Acodaduras Ureterales (Kinking)

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Surg Radiol Anat

DOI 10.1007/s00276-016-1689-7

ORIGINAL ARTICLE

Kinking of the upper ureter in CT urography: anatomic


and clinical significance
Minobu Kamo1,2 • Taiki Nozaki1 • Kyoko Yoshida3 • Ukihide Tateishi2 •

Keiichi Akita3

Received: 1 December 2015 / Accepted: 31 March 2016


 Springer-Verlag France 2016

Abstract Conclusions Kinking of the upper ureter is not a clinically


Purpose Although the course of the ureter is described as a significant finding and arises from the ureter having a rel-
straight descent in the retroperitoneum, kinking of the atively mobile portion in the perirenal space compared to
upper ureter is often seen at imaging. The aim of this study its caudal portion. The fixation boundary can be identified
was to investigate kinking of the ureter and its underlying by observing the CP.
anatomico-clinical significance.
Methods We evaluated 176 computed tomography (CT) Keywords Ureter  CT urography  Renal fascia  Psoas
images and classified kinking into three grades: no/mild fascia  Radiological anatomy
kinking as Grade 1, moderate as Grade 2, and severe as
Grade 3. We defined the ‘‘crossing point’’ (CP) as where
the ureter crosses over the gonadal vein and assessed its Introduction
relation to the kinking. Fourteen halves from seven
cadavers were used for examination. Approaching anteri- It is generally accepted that the ureter descends straight in
orly, we macroscopically observed the ureter and sur- the retroperitoneal space [1, 2]. However, on retrograde
rounding structures. pyelography or computed tomography (CT) urography
Results On CT, the rate of the radiologically ‘‘significant’’ performed routinely in clinical practice, kinking of the
kinking classified into either Grade 2 or 3 was 18.4 % on upper ureter often occurs near its crossing over the ipsi-
the right and 21.8 % on the left. All kinking was either at or lateral gonadal vein (Fig. 1). Since kinking is sometimes
above the level of the CP. In cadavers, the ureter was very prominent, one might imagine that it could cause
relatively mobile in the perirenal fat and then beginning at clinical problems, for example predisposing patients to
approximately the level of the CP became firmly fixed to ureteric stone obstruction at this location. Additionally, it
the anteromedial aspect of the psoas major muscle. could make endo-ureteric procedures difficult. However, to
the best of our knowledge, there have been no descriptions
in the literature that kinking here poses a problem, possibly
for lack of clinical significance, or perhaps because this
& Keiichi Akita finding has heretofore been overlooked. Another question
akita.fana@tmd.ac.jp is why kinking is almost always seen at approximately the
1
same level within the upper ureter. It has long been known
Department of Radiology, St. Luke’s International Hospital,
9-1 Akashi-cho, Chuo-ku, Tokyo 104-8560, Japan
that there are three physiologically narrow points in the
2
upper urinary tract: the ureteropelvic junction (UPJ), the
Department of Radiology, Tokyo Medical and Dental
pelvic brim where ureter crosses over the common iliac
University, 1-5-45, Yushima, Bunkyo-ku, Tokyo 113-8519,
Japan vessels, and the ureterovesical junction [2, 5]. However,
3 recent studies focusing on the location of ureteral stones
Department of Clinical Anatomy, Tokyo Medical and Dental
University, 1-5-45, Yushima, Bunkyo-ku, Tokyo 113-8519, using CT images revealed one of the most frequent levels
Japan where stones obstruct was actually in the upper ureter, the

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Surg Radiol Anat

such as ultrasound (n = 31), pre-treatment evaluation of


bladder carcinoma (n = 24), follow-up examination after
transurethral resection of bladder tumor (n = 23) or eval-
uation of the urinary tract as a recipient before kidney
transplantation (n = 3). Exclusion criteria were as follows:
congenital abnormality of the upper urinary tract such as
duplicated renal pelvis and ureter or horse-shoe kidney,
acquired abnormality of the upper urinary tract including
neoplasm, a stone of the UPJ or the upper ureter, prior
history of an open/laparoscopic surgery of the abdomen or
pelvis, and other abnormalities around the upper ureter
which could potentially affect the course of the ureter. This
study was approved by the Institutional Review Board.
Informed consent was waived because of the retrospective
nature of the study.
For all patients, 2 mL/kg of intravenous non-ionic
contrast material (iohexol, Ominipaque 300, Daiichi
Pharmaceutical, Tokyo, Japan; iopamidol, Iopamiron 300,
Bayer Healthcare, Osaka, Japan) was injected as a bolus.
CT examinations were performed with either of two
64-detector CT scanners (Aquilion, TOHSHIBA, Japan
and Optima CT660, GE, USA). The excretory phase
scanning was acquired 6 min after completion of an
injection of contrast. The CT parameters were as follows:
tube voltage 120 kv, tube current 100–500 mA/s, colli-
Fig. 1 A coronal reconstructed image in the excretory phase of CT
mation 32 mm, pitch 0.844, field of view 320 mm, matrix
(maximum intensity projection). In the image of CT urography, 512 9 512 for the Aquilion unit, tube voltage 120 kv, tube
kinking (arrow) of the upper ureter is often noticed. Li liver, Kn current 50–560 mA/s, collimation 40 mm, pitch 0.984,
kidney, Ur ureter, L1 first lumbar vertebra, L2s lumbar vertebra, L3 field of view 320 mm, matrix 512 9 512 for the Optima
third lumbar vertebra
CT660 unit. The axial and coronal images were recon-
structed at 1–1.25 and 2–3 mm slice thickness, respec-
cause of which was not specifically mentioned [4, 7]. One tively. Three-dimensional reconstructed images of the
might be able to speculate that there is some anatomical excretory phase (CT urography) were obtained using a
relationship between obstruction of stones and kinking, three-dimensional workstation.
both of which occur in the upper ureter. We classified kinking of the upper ureter into three
The aim of this study was to determine the prevalence, grades (Fig. 2): no/mild kinking of the upper ureter (Grade
location, and degree of kinking seen in the upper ureter on 1), moderate kinking containing a horizontal portion
CT urography and investigate its underlying anatomico- (Grade 2), and severe kinking containing a retrograde
clinical significance by dissecting cadavers. portion (Grade 3). That is, either being classified into
Grade 2 or 3 was regarded as radiologically ‘‘significant’’
kinking. As shown in Fig. 2, we measured the width of the
Materials and methods kinking in Grade 2 and the width and the height in Grade 3
using the coronal view. Next, we named the point where
CT urography the ureter crosses over the ipsilateral gonadal vein as the
‘‘crossing point’’ (CP) and measured the vertebral level of
We retrospectively evaluated 176 consecutive patients (117 each CP. As shown in Fig. 3, we divided each vertebra into
males and 59 female patients, mean age 64.2 years, range thirds and numbered lower third of L2 vertebra to lower
21–92 years) who underwent enhanced abdominal CT third of L5 as 1–10 and analyzed each location. The
including an excretory phase (CT urography) from April location of the kinking in relation to the CP was also
2014 to March 2015 at our hospital. CT urography was analyzed.
performed for any of the following clinical purposes: All CT exams were reviewed by two board-certified
investigation of hematuria (n = 95), investigation of sus- radiologists (MK and TN) with 8 and 13 years of experi-
pected abnormality found on other diagnostic modalities ence, respectively.

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Surg Radiol Anat

To examine the ureter, we removed the skin, the sub-


cutaneous tissues and the alimentary tract from the body.
Then we approached the retroperitoneal space from the
anterior side and macroscopically observed the position of
the ureter and its vascular and nervous distribution. We
also visualized the gonadal vein and evaluated its relation
to the ureter.

Statistical analysis

According to a power analysis based on a Chi-square


goodness of fit test model from a prior study [3], this
sample size (n = 176) yielded 100 % power at the sig-
nificance level of 0.05 for medium size effect. The Chi-
square test was performed to assess laterality in the grade
Fig. 2 Grade of kinking seen in the upper ureter. Grade 1 no/mild of kinking seen in the upper ureter. The paired t test was
kinking, Grade 2 moderate kinking containing a horizontal portion, used to compare the vertebral level of the CP by side and
Grade 3 severe kinking containing a retrograde portion. The width of
the kinking in Grade 2 and the width and the height in Grade 3 were one-way ANOVA was used to compare the vertebral levels
measured using the coronal view of the CP among kinking grades bilaterally. All statistical
analyses were performed using R for Windows software (R
Development Core Team, version 3.0.2; Vienna, Austria).
The level of significance for all calculations was defined at
p \ 0.05.

Results

CT urography

Of 176 cases, 2 right ureters and 2 left ureters were not


evaluated because of difficulty in identifying the ureter or
the gonadal vein. Kinking of the upper ureter on the right
was seen in 142 cases as Grade 1 (81.6 %), 17 cases as
Grade 2 (9.8 %) and 15 cases as Grade 3 (8.6 %). On the
left, it was seen in 137 cases as Grade 1 (78. 2 %), 26
cases as Grade 2 (15.5 %) and 11 cases as Grade 3
(6.3 %) (Fig. 4a–c). The findings are summarized in
Table 1. The rate of the radiologically ‘‘significant’’
kinking classified into either Grade 2 or 3 was 18.4 % on
Fig. 3 Vertebral level of CP where the upper ureter crosses over the the right and 21.8 % on the left. There was no laterality in
ipsilateral gonadal vein. We divided each vertebra into thirds and the grade of kinking (p = 0.22). All kinking was seen
numbered lower third of L2 vertebra to lower third of L5 as 1–10 and either at the same vertebral level or above the level of the
analyzed each location
CP. In Grade 2 kinking, mean width of the kinking was
13 mm (range 3–25 mm) on the right side and 14 mm
Cadaveric study (range 7–32 mm) on the left side. In Grade 3 kinking,
mean width was 11 mm (range 6–20 mm) and mean
Fourteen halves from seven cadavers (two males and five height was 8.7 mm (range 3–15 mm) on the right side,
females, all of Japanese ancestry, mean age at the time of mean width was 18 mm (6–28) and mean height was
death 85.4 years; range 56–97 years) were used for the 9.5 mm (range 4–20 mm) on the left side. The average
dissecting examination. All cadavers were donated to the level of the CP was 6.4 (middle third of L4 vertebra) on
Department of Anatomy of Tokyo Medical and Dental the right side and 5.1 (upper third of L4 vertebra) on the
University. Cadavers were fixed in 8 % formalin and pre- left side. The CP was significantly lower in the right side
served in 30 % ethanol. (p \ 0.01) (Fig. 5). On the other hand, there was no

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Fig. 4 Three-dimensional reconstructed images of CT urography. ureter in a 58-year-old man classified into Grade 3. Kn kidney, Ur
a No kinking of the left upper ureter in a 65-year-old man classified ureter, GV gonadal vein, L3 third lumbar vertebra, L4 fourth lumbar
into Grade 1. b Moderate kinking of the left upper ureter in a 48-year- vertebra
old female classified into Grade 2. c Severe kinking of the left upper

Table 1 Grade distribution of kinking seen in the upper ureter Cadaveric study
Grade 1 Grade 2 Grade 3
By removing the peritoneum and the anterior renal fascia,
Right 142 (81.6) 17 (9.8) 15 (8.6) the ureter and the gonadal vessels were visualized. After
Left 136 (78.7) 27 (14.9) 11 (6.3) passing through in the perirenal fat where the ureter was
Data are absolute numbers; incidence rates (%) are given in relatively mobile, the ureter was fixed firmly to the medial
parentheses anterior aspect of the fascia of the psoas major muscle. The
There was no laterality in the grade of kinking (p = 0.22) upper border of the firm fixation was approximately where
the gonadal vein crosses over the ureter (Fig. 6). The ureter
had a scarce supply of the vessels and nerves at this rela-
tively fixed area (Fig. 6d, area of asterisk). No direct vessel
or nervous distribution was found at the medial side in this
area. Above the firmly fixed area, the ureter had arterial and
nervous supply from the renal hilum and venous drainage
to the renal vein to IVC near the renal hilum. Below the
firmly fixed area, it was supplied from or drained by the
ipsilateral iliac vessels. No cadaveric specimen demon-
strated significant kinking.

Discussion

The ureters are a pair of long cylindrical structures in the


retroperitoneal space which connect the kidney and the
bladder. The ureteral length is 25–30 cm in adult [6].
While the bladder is to some extent fixed to the pelvis, the
kidney is located just under the diaphragm and changes its
Fig. 5 The vertebral level of CP. The crossing point was significantly position dramatically according to physiological movement
lower in the right side (p \ 0.01) such as respiration [5, 13]. Its position can be also changed
under degenerative change of the lumbar vertebra or
significant difference of the vertebral level of the CP by weakening of supporting tissues around it. These reversible
kinking grade on either side (p = 0.78 on the right, or irreversible changes of the kidney position always force
p = 0.42 on the left). the ureter to adjust its length.

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Fig. 6 The ureter and its surrounding structures in the cadaver. a The asterisk). The area of the ureter had a scarce supply of the vessels and
anterior renal fascia was exposed after removal of the peritoneum. nerves. RF renal fascia, Pr peritoneum, GA gonadal artery, GV
b The gonadal artery and vein were revealed beneath the peritoneum. gonadal vein, PM psoas major muscle, IVC inferior vena cava, Ao
c The ureter was observed beneath the layer of the gonadal vessels. aorta, Ur ureter, CIA common iliac artery, Kn kidney, RV renal vein,
d After passing through in the perirenal fat, the ureter was fixed firmly RA renal artery, IIA internal iliac artery, EIA external iliac artery
to the medial aspect of the fascia of the psoas major muscle (area of

Intravenous pyelography (IVP) has been long used to space. The boundary of the perirenal portion of the ureter
assess the ureter. CT urography, however, has recently can be determined approximately by finding the level of the
largely replaced this exam and plays a major role in CP (Fig. 8). From an embryo-anatomical point of view, it
evaluating urinary tract owing to its availability to provide is not clear why the CP is associated with fixation of the
more detail using multi-planar reconstructed images [9, ureter; after passing through the perirenal space, both the
12]. One of the differences between these examinations lies ureter and the gonadal vein are sandwiched between the
in the timing of imaging. In IVP, images are taken in the anterior renal fascia and the posterior renal fascia on the
expiratory phase, while in CT urography, images are usu- medial side in the retroperitoneal space. Both structures run
ally taken in the inspiratory phase just like other abdominal cranio-caudally in the space and have to cross eventually
CT examinations. That is, the images of CT urography are from the renal hilum to the pelvis. The CP turns out to be at
taken in a condition when the kidney descends. Routine a very practical landmark: the boundary where the ureter
observation of the urinary tract in the inspiratory phase is exits the perirenal space and is fixed more firmly in the
therefore a relatively recent phenomenon. anterior medial aspect of the psoas muscle.
In this CT urography study, we found kinking in the Ureteral kinking did not show laterality in this study. On
upper ureter to be common; additionally, it always occurs the other hand, the level of the CP was slightly lower on the
at or just above the level where the ureter crosses over the right side. This can be explained by the fact that kidney is
ipsilateral gonadal vein. In cadavers, the ureter was rela- located lower on the right side because of the liver being
tively mobile as it passed through the perirenal fat and then just above the right kidney [5, 10, 13]. Fixation of the
became fixed firmly to the anterior medial side of the psoas upper ureter is also probably slightly lower on the right
major muscle. The level of the ureter’s fixation was side. The vertebral level of the CP was not significantly
approximately where it crossed over the gonadal vein. different with respect to the grade of the kinking. Thus, it
Considering these results together, we speculate that the does not appear that kinking is caused by a higher/lower
kinking probably arises as a consequence of the ureter positioning of the point of fixation.
adjusting length when the kidney descends. This hypothe- Although most radiologists or urologists who read CT
sis is also supported by observing dynamic images of the urography regularly in their daily practice are very familiar
upper ureter during angiography or retrograde pyelogra- with kinking of the upper ureter, there have been very few
phy, in which dynamic change of the upper ureter synced reports focusing on this finding. Indeed, one anatomical
to the movement of the kidney is well visualized (Fig. 7). It text states, ‘‘in its abdominal portion the ureter pursues an
is thought that kinking is seen at the area where the ureter almost vertical course downward and medially on the
is relatively mobile, that is, where it runs in the perirenal anterior surface of the psoas muscle’’ [1]. Additionally,

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Fig. 7 Dynamic images of the ureter during angiography. A 38-year- kinking is most prominent in the inspiratory phase and mild in the
old female with atonic uterine bleeding. During angiography (uterine expiratory phase. Ur ureter, L3 third lumbar vertebra, L4 fourth
artery embolization), dynamic changes of the upper ureter in lumbar vertebra, Catheter catheters in the right internal iliac artery
synchrony with the movement of the kidney is well visualized. The

mentioned ‘‘the proximal ureter is easily visible endo-


scopically as the variations of kidney position with
breathing cause movement of this area secondary to its
fixed, non-mobile nature compared with the mobile renal
pelvis…,’’ and ‘‘…a bend of mucosa’’ is noticed around
UPJ junction endoscopically [8]. This ‘‘bend’’ may be
coincident with the kinking in our study. In our cadaveric
study, on the other hand, none of the specimens demon-
strated significant kinking. Since cadavers fixed in formalin
assume an expiratory configuration because of muscular
laxity, the kidney tends to be positioned cranially and the
ureteral kinking is therefore absent. Thus, we hypothesize
that this is one of the main reasons ureteral kinking has not
been previously noted.
So, what, if any, relationship does the area where
kinking arises have to clinical problems of the ureter?
While the previously mentioned, well-known tendency for
obstruction at the UPJ is helpful in theory, in daily prac-
tice we often encounter cases in which a stone obstructs at
the upper ureter, slightly distal to the UPJ where the cal-
iber change occurs (Fig. 9). Recent studies investigating
the distribution of ureteral stone location using multi-
planar CT images also mentioned that one of the most
Fig. 8 Mechanism of causing kinking. Kinking arises as a conse- common levels of ureteral stone obstruction is in the upper
quence of the ureter adjusting length when the kidney descends. ureter [4, 7]. Although the cause of this obstruction was
Kinking is seen at the area where the ureter is relatively mobile, that
is, where it runs in the perirenal space. The boundary of the perirenal not described in detail in these articles, it would be diffi-
portion of the ureter can be determined approximately by finding the cult to imagine that the diameter of the ureter is the sole
level of the CP. Kn kidney, IVC inferior vena cava, Ao aorta, GA cause. We speculate that this area of the upper ureter
gonadal artery, GV gonadal vein, PM psoas major muscle, Ur ureter would likely be near the CP where the ureter is fixed more
firmly in the retroperitoneal space and just below where
Silverman et al. published a ‘‘normal’’ three-dimensional kinking is observed. Some stone obstructions do occur at
urography CT image in which grade 3 kinking was seen on the UPJ, the physiological area of narrowing near the renal
the right side, an example of how this finding had been hilum, but these stones tend to be quite large. Smaller
ignored thus far [11]. On the other hand, Motola et al. stones tend to obstruct in the proximal upper ureter near

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Surg Radiol Anat

Conclusion

Kinking of the upper ureter is not a clinically significant


finding, which is often seen in CT urography. This finding
can arise due to the fact that the upper ureter passing
through the perirenal space has more mobility compared to
its caudal portion which is more firmly fixed in the
retroperitoneal space. This boundary can be identified by
observing CP where the ureter crosses over the ipsilateral
gonadal vein.

Acknowledgments The authors are grateful to Jay Starkey, M.D. for


the revision of the English text, and Daisuke Unai, R.T. for the
assistance of creating the CT images. This work is supprted by JSPS
KAKENHI Grant Number 15K08129.

Compliance with ethical standards

Conflict of interest The authors declare no conflict of interests.

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