ultrasound attempts (TVU), were also and madelater toof standardizetransabdominal the examination ultrasound of(TAU) the venous in the system diagnosis of the of pelvisPVI. Numerous and the abdominal attempts cavitywere also using made duplex to standardize ultrasound [the16– examination20]. of the venous system of the pelvis and the abdominalThe following cavity using years duplex saw the ultrasound development [16–20]. and increase in the frequency of an- giographicThe following examinations years insaw computed the development tomography and andincrease magnetic in the resonance frequency imaging.of angio- [4graphic,21–23] .examinations The first attempts in computed were also tomography made to and standardize magnetic this resonance type of imaging. research [4,21– and to23]. create The thefirst firstattempts classifications were also describingmade to stan thedardize phenomenon this type of of pelvic research venous and to insuffi- create ciencythe first [4, 21classifications–23]. In the newest describing international the phenomenon consensuses of [pelvic24,25] venous the authors insufficiency briefly present [4,21– 4-grades23]. In the (GI-GIV) newest ofinternational pelvic venous consensuses reflux criteria [24,25] for the cross-sectional authors briefly imaging present diagnosis 4-grades of(GI-GIV) PVI. of pelvic venous reflux criteria for cross-sectional imaging diagnosis of PVI. However,However, to to date, date, none none of theof the existing existing classifications classifications has gainedhas gained universal universal approval approval [25]. Taking[25]. Taking the above the above into account, into account, the authors the authors attempted attempted to create to acreate simple a simple hemodynamic hemody- –radiologicalnamic–radiological classification classification that would that would stratify stratify the grade the grade of ovarian of ovarian veins veins system system insuffi- in- ciency.sufficiency. For this For purpose, this purpose, a retrospective a retrospective analysis analysis of the resultsof the ofresults various of imagingvarious imaging exami- nationsexaminations was performed, was performed,