a case study of malrotated kidneys with asymmetric...

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Case Report A Case Study of Malrotated Kidneys with Asymmetric Multiple Renal Arteries, Variant Venous Drainage, and Unilateral Ureteral Duplication Martine Dunnwald and Marc A. Pizzimenti Department of Anatomy and Cell Biology, Roy J. and Lucille A. Carver College of Medicine, University of Iowa, Iowa City, Iowa, USA Correspondence should be addressed to Marc A. Pizzimenti; [email protected] Received 21 December 2018; Accepted 18 February 2019; Published 18 March 2019 Academic Editor: Muzaffer Sindel Copyright © 2019 Martine Dunnwald and Marc A. Pizzimenti. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Variations in the arterial, venous, and ureteral patterning of the right (r) and leſt (l) kidneys are common; however, concomitant involvement with all three systems is rare. Specimens that demonstrate anatomic variation across multiple systems provide an opportunity to illustrate links between anatomic concepts, embryologic development, clinical practice, and education. During anatomic study of the abdominal cavity, a total of five major arteries (3l and 2r) emerged from the aortic and common iliac axes in a cadaveric donor. rough continued study, multiple contributing veins, of different caliber, coalesced into four major renal veins (2l and 2r) that returned blood from the kidneys to the inferior vena cava (IVC) at different locations. In addition, unilateral duplication of the kidney with concomitant ureters was evident on the right side. Both ureters continued inferiorly and independently entered the bladder, each with an observable orifice adjacent to the bladder trigone. Most evident in the specimen was the anteriorly directed hilum for both kidneys. Reported measures for each of the observed anatomic variations suggest that the current specimen has an estimated incidence of less than 0.3%. is comparatively rare specimen provides an example of important anatomic concepts that are relevant to educational and clinical practices. 1. Introduction Although variations in the arterial, venous, and ureteral patterning of the kidneys are common, concomitant involve- ment of variant anatomy in all of these systems appears to be much rarer. Arterial variants that diverge from the generalized pattern of paired renal arteries emerging lat- erally from the aorta, inferior to the level of the superior mesenteric artery, have been observed in approximately 30% of individuals (e.g., [1, 2]). In the venous system, variations in the drainage pattern that diverge from the classically described paired vessels flowing into the inferior vena cava (IVC) have been well documented and can have an incidence rate similar to that of the arterial system (e.g., [3]). However, variation in the ureteral pattern is not as common as that found in the vascular system. Reports indicate that genetic factors contribute to ureteric variations [4, 5] which occur with an approximate incidence of 1% [6, 7]. e case study presented here demonstrates concomitant variation in the arterial, venous, and ureteric systems of the kidney. Collectively, this case provides examples of impor- tant anatomic considerations that relate the foundational anatomical science with educational practice. ese include the generalized concept of anatomic variation, the process of renal morphogenesis with variant presentations, and considerations for clinical procedures with involved variant anatomy. 2. Case Report During anatomic study of the abdominal cavity, additional renal branches from the aortic axis were revealed in a 97- year-old male Caucasian cadaveric donor. Continued dis- section outlined notable anatomic variations in the arterial, venous, and ureteric patterns. No urologic or cardiovascular issues were reported by the donor or family at the time of enrolment in the Deeded Body Program. For this type of Hindawi Case Reports in Vascular Medicine Volume 2019, Article ID 1893137, 7 pages https://doi.org/10.1155/2019/1893137

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Page 1: A Case Study of Malrotated Kidneys with Asymmetric ...downloads.hindawi.com/journals/crivam/2019/1893137.pdf · CaseReport A Case Study of Malrotated Kidneys with Asymmetric Multiple

Case ReportA Case Study of Malrotated Kidneys withAsymmetric Multiple Renal Arteries Variant Venous Drainageand Unilateral Ureteral Duplication

Martine Dunnwald andMarc A Pizzimenti

Department of Anatomy and Cell Biology Roy J and Lucille A Carver College of Medicine University of Iowa Iowa City Iowa USA

Correspondence should be addressed to Marc A Pizzimenti marc-pizzimentiuiowaedu

Received 21 December 2018 Accepted 18 February 2019 Published 18 March 2019

Academic Editor Muzaffer Sindel

Copyright copy 2019 Martine Dunnwald and Marc A Pizzimenti This is an open access article distributed under the CreativeCommons Attribution License which permits unrestricted use distribution and reproduction in any medium provided theoriginal work is properly cited

Variations in the arterial venous and ureteral patterning of the right (r) and left (l) kidneys are common however concomitantinvolvement with all three systems is rare Specimens that demonstrate anatomic variation across multiple systems provide anopportunity to illustrate links between anatomic concepts embryologic development clinical practice and education Duringanatomic study of the abdominal cavity a total of five major arteries (3l and 2r) emerged from the aortic and common iliac axes in acadaveric donorThrough continued study multiple contributing veins of different caliber coalesced into fourmajor renal veins (2land 2r) that returned blood from the kidneys to the inferior vena cava (IVC) at different locations In addition unilateral duplicationof the kidney with concomitant ureters was evident on the right side Both ureters continued inferiorly and independently enteredthe bladder eachwith an observable orifice adjacent to the bladder trigoneMost evident in the specimenwas the anteriorly directedhilum for both kidneys Reported measures for each of the observed anatomic variations suggest that the current specimen has anestimated incidence of less than 03This comparatively rare specimen provides an example of important anatomic concepts thatare relevant to educational and clinical practices

1 Introduction

Although variations in the arterial venous and ureteralpatterning of the kidneys are common concomitant involve-ment of variant anatomy in all of these systems appearsto be much rarer Arterial variants that diverge from thegeneralized pattern of paired renal arteries emerging lat-erally from the aorta inferior to the level of the superiormesenteric artery have been observed in approximately30 of individuals (eg [1 2]) In the venous systemvariations in the drainage pattern that diverge from theclassically described paired vessels flowing into the inferiorvena cava (IVC) have been well documented and can havean incidence rate similar to that of the arterial system (eg[3]) However variation in the ureteral pattern is not ascommon as that found in the vascular system Reportsindicate that genetic factors contribute to ureteric variations[4 5] which occur with an approximate incidence of 1[6 7]

The case study presented here demonstrates concomitantvariation in the arterial venous and ureteric systems of thekidney Collectively this case provides examples of impor-tant anatomic considerations that relate the foundationalanatomical science with educational practice These includethe generalized concept of anatomic variation the processof renal morphogenesis with variant presentations andconsiderations for clinical procedures with involved variantanatomy

2 Case Report

During anatomic study of the abdominal cavity additionalrenal branches from the aortic axis were revealed in a 97-year-old male Caucasian cadaveric donor Continued dis-section outlined notable anatomic variations in the arterialvenous and ureteric patterns No urologic or cardiovascularissues were reported by the donor or family at the time ofenrolment in the Deeded Body Program For this type of

HindawiCase Reports in Vascular MedicineVolume 2019 Article ID 1893137 7 pageshttpsdoiorg10115520191893137

2 Case Reports in Vascular Medicine

RARA

RV

RP

RVRA

AA

IVC

RA

U

CIACIA RARA

RV U

RP

RAIM

A

Figure 1 Renal system in situ Macroscopic view of the renal systemwithin the abdominal cavity of the donor AA = abdominal aortaCIA = common iliac artery IMA = inferior mesenteric artery IVC= inferior vena cava RA = renal artery RP = renal pelvis RV = renalvein U = ureter Image scale bar = 2 cm

study Institutional Review Board approval is not required forresearch conducted with cadaveric specimens

Both kidneys were retroperitoneal and similar in sizewith measurements of 123 cm (l) and 127 cm (r) in thecraniocaudal direction Despite the fact that the lengthswere similar there were marked differences in the relativepositioning of the superior and inferior poles The superiorpole of the right kidney was situated more superiorly Theinferior pole of the left kidney was positioned near thesuperior border of the left common iliac artery Althougheach kidney occupied an extended volume neither kidneyhad a pelvic component Hilar structures enteredexited theorgans anteriorly not with the typical medially projectedhilum (Figure 1)

21 Arterial Pattern A total of five major arteries (3l and2r) emerged from the aortic and common iliac axes (Figures2(a) and 2(b)) The superior left renal artery originated fromthe abdominal aorta and supplied the superior pole Thisartery (52mmdiameter) branched into two vessels of similarcaliber to supply the upper third of the organ Supply to theleft gonad originated from the more inferior of these twobranches (Figures 2(b) and 3(b))Themiddle left renal artery(61 mm diameter) originated from the iliac junction justanterior to the median sacral artery (Figures 3(a) and 3(b))The inferior left renal artery (54 mm diameter) originatedfrom the common iliac artery and coursed posteriorly to thekidney before entering the hilum anteriorly (from the lateral

aspect of the organ) to supply the inferior pole (Figures 3(b)3(c) and 3(d)) On the contralateral side the vasculature tothe right kidney consisted of only two renal arteries bothoriginating from the abdominal aorta The superior renalartery (62 mm diameter) branched laterally from the aorta(at the same level as the left superior renal) and supplied thesuperior pole As with the contralateral side this artery alsobranched into two vessels of similar caliber but supplied thesuperior half of the organ (Figures 4(a) and 4(b)) In contrastto the contralateral side the right gonadal artery brancheddirectly from the aorta at its generally observed positionjust inferior to the (superior) renal artery Arterial supply tothe inferior pole (65 mm diameter) originated on the lateralaorta at a level inferior to the inferior mesenteric artery andbranched into two arteries (Figures 4(b) 4(c) and 4(d))

22 Venous Pattern Multiple contributing veins of differentcaliber coalesced into four major renal veins (2l and 2r) thatreturned blood from the kidneys to the IVC (Figure 2(c))Therelative positioning of the superior renal veins followed theconventional pattern entering the IVC through single vesselsat a level just inferior to the superior mesenteric artery as itemerged from the aorta On the right side three major veinsmerged into a short segment (3 mm in length) to drain thesuperior 23 of the organ The inferior 13 of the organ wasdrained through two primary contributors that merged into asingle vein that ultimately drained into the IVC at the level ofthe previously described right inferior renal artery A visibleand substantive anastomotic connectionwas evident betweenthe superior and inferior venous pathways (Figure 3(b)) Onthe left side the superior renal vein received contributionsfrom the suprarenal gland and the superior half of the kidneyVenous return from the left gonad ultimately merged intothe most inferior branch of the three primary contributors tothe superior renal vein (Figures 2(c) and 3(b)) The inferiorrenal vein drained directly into the anterior aspect of theIVC at the junction of the common iliac veins posteriorto the bifurcation of the aorta The most inferior of thethree primary contributors to the inferior renal vein emergedfrom the posterior lateral aspect of kidney and spanned thehilum to ultimately converge into the inferior renal veinThe middle contributor emerged from the parenchyma butwas unremarkable As on the contralateral side a visibleand substantive venous anastomotic connection was evidentbetween the superior and inferior aspects of the kidney(Figure 4(b))

23 Ureteral Pattern Unilateral duplication of the kidneywith concomitant ureters was evident for the right side(Figure 2(d)) Aligned with the arterial pattern of this organthe superior ureter demonstrated a discreet collecting systemwith well-formed minor and major calyces draining intoa defined renal pelvis The majority of the superior renalpelvis was positioned posterior to the vasculature (Figures4(a) and 4(b)) At the inferior portion of the kidney thehilum was more anteriorly directed with the calyces andrenal pelvismore evident given their anterior position relativeto the vasculature Both ureters continued inferiorly andindependently to enter the bladder (Figure 1) Histological

Case Reports in Vascular Medicine 3

lsRA

lmRAriRA

rCiA lCiA

rsRA

IMA

lsRV

rsRV

riRV

IVC

liRV

rSU

rRPlRP

lU

riU

(a) (b) (c) (d)

Figure 2 Ex situ renal system exhibits anatomical variations from normal pattern (a) Uncolorized renal system ex situ (b) Arterial networkpseudocolorized in red rsRA = right superior renal artery lsRA = left superior renal artery IMA = inferior mesenteric artery riRA = rightinferior renal artery lmRA = leftmiddle renal artery liRA = left inferior renal artery rCiRA = right common iliac artery lCiA = left commoniliac artery (c) Venous network pseudocolorized in blue IVC = inferior vena cava rsRV = right superior renal vein lsRV = left superior renalvein riRV = right inferior renal vein liRV = left inferior renal vein (d) Ureters pseudocolorized in yellow with rRP = right renal pelvis lRP= left renal pelvis rU = right ureters lU= left ureter Pseudocolorization created using Adobe Photoshop Image scale bar = 2 cm

(a) (b) (c) (d)

lU

lRP

liRV

lsRVlsRA

liRA

lCiV

lCiA

liRV

lmRA

IMA

lsRA

lmRA

liRA

Figure 3 Ex situ left kidney exhibits anatomical variations Anterior (a b) and posterior (c d) views of the left kidney Arterial venous andureteric systems (b d) are pseudocolorized in red (arterial) blue (venous) and yellow (ureteric) Renal veins (lsRV liRV) are reflected to betterillustrate the arterial pattern Image scale bar = 2 cm

investigation of the ureterovesical junctions was not com-pleted however a distinct orifice near the bladder trigone wasevident for each ureter On the contralateral side the singleureter emerged from a widened and anteriorly projectedhilum (Figure 3(b)) Major calyces from the peripheralparenchyma were evident and these calyces contributed to anelongated renal pelvisThe remaining course of the left ureterwas unremarkable

3 Discussion

Rare case studies present opportunities to not only considerthe observed morphological variations but also revisit under-lying concepts in embryology and the associated educationalimplications Variations in the arterial venous and ureteral

patterning of the kidneys are common however involve-ment with all three systems is very rare The current casedemonstrates concomitant variation in the arterial venousand ureteral systems which is conservatively estimated tohave an incidence of less than 03

31 Anatomic Variation Arterial variants have been ob-served in approximately 30of individuals althoughpopula-tion specific incidences have been shown to vary considerably[1 8] Studies documenting the major renal branches ratherthan the branching pattern into kidney parenchyma suggestthat arterial origins along the entire abdominal aortic axisare possible Branches at or superior to the level of thesuperior mesenteric artery [9] and along the lumbar region[10ndash14] have been well documented Arterial branching from

4 Case Reports in Vascular Medicine

rsRA

rsU

riRV

rRP

riU

riRA

rsRV

IVC

riRV

rsU

riU

riRA

rsRV

rsRA

(a) (b) (c) (d)

Figure 4 Ex situ right kidney exhibits anatomical variations Anterior (a b) and posterior (c d) views of the right kidney Arterial venousand ureteric systems (b d) are pseudocolorized in red (arterial) blue (venous) and yellow (ureteric)

the iliac axis has also been documented particularly inectopic kidneys [15ndash17] however ectopic specimens withoutpelvic involvement have also demonstrated branches arisingfrom the iliac region [14 18] Bilateral variation in thearterial patterning has been quantified with an incidence ofapproximately 10 [19] while unilateral arterial supply tothe kidney arising from all of these regions has a suggestedincidence of approximately 04 [20 21]

Although early modern attempts to quantify patterningthrough direct patient (andor cadaveric) observation (eg[22ndash24]) were compelling more recent studies using imaging(eg [18 19 21]) have verified and improved our understand-ing of the incidence for these arterial patterns They havebeen classified in Patterns (I-V) and Types (A-E) based onthe number of vessels observed and the location from whichthe vessels arise respectively From these studies the arterialdistribution to the right kidney in the current specimengenerally fits the description for Pattern II and Type D wheretwo arteries enter the kidney and the inferior renal segmentis supplied directly from the aorta This arterial patterntypehas an incidence rate of approximately 2 The left kidneyin the current specimen most closely demonstrates PatternIII with 3-4 distinct arteries but the Type descriptor fallsoutside of the general classification schema Here the currentspecimen is most similar to case studies presented throughdirect observation in cadaveric specimens [25] or visualizedthrough CT-3D reconstruction [18] Although Cases et aldid not include a reconstructed case in the analysis thedata set would suggest an hypothesized incidence for thecurrent arterial pattern to be at minimum of 04 Howevera statistically sound meta-analysis that includes specificbranching categories across studies has yet to be completed

As with the arterial system variation in renal veinpatterning is not uncommon Studies with large sample sizes(eg gt100) suggest that variation in venous patterning hasan incidence of 235-30 as observed through computedtomography (CT) [3 26ndash28] This reported incidence hasalso been observed in 105 cases of horseshoe kidney [29]Given the high incidence of renal vein variation a recentstudy used CT to observe and classify these variations within

a comparatively large sample size (1452 patients) [28] Inthis classification system the venous drainage of the rightkidney in the current specimen could be described as Type2A (03 incidence) with direct drainage into the IVC fromtwo renal veins The venous drainage of the left kidney couldbe described as Type IB (14 incidence) with drainage intothe IVC and common iliac vein What is unclear from thesestudies is if the incidence rates are applicable for bilateralvariations

Variation in ureteral patterning is not as common asthat found in the vascular system but reports indicate anapproximate incidence of 1 [6 7] with unilateral duplexkidney reported as high as 18 [30] Incidence of ureteralduplication appears to have a familial pattern of inheritance[4 5] that for a duplex kidney results from more than oneureteric bud outgrowth from the mesonephric duct duringfetal development

As outlined above aspects of the variations described inthe current case have been observed elsewhere Howeverfew of those cases have provided detailed descriptions andillustrations of concomitant involvement of each systemCollectively this case appears to be rare given the lowincidence rates for each (independent) system arterial 04venous 03-14 and ureteral 1-18 Based on this reviewof studies and using the reported systems-related variationthe incidence rate for the current specimen is conservativelyestimated at less than 03 of the population

32 Educational and Embryological Considerations Studentswho participate in dissection courses early in their trainingor students rotating through their clinical training learnthe basic premise of anatomic variationmdashthat organsregionsunder study often do not appear at least at first as out-lined in a referenced source Distinguishing which variationshave clinical significance requires both breadth and depthof training particularly within each clinical specialty [31]Although exposure to the concept of variation usually occursearly in training and primarily through dissection courses[31] many of the regionorgan details are often revisitedwithin clinical clerkships and during residency training [32]

Case Reports in Vascular Medicine 5

embryonic anatomicvariations

anatomicvariations

subcardinal vsupracardinal vposterior cardinal v

anatomicvariations

7 wee

ks6

week

s5

week

s

7 wee

ks6

week

s5

week

sstages

embryonicstages

embryonicem

bryo

logy

case

stud

ystages

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

(=)() (<)

(a) (b) (c)

Figure 5 Simplified schematic representation of renal development Around 5 weeks of fetal life kidneys are formed from the metanephrosThey are situated at the level of the pelvis and pelvic branches of the common iliac artery provide initial arterial blood supply During thefollowing 3 weeks the kidneys ascend in the abdominal cavity (a) to their adult retroperitoneal location As they move cranially and themetanephros coalesces the lower arteries degenerate to most often leave a single renal artery as the main arterial supply Occasionally thetemporary arteries (dotted lines (a)) do not degenerate leading to anatomical variations in the adult (a1015840) The cardinal systems contributeto the developing venous network of the kidney as it ascends (b) Persistence of some aspects of the developing venous network may leadto anatomical variations in the adult (dotted lines (b) (b1015840)) More than one ureteric bud may penetrate the metanephric mesoderm duringureteral development (c) that results in duplex kidney (left (c1015840))

For example variations in renal arterial patterning mayhave little clinical significance unless they are coupled withhypertension or require mapping for clinical procedures suchas surgical resection (eg [33]) transplantation (eg [34]) orpercutaneous access (eg [35]) Given the multisystem (iearterial venous and ureteral) involvement this case clearlydemonstrates the anatomical aspect of this concept

Collectively the anatomic variations of the current casealso reflect important concepts related to the morphologicaldevelopment of the kidney and its collecting system Duringhuman development three slightly overlapping renal systemsare formed in a cranial to caudal fashion pronephrosmesonephros and metanephros [36] The pronephros is atemporary organ that regresses at the end of the fourthweek of fetal life while the mesonephros contributes toBowmanrsquos capsule and the Wolffian duct in adult kidneysThe metanephros appears in the fifth week of fetal life andwill give rise to the adult kidney The renal excretory unitsoriginate from the metanephric mesoderm and collectingducts from the ureteric bud that penetrates the mesodermictissue While the primordial kidneys are initially locatedwithin the pelvis with their hila projected anteriorly to receivetheir arterial supply from a pelvic branch of the aorta thisorientation changeswith development Following growth andchange in body length at the lumbar and sacral regionsthe kidneys undergo a relative ldquoascentrdquo in the abdomen asthey shift to a more cranial position [37 38] This ascent is

accompanied by a transitioning arterial supply originatingfrom aortic branches at sequentially higher levels and medialrotation of the developing kidney as schematically depictedin Figure 5(a) The lower vessels usually degenerate butoccasionally some remain leading to anatomical variationsin the adult (Figures 2(b) 3(b) 3(c) 4(b) 4(d) and 5(a1015840))

Unlike the arterial system the venous system for the kid-ney arises from anastomotic connections between the devel-oping cardinal veins [38] Briefly at 5-6weeks of developmentthe posterior and subcardinal veins exhibit anastomoticconnections in a segment-like fashion that drain aspects ofthe early mesonephros The subcardinal veins anastomoseand coalesce in the midline contributing to the prerenalportion of the IVC and what is generally considered thedeveloped right renal vein Supracardinal veins like the otherrenal contributors begin as bilaterally symmetric havingsegmental connections with the posterior cardinal veins Asdevelopment continues the posterior cardinal veins degener-ate losing the segmental nature of the connections that wereestablished earlier with the subcardinal and supracardinalnetwork Ultimately the supracardinal system contributes tothe postrenal segment of the IVC This segment fuses withcaudal posterior cardinal segment that in turn gives rise tothe common iliac veins Concomitantly the supracardinalsystem on the left side loses connections with the developedleft renal vein and the hemiazygos system Even with thissimplified overview of a very complex developmental process

6 Case Reports in Vascular Medicine

(Figure 5(b)) the persistent connections between the venouscardinal networks (Figures 2(c) 3(b) 4(b) and 5(b1015840)) can beobserved in the current specimen

Development of the ureters arises from bud outgrowthsof the mesonephric duct For each kidney the ureteric budpenetrates the metanephric mesoderm (metanephrogenicblastema) that forms a cap intowhich the renal pelvis calyxesand collecting tubules develop through branching morpho-genesis [36] The stalk of the ureteric bud elongates as thekidney undergoes its relative ascent resulting in the formedureter by the ninth week of development (Figure 5(c)) Thesimultaneous morphogenesis of the vascular and uretericstructures influences themedial rotation of the hilum for eachdeveloping kidney Details of the signaling pathways and thegenes that regulate this entire process have been effectivelysummarized in the literature [39 40] and are beyond thescope of this case studyThese processes coupled with geneticfactors may give rise to variations in the ureteric pattern(Figures 2(d) 4(b) 4(d) 5(c) and 5(c1015840))

4 Conclusion

Anatomic variations in the systems of the developing kidneyare common however concomitant involvement of thearterial venous and ureteric systems is rare The currentcase study demonstrates a cadaveric specimen with anatomicvariations having an estimated incidence of less than 03Collectively this case illustrates examples of importantanatomic concepts that are relevant for educational andclinical practice

Conflicts of Interest

This work was completed without financial sponsorshipThe authors declare no conflicts of interest Portions of thiswork have been presented in abstract form at conferenceproceedings

Authorsrsquo Contributions

Marc A Pizzimenti contributed in project developmentdissection and manuscript writing Martine Dunnwald con-tributed in dissection illustrations and manuscript writing

Acknowledgments

The authors would like to thank the families of individualswho through their most generous gift to the Deeded BodyProgram allow us to continue studying the human body

References

[1] E Gulas G Wysiadecki T Cecot et al ldquoAccessory (multi-ple) renal arteries ndash Differences in frequency according topopulation visualizing techniques and stage of morphologicaldevelopmentrdquo Vascular vol 24 no 5 pp 531ndash537 2016

[2] R Bergman SThompson AAfifi and F SaadehCompendiumofHumanAnatomic Variation Text Atlas andWorld Literature

Urban amp Scharzenberg Inc Baltimore Munich Germany1988

[3] Z Koc S Ulusan L Oguzkurt and N Tokmak ldquoVenousvariants and anomalies on routine abdominal multi-detectorrow CTrdquo European Journal of Radiology vol 61 no 2 pp 267ndash278 2007

[4] J D Atwell P L Cook C J Howell I Hyde and B C ParkerldquoFamilial incidence of bifid and double uretersrdquo Archives ofDisease in Childhood vol 49 no 5 pp 390ndash393 1974

[5] J Whitaker and D M Danks ldquoA study of the inheritance ofduplication of the kidneys and uretersrdquoThe Journal of Urologyvol 95 no 2 pp 176ndash178 1966

[6] V Alberts R Minnee K van Donselaar-van der Pant et alldquoDuplicated ureters and renal transplantation a case-controlstudy and review of the literaturerdquoTransplantation Proceedingsvol 45 no 9 pp 3239ndash3244 2013

[7] R Pollak B F Prusak and M F Mozes ldquoAnatomic abnormal-ities of cadaver kidneys procured for purposes of transplanta-tionrdquoThe American Surgeon vol 52 no 5 pp 233ndash235 1986

[8] K S Satyapal A A Haffejee B Singh L Ramsaroop J VRobbs and J M Kalideen ldquoAdditional renal arteries Incidenceand morphometryrdquo Surgical and Radiologic Anatomy vol 23no 1 pp 33ndash38 2001

[9] C Dalcik T Colak A Ozbek and H Dalcik ldquoUnusual originof the right renal artery a case reportrdquo Surgical and RadiologicAnatomy vol 22 no 2 pp 117-118 2000

[10] U G Rossi M Romano and C Ferro ldquoSeven renal arteriesrdquoClinical Anatomy vol 19 no 7 pp 632-633 2006

[11] P Mazengenya ldquoMultiple variations of the renal and testicularvessels possible embryological basis and clinical importancerdquoSurgical and Radiologic Anatomy vol 38 no 6 pp 729ndash7332016

[12] K Morishima T Miyaki and H Ito ldquoA rare case of a kidneywith an (sic) widely opened hilus and supernumerary renalvesselsrdquoKaibogaku Zasshi Journal of Anatomy vol 71 no 3 pp215ndash218 1996

[13] H Narita T Tani and Y Tonosaki ldquoAssociations betweenkidney position and surplus renal arteries in horseshoe kidneyCase report and analysisrdquo Okajimas Folia Anatomica Japonicavol 89 no 1 pp 7ndash13 2012

[14] S T Patil MMMeshram and A P Kasote ldquoBilateral malrota-tion and lobulation of kidney with altered hilar anatomy a rarecongenital variationrdquo Surgical and Radiologic Anatomy vol 33no 10 pp 941ndash944 2011

[15] S Degani Z Leibovitz I Shapiro and G Ohel ldquoVariationsof the origin of renal arteries in the fetus identified on powerDoppler and 3D sonographyrdquo Journal of Clinical Ultrasoundvol 38 no 2 pp 59ndash65 2009

[16] J Singh N Singh K Kapoor and M Sharma ldquoBilateral mal-rotation and a congenital pelvic kidney with varied vasculatureand altered hilar anatomyrdquo Case Reports in Medicine vol 2015Article ID 848949 3 pages 2015

[17] C Krishnaveni and R Kulkarni ldquoA right ectopic kidney withbilateral multiple anomalies of the renal vasculature ndash a casereportrdquo Journal of Clinical and Diagnostic Research vol 7 pp150ndash153 2013

[18] C Cases L Garcıa-Zoghby P Manzorro et al ldquoAnatomicalvariations of the renal arteries Cadaveric and radiologic studyreview of the literature and proposal of a new classification ofclinical interestrdquo Annals of Anatomy - Anatomischer Anzeigervol 211 pp 61ndash68 2017

Case Reports in Vascular Medicine 7

[19] O Kornafel B Baran I Pawlikowska P Laszczynski MGuzinski and M Sasiadek ldquoAnalysis of anatomical variationsof the main arteries branching from the abdominal aorta with64-detector computed tomographyrdquoPolish Journal of Radiologyvol 75 pp 38ndash45 2010

[20] F J B Sampaio and M A R F Passos ldquoRenal arteriesanatomic study for surgical and radiological practicerdquo Surgicaland Radiologic Anatomy vol 14 no 2 pp 113ndash117 1992

[21] D T Tardo C Briggs G Ahern A Pitman and S SinhaldquoAnatomical variations of the renal arterial vasculature AnAus-tralian perspectiverdquo Journal of Medical Imaging and RadiationOncology vol 61 no 5 pp 643ndash649 2017

[22] J R Geyer and E F Poutasse ldquoIncidence of multiple renalarteries on aortography report of a series of 400 patients 381of whom had arterial hypertensionrdquo Journal of the AmericanMedical Association vol 182 no 2 pp 120ndash125 1962

[23] F T Graves ldquoThe arterial anatomy of the congenitally abnormalkidneyrdquo British Journal of Surgery vol 56 no 7 pp 533ndash5411969

[24] R J Merklin and N A Michels ldquoThe variant renal andsuprarenal blood supply with data on the inferior phrenicureteral and gonadal arteries A statistical analysis based on185 dissections and review of the literaturerdquo Journal of theInternational College of Surgeons vol 29 no 1 pp 41ndash76 1958

[25] A H Young and P Thompson ldquoAbnormalities of the renalarteries with remarks on their development and morphologyrdquoJournal of Anatomy vol 38 pp 1ndash14 1903

[26] J-P Trigaux S Vandroogenbroek J-F De Wispelaere MLacrosse and J Jamart ldquoCongenital anomalies of the inferiorvena cava and left renal vein Evaluation with spiral ctrdquo Journalof Vascular and Interventional Radiology vol 9 no 2 pp 339ndash345 1998

[27] S Kawamoto L P Lawler andE K Fishman ldquoEvaluation of therenal venous system on late arterial and venous phase imageswith MDCT angiography in potential living laparoscopic renaldonorsrdquo American Journal of Roentgenology vol 184 no 2 pp539ndash545 2005

[28] J Zhu L Zhang Z Yang H Zhou and G Tang ldquoClassificationof the renal vein variations a study with multidetector com-puted tomographyrdquo Surgical and Radiologic Anatomy vol 37no 6 pp 667ndash675 2015

[29] T Ichikawa S Kawada J Koizumi et al ldquoMajor venousanomalies are frequently associated with horseshoe kidneysrdquoCirculation Journal vol 75 no 12 pp 2872ndash2877 2011

[30] J T J Privett W D Jeans and J Roylance ldquoThe incidence andimportance of renal duplicationrdquo Clinical Radiology vol 27 no4 pp 521ndash530 1976

[31] P L Willan and J R Humpherson ldquoConcepts of variation andnormality in morphology Important issues at risk of neglect inmodern undergraduatemedical coursesrdquoClinical Anatomy vol12 pp 186ndash190 1999

[32] A Raikos and J D Smith ldquoAnatomical variations How dosurgical and radiology training programs teach and assess themin their training curriculardquoClinical Anatomy vol 28 no 6 pp717ndash724 2015

[33] N Rani S Singh P Dhar and R Kumar ldquoSurgical impor-tance of arterial segments of human kidneys An angiographyand corrosion cast studyrdquo Journal of Clinical and DiagnosticResearch vol 8 pp 1ndash3 2014

[34] S Ersoz A Tuzuner B Erkek S Esen and E Anadol ldquoDou-ble renal arteries in living-related kidney transplantationrdquoTransplantation Proceedings vol 32 no 3 p 604 2000

[35] V Ravery O Cussenot F Desgrandchamps et al ldquoVariationsin arterial blood supply and the risk of hemorrhage duringpercutaneous treatment of lesions of the pelviureteral junctionobstruction report of a case of testicular artery arising froman inferior polar renal arteryrdquo Surgical and Radiologic Anatomyvol 15 no 4 pp 355ndash359 1993

[36] T Sadler ldquoUrogenital systemrdquo in Langmanrsquos medical embryol-ogy Lippinott Williams amp Wilkins Baltimore MD USA 12thedition 2012

[37] K L Moore and T V N Persaud ldquoThe cardiovascular systemrdquoin The Developing Human Clinically Oriented Embryology pp330ndash335 Saunders Philadelphia Pa USA 7th edition 2003

[38] G C Schoenwolf S B Bleyl P R Brauer and P H Francis-West ldquoDevelopment of the vasculaturerdquo in Larsenrsquos humanembryology pp 385ndash432 Churchhill Livingstone PhiladelphiaPa USA 4th edition 2009

[39] K I Glassberg ldquoNormal and abnormal development of thekidney A clinicianrsquos interpretation of current knowledgerdquoThe Journal of Urology vol 167 no 6 pp 2339ndash2350 2002discussion 2350-2331

[40] N D Rosenblum ldquoDevelopmental biology of the humankidneyrdquo Seminars in Fetal and Neonatal Medicine vol 13 no3 pp 125ndash132 2008

Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

EndocrinologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Disease Markers

Hindawiwwwhindawicom Volume 2018

BioMed Research International

OncologyJournal of

Hindawiwwwhindawicom Volume 2013

Hindawiwwwhindawicom Volume 2018

Oxidative Medicine and Cellular Longevity

Hindawiwwwhindawicom Volume 2018

PPAR Research

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Immunology ResearchHindawiwwwhindawicom Volume 2018

Journal of

ObesityJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Computational and Mathematical Methods in Medicine

Hindawiwwwhindawicom Volume 2018

Behavioural Neurology

OphthalmologyJournal of

Hindawiwwwhindawicom Volume 2018

Diabetes ResearchJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Research and TreatmentAIDS

Hindawiwwwhindawicom Volume 2018

Gastroenterology Research and Practice

Hindawiwwwhindawicom Volume 2018

Parkinsonrsquos Disease

Evidence-Based Complementary andAlternative Medicine

Volume 2018Hindawiwwwhindawicom

Submit your manuscripts atwwwhindawicom

Page 2: A Case Study of Malrotated Kidneys with Asymmetric ...downloads.hindawi.com/journals/crivam/2019/1893137.pdf · CaseReport A Case Study of Malrotated Kidneys with Asymmetric Multiple

2 Case Reports in Vascular Medicine

RARA

RV

RP

RVRA

AA

IVC

RA

U

CIACIA RARA

RV U

RP

RAIM

A

Figure 1 Renal system in situ Macroscopic view of the renal systemwithin the abdominal cavity of the donor AA = abdominal aortaCIA = common iliac artery IMA = inferior mesenteric artery IVC= inferior vena cava RA = renal artery RP = renal pelvis RV = renalvein U = ureter Image scale bar = 2 cm

study Institutional Review Board approval is not required forresearch conducted with cadaveric specimens

Both kidneys were retroperitoneal and similar in sizewith measurements of 123 cm (l) and 127 cm (r) in thecraniocaudal direction Despite the fact that the lengthswere similar there were marked differences in the relativepositioning of the superior and inferior poles The superiorpole of the right kidney was situated more superiorly Theinferior pole of the left kidney was positioned near thesuperior border of the left common iliac artery Althougheach kidney occupied an extended volume neither kidneyhad a pelvic component Hilar structures enteredexited theorgans anteriorly not with the typical medially projectedhilum (Figure 1)

21 Arterial Pattern A total of five major arteries (3l and2r) emerged from the aortic and common iliac axes (Figures2(a) and 2(b)) The superior left renal artery originated fromthe abdominal aorta and supplied the superior pole Thisartery (52mmdiameter) branched into two vessels of similarcaliber to supply the upper third of the organ Supply to theleft gonad originated from the more inferior of these twobranches (Figures 2(b) and 3(b))Themiddle left renal artery(61 mm diameter) originated from the iliac junction justanterior to the median sacral artery (Figures 3(a) and 3(b))The inferior left renal artery (54 mm diameter) originatedfrom the common iliac artery and coursed posteriorly to thekidney before entering the hilum anteriorly (from the lateral

aspect of the organ) to supply the inferior pole (Figures 3(b)3(c) and 3(d)) On the contralateral side the vasculature tothe right kidney consisted of only two renal arteries bothoriginating from the abdominal aorta The superior renalartery (62 mm diameter) branched laterally from the aorta(at the same level as the left superior renal) and supplied thesuperior pole As with the contralateral side this artery alsobranched into two vessels of similar caliber but supplied thesuperior half of the organ (Figures 4(a) and 4(b)) In contrastto the contralateral side the right gonadal artery brancheddirectly from the aorta at its generally observed positionjust inferior to the (superior) renal artery Arterial supply tothe inferior pole (65 mm diameter) originated on the lateralaorta at a level inferior to the inferior mesenteric artery andbranched into two arteries (Figures 4(b) 4(c) and 4(d))

22 Venous Pattern Multiple contributing veins of differentcaliber coalesced into four major renal veins (2l and 2r) thatreturned blood from the kidneys to the IVC (Figure 2(c))Therelative positioning of the superior renal veins followed theconventional pattern entering the IVC through single vesselsat a level just inferior to the superior mesenteric artery as itemerged from the aorta On the right side three major veinsmerged into a short segment (3 mm in length) to drain thesuperior 23 of the organ The inferior 13 of the organ wasdrained through two primary contributors that merged into asingle vein that ultimately drained into the IVC at the level ofthe previously described right inferior renal artery A visibleand substantive anastomotic connectionwas evident betweenthe superior and inferior venous pathways (Figure 3(b)) Onthe left side the superior renal vein received contributionsfrom the suprarenal gland and the superior half of the kidneyVenous return from the left gonad ultimately merged intothe most inferior branch of the three primary contributors tothe superior renal vein (Figures 2(c) and 3(b)) The inferiorrenal vein drained directly into the anterior aspect of theIVC at the junction of the common iliac veins posteriorto the bifurcation of the aorta The most inferior of thethree primary contributors to the inferior renal vein emergedfrom the posterior lateral aspect of kidney and spanned thehilum to ultimately converge into the inferior renal veinThe middle contributor emerged from the parenchyma butwas unremarkable As on the contralateral side a visibleand substantive venous anastomotic connection was evidentbetween the superior and inferior aspects of the kidney(Figure 4(b))

23 Ureteral Pattern Unilateral duplication of the kidneywith concomitant ureters was evident for the right side(Figure 2(d)) Aligned with the arterial pattern of this organthe superior ureter demonstrated a discreet collecting systemwith well-formed minor and major calyces draining intoa defined renal pelvis The majority of the superior renalpelvis was positioned posterior to the vasculature (Figures4(a) and 4(b)) At the inferior portion of the kidney thehilum was more anteriorly directed with the calyces andrenal pelvismore evident given their anterior position relativeto the vasculature Both ureters continued inferiorly andindependently to enter the bladder (Figure 1) Histological

Case Reports in Vascular Medicine 3

lsRA

lmRAriRA

rCiA lCiA

rsRA

IMA

lsRV

rsRV

riRV

IVC

liRV

rSU

rRPlRP

lU

riU

(a) (b) (c) (d)

Figure 2 Ex situ renal system exhibits anatomical variations from normal pattern (a) Uncolorized renal system ex situ (b) Arterial networkpseudocolorized in red rsRA = right superior renal artery lsRA = left superior renal artery IMA = inferior mesenteric artery riRA = rightinferior renal artery lmRA = leftmiddle renal artery liRA = left inferior renal artery rCiRA = right common iliac artery lCiA = left commoniliac artery (c) Venous network pseudocolorized in blue IVC = inferior vena cava rsRV = right superior renal vein lsRV = left superior renalvein riRV = right inferior renal vein liRV = left inferior renal vein (d) Ureters pseudocolorized in yellow with rRP = right renal pelvis lRP= left renal pelvis rU = right ureters lU= left ureter Pseudocolorization created using Adobe Photoshop Image scale bar = 2 cm

(a) (b) (c) (d)

lU

lRP

liRV

lsRVlsRA

liRA

lCiV

lCiA

liRV

lmRA

IMA

lsRA

lmRA

liRA

Figure 3 Ex situ left kidney exhibits anatomical variations Anterior (a b) and posterior (c d) views of the left kidney Arterial venous andureteric systems (b d) are pseudocolorized in red (arterial) blue (venous) and yellow (ureteric) Renal veins (lsRV liRV) are reflected to betterillustrate the arterial pattern Image scale bar = 2 cm

investigation of the ureterovesical junctions was not com-pleted however a distinct orifice near the bladder trigone wasevident for each ureter On the contralateral side the singleureter emerged from a widened and anteriorly projectedhilum (Figure 3(b)) Major calyces from the peripheralparenchyma were evident and these calyces contributed to anelongated renal pelvisThe remaining course of the left ureterwas unremarkable

3 Discussion

Rare case studies present opportunities to not only considerthe observed morphological variations but also revisit under-lying concepts in embryology and the associated educationalimplications Variations in the arterial venous and ureteral

patterning of the kidneys are common however involve-ment with all three systems is very rare The current casedemonstrates concomitant variation in the arterial venousand ureteral systems which is conservatively estimated tohave an incidence of less than 03

31 Anatomic Variation Arterial variants have been ob-served in approximately 30of individuals althoughpopula-tion specific incidences have been shown to vary considerably[1 8] Studies documenting the major renal branches ratherthan the branching pattern into kidney parenchyma suggestthat arterial origins along the entire abdominal aortic axisare possible Branches at or superior to the level of thesuperior mesenteric artery [9] and along the lumbar region[10ndash14] have been well documented Arterial branching from

4 Case Reports in Vascular Medicine

rsRA

rsU

riRV

rRP

riU

riRA

rsRV

IVC

riRV

rsU

riU

riRA

rsRV

rsRA

(a) (b) (c) (d)

Figure 4 Ex situ right kidney exhibits anatomical variations Anterior (a b) and posterior (c d) views of the right kidney Arterial venousand ureteric systems (b d) are pseudocolorized in red (arterial) blue (venous) and yellow (ureteric)

the iliac axis has also been documented particularly inectopic kidneys [15ndash17] however ectopic specimens withoutpelvic involvement have also demonstrated branches arisingfrom the iliac region [14 18] Bilateral variation in thearterial patterning has been quantified with an incidence ofapproximately 10 [19] while unilateral arterial supply tothe kidney arising from all of these regions has a suggestedincidence of approximately 04 [20 21]

Although early modern attempts to quantify patterningthrough direct patient (andor cadaveric) observation (eg[22ndash24]) were compelling more recent studies using imaging(eg [18 19 21]) have verified and improved our understand-ing of the incidence for these arterial patterns They havebeen classified in Patterns (I-V) and Types (A-E) based onthe number of vessels observed and the location from whichthe vessels arise respectively From these studies the arterialdistribution to the right kidney in the current specimengenerally fits the description for Pattern II and Type D wheretwo arteries enter the kidney and the inferior renal segmentis supplied directly from the aorta This arterial patterntypehas an incidence rate of approximately 2 The left kidneyin the current specimen most closely demonstrates PatternIII with 3-4 distinct arteries but the Type descriptor fallsoutside of the general classification schema Here the currentspecimen is most similar to case studies presented throughdirect observation in cadaveric specimens [25] or visualizedthrough CT-3D reconstruction [18] Although Cases et aldid not include a reconstructed case in the analysis thedata set would suggest an hypothesized incidence for thecurrent arterial pattern to be at minimum of 04 Howevera statistically sound meta-analysis that includes specificbranching categories across studies has yet to be completed

As with the arterial system variation in renal veinpatterning is not uncommon Studies with large sample sizes(eg gt100) suggest that variation in venous patterning hasan incidence of 235-30 as observed through computedtomography (CT) [3 26ndash28] This reported incidence hasalso been observed in 105 cases of horseshoe kidney [29]Given the high incidence of renal vein variation a recentstudy used CT to observe and classify these variations within

a comparatively large sample size (1452 patients) [28] Inthis classification system the venous drainage of the rightkidney in the current specimen could be described as Type2A (03 incidence) with direct drainage into the IVC fromtwo renal veins The venous drainage of the left kidney couldbe described as Type IB (14 incidence) with drainage intothe IVC and common iliac vein What is unclear from thesestudies is if the incidence rates are applicable for bilateralvariations

Variation in ureteral patterning is not as common asthat found in the vascular system but reports indicate anapproximate incidence of 1 [6 7] with unilateral duplexkidney reported as high as 18 [30] Incidence of ureteralduplication appears to have a familial pattern of inheritance[4 5] that for a duplex kidney results from more than oneureteric bud outgrowth from the mesonephric duct duringfetal development

As outlined above aspects of the variations described inthe current case have been observed elsewhere Howeverfew of those cases have provided detailed descriptions andillustrations of concomitant involvement of each systemCollectively this case appears to be rare given the lowincidence rates for each (independent) system arterial 04venous 03-14 and ureteral 1-18 Based on this reviewof studies and using the reported systems-related variationthe incidence rate for the current specimen is conservativelyestimated at less than 03 of the population

32 Educational and Embryological Considerations Studentswho participate in dissection courses early in their trainingor students rotating through their clinical training learnthe basic premise of anatomic variationmdashthat organsregionsunder study often do not appear at least at first as out-lined in a referenced source Distinguishing which variationshave clinical significance requires both breadth and depthof training particularly within each clinical specialty [31]Although exposure to the concept of variation usually occursearly in training and primarily through dissection courses[31] many of the regionorgan details are often revisitedwithin clinical clerkships and during residency training [32]

Case Reports in Vascular Medicine 5

embryonic anatomicvariations

anatomicvariations

subcardinal vsupracardinal vposterior cardinal v

anatomicvariations

7 wee

ks6

week

s5

week

s

7 wee

ks6

week

s5

week

sstages

embryonicstages

embryonicem

bryo

logy

case

stud

ystages

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

(=)() (<)

(a) (b) (c)

Figure 5 Simplified schematic representation of renal development Around 5 weeks of fetal life kidneys are formed from the metanephrosThey are situated at the level of the pelvis and pelvic branches of the common iliac artery provide initial arterial blood supply During thefollowing 3 weeks the kidneys ascend in the abdominal cavity (a) to their adult retroperitoneal location As they move cranially and themetanephros coalesces the lower arteries degenerate to most often leave a single renal artery as the main arterial supply Occasionally thetemporary arteries (dotted lines (a)) do not degenerate leading to anatomical variations in the adult (a1015840) The cardinal systems contributeto the developing venous network of the kidney as it ascends (b) Persistence of some aspects of the developing venous network may leadto anatomical variations in the adult (dotted lines (b) (b1015840)) More than one ureteric bud may penetrate the metanephric mesoderm duringureteral development (c) that results in duplex kidney (left (c1015840))

For example variations in renal arterial patterning mayhave little clinical significance unless they are coupled withhypertension or require mapping for clinical procedures suchas surgical resection (eg [33]) transplantation (eg [34]) orpercutaneous access (eg [35]) Given the multisystem (iearterial venous and ureteral) involvement this case clearlydemonstrates the anatomical aspect of this concept

Collectively the anatomic variations of the current casealso reflect important concepts related to the morphologicaldevelopment of the kidney and its collecting system Duringhuman development three slightly overlapping renal systemsare formed in a cranial to caudal fashion pronephrosmesonephros and metanephros [36] The pronephros is atemporary organ that regresses at the end of the fourthweek of fetal life while the mesonephros contributes toBowmanrsquos capsule and the Wolffian duct in adult kidneysThe metanephros appears in the fifth week of fetal life andwill give rise to the adult kidney The renal excretory unitsoriginate from the metanephric mesoderm and collectingducts from the ureteric bud that penetrates the mesodermictissue While the primordial kidneys are initially locatedwithin the pelvis with their hila projected anteriorly to receivetheir arterial supply from a pelvic branch of the aorta thisorientation changeswith development Following growth andchange in body length at the lumbar and sacral regionsthe kidneys undergo a relative ldquoascentrdquo in the abdomen asthey shift to a more cranial position [37 38] This ascent is

accompanied by a transitioning arterial supply originatingfrom aortic branches at sequentially higher levels and medialrotation of the developing kidney as schematically depictedin Figure 5(a) The lower vessels usually degenerate butoccasionally some remain leading to anatomical variationsin the adult (Figures 2(b) 3(b) 3(c) 4(b) 4(d) and 5(a1015840))

Unlike the arterial system the venous system for the kid-ney arises from anastomotic connections between the devel-oping cardinal veins [38] Briefly at 5-6weeks of developmentthe posterior and subcardinal veins exhibit anastomoticconnections in a segment-like fashion that drain aspects ofthe early mesonephros The subcardinal veins anastomoseand coalesce in the midline contributing to the prerenalportion of the IVC and what is generally considered thedeveloped right renal vein Supracardinal veins like the otherrenal contributors begin as bilaterally symmetric havingsegmental connections with the posterior cardinal veins Asdevelopment continues the posterior cardinal veins degener-ate losing the segmental nature of the connections that wereestablished earlier with the subcardinal and supracardinalnetwork Ultimately the supracardinal system contributes tothe postrenal segment of the IVC This segment fuses withcaudal posterior cardinal segment that in turn gives rise tothe common iliac veins Concomitantly the supracardinalsystem on the left side loses connections with the developedleft renal vein and the hemiazygos system Even with thissimplified overview of a very complex developmental process

6 Case Reports in Vascular Medicine

(Figure 5(b)) the persistent connections between the venouscardinal networks (Figures 2(c) 3(b) 4(b) and 5(b1015840)) can beobserved in the current specimen

Development of the ureters arises from bud outgrowthsof the mesonephric duct For each kidney the ureteric budpenetrates the metanephric mesoderm (metanephrogenicblastema) that forms a cap intowhich the renal pelvis calyxesand collecting tubules develop through branching morpho-genesis [36] The stalk of the ureteric bud elongates as thekidney undergoes its relative ascent resulting in the formedureter by the ninth week of development (Figure 5(c)) Thesimultaneous morphogenesis of the vascular and uretericstructures influences themedial rotation of the hilum for eachdeveloping kidney Details of the signaling pathways and thegenes that regulate this entire process have been effectivelysummarized in the literature [39 40] and are beyond thescope of this case studyThese processes coupled with geneticfactors may give rise to variations in the ureteric pattern(Figures 2(d) 4(b) 4(d) 5(c) and 5(c1015840))

4 Conclusion

Anatomic variations in the systems of the developing kidneyare common however concomitant involvement of thearterial venous and ureteric systems is rare The currentcase study demonstrates a cadaveric specimen with anatomicvariations having an estimated incidence of less than 03Collectively this case illustrates examples of importantanatomic concepts that are relevant for educational andclinical practice

Conflicts of Interest

This work was completed without financial sponsorshipThe authors declare no conflicts of interest Portions of thiswork have been presented in abstract form at conferenceproceedings

Authorsrsquo Contributions

Marc A Pizzimenti contributed in project developmentdissection and manuscript writing Martine Dunnwald con-tributed in dissection illustrations and manuscript writing

Acknowledgments

The authors would like to thank the families of individualswho through their most generous gift to the Deeded BodyProgram allow us to continue studying the human body

References

[1] E Gulas G Wysiadecki T Cecot et al ldquoAccessory (multi-ple) renal arteries ndash Differences in frequency according topopulation visualizing techniques and stage of morphologicaldevelopmentrdquo Vascular vol 24 no 5 pp 531ndash537 2016

[2] R Bergman SThompson AAfifi and F SaadehCompendiumofHumanAnatomic Variation Text Atlas andWorld Literature

Urban amp Scharzenberg Inc Baltimore Munich Germany1988

[3] Z Koc S Ulusan L Oguzkurt and N Tokmak ldquoVenousvariants and anomalies on routine abdominal multi-detectorrow CTrdquo European Journal of Radiology vol 61 no 2 pp 267ndash278 2007

[4] J D Atwell P L Cook C J Howell I Hyde and B C ParkerldquoFamilial incidence of bifid and double uretersrdquo Archives ofDisease in Childhood vol 49 no 5 pp 390ndash393 1974

[5] J Whitaker and D M Danks ldquoA study of the inheritance ofduplication of the kidneys and uretersrdquoThe Journal of Urologyvol 95 no 2 pp 176ndash178 1966

[6] V Alberts R Minnee K van Donselaar-van der Pant et alldquoDuplicated ureters and renal transplantation a case-controlstudy and review of the literaturerdquoTransplantation Proceedingsvol 45 no 9 pp 3239ndash3244 2013

[7] R Pollak B F Prusak and M F Mozes ldquoAnatomic abnormal-ities of cadaver kidneys procured for purposes of transplanta-tionrdquoThe American Surgeon vol 52 no 5 pp 233ndash235 1986

[8] K S Satyapal A A Haffejee B Singh L Ramsaroop J VRobbs and J M Kalideen ldquoAdditional renal arteries Incidenceand morphometryrdquo Surgical and Radiologic Anatomy vol 23no 1 pp 33ndash38 2001

[9] C Dalcik T Colak A Ozbek and H Dalcik ldquoUnusual originof the right renal artery a case reportrdquo Surgical and RadiologicAnatomy vol 22 no 2 pp 117-118 2000

[10] U G Rossi M Romano and C Ferro ldquoSeven renal arteriesrdquoClinical Anatomy vol 19 no 7 pp 632-633 2006

[11] P Mazengenya ldquoMultiple variations of the renal and testicularvessels possible embryological basis and clinical importancerdquoSurgical and Radiologic Anatomy vol 38 no 6 pp 729ndash7332016

[12] K Morishima T Miyaki and H Ito ldquoA rare case of a kidneywith an (sic) widely opened hilus and supernumerary renalvesselsrdquoKaibogaku Zasshi Journal of Anatomy vol 71 no 3 pp215ndash218 1996

[13] H Narita T Tani and Y Tonosaki ldquoAssociations betweenkidney position and surplus renal arteries in horseshoe kidneyCase report and analysisrdquo Okajimas Folia Anatomica Japonicavol 89 no 1 pp 7ndash13 2012

[14] S T Patil MMMeshram and A P Kasote ldquoBilateral malrota-tion and lobulation of kidney with altered hilar anatomy a rarecongenital variationrdquo Surgical and Radiologic Anatomy vol 33no 10 pp 941ndash944 2011

[15] S Degani Z Leibovitz I Shapiro and G Ohel ldquoVariationsof the origin of renal arteries in the fetus identified on powerDoppler and 3D sonographyrdquo Journal of Clinical Ultrasoundvol 38 no 2 pp 59ndash65 2009

[16] J Singh N Singh K Kapoor and M Sharma ldquoBilateral mal-rotation and a congenital pelvic kidney with varied vasculatureand altered hilar anatomyrdquo Case Reports in Medicine vol 2015Article ID 848949 3 pages 2015

[17] C Krishnaveni and R Kulkarni ldquoA right ectopic kidney withbilateral multiple anomalies of the renal vasculature ndash a casereportrdquo Journal of Clinical and Diagnostic Research vol 7 pp150ndash153 2013

[18] C Cases L Garcıa-Zoghby P Manzorro et al ldquoAnatomicalvariations of the renal arteries Cadaveric and radiologic studyreview of the literature and proposal of a new classification ofclinical interestrdquo Annals of Anatomy - Anatomischer Anzeigervol 211 pp 61ndash68 2017

Case Reports in Vascular Medicine 7

[19] O Kornafel B Baran I Pawlikowska P Laszczynski MGuzinski and M Sasiadek ldquoAnalysis of anatomical variationsof the main arteries branching from the abdominal aorta with64-detector computed tomographyrdquoPolish Journal of Radiologyvol 75 pp 38ndash45 2010

[20] F J B Sampaio and M A R F Passos ldquoRenal arteriesanatomic study for surgical and radiological practicerdquo Surgicaland Radiologic Anatomy vol 14 no 2 pp 113ndash117 1992

[21] D T Tardo C Briggs G Ahern A Pitman and S SinhaldquoAnatomical variations of the renal arterial vasculature AnAus-tralian perspectiverdquo Journal of Medical Imaging and RadiationOncology vol 61 no 5 pp 643ndash649 2017

[22] J R Geyer and E F Poutasse ldquoIncidence of multiple renalarteries on aortography report of a series of 400 patients 381of whom had arterial hypertensionrdquo Journal of the AmericanMedical Association vol 182 no 2 pp 120ndash125 1962

[23] F T Graves ldquoThe arterial anatomy of the congenitally abnormalkidneyrdquo British Journal of Surgery vol 56 no 7 pp 533ndash5411969

[24] R J Merklin and N A Michels ldquoThe variant renal andsuprarenal blood supply with data on the inferior phrenicureteral and gonadal arteries A statistical analysis based on185 dissections and review of the literaturerdquo Journal of theInternational College of Surgeons vol 29 no 1 pp 41ndash76 1958

[25] A H Young and P Thompson ldquoAbnormalities of the renalarteries with remarks on their development and morphologyrdquoJournal of Anatomy vol 38 pp 1ndash14 1903

[26] J-P Trigaux S Vandroogenbroek J-F De Wispelaere MLacrosse and J Jamart ldquoCongenital anomalies of the inferiorvena cava and left renal vein Evaluation with spiral ctrdquo Journalof Vascular and Interventional Radiology vol 9 no 2 pp 339ndash345 1998

[27] S Kawamoto L P Lawler andE K Fishman ldquoEvaluation of therenal venous system on late arterial and venous phase imageswith MDCT angiography in potential living laparoscopic renaldonorsrdquo American Journal of Roentgenology vol 184 no 2 pp539ndash545 2005

[28] J Zhu L Zhang Z Yang H Zhou and G Tang ldquoClassificationof the renal vein variations a study with multidetector com-puted tomographyrdquo Surgical and Radiologic Anatomy vol 37no 6 pp 667ndash675 2015

[29] T Ichikawa S Kawada J Koizumi et al ldquoMajor venousanomalies are frequently associated with horseshoe kidneysrdquoCirculation Journal vol 75 no 12 pp 2872ndash2877 2011

[30] J T J Privett W D Jeans and J Roylance ldquoThe incidence andimportance of renal duplicationrdquo Clinical Radiology vol 27 no4 pp 521ndash530 1976

[31] P L Willan and J R Humpherson ldquoConcepts of variation andnormality in morphology Important issues at risk of neglect inmodern undergraduatemedical coursesrdquoClinical Anatomy vol12 pp 186ndash190 1999

[32] A Raikos and J D Smith ldquoAnatomical variations How dosurgical and radiology training programs teach and assess themin their training curriculardquoClinical Anatomy vol 28 no 6 pp717ndash724 2015

[33] N Rani S Singh P Dhar and R Kumar ldquoSurgical impor-tance of arterial segments of human kidneys An angiographyand corrosion cast studyrdquo Journal of Clinical and DiagnosticResearch vol 8 pp 1ndash3 2014

[34] S Ersoz A Tuzuner B Erkek S Esen and E Anadol ldquoDou-ble renal arteries in living-related kidney transplantationrdquoTransplantation Proceedings vol 32 no 3 p 604 2000

[35] V Ravery O Cussenot F Desgrandchamps et al ldquoVariationsin arterial blood supply and the risk of hemorrhage duringpercutaneous treatment of lesions of the pelviureteral junctionobstruction report of a case of testicular artery arising froman inferior polar renal arteryrdquo Surgical and Radiologic Anatomyvol 15 no 4 pp 355ndash359 1993

[36] T Sadler ldquoUrogenital systemrdquo in Langmanrsquos medical embryol-ogy Lippinott Williams amp Wilkins Baltimore MD USA 12thedition 2012

[37] K L Moore and T V N Persaud ldquoThe cardiovascular systemrdquoin The Developing Human Clinically Oriented Embryology pp330ndash335 Saunders Philadelphia Pa USA 7th edition 2003

[38] G C Schoenwolf S B Bleyl P R Brauer and P H Francis-West ldquoDevelopment of the vasculaturerdquo in Larsenrsquos humanembryology pp 385ndash432 Churchhill Livingstone PhiladelphiaPa USA 4th edition 2009

[39] K I Glassberg ldquoNormal and abnormal development of thekidney A clinicianrsquos interpretation of current knowledgerdquoThe Journal of Urology vol 167 no 6 pp 2339ndash2350 2002discussion 2350-2331

[40] N D Rosenblum ldquoDevelopmental biology of the humankidneyrdquo Seminars in Fetal and Neonatal Medicine vol 13 no3 pp 125ndash132 2008

Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

EndocrinologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Disease Markers

Hindawiwwwhindawicom Volume 2018

BioMed Research International

OncologyJournal of

Hindawiwwwhindawicom Volume 2013

Hindawiwwwhindawicom Volume 2018

Oxidative Medicine and Cellular Longevity

Hindawiwwwhindawicom Volume 2018

PPAR Research

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Immunology ResearchHindawiwwwhindawicom Volume 2018

Journal of

ObesityJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Computational and Mathematical Methods in Medicine

Hindawiwwwhindawicom Volume 2018

Behavioural Neurology

OphthalmologyJournal of

Hindawiwwwhindawicom Volume 2018

Diabetes ResearchJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Research and TreatmentAIDS

Hindawiwwwhindawicom Volume 2018

Gastroenterology Research and Practice

Hindawiwwwhindawicom Volume 2018

Parkinsonrsquos Disease

Evidence-Based Complementary andAlternative Medicine

Volume 2018Hindawiwwwhindawicom

Submit your manuscripts atwwwhindawicom

Page 3: A Case Study of Malrotated Kidneys with Asymmetric ...downloads.hindawi.com/journals/crivam/2019/1893137.pdf · CaseReport A Case Study of Malrotated Kidneys with Asymmetric Multiple

Case Reports in Vascular Medicine 3

lsRA

lmRAriRA

rCiA lCiA

rsRA

IMA

lsRV

rsRV

riRV

IVC

liRV

rSU

rRPlRP

lU

riU

(a) (b) (c) (d)

Figure 2 Ex situ renal system exhibits anatomical variations from normal pattern (a) Uncolorized renal system ex situ (b) Arterial networkpseudocolorized in red rsRA = right superior renal artery lsRA = left superior renal artery IMA = inferior mesenteric artery riRA = rightinferior renal artery lmRA = leftmiddle renal artery liRA = left inferior renal artery rCiRA = right common iliac artery lCiA = left commoniliac artery (c) Venous network pseudocolorized in blue IVC = inferior vena cava rsRV = right superior renal vein lsRV = left superior renalvein riRV = right inferior renal vein liRV = left inferior renal vein (d) Ureters pseudocolorized in yellow with rRP = right renal pelvis lRP= left renal pelvis rU = right ureters lU= left ureter Pseudocolorization created using Adobe Photoshop Image scale bar = 2 cm

(a) (b) (c) (d)

lU

lRP

liRV

lsRVlsRA

liRA

lCiV

lCiA

liRV

lmRA

IMA

lsRA

lmRA

liRA

Figure 3 Ex situ left kidney exhibits anatomical variations Anterior (a b) and posterior (c d) views of the left kidney Arterial venous andureteric systems (b d) are pseudocolorized in red (arterial) blue (venous) and yellow (ureteric) Renal veins (lsRV liRV) are reflected to betterillustrate the arterial pattern Image scale bar = 2 cm

investigation of the ureterovesical junctions was not com-pleted however a distinct orifice near the bladder trigone wasevident for each ureter On the contralateral side the singleureter emerged from a widened and anteriorly projectedhilum (Figure 3(b)) Major calyces from the peripheralparenchyma were evident and these calyces contributed to anelongated renal pelvisThe remaining course of the left ureterwas unremarkable

3 Discussion

Rare case studies present opportunities to not only considerthe observed morphological variations but also revisit under-lying concepts in embryology and the associated educationalimplications Variations in the arterial venous and ureteral

patterning of the kidneys are common however involve-ment with all three systems is very rare The current casedemonstrates concomitant variation in the arterial venousand ureteral systems which is conservatively estimated tohave an incidence of less than 03

31 Anatomic Variation Arterial variants have been ob-served in approximately 30of individuals althoughpopula-tion specific incidences have been shown to vary considerably[1 8] Studies documenting the major renal branches ratherthan the branching pattern into kidney parenchyma suggestthat arterial origins along the entire abdominal aortic axisare possible Branches at or superior to the level of thesuperior mesenteric artery [9] and along the lumbar region[10ndash14] have been well documented Arterial branching from

4 Case Reports in Vascular Medicine

rsRA

rsU

riRV

rRP

riU

riRA

rsRV

IVC

riRV

rsU

riU

riRA

rsRV

rsRA

(a) (b) (c) (d)

Figure 4 Ex situ right kidney exhibits anatomical variations Anterior (a b) and posterior (c d) views of the right kidney Arterial venousand ureteric systems (b d) are pseudocolorized in red (arterial) blue (venous) and yellow (ureteric)

the iliac axis has also been documented particularly inectopic kidneys [15ndash17] however ectopic specimens withoutpelvic involvement have also demonstrated branches arisingfrom the iliac region [14 18] Bilateral variation in thearterial patterning has been quantified with an incidence ofapproximately 10 [19] while unilateral arterial supply tothe kidney arising from all of these regions has a suggestedincidence of approximately 04 [20 21]

Although early modern attempts to quantify patterningthrough direct patient (andor cadaveric) observation (eg[22ndash24]) were compelling more recent studies using imaging(eg [18 19 21]) have verified and improved our understand-ing of the incidence for these arterial patterns They havebeen classified in Patterns (I-V) and Types (A-E) based onthe number of vessels observed and the location from whichthe vessels arise respectively From these studies the arterialdistribution to the right kidney in the current specimengenerally fits the description for Pattern II and Type D wheretwo arteries enter the kidney and the inferior renal segmentis supplied directly from the aorta This arterial patterntypehas an incidence rate of approximately 2 The left kidneyin the current specimen most closely demonstrates PatternIII with 3-4 distinct arteries but the Type descriptor fallsoutside of the general classification schema Here the currentspecimen is most similar to case studies presented throughdirect observation in cadaveric specimens [25] or visualizedthrough CT-3D reconstruction [18] Although Cases et aldid not include a reconstructed case in the analysis thedata set would suggest an hypothesized incidence for thecurrent arterial pattern to be at minimum of 04 Howevera statistically sound meta-analysis that includes specificbranching categories across studies has yet to be completed

As with the arterial system variation in renal veinpatterning is not uncommon Studies with large sample sizes(eg gt100) suggest that variation in venous patterning hasan incidence of 235-30 as observed through computedtomography (CT) [3 26ndash28] This reported incidence hasalso been observed in 105 cases of horseshoe kidney [29]Given the high incidence of renal vein variation a recentstudy used CT to observe and classify these variations within

a comparatively large sample size (1452 patients) [28] Inthis classification system the venous drainage of the rightkidney in the current specimen could be described as Type2A (03 incidence) with direct drainage into the IVC fromtwo renal veins The venous drainage of the left kidney couldbe described as Type IB (14 incidence) with drainage intothe IVC and common iliac vein What is unclear from thesestudies is if the incidence rates are applicable for bilateralvariations

Variation in ureteral patterning is not as common asthat found in the vascular system but reports indicate anapproximate incidence of 1 [6 7] with unilateral duplexkidney reported as high as 18 [30] Incidence of ureteralduplication appears to have a familial pattern of inheritance[4 5] that for a duplex kidney results from more than oneureteric bud outgrowth from the mesonephric duct duringfetal development

As outlined above aspects of the variations described inthe current case have been observed elsewhere Howeverfew of those cases have provided detailed descriptions andillustrations of concomitant involvement of each systemCollectively this case appears to be rare given the lowincidence rates for each (independent) system arterial 04venous 03-14 and ureteral 1-18 Based on this reviewof studies and using the reported systems-related variationthe incidence rate for the current specimen is conservativelyestimated at less than 03 of the population

32 Educational and Embryological Considerations Studentswho participate in dissection courses early in their trainingor students rotating through their clinical training learnthe basic premise of anatomic variationmdashthat organsregionsunder study often do not appear at least at first as out-lined in a referenced source Distinguishing which variationshave clinical significance requires both breadth and depthof training particularly within each clinical specialty [31]Although exposure to the concept of variation usually occursearly in training and primarily through dissection courses[31] many of the regionorgan details are often revisitedwithin clinical clerkships and during residency training [32]

Case Reports in Vascular Medicine 5

embryonic anatomicvariations

anatomicvariations

subcardinal vsupracardinal vposterior cardinal v

anatomicvariations

7 wee

ks6

week

s5

week

s

7 wee

ks6

week

s5

week

sstages

embryonicstages

embryonicem

bryo

logy

case

stud

ystages

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

(=)() (<)

(a) (b) (c)

Figure 5 Simplified schematic representation of renal development Around 5 weeks of fetal life kidneys are formed from the metanephrosThey are situated at the level of the pelvis and pelvic branches of the common iliac artery provide initial arterial blood supply During thefollowing 3 weeks the kidneys ascend in the abdominal cavity (a) to their adult retroperitoneal location As they move cranially and themetanephros coalesces the lower arteries degenerate to most often leave a single renal artery as the main arterial supply Occasionally thetemporary arteries (dotted lines (a)) do not degenerate leading to anatomical variations in the adult (a1015840) The cardinal systems contributeto the developing venous network of the kidney as it ascends (b) Persistence of some aspects of the developing venous network may leadto anatomical variations in the adult (dotted lines (b) (b1015840)) More than one ureteric bud may penetrate the metanephric mesoderm duringureteral development (c) that results in duplex kidney (left (c1015840))

For example variations in renal arterial patterning mayhave little clinical significance unless they are coupled withhypertension or require mapping for clinical procedures suchas surgical resection (eg [33]) transplantation (eg [34]) orpercutaneous access (eg [35]) Given the multisystem (iearterial venous and ureteral) involvement this case clearlydemonstrates the anatomical aspect of this concept

Collectively the anatomic variations of the current casealso reflect important concepts related to the morphologicaldevelopment of the kidney and its collecting system Duringhuman development three slightly overlapping renal systemsare formed in a cranial to caudal fashion pronephrosmesonephros and metanephros [36] The pronephros is atemporary organ that regresses at the end of the fourthweek of fetal life while the mesonephros contributes toBowmanrsquos capsule and the Wolffian duct in adult kidneysThe metanephros appears in the fifth week of fetal life andwill give rise to the adult kidney The renal excretory unitsoriginate from the metanephric mesoderm and collectingducts from the ureteric bud that penetrates the mesodermictissue While the primordial kidneys are initially locatedwithin the pelvis with their hila projected anteriorly to receivetheir arterial supply from a pelvic branch of the aorta thisorientation changeswith development Following growth andchange in body length at the lumbar and sacral regionsthe kidneys undergo a relative ldquoascentrdquo in the abdomen asthey shift to a more cranial position [37 38] This ascent is

accompanied by a transitioning arterial supply originatingfrom aortic branches at sequentially higher levels and medialrotation of the developing kidney as schematically depictedin Figure 5(a) The lower vessels usually degenerate butoccasionally some remain leading to anatomical variationsin the adult (Figures 2(b) 3(b) 3(c) 4(b) 4(d) and 5(a1015840))

Unlike the arterial system the venous system for the kid-ney arises from anastomotic connections between the devel-oping cardinal veins [38] Briefly at 5-6weeks of developmentthe posterior and subcardinal veins exhibit anastomoticconnections in a segment-like fashion that drain aspects ofthe early mesonephros The subcardinal veins anastomoseand coalesce in the midline contributing to the prerenalportion of the IVC and what is generally considered thedeveloped right renal vein Supracardinal veins like the otherrenal contributors begin as bilaterally symmetric havingsegmental connections with the posterior cardinal veins Asdevelopment continues the posterior cardinal veins degener-ate losing the segmental nature of the connections that wereestablished earlier with the subcardinal and supracardinalnetwork Ultimately the supracardinal system contributes tothe postrenal segment of the IVC This segment fuses withcaudal posterior cardinal segment that in turn gives rise tothe common iliac veins Concomitantly the supracardinalsystem on the left side loses connections with the developedleft renal vein and the hemiazygos system Even with thissimplified overview of a very complex developmental process

6 Case Reports in Vascular Medicine

(Figure 5(b)) the persistent connections between the venouscardinal networks (Figures 2(c) 3(b) 4(b) and 5(b1015840)) can beobserved in the current specimen

Development of the ureters arises from bud outgrowthsof the mesonephric duct For each kidney the ureteric budpenetrates the metanephric mesoderm (metanephrogenicblastema) that forms a cap intowhich the renal pelvis calyxesand collecting tubules develop through branching morpho-genesis [36] The stalk of the ureteric bud elongates as thekidney undergoes its relative ascent resulting in the formedureter by the ninth week of development (Figure 5(c)) Thesimultaneous morphogenesis of the vascular and uretericstructures influences themedial rotation of the hilum for eachdeveloping kidney Details of the signaling pathways and thegenes that regulate this entire process have been effectivelysummarized in the literature [39 40] and are beyond thescope of this case studyThese processes coupled with geneticfactors may give rise to variations in the ureteric pattern(Figures 2(d) 4(b) 4(d) 5(c) and 5(c1015840))

4 Conclusion

Anatomic variations in the systems of the developing kidneyare common however concomitant involvement of thearterial venous and ureteric systems is rare The currentcase study demonstrates a cadaveric specimen with anatomicvariations having an estimated incidence of less than 03Collectively this case illustrates examples of importantanatomic concepts that are relevant for educational andclinical practice

Conflicts of Interest

This work was completed without financial sponsorshipThe authors declare no conflicts of interest Portions of thiswork have been presented in abstract form at conferenceproceedings

Authorsrsquo Contributions

Marc A Pizzimenti contributed in project developmentdissection and manuscript writing Martine Dunnwald con-tributed in dissection illustrations and manuscript writing

Acknowledgments

The authors would like to thank the families of individualswho through their most generous gift to the Deeded BodyProgram allow us to continue studying the human body

References

[1] E Gulas G Wysiadecki T Cecot et al ldquoAccessory (multi-ple) renal arteries ndash Differences in frequency according topopulation visualizing techniques and stage of morphologicaldevelopmentrdquo Vascular vol 24 no 5 pp 531ndash537 2016

[2] R Bergman SThompson AAfifi and F SaadehCompendiumofHumanAnatomic Variation Text Atlas andWorld Literature

Urban amp Scharzenberg Inc Baltimore Munich Germany1988

[3] Z Koc S Ulusan L Oguzkurt and N Tokmak ldquoVenousvariants and anomalies on routine abdominal multi-detectorrow CTrdquo European Journal of Radiology vol 61 no 2 pp 267ndash278 2007

[4] J D Atwell P L Cook C J Howell I Hyde and B C ParkerldquoFamilial incidence of bifid and double uretersrdquo Archives ofDisease in Childhood vol 49 no 5 pp 390ndash393 1974

[5] J Whitaker and D M Danks ldquoA study of the inheritance ofduplication of the kidneys and uretersrdquoThe Journal of Urologyvol 95 no 2 pp 176ndash178 1966

[6] V Alberts R Minnee K van Donselaar-van der Pant et alldquoDuplicated ureters and renal transplantation a case-controlstudy and review of the literaturerdquoTransplantation Proceedingsvol 45 no 9 pp 3239ndash3244 2013

[7] R Pollak B F Prusak and M F Mozes ldquoAnatomic abnormal-ities of cadaver kidneys procured for purposes of transplanta-tionrdquoThe American Surgeon vol 52 no 5 pp 233ndash235 1986

[8] K S Satyapal A A Haffejee B Singh L Ramsaroop J VRobbs and J M Kalideen ldquoAdditional renal arteries Incidenceand morphometryrdquo Surgical and Radiologic Anatomy vol 23no 1 pp 33ndash38 2001

[9] C Dalcik T Colak A Ozbek and H Dalcik ldquoUnusual originof the right renal artery a case reportrdquo Surgical and RadiologicAnatomy vol 22 no 2 pp 117-118 2000

[10] U G Rossi M Romano and C Ferro ldquoSeven renal arteriesrdquoClinical Anatomy vol 19 no 7 pp 632-633 2006

[11] P Mazengenya ldquoMultiple variations of the renal and testicularvessels possible embryological basis and clinical importancerdquoSurgical and Radiologic Anatomy vol 38 no 6 pp 729ndash7332016

[12] K Morishima T Miyaki and H Ito ldquoA rare case of a kidneywith an (sic) widely opened hilus and supernumerary renalvesselsrdquoKaibogaku Zasshi Journal of Anatomy vol 71 no 3 pp215ndash218 1996

[13] H Narita T Tani and Y Tonosaki ldquoAssociations betweenkidney position and surplus renal arteries in horseshoe kidneyCase report and analysisrdquo Okajimas Folia Anatomica Japonicavol 89 no 1 pp 7ndash13 2012

[14] S T Patil MMMeshram and A P Kasote ldquoBilateral malrota-tion and lobulation of kidney with altered hilar anatomy a rarecongenital variationrdquo Surgical and Radiologic Anatomy vol 33no 10 pp 941ndash944 2011

[15] S Degani Z Leibovitz I Shapiro and G Ohel ldquoVariationsof the origin of renal arteries in the fetus identified on powerDoppler and 3D sonographyrdquo Journal of Clinical Ultrasoundvol 38 no 2 pp 59ndash65 2009

[16] J Singh N Singh K Kapoor and M Sharma ldquoBilateral mal-rotation and a congenital pelvic kidney with varied vasculatureand altered hilar anatomyrdquo Case Reports in Medicine vol 2015Article ID 848949 3 pages 2015

[17] C Krishnaveni and R Kulkarni ldquoA right ectopic kidney withbilateral multiple anomalies of the renal vasculature ndash a casereportrdquo Journal of Clinical and Diagnostic Research vol 7 pp150ndash153 2013

[18] C Cases L Garcıa-Zoghby P Manzorro et al ldquoAnatomicalvariations of the renal arteries Cadaveric and radiologic studyreview of the literature and proposal of a new classification ofclinical interestrdquo Annals of Anatomy - Anatomischer Anzeigervol 211 pp 61ndash68 2017

Case Reports in Vascular Medicine 7

[19] O Kornafel B Baran I Pawlikowska P Laszczynski MGuzinski and M Sasiadek ldquoAnalysis of anatomical variationsof the main arteries branching from the abdominal aorta with64-detector computed tomographyrdquoPolish Journal of Radiologyvol 75 pp 38ndash45 2010

[20] F J B Sampaio and M A R F Passos ldquoRenal arteriesanatomic study for surgical and radiological practicerdquo Surgicaland Radiologic Anatomy vol 14 no 2 pp 113ndash117 1992

[21] D T Tardo C Briggs G Ahern A Pitman and S SinhaldquoAnatomical variations of the renal arterial vasculature AnAus-tralian perspectiverdquo Journal of Medical Imaging and RadiationOncology vol 61 no 5 pp 643ndash649 2017

[22] J R Geyer and E F Poutasse ldquoIncidence of multiple renalarteries on aortography report of a series of 400 patients 381of whom had arterial hypertensionrdquo Journal of the AmericanMedical Association vol 182 no 2 pp 120ndash125 1962

[23] F T Graves ldquoThe arterial anatomy of the congenitally abnormalkidneyrdquo British Journal of Surgery vol 56 no 7 pp 533ndash5411969

[24] R J Merklin and N A Michels ldquoThe variant renal andsuprarenal blood supply with data on the inferior phrenicureteral and gonadal arteries A statistical analysis based on185 dissections and review of the literaturerdquo Journal of theInternational College of Surgeons vol 29 no 1 pp 41ndash76 1958

[25] A H Young and P Thompson ldquoAbnormalities of the renalarteries with remarks on their development and morphologyrdquoJournal of Anatomy vol 38 pp 1ndash14 1903

[26] J-P Trigaux S Vandroogenbroek J-F De Wispelaere MLacrosse and J Jamart ldquoCongenital anomalies of the inferiorvena cava and left renal vein Evaluation with spiral ctrdquo Journalof Vascular and Interventional Radiology vol 9 no 2 pp 339ndash345 1998

[27] S Kawamoto L P Lawler andE K Fishman ldquoEvaluation of therenal venous system on late arterial and venous phase imageswith MDCT angiography in potential living laparoscopic renaldonorsrdquo American Journal of Roentgenology vol 184 no 2 pp539ndash545 2005

[28] J Zhu L Zhang Z Yang H Zhou and G Tang ldquoClassificationof the renal vein variations a study with multidetector com-puted tomographyrdquo Surgical and Radiologic Anatomy vol 37no 6 pp 667ndash675 2015

[29] T Ichikawa S Kawada J Koizumi et al ldquoMajor venousanomalies are frequently associated with horseshoe kidneysrdquoCirculation Journal vol 75 no 12 pp 2872ndash2877 2011

[30] J T J Privett W D Jeans and J Roylance ldquoThe incidence andimportance of renal duplicationrdquo Clinical Radiology vol 27 no4 pp 521ndash530 1976

[31] P L Willan and J R Humpherson ldquoConcepts of variation andnormality in morphology Important issues at risk of neglect inmodern undergraduatemedical coursesrdquoClinical Anatomy vol12 pp 186ndash190 1999

[32] A Raikos and J D Smith ldquoAnatomical variations How dosurgical and radiology training programs teach and assess themin their training curriculardquoClinical Anatomy vol 28 no 6 pp717ndash724 2015

[33] N Rani S Singh P Dhar and R Kumar ldquoSurgical impor-tance of arterial segments of human kidneys An angiographyand corrosion cast studyrdquo Journal of Clinical and DiagnosticResearch vol 8 pp 1ndash3 2014

[34] S Ersoz A Tuzuner B Erkek S Esen and E Anadol ldquoDou-ble renal arteries in living-related kidney transplantationrdquoTransplantation Proceedings vol 32 no 3 p 604 2000

[35] V Ravery O Cussenot F Desgrandchamps et al ldquoVariationsin arterial blood supply and the risk of hemorrhage duringpercutaneous treatment of lesions of the pelviureteral junctionobstruction report of a case of testicular artery arising froman inferior polar renal arteryrdquo Surgical and Radiologic Anatomyvol 15 no 4 pp 355ndash359 1993

[36] T Sadler ldquoUrogenital systemrdquo in Langmanrsquos medical embryol-ogy Lippinott Williams amp Wilkins Baltimore MD USA 12thedition 2012

[37] K L Moore and T V N Persaud ldquoThe cardiovascular systemrdquoin The Developing Human Clinically Oriented Embryology pp330ndash335 Saunders Philadelphia Pa USA 7th edition 2003

[38] G C Schoenwolf S B Bleyl P R Brauer and P H Francis-West ldquoDevelopment of the vasculaturerdquo in Larsenrsquos humanembryology pp 385ndash432 Churchhill Livingstone PhiladelphiaPa USA 4th edition 2009

[39] K I Glassberg ldquoNormal and abnormal development of thekidney A clinicianrsquos interpretation of current knowledgerdquoThe Journal of Urology vol 167 no 6 pp 2339ndash2350 2002discussion 2350-2331

[40] N D Rosenblum ldquoDevelopmental biology of the humankidneyrdquo Seminars in Fetal and Neonatal Medicine vol 13 no3 pp 125ndash132 2008

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Disease Markers

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Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

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Evidence-Based Complementary andAlternative Medicine

Volume 2018Hindawiwwwhindawicom

Submit your manuscripts atwwwhindawicom

Page 4: A Case Study of Malrotated Kidneys with Asymmetric ...downloads.hindawi.com/journals/crivam/2019/1893137.pdf · CaseReport A Case Study of Malrotated Kidneys with Asymmetric Multiple

4 Case Reports in Vascular Medicine

rsRA

rsU

riRV

rRP

riU

riRA

rsRV

IVC

riRV

rsU

riU

riRA

rsRV

rsRA

(a) (b) (c) (d)

Figure 4 Ex situ right kidney exhibits anatomical variations Anterior (a b) and posterior (c d) views of the right kidney Arterial venousand ureteric systems (b d) are pseudocolorized in red (arterial) blue (venous) and yellow (ureteric)

the iliac axis has also been documented particularly inectopic kidneys [15ndash17] however ectopic specimens withoutpelvic involvement have also demonstrated branches arisingfrom the iliac region [14 18] Bilateral variation in thearterial patterning has been quantified with an incidence ofapproximately 10 [19] while unilateral arterial supply tothe kidney arising from all of these regions has a suggestedincidence of approximately 04 [20 21]

Although early modern attempts to quantify patterningthrough direct patient (andor cadaveric) observation (eg[22ndash24]) were compelling more recent studies using imaging(eg [18 19 21]) have verified and improved our understand-ing of the incidence for these arterial patterns They havebeen classified in Patterns (I-V) and Types (A-E) based onthe number of vessels observed and the location from whichthe vessels arise respectively From these studies the arterialdistribution to the right kidney in the current specimengenerally fits the description for Pattern II and Type D wheretwo arteries enter the kidney and the inferior renal segmentis supplied directly from the aorta This arterial patterntypehas an incidence rate of approximately 2 The left kidneyin the current specimen most closely demonstrates PatternIII with 3-4 distinct arteries but the Type descriptor fallsoutside of the general classification schema Here the currentspecimen is most similar to case studies presented throughdirect observation in cadaveric specimens [25] or visualizedthrough CT-3D reconstruction [18] Although Cases et aldid not include a reconstructed case in the analysis thedata set would suggest an hypothesized incidence for thecurrent arterial pattern to be at minimum of 04 Howevera statistically sound meta-analysis that includes specificbranching categories across studies has yet to be completed

As with the arterial system variation in renal veinpatterning is not uncommon Studies with large sample sizes(eg gt100) suggest that variation in venous patterning hasan incidence of 235-30 as observed through computedtomography (CT) [3 26ndash28] This reported incidence hasalso been observed in 105 cases of horseshoe kidney [29]Given the high incidence of renal vein variation a recentstudy used CT to observe and classify these variations within

a comparatively large sample size (1452 patients) [28] Inthis classification system the venous drainage of the rightkidney in the current specimen could be described as Type2A (03 incidence) with direct drainage into the IVC fromtwo renal veins The venous drainage of the left kidney couldbe described as Type IB (14 incidence) with drainage intothe IVC and common iliac vein What is unclear from thesestudies is if the incidence rates are applicable for bilateralvariations

Variation in ureteral patterning is not as common asthat found in the vascular system but reports indicate anapproximate incidence of 1 [6 7] with unilateral duplexkidney reported as high as 18 [30] Incidence of ureteralduplication appears to have a familial pattern of inheritance[4 5] that for a duplex kidney results from more than oneureteric bud outgrowth from the mesonephric duct duringfetal development

As outlined above aspects of the variations described inthe current case have been observed elsewhere Howeverfew of those cases have provided detailed descriptions andillustrations of concomitant involvement of each systemCollectively this case appears to be rare given the lowincidence rates for each (independent) system arterial 04venous 03-14 and ureteral 1-18 Based on this reviewof studies and using the reported systems-related variationthe incidence rate for the current specimen is conservativelyestimated at less than 03 of the population

32 Educational and Embryological Considerations Studentswho participate in dissection courses early in their trainingor students rotating through their clinical training learnthe basic premise of anatomic variationmdashthat organsregionsunder study often do not appear at least at first as out-lined in a referenced source Distinguishing which variationshave clinical significance requires both breadth and depthof training particularly within each clinical specialty [31]Although exposure to the concept of variation usually occursearly in training and primarily through dissection courses[31] many of the regionorgan details are often revisitedwithin clinical clerkships and during residency training [32]

Case Reports in Vascular Medicine 5

embryonic anatomicvariations

anatomicvariations

subcardinal vsupracardinal vposterior cardinal v

anatomicvariations

7 wee

ks6

week

s5

week

s

7 wee

ks6

week

s5

week

sstages

embryonicstages

embryonicem

bryo

logy

case

stud

ystages

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

(=)() (<)

(a) (b) (c)

Figure 5 Simplified schematic representation of renal development Around 5 weeks of fetal life kidneys are formed from the metanephrosThey are situated at the level of the pelvis and pelvic branches of the common iliac artery provide initial arterial blood supply During thefollowing 3 weeks the kidneys ascend in the abdominal cavity (a) to their adult retroperitoneal location As they move cranially and themetanephros coalesces the lower arteries degenerate to most often leave a single renal artery as the main arterial supply Occasionally thetemporary arteries (dotted lines (a)) do not degenerate leading to anatomical variations in the adult (a1015840) The cardinal systems contributeto the developing venous network of the kidney as it ascends (b) Persistence of some aspects of the developing venous network may leadto anatomical variations in the adult (dotted lines (b) (b1015840)) More than one ureteric bud may penetrate the metanephric mesoderm duringureteral development (c) that results in duplex kidney (left (c1015840))

For example variations in renal arterial patterning mayhave little clinical significance unless they are coupled withhypertension or require mapping for clinical procedures suchas surgical resection (eg [33]) transplantation (eg [34]) orpercutaneous access (eg [35]) Given the multisystem (iearterial venous and ureteral) involvement this case clearlydemonstrates the anatomical aspect of this concept

Collectively the anatomic variations of the current casealso reflect important concepts related to the morphologicaldevelopment of the kidney and its collecting system Duringhuman development three slightly overlapping renal systemsare formed in a cranial to caudal fashion pronephrosmesonephros and metanephros [36] The pronephros is atemporary organ that regresses at the end of the fourthweek of fetal life while the mesonephros contributes toBowmanrsquos capsule and the Wolffian duct in adult kidneysThe metanephros appears in the fifth week of fetal life andwill give rise to the adult kidney The renal excretory unitsoriginate from the metanephric mesoderm and collectingducts from the ureteric bud that penetrates the mesodermictissue While the primordial kidneys are initially locatedwithin the pelvis with their hila projected anteriorly to receivetheir arterial supply from a pelvic branch of the aorta thisorientation changeswith development Following growth andchange in body length at the lumbar and sacral regionsthe kidneys undergo a relative ldquoascentrdquo in the abdomen asthey shift to a more cranial position [37 38] This ascent is

accompanied by a transitioning arterial supply originatingfrom aortic branches at sequentially higher levels and medialrotation of the developing kidney as schematically depictedin Figure 5(a) The lower vessels usually degenerate butoccasionally some remain leading to anatomical variationsin the adult (Figures 2(b) 3(b) 3(c) 4(b) 4(d) and 5(a1015840))

Unlike the arterial system the venous system for the kid-ney arises from anastomotic connections between the devel-oping cardinal veins [38] Briefly at 5-6weeks of developmentthe posterior and subcardinal veins exhibit anastomoticconnections in a segment-like fashion that drain aspects ofthe early mesonephros The subcardinal veins anastomoseand coalesce in the midline contributing to the prerenalportion of the IVC and what is generally considered thedeveloped right renal vein Supracardinal veins like the otherrenal contributors begin as bilaterally symmetric havingsegmental connections with the posterior cardinal veins Asdevelopment continues the posterior cardinal veins degener-ate losing the segmental nature of the connections that wereestablished earlier with the subcardinal and supracardinalnetwork Ultimately the supracardinal system contributes tothe postrenal segment of the IVC This segment fuses withcaudal posterior cardinal segment that in turn gives rise tothe common iliac veins Concomitantly the supracardinalsystem on the left side loses connections with the developedleft renal vein and the hemiazygos system Even with thissimplified overview of a very complex developmental process

6 Case Reports in Vascular Medicine

(Figure 5(b)) the persistent connections between the venouscardinal networks (Figures 2(c) 3(b) 4(b) and 5(b1015840)) can beobserved in the current specimen

Development of the ureters arises from bud outgrowthsof the mesonephric duct For each kidney the ureteric budpenetrates the metanephric mesoderm (metanephrogenicblastema) that forms a cap intowhich the renal pelvis calyxesand collecting tubules develop through branching morpho-genesis [36] The stalk of the ureteric bud elongates as thekidney undergoes its relative ascent resulting in the formedureter by the ninth week of development (Figure 5(c)) Thesimultaneous morphogenesis of the vascular and uretericstructures influences themedial rotation of the hilum for eachdeveloping kidney Details of the signaling pathways and thegenes that regulate this entire process have been effectivelysummarized in the literature [39 40] and are beyond thescope of this case studyThese processes coupled with geneticfactors may give rise to variations in the ureteric pattern(Figures 2(d) 4(b) 4(d) 5(c) and 5(c1015840))

4 Conclusion

Anatomic variations in the systems of the developing kidneyare common however concomitant involvement of thearterial venous and ureteric systems is rare The currentcase study demonstrates a cadaveric specimen with anatomicvariations having an estimated incidence of less than 03Collectively this case illustrates examples of importantanatomic concepts that are relevant for educational andclinical practice

Conflicts of Interest

This work was completed without financial sponsorshipThe authors declare no conflicts of interest Portions of thiswork have been presented in abstract form at conferenceproceedings

Authorsrsquo Contributions

Marc A Pizzimenti contributed in project developmentdissection and manuscript writing Martine Dunnwald con-tributed in dissection illustrations and manuscript writing

Acknowledgments

The authors would like to thank the families of individualswho through their most generous gift to the Deeded BodyProgram allow us to continue studying the human body

References

[1] E Gulas G Wysiadecki T Cecot et al ldquoAccessory (multi-ple) renal arteries ndash Differences in frequency according topopulation visualizing techniques and stage of morphologicaldevelopmentrdquo Vascular vol 24 no 5 pp 531ndash537 2016

[2] R Bergman SThompson AAfifi and F SaadehCompendiumofHumanAnatomic Variation Text Atlas andWorld Literature

Urban amp Scharzenberg Inc Baltimore Munich Germany1988

[3] Z Koc S Ulusan L Oguzkurt and N Tokmak ldquoVenousvariants and anomalies on routine abdominal multi-detectorrow CTrdquo European Journal of Radiology vol 61 no 2 pp 267ndash278 2007

[4] J D Atwell P L Cook C J Howell I Hyde and B C ParkerldquoFamilial incidence of bifid and double uretersrdquo Archives ofDisease in Childhood vol 49 no 5 pp 390ndash393 1974

[5] J Whitaker and D M Danks ldquoA study of the inheritance ofduplication of the kidneys and uretersrdquoThe Journal of Urologyvol 95 no 2 pp 176ndash178 1966

[6] V Alberts R Minnee K van Donselaar-van der Pant et alldquoDuplicated ureters and renal transplantation a case-controlstudy and review of the literaturerdquoTransplantation Proceedingsvol 45 no 9 pp 3239ndash3244 2013

[7] R Pollak B F Prusak and M F Mozes ldquoAnatomic abnormal-ities of cadaver kidneys procured for purposes of transplanta-tionrdquoThe American Surgeon vol 52 no 5 pp 233ndash235 1986

[8] K S Satyapal A A Haffejee B Singh L Ramsaroop J VRobbs and J M Kalideen ldquoAdditional renal arteries Incidenceand morphometryrdquo Surgical and Radiologic Anatomy vol 23no 1 pp 33ndash38 2001

[9] C Dalcik T Colak A Ozbek and H Dalcik ldquoUnusual originof the right renal artery a case reportrdquo Surgical and RadiologicAnatomy vol 22 no 2 pp 117-118 2000

[10] U G Rossi M Romano and C Ferro ldquoSeven renal arteriesrdquoClinical Anatomy vol 19 no 7 pp 632-633 2006

[11] P Mazengenya ldquoMultiple variations of the renal and testicularvessels possible embryological basis and clinical importancerdquoSurgical and Radiologic Anatomy vol 38 no 6 pp 729ndash7332016

[12] K Morishima T Miyaki and H Ito ldquoA rare case of a kidneywith an (sic) widely opened hilus and supernumerary renalvesselsrdquoKaibogaku Zasshi Journal of Anatomy vol 71 no 3 pp215ndash218 1996

[13] H Narita T Tani and Y Tonosaki ldquoAssociations betweenkidney position and surplus renal arteries in horseshoe kidneyCase report and analysisrdquo Okajimas Folia Anatomica Japonicavol 89 no 1 pp 7ndash13 2012

[14] S T Patil MMMeshram and A P Kasote ldquoBilateral malrota-tion and lobulation of kidney with altered hilar anatomy a rarecongenital variationrdquo Surgical and Radiologic Anatomy vol 33no 10 pp 941ndash944 2011

[15] S Degani Z Leibovitz I Shapiro and G Ohel ldquoVariationsof the origin of renal arteries in the fetus identified on powerDoppler and 3D sonographyrdquo Journal of Clinical Ultrasoundvol 38 no 2 pp 59ndash65 2009

[16] J Singh N Singh K Kapoor and M Sharma ldquoBilateral mal-rotation and a congenital pelvic kidney with varied vasculatureand altered hilar anatomyrdquo Case Reports in Medicine vol 2015Article ID 848949 3 pages 2015

[17] C Krishnaveni and R Kulkarni ldquoA right ectopic kidney withbilateral multiple anomalies of the renal vasculature ndash a casereportrdquo Journal of Clinical and Diagnostic Research vol 7 pp150ndash153 2013

[18] C Cases L Garcıa-Zoghby P Manzorro et al ldquoAnatomicalvariations of the renal arteries Cadaveric and radiologic studyreview of the literature and proposal of a new classification ofclinical interestrdquo Annals of Anatomy - Anatomischer Anzeigervol 211 pp 61ndash68 2017

Case Reports in Vascular Medicine 7

[19] O Kornafel B Baran I Pawlikowska P Laszczynski MGuzinski and M Sasiadek ldquoAnalysis of anatomical variationsof the main arteries branching from the abdominal aorta with64-detector computed tomographyrdquoPolish Journal of Radiologyvol 75 pp 38ndash45 2010

[20] F J B Sampaio and M A R F Passos ldquoRenal arteriesanatomic study for surgical and radiological practicerdquo Surgicaland Radiologic Anatomy vol 14 no 2 pp 113ndash117 1992

[21] D T Tardo C Briggs G Ahern A Pitman and S SinhaldquoAnatomical variations of the renal arterial vasculature AnAus-tralian perspectiverdquo Journal of Medical Imaging and RadiationOncology vol 61 no 5 pp 643ndash649 2017

[22] J R Geyer and E F Poutasse ldquoIncidence of multiple renalarteries on aortography report of a series of 400 patients 381of whom had arterial hypertensionrdquo Journal of the AmericanMedical Association vol 182 no 2 pp 120ndash125 1962

[23] F T Graves ldquoThe arterial anatomy of the congenitally abnormalkidneyrdquo British Journal of Surgery vol 56 no 7 pp 533ndash5411969

[24] R J Merklin and N A Michels ldquoThe variant renal andsuprarenal blood supply with data on the inferior phrenicureteral and gonadal arteries A statistical analysis based on185 dissections and review of the literaturerdquo Journal of theInternational College of Surgeons vol 29 no 1 pp 41ndash76 1958

[25] A H Young and P Thompson ldquoAbnormalities of the renalarteries with remarks on their development and morphologyrdquoJournal of Anatomy vol 38 pp 1ndash14 1903

[26] J-P Trigaux S Vandroogenbroek J-F De Wispelaere MLacrosse and J Jamart ldquoCongenital anomalies of the inferiorvena cava and left renal vein Evaluation with spiral ctrdquo Journalof Vascular and Interventional Radiology vol 9 no 2 pp 339ndash345 1998

[27] S Kawamoto L P Lawler andE K Fishman ldquoEvaluation of therenal venous system on late arterial and venous phase imageswith MDCT angiography in potential living laparoscopic renaldonorsrdquo American Journal of Roentgenology vol 184 no 2 pp539ndash545 2005

[28] J Zhu L Zhang Z Yang H Zhou and G Tang ldquoClassificationof the renal vein variations a study with multidetector com-puted tomographyrdquo Surgical and Radiologic Anatomy vol 37no 6 pp 667ndash675 2015

[29] T Ichikawa S Kawada J Koizumi et al ldquoMajor venousanomalies are frequently associated with horseshoe kidneysrdquoCirculation Journal vol 75 no 12 pp 2872ndash2877 2011

[30] J T J Privett W D Jeans and J Roylance ldquoThe incidence andimportance of renal duplicationrdquo Clinical Radiology vol 27 no4 pp 521ndash530 1976

[31] P L Willan and J R Humpherson ldquoConcepts of variation andnormality in morphology Important issues at risk of neglect inmodern undergraduatemedical coursesrdquoClinical Anatomy vol12 pp 186ndash190 1999

[32] A Raikos and J D Smith ldquoAnatomical variations How dosurgical and radiology training programs teach and assess themin their training curriculardquoClinical Anatomy vol 28 no 6 pp717ndash724 2015

[33] N Rani S Singh P Dhar and R Kumar ldquoSurgical impor-tance of arterial segments of human kidneys An angiographyand corrosion cast studyrdquo Journal of Clinical and DiagnosticResearch vol 8 pp 1ndash3 2014

[34] S Ersoz A Tuzuner B Erkek S Esen and E Anadol ldquoDou-ble renal arteries in living-related kidney transplantationrdquoTransplantation Proceedings vol 32 no 3 p 604 2000

[35] V Ravery O Cussenot F Desgrandchamps et al ldquoVariationsin arterial blood supply and the risk of hemorrhage duringpercutaneous treatment of lesions of the pelviureteral junctionobstruction report of a case of testicular artery arising froman inferior polar renal arteryrdquo Surgical and Radiologic Anatomyvol 15 no 4 pp 355ndash359 1993

[36] T Sadler ldquoUrogenital systemrdquo in Langmanrsquos medical embryol-ogy Lippinott Williams amp Wilkins Baltimore MD USA 12thedition 2012

[37] K L Moore and T V N Persaud ldquoThe cardiovascular systemrdquoin The Developing Human Clinically Oriented Embryology pp330ndash335 Saunders Philadelphia Pa USA 7th edition 2003

[38] G C Schoenwolf S B Bleyl P R Brauer and P H Francis-West ldquoDevelopment of the vasculaturerdquo in Larsenrsquos humanembryology pp 385ndash432 Churchhill Livingstone PhiladelphiaPa USA 4th edition 2009

[39] K I Glassberg ldquoNormal and abnormal development of thekidney A clinicianrsquos interpretation of current knowledgerdquoThe Journal of Urology vol 167 no 6 pp 2339ndash2350 2002discussion 2350-2331

[40] N D Rosenblum ldquoDevelopmental biology of the humankidneyrdquo Seminars in Fetal and Neonatal Medicine vol 13 no3 pp 125ndash132 2008

Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

EndocrinologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Disease Markers

Hindawiwwwhindawicom Volume 2018

BioMed Research International

OncologyJournal of

Hindawiwwwhindawicom Volume 2013

Hindawiwwwhindawicom Volume 2018

Oxidative Medicine and Cellular Longevity

Hindawiwwwhindawicom Volume 2018

PPAR Research

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Immunology ResearchHindawiwwwhindawicom Volume 2018

Journal of

ObesityJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Computational and Mathematical Methods in Medicine

Hindawiwwwhindawicom Volume 2018

Behavioural Neurology

OphthalmologyJournal of

Hindawiwwwhindawicom Volume 2018

Diabetes ResearchJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Research and TreatmentAIDS

Hindawiwwwhindawicom Volume 2018

Gastroenterology Research and Practice

Hindawiwwwhindawicom Volume 2018

Parkinsonrsquos Disease

Evidence-Based Complementary andAlternative Medicine

Volume 2018Hindawiwwwhindawicom

Submit your manuscripts atwwwhindawicom

Page 5: A Case Study of Malrotated Kidneys with Asymmetric ...downloads.hindawi.com/journals/crivam/2019/1893137.pdf · CaseReport A Case Study of Malrotated Kidneys with Asymmetric Multiple

Case Reports in Vascular Medicine 5

embryonic anatomicvariations

anatomicvariations

subcardinal vsupracardinal vposterior cardinal v

anatomicvariations

7 wee

ks6

week

s5

week

s

7 wee

ks6

week

s5

week

sstages

embryonicstages

embryonicem

bryo

logy

case

stud

ystages

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

CT

SMA

IMA

(=)() (<)

(a) (b) (c)

Figure 5 Simplified schematic representation of renal development Around 5 weeks of fetal life kidneys are formed from the metanephrosThey are situated at the level of the pelvis and pelvic branches of the common iliac artery provide initial arterial blood supply During thefollowing 3 weeks the kidneys ascend in the abdominal cavity (a) to their adult retroperitoneal location As they move cranially and themetanephros coalesces the lower arteries degenerate to most often leave a single renal artery as the main arterial supply Occasionally thetemporary arteries (dotted lines (a)) do not degenerate leading to anatomical variations in the adult (a1015840) The cardinal systems contributeto the developing venous network of the kidney as it ascends (b) Persistence of some aspects of the developing venous network may leadto anatomical variations in the adult (dotted lines (b) (b1015840)) More than one ureteric bud may penetrate the metanephric mesoderm duringureteral development (c) that results in duplex kidney (left (c1015840))

For example variations in renal arterial patterning mayhave little clinical significance unless they are coupled withhypertension or require mapping for clinical procedures suchas surgical resection (eg [33]) transplantation (eg [34]) orpercutaneous access (eg [35]) Given the multisystem (iearterial venous and ureteral) involvement this case clearlydemonstrates the anatomical aspect of this concept

Collectively the anatomic variations of the current casealso reflect important concepts related to the morphologicaldevelopment of the kidney and its collecting system Duringhuman development three slightly overlapping renal systemsare formed in a cranial to caudal fashion pronephrosmesonephros and metanephros [36] The pronephros is atemporary organ that regresses at the end of the fourthweek of fetal life while the mesonephros contributes toBowmanrsquos capsule and the Wolffian duct in adult kidneysThe metanephros appears in the fifth week of fetal life andwill give rise to the adult kidney The renal excretory unitsoriginate from the metanephric mesoderm and collectingducts from the ureteric bud that penetrates the mesodermictissue While the primordial kidneys are initially locatedwithin the pelvis with their hila projected anteriorly to receivetheir arterial supply from a pelvic branch of the aorta thisorientation changeswith development Following growth andchange in body length at the lumbar and sacral regionsthe kidneys undergo a relative ldquoascentrdquo in the abdomen asthey shift to a more cranial position [37 38] This ascent is

accompanied by a transitioning arterial supply originatingfrom aortic branches at sequentially higher levels and medialrotation of the developing kidney as schematically depictedin Figure 5(a) The lower vessels usually degenerate butoccasionally some remain leading to anatomical variationsin the adult (Figures 2(b) 3(b) 3(c) 4(b) 4(d) and 5(a1015840))

Unlike the arterial system the venous system for the kid-ney arises from anastomotic connections between the devel-oping cardinal veins [38] Briefly at 5-6weeks of developmentthe posterior and subcardinal veins exhibit anastomoticconnections in a segment-like fashion that drain aspects ofthe early mesonephros The subcardinal veins anastomoseand coalesce in the midline contributing to the prerenalportion of the IVC and what is generally considered thedeveloped right renal vein Supracardinal veins like the otherrenal contributors begin as bilaterally symmetric havingsegmental connections with the posterior cardinal veins Asdevelopment continues the posterior cardinal veins degener-ate losing the segmental nature of the connections that wereestablished earlier with the subcardinal and supracardinalnetwork Ultimately the supracardinal system contributes tothe postrenal segment of the IVC This segment fuses withcaudal posterior cardinal segment that in turn gives rise tothe common iliac veins Concomitantly the supracardinalsystem on the left side loses connections with the developedleft renal vein and the hemiazygos system Even with thissimplified overview of a very complex developmental process

6 Case Reports in Vascular Medicine

(Figure 5(b)) the persistent connections between the venouscardinal networks (Figures 2(c) 3(b) 4(b) and 5(b1015840)) can beobserved in the current specimen

Development of the ureters arises from bud outgrowthsof the mesonephric duct For each kidney the ureteric budpenetrates the metanephric mesoderm (metanephrogenicblastema) that forms a cap intowhich the renal pelvis calyxesand collecting tubules develop through branching morpho-genesis [36] The stalk of the ureteric bud elongates as thekidney undergoes its relative ascent resulting in the formedureter by the ninth week of development (Figure 5(c)) Thesimultaneous morphogenesis of the vascular and uretericstructures influences themedial rotation of the hilum for eachdeveloping kidney Details of the signaling pathways and thegenes that regulate this entire process have been effectivelysummarized in the literature [39 40] and are beyond thescope of this case studyThese processes coupled with geneticfactors may give rise to variations in the ureteric pattern(Figures 2(d) 4(b) 4(d) 5(c) and 5(c1015840))

4 Conclusion

Anatomic variations in the systems of the developing kidneyare common however concomitant involvement of thearterial venous and ureteric systems is rare The currentcase study demonstrates a cadaveric specimen with anatomicvariations having an estimated incidence of less than 03Collectively this case illustrates examples of importantanatomic concepts that are relevant for educational andclinical practice

Conflicts of Interest

This work was completed without financial sponsorshipThe authors declare no conflicts of interest Portions of thiswork have been presented in abstract form at conferenceproceedings

Authorsrsquo Contributions

Marc A Pizzimenti contributed in project developmentdissection and manuscript writing Martine Dunnwald con-tributed in dissection illustrations and manuscript writing

Acknowledgments

The authors would like to thank the families of individualswho through their most generous gift to the Deeded BodyProgram allow us to continue studying the human body

References

[1] E Gulas G Wysiadecki T Cecot et al ldquoAccessory (multi-ple) renal arteries ndash Differences in frequency according topopulation visualizing techniques and stage of morphologicaldevelopmentrdquo Vascular vol 24 no 5 pp 531ndash537 2016

[2] R Bergman SThompson AAfifi and F SaadehCompendiumofHumanAnatomic Variation Text Atlas andWorld Literature

Urban amp Scharzenberg Inc Baltimore Munich Germany1988

[3] Z Koc S Ulusan L Oguzkurt and N Tokmak ldquoVenousvariants and anomalies on routine abdominal multi-detectorrow CTrdquo European Journal of Radiology vol 61 no 2 pp 267ndash278 2007

[4] J D Atwell P L Cook C J Howell I Hyde and B C ParkerldquoFamilial incidence of bifid and double uretersrdquo Archives ofDisease in Childhood vol 49 no 5 pp 390ndash393 1974

[5] J Whitaker and D M Danks ldquoA study of the inheritance ofduplication of the kidneys and uretersrdquoThe Journal of Urologyvol 95 no 2 pp 176ndash178 1966

[6] V Alberts R Minnee K van Donselaar-van der Pant et alldquoDuplicated ureters and renal transplantation a case-controlstudy and review of the literaturerdquoTransplantation Proceedingsvol 45 no 9 pp 3239ndash3244 2013

[7] R Pollak B F Prusak and M F Mozes ldquoAnatomic abnormal-ities of cadaver kidneys procured for purposes of transplanta-tionrdquoThe American Surgeon vol 52 no 5 pp 233ndash235 1986

[8] K S Satyapal A A Haffejee B Singh L Ramsaroop J VRobbs and J M Kalideen ldquoAdditional renal arteries Incidenceand morphometryrdquo Surgical and Radiologic Anatomy vol 23no 1 pp 33ndash38 2001

[9] C Dalcik T Colak A Ozbek and H Dalcik ldquoUnusual originof the right renal artery a case reportrdquo Surgical and RadiologicAnatomy vol 22 no 2 pp 117-118 2000

[10] U G Rossi M Romano and C Ferro ldquoSeven renal arteriesrdquoClinical Anatomy vol 19 no 7 pp 632-633 2006

[11] P Mazengenya ldquoMultiple variations of the renal and testicularvessels possible embryological basis and clinical importancerdquoSurgical and Radiologic Anatomy vol 38 no 6 pp 729ndash7332016

[12] K Morishima T Miyaki and H Ito ldquoA rare case of a kidneywith an (sic) widely opened hilus and supernumerary renalvesselsrdquoKaibogaku Zasshi Journal of Anatomy vol 71 no 3 pp215ndash218 1996

[13] H Narita T Tani and Y Tonosaki ldquoAssociations betweenkidney position and surplus renal arteries in horseshoe kidneyCase report and analysisrdquo Okajimas Folia Anatomica Japonicavol 89 no 1 pp 7ndash13 2012

[14] S T Patil MMMeshram and A P Kasote ldquoBilateral malrota-tion and lobulation of kidney with altered hilar anatomy a rarecongenital variationrdquo Surgical and Radiologic Anatomy vol 33no 10 pp 941ndash944 2011

[15] S Degani Z Leibovitz I Shapiro and G Ohel ldquoVariationsof the origin of renal arteries in the fetus identified on powerDoppler and 3D sonographyrdquo Journal of Clinical Ultrasoundvol 38 no 2 pp 59ndash65 2009

[16] J Singh N Singh K Kapoor and M Sharma ldquoBilateral mal-rotation and a congenital pelvic kidney with varied vasculatureand altered hilar anatomyrdquo Case Reports in Medicine vol 2015Article ID 848949 3 pages 2015

[17] C Krishnaveni and R Kulkarni ldquoA right ectopic kidney withbilateral multiple anomalies of the renal vasculature ndash a casereportrdquo Journal of Clinical and Diagnostic Research vol 7 pp150ndash153 2013

[18] C Cases L Garcıa-Zoghby P Manzorro et al ldquoAnatomicalvariations of the renal arteries Cadaveric and radiologic studyreview of the literature and proposal of a new classification ofclinical interestrdquo Annals of Anatomy - Anatomischer Anzeigervol 211 pp 61ndash68 2017

Case Reports in Vascular Medicine 7

[19] O Kornafel B Baran I Pawlikowska P Laszczynski MGuzinski and M Sasiadek ldquoAnalysis of anatomical variationsof the main arteries branching from the abdominal aorta with64-detector computed tomographyrdquoPolish Journal of Radiologyvol 75 pp 38ndash45 2010

[20] F J B Sampaio and M A R F Passos ldquoRenal arteriesanatomic study for surgical and radiological practicerdquo Surgicaland Radiologic Anatomy vol 14 no 2 pp 113ndash117 1992

[21] D T Tardo C Briggs G Ahern A Pitman and S SinhaldquoAnatomical variations of the renal arterial vasculature AnAus-tralian perspectiverdquo Journal of Medical Imaging and RadiationOncology vol 61 no 5 pp 643ndash649 2017

[22] J R Geyer and E F Poutasse ldquoIncidence of multiple renalarteries on aortography report of a series of 400 patients 381of whom had arterial hypertensionrdquo Journal of the AmericanMedical Association vol 182 no 2 pp 120ndash125 1962

[23] F T Graves ldquoThe arterial anatomy of the congenitally abnormalkidneyrdquo British Journal of Surgery vol 56 no 7 pp 533ndash5411969

[24] R J Merklin and N A Michels ldquoThe variant renal andsuprarenal blood supply with data on the inferior phrenicureteral and gonadal arteries A statistical analysis based on185 dissections and review of the literaturerdquo Journal of theInternational College of Surgeons vol 29 no 1 pp 41ndash76 1958

[25] A H Young and P Thompson ldquoAbnormalities of the renalarteries with remarks on their development and morphologyrdquoJournal of Anatomy vol 38 pp 1ndash14 1903

[26] J-P Trigaux S Vandroogenbroek J-F De Wispelaere MLacrosse and J Jamart ldquoCongenital anomalies of the inferiorvena cava and left renal vein Evaluation with spiral ctrdquo Journalof Vascular and Interventional Radiology vol 9 no 2 pp 339ndash345 1998

[27] S Kawamoto L P Lawler andE K Fishman ldquoEvaluation of therenal venous system on late arterial and venous phase imageswith MDCT angiography in potential living laparoscopic renaldonorsrdquo American Journal of Roentgenology vol 184 no 2 pp539ndash545 2005

[28] J Zhu L Zhang Z Yang H Zhou and G Tang ldquoClassificationof the renal vein variations a study with multidetector com-puted tomographyrdquo Surgical and Radiologic Anatomy vol 37no 6 pp 667ndash675 2015

[29] T Ichikawa S Kawada J Koizumi et al ldquoMajor venousanomalies are frequently associated with horseshoe kidneysrdquoCirculation Journal vol 75 no 12 pp 2872ndash2877 2011

[30] J T J Privett W D Jeans and J Roylance ldquoThe incidence andimportance of renal duplicationrdquo Clinical Radiology vol 27 no4 pp 521ndash530 1976

[31] P L Willan and J R Humpherson ldquoConcepts of variation andnormality in morphology Important issues at risk of neglect inmodern undergraduatemedical coursesrdquoClinical Anatomy vol12 pp 186ndash190 1999

[32] A Raikos and J D Smith ldquoAnatomical variations How dosurgical and radiology training programs teach and assess themin their training curriculardquoClinical Anatomy vol 28 no 6 pp717ndash724 2015

[33] N Rani S Singh P Dhar and R Kumar ldquoSurgical impor-tance of arterial segments of human kidneys An angiographyand corrosion cast studyrdquo Journal of Clinical and DiagnosticResearch vol 8 pp 1ndash3 2014

[34] S Ersoz A Tuzuner B Erkek S Esen and E Anadol ldquoDou-ble renal arteries in living-related kidney transplantationrdquoTransplantation Proceedings vol 32 no 3 p 604 2000

[35] V Ravery O Cussenot F Desgrandchamps et al ldquoVariationsin arterial blood supply and the risk of hemorrhage duringpercutaneous treatment of lesions of the pelviureteral junctionobstruction report of a case of testicular artery arising froman inferior polar renal arteryrdquo Surgical and Radiologic Anatomyvol 15 no 4 pp 355ndash359 1993

[36] T Sadler ldquoUrogenital systemrdquo in Langmanrsquos medical embryol-ogy Lippinott Williams amp Wilkins Baltimore MD USA 12thedition 2012

[37] K L Moore and T V N Persaud ldquoThe cardiovascular systemrdquoin The Developing Human Clinically Oriented Embryology pp330ndash335 Saunders Philadelphia Pa USA 7th edition 2003

[38] G C Schoenwolf S B Bleyl P R Brauer and P H Francis-West ldquoDevelopment of the vasculaturerdquo in Larsenrsquos humanembryology pp 385ndash432 Churchhill Livingstone PhiladelphiaPa USA 4th edition 2009

[39] K I Glassberg ldquoNormal and abnormal development of thekidney A clinicianrsquos interpretation of current knowledgerdquoThe Journal of Urology vol 167 no 6 pp 2339ndash2350 2002discussion 2350-2331

[40] N D Rosenblum ldquoDevelopmental biology of the humankidneyrdquo Seminars in Fetal and Neonatal Medicine vol 13 no3 pp 125ndash132 2008

Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

EndocrinologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Disease Markers

Hindawiwwwhindawicom Volume 2018

BioMed Research International

OncologyJournal of

Hindawiwwwhindawicom Volume 2013

Hindawiwwwhindawicom Volume 2018

Oxidative Medicine and Cellular Longevity

Hindawiwwwhindawicom Volume 2018

PPAR Research

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Immunology ResearchHindawiwwwhindawicom Volume 2018

Journal of

ObesityJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Computational and Mathematical Methods in Medicine

Hindawiwwwhindawicom Volume 2018

Behavioural Neurology

OphthalmologyJournal of

Hindawiwwwhindawicom Volume 2018

Diabetes ResearchJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Research and TreatmentAIDS

Hindawiwwwhindawicom Volume 2018

Gastroenterology Research and Practice

Hindawiwwwhindawicom Volume 2018

Parkinsonrsquos Disease

Evidence-Based Complementary andAlternative Medicine

Volume 2018Hindawiwwwhindawicom

Submit your manuscripts atwwwhindawicom

Page 6: A Case Study of Malrotated Kidneys with Asymmetric ...downloads.hindawi.com/journals/crivam/2019/1893137.pdf · CaseReport A Case Study of Malrotated Kidneys with Asymmetric Multiple

6 Case Reports in Vascular Medicine

(Figure 5(b)) the persistent connections between the venouscardinal networks (Figures 2(c) 3(b) 4(b) and 5(b1015840)) can beobserved in the current specimen

Development of the ureters arises from bud outgrowthsof the mesonephric duct For each kidney the ureteric budpenetrates the metanephric mesoderm (metanephrogenicblastema) that forms a cap intowhich the renal pelvis calyxesand collecting tubules develop through branching morpho-genesis [36] The stalk of the ureteric bud elongates as thekidney undergoes its relative ascent resulting in the formedureter by the ninth week of development (Figure 5(c)) Thesimultaneous morphogenesis of the vascular and uretericstructures influences themedial rotation of the hilum for eachdeveloping kidney Details of the signaling pathways and thegenes that regulate this entire process have been effectivelysummarized in the literature [39 40] and are beyond thescope of this case studyThese processes coupled with geneticfactors may give rise to variations in the ureteric pattern(Figures 2(d) 4(b) 4(d) 5(c) and 5(c1015840))

4 Conclusion

Anatomic variations in the systems of the developing kidneyare common however concomitant involvement of thearterial venous and ureteric systems is rare The currentcase study demonstrates a cadaveric specimen with anatomicvariations having an estimated incidence of less than 03Collectively this case illustrates examples of importantanatomic concepts that are relevant for educational andclinical practice

Conflicts of Interest

This work was completed without financial sponsorshipThe authors declare no conflicts of interest Portions of thiswork have been presented in abstract form at conferenceproceedings

Authorsrsquo Contributions

Marc A Pizzimenti contributed in project developmentdissection and manuscript writing Martine Dunnwald con-tributed in dissection illustrations and manuscript writing

Acknowledgments

The authors would like to thank the families of individualswho through their most generous gift to the Deeded BodyProgram allow us to continue studying the human body

References

[1] E Gulas G Wysiadecki T Cecot et al ldquoAccessory (multi-ple) renal arteries ndash Differences in frequency according topopulation visualizing techniques and stage of morphologicaldevelopmentrdquo Vascular vol 24 no 5 pp 531ndash537 2016

[2] R Bergman SThompson AAfifi and F SaadehCompendiumofHumanAnatomic Variation Text Atlas andWorld Literature

Urban amp Scharzenberg Inc Baltimore Munich Germany1988

[3] Z Koc S Ulusan L Oguzkurt and N Tokmak ldquoVenousvariants and anomalies on routine abdominal multi-detectorrow CTrdquo European Journal of Radiology vol 61 no 2 pp 267ndash278 2007

[4] J D Atwell P L Cook C J Howell I Hyde and B C ParkerldquoFamilial incidence of bifid and double uretersrdquo Archives ofDisease in Childhood vol 49 no 5 pp 390ndash393 1974

[5] J Whitaker and D M Danks ldquoA study of the inheritance ofduplication of the kidneys and uretersrdquoThe Journal of Urologyvol 95 no 2 pp 176ndash178 1966

[6] V Alberts R Minnee K van Donselaar-van der Pant et alldquoDuplicated ureters and renal transplantation a case-controlstudy and review of the literaturerdquoTransplantation Proceedingsvol 45 no 9 pp 3239ndash3244 2013

[7] R Pollak B F Prusak and M F Mozes ldquoAnatomic abnormal-ities of cadaver kidneys procured for purposes of transplanta-tionrdquoThe American Surgeon vol 52 no 5 pp 233ndash235 1986

[8] K S Satyapal A A Haffejee B Singh L Ramsaroop J VRobbs and J M Kalideen ldquoAdditional renal arteries Incidenceand morphometryrdquo Surgical and Radiologic Anatomy vol 23no 1 pp 33ndash38 2001

[9] C Dalcik T Colak A Ozbek and H Dalcik ldquoUnusual originof the right renal artery a case reportrdquo Surgical and RadiologicAnatomy vol 22 no 2 pp 117-118 2000

[10] U G Rossi M Romano and C Ferro ldquoSeven renal arteriesrdquoClinical Anatomy vol 19 no 7 pp 632-633 2006

[11] P Mazengenya ldquoMultiple variations of the renal and testicularvessels possible embryological basis and clinical importancerdquoSurgical and Radiologic Anatomy vol 38 no 6 pp 729ndash7332016

[12] K Morishima T Miyaki and H Ito ldquoA rare case of a kidneywith an (sic) widely opened hilus and supernumerary renalvesselsrdquoKaibogaku Zasshi Journal of Anatomy vol 71 no 3 pp215ndash218 1996

[13] H Narita T Tani and Y Tonosaki ldquoAssociations betweenkidney position and surplus renal arteries in horseshoe kidneyCase report and analysisrdquo Okajimas Folia Anatomica Japonicavol 89 no 1 pp 7ndash13 2012

[14] S T Patil MMMeshram and A P Kasote ldquoBilateral malrota-tion and lobulation of kidney with altered hilar anatomy a rarecongenital variationrdquo Surgical and Radiologic Anatomy vol 33no 10 pp 941ndash944 2011

[15] S Degani Z Leibovitz I Shapiro and G Ohel ldquoVariationsof the origin of renal arteries in the fetus identified on powerDoppler and 3D sonographyrdquo Journal of Clinical Ultrasoundvol 38 no 2 pp 59ndash65 2009

[16] J Singh N Singh K Kapoor and M Sharma ldquoBilateral mal-rotation and a congenital pelvic kidney with varied vasculatureand altered hilar anatomyrdquo Case Reports in Medicine vol 2015Article ID 848949 3 pages 2015

[17] C Krishnaveni and R Kulkarni ldquoA right ectopic kidney withbilateral multiple anomalies of the renal vasculature ndash a casereportrdquo Journal of Clinical and Diagnostic Research vol 7 pp150ndash153 2013

[18] C Cases L Garcıa-Zoghby P Manzorro et al ldquoAnatomicalvariations of the renal arteries Cadaveric and radiologic studyreview of the literature and proposal of a new classification ofclinical interestrdquo Annals of Anatomy - Anatomischer Anzeigervol 211 pp 61ndash68 2017

Case Reports in Vascular Medicine 7

[19] O Kornafel B Baran I Pawlikowska P Laszczynski MGuzinski and M Sasiadek ldquoAnalysis of anatomical variationsof the main arteries branching from the abdominal aorta with64-detector computed tomographyrdquoPolish Journal of Radiologyvol 75 pp 38ndash45 2010

[20] F J B Sampaio and M A R F Passos ldquoRenal arteriesanatomic study for surgical and radiological practicerdquo Surgicaland Radiologic Anatomy vol 14 no 2 pp 113ndash117 1992

[21] D T Tardo C Briggs G Ahern A Pitman and S SinhaldquoAnatomical variations of the renal arterial vasculature AnAus-tralian perspectiverdquo Journal of Medical Imaging and RadiationOncology vol 61 no 5 pp 643ndash649 2017

[22] J R Geyer and E F Poutasse ldquoIncidence of multiple renalarteries on aortography report of a series of 400 patients 381of whom had arterial hypertensionrdquo Journal of the AmericanMedical Association vol 182 no 2 pp 120ndash125 1962

[23] F T Graves ldquoThe arterial anatomy of the congenitally abnormalkidneyrdquo British Journal of Surgery vol 56 no 7 pp 533ndash5411969

[24] R J Merklin and N A Michels ldquoThe variant renal andsuprarenal blood supply with data on the inferior phrenicureteral and gonadal arteries A statistical analysis based on185 dissections and review of the literaturerdquo Journal of theInternational College of Surgeons vol 29 no 1 pp 41ndash76 1958

[25] A H Young and P Thompson ldquoAbnormalities of the renalarteries with remarks on their development and morphologyrdquoJournal of Anatomy vol 38 pp 1ndash14 1903

[26] J-P Trigaux S Vandroogenbroek J-F De Wispelaere MLacrosse and J Jamart ldquoCongenital anomalies of the inferiorvena cava and left renal vein Evaluation with spiral ctrdquo Journalof Vascular and Interventional Radiology vol 9 no 2 pp 339ndash345 1998

[27] S Kawamoto L P Lawler andE K Fishman ldquoEvaluation of therenal venous system on late arterial and venous phase imageswith MDCT angiography in potential living laparoscopic renaldonorsrdquo American Journal of Roentgenology vol 184 no 2 pp539ndash545 2005

[28] J Zhu L Zhang Z Yang H Zhou and G Tang ldquoClassificationof the renal vein variations a study with multidetector com-puted tomographyrdquo Surgical and Radiologic Anatomy vol 37no 6 pp 667ndash675 2015

[29] T Ichikawa S Kawada J Koizumi et al ldquoMajor venousanomalies are frequently associated with horseshoe kidneysrdquoCirculation Journal vol 75 no 12 pp 2872ndash2877 2011

[30] J T J Privett W D Jeans and J Roylance ldquoThe incidence andimportance of renal duplicationrdquo Clinical Radiology vol 27 no4 pp 521ndash530 1976

[31] P L Willan and J R Humpherson ldquoConcepts of variation andnormality in morphology Important issues at risk of neglect inmodern undergraduatemedical coursesrdquoClinical Anatomy vol12 pp 186ndash190 1999

[32] A Raikos and J D Smith ldquoAnatomical variations How dosurgical and radiology training programs teach and assess themin their training curriculardquoClinical Anatomy vol 28 no 6 pp717ndash724 2015

[33] N Rani S Singh P Dhar and R Kumar ldquoSurgical impor-tance of arterial segments of human kidneys An angiographyand corrosion cast studyrdquo Journal of Clinical and DiagnosticResearch vol 8 pp 1ndash3 2014

[34] S Ersoz A Tuzuner B Erkek S Esen and E Anadol ldquoDou-ble renal arteries in living-related kidney transplantationrdquoTransplantation Proceedings vol 32 no 3 p 604 2000

[35] V Ravery O Cussenot F Desgrandchamps et al ldquoVariationsin arterial blood supply and the risk of hemorrhage duringpercutaneous treatment of lesions of the pelviureteral junctionobstruction report of a case of testicular artery arising froman inferior polar renal arteryrdquo Surgical and Radiologic Anatomyvol 15 no 4 pp 355ndash359 1993

[36] T Sadler ldquoUrogenital systemrdquo in Langmanrsquos medical embryol-ogy Lippinott Williams amp Wilkins Baltimore MD USA 12thedition 2012

[37] K L Moore and T V N Persaud ldquoThe cardiovascular systemrdquoin The Developing Human Clinically Oriented Embryology pp330ndash335 Saunders Philadelphia Pa USA 7th edition 2003

[38] G C Schoenwolf S B Bleyl P R Brauer and P H Francis-West ldquoDevelopment of the vasculaturerdquo in Larsenrsquos humanembryology pp 385ndash432 Churchhill Livingstone PhiladelphiaPa USA 4th edition 2009

[39] K I Glassberg ldquoNormal and abnormal development of thekidney A clinicianrsquos interpretation of current knowledgerdquoThe Journal of Urology vol 167 no 6 pp 2339ndash2350 2002discussion 2350-2331

[40] N D Rosenblum ldquoDevelopmental biology of the humankidneyrdquo Seminars in Fetal and Neonatal Medicine vol 13 no3 pp 125ndash132 2008

Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

EndocrinologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Disease Markers

Hindawiwwwhindawicom Volume 2018

BioMed Research International

OncologyJournal of

Hindawiwwwhindawicom Volume 2013

Hindawiwwwhindawicom Volume 2018

Oxidative Medicine and Cellular Longevity

Hindawiwwwhindawicom Volume 2018

PPAR Research

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Immunology ResearchHindawiwwwhindawicom Volume 2018

Journal of

ObesityJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Computational and Mathematical Methods in Medicine

Hindawiwwwhindawicom Volume 2018

Behavioural Neurology

OphthalmologyJournal of

Hindawiwwwhindawicom Volume 2018

Diabetes ResearchJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Research and TreatmentAIDS

Hindawiwwwhindawicom Volume 2018

Gastroenterology Research and Practice

Hindawiwwwhindawicom Volume 2018

Parkinsonrsquos Disease

Evidence-Based Complementary andAlternative Medicine

Volume 2018Hindawiwwwhindawicom

Submit your manuscripts atwwwhindawicom

Page 7: A Case Study of Malrotated Kidneys with Asymmetric ...downloads.hindawi.com/journals/crivam/2019/1893137.pdf · CaseReport A Case Study of Malrotated Kidneys with Asymmetric Multiple

Case Reports in Vascular Medicine 7

[19] O Kornafel B Baran I Pawlikowska P Laszczynski MGuzinski and M Sasiadek ldquoAnalysis of anatomical variationsof the main arteries branching from the abdominal aorta with64-detector computed tomographyrdquoPolish Journal of Radiologyvol 75 pp 38ndash45 2010

[20] F J B Sampaio and M A R F Passos ldquoRenal arteriesanatomic study for surgical and radiological practicerdquo Surgicaland Radiologic Anatomy vol 14 no 2 pp 113ndash117 1992

[21] D T Tardo C Briggs G Ahern A Pitman and S SinhaldquoAnatomical variations of the renal arterial vasculature AnAus-tralian perspectiverdquo Journal of Medical Imaging and RadiationOncology vol 61 no 5 pp 643ndash649 2017

[22] J R Geyer and E F Poutasse ldquoIncidence of multiple renalarteries on aortography report of a series of 400 patients 381of whom had arterial hypertensionrdquo Journal of the AmericanMedical Association vol 182 no 2 pp 120ndash125 1962

[23] F T Graves ldquoThe arterial anatomy of the congenitally abnormalkidneyrdquo British Journal of Surgery vol 56 no 7 pp 533ndash5411969

[24] R J Merklin and N A Michels ldquoThe variant renal andsuprarenal blood supply with data on the inferior phrenicureteral and gonadal arteries A statistical analysis based on185 dissections and review of the literaturerdquo Journal of theInternational College of Surgeons vol 29 no 1 pp 41ndash76 1958

[25] A H Young and P Thompson ldquoAbnormalities of the renalarteries with remarks on their development and morphologyrdquoJournal of Anatomy vol 38 pp 1ndash14 1903

[26] J-P Trigaux S Vandroogenbroek J-F De Wispelaere MLacrosse and J Jamart ldquoCongenital anomalies of the inferiorvena cava and left renal vein Evaluation with spiral ctrdquo Journalof Vascular and Interventional Radiology vol 9 no 2 pp 339ndash345 1998

[27] S Kawamoto L P Lawler andE K Fishman ldquoEvaluation of therenal venous system on late arterial and venous phase imageswith MDCT angiography in potential living laparoscopic renaldonorsrdquo American Journal of Roentgenology vol 184 no 2 pp539ndash545 2005

[28] J Zhu L Zhang Z Yang H Zhou and G Tang ldquoClassificationof the renal vein variations a study with multidetector com-puted tomographyrdquo Surgical and Radiologic Anatomy vol 37no 6 pp 667ndash675 2015

[29] T Ichikawa S Kawada J Koizumi et al ldquoMajor venousanomalies are frequently associated with horseshoe kidneysrdquoCirculation Journal vol 75 no 12 pp 2872ndash2877 2011

[30] J T J Privett W D Jeans and J Roylance ldquoThe incidence andimportance of renal duplicationrdquo Clinical Radiology vol 27 no4 pp 521ndash530 1976

[31] P L Willan and J R Humpherson ldquoConcepts of variation andnormality in morphology Important issues at risk of neglect inmodern undergraduatemedical coursesrdquoClinical Anatomy vol12 pp 186ndash190 1999

[32] A Raikos and J D Smith ldquoAnatomical variations How dosurgical and radiology training programs teach and assess themin their training curriculardquoClinical Anatomy vol 28 no 6 pp717ndash724 2015

[33] N Rani S Singh P Dhar and R Kumar ldquoSurgical impor-tance of arterial segments of human kidneys An angiographyand corrosion cast studyrdquo Journal of Clinical and DiagnosticResearch vol 8 pp 1ndash3 2014

[34] S Ersoz A Tuzuner B Erkek S Esen and E Anadol ldquoDou-ble renal arteries in living-related kidney transplantationrdquoTransplantation Proceedings vol 32 no 3 p 604 2000

[35] V Ravery O Cussenot F Desgrandchamps et al ldquoVariationsin arterial blood supply and the risk of hemorrhage duringpercutaneous treatment of lesions of the pelviureteral junctionobstruction report of a case of testicular artery arising froman inferior polar renal arteryrdquo Surgical and Radiologic Anatomyvol 15 no 4 pp 355ndash359 1993

[36] T Sadler ldquoUrogenital systemrdquo in Langmanrsquos medical embryol-ogy Lippinott Williams amp Wilkins Baltimore MD USA 12thedition 2012

[37] K L Moore and T V N Persaud ldquoThe cardiovascular systemrdquoin The Developing Human Clinically Oriented Embryology pp330ndash335 Saunders Philadelphia Pa USA 7th edition 2003

[38] G C Schoenwolf S B Bleyl P R Brauer and P H Francis-West ldquoDevelopment of the vasculaturerdquo in Larsenrsquos humanembryology pp 385ndash432 Churchhill Livingstone PhiladelphiaPa USA 4th edition 2009

[39] K I Glassberg ldquoNormal and abnormal development of thekidney A clinicianrsquos interpretation of current knowledgerdquoThe Journal of Urology vol 167 no 6 pp 2339ndash2350 2002discussion 2350-2331

[40] N D Rosenblum ldquoDevelopmental biology of the humankidneyrdquo Seminars in Fetal and Neonatal Medicine vol 13 no3 pp 125ndash132 2008

Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

EndocrinologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Disease Markers

Hindawiwwwhindawicom Volume 2018

BioMed Research International

OncologyJournal of

Hindawiwwwhindawicom Volume 2013

Hindawiwwwhindawicom Volume 2018

Oxidative Medicine and Cellular Longevity

Hindawiwwwhindawicom Volume 2018

PPAR Research

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Immunology ResearchHindawiwwwhindawicom Volume 2018

Journal of

ObesityJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Computational and Mathematical Methods in Medicine

Hindawiwwwhindawicom Volume 2018

Behavioural Neurology

OphthalmologyJournal of

Hindawiwwwhindawicom Volume 2018

Diabetes ResearchJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Research and TreatmentAIDS

Hindawiwwwhindawicom Volume 2018

Gastroenterology Research and Practice

Hindawiwwwhindawicom Volume 2018

Parkinsonrsquos Disease

Evidence-Based Complementary andAlternative Medicine

Volume 2018Hindawiwwwhindawicom

Submit your manuscripts atwwwhindawicom

Page 8: A Case Study of Malrotated Kidneys with Asymmetric ...downloads.hindawi.com/journals/crivam/2019/1893137.pdf · CaseReport A Case Study of Malrotated Kidneys with Asymmetric Multiple

Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

MEDIATORSINFLAMMATION

of

EndocrinologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Disease Markers

Hindawiwwwhindawicom Volume 2018

BioMed Research International

OncologyJournal of

Hindawiwwwhindawicom Volume 2013

Hindawiwwwhindawicom Volume 2018

Oxidative Medicine and Cellular Longevity

Hindawiwwwhindawicom Volume 2018

PPAR Research

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Immunology ResearchHindawiwwwhindawicom Volume 2018

Journal of

ObesityJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Computational and Mathematical Methods in Medicine

Hindawiwwwhindawicom Volume 2018

Behavioural Neurology

OphthalmologyJournal of

Hindawiwwwhindawicom Volume 2018

Diabetes ResearchJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Research and TreatmentAIDS

Hindawiwwwhindawicom Volume 2018

Gastroenterology Research and Practice

Hindawiwwwhindawicom Volume 2018

Parkinsonrsquos Disease

Evidence-Based Complementary andAlternative Medicine

Volume 2018Hindawiwwwhindawicom

Submit your manuscripts atwwwhindawicom