Multiplanar imaging of inferior vena cavavariants

Muhammad Awais,1 Abdul Rehman,2 Noor Ul-Ain Baloch,2 Basit Salam1

1Department of Radiology, Aga Khan University Hospital, Karachi, Sindh, Pakistan2Department of Biological & Biomedical Sciences, Aga Khan University, Karachi, Sindh, Pakistan

Abstract

Inferior vena cava (IVC) variants are rare and are usuallydetected incidentally. Even though, these variants are bythemselves asymptomatic, they can have importantclinical, radiological, and surgical implications. In thispictorial essay, we sensitize the reader to various IVCvariants by presenting reports of actual patients. A suc-cinct description of the embryological development ofthese anatomic variants is also provided.

Key words: Inferior vena cava—Inferior vena cavaabnormalities—Inferior vena cavaradiography—Inferior vena cava surgery

Anomalies of the inferior vena cava (IVC) are oftenasymptomatic and are diagnosed incidentally. Theprevalence of various IVC anomalies has been reportedto be 0.07–8.7% in the general population [1]. Albeitasymptomatic, these anomalies can lead to significantmorbidity and mortality if not diagnosed properly [2].Working knowledge of the normal developmental anat-omy is crucial to understanding these abnormalities. Thisin turn has important implications in the management ofpatients with these variants and to prevent any potentialcatastrophe occurring intra-operatively. Newer imagingmodalities like multi-detector CT (MDCT) with facilitiesof 3-dimensional reformatted coronal and sagittalimaging have allowed accurate visualization of thesevariants and thorough evaluation of any associatedabnormalities. In this pictorial essay, we enumerate thediverse anatomical variants of the IVC that can occur,the embryological development which leads to the for-mation of these variants and their potential clinicalrepercussions if left undiagnosed. Emphasis has beenplaced on newer imaging modalities (like MDCT) that

have revolutionized the evaluation of these anatomicalvariants and their associated abnormalities.

Embryology

In order to understand the complex developmentalembryology of this important venous channel, it ishelpful to divide the IVC into various segments on thebasis of the primitive vessels that give rise to these seg-ments. Table 1 summarizes these segments along withtheir relevant primitive vessels. It is important to recog-nize that each of these segments develops separately andperturbations in the development of these segments leadto the formation of complex IVC variants.

IVC usually starts to develop in the sixth week ofintrauterine life from three pairs of primitive venouschannels that are formed serially. These venous conduitsundergo sequential anastomosis and regression in orderto form a composite venous channel [3]. The three pairsof precursor venous channels, in order of the timing oftheir appearance, are posterior cardinal veins, subcardi-nal veins, and supracardinal veins. All these venouschannels are formed bilaterally and usually have ap-peared by the eighth week of intrauterine life.

The first of the primitive vessels to appear are theposterior cardinal veins, which drain the caudal half ofthe fetus. Posterior cardinal veins themselves drain intothe common cardinal veins, which also receive the ante-rior cardinal veins (draining the cranial half of the body).All these venous channels eventually drain into the sinusvenosus.

Two subcardinal veins develop shortly after thedevelopment of the posterior cardinal veins. These ini-tially lie medial to the posterior cardinal veins, but,eventually replace the posterior cardinal veins for thevenous drainage of the lower half of the body. Theposterior cardinal veins gradually regress in their cranialmost parts and only their caudal most part is retained,where these are joined by the sacrocardinal veins to formthe common iliac veins.Correspondence to: Muhammad Awais; email: awais_aku@yahoo.com

ª Springer Science+Business Media New York 2014

AbdominalImaging

Abdom Imaging (2014)

DOI: 10.1007/s00261-014-0187-9

Simultaneous with the development of subcardinalveins, hepatic sinusoids also develop from the vitellineveins. These anastomose with each other and with the cra-nial aspect of the right subcardinal vein. This anastomosisbetween the developing hepatic sinusoids and the cranialmost part of the right subcardinal vein forms the hepaticportion of the IVC. Just inferior to this, the remainingcranial portion of the right subcardinal vein forms the su-pra-renal portion of the IVC. The cranial most part of theleft subcardinal vein persists as the left adrenal vein.

Concurrent to the development of hepatic sinusoids isthe development of the last pair of the primitive venouschannels—supracardinal veins. Supracardinal veinsgradually replace the caudal parts of the subcardinalvessels and overtake the venous drainage of the lowerhalf of the body. The subcardinal veins, however, persistin their caudal most extremes forming the gonadal ves-sels. The supracardinal veins are not only responsible forforming the infra-renal portion of the IVC, but also forthe formation of the renal veins, which form as a result ofthe anastomosis between the regressing subcardinal veinsand the newly developed supracardinal veins. The soformed renal veins initially appear as a pair of dorsal andventral renal veins on each side, but subsequently, thedorsal parts regress and only the ventral portions areretained as the renal veins.

To recapitulate, the embryological development ofIVC is a complex process involving the sequential for-mation, anastomosis and regression of three pairs ofvenous channels. Many classification systems have beendevised for the categorization of IVC variants based ontheir embryological development [4]. One such system isgiven in Table 1. Understanding the development of theIVC is crucial for appreciating its various variants andtheir classification.

Clinical implications

Intra-operative catastrophe

Non-recognition of IVC variants like retro-aortic orcircum-aortic renal veins can lead to significant injury

Table 1. Classification of IVC variants on the basis of primitive venous channels

Primitive vessels Embryological derivatives Anatomic variants

Posterior cardinal veins Usually regress and do not form anymajor segment of the IVC

Persistence of this channel leads to the formation of amore medially and posteriorly placed retro-cavalureter

Subcardinal veins Form the suprarenal portion ofthe IVC; their anastomosis with hepatic sinusoidslead to the formation of the hepatic portion of the IVC

Failure to develop, or regression, of these vessels canlead to an interrupted IVC with or without azygouscontinuation

If these vessels persist on the left side, they can leadto the formation of a left-sided supra-renal IVC

Supracardinal veins Form the infra-renal part of the IVC Failure of these vessels to regress on the left sideleads to the formation of a duplicated IVC

If there is persistence of these vessels on the left sidewith regression on the right side, a left-sided IVCcan occur

If these vessels fail to develop or regress bilaterally,there may be an altogether absent infra-renal IVC

Renal veins Usually formed only from the ventral divisions; theirdorsal portions regress bilaterally

Persistence of both the ventral and dorsal portionsgives rise to a circum-aortic left renal vein

If the dorsal segment persists instead of the ventralportion, it leads to the formation of a retro-aorticleft renal vein

IVC, inferior vena cava

Fig. 1. A IVC lying on the left side of the aorta with a typicalvenous wave pattern noted on pulsed Doppler. B Arterialwave pattern of the aorta demonstrated to the right of the IVC.

M. Awais et al.: Multiplanar imaging of IVC variants

to these vessels during intra-abdominal exploration.Often, these anomalous venous channels are very tor-tuous and dilated, making them even more prone toinjury during surgery. Since IVC is a major venous

conduit draining almost all of the lower half of thebody, potentially life-threatening hemorrhagecan result from iatrogenic injury to this structure[5].

Fig. 2. A Normal position of the infra-hepatic portion (yellowarrow) of the IVC as seen on axial sections. B IVC crossingthe midline just anterior to the aorta. C IVC lying to the left of

the aorta. D Reformatted coronal image demonstrating theIVC (yellow arrows) crossing to the left of the aorta (blue ar-row).

M. Awais et al.: Multiplanar imaging of IVC variants

Studies published in the past have reported aorticdissection and aortic transection occurring in cases ofunrecognized retro-aortic or circum-aortic IVC [6].Furthermore, in these patients, it becomes extremelydifficult to control bleeding from the injured aorta owingto poor control of the proximal aorta. In some instances,ureters have been misrecognized as vessels and subse-quently injured during surgery [7]. Some literature sug-

gests that extensive manipulation during abdominalsurgery in these patients can result in an increased inci-dence of post-operative pancreatitis and injury to thesurrounding major branches of abdominal aorta [8].Surgeons performing surgical procedures in such patientsshould always apply gentle traction on these vessels asextensive dissection of these structures is associated withan increased risk of complications.

Fig. 3. A Axial section demonstrating bilateral IVC (yellowarrows) on either side of the aorta. B Left-sided IVC crossingthe midline anterior to the aorta to join the right-sided IVC. C

Coronal images re-demonstrate the duplicated IVC. D Acommon right-sided IVC passing through the liver to drain intothe right atrium.

M. Awais et al.: Multiplanar imaging of IVC variants

Thromboembolic complications

A thrombus in an anatomical variant may undergounrecognized and can subsequently lead to pulmonary

embolism and cerebrovascular accidents [9–11]. In pa-tients with IVC duplication, two Greenfield filters arerequired for effective protection against thromboembo-lism; failing to recognize this variant may result in em-bolic events even after the placement of a single IVCfilter. Likewise, patients who continue to experienceembolic events following the placement of an IVC filtermay have an undiagnosed IVC duplication [12].

There are few instances in which thrombosed IVCvariants have been misdiagnosed as retroperitoneal tu-mors [13]. In one case, the azygous continuation of theIVC was misdiagnosed as dissection of the aorta and amediastinal mass lesion [14]. These cases show that it isimperative for all radiologists and surgeons to recognizethese anatomic variants to avoid wrong diagnoses andintra-operative catastrophes.

Tumor staging

Extension of renal cell carcinoma and other malignantneoplasms into IVC variants can be missed easily. Thiscan lead to erroneous tumor staging with subsequentinappropriate management and potentially grave out-comes for the patient [15]. Variations may also exist inthe lymphatic drainage along these venous variants,which may require extensive lymph node dissectionduring surgery for pelvic tumors [16, 17]. Therefore, thepossibility of neoplastic extension in to these variantsand any associated variations in the lymphatic drainageshould be thoroughly considered and accurately evalu-ated in such patients.

Common variants

In this section, we present an account of various cases,seen at our institution, of IVC anomalies.

Left-sided IVC

A 34-year-old male presented with mild pain in the righthypochondrium. Baseline laboratory investigations re-vealed a raised alanine aminotransferase level. Ultraso-nography of the liver was performed, which revealed aleft-sided IVC (Fig. 1), but, it was otherwise unremark-able. Further laboratory work-up revealed that the pa-tient had hepatitis B virus (HBV) and hepatitis E virus(HEV) co-infection as evidenced by positive HBV DNAand positive HEV antibodies. The finding of left-sidedIVC in this patient was incidental and it was picked upon ultrasonography.

Another patient, a 53-year-old male with knownhepatocellular carcinoma, had undergone transarterialchemoembolization of hepatoma at our institution. Afollow-up CT scan was performed, which was the firstscan of this patient at our institution. Again, there wasan incidental finding of left-sided IVC, accurately iden-

Fig. 4. A Duplication of IVC noted on an axial section (yel-low arrows). B The left-sided IVC passing posterior to theaorta to drain into the right-sided IVC. C Absence of the intra-hepatic portion of the IVC along with a prominent azygousvein (blue arrow) just to the right of the aorta behind the rightcrus of diaphragm.

M. Awais et al.: Multiplanar imaging of IVC variants

tified on multiplanar CT examination. The completeextent and relationship of this variant with otherimportant structures could be easily appreciated on themultiplanar images (Fig. 2).

Duplication of IVC

A 50-year-old lady with a history of ovarian carcinomasuddenly developed shortness of breath. A CT scan wasperformed for the evaluation of possible pulmonaryembolism and/or progression of disease. On this scan, anincidental finding of duplication of IVC was identified(Fig. 3). In this case, documentation of duplication ofIVC was important as the patient may require two IVCfilters for protection against pulmonary embolism.

However, the patient did not have any evidence of pul-monary embolism or deep vein thrombosis.

Interrupted right-sided IVC with azygouscontinuation

A 28-years-old man presented with complaints of peri-umbilical abdominal pain, which had now shifted to theright iliac fossa. Associated right iliac fossa tendernessand leukocytosis were noted on laboratory investiga-tions. A CT scan was performed with the clinical suspi-cion of acute appendicitis. In this patient, an incidentalfinding of interrupted right-sided IVC with azygouscontinuation was noted (Fig. 4). The importance ofdocumenting this finding pre-operatively in this case is

Fig. 5. A IVC identified to the left of the aorta (yellow arrow)on this axial section; associated findings include midline liver,multiple spleens, and right-sided stomach. B Absence of theleft-sided IVC on this section suggests interruption of the IVC;a prominent azygous vein, just to the left of the aorta, repre-

sents an azygous continuation. C Coronal section re-dem-onstrating a left-sided IVC, which becomes attenuated justbelow the left hemi-diaphragm. D A prominent azygous vein,instead of the IVC, is located posterior to the aorta (pinkarrow).

M. Awais et al.: Multiplanar imaging of IVC variants

that the interrupted right-sided IVC might be confusedwith post-operative collection or lymphadenopathy onsubsequent scans.

Interrupted left-sided IVC with azygouscontinuation

A 15-years-old boy was brought for the evaluation ofcomplex congenital heart disease. Trans-thoracic echo-cardiography was performed, which revealed situs inver-sus with levocardia and an unbalanced completeatrioventricular septal defect. A single ventricle of rightventricular morphology was identified with double out-flow tract and a large patent ductus arteriosus. CT angi-ography was requested for delineation of the complexanatomy, which revealed an interrupted left-sided IVCwith azygous vein continuation on the left side (Fig. 5). Inthis patient, accurate delineation of anatomy was neces-sary for subsequent planning of surgical management.

Circum-aortic left renal vein

A 24-years-old lady presented with complaints of painand swelling in the right knee for the past 6 months. A

plain radiograph of the right knee joint was obtainedfollowed by an MRI. Based on the radiographicappearances, there was a strong suspicion of giant celltumor. Patient then underwent a CT examination aspart of staging work-up, which revealed multiple en-larged para-aortic lymph nodes and lung metastases.There was also an incidental finding of circum-aorticleft renal vein in this patient (Fig. 6). Again, thisimportant finding if left undiagnosed could lead tosignificant morbidity during any subsequent abdominalsurgery.

Retrocaval ureter

A 60-year-old woman presented with lower urinary tractsymptoms. An intravenous pyelogram was obtained todetect any possible renal abnormalities. On this exami-nation, kinking of the right ureter was noted at the levelof the lower pole of the right kidney along with proximalhydroureter and hydronephrosis. The lower mid-portionof the ureter seemed more medial than usual suggestiveof a retro-caval position of the ureter along with mildproximal obstruction.

Fig. 6. A A persistent dorsal left renal vein (blue arrow)noted on this axial section, in addition to the normal (ventral)left renal vein (yellow arrow); the ventral left renal vein passesanterior to the aorta to drain into the IVC. B The dorsal left

renal vein passing posteriorly to the aorta to drain into theIVC. C Sagittal images demonstrating a circum-aortic collar(pink arrow) formed by the ventral and dorsal left renal veins.

M. Awais et al.: Multiplanar imaging of IVC variants

Conclusion

Understanding the embryological development of theIVC is crucial to appreciate its various anatomic vari-ants. It is imperative for all radiologists and surgeons tobe able to recognize these anatomic variants as aninability to do so can result in potentially lethal intra-operative catastrophes.

Conflict of interests The authors of this manuscript declare no conflictof interests regarding the findings reported herein.

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M. Awais et al.: Multiplanar imaging of IVC variants