The Egyptian Journal of Radiology and Nuclear Medicine (2016) 47, 883–890

Egyptian Society of Radiology and Nuclear Medicine The Egyptian Journal of Radiology and Nuclear Medicine

www.elsevier.com/locate/ejrnm www.sciencedirect.com

ORIGINAL ARTICLE Congenital anomalies of the inferior vena cava and iliac : A cross-sectional study by multi-detector computed tomography

Mohamed Samir Shaaban *

Diagnostic and Interventional Radiology Department, Faculty of Medicine, Alexandria University, Egypt

Received 29 February 2016; accepted 4 May 2016 Available online 26 May 2016

KEYWORDS Abstract Purpose: To study the prevalence of the anomalies of inferior vena cava and iliac veins IVC; branching patterns by multi-detector CT. Iliac veins; Materials and methods: Retrospective analysis of the images of 1167 patients who underwent Anomalies; contrast-enhanced MDCT examination of the and during the period from first Variations; of November 2014 to the 31st of October 2015, with recording of the detected IVC and iliac veins MDCT branching patterns anomalies. Results: Of 1167 patients who underwent imaging, 1144 were included in the study. They included 571 males (50%) and 573 (50%) females, ages ranged from one year old to 90 years old, with a mean of 49.7 years (±16.3). 918 patients (80%) had normal IVC and normal iliac veins branching pat- tern, 110 cases showed isolated IVC anomalies with normal iliac veins branching pattern (49%), 110 showed isolated iliac veins branching anomalies (49%), and six patients showed combined IVC and iliac veins anomalies (2%). No statistically significant sex correlation with the anomalies was found. Conclusion: Multi-detector CT can display different anomalies and variations in IVC and the iliac , findings of potential clinical and operative importance in abdominal and pelvic surgeries. Ó 2016 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc- nd/4.0/).

1. Introduction shunt and azygos continuation of the IVC in a child with com- plex cardiac anomalies (1). Congenital anomalies of the IVC Anomalies of the IVC have been first described by Abernethy have been counted to be about 14 in number; however, only in 1793 when he described a case of congenital mesocaval few anomalies have clinical significance such as relatively high rate of thromboembolic accidents and ureteric obstruction (1–3). IVC anomalies can also affect surgical or endoscopic * Address: 27 Ahmad Foad Nour Str., Camp Caesar, Alexandria interventions to abdominal or pelvic pathologies (4,5). 21525, Egypt. Tel.: +20 (003)01001948320. Embryological origin of the inferior vena cava (IVC) is E-mail address: [email protected]. complex and included appearance and disappearance of multi- Peer review under responsibility of The Egyptian Society of Radiology and Nuclear Medicine. ple abdominal and thoracoabdominal veins during the sixth to http://dx.doi.org/10.1016/j.ejrnm.2016.05.003 0378-603X Ó 2016 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 884 M.S. Shaaban tenth week of gestation (1). During the 4th week of fetal life, Table 1 Correlation between patients sex and the IVC paired posterior cardinal veins drain the caudal portion of anomalies. the embryo. These veins are progressively replaced, first by the sub-cardinal veins and later by the supra-cardinal veins. Sex IVC The hepatic IVC is formed by the right vitelline vein. The anomaly suprarenal IVC is formed by the right sub-cardinal vein, while Spearman’s Sex Correlation 1.000 .021 the infra renal IVC is formed by the right supra-cardinal vein. rho coefficient Anastomotic veins between the supra-cardinal and sub- Sig. (2-tailed) . .487 cardinal veins form the renal segment of the IVC. Caudally, IVC Correlation .021 1.000 the persistent posterior cardinal veins form the iliac veins anomaly coefficient Sig. (2-tailed) .487 . (6,7) Fig. 1. Typically the normal IVC extends from the right atrium of Significant if P < 0.05. the heart downward to the right to the midline alongside the abdominal aorta, down to the level of LV5 where it bifurcates into a common on each side, each Retrocaval , Absence of the Infrarenal IVC, Retroaortic then divides into an internal and an (8). Con- and Circumaortic Left , and interruption of the genital anomalies of the IVC include Left IVC, Double IVC, IVC with Azygous or Hemiazygos Continuation (7).

Fig. 1 Drawing illustrates the embryologic development of the IVC. Three pairs of veins – the posterior cardinal (blue), subcardinal (vertical red), and supracardinal (purple) veins – develop in succession on either side of the aorta (gray). Portions of these venous channels regress (dashed colored lines), whereas others persist (solid colored lines) to form the infrahepatic IVC. The right subcardinal vein forms the suprarenal segment of the IVC, and the right supracardinal vein forms the infrarenal segment. The hepatic segment is derived from the vitelline vein (green). Anastomotic channels (black) connect the various segments of the IVC. An intersubcardinal anastomosis that passes anterior to the aorta forms the left renal vein (horizontal red line), whereas intersupracardinal and interposterior cardinal anastomoses normally regress. The supracardinal veins continue as the azygous and hemiazygos veins; the iliac veins are derived from the persistent posterior cardinal veins. AN = anastomosis, V = vein. Congenital anomalies of the inferior vena cava and iliac veins 885

Table 2 Correlation between patient sex and iliac veins anomalies. Sex Iliac veins anomaly Spearman’s rho Sex Correlation coefficient 1.000 À.163 Sig. (2-tailed) . .083 Iliac veins anomaly Correlation coefficient À.163 1.000 Sig. (2-tailed) .083 . Significant if P < 0.05.

Table 3 Relative frequencies of the IVC anomalies in the studied group. IVC anomaly Number Percentage within Percentage within all the IVC anomalies (%) studied population (%) Circum-aortic left renal vain 58 50 5.07 Retro-aortic left renal vein 46 40 4.02 Left sided IVC 4 3 0.35 Fenestrated IVC 3 2.5 0.26 Retro-caval ureter 3 2.5 0.26 Double IVC 2 2 0.17 Total 116 100% 10.14

Fig. 2 Axial contrast-enhanced CT with thin MIP reformatting in axial (a) and sagittal (b) planes, showing circum-aortic left renal vein encircling the abdominal aorta anteriorly (yellow arrow) and posteriorly (green arrow).

Fig. 3 Axial contrast-enhanced CT with thin MIP reformatting in axial (a) and sagittal (b) planes, showing retro-aortic left renal vein (blue arrow) passing posterior to the abdominal aorta. 886 M.S. Shaaban

Fig. 4 Coronal contrast-enhanced CT with thin MIP reformatting in axial plane (a) with the corresponding coronal VRT clip (b), showing left sided IVC (yellow arrow) crossing to the left side of the abdominal aorta (green arrow).

3. Patients and methods

3.1. Patients

This retrospective study was approved by the institutional review board of our hospital, and the requirements for informed consent were waived. CT scans of all patients who had been referred to undergo contrast-enhanced MDCT of the abdomen and pelvis regions, during the period from the first of November 2014 to the 31st of October 2015 were retrospectively reviewed, by a senior consultant radiologist with 10 years experience in abdominal imaging, with recording of the detected IVC and iliac veins branching patterns anomalies.

3.2. CT protocol

Fig. 5 Coronal contrast-enhanced CT in the abdomen, showing CT examinations were performed with 4 detectors CT scanner small fenestration within the IVC (yellow arrow) just above its (bright speed, GE Healthcare, Milwaukee, Wisconsin, USA), bifurcation. 16 detectors CT scanner (Brilliance, Philips Medical Systems, Amsterdam, the Netherlands), and 46 detectors CT scanner (Siemens Perspective, Erlangen, Germany). All patients received an intravenous dose of contrast med- With the widespread use of imaging techniques, especially ium (iohexol, 300 mg I/mL – Omnipaque 300, GE Healthcare), computed tomography (CT), incidentally discovered IVC with variable rate and amount, according to patient age, anomalies have increased, and recognition and reporting of weight and CT examination. Slice thickness of the CT scans such anomalies have been proposed to decrease complications ranged from 1 to 1.5 mm. in abdominal surgeries, especially related to the kidneys, and a Images were reviewed on Osirix Lite 7 software in Multi- detailed knowledge of these anomalies is crucial for IVC filter planar reformatting, Maximal intensity projection and Volume placement, spermatic vein embolization, and adrenal or renal rendering techniques. venous sampling (9–11). 3.3. Inclusion criteria 2. Aim of work All patients underwent a contrast CT study of the abdomen The aim of this work was to study the prevalence of the and pelvis that entailed enhancement of the IVC from the right anomalies of inferior vena cava and iliac veins branching atrium to the bifurcation of the common iliac vessels, regard- patterns by multi-detector CT. less of the indications and technique of the CT examination. Congenital anomalies of the inferior vena cava and iliac veins 887

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Fig. 6 25-year old female patient with right hydronephrosis. CT examination of the abdomen and pelvis in delayed post-contrast phase at the level of the kidneys (a), at LV4, and at LV5 showing moderate right hydronephrosis (a), with the ureter (yellow arrow) passing posterior to the IVC (b) to run medial to it (c). (d) Coronal contrast-enhanced CT in the abdomen in MIP reformatting showing retro- caval right ureter with backpressure effect.

Fig. 7 Axial (a) and coronal (b) contrast-enhanced CT, showing double IVC (yellow and green arrows).

3.4. Exclusion criteria 4. Results

Patients who did not receive IV contrast opacifying the IVC CT scans of 1167 patients were retrieved. 23 cases were and iliac veins, patients with mass lesions grossly infiltrating excluded from the study due to renal congenital anomalies the IVC and/or iliac veins, the presence of congenital renal (n = 14), lymphoma with massive lymphadenopathy com- anomalies, and patients who underwent abdominal surgery pressing the IVC and iliac veins (n = 5), complete situs inver- that changed the anatomy of the IVC and/or iliac veins. sus (n = 2) and two cases of large retroperitoneal pelvic masses markedly compressing the iliac veins. 3.5. Statistical analysis 1144 were included in the study. Patients were 571 males (50%) and 573 (50%) females, ages ranged from one year to Data were analyzed using IBM SPSS 20. Relative frequencies, 90 years, with a mean of 49.7 years (±16.3). means and standard deviations were calculated. Correlation CT examinations included in this study were 364 routine between the sex and various anomalies was performed by CT Abdomen and Pelvis (32%), 325 Triphasic Liver CT (28%), Spearman Correlation test. 246 CT Urography (22%), 170 CT Entero-colonography 888 M.S. Shaaban

Fig. 8 Coronal contrast-enhanced CT (a) with the corresponding coronal VRT image (b), showing the left renal vein (yellow arrow) draining into the left common iliac vein (green arrow).

(15%), 25 Multiphasic Pancreas (2%), nine CT Aortography (0.5%) and five Dynamic Adrenal CT (0.5%). 918 of the cases showed the normal typical anatomy of the IVC and its normal branching into two common iliac veins, each in turn branching into an external and an internal iliac vein, constituting 80% of all 1144 cases included in this study. Of the 226 cases which showed IVC and/or iliac veins anomalies, 110 cases showed isolated IVC anomalies with nor- mal iliac veins branching pattern (49%), 110 showed isolated iliac veins branching anomalies (49%), and six patients showed combined IVC and iliac veins anomalies (2%). There was no significant correlation between the sex and the IVC anomalies (Table 1), or the iliac vein anomalies (Table 2). Table 3 displays the IVC anomalies found in the studied group and their relative frequencies, the most common of IVC anomalies was circum-aortic left renal vein (n = 58), con- stituting 50% of all IVC anomalies and 5.07% of the studied Fig. 9 Coronal contrast-enhanced CT, showing the left internal population (Fig. 2), followed by retro-aortic left renal vein iliac vein (yellow arrow) drains into the right common iliac vein. (n = 46), 40% of all IVC anomalies and 4.02% of the studied population (Fig. 3), other IVC anomalies included left sided IVC (3%) (Fig. 4), fenestrated IVC just above its bifurcation (2.5%) (Fig. 5), retrocaval ureter (2.5%) (Fig. 6) and double IVC (2%) (Fig. 7). Regarding anomalies of iliac veins, they were divided into three categories: the first was unilateral anomalies where anomalous branching was found in one side in 46 cases (40%) (Fig. 8), bilateral anomalies in which anomalous branching pattern was found in both sides in eight cases (7%), and anomalies connecting the two sides with each other in 62 cases (53%) (Figs. 9 and 10). Table 4 displays the differ- ent types of iliac veins anomalies. Regarding the 6 cases with concomitant IVC and iliac veins anomalies, the most IVC anomaly was retro-aortic left renal vein in 3 cases (50%), while no iliac vein anomaly was repre- sented more than once in the study sample Table 5.

5. Discussion

IVC and iliac vein congenital anomalies are complex and may Fig. 10 Coronal contrast-enhanced CT, showing the right imply clinical and surgical significance. This was found in a internal iliac vein (yellow arrow) drains into the left common number of studies reporting cases with congenital anomalies iliac vein. were correlated with venous varices in a child (Lesanu et al. Congenital anomalies of the inferior vena cava and iliac veins 889

Table 4 Relative frequencies of the iliac veins anomalies in the studied group. Category Iliac veins anomaly Number Percentage (%) Anomalies Some branches of the right internal iliac vein drain into left common iliac vein 19 16 connecting both sides The left internal iliac vein completely drains into the right common iliac vein 11 9 Some tributaries of the left internal iliac vein drain into right common iliac vein 8 7 The right internal iliac vein completely drains into the left common iliac vein 24 21 Total 62 53 Bilateral anomalies Some tributaries of each internal iliac vein drain into the ipsilateral external iliac vein 4 3 Both internal iliac veins completely directly drain into the IVC 3 3 An anomalous vein connects the left external and left internal iliac veins, and some tributaries 11 from the right internal iliac vein drain into the right external iliac vein Total 87 Unilateral anomalies Fenestrated left common iliac vein 2 2 The left renal vein drain into the left common iliac vein 1 1 Some tributaries of the left internal iliac vein drain into the left common iliac vein 2 2 Some tributaries of the left internal iliac vein drain into the left external iliac vein 10 9 The left internal iliac vein directly drains into the IVC 1 1 Agenesis of the left common iliac vein 1 1 Some tributaries of the right internal iliac vein drain into the right common iliac vein 2 2 Some tributaries of the right internal iliac vein drain into the right external iliac vein 14 12 The right internal iliac vein directly drains into the IVC 4 3 Anomalous vein connecting the left external and left internal iliac veins 5 4 Anomalous vein connecting the right external and right internal iliac veins 3 3 The left internal iliac vein directly drains into the IVC, with some of its tributaries originating 11 from the left external iliac vein Total 46 40

the current study IVC anomalies in the current study were pre- Table 5 Frequencies of the concomitant IVC and iliac veins sent in 10.14% of the studied population. Smillie et al. (18) and anomalies in the studied group. Bass et al. (19), both stated the prevalence of duplication of the Concomitant IVC and iliac veins anomalies Number IVC, left-sided IVC, and azygos continuation of the IVC as Circum-aortic left renal vein – some branches of the 1 0.2–0.3%, 0.2–0.5%, and 0.6% respectively. Bass et al. (19) internal iliac veins bilaterally drain into the ipsilateral stated the prevalence of circum-aortic left renal vein and external iliac vein retro-aortic left renal vein as 8.7% and 2.1% respectively. In Circum-aortic left renal vein – some branches of the left 1 the current study, the incidence of left-sided IVC, azygos internal iliac vein drain into the left external iliac vein continuation of the IVC, circum-aortic left renal vein, and Left sided IVC – left internal iliac vein completely drain 1 retro-aortic left renal vein were 0.35%, 0.17%, 5.07%, and into the right common iliac vein 4.02% respectively. Retro-aortic left renal vein – an anomalous vein 1 Regarding the iliac vein anomalies, Shin et al. (20) showed connects the left CIV and the Left renal vein Retro-aortic left renal vein – left internal iliac vein 1 iliac vein variation prevalence of 20.9%, while in the current completely drain into the right common iliac vein study, iliac vein anomalies were present in only 4% of the Retro-aortic left renal vein – right internal iliac vein 1 studied population. In Shin et al. (20), the prevalence of right directly drain into the IVC internal iliac vein joining the left common iliac vein was 2.1%, left internal iliac vein joining the right common iliac vein 0.2%, and Common iliac vein fenestration 0.4%. In the current study, the prevalence of right internal iliac vein joining the left (12)), deep iliac vein (Sarlon et al. (13)), and common iliac vein was 2%, left internal iliac vein joining the ureteric obstruction (Shin et al. (14), Basok et al. (15) and right common iliac vein 1%, and Common iliac vein fenestra- Abraham et al. (16)). Strauss et al. (17) concluded that aware- tion 0.1%. The results of Shin et al. (20) and the current study ness of retroperitoneal abnormal vessels is crucial to avoid are near matched, despite the different sample size in both diagnostic pitfalls and intraoperative complications. studies (2488 in Shin et al. (20), and 1144 in the current study). The current study did not correlate between venous anoma- lies and the clinical or operative implications; however, three 6. Conclusion of the cases had retro-caval right , with consequent backpressure effect. Multi-detector CT can display different anomalies and Regarding the incidence of the congenital anomalies of variations in IVC and the iliac vein, and findings of potential IVC, a review article by Smillie et al. (18) stated that IVC clinical and operative importance in abdominal and pelvic anomalies are present in about 4% of population, while in surgeries. 890 M.S. Shaaban

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