European Journal of Radiology 85 (2016) 1695–1700

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European Journal of Radiology

journal homepage: www.elsevier.com/locate/ejrad

Intestinal malrotation in patients with situs anomaly: Implication of

the relative positions of the superior mesenteric artery and vein
Kyu Sung Choi (M.D.) a , Young Hun Choi (M.D.) a,b,∗,1 , Jung-Eun Cheon (M.D.) a,b,c ,
Woo Sun Kim (M.D.) a,b,c , In One Kim (M.D.) a,b,c
a
Department of Radiology, Seoul National University Hospital, Republic of Korea
b
Department of Radiology, Seoul National University College of Medicine, Republic of Korea
c
Institute of Radiation Medicine, Seoul National University Medical Research Center, Republic of Korea

a r t i c l e i n f o a b s t r a c t

Article history: Purpose: To assess the usefulness of the relative position of the superior mesenteric artery (SMA) and
Received 13 June 2016 superior mesenteric vein (SMV) in diagnosing intestinal malrotation in situs anomaly.
Received in revised form 15 July 2016 Materials and methods: From January 2004 to April 2015, 33 patients with situs anomalies were enrolled
Accepted 19 July 2016
in this study who underwent abdominal USG, CT or MRI as well as upper gastrointestinal series (UGIS) or
surgery: situs inversus (n = 16), left isomerism (n = 10), and right isomerism (n = 7); age 21.2 ± 23.2 years
Keywords:
(mean ± standard deviation), range 0–72 years. The intestinal malrotation was confirmed with UGIS
Situs ambiguus
and/or operation in 16 patients. Relative positions of the SMV to the SMA were classified into four groups
Heterotaxy syndrome
Intestinal malrotation
by reviewing abdominal USG, CT, or MRI: right sided, left sided, ventral sided, and dorsal sided. The
Superior mesenteric artery incidence of malrotation was analyzed for each group.
Intestinal volvulus Results: In 16 patients with situs inversus, there was reversed SMA-SMV relationship: left sided (n = 11)
or ventral sided (n = 5). One situs inversus patient with ventral sided SMV had intestinal malrotation
(6.25%). 17 patients with situs ambiguus showed various SMA-SMV relationships (ventral sided, n = 7;
left sided, n = 5; right sided, n = 4; dorsal sided, n = 1). Among them, 15 patients (88.2%) had intestinal
malrotation. Two patients with normal rotation had either right sided or dorsal sided SMV.
Conclusion: Situs ambiguus was commonly associated with intestinal malrotation with a variable SMA-
SMV relationship. Reversal of the mesenteric vascular relationship was observed in situs inversus with
normal rotation, not excluding the possibility of intestinal malrotation.
© 2016 Published by Elsevier Ireland Ltd.

1. Introduction Situs refers to the arrangement of organs, such as the lungs,

It is well-established that an abnormal relative position of the
superior mesenteric vein and artery can be present in patients with
intestinal malrotation [1]. Intestinal malrotation is a potentially life
threatening condition when complicated with midgut volvulus or
associated with intestinal obstruction due to the presence of Ladd’s
bands.
Abbreviations: USG, ultrasonography; CT, computed tomography; MRI, magnetic
resonance imaging; UGIS, upper gastrointestinal series; SMA, superior mesenteric
artery; SMV, superior mesenteric vein.
∗ Corresponding author at: Department of Radiology, Seoul National University
Hospital, 101 Daehak-ro, Jongno-gu, Seoul, 110-744, Republic of Korea.
E-mail address: iater@snu.ac.kr (Y.H. Choi).
1
Department of Radiology, Seoul National University College of Medicine, 103
Daehak-ro, Jongno-gu, Seoul, 110-799, Republic of Korea.
liver, spleen, and atria in reference to the midline, i.e., the right-
left relationship of the organ arrangement. Situs inversus refers
to the reversed right-left relationship of the organ arrangement.
Situs ambiguus, i.e. heterotaxy refers to the arrangement of the
organs that is neither situs solitus nor situs inversus. Heterotaxy
is characterized by symmetric arrangement of some body organs
such as airway, branch pulmonary arteries and atrial appendages.
Therefore, heterotaxy is divided into heterotaxy with right iso-
merism and heterotaxy with left isomerism, where isomerism is
defined as symmetrical arrangement of organs that are normally
asymmetrical [2,3]. Although situs ambiguus is not a common
congenital anomaly (incidence of 0.01%) [4–6], it is known to be
frequently associated with intestinal malrotation (40–90%) [2,4,7].
Therefore, it is important to identify radiological clues to diagnose
intestinal malrotation in patients with situs anomaly. Thorough
evaluation for a complete retroperitoneal course of the duodenum
and the lower abdominal positioning of the cecum producing a

http://dx.doi.org/10.1016/j.ejrad.2016.07.013
0720-048X/© 2016 Published by Elsevier Ireland Ltd.
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sufficiently broad mesenteric base is required in order to safely
exclude intestinal malrotation [8]. However, such evaluation can be
difficult and require additional studies such as fluoroscopic stud-
ies or even surgery. In clinical practice, the relationship between
the superior mesenteric artery and vein has been used as a use-
ful initial clue to evaluate abnormalities of intestinal rotation in
patients with normal situs because it is easy to evaluate on USG
or other tomographic studies, although false positive or false neg-
ative cases can be present [1,9]. To our knowledge, there has been
no comprehensive study about the relative position of the supe-
rior mesenteric artery and vein as well as the association between
intestinal malrotation and the relative position of the mesenteric
vessels in patients with abnormal situs. Therefore, the purpose of
this retrospective study was to assess the usefulness of the rel-
ative relationship between the superior mesenteric artery (SMA)
and superior mesenteric vein (SMV) for predicting the intestinal
malrotation in patients with situs anomalies.
2. Materials and methods
The Institutional Review Board of Seoul National University Hos-
pital approved this retrospective observational study and waived
the requirement for patient informed consent.
2.1. Patients
In order to identify patients with situs anomaly, we searched
the radiology reports database from January 2004 to April 2015.
USG, CT or MRI examinations with any of the following key-
words in their final reports were investigated; “situs”; “isomerism”;
“heterotaxia”; “polysplenia”; “asplenia”; and “inferior vena cava
interruption”. From this search; 1918 patients were found. Among
them; only 39 patients underwent gastrointestinal series (UGIS);
which is a fluoroscopic examination of upper gastrointestinal tract;
and/or abdominal surgery; from which intestinal rotation status
could be confirmed. Among 39 patients; 6 patients were excluded
from the study; as the relative positions of the SMA and the SMV
could not be adequately evaluated on USG; CT or MR images.
Finally; 33 eligible patients comprised the study cohort (20 male
and 13 female; mean age 21.2 ± 23.2 years; range 0–72 years).
2.2. Situs anomaly
Two radiologists (C.K.S and C.Y.H) identified the type of situs
anomaly for each of the 33 patients, in consensus, by review-
ing the findings of all available imaging studies, including chest
radiography, USG, CT and MRI. Situs anomaly was divided into
two groups: situs inversus, and situs ambiguus. Situs inversus
was defined when the normal organs such as lungs, liver, spleen,
and atria were positioned reversed (i.e. reversed arrangement of
organs) [2]. Situs ambiguus was subdivided into two groups: right-
sided isomerism (asplenia) and left-sided isomerism (polysplenia),
where isomerism indicates the symmetrical arrangement of organs
that are typically asymmetrical. Right isomerism was defined when
bilateral right-sidedness, including bilateral ‘right’ lungs and atria,
and absence of the spleen was noted. Left isomerism was defined
by a tendency towards bilateral left-sidedness with bilateral ‘left’
lungs and atria, and multiple spleens were noted [3].
2.3. Intestinal malrotation
The presence of intestinal malrotation was identified by eval-
uating findings from fluoroscopic studies and/or surgery. In 26
patients, UGIS was performed in the standardized way, with both
lateral and AP views on each patient, using barium as contrast
media. The same two radiologists reviewed UGIS retrospectively to
Fig. 1. Classification diagram for the relative position of the SMV to SMA.
determine the intestinal rotation status of each patient. Intestinal
rotation was considered normal when the duodenojejunal junction
(ligament of Treitz) was located laterally to the ipsilateral verte-
bral pedicle with the stomach and at the level of the duodenal bulb
and the cecum was located in the lower abdomen contralateral to
the duoduenojejunal junction. In all other cases, intestinal arrange-
ment was considered malrotated [2]. In 10 patients, surgery was
performed and the intestinal rotation status determined based on
the surgical findings.
2.4. Relative position of the SMV and SMA
Normal relative position of the SMV to SMA was defined when
the SMV is located at 9–11 o’clock relative to the SMA [1]. The rel-
ative position of the SMV to the SMA was determined at the level
of the proximal SMA and SMV by reviewing the images from the
abdominal USG (n = 10), CT (n = 22) and/or MR (n = 1). The relative
position of the SMV to SMA was divided into four groups: [1] ven-
tral, when the SMV is located at 11–1 o’clock relative to the SMA;
[2] right sided, when the SMV is located at 9–11 o’clock relative to
the SMA; [3] left sided, when the SMV is located at 1–3 o’clock rela-
tive to the SMA; and [4] dorsal, when SMV is located at 3–9 o’clock
relative to the SMA (Fig. 1). We evaluated the association between
the relative position of the SMA to the SMV with the presence of
intestinal malrotation in patients with situs anomaly.
2.5. Statistical analysis
Fisher’s exact test was performed to analyze association
between intestinal malrotation and situs anomalies (i.e. situs inver-
sus and ambiguus). All statistical analyses were performed with
commercially available software, SPSS 21.0 for Windows (SPSS Inc,
Chicago, IL, USA). P < 0.05 was considered to indicate a significant
difference.
3. Results
3.1. Types of situs anomaly
In 33 patients with situs anomaly, 16 patients exhibited situs
inversus (Fig. 2), with the other 17 patients having situs ambiguus
(Fig. 3). Among those exhibiting situs ambiguus, 7 patients had right
isomerism, and the other 10 patients had left isomerism.
3.2. Association of malrotation with situs anomaly
Intestinal malrotation was confirmed in 16 out of 33 patients
with a situs anomaly. In 6, the diagnosis was based on UGIS alone,
in 3 on the combination of UGIS and surgical findings while the
remaining 7 patients were operated without UGIS and the diagnosis
was surgically confirmed.
Among the 16 patients with situs inversus, 15 patients had
normal rotation (93.75%), and only 1 patient (6.25%) exhibited mal-
 K.S. Choi et al. / European Journal of Radiology 85 (2016) 1695–1700 1697

Fig. 2. An 11-year old female patient with situs inversus.

(a) On the axial image of the upper abdomen included in a cardiac CT, the stomach and spleen are located on the right side, while the liver and IVC are located on the left
side, as typically observed with situs inversus. (b,c) Intestinal rotation is normal, as shown on UGIS. The duodenojejunal junction (arrowhead) is located on the right side of
the spine, ipsilateral to the stomach. The cecum and appendix (thick arrow) are located in the left lower quadrant. (d) The SMV (dotted arrow) is located to the left of the
SMA (arrow) on USG.

Table 1 exhibited a dorsal sided or right sided position of the SMV, respec-
Association of malrotation with situs anomaly.
tively (Fig. 4).
Normal rotation Malrotation

Situs inversus (n = 16) 15 (93.75%) 1 (6.25%)

Situs ambiguus (n = 17) 2 (11.8%) 15 (88.2%)
Right isomerism (n = 7) 1 (5.9%) 6 (35.3%)
Left isomerism (n = 10) 1 (5.9%) 9 (52.9%)
rotation (Table 1). Among the 17 patients with situs ambiguus,
15 patients had malrotation (88.2%), with the other 2 patients
exhibiting normal rotation (11.8%) (Table 1). Presence of situs
ambiguus was significantly associated with intestinal malrotation,
when compared to those with situs inversus (P < 0.001).
3.3. Relative positions of the SMV to the SMA in situs anomaly
Of the 16 patients with situs inversus, the SMV was left sided
relative to the SMA in 12 patients (75%), and dorsal sided relative to
the SMA in 4 patients (25%). In the 17 patients with situs ambiguus,
various mesenteric vascular relationships were observed (ventral,
n = 7; left sided, n = 5; right sided, n = 4; dorsal, n = 1) (Table 2).
The single patient exhibiting situs inversus and intestinal mal-
rotation had the SMV located left sided relative to the SMA on USG.
The 2 patients with normal rotation and right or left isomerism
4. Discussion
Even though intestinal malrotation does not necessarily mean
that the patient will develop intestinal obstruction associated with
volvulus, volvulus can be life-threatening once it develops. There-
fore, early diagnosis of intestinal malrotation is important and
our study was intended to reveal whether SMA-SMV relationship
could be a helpful clue for the diagnosis of intestinal malrotation
in patients with situs anomaly. Our study reveals that the expected
presence of inverse relationship of mesenteric vessels in patients
with situs inversus is usually not associated with intestinal malro-
tation but cannot exclude malrotation. Moreover, situs ambiguus
usually coexisted with intestinal malrotation as expected [7,10].
However, variable relationships of mesenteric vessels in patients
with situs ambiguus cannot confirm or exclude intestinal malrota-
tion in this group of patients.
In patients with situs solitus (i.e. normal situs), it is well-
established that reversal of the SMA-SMV relationship can be
associated with the intestinal malrotation [1]. However, most
of previous studies on situs anomaly, especially situs ambiguus,
reported on the anatomical differences of other internal organs,
specifically the liver, spleen, and vascular structures, such as the
1698 K.S. Choi et al. / European Journal of Radiology 85 (2016) 1695–1700

Fig. 3. A 10-month old male patient with right isomerism and intestinal malrotation.
(a,b) The cardiac CT performed for evaluation of congenital heart disease reveals bilateral right bronchi, a right-sided stomach (marked as ‘s’). (c) On the anteroposterior view
from a UGIS, the duodenum (arrowhead) does not cross midline and the proximal jejunal loops are located in the right abdomen. Hiatal hernia was incidentally detected.
(d,e) on the anteoposterior and lateral 18-h delayed images of the abdomen, the cecum (arrowheads) and appendix are located in the right upper quadrant and not in the
retroperitoneal location. (f) The SMV is located ventral to the SMA on USG.
 K.S. Choi et al. / European Journal of Radiology 85 (2016) 1695–1700
Table 2
Relative positions of the SMV to the SMA in situs anomaly.
Relative position of the SMV to SMA Ventral
Situs inversus (n = 16) 4 (25.0%)
Situs ambiguus (n = 17) 7 (41.2%)
Right isomerism (n = 7) 3 (17.6%)
Left isomerism (n = 10) 4 (23.6%)
Fig. 4. Relative position of the SMV to SMA in patients with normal intestinal rotation or malrotation in (a) situs inversus, (b) right isomerism, and (c) left isomerism.
inferior vena cava (IVC) or azygos/hemiazygos veins [10–13], but
have not examined the SMA-SMV relationship. Only a few studies
have reported about the relative positions of the SMV and SMA
in patients with situs anomaly [7,14]. We think that this study
has a value in elucidation of the unknown SMA-SMV relationship
in situs anomaly, as well as potential associations with intestinal
malrotation.
In clinical practice, USG has been used as a noninvasive initial
screening imaging modality for evaluating abdominal abnormali-
ties. However, it is difficult to directly assess the retroperitoneal
positioning of the duodenum and the location of the duodenojeju-
nal junction on USG. Thus, we remain dependent on the SMA-SMV
relationship to suggest intestinal malrotation when examining
USG. It would be clinically useful if we could ascertain the signifi-
cance of the SMA-SMV relationship in patients with situs anomaly,
with respect to the diagnosis of intestinal malrotation, just as in
patients with situs solitus.
In our study, situs ambiguus was commonly associated with
intestinal malrotation, as previously observed in literature [2,7,15]
and the SMA-SMV relationship was variable, which may be due to
variability of embryological development. Newman and colleagues
have also reported this variability of the SMA-SMV relationship
in patients with situs ambiguus and intestinal malrotation [7].
Therefore, in patients with situs ambiguus, USG examination of the
SMA-SMV relationship does not aid in the diagnosis of associated
intestinal malrotation, and UGIS and small bowel follow-through
are recommended to rule out intestinal malrotation [2].
On the contrary, reversal of the mesenteric vascular relationship
was commonly observed in situs inversus patients with inverted
1699
Right sided Left sided Dorsal
0 12 (75.0%) 0
4 (23.5%) 5 (29.4%) 1 (5.9%)
1 (5.9%) 2 (11.8%) 1 (5.9%)
3 (17.6%) 3 (17.6%) 0
intestinal rotation without any signs of malrotation, which is con-
sistent with the reversed position of other organs in situs inversus
[10]. However, considering that one patient with situs inversus and
intestinal malrotation showed left sided SMV, a reversed SMA-SMV
relationship could not safely exclude the possibility of intestinal
malrotation in situs inversus. In a similar manner, it has been well
known that a normal SMA-SMV relationship does not completely
exclude the possibility of intestinal malrotation and an abnormal
SMA-SMV relationship is not always associated with intestinal mal-
rotation in patients with normal situs solitus. Therefore, if situs
inversus is suspected, a reversed SMA-SMV relationship is not nec-
essarily pathological or a clinical indicator of associated intestinal
malrotation, as it may be in situs solitus patients.
Regarding management, heterotaxy syndrome have different
degree of intestinal malrotation – typical malrotation, nonrota-
tion, and atypical duodenal malposition – and subsequent risk of
development of volvulus is variable [4,16,17]. For example, typi-
cal malrotation with narrow mesenteric stalk shows high risk of
developing midgut volvulus. On the other hand, nonrotation with
broad mesentery or atypical duodenal malposition shows relatively
low risk of developing midgut volvulus [4]. In acute symptomatic
patients, prompt surgery is required to avoid small bowel infarction
[16]. However, in asymptomatic patients with heterotaxy syn-
drome, there has been significant controversy regarding the need
and outcome of prophylactic Ladd’s procedure [16,17]. Although
complication rate of Ladd’s procedure in asymptomatic children
with heterotaxy syndrome is reportedly higher than that of symp-
tomatic children without heterotaxy syndrome [17], surgery could
prevent development of volvulus in patients with typical malro-
1700 K.S. Choi et al. / European Journal of Radiology 85 (2016) 1695–1700
tation with narrow mesenteric stalk [4]. Moreover, elective Ladd’s
procedure after stabilization of the cardiac condition is now advo-
cated as a better strategy in asymptomatic patients with heterotaxy
syndrome and intestinal malrotation, considering high prevalence
of congenital heart anomaly in heterotaxy syndrome [4,16–19].
Watchful awaiting might be helpful to reduce mortality and mor-
bidity because asymptomatic patients with heterotaxy syndrome
have a low risk of intestinal complication [4,20]. Above all, patients
with heterotaxy syndrome should undergo UGIS to evaluate asso-
ciated intestinal malrotation and subsequent risk of development
of midgut volvulus that can determine the need and timing for pro-
phylactic Ladd’s procedure [16]. This study has several limitations.
First, due to the retrospective nature of this study, only a small por-
tion of the patients having situs anomaly during the study period
were included for assessment. In our institution, UGIS or prophylac-
tic Ladd operation has not been routinely performed. Therefore, the
study population in our study would have been biased for abdomi-
nal pathology and the incidence of intestinal malrotation in patients
with situs anomaly could have been overestimated, because clini-
cally suspected patients tended to undergo UGIS or surgery. Second,
the study population was relatively small due to low incidence
(0.01%) of situs ambiguus [4–6] as well as intestinal malrotation,
which is 3.9–20 in 10000 live births [4,8,16].
5. Conclusions
Situs ambiguus was commonly associated with intestinal mal-
rotation, with a variable SMA-SMV relationship. Reversal of the
mesenteric vascular relationship was generally observed in situs
inversus patients with normal intestinal rotation, but could not
exclude the possibility of intestinal malrotation. Therefore, the
SMA-SMV relationship does not appear to predict the presence
of intestinal malrotation in patients with situs anomaly. If situs
anomaly is suspected, UGIS and small bowel follow-through are
recommended for the diagnosis of intestinal malrotation.
Conflict of interest
All the authors declare that he/she has no conflict of interest.
Ethical approval
This article does not contain any studies with human partici-
pants or animals performed by any of the authors.
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