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1 Department of Radiology, NTT East Corporation Sapporo Hospital, W-15, S-1,
Chuo-Ku, Sapporo 0600061, Japan.
2 Department of Radiology, Hokkaido University School of Medicine, W-7, N-15,
Kita-Ku, Sapporo 0608638, Japan.
3 Department of Surgery, NTT East Corporation Sapporo Hospital, Sapporo,
0600061, Japan.
4 Department of Internal Medicine, NTT East Corporation Sapporo Hospital,
Sapporo 0600061, Japan.
Received February 7, 2004;
accepted after revision April 3, 2004.
Address correspondence to T. Hiromura
(hiromura{at}smc.mhc.east.ntt.co.jp).
Abstract
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MATERIALS AND METHODS. One hundred ten multiparous or uniparous and 41 nulliparous asymptomatic women were examined on MDCT. Degree, pathway, and associated findings of ovarian vein reflux were evaluated. We measured the diameters of the left renal vein (LRV), the ovarian veins, and the parauterine veins. Ratios of LRV diameters (lateral–aortomesenteric) were obtained. These data were then compared between the women with reflux and those without reflux.
RESULTS. Reflux was found in 44% (48/110) of parous and 5% (2/41) of nulliparous women. Reflux flowed into the right ovarian vein through the parauterine and uterine veins in 25 women. Twenty-four of these 25 women were multiparous. In these cases, the parauterine veins showed varicose dilation (5.9 ± 1.6 mm [mean ± SD]). There was a statistically significant difference in left ovarian vein diameter (8.3 ± 2.1 mm vs 4.9 ± 1.3 mm, p < 0.0001) between parous women with reflux and those without reflux, respectively. The LRV diameter ratio (lateral–aortomesenteric) was also statistically significant (3.6 ± 1.3 vs 1.7 ± 0.7, p < 0.0001) between the same two groups.
CONCLUSION. Reflux into the left ovarian vein is seen up into the contralateral ovarian plexus by passing through the dilated parauterine and uterine veins. This CT finding is common in asymptomatic multiparous women. Narrowing of the LRV at its aortomesenteric portion can be one of the causes of such reflux.
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Ovarian vein reflux is an interesting phenomenon because it can be seen to some degree in disease-free women, but it can also be a sign of disease (e.g., pelvic congestion syndrome [PCS]). PCS is characterized by chronic pelvic pain of at least 6 months' duration without any identifiable organic cause [3, 4]. Most patients with PCS are multiparous women. CT, MRI, and selective ovarian venography show incompetent dilated ovarian veins and pelvic varices [3–9]. Some authors have reported that reflux in the left ovarian vein leads to the development of pelvic varices [8, 9].
With the installation of a new generation of MDCT scanners in our hospital, it has become easier to scan the entire abdomen, from the top of the liver to the bottom of the pelvis, because of the short scanning time. We can visualize a wide range of anatomy in the same blood flow phases. Thus, both the reflux pathway and its associated findings can be assessed fully from the kidneys to the pelvic floor on MDCT. In this study, we report MDCT findings of left ovarian vein reflux in asymptomatic women and discuss the possible causes of such reflux.
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For the study subject selection, we carefully reviewed the medical records and CT images of all patients. Regarding symptoms, parity, and a history of surgery, study subjects completed a uniform questionnaire at the time of follow-up examination in our department. This questionnaire allowed us to confirm the absence of specific gynecologic and urologic symptoms (chronic pelvic pain and heaviness, vulvar varices, bladder urgency, and hematuria). The mean age of the study subjects was 56.5 years (range, 19–90 years). One hundred ten subjects were multi- or uniparous, and 41 were nulliparous women. Institutional review board approval and informed consent from the patients participating in this retrospective study were obtained.
CT Technique
Scans were obtained with an MDCT scanner (LightSpeed Ultra, GE Healthcare)
using the following technique: an 8 x 1.25 mm configuration, gantry
rotation speed of 0.5 sec, table speed of 17.5 mm per rotation, 120 kVp, and
200–220 mA. All subjects received 100 mL of low-osmolarity contrast
medium (Omnipaque [iohexol, 300 mg I/mL], Daiichi Pharmaceutical) at a rate of
2.5–3 mL/sec through a 20-gauge plastic IV catheter via a power
injector. Scanning was performed from the top of the liver to the floor of the
pelvis with inspiratory breath-holding and was started 50–80 sec after
the beginning of contrast media injection. The total acquisition time was
approximately 15 sec.
Assessment
All CT images were stored in DICOM servers. The images were independently
assessed on a liquid-crystal-display monitor by two experienced radiologists,
and conclusions were reached by consensus. Reflux into the left ovarian vein
was defined as early opacification of the ovarian vein occurring
simultaneously with opacification of the renal veins
[1].
The degree of reflux was divided into three grades. In grade I, retrograde flow remained in the left ovarian vein, not reaching the parauterine veins. In grade II, the retrograde flow advanced into the ipsilateral parauterine veins and no farther. Finally, in grade III, the retrograde flow crossed the midline passing through the uterus from the left into the right parauterine plexus (Fig. 1). The flow-pathway was assessed from the level of the kidneys to the pelvic floor.
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Diameters of the left and right ovarian veins were measured in the axial plane and compared between parous and nulliparous women. Comparison was also made between parous women with and without reflux. Anteroposterior diameters of the LRV were measured in the axial plane at two points: one, where the left ovarian vein drains into the LRV and the other, at the narrowest point that the LRV passes between the aorta and the superior mesenteric artery (Fig. 2). LRV diameter ratios (lateral–aortomesenteric) were obtained for each patient. In grade III cases, maximal diameters of the parauterine veins were measured. When measuring the diameters, we magnified images two times on the monitor, and a measuring tool was used. Each diameter was independently measured by two radiologists, and the mean values were used for analysis.
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We used a cine-mode display, in which multiple original transverse sections can be observed by scrolling the images. This method facilitated tracking the pathway of the reflux and identifying nonopacified ovarian veins.
Statistical Analysis
Statistical analysis was performed with the StatView 5.0 for Windows
(Microsoft) program (SAS Institute). Data are expressed as mean ± SD.
Differences in diameter with respect to the ovarian vein and the LRV were
tested using the unpaired Student's t test. Differences between the
LRV ratios (lateral–aortomesenteric) were tested using the Mann-Whitney
U test. A p value of less than 0.05 was considered
statistically significant.
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A vascular anomaly of the right ovarian vein, in which it drained into the right renal vein, was found in 12 women. Reflux was seen in four of these patients, all noted only in the left ovarian vein and not in the right ovarian vein.
CT Findings Associated with Grade III Reflux
In grade III reflux, flow was seen into the right ovarian vein (Fig.
3A,
3B,
3C,
3D,
3E). In these cases, the mean
diameter of the left ovarian vein and the mean ratio of LRV diameters
(lateral–aortomesenteric) were 9.5 ± 1.5 mm (range,
7.0–12.5 mm) and 3.8 ± 0.8 mm (range, 2.0–6.0 mm),
respectively. When crossing the midline, the contrast medium passed through
the parauterine and uterine veins. No other flow pathways were seen. Both the
right and left parauterine veins were tortuous and dilated in all 25 cases,
with a mean vein diameter of 5.9 ± 1.6 mm (range, 4.3–8.0 mm). No
dilation was noted in other pelvic veins.
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Diameter of the Ovarian Veins
The right and left ovarian vein diameters are summarized in
Table 1. Parous women had wider
ovarian veins than nulliparous women (for each side, p < 0.001).
In parous women, those with reflux had significantly wider left ovarian veins
than those without reflux (p < 0.0001). Patients with an anomalous
right ovarian vein that joined the right renal vein did not have dilation of
the right ovarian vein; the mean diameter was 4.1 ± 1.1 mm.
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Diameter of the LRV
Diameters of the LRV at the lateral and the aortomesenteric portions and
the ratios between the two are summarized in
Table 2. The diameter of LRV at
the aortomesenteric portion was smaller in parous women with reflux than in
those without reflux (p < 0.0001). The LRV diameter ratio was
significantly higher in parous women with reflux than in those without reflux
(p < 0.0001) (Fig.
4). The median diameter ratio for the 110 parous women was 2.1.
The incidence of reflux was 75% (41/55) in parous women with LRV ratios
greater than 2.1.
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In our study, reflux was predominantly seen in multiparous women. This result suggests that pregnancy has an effect on the development of reflux. In an autopsy study, incompetent ovarian veins were found in multiparous women more often than in uniparous or nulliparous women [10]. The dilation of ovarian veins that normally occurs during pregnancy to compensate for a 60-fold increase in blood flow [11] is a likely cause of subsequent venous incompetence [7, 10]. The autopsy study showed a frequency of left ovarian vein incompetence of 53% in multiparous women [10]. In our study, the frequency of left ovarian vein reflux (i.e., left ovarian vein incompetence) in multiparous women was 47% (42/90), which is consistent with the autopsy study data. A new finding obtained in our study was that in parous women with narrowed LRVs (diameter ratio, > 2.1), the frequency of left ovarian vein incompetence was much higher (75%) than in other parous women. Our results, together with those of previous reports on valvular incompetence, indicate that parous women tend to have left ovarian vein reflux when they have narrowed LRVs. Two nulliparous women had left ovarian vein reflux and dilatation. These two may have had a congenital absence of the venous valves, with primary venous reflux and subsequent dilatation [1].
When narrowing of the LRV at the aortomesenteric portion and collateral pathways is seen, one should suspect the nutcracker syndrome. This syndrome is characterized by intermittent gross hematuria due to LRV hypertension [12]. The syndrome has elevated venous pressure gradients of more than 1–3 mm Hg between the LRV and inferior vena cava and leads to backflow in collateral veins, including the gonadal, ascending, adrenal, periureteral, and capsular veins [13–15]. The diagnosis is suspected from findings on sonography, CT, or MRI and confirmed by retrograde renal venography combined with measurement of the pressure gradient between the LRV and the inferior vena cava [13–15]. The syndrome can cause ovarian vein reflux, pelvic varices, and symptoms of pelvic congestion [16, 17]. Our reflux series had CT findings similar to those found in the nutcracker syndrome. Why then were the patients asymptomatic? A possible explanation is that their venous pressure gradients may have been lower than those typically seen in patients with nutcracker syndrome. The mean LRV diameter ratio in our reflux series was 3.6, which is lower than the cutoff value of 5.0 for the diagnosis of the nutcracker syndrome [15]. No other collateral veins in our reflux series suggested lower pressure in the LRV.
Previous studies emphasized the incidence of reflux in asymptomatic parous women but did not address additional pelvic findings [1, 2]. Our study showed the pelvic findings associated with the reflux. In the severe reflux group (grade III), contrast medium retrogradely filled tortuous and dilated parauterine veins. These vascular findings are similar to those reported in PCS, which shows reflux and dilatation of ovarian veins and parauterine varices on CT and MRI, with dilations up to 8 mm or more and 4 mm or more, respectively [8, 18, 19]. Our patients with grade III reflux had mean diameters of 9.5 mm for the left ovarian vein and 5.9 mm for the parauterine veins; these results were consistent with those of PCS. Venography in PCS shows additional findings, such as the contrast medium crossing the midline and filling varicosities of the vulva and thighs, uterine venous engorgement, and congestion of the ovarian plexus [5, 6, 9]. In our patients with grade III reflux, contrast medium crossed the midline but did not fill other pelvic veins. As for venous congestion, we could not assess it in our subjects because we could not obtain their delayed scans in this retrospective study. Unfortunately, we had few cases of PCS in the overall study group and could not compare the CT findings of grade III reflux with those of PCS. Future studies, including such comparisons, may clarify the difference between pathologic and nonpathologic reflux. We showed earlier that our CT findings are similar to those in the nutcracker syndrome or PCS. The clinical significance of these results is that ovarian vein reflux and parauterine varices can be seen in asymptomatic parous women on CT: in other words, these findings are not specific to PCS or the nutcracker syndrome.
As for scanning-delay time of the CT examination, 20 or 30 sec was used in previous studies with a single-detector helical scanner [1, 19]. Although our delay times were 50–80 sec, which were longer than theirs [1], our left ovarian vein flows were considered to be retrograde for the following reason: Our 8-MDCT scanner completes the entire abdominal scanning within 15 sec and thus finishes the pelvic scanning 65–95 sec after the start of contrast injection. During these times, the uterus enhances in its preparenchymal phase [20], and uterine and parauterine veins are not yet opacified. In this phase, opacification of parauterine and uterine veins after left ovarian vein opacification indicates contrast flow from the left ovarian vein to the parauterine and uterine veins. Flows from the left ovarian vein in patients with grade II and III are therefore retrograde (Fig. 1). Flows into the left ovarian vein in patients with grade I are apparently retrograde (Fig. 1).
In conclusion, there were significant differences in LRV diameter and in LRV diameter ratio between reflux and nonreflux groups. Narrowing of the LRV at the aortomesenteric portion can be one of the causes of reflux. Our study gives useful clinical information. Reflux into the left ovarian vein and the associated parauterine varices is often seen in asymptomatic multiparous women. These findings may be mistaken for signs of nutcracker syndrome or PCS but are not always pathologic in multiparous women.
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  Z Koc, S Ulusan, N Tokmak, L Oguzkurt, and T Yildirim Double retroaortic left renal veins as a possible cause of pelvic congestion syndrome: imaging findings in two patients. Br. J. Radiol., October 1, 2006; 79(946): e152 - e155. [Abstract] [Full Text] [PDF]
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