Accepted Manuscript

The horseshoe kidney: surgical anatomy and embryology

K. Taghavi, J. Kirkpatrick, S.A. Mirjalili

PII: S1477-5131(16)30097-3
DOI: 10.1016/j.jpurol.2016.04.033
Reference: JPUROL 2213

To appear in: Journal of Pediatric Urology

Received Date: 19 December 2015

Accepted Date: 10 April 2016

Please cite this article as: Taghavi K, Kirkpatrick J, Mirjalili SA, The horseshoe kidney: surgical anatomy
and embryology, Journal of Pediatric Urology (2016), doi: 10.1016/j.jpurol.2016.04.033.

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 ACCEPTED MANUSCRIPT

The horseshoe kidney: surgical anatomy and embryology

K. Taghavia, J. Kirkpatrickb, S. A. Mirjalilic,*

a
Department of Paediatric Surgery, Wellington Children’s Hospital, Wellington, New
Zealand

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b
School of Medicine, University of Auckland, Auckland, New Zealand
c
Department of Anatomy, University of Auckland, Auckland, New Zealand

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*Corresponding author: Department of Anatomy with Radiology, University of

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Auckland, Auckland, New Zealand. Tel.:
E-mail address: a.mirjalili@auckland.ac.nz (S. A. Mirjalili)

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Summary
Horseshoe kidneys are a common, yet enigmatic, renal malformation. This review
critically appraised the literature surrounding the embryology, etiology and clinical
anatomy of horseshoe kidneys. The systematic literature search produced 104 articles,
and 56 primary and further secondary references. There were several etiological
theories regarding horseshoe kidneys. The established view was that during ascent,
the kidneys come into close apposition as they pass through an arterial fork. Another
possible mechanism related to lateral flexion of the trunk or rotation of the caudal

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embryo; the association of asymmetrical horseshoe kidneys with a number of
vertebral conditions supported this hypothesis. More recent animal models implicated
the notochord and sonic hedgehog signaling. Furthermore, it has been suggested that

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the isthmus may be the result of ectopic mesenchymal tissue. Surgical anatomy of the
horseshoe kidney is complex, due to variability in location, orientation and blood
supply. Both arterial and venous anatomy is highly variable. This raised the question

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of whether anomalous blood supply is the cause or result of abnormal renal position.
In the majority of cases, the isthmus contained functional renal parenchyma. In over
90% of cases, fusion between the kidneys occurred at the lower pole. Despite

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commonly being quoted as ‘held back by the inferior mesenteric artery’ at L3, in
reality the isthmus was only found immediately inferior to this in 40% of cases.
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Keywords: Horseshoe kidney; Renal fusion; Renal ectopia; Ectopic kidney

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Introduction

Horseshoe kidneys are the most common fusion defect of the kidney, with a reported frequency of

approximately 1:500 [1]. They were first described during autopsies performed by da Carpi in 1522 and

are characterized by abnormalities in three major domains: renal position, rotation and vascular supply

[2]. Several etiological factors may contribute to the development of a horseshoe kidney, including: the

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intrauterine environment, genetic/chromosomal predisposition, and structural factors that affect the

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development and migration of the kidneys [3]. Horseshoe kidneys have important clinical relations with

regards to: secondary renal pathology, associated syndromes, and subsequent malignancy. Although

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many articles have been written regarding renal fusion and ectopia, there is a scarcity of comprehensive

reviews that systematically abridge the current understanding of this malformation. This study critically

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appraised the literature surrounding the clinical anatomy, etiology, and embryology of horseshoe

kidneys.
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Literature search
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A systematic literature search was performed using Scopus and PubMed. Search terms included were:
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‘Horseshoe Kidney’, ‘Ectopic’ or ‘Fusion’ and ‘Kidney’ or ‘Renal’, ‘Urogenital’ or ‘Urinary’ and
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‘Malformation’, ‘Horseshoe kidney’ and ‘Surgery’. A total of 104 journal articles and textbook

references were retrieved and reviewed. Primary articles were systematically reviewed and secondary
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references were obtained and subsequently reviewed with relevance to embryology, etiology and
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surgical anatomy. The search was restricted to English-language articles but no date restriction was

placed. Finally, 56 primary and 12 secondary references were reviewed. The 42 references included in

the final manuscript have been abbreviated to reduce redundancy and to meet the journal’s

requirements.

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Embryology and etiology

From an embryological point of view, each kidney consists of two distinct cell populations: the ureteric

bud and the metanephric blastema. The ureteric bud forms the collecting system, while the functioning

kidney is derived from the metanephric blastema. These two structures meet in the upper sacral region

(S1-S2) through reciprocal induction during the fourth week of development [4]. Aberrations of this

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process are responsible for a wide spectrum of congenital urological conditions [5].

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Reference textbooks quote renal fusion anomalies as occurring between 4-6 weeks of

development [6, 7]. Other authors allow for a time frame of up to 9 weeks, particularly in cases of a

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fibrous isthmus [5, 8]. There are numerous hypotheses regarding the cause of horseshoe kidneys, and

they represent a common end-point of multiple etiologies. The various mechanisms can be considered

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as: positional factors and anomalous fusion related to proximity, abnormalities in migration of

metanephric cells, intrauterine factors (maternal environment and exposure to teratogens), and
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associated genetic factors and chromosomal abnormalities [3].

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Physical environment
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Fusion defects may be caused by abnormal fluctuations in growth and ventral flexion of the caudal fetus

within a confined true pelvis [9]. It has been confirmed that the metanephric blastemas in normal
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embryos are in close proximity to each other prior to ascent [10]. The established view is that during
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ascent (as depicted in Fig. 1.B), they come into close apposition as they pass through an arterial fork
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[11]. However, there is discussion about which anatomical entity this occurs around: the aortic

bifurcation [6, 12] or the umbilical arteries [13, 14]. Generally, the more complete the fusion, the more

ectopic the position [7].

Also, during renal ascent, flexion or rotation of the caudal end or spine (even within normal

developmental variability) may be sufficient to cause fusion [9]. In a similar manner, even slight

alterations in the position of key arteries (e.g. umbilical or common iliac) may cause an alteration in the
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path of renal migration and consequent fusion [15]. A related point to note is that even in normal

individuals, both kidneys share a common perirenal space (crossing the midline) [16].

The fact that fusion anomalies may occur both symmetrically or asymmetrically provides

further insights into causation (distribution of these variants are depicted in Fig. 2) [4]. Symmetrical

horseshoe kidneys are the result of factors that influence both renal masses equally [9]. These may

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include abnormalities of growth or ventral flexion within a constricted embryonic pelvis [4]. Also,

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delayed straightening of the caudal fetus may postpone renal ascent long enough for fusion to occur [4].

Asymmetrical or laterally fused horseshoe kidneys are the result of differential displacement of the renal

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masses [9]. Etiology of these may include lateral flexion of the trunk or rotation of the caudal embryo

[4]. The association of asymmetrical horseshoe kidneys with a number of vertebral conditions supports

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this hypothesis (e.g. scoliosis, vertebral agenesis, hemivertebra and spina bifida) [4, 9, 17]. The
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genitourinary system and vertebral column originate from distinct components of the mesoderm, but are
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relatively synchronous in their development, and so this association may also represent a developmental

field defect or sequence [18].

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Abnormal metanephric migration

It has been suggested that the etiology of the characteristic isthmus or bridge may be due to ectopic
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mesenchymal tissue rather then ‘primary fusion’. This has followed the observation that in the majority
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of horseshoe kidneys, the ‘isthmus’ is composed of substantial parenchymal tissue (as in Fig. 2) [19].
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This ectopic nephrogenic tissue is said to arise due to incomplete or abnormal migration of posterior

nephrogenic cells across the primitive streak [5, 19]. This anomalous proliferation of the metanephric

blastema may explain the propensity to certain tumors in horseshoe kidneys [20].

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Genetic and autosomal disorders

No clear genetic cause of horseshoe kidney has been described in humans; however, a number of

regulatory steps in kidney development have not been fully elucidated and may offer future insight into

etiology [21]. In animal models, the notochord has been implicated as determining the position of

metanephric tissue. Furthermore, depletion of the axial source of Sonic Hedgehog (SHH) has been

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shown to be sufficient to cause renal fusion, even in the presence of the notochord [22].

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There is a well-described male preponderance (2:1) [1]. Also, there are case reports of familial

clustering between father and son [21] and monozygotic twins [23]. In one family, three siblings had

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horseshoe kidneys and the mother had a malrotated kidney [24]. This offers circumstantial evidence that

fetal genetic programming may play an etiological role. However, there are also case reports of

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monozygotic twins where only one child is affected [25].
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Some authors contend that urological malformations associated with chromosomal
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abnormalities are partly a consequence of delayed development of the nephrogenic blastema and the

ureteric bud [26]. In Edwards syndrome, horseshoe kidneys occur in two-thirds of patients [27], and in
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Downs syndrome, the incidence of horseshoe kidneys is probably <1% [28]. In Turner syndrome,
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horseshoe kidneys occur in 14-20% of patients [29], with a lower incidence of renal malformations in

those with mosaicism [30].

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Anatomy of the horseshoe kidney

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Renal isthmus and its relations

The bridge connecting the two renal masses has variable anatomical relations and substance (as depicted

in Fig. 2). Its midline or lateral position, relative to the vertebral column, establishes whether the

horseshoe kidney is symmetric or asymmetric [8]. Asymmetrical systems are more commonly left

dominant (70%) rather than right dominant (30%) [1]. In 80% of cases, the isthmus contains functional

renal parenchyma, which can provide a challenge to safely divide at surgery. In over 90% of cases,
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fusion between the kidneys occurs at the lower pole; although it may also occur at the upper pole,

resulting in an ‘inverted horseshoe’ (5-10%), or at both poles resulting in a ‘disc kidney’ [8, 31]. There

may also be double ureters present on one or both sides (6%) [1]. One or both ureters may rarely travel

posterior to the isthmus [7]. The isthmus typically crosses anterior to the great vessels, but can cross

posteriorly, or even more rarely run between them [32, 33].

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Migration and location

The developing kidneys initially lie adjacent to each other below the umbilical arteries in the embryonic

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pelvis at 4 [11] to 5 [34] weeks of gestation (5-mm or 7-mm human embryo). During their relative

ascent, they become anatomically separated to reach their final positions in the retroperitoneal renal

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fossa [11]. The kidneys ascend out of the pelvis during the seventh week and have reached their final
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position by the end of the eighth [4, 8] or ninth [34] week (see Fig. 1). This occurs due to
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disproportionate growth of lumbar and sacral regions in conjunction with general straightening of the

embryo. This results in the body wall shifting inferiorly, with relative ascent of the kidney [6, 12].
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During migration, the shape of the developing kidneys fluctuates: it becomes thin and oblong while
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passing the narrow space of the umbilical arteries before rounding out to take on the mature form and

position [34]. Horseshoe kidneys generally don’t migrate superiorly to the same extent [13]. The ascent
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of these kidneys is often quoted to be ‘held back by the inferior mesenteric artery’ at L3 [6, 13, 33].
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However, in reality, the isthmus is only found immediately inferior to the inferior mesenteric artery in
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40% of cases; a further 20% never leave the pelvis (see Fig. 1) [7, 33].

Rotation

During weeks 6-8 of development, renal ascent is coupled with a 90º medial rotation [14]. This results

in the hilum rotating from an anterior to a medial position, as well as a tilt in the renal axis, with the

upper pole lying posteromedial relative to the lower pole [6]. The spectrum of abnormalities in

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horseshoe kidney include malrotation, and consequently the ureters either pass over the isthmus or down

the anterior surface of the kidneys [8, 33]. The most common occurrences are incomplete rotation or

non-rotation, however, hyper-rotation and reverse rotation can also occur [14].

Blood supply

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The developing kidney gains and loses several sources of vascular supply during ascent [33]. In the

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pelvis, the median sacral artery and the internal and external iliac vessels supply it. Later, it may be

directly supplied by the aorta, or a branch from it (the common and inferior mesenteric artery), before

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gaining the renal artery [35]. As cranial migration continues, the caudal arteries degrade [13]. Reports

have demonstrated inhibition of cranial migration via persistent embryonic arteries [36]. This raises the

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question of whether these anomalous blood vessels are the cause or result of abnormal renal position.
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This point requires particular clarification in the case of an inverted horseshoe kidney, and when there
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are variable relations to the great vessels [2].

Ectopic kidneys show great variation in: origin, number, and size of renal arteries and veins,
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depending on where during development ascent has terminated [14]. Due to the surgical significance of
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these variations, attempts have been made to map the arterial supply [1, 31, 37]. Graves considered the

vascular pattern of horseshoe kidneys in six groups (see Fig. 3) [35]. However, this is a simplification of
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highly variable vascular anatomy and does not allow for arteries that supply contralateral kidney tissue
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(this occurs in approximately 25% of horseshoe kidneys). Furthermore, this system does not describe the
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wide range of possible arterial origins that include the: common iliac artery (40%), median sacral artery

(3%), lumbar artery (3%), internal iliac artery (2%), external iliac artery (1%) and phrenic artery

(0.97%) [1].

More contemporary studies have employed modern imaging techniques to describe the

extensive variation of the vascular anatomy, and general conclusions can be drawn. In a study of 90

horseshoe kidneys, 387 feeding arteries were identified (on average two or more arterial supplies per

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renal unit), with more arteries supplying the right side (219 vs 168) [1]. The most cranial of the renal

arteries were more consistent in position, and arose more posteriorly from the aorta when compared with

those originating caudally. The percentage of vessels originating from the aorta decreased with number

from 99% for the first arising artery to 50% for the fifth [1].

Nevertheless, even in horseshoe kidneys, the normal vascular segmental pattern remains [35].

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Although these vessels are considered anomalous, their ligation or division results in ischemic necrosis

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due to their autonomous supply [38]. The blood supply of the isthmus carries particular interest and

exhibits considerable variation; it may, in some cases, supply the entire kidney [33]. The isthmus may

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receive its blood supply from: the main renal artery, a branch from the abdominal aorta (originating

above or below the isthmus), the common iliac artery or the inferior mesenteric artery [2, 39].

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The incidence of renal vein anomalies in horseshoe kidneys is also high (23%) [40].
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Anomalous veins in the horseshoe kidney commonly drain into either the vena cava or iliac veins [1].
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Variations of inferior vena cava (IVC) anatomy (including double IVCs and left IVCs) are observed ten

times more frequently in those with horseshoe kidneys (5.7%) [41]. Important variations in vascular
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supply can make upper tract surgery, kidney transplant or surgical and endovascular procedures
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challenging [1]. Indeed, operating on horseshoe kidneys has been described as a ‘minefield for open

vascular surgery’ [40].

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Conclusion
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Horseshoe kidneys reveal a veritable range of anatomical and embryological peculiarities. There are

multiple mechanical and genetic associations that have been implicated. The close apposition of the

renal blastemas during renal ascent may play an important role in their development. Their relative

migration is incomplete, resulting in a final position ranging from the normal renal fossa to the true

pelvis. Their medial rotation is also interrupted and results in a more anterior pelvis and ectopic ureter

path. Their arterial relations and supply are highly variable. Furthermore, they are associated with
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various ureteric configurations and venous anomalies. These have important implications in operative

planning.

Conflict(s) of interest: None to declare.

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Figure legends

Fig. 1. Ascent of the developing kidney.

A. Normal kidney position and incidence of ectopia with horseshoe kidneys [42].

B. Normal morphological and positional changes in the kidney during

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development with relation to the vertebral column and umbilical artery,

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based on studies of human embryos [34].

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The diagrams represent the following gestational ages: a) 6 weeks + 3 days; b) 7

weeks + 1 day; c) 7 weeks + 2 days; d) 8 weeks + 3 days; e) 9 weeks + 2

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days
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Fig. 2. Incidence of the various morphological configurations of horseshoe

kidneys and their isthmus [9].

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Fig. 3. Graves’ description of the various segmental arterial patterns of horseshoe

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kidneys [35].
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